Dry Forests: Ecology, Species Diversity and Sustainable Management

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ENVIRONMENTAL HEALTH - PHYSICAL, CHEMICAL

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DRY FORESTS

ECOLOGY, SPECIES DIVERSITY AND

SUSTAINABLE MANAGEMENT

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ENVIRONMENTAL HEALTH - PHYSICAL, CHEMICAL

AND BIOLOGICAL FACTORS

DRY FORESTS

ECOLOGY, SPECIES DIVERSITY AND

SUSTAINABLE MANAGEMENT

FRANCIS ELIOTT GREER

EDITOR

New York


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Library of Congress Cataloging-in-Publication Data

Dry forests : ecology, species diversity, and sustainable management / editor, Francis Eliott Greer.

pages cm -- (Environmental health : physical, chemical and biological factors) Includes index.

1. Tropical dry forests. 2. Forest animals--Tropics. I. Greer, Francis Eliott. QH541.5.T66D79 2014

578.730913--dc23

2014021846

Published by Nova Science Publishers, Inc. † New York

ISBN: 978-1-63321-292-3 (eBook)


CONTENTS

Preface vii

Chapter 1 A Biogeographical Overview of the “Lianescent

Clade” of Violaceae in the Neotropical Region 1 Juliana de Paula-Souza and José Rubens Pirani

Chapter 2 Diversity and Distribution of Hymenoptera Aculeata

in Midwestern Brazilian Dry Forests 29 Rogerio Silvestre, Manoel Fernando Demétrio,

Bhrenno Maykon Trad,

Felipe Varussa de Oliveira Lima,

Tiago Henrique Auko and Paulo Robson de Souza

Chapter 3 The Brazilian "Caatinga": Ecology and Vegetal

Biodiversity of a Semiarid Region 81 Heloisa Helena Gomes Coe and

Leandro de Oliveira Furtado de Sousa

Chapter 4 Changes in the Labile and Recalcitrant Organic

Matter Fractions due to Transformation of

Semi-Deciduous Dry Tropical Forest to Pasture

in the Western Llanos, Venezuela 105 A. González-Pedraza and N. Dezzeo

Chapter 5 Ecology and Management of the Dry Forests and

Savannas of the Western Chaco Region, Argentina 133 Carlos Kunst, Sandra Bravo, Roxana Ledesma,

Marcelo Navall, Analía Anríquez, Darío Coria, Juan Silberman, Adriana Gómez and Ada Albanesi


Contents vi

Chapter 6 Predicting Pasture Security in Rangeland Districts

of Kenya Using 1 km Resolution Spot Vegetation

Sensor NDVI Data 165 Mwangi J. Kinyanjui

Index 179


PREFACE

Fossil records indicate the Neotropical Dry Forests had a more continuous

distribution in the recent geological past, especially in the late Pleistocene,

more precisely at the end of the last glacial period. Seasonal Deciduous

Forests are remnants of a broader continuous distribution that was present in

the past, ranging from North-Eastern Brazil to Argentina in the Pleistocene dry

period. This currently fragmented structure is the result of the dry, cold climate

that caused the retraction of Wet Forests to riversides and the spread of

seasonal forests. This book discusses the ecology, species diversity and

sustainable management of dry forests. The topics include a biogeographical

overview of the “lianescent clade” of violaceae in the Neotropical region;

diversity and distribution of hymenoptera aculeate in mid-western Brazilian

dry forests; the Brazilian "caatinga”; changes in the labile and recalcitrant

organic matter fractions due to transformation of semi-deciduous dry tropical

forest to pasture in the western llanos, Venezuela; ecology and management of

the dry forests and savannas of the western Chaco region, Argentina;

predicting pasture security in rangeland districts of Kenya using 1 km

resolution spot vegetation sensor ndvi data.

Chapter 1 - Violaceae is a cosmopolitan family comprising 22 currently

recognized genera and 1000-1100 species of trees, shrubs, subshrubs, herbs

and vines, occupying a wide range of habitat types and regions around the

world. Roughly half of the species in the family belong to a single genus,

Viola, which is almost exclusively herbaceous and occurs in temperate and

high altitude tropical zones. The remaining genera are confined to warm

regions of the tropics and subtropics and exhibit the wide diversity of mostly

woody growth forms previously mentioned. Independent phylogenetic studies

based on molecular data have consistently grouped all the vines of the family


Francis Eliott Greer viii

together, converging to the recognition of a strongly supported "lianescent

clade", which includes Agatea (ca. 8 spp.), from the South Pacific Islands, and

the Neotropical Anchietea (7 spp.), Hybanthopsis (1 sp.) and Calyptrion (7

spp.). Apart from this intriguing disjunction which alone stimulates an

interesting biogeographic discussion, the phylogeny of the Neotropical

lianescent clade provides evidences for shifts between arid and humid habitats

in the distribution of taxa throughout the group‟s evolutionary history. In this

context, the present study discusses the differentiation of an

Amazonian/Mesoamerican moist forest lineage (Calyptrion) emerging from

what now forms a characteristically SDTF endemic group (the South

American Anchietea and Hybanthopsis), and further shifts in environmental

preferences within the species of the latter, from dry, open conditions to water-

related, forested habitats. Most of these shifts were found to be strongly

associated with particular morphological features.

Chapter 2 - The highly diverse Hymenoptera fauna in Neotropical forests

has been the focus of many studies investigating the structure of ecological

communities, particularly in the last ten years. Studies on the biogeography

and diversity of Hymenoptera, as well as the processes affecting their

maintenance, can be of great interest for planning effective conservation of the

biota on a regional scale. Such studies can also contribute to producing new

ecological and taxonomic data, particularly in areas where no previous records

exist for the group, as in the case of dry forests located in the middle of South

America.

In this context the authors present the first systematic inventory of

Hymenoptera made in the pristine dry forests of midwestern Brazil. The study

was conducted over eight years, in two regions; Bodoquena Mountain Range

and Brazilian Chaco. These locations are set in a large open area in a diagonal

formation of South America, the so-called "Pleistocenic Arc", extending from

the Caatinga in northeastern Brazil to the Chaco in Argentina, where the

contact areas occur between the Pantanal, Cerrado, Chaco, and Atlantic Forest.

The authors investigated the distribution patterns from each Hymenoptera

group and described the faunistic structure. An expressive number of rare and

endemic species was detected, and high beta diversity was revealed for all

Hymenoptera groups along the dry forest fragments. All groups studied

showed a similar species abundance distribution profile, denoting a model that

follows a truncated lognormal pattern. In order to identify species richness, the

most diverse taxon in a regional spectrum of the dry forests analyzed was

Formicidae with 294 species and morphospecies records, followed by Apidae

(150), Pompilidae (103), Vespidae (79), Crabronidae (74), Mutillidae (21),


Preface ix

Sphecidae (20), Tiphiidae (15), Scoliidae (6), and Rhopalossomatide (1). In

total, 763 species were identified and morphospecies in 236 genera in ten

families. Despite the biogeographical relationships of the vegetation,

evolutionary effects of environmental formations and anthropogenic current

impacts may be reflected in the structure of the whole Hymenoptera

community on dry forests from mid-western Brazil. This region is considered

of very high biological importance, being extremely diverse, and it urgently

needs to be reflected as a hotspot.

Chapter 3 - In this chapter the authors present the ecological

characteristics and vegetal biodiversity of a typical Brazilian biome; Caatinga.

The name "Caatinga" comes from a Tupi-Guarani term that means "white

forest" or "clear forest" in reference to the clear gray appearance of the

vegetation during the dry season. It is an exclusively Brazilian semi-arid

ecosystem covering about 11% of the country. It extends over all the states of

the Northeast region and the north of Minas Gerais State, comprising an area

of 800,000 km2. The caatinga area extends from 2º54'S in the states of Ceará

and Rio Grande do Norte to 17º21'S in Minas Gerais State.

Generally, Caatinga is recognized as low-growing forest with

discontinuous canopy, deciduous foliage during the dry season and

xeromorphic characteristics shared by the species. However, Caatinga

physiognomies are extremely variable, depending on the rainfall regime

which, in general, does not exceed 1,000 mm/year and is concentrated in three

or four months of the year. They also depend on the characteristics of soils of

different geomorphological and geological origins, varying from high dry

forests up to 15-20 m tall, in more favorable soils in more humid

environments, to rocky outcrops with sparse low shrubs and Cactaceae and

Bromeliaceae in the crevices.

Caatinga stands out for presenting a large diversity of plant species,

currently having 4,478 recognized species in 8 eco-regions with 12 different

types of vegetation, many of which are endemic to the biome, and others that

can exemplify biogeographical relationships which help to clarify the

historical vegetation dynamics of the Caatinga itself as well as the entire

eastern area of South America.

Caatinga has been highly modified by diverse human activities. The

northeastern soils are suffering an intense process of desertification due to

replacement of natural vegetation with crops, done mainly through slash and

burn. Deforestation and irrigated cultivation are leading to soil salinization,

further increasing the evaporation of the soil water and accelerating the

process of desertification. Only the presence of the adapted vegetation of


Francis Eliott Greer x

Caatinga has prevented the transformation of northeastern Brazil into a vast

desert. Despite threats to the biome, less than 2% of the Caatinga is protected

as conservation units under full protection.

Chapter 4 - The changes of labile and recalcitrant organic matter fractions

due to transformation of semi-deciduous tropical forest to pasture were

evaluated in an area of tropical dry forest in the western Llanos of Venezuela.

In this area, natural forest was converted to pasture by slash-and-burn. Estrella

grass (Cynodon nlemfuencis L) grows for cattle use. For determining microbial

activity, twelve soil samples were collected at 0-5 and 5-10 cm depth in

natural forest and in two pastures of 5 and 18-year-old (YP and OP,

respectively) on three periods along the year: at the beginning of the rainy

season (May), at the end of the rainy season (November) and during the dry

season (March). To determine total soil organic carbon (SOC) and total

extractable carbon (TEC), 12 samples were additionally collected at each site

at 0-5, 5-10, 10-20, 20-30, and 30-40 cm depth. SOC was determined by

Walkley and Black method and TEC was extracted with alkali solution. Cmic

was determined according to the CHCl3 fumigation-extraction method using

K2SO4. The water soluble carbon (WSC) was obtained by water extraction,

and the basal respiration (C-CO2) was carried out following the colorimetric

method of static incubations. The data sets were subjected to one-way analysis

of variance. Because clay content showed significant differences between

forest and pastures, it was used as a co-variable to adjust the data. Means were

separated with Tukey‟s test when statistical differences (P < 0.05) were

observed. SOC increased with the change from forest to pasture. YP showed

the highest SOC content, which was positively correlated with the clay

percentage. TEC was significantly higher in pastures than in forest. Cmic was

higher in OP during March, which can indicate that the organic matter there

was easily decomposed and therefore allowed to maintain a high microbial

population. Cmic decreased in the pasture soils in May, probably due to a

slower response of microbial communities to sudden changes in soil moisture.

The pastures showed higher WSC contents than the forest, probably due to a

less efficient use of the labile organic matter mineralized during the previous

rains. The lowest C-CO2 value was found in YP in November, which can

indicate lower efficiency of microorganisms to decompose the organic matter.

OP showed the highest C-CO2 value, probably due to a higher content of labile

organic matter, evidenced by the higher values of Cmic, WSC and TEC in this

site.

Chapter 5 - The Chaco region is a vast plain that extends into

northwestern Argentina and surrounding countries. Chaco is a quichua word


Preface xi

meaning „a place for hunting‟ or „a place where I am self-sufficient‟ (Metraux

1946, Berton 2014, personal communication). Its northern limit is the

Amazon. At the southeast, it limits with the Pampas, and to the southwest with

the Monte, other key natural regions of Argentina. At the west, the Chaco

borders the tropical jungles. Boundaries among those regions are gradual, and

there are many shared plant and wildlife species.

In this chapter, the authors will give an overview of the ecological

features, research concepts and field methods applied, and research results

aimed to a sustainable management of the forests, grassland and savannas of

semiarid and arid Chaco subregions of Argentina, based in findings and

publications from INTA, UNSE as well as other institutions.

Chapter 6 - Ten day interval Normalized Difference Vegetation Index

(NDVI) data recorded from 1 km resolution SPOT VEGETATION sensor for

the period 2000 – 2011 was used to show variations in vegetation health in the

northern rangeland counties of Kenya to advise on pasture availability over

time and space. Using FAO land cover classification categories, three land

cover types were selected for pasture areas; Herbaceous, Herbaceous with

shrub and Open shrubs. The NDVI data was summarized for each vegetation

type in 8 counties in the northern rangelands of Kenya. Yearly trends of

vegetation were plotted and polynomial regression used to predict vegetation

indices at different times of the year. Results show that pasture specific

vegetation in the study areas cover over 17 million ha, a significant portion of

the total 59 million hectares of Kenya‟s land area making them very potential

for grazing and the national economic planning. The vegetation health was

very dependent on the hydrological fluxes and regression models for

predicting vegetation indices at specific periods of the year gave near perfect

fit in Garissa, Mandera and Wajir counties with coefficients of Determination

(R2) higher than 0.9 in all cases. ANOVA indicated no differences in

vegetation among areas, seasons and years implying that effects of climate

change and increased human activities have not compromised vegetation in the

study period. The study proposes enhancement of the pasture by promoting

nutritious and palatable grasses.


In: Dry Forests ISBN: 978-1-63321-291-6

Editor: Francis Eliott Greer © 2014 Nova Science Publishers, Inc.

Chapter 1

A BIOGEOGRAPHICAL OVERVIEW

OF THE “LIANESCENT CLADE” OF

VIOLACEAE IN THE NEOTROPICAL REGION

Juliana de Paula-Souza1

and José Rubens Pirani2

1Department of Environmental and Plant Biology,

Ohio University, US 2Instituto de Biociências, Universidade de São Paulo, Brazil

ABSTRACT

Violaceae is a cosmopolitan family comprising 22 currently

recognized genera and 1000-1100 species of trees, shrubs, subshrubs,

herbs and vines, occupying a wide range of habitat types and regions

around the world. Roughly half of the species in the family belong to a

single genus, Viola, which is almost exclusively herbaceous and occurs in

temperate and high altitude tropical zones. The remaining genera are

confined to warm regions of the tropics and subtropics and exhibit the

wide diversity of mostly woody growth forms previously mentioned.

Independent phylogenetic studies based on molecular data have

consistently grouped all the vines of the family together, converging to

the recognition of a strongly supported "lianescent clade", which includes

Agatea (ca. 8 spp.), from the South Pacific Islands, and the Neotropical

Anchietea (7 spp.), Hybanthopsis (1 sp.) and Calyptrion (7 spp.). Apart

from this intriguing disjunction which alone stimulates an interesting


Juliana de Paula-Souza and José Rubens Pirani 2

biogeographic discussion, the phylogeny of the Neotropical lianescent

clade provides evidences for shifts between arid and humid habitats in the

distribution of taxa throughout the group‟s evolutionary history. In this

context, the present study discusses the differentiation of an

Amazonian/Mesoamerican moist forest lineage (Calyptrion) emerging

from what now forms a characteristically SDTF endemic group (the

South American Anchietea and Hybanthopsis), and further shifts in

environmental preferences within the species of the latter, from dry, open

conditions to water-related, forested habitats. Most of these shifts were

found to be strongly associated with particular morphological features.

INTRODUCTION

The Violaceae is a cosmopolitan family that comprises roughly 1000-1100

species distributed among 22 genera (Ballard et al. 2014, Wahlert et al. 2014).

Approximately half of the species of the family belongs to a single genus, the

predominantly herbaceous Viola, which is widely distributed in the temperate

Northern Hemisphere and high altitude areas of the Southern Hemisphere. The

remaining 21 genera are restricted to warm subtropical or tropical regions of

the world (except for a few species of Hybanthus s.l.), and they account for the

great diversity of life forms and reproductive traits observed in the family

(Ballard et al. 2014), including trees, shrubs, subshrubs, herbs and vines.

The “lianescent clade” is an informal term that was coined from the results

of recent phylogenetic studies (Feng 2005, Tokuoka 2008, Paula-Souza, 2009,

Wahlert et al. 2014), to refer to a strongly supported clade that comprises all

four lianescent genera in the family.

The lianescent clade includes ca. 20 species distributed among the South

Pacific Agatea A.Gray (8 spp.) and the Neotropical Anchietea A.St.-Hil.

(6 described and 1 new sp.), Calyptrion Ging. (4 described, 3 new spp.), and

the monotypic Hybanthopsis Paula-Souza. Besides sharing the twining life

form, all genera in this clade have in common strongly flattened seeds, which

are in most cases also winged. The diverse morphology of seed types is

suggested to be strongly correlated with dispersal strategies and occupancy of

habitats.

Raven & Axelrod (1974) postulated that the Violaceae probably

differentiated in South America after drifting from Africa, and have widely

spread from the new continent to occupy the most diverse habitats through-out

the world. In fact, recent fossil-calibrated dating analyses have confirmed that

the Malpighiales (where Violaceae belongs) originated in the Cretaceous and


A Biogeographical Overview of the “Lianescent Clade” … 3

rapidly radiated, so that most of its families have origins at about 100 Ma ago

(Davis et al. 2005, Wang et al. 2009). However, apart from diaspores of

European Viola species in sediments from the Miocene (Meller & Hofmann

2004, Kovar-Eder 1999, Kovar-Eder & Hably 2006), the fossil record of

Violaceae is extremely sparce, and so far no attempts have been made to

obtain divergence dates within the family, except for a small group of North

American Viola (Marcussen et al. 2011). The reconstruction of the

biogeographical history of the Violaceae still lacks a global phylogeny

including the divergence time of the lineages (Santos & Amorim 2007;

Magallón 2004).

Biogeographical studies within the Violaceae have likewise been

restricted to small groups in Viola (Ballard, Jr. 2000; Havran et al. 2009),

despite the fertile grounds for this kind of investigation in the family,

uncovered by the recent evolutionary evidence. In this chapter we will discuss

a few hypotheses regarding the biogeographical history of the four genera

included in the lianescent clade of the family, with emphasis on the

Neotropical taxa, based on phylogenetic, morphological and ecological

evidence observed in the light of environmental changes through time.

THE PHYLOGENY OF THE LIANESCENT

GENERA OF THE VIOLACEAE

Before discussing biogeographical aspects of the lianescent clade of the

Violaceae, it is important to summarize and briefly discuss the phylogenetic

relationships among its taxa, according to recent molecular studies. The four

genera were segregated from the subtribes where they had traditionally been

placed based on a corolla feature: the presence of a distinct spur (Anchietea

and Calyptrion from subtribe Violinae) or a merely gibose sac (Agatea and

Hybanthopsis from subtribe Hybanthinae) at the base of the anterior petal.

Taylor (1972) had already found similarities between Agatea, Anchietea and

Calyptrion based on wood anatomy, but the idea of an evolutionary

relationship was rejected due to the then-inconceivable geographical

disjunction implicit in this group.

Although all four genera are represented in the available phylogenies

inferred from plastid DNA sequences (Paula-Souza, 2009; Wahlert et al.

2014), the evolutionary relationships among the taxa are not fully resolved.

Anchietea and Agatea are always each supported as monophyletic, however,



the results from the analyses of the trnL intron plus the trnL–trnF intergenic

spacer region are incongruent with the rbcL phylogeny alone and the

combined analyses, specifically concerning the affinities of Hybanthopsis and

the monophyly of Calyptrion (Figure 1).

In the first analysis, Calyptrion is paraphyletic in relation to Agatea, and

Hybanthopsis is sister to the remaining genera. In the rbcL analysis, this

monotypic genus has a moderate support as sister to Calyptrion + Agatea.

Here, the monophyly of Calyptrion is highly supported. The combined

analysis is similar to the rbcL alone, except for a weaker support to the

position of Hybanthopsis, and the low resolution between the sampled species

of Calyptrion, preventing any conclusion in respect to its monophyly. More

recent results of Maximum parsimony and Maximum likelihood analyses

based on a combined dataset of the same plastid DNA regions (Wahlert et al.

2014) showed the same topology as the previous combined analysis, but

slightly more resolved in regard to the paraphyly of Calyptrion. However,

considering the striking morphological differences combined with the

significant geographical gap between Calyptrion and Agatea, these two

lineages are still being treated as distinct genera, albeit indisputably with a

strong evolutionary affinity.

The biogeographical hypotheses presented here are based on the trnL

/trnL-trnF analysis of Paula-Souza (2009), since it includes a larger sampling

of South American taxa. It is important to point out, however, that whatever

analysis is used, the ultimate biogeographical conclusions related to the

original habitats of the lianescent clade and shifts of the lineages from wet to

dry environments would remain unchanged.

Figure 1. Details of phylogenetic hypotheses for the relationships among the lianescent

genera of the Violaceae, inferred from Maximum parsimony (MP) analysis of datasets

of trnL /trnL-trnF (a), rbcL (b) and trnL /trnL-trnF + rbcL (c). Numbers above

branches are bootstrap (BS) percentages. Extracted from Paula-Souza, 20091.

1 Refer to this author for the complete phylogenetic tree, methodology and vouchers.



THE NEOTROPICAL LIANESCENT GENERA

OF THE VIOLACEAE

The Neotropical genera of the Violaceae are widely distributed throughout

South America (Figure 2). Calyptrion is a predominantly Amazonian genus

(one species extending north up to Mexico; Paula-Souza & Pirani, in press),

whose species exhibit a close association with seasonally wet to flooded areas,

being often found along “igapós” or less frequently in “várzea” forests.

Anchietea and Hybanthopsis are distributed in much drier and markedly

seasonal environments, such as the semideciduous forests of southeastern

Brazil or even the semi-arid northeastern Brazilian Caatinga and dry forests

(“bosques secos”) in Bolivia, northern Argentina and western slopes of the

Andes.

The phylogeny of the lianescent representants of the family (Figure 3)

supports the hypothesis of a past connection between all or most of seasonally

dry forests in South America. This can be evidenced by the close affinity

between Anchietea ferrucciae (narrowly endemic to caatingas of Abaíra in

Bahia state, Brazil) and Anchietea peruviana, native to the Andes of Peru and

Ecuador.

Figure 2. Geographical distribution of the lianescent Neotropical genera of Violaceae.



It is reasonable to consider Anchietea an endemic2 genus of the

Neotropical Seasonally Dry Forests (Pennington et al. 2000, 2003), or Tropical

Seasonal Forests Region (Prado 2000, previously designated as “Pleistocenic

Arc” by Prado & Gibbs 1993), occurring in all areas of the “dry diagonal”

described by Prado & Gibbs (1993). Thus, the species of Anchietea are found

from the Caatingas of northeastern Brazil (A. selloviana, A. ferrucciae), to

semideciduous forests of São Paulo and Paraná states in southeastern Brazil, in

forests from the valley of the upper Uruguay river and from the Paraguay-

Paraná system, Piedmont forests in transitional areas of northwestern

Argentina and southwestern Bolivia (A. pyrifolia, which can also occur in

wetter areas of the Atlantic Coastal forest), dry forests in serranías Chiquitanas

of southeast Bolivia (A. selloviana), and more sparsely in patches in arid and

semi-arid valleys from northern Bolivia through Peru, reaching southwestern

Ecuador (A. peruviana) (Figure 6). One still undescribed species, despite being

endemic to the Mata Atlântica domain, occurs in xeric habitats on rocky

outcrops of inselbergs, which clearly reflects the current fragmentation of

forested habitats as “land islands” (Prance 1996, Porembski & Barthlott 2000,

Porembski 2007).

The phylogenetic topology enables us to infer that the lianescent lineage

of Violaceae were originally adapted to dry habitats (Figure 4), having

secondarily spread to moister ones, as observed in the clade comprised by

Calyptrion + Agatea, and A. exalata + A. pyrifolia. The results of the

phylogenetic studies invoke the effect of the theories of niche conservatism

and niche evolution (Wiens 2004, Wiens & Donoghue 2004, Hawkins et al.

2006, Ricklefs 2006).

Figure 3. Details of the phylogenetic hypotheses of the relationships between the

lianescent genera of the Violaceae, based on trnL /trnL-trnF sequences: Mapping of

the vegetational types where the taxa occur (*extracted from Munzinger 2000, 2001).

2 It is also found at the Brazilian Cerrado, which is not included in any of these authors‟ seasonal

forests, but rather being considered as the distinct - though still definitely seasonal -, more

open vegetation type Savanna.



Niche conservatism determines which environmental conditions the

members of a clade can tolerate, to which areas they can be dispersed, and the

nature of ecological barriers to their dispersal. On the other hand, niche

evolution allows a particular species and its decendants to disperse to new

habitats and climatic conditions, and to persist in environments that are prone

to changes. In this context, we could argue that the ancestral niche of the

lianescent Violaceae corresponds to the Seasonally Dry Tropical Forest

(SDTF) of South America, and the conquest of mesic or wetter habitats in this

group might have occurred with the emergence of the lineage from which

Calyptrion and Agatea diverged. The fact that A. pyrifolia is the most

widespread and frequently found species of this genus might be a consequence

of niche evolution at population level, as well as the expansion of its

preferential habitats and retraction of drier environments, more suitable for the

occupancy of the other species of the genus.

Several recent phylogeographic studies on Neotropical plant and animal

species lineages have shown the complexity of histories discovered, as well as

common patterns, for example cases of strong genetic structure and

Pleistocene to pre-Pleistocene divergence histories, which represent radiations

allowing to investigate broad biogeographic histories of associated biomes

(e.g. Martins 2001, Turchetto-Zolet et al. 2012), including analysis especially

concerned to the South American dry-diagonal (Werneck et al. 2012).

Figure 4. Details of the phylogenetic hypotheses of the relationships between the

lianescent genera of the Violaceae, based on trnL /trnL-trnF sequences: Mapping of

the type of habitat where they preferably occur (*extracted from Munzinger 2000,

2001).



The South American continent has a highly complex mosaic of

phylogeographical patterns, being composed of a variety of different

ecoregions (Morrone 2004, 2006, Aragon et al. 2011) and particularly

regarding to Amazonian taxa, speciation models are not still completely

satisfactory (Bush 1994, Turchetto-Zolet et al. 2012). In the case of the

lianescent genera of Violaceae, this situation is aggravated by the lack of a

resolved phylogeny indicating the pathways and timing of its colonization of

the Amazonian lowlands, either from the Atlantic Coastal Forest or from the

rising Andean Cordillera as explained below.

The hypothesis of a past connection between the Amazon and the Atlantic

Coastal Forest (Oliveira et al. 1999, 2005) concur with a possible migration of

a lianescent lineage of the Violaceae from the Caatinga to the Amazon. Many

authors (e.g. Oliveira-Filho & Ratter 1995, Meave et al. 1991) argued that

migrations from Amazonian taxa to the Atlantic Forest and vice-versa may

have occurred during the several humid phases of the Pleistocene or even prior

to that, which would have possibly been facilitated by a past dendritic network

of gallery forests, probably much more extensive than the present one.

Furthermore, paleoenvironmental records and fossils of the megafauna provide

strong evidence that tropical moist forests once occupied areas that are

currently covered by Caatinga (Hartwig & Cartelle 1996 apud Oliveira et al.

1999, Cartelle & Hartwig 1996 apud Oliveira et al. 1999, Behling et al. 2000).

This scenario might have further favored the migration and the establishment

of the lianescent lineage of Violaceae that later diversified in the Amazon and

further north.

Alternatively, we could also infer that the Amazonian lianescent lineage

had its origins from the southern part of the South American continent, from

populations of a past SDTF landscape covering a rising Andean Cordillera that

are currently restricted to the Piedmont Nucleus in Bolivia and northern

Argentina (Figure 2).

The Miocene-Pliocene paleobotanical and palynological records from the

high plain of Bogotá at 2475 m altitude (Cordillera Central, Colombia) include

taxa that are currently found on the Amazonian alluvial plains, indicating a

past lowland environment with swamp forests occurring in a few sites

(Wijninga 1996).

In addition to lowland taxa, the presence of typically montane elements in

the fossil record suggests the presence of mountains in the region, but

paleovegetation characteristics suggest a paleoelevation below 700 m. Besides

“terra firme” upland elements, the fossil record for lowland taxa in some sites

mainly represents the forest that covered drainage areas of rivers. In fact, the



co-occurrence of montane and lowland pollen taxa in a particular deposit

generally reflects a past network of streams draining montane areas, the

sediments being carried down to the lowlands by rivers draining the montane

hinterland (Wijninga 1996). This past scenario of the Bogotá Plateau,

combined with the fossil record indicating the existence of SDTF forests in the

Andes during the Miocene (Burnham 1995, Burnham & Carranco 2004,

Hughes et al. 2004, Pennington et al. 2010), support the idea of a midelevation

montane, SDTF lineage ancestral to Anchietea coming from the south and later

giving rise to a lowland group adapted to moister environments like

Calyptrion.

According to this second hypothesis, therefore, the emergence of an

Amazonian lianescent lineage would be less related to climate changes and

associated glaciations of the Pleistocene, rather being more directly influenced

by earlier tectonism and orogeny which substantially predate the Milankovitch

Cycles of the Quaternary. The idea of an older divergence time to Calyptrion

(e.g. prior to the final rapid Andean uplift at ca. 10 Ma) is also coherent with

the expansion of a typically lowland Amazonian taxon in Central America.

Paleovegetational reconstructions show that the initial Andean uplift

(Early/Mid Miocene at 23-10 Ma) through the Pliocene provided habitats

comparable to those north of the Isthmus of Panama (Wijninga 1996, Koecke

et al. 2013) – a complex vegetation mosaic composed by low-mid

semievergreen forests, rain forests, fresh-water swamps and mangroves

(Retallack & Kirby, 2007). Interestingly, there are currently several records of

Calyptrion from mangroves in both eastern and western coasts of Central

America (especially in Mexico), while its occurrence in the same habitat in

South America is practically null. It is not possible to assert whether it was an

event of local southern extinction, or if the northern plants acquired a higher

salt tolerance after they became isolated from their South American sister-

groups.

The importance of the Panama Isthmus in the great biological exchange

established between the South American continent and Laurasian terrains is

very well known. From the botanical and zoological paleontological records,

the arrival of holartic elements in northern South America, as well as of

Gondwanan elements in Central America, have been extensively documented

(Burnham & Graham 1999).

The uplift of this landbridge and the final closure of the Central American

seaway during the late Pliocene to early Pleistocene (3.0 – ∼2.5 Ma) for many

years has been considered a defining event in biogeography, providing the

times for divergence resulting from vicariance between related groups



(Simpson, 1980; Gentry 1982a; Stehli & Webb 1985; Graham 1992; Wendt

1993; Burnham & Graham 1999, McCartney et al. 2000).

However, the “Great American Biotic Interchange” (GABI, Stehli &

Webb 1985) paradigm, which is mostly based on zoological patterns, should

be applied with caution. Recent studies have shown that due to a greater

readiness for dispersal, plants crossed between the Americas earlier than

animals and frequently exhibit disjunct distributions that are not

chronologically correlated with geological events (Cody 2010, Leigh et al.

2014). For instance, based on a dated phylogeny of the genus Inga (Fabaceae),

Richardson et al. (2001) provide probable dates for the presence of species of

the genus in continental and insular Central America a little older than what is

generally assumed for the connection of the isthmus. However, the authors

stressed the possibility of the colonization of Central American areas by some

species of Inga through islands that were formed prior to the full establishment

of the isthmus. Moreover, it has been suggested that the gap between the

landmasses by the Late Pliocene/Early Pleistocene was much narrower than

previously thought (Farris et al. 2011, Montes et al. 2012), which might have

facilitated a much earlier migration for many groups other than plants (e.g.

amphibians, Flynn et al. 2005, Pinto-Sánchez 2012; birds, Barker 2007, Weir

et al. 2009).

We believe that the hypothesis of water dispersal instead of land crossing

is the most plausible interpretation for the present distribution of Calyptrion in

Central America, since local ocean currents do not seem to represent barriers

to their propagules, given all the evidences supporting long-distance dispersal

as the explanation for the disjunction between that genus and Agatea. The

absence of records of Calyptrion in the Antilles is better explained on the light

of unfavorable ocean currents, rather than this being an evidence of its

expansion by land after the complete closure of the Panama Isthmus.

Paleoceanographical data indicates that prior to the Pliocene, local current-

flows would have delivered South American waifs to the Central American

coast, not to the Caribbean Islands, and present-day records still suggest that

surface-current dispersal and final deposition of propagules in the Antilles

coming from the northern South American shoreline is highly unpredictable,

even considering a northward flow with respect to this continent‟s coast

(Iturrialde-Vinent & MacPhee 1999).

A similar pattern is also observed in other groups within the Violaceae

(namely some lineages of Hybanthus s.l.), in which the continental

Mesoamerican floristic composition does not have common elements with the

islands‟.



EVOLUTION IN SEED MORPHOLOGY AND ITS

ASSOCIATION TO SHIFTS IN PREFERABLE HABITATS

A probable synapomorphy of the lianescent clade, the flattened seeds of

Agatea, Calyptrion and Anchietea differ drastically from the predominantly

globose seeds in the rest of Violaceae (Figure 5). The only deviation in this

group is the seeds of Hybanthopsis, which, although flattened, show a

completely discordant morphology in relation to the remaining species of the

family as a whole. In fact, according to Gentry (1995), there is a strong

correlation between lianescent habit, anemochory and open habitats, an

inference that is clearly supported by the evolutionary history of the lianescent

genera of the Violaceae. The winged seeds of Anchietea suggest an

anemochorous dispersal through the predominantly arid or semi-arid

environments where this genus typically occurs. On the other hand, the

wingless, thick seeds of the Amazonian Calyptrion and its distribution along

water courses are hypothesized to be related to shifts in the dispersal strategy

of its species to hydrochory. This would lead us to the conclusion, based on

phylogenetic evidence, that the winged seeds of the South Pacific Agatea may

be related to a secondary shift to wind dispersal.

Ridley (1930 apud Good 1974) mentioned that in most cases, the presence

of wings on the propagules is related to dispersion, just as reduction and

thickening of the wings reflect adaptive changes in the dispersion from wind to

water (Gentry 1973, 1980, Pijl 1982).

Figure 5. Morphological diversity in seed shape among the lianescent genera of

Violaceae: a. Calyptrion pubescens, b-c. Calyptrion arboreum (dorsal and ventral

views); d. Anchietea pyrifolia, e. Anchietea ferrucciae, f. Anchietea selloviana, g.

Anchietea exalata, h. Anchietea peruviana, i. Agatea sp., j-k. Hybanthopsis bahiensis

(dorsal and lateral views).



Good (1974) further states that in vesicular fruits, the thin and

membranous carpel walls enable the whole structure to be carried by the wind

or eventually float up in water currents. All these features can be observed in

the lianescent genera of Violaceae. In Anchietea, for example, most species

have winged seeds, namely the two most widespread taxa, A. pyrifolia and A.

selloviana, which occur either in open areas of Caatingas and Savannas, or in

the border of more dense forests. Personal observations of natural populations

of A. exalata (in which the wings are greatly reduced and thickened) showed

that even though it is often registered as a forest species, it usually grows in

direct contact to water courses and is perhaps more properly considered

riparian. The close association of Calyptrion with watercourses is even more

easily observed, and its thick and unwinged seeds are an example of a

phenomenon common to other groups of species of plants that are considered

dissonant from their congeners due to the adaptations of the seeds to seasonal

environments flooded where they live, with several references to Amazonian

taxa (e. g. Tabebuia barbata, Gottsberger 1978, Gentry 1982; Erisma

calcaratum, Sytsma et al. 2004). This ability to float and be carried by water

currents is among the handful of evidence supporting a long-distance dispersal

as the most plausible explanation for the disjunction between Calyptrion and

the South Pacific Agatea.

ANCHIETEA, A GENUS MOSTLY RESTRICTED TO SDTF

As previously stated, the distribution of the species of Anchietea matches

the SDTF area in South America (Figure 6). Although there are overlappings

in their distribution ranges, we can observe a preference for mesic to wet

environments by Anchietea pyrifolia, and for drier conditions by A. selloviana.

Therefore, their distributions are complementary in the “dry diagonal” of

seasonal woodlands in South America (Prado & Gibbs 1993, Pennington et al.

2000, 2003). A. pyrifolia occurs in southeastern-south Brazil and adjacent

Paraguay and Argentina, with a disjunction at the Andean Yungas of

northwestern Argentina and southern Bolivia (Piedmont Nucleus according to

Prado & Gibbs 1993, Pennington et al. 2000). Anchietea selloviana, on the

other hand, shows a disjunct distribution in a large area in eastern Brazil and

Caatingas in the eastern part of this country, and a smaller area comprising dry

forests between Mato Grosso and Mato Grosso do Sul in Brazil and Bolivian

dry forests (“bosques secos chiquitanos”), also included in the Piedmont

Nucleus (Prado & Gibbs 1993, Pennington et al. 2000). The remaining two



species (plus an undescribed one) show narrower distributions in eastern

Brazil (A. ferrucciae and Anchietea sp.) and the Andean Cordillera (A.

frangulifolia and A. peruviana). These later species can be considered

elements of the Bolivian and Peruvian Inter-Andean valleys as defined by

Pennington et al. 2000, extending farther north up to the Massif of Bogotá, but

it is noteworthy that they have completely disparate environmental preferences

– while A. peruviana is predominantly found in dry, open areas (“matorrales”,

“escrubes”, “laderas”), A. frangulifolia occurs preferentially in moist cloud

forests. Interestingly, the same pattern was observed by Havran et al. (2009)

for the Hawaiian violet lineage, for which the authors detected a dry and wet

clade for the Viola growing along the Hawaiian mountains.

The appearance of a new reproductive feature corresponding to a

tomentose ovary might be related to the conquest of environments with colder

climate by this genus. This is an autapomorphy of the Andean species of

Anchietea, which occurs exclusively in median altitudes of this mountain

range.

Figure 6. Geographical distribution of the species in Anchietea.



Figure 7. Examples of morphological diversity in indument and shape among the seeds

of Anchietea frangulifolia.

Miller (1986) stated that a noteworthy aspect of alpine tropical systems

around the world is the high occurrence of indument on their plants, covering

vegetative and/or reproductive parts. A probable evolutionary advantage of

coating structures with trichomes include protection against heat loss by

radiation and frosts (Miller 1986), a strong correlation being observed between

altitudinal gradient and density of indument in many groups of plants, e.g.

Puya (Bromeliaceae, Miller 1986), Encelia (Asteraceae, Ehleringer et al.

1981) and Espeletia (Asteraceae, Meinzer & Rundel 1985). In Puya, the dense

coat of trichomes on the inflorescence provides not only an increase in heat

gain, but also keeps the temperature inside the flowers significantly higher

compared to the glabrous flowers of species in lower elevations. Miller (1986)

concluded that the development of a dense indument in Puya species seemed

to be a functional response to the low temperatures of the Páramos, and an

important factor in their reproductive success, since higher floral temperatures

have been associated with significant increase of seed production. In

Anchietea, the trichome coating, even if only on the pistil, seems to provide

enough additional protection to the ovules in less favorable environments,

leading to the emergence of a distinct lineage in the group, occupying hitherto

unexplored niches not only for this genus, but the lianescent group as a whole.

The reasons for the development of an indument on the seeds of A.

frangulifolia, however, are still obscure. Other adaptative advantages resulting

from the coverage of plant organs by trichomes are the protection against

herbivory (Baruch & Smith 1979, Woodman & Fernandez 1991) and frosts

(Hedberg 1964), as mentioned above, in addition to repelling water, which

could prevent the establishment of pathogens during warmer seasons (Brewer



& Smith 1997). Still, even if this evolutionary novelty confers some adaptative

advantage to plants that is still unknown to science, it does not seem to be

completely fixed in A. frangulifolia, appearing sporadically in some

populations (Figure 7), mainly from the northern Andes, and currently

available data preclude the formulation of hypotheses on this issue.

ANCHIETEA AND THE AMOTAPE-HUANCABAMBA ZONE

As previously stated, the fossil record suggests that the SDTF existed in

the Andes before the rapid final phase of the Andean orogeny during the late

Miocene (ca. 10 Ma). The Andean SDTF is currently restricted to valleys

between ca. 500-2,500 m altitude, and for many of the SDTF species confined

to the these valleys, the surrounding cordilleras represent a very effective

physical barrier for dispersal. Their biogeography was therefore highly

influenced by the rapid orogenetic movement, resulting, for example, in

altitudes of 4,000-5,000 m precluding the contact of midelevation montane

forest populations of the legume Cyathostegia occurring in adjacent valleys

(Pennington et al. 2010).

With respect to lowest altitudinal constraints, the existence of three

morphotypes of Anchietea with distinct distributions in the Andes – A.

peruviana and two disjunct populations of A. frangulifolia – suggests a strong

present or past influence of the Amotape-Huancabamba Zone, which is also

observed in other plant groups (Passiflora lobbii group, Passifloraceae,

Skrabal et al. 2001; Fuchsia, Onagraceae, Berry 1982; Calceolaria,

Calceolariaceae, Molau 1988; Urtica, Urticaceae, Ribes, Grossulariaceae and

Loasaceae, Weigend 2004, Weigend et al. 2005) and vertebrates (Duellman

1979; Duellman & Pramuk 1999). The Amotape-Huancabamba Zone is

situated from southern Ecuador to northwestern Peru, where the Andean

Cordilleras are partially interrupted by the drainage system of the Chamaya

and Marañón rivers. The Central and Eastern Cordilleras are at this site

completely interrupted by the formed valleys, and only the Western Cordillera

persists throughout the region, with its lowest elevation reaching 2145msm at

Abra de Porculla, in Peru (Weigend 2002, 2004). The area is characterized by

very high biological diversity and high rates of (micro)endemism (Young &

Reinel 1997), which are probably a result of the habitat mosaics and repeated

isolation of these fragments following the retreat of mountain forests that once

spread more widely over the area (Weigend 2002, Weigend et al. 2005,

2005a). It is suggested that the drastic reduction in width and altitude of the



Andean chain and disruption of habitats of this area (especially high montane)

were important in limiting dispersal of taxa between the northern and central

Andes, although this barrier has been more effective in cases of taxa adapted

to high altitudes. Furthermore, since the Marañón Valley runs in a north-south

direction, it probably remained sheltered from the moist air coming from the

east or the west, leading to a persistent semi-arid condition in the valley, which

may explain both the abundance of endemic plants adapted to this type of

habitat, and the disruption of migration across the valley slopes, especially for

taxa of high-montane humid environments (Simpson 1975, Weigend 2002).

The eastern slope of the Cordillera in this region is characterized by gradual

climate changes and less arid habitats, while the west slope and valleys are

covered by arid and semi-arid scrubs with isolated patches of cloud forests

(Simpson 1975, Weigend 2002, Weigend et al. 2005). Weigend et al. (2005a)

further state that these humid montane forest fragments exist between the

altitudes of 2600-3200msm of the arid slopes of the Northern and Central

Andes, and are considered remnants of a nearly continuous band that in past

eras covered larger areas in this region (Simpson 1975, Jaramillo et al. 2006).

The delineation of the Amotape-Huancabamba Zone is determined from

overlapping species or group of species from the north and the south, and the

presence of certain groups of plants that are endemic or at least have a higher

concentration of species in this area. Although Anchietea is represented by

only two species in the Andes, the morphological entity corresponding to A.

peruviana is restricted to dry areas of the Amotape-Huancabamba Zone

(Figure 8), and A. frangulifolia has a disjunct distribution in cloud forests

immediately south of this area (central Peru and western Bolivia) and more

isolated to the north (Massif of Bogotá). We could infer a past broader

distribution of A. frangulifolia along the moist montane forests that probably

extended over a wider area, which allowed continuity between the two

currently disjunct populations of this species. With the discontinuation of the

Eastern and Central Cordilleras, gene flow between populations of the north

and south would have been compromised, due the retreat of the moist forests

to the west of the Western Cordillera after the glacial period, and the barrier

imposed by the inter-Andean dry valleys. Some populations were able to

survive and thrive under such drier conditions, and differentiate into what is

now considered A. peruviana. Even so, some migration would still have been

possible, either through the relicts of rainforests on the western slope, or even

through the Abra de Porculla, thanks to the altitudinal distribution of A.

frangulifolia. This may explain the subtle morphological differences observed

between the disjunct populations of A. frangulifolia, which would be a result



of its partial isolation, potentially leading to the emergence of two distinct taxa

in the future (Figure 8).

In this sense, we can apply to the populations of Andean Anchietea the

hypothesis raised by Fjeldså (1995: 98, apud Weigend 2002) against the

barrier effect of the Amotape-Huancabamba Zone, that the mere presence of

physical barriers is of less importance than are some specific ecological

conditions on both sides separately. Weigend (2002) argued that an important

contributing factor to the high number of species in the Amotape-

Huancabamba Zone is the colonization of atypical habitats, i.e. habitats where

either the genus as a whole or at least all the other species of a given group are

not usually found, so that closely related taxa may occur in environments as

diverse as arid slopes and cloud forests (such as Xylopodia and Klaprothia,

Loasaceae). As previously mentioned, this kind of colonization is observed in

the Andean Anchietea, with A. peruviana being more characteristically found

in arid environments compared to A. frangulifolia, which is found almost

exclusively in the wet montane forests.

Figure 8. Geographical distribution of Anchietea in the Andes.

We observe in this case that ecological constraints were indeed more

effective in the process of speciation than the geographical barrier imposed by



the interruption of the Cordillera. These data corroborate the results of other

studies of fauna and flora, in which the barrier effect of the Amotape-

Huancabamba Zone also was not explicitly noted (Fuchsia, Berry 1982;

Loasaceae, Weigend 2002; Asteraceae, Ferreyra, 1995; reptiles and

amphibians, Duellman 1979, Duellman & Pramuk 1999). However, it is worth

noting that this finding applies to low/medium montane organisms (such as

Anchietea), since one would expect a much greater influence of altitudinal

barrier in the upper montane populations of this region, as observed in

Lysipomia (Campanulaceae, Ayers 1999).

Unfortunately, the available phylogenies do not allow any reliable

conclusion as to the kind of environment the ancestral lineage of Anchietea

that reached the Andes would have originally occupied. The most

parsimonious hypothesis is that this lineage would primarily have established

in drier areas such as where A. peruviana is currently found, having

subsequently spread to the cloud forests where the typical subspecies is now

distributed. In either case, it clearly illustrates the shifts between dry and wet

environments as preferable habitats for the species within the lianescent clade.

CONCLUSION

As was highlighted by Santos & Amorim (2007), the value of

biogeographic reconstructions is dependent on available evidence supporting

monophyletic lineages, and “false taxa” (i.e., non-monophyletic) generate

inaccurate information in the search for general biogeographical patterns.

Therefore, any inferences about the biogeographic history of clades within the

Violaceae are still premature, and further studies should provide stronger

evidence to thoroughly evaluate the consistency of the hypotheses proposed

here. Moreover, even the dating methods of lineages in phylogenies based on

molecular data have been viewed with reservations, or even received harsh

criticism by many biologists and biogeographers (e.g. Heads 2005, 2008) and

the development of new tools or the improvement of existing ones is expected,

with a view to achieving greater consistency between estimates of molecular

and geological dating.

The available phylogeny for the Violaceae with respect to the lianescent

genera is still poorly resolved, and to a great extent limits the reconstruction of

reliable hypotheses for its taxa. Although the sampling for Anchietea is almost

complete, the inclusion of additional taxa of Calyptrion and Agatea, as well as

the analysis of different DNA markers, could greatly improve the resolution



within the group. The available evidence, however, allows us to weave

interesting conjectures regarding the evolution of some morphological traits

associated with the environmental conditions where the taxa occur, and their

plasticity related to shifts between dry and moist habitats. Hopefully this will

provide a good starting point for future biogeographical studies with this

group. Despite the high levels of biodiversity observed in South America,

phylogeographical studies comprising members of its biota are still scanty to

provide a “big picture”, so every effort put into understanding the complexity

of its ecosystems is encouraged. This is even more urgent for poorly known

and threatened ecoregions such as the Amazonia and the Andes, the latter

comprising habitats that are considered cradles of ongoing diversification that

have been mostly overlooked by scientists and conservationists.

Understanding the evolutionary history of key elements of that biota, mainly

the mechanisms and adaptations that allowed organisms to survive and thrive

under geological instability and drastic climatic fluctuations over the last

million years, may allow us to trace strategies for our own future.

ACKNOWLEDGMENTS

This study was part of JPS‟ Ph.D. dissertation at Universidade de São

Paulo (USP), Brazil. Financial support for this project was provided by

FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo), USP,

Myndel Botanica Foundation, IAPT (International Association for Plant

Taxonomy), and SSB (Society of Systematic Biologists). The authors thank

Dr. Melanie Schori (Ohio University, USA) and Dr. Alessandra dos Santos

Penha (Universidade Federal de São Carlos, Brazil) for the English review

(MS), critical reading and valuable suggestions for the manuscript.

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Chapter 2

DIVERSITY AND DISTRIBUTION OF

HYMENOPTERA ACULEATA IN MIDWESTERN

BRAZILIAN DRY FORESTS

Rogerio Silvestre1,2

, Manoel Fernando Demétrio1,2

,

Bhrenno Maykon Trad1,2

,

Felipe Varussa de Oliveira Lima1,2

,

Tiago Henrique Auko1,2

and Paulo Robson de Souza3

1Laboratório de Ecologia de Hymenoptera HECOLAB,

Faculdade de Ciências Biológicas e Ambientais- FCBA,

Universidade Federal da Grande Dourados- UFGD,

Rodovia Dourados Itahum, Cidade Universitária, Dourados, MS, Brazil 2Programa de Pós Graduação em Entomologia e Conservação da

Biodiversidade- PPGECB,

Universidade Federal da Grande Dourados- UFGD 3Programa de Pós-Graduação em Ecologia e Conservação,

Universidade Federal de Mato Grosso do Sul, Cidade Universitária,

Campo Grande, MS, Brasil

ABSTRACT

The highly diverse Hymenoptera fauna in Neotropical forests has

been the focus of many studies investigating the structure of ecological


R. Silvestre, M. Fernando Demétrio, B. Maykon Trad et al. 30

communities, particularly in the last ten years. Studies on the

biogeography and diversity of Hymenoptera, as well as the processes

affecting their maintenance, can be of great interest for planning effective

conservation of the biota on a regional scale. Such studies can also

contribute to producing new ecological and taxonomic data, particularly

in areas where no previous records exist for the group, as in the case of

dry forests located in the middle of South America.

In this context we present the first systematic inventory of

Hymenoptera made in the pristine dry forests of midwestern Brazil. The

study was conducted over eight years, in two regions; Bodoquena

Mountain Range and Brazilian Chaco. These locations are set in a large

open area in a diagonal formation of South America, the so-called

"Pleistocenic Arc", extending from the Caatinga in northeastern Brazil to

the Chaco in Argentina, where the contact areas occur between the

Pantanal, Cerrado, Chaco, and Atlantic Forest. We investigated the

distribution patterns from each Hymenoptera group and described the

faunistic structure. An expressive number of rare and endemic species

was detected, and high beta diversity was revealed for all Hymenoptera

groups along the dry forest fragments. All groups studied showed a

similar species abundance distribution profile, denoting a model that

follows a truncated lognormal pattern. In order to identify species

richness, the most diverse taxon in a regional spectrum of the dry forests

analyzed was Formicidae with 294 species and morphospecies records,

followed by Apidae (150), Pompilidae (103), Vespidae (79), Crabronidae

(74), Mutillidae (21), Sphecidae (20), Tiphiidae (15), Scoliidae (6), and

Rhopalossomatide (1). In total, 763 species were identified and

morphospecies in 236 genera in ten families. Despite the biogeographical

relationships of the vegetation, evolutionary effects of environmental

formations and anthropogenic current impacts may be reflected in the

structure of the whole Hymenoptera community on dry forests from mid-

western Brazil. This region is considered of very high biological

importance, being extremely diverse, and it urgently needs to be reflected

as a hotspot.

Keywords: Ants, Bees, Wasps, Beta diversity, Neotropical region,

Pleistocenic arc


Diversity and Distribution of Hymenoptera Aculeata ... 31

INTRODUCTION

Brazilian Dry Forests

On a large time-scale changes in climate and relief configuration would

have caused expansions and retractions of wet and dry forests in South

America. The Brazilian dry forests are represented by those which lose part of

their leaves during a particular time of year (semideciduous) and those which

lose all of their leaves during a particular season (deciduous), located in

Caatinga, Cerrado and Chaco (Prado 2000).

Fossil records indicate that in Tertiary and Quaternary periods, the

Neotropical dry forests had a more continuous distribution in the recent

geological past, especially in the late Pleistocene era, and more precisely at the

end of the last glacial period, between 18,000 and 8,000 years ago (Werneck et

al. 2012, Pennington et al. 2009). Prado and Gibbs (1993) pointed out that

seasonal deciduous forests are remnants of a broader continuous distribution

that was present in the past, ranging from northeastern Brazil to Argentina in

the Pleistocene dry period. This currently fragmented structure is the result of

the dry, cold climate that caused the retraction of wet forests to riversides and

the spread of seasonal forests (Pennington et al. 2009). Deciduous forests

comprise discontinuous patches along fertile valleys and basaltic and

calcareous rocks in a matrix of Cerrado on the Brazilian Central Plateau. Some

of these dry forests operate as islands or are mixed with other formations. This

Cerrado matrix, intersected by riparian forests, acts as a connection among dry

forests in northeastern Brazil, east of Minas Gerais and São Paulo states, and

forest remnants in Pantanal.

The midwestern Brazilian Dry Forests, within the Chacoan sub-region,

border the provinces of Chacoan, Cerrado, Pantanal and Parana Forest

(Morrone 2014) and still remain poorly sampled with respect to the

Hymenoptera fauna.

THE HYMENOPTERA GROUP

Hymenoptera are one of the largest orders of insects, comprising sawflies,

wasps, ants and bees. Over 150,000 species are recognized, with many more

remaining to be described. Hymenoptera have a great biodiversity and a great

biological, ecological and economic importance, participating in more than



50% of terrestrial food chains. They are great deprecators of other life forms.

The majority of wasp species (well over 100,000 species) are "parasitic"

(technically known as parasitoids), and the ovipositor is used simply to lay

eggs, often directly into the body of the host. Based on the feeding habits of

the known world Hymenoptera, 85% species represent parasitic forms and

15% are predatory forms (Grissel 2010, Godfray 1994).

Taxonomists traditionally divide this group into Symphyta and Apocrita,

the first being a relatively small and probably the most ancestral taxon, with

representatives of the Triassic fossils from 200 million years ago. The

Symphyta (sawfly) have few living species; the main feature is a constriction

between the thorax and the first segment of the abdomen (Goulet & Huber

1993). Apocrita is the group that contains most species of the Hymenoptera

and is divided into two groups: Parasitic and Aculeata (Gauld & Bolton 1988).

The Aculeata branch is characterized by special modifications of the

ovipositor, a complex device found only in the adult female. The mechanism

serves both as an egg depositing tube and a sting, allowing a female wasp to

temporarily paralyze a host so that an egg can be laid upon or within its host

(O‟Neill 2001).

The most familiar wasps belong to Aculeata, whose ovipositors have

adapted with a venomous sting, though many aculeate species do not sting.

Traditionally, nine families of wasps are recognized inside Vespoidea

(Fernández 2006, Brothers 1999), and traditionally the Apoidea comprises the

lineage bees and spheciform wasps, and the number of families changes

according to the adopted classification (Johnson et al. 2013, Debevec et al.

2012, Michener 2007, Melo & Gonçalves 2005, Brothers 1975). The

parasitism can occur in species of the Chrysidoidea group (La Salle & Gauld

1993) that is classified inside Aculeata and have a group relationship with

Vespoidea and Apoidea, representing an evolutionary link between wasps that

have stinger apparatus and those which are parasitic.

Formicidae, with more than 14,954 names of valid species and subspecies

worldwide, present estimates that can exceed 20,000 species (AntWeb 2014).

21 subfamilies are currently recognized, diagnosed from potential

synapomorphies (Fernandez & Sendoya 2004, Agosti & Alonso 2000). The

Neotropical region comprises 15 of these, with 136 genera and 4,164 species

and subspecies, of which 1,906 species are endemic. In Brazil 1,456 species

and 103 genera are recognized (AntWiki 2014).

Ants are one of the most important groups of insects in tropical forests.

They strongly influence the ecosystem since it is important in the

incorporation of nutrients to the soil and aeration, and they are predators of



other organisms in the environment regulating diversity (Hölldobler & Wilson

1990). Although they occupy all strata of an environment, many groups have

close relationships with plants, getting features like pollen and floral and extra

floral nectar and mostly protecting the plant host from other herbivores

(Delabie et al. 2007). The species composition of ants within assemblages is

influenced by the distribution of resources to be exploited and the strategies

used for obtaining, in this way, share the ecological niche with other

organisms (Silva & Brandão 2010, Silvestre et al. 2003).

The ant fauna, in comparative terms, is especially suitable for use as a bio-

indicator tool (ecological, environmental, and diversity) by presenting

relatively high local abundance, high local species richness (alpha diversity)

and high regional species richness (gamma diversity); it has many specialized

taxa which present with higher sensitivity to changes in the environment and

vegetation. Moreover, the taxon is sampled at a relatively low cost of

collection methodology; one previously defined sampling protocol, and is

usually easily separated into morphospecies, which make efficient processes

for conducting rapid inventories of biodiversity (Silvestre et al. 2012,

Hölldobler & Wilson 1990).

Inside the superfamily Vespoidea, Sapygidae, Bradynobaenidae,

Sierolomorphidae, and Rhopalosomatidae are considered rare with restricted

distribution and abundance, and Mutillidae, Pompilidae, Vespidae, Tiphiidae

and Scollidae are common in surveys in Brazil. These wasps are

phylogenetically related to the following groups: Chrysididae, Bethylidae,

Plumaridae and Apoidea Spheciformes (Peters et al. 2011).

Pompilidae contains 4,200 species distributed worldwide (Brothers &

Finnamore 1993) and the Neotropics have about 750 species (Fernández

2000).

Vespidae has about 4,500 described species, distributed in 268 genera

(Brothers & Finnamore 1993). Only three subfamilies are found in Brazil:

Masarinae, Eumeninae and Polistinae (Carpenter & Marques 2001).

Mutillidae contains around 10,000 species in the world and two of the

seven extant subfamilies are found in the Neotropics: Sphaerophtalminae and

Mutillinae (Brothers 2006, Brothers & Carpenter 1993). Their common name

velvet ant refers to their dense pile of hair. Their bright colors serve as

aposematic signals. Mutillidae exhibit extreme sexual dimorphism; the males

are winged and the females are wingless. Mutillidae are commonly associated

with the parasitism of bees.

Tiphiidae wasps are cosmopolitan, with predominance in tropical regions,

containing about 1,500 species distributed into seven subfamilies. The most



common species are parasitoids of Scarabaeoidea. Only some females and all

males are winged (Kimsey & Brothers 2006).

Scoliidae has about 300 species and five genera in the world and in the

Neotropics two genera of the subfamily Scoliinae are found: Campsomeris and

Scolia. The females have a robust aspect and digger habits. The most common

species are parasitoids of Scarabaeidae, Passalidae and Lucanidae (Fernández

2006).

Rhopalosomatidae consists of four genera and 40 species described

worldwide, and three genera and 20 species are known in Neotropical region

(Sarmiento 2006), and the genus Rhopalossoma is more commonly found in

open areas and sandbanks in Brazil.

The wasps are essential organisms for the maintenance of the population

of many arthropods, due to the fact that the diet of the larvae is based on

animal protein. Pompilidae feed on spiders almost exclusively;

Rhopalosomatidae feed on crickets; Vespidae eats mainly caterpillars, while

Scoliidae and Tiphiidae prefer beetles which they use for the development of

their larvae. The adults preferentially feed on nectar and so are potential

pollinators, or even mandatory Anthophilous (Auko et al. 2013, Hunt 1991).

Traditionally, all species of Vespoidea are called predators, while in the

development maturity the social wasps are progressively fed by adults, who

use more than one individual, thus being characterized as predation feeding

habits; the solitary species, which feed their larvae a different way, use only

one individual (except Eumeninae) as a host for their larvae, thus

characterizing a life cycle very similar to that found in the parasitic wasp,

traditionally called parasitoids (Godfray 1994). The difficulty in defining

groups Vespoidea inside the predatory and/or parasitoids behaviors should be

the great diversity of species presented in this group, which allows a wide

variety of habits and strategies, although belonging to the same taxon. Wasps

are a key element in understanding the evolution of social behavior, as they

comprise both species with solitary behavior and species that are truly social

(eusocial) (Hermes 2013).

Spheciforms refers to an extremely diverse cosmopolitan group of wasps.

There are currently 9,716 known living species in the world, distributed

among the following families: Heterogynaidae (8), Ampulicidae (200),

Sphecidae (735) e Crabronidae (8,773) (Pulawski 2014). Angarosphecidae is

extinct, and Heterogynaidae is restricted to the Old World (Amarante 2006,

Engel 2001). Amarante (2005, 2002) cataloged 1,928 species in the Neotropics

with the following richness: Crabronidae (1,732 species), and Sphecidae (196)

considering Ampulicinae as a subfamily of Sphecidae.



The females are usually solitary with hunters‟ habits; however, various

levels of social behaviors are found, including at least one example of

eusociality (Matthews 1991). Females can lay their nests by digging the sand,

soil, wood, occupying pre-existing cavities or even using materials such as

clay, waxes and plants for the construction of brood cells, which can be

individualized or joint (Amarante 1999). Almost all orders of insects are used

as prey, and some groups of springtails and spiders (Buschini et al. 2008,

Evans 2002, Bohart & Menke 1976).

In the world 16,000 species of bees are described with estimates of up to

20,000 species (Brady et al. 2009, Michener 2007, Pedro & Camargo 2000).

According to Roubik (1989), considering the new species proportionately

framed in groups under review; perhaps we would reach 40,000 species of

bees in the world. In the Neotropical region 5,600 species of bees are

recognized (Roubik 1995) and for the Brazil, Pedro & Camargo (2000)

estimate there are 3,000 species. According with Melo & Gonçalves (2005)

the faunal diversity of bees is restricted to a single family (Apidae),

considering five subfamilies Andreninae, Apinae, Colletinae, Halictinae and

Megachilinae, with 42 tribes and 219 species. The number of genera known in

Brazil for each subfamily of Apidae is: Halictinae (34), Colletinae (30),

Andreninae (30), Megachilinae (28) and Apinae 27 (+70), without the

inclusion of Anthophoridae (Silveira et al. 2006).

Bees, both social and solitary, are responsible for the maintenance of plant

diversity and ecological balance in most terrestrial ecosystems, and are

considered a keystone mutualistic species (O'Toole, 1993). They are one of the

most important pollinators in tropical forests in terms of number of species of

plants pollinated (Momose et al. 1998). If the bees disappeared the forests‟

structure would alter, because the plant species fertilized by bees would have a

diminished capacity to produce seeds. This essential "environmental service"

determines the formation of fruit and fertile seeds, which maintains genetic

diversity. The bees are not immune to "biodiversity crisis"; this is a big and

serious problem, because about 30% of human food derived from plants is

pollinated by bees (McGregor 1976 apud O'Toole, 1993).

In this study we described a species occurrence for Hymenoptera in two

expressive continuous dry forests along midwestern Brazil, trying to estimate

species richness for each taxon and check which model the distribution of

these groups of aculeate Hymenoptera present in this type of forestry

formation.



METHODS

Study Site

We had been surveying two particular dry forest regions located in Brazil.

We surveyed seventeen localities along one continuous block of deciduous

forest from September 2005 to February 2013. Seventeen wild expeditions

were performed in this period with seven days of collections in each, but not

with all expert groups together. To compose the sample unit we combined the

expeditions that have been made to the same location, and those performed in

nearby sites within a radius of 10 km buffers were grouped. Nine sites

emerged from this combination of collecting expeditions.

Plate 1. Nine buffers with 10 kilometers‟ radius sampled to Hymenoptera fauna in

deciduous forests areas in Bodoquena plateau and in Brazilian Chaco.

Parque Nacional da Serra da Bodoquena

The Bodoquena´s mountain range park (21º07´14,7”S 56º43´08,2”W-

central location) possesses 77,232 ha frames on Cerrado-Pantanal Biodiversity



Corridor; it is inserted on a core area of Atlantic Forest Biosphere Reserve.

The area is an environmental planning unit, being a watershed which supplies

the hydrological basin of western Brazil. The locality is sustained by

calcareous rocks of the Corumbá group-Neoproterozoic III. The lithological

characteristic of the tufas makes it possible to create a new unit, named Serra

da Bodoquena formation (Sallun Filho et al. 2009). It is characterized by a

high rocky massif, with altitudes varying between 200m and 770m asl.

Exposed limestone from the Tamengo formation predominates in this karstic

region, where rivers are found within canyons. The annual average

temperatures of the area fluctuate between 22°C and 26°C. The minimum

temperature can be as low as 0°C. The relative humidity is low and rarely

reaches 80%, and rainfall varies between 1300 mm and 1700 mm a year. The

hot and rainy season occurs between October and April, and the cold and dry

season from May to September.

Plate 2. Bodoquena mountain range in midwestern Brazil, with predominance of

deciduous and semi-deciduous plants species in carbonate rocks formation and iron

formation.

Brazilian Chaco

Porto Murtinho municipality, Mato Grosso do Sul State (MS) (21°42‟04”S

57°53‟06”W). Located in Central South America, the Gran Chaco is the more

extensive subtropical dry forest in the continent, and has approximately 3,400

plant species, including great diversity of plants with xeromorphic features

such as microfilia (small leaves), abundant thorns, underground systems and

stems adapted to drought (Pott et al. 2008, Prado 2000). With approximately

850,000 km2 and classified as Stepic Savanna (Silva & Abdon 2006), it covers



northern Argentina, western Paraguay, Bolivia and a small range in

southeastern Brazil (only 7 %). The Chaco is one of the major wooded

grassland areas in Central South America, and could therefore be of major

economic importance, although this resource is being overutilized and suffers

from intense degradation through unrestricted forest and bush clearing,

overgrazing and continuous monoculture. It is important to stress that there is

no desert zone within the Gran Chaco and that it extends into both tropical and

temperate zones. This vast region is an almost flat plain sloping gradually

eastwards, varying from 100 - 500 m above sea level, except for the Sierras in

Cordoba, Argentina, which reach 2,800 m; some hills in Paraguay are over

700 m (Riveros, 2002).

The name Chaco derives from the Quechua "Chaku" which means

"hunting territory", an allusion to the annual hunting expeditions, undertaken

by the Inca Empire in the region in pre-Columbian period (Pott et al. 2008). It

presents great diversity of ecosystems, high species diversity and endemism of

relatively high compared to other arid environments, semi-arid and sub-humid

(Silva et al. 2000, Redford et al. 1990).

Plate 3. Brazilian Chaco in Porto Murtinho Municipality. Aspects of diversified dry

forest vegetation.

A small fraction of the Chaco located in Brazil, bordering the extreme

south of Pantanal lowland, named Nabileque sub-region, is a part of the

portion known as Oriental or Humid Chaco, presents floristic contacts between

Chaco/Cerrado, Chaco/Dry Forest, Chaco/Limestone Forest, and others as an



extensive arboreal monodominant formation named Carandazal-Copernicia

alba Morong (Fava et al. 2008, Delsinne et al. 2007, Abdon & Silva 2006).

Sampling Protocol

For sampling Hymenoptera we used the following techniques:

Entomological net: The search for Hymenoptera specimens was

performed on trails in the woods, flowers on the banks of rivers and

streams, and directly into the nests. The sampling effort was five days

per location for a total of six hours daily.

Moërick traps: For each sampling event we utilized 50 yellow pans

arranged in transects of 500 m with 10 m distance between traps, and

collected after 24 hours. The specimens were transferred to alcohol

96%.

Malaise traps: A Malaise trap is a large, tent-like structure used

for trapping flying insects, particularly Hymenoptera and Diptera.

Insects fly into the tent wall and are funneled into a collecting vessel

attached to the highest point. Four Malaise traps were set at ground

level in each area, arranged for a period of five days per locality.

Mini-Winkler apparatus: The leaf-litter sampling was realized

following Ants of the Leaf Litter protocol. For each sample unit one

square meter of leaf-litter was extracted in Winkler´s apparatuses

covering one area with 10,000 m2. The sampling site was chosen by

selective form inside of each point, seeking the best micro-habitats for

the leaf-litter extraction in the forest, in general, near to the biggest

trees. In each sampling point material was extracted until we reached

the superficial soil layer. The sifted volume with up to 2 kg was

transferred to a collector bag. In the field laboratory this material was

extracted with mini-Winkler apparatus for 24 hours, and after this

period, the specimens were put in Eppendorfs pots.

Attractive baits: The bait, containing 1 cm3 of sardine, was dispersed

in a piece of paper for 1 h. A total of 100 baits were used in each of

the sampled areas.

Aromatic essences: Attractive with aromatic compounds for capturing

Euglossine males contain cineol, methyl salicylate, methyl benzoate,



eugenol, and vanillin. Fifty traps were performed (ten sets of five

baits) dispersed at 200 meter intervals.

In the Hymenoptera Ecology Laboratory (HECOLAB-UFGD) all

Hymenoptera species were kept in entomological pins. The voucher specimens

were deposited in the Biodiversity Museum of Universidade Federal da

Grande Dourados (UFGD), Mato Grosso do Sul State, Brazil.

Data Analyses

We adopt the concept of range, which is defined as the number of sites

occupied by a species within a region and the concept of relative abundance of

species, which is defined as the frequency distribution of absolute abundance

of the sites, is used to refer to the common or rare species in a community

(Magurran & McGill 2011).

The frequencies of species based in presence/absence were analyzed in the

range of region and grouped into classes or octaves of abundance (Lobo &

Favila 1999, Magurran 1988). The number of species in each octave varied as

follows: 1 (0-2); 2 (2-4); 3 (4-8), 4 (8-16) and so on, allowing us to view the

richness and quantitative distribution of species per sample unit. The data set

was analyzed using R software with the Vegan package (R Development Core

Team, 2010).

The sampling data of the nine samples localities were organized in

different data matrix for each family of the aculeate Hymenoptera plotted in

the software Microsoft Excel (2007). Only the presence/absence (occurrence)

of species sampled, importing the data matrix into the EstimateS (Colwell,

2013), assess and compare the diversity and composition of species

assemblages based on sampling data computed on this software. We built a

table with the same values obtained of diversity analyses, as the Shannon

diversity index, Chao 1 richness estimator and Second-order Jackknife

richness estimator (Jack2). When comparing species similarity of nine

localities, we calculate and use Morisita-Horn sample similarity index, using

also distance in kilometers between localities obtained with the software

Google Earth 7.1.2., which was compared with the similarity values obtained

and distance using a Pearson correlation computed on the software Statistica

8.0 (Statsoft Inc. 2007).



RESULTS

In total 763 species were identified and morphospecies of Hymenoptera

Aculeata (excluding Chrysidoidea) in 236 genera, classified in 10 families

(Appendix), in midwestern Brazilian dry forest, with 1,551 registers in nine

localities sampled. Some species illustrating the Hymenoptera fauna are in

Plates 4-10.

Formicidae was represented by all live subfamilies in the Neotropical

region. We sampled 294 species in 66 genera. The richest genera sampled was

Pheidole (27 species), Hypoponera (21), Pachycondyla (17), and Cephalotes,

and Camponotus with 16 species each.

We sampled for the Apidae 992 individuals belonging to 150 species in 65

genera, but 59 species could not be named or properly classified; only

morphospecies by a single expert, that was due to the absence of current

revisions of some genera and species of bees. All Apidae subfamilies present

in Brazil were sampled in the Bodoquena Plateau and Brazilian Chaco, Porto

Murtinho region. Apinae was the richest subfamily with 87 species and 41

genera, of which 18 species correspond to stingless bees (Meliponina). The

other subfamilies, in decreasing order, were Halictinae (28 species in nine

genera), Megachilinae (27 species in 10 genera), Colletinae (six species in

three genera), and Andreninae (two species in 2 genera). The richest genera

sampled were Megachile (15 species), and Ceratina and Augochlora with nine

species each.

We sampled 94 species of Spheciformes wasps (Apoidea) in 42 genera

being Crabronidae (74 species in 34 genera), and Sphecidae (20 species in 8

genera). Eremnophila binodis (Fabricius) (Sphecidae) was the most abundant

species recorded from the Spheciformes with 35 individuals collected. The

Crabronidae species Clitemnestra paraguayana Bohart, 2000, Trypoxylon

marginatum Cameron, 1912, and Stenogorytes megalommiformis (Strand,

1910) are recorded for the first time in Brazil.

A total of 225 species and 63 genera of the Vespoidea, in six families

(excluding Formicidae), were sampled, being Pompilidae (103 species and 22

genera), Vespidae (79 species and 25 genera), Mutillidae (21 species and 8

genera), Tiphiidae (15 species and 6 genera), Scoliidae (six species and one

genus), and Rophalosomatidae (one species and one genus). The more diverse

genera were Notochypus (Pompilidae) and Mischocyttarus (Vespidae) with

about 12 species sampled, and Ageniella and Pepsis with 10 species recorded,

both Pompilidae. Epipompilus aztecus (Cresson, 1869) (Pompilidae) was

registered for the first time in South America (Silvestre et al. 2010).



Plate 4. Bombus sp. (Apidae).

Plate 5. Argogorytes umbratilis (Crabronidae).



Plate 6. Poecilopompilus sp. (Pompilidae).

Plate 7. Proctonectarina sp. (Vespidae).



Plate 8. Traumatomutilla sp. (Mutillidae).

Plate 9. Cephalotes clypeatus (Formicidae).



Plate 10. Cylindromyrmex brasiliensis (Formicidae).

The estimated richness and Shannon diversity index for all taxa is

presented in Table 1. The richness for Hymenoptera Aculeata is estimated to

be up to 1,400 species, excluding Chrysidoidea wasps.

In the species abundance distribution (SAD) a truncated lognormal

distribution profile was verified for all taxa analyzed (Figure 1). This kind of

distribution denotes expressive rarity of species where the “hollow curve” is

configured between the first and second abundance octaves.

The similarity between the sampled point‟s buffers with 10 km radius

indicates no correlation with distance. Less than 40% of faunistic similarity is

explained by the proximity of the areas (r= -0,397). This pattern indicates high

beta diversity in this region (Figure 2).

Table 1. Richness estimated for Hymenoptera Aculeata in midwestern

Brazilian dry forest, and diversity index

Taxon Species Jack-II Chao 1 Shannon

Observed Estimated Estimated Diversity Index

Ants 294 468.58 443.50 5.40

Bees 150 310.63 369.19 4.84

Spheciformes 94 182.05 186.42 4.34

Vespoidea 225 444.81 516.26 5.12

Total 763 1,406.09 1,476.77 6.36



Figure 1. Distribution models for Hymenoptera, based on abundance of octaves,

sampled in midwestern Brazilian dry forest, between the years 2005 and 2013, in 9

buffer localities from Bodoquena mountain range to Brazilian Chaco.

Figure 2. Correlation analysis between similarities, based on Morisita-Horn index, and

distance in kilometers of the sampled points in midwestern Brazilian dry forest,

between the years 2005 and 2013, in 9 buffer localities from Bodoquena mountain

range to Brazilian Chaco (r= -0,397).

0

0.1

0.2

0.3

0.4

0.5

0 50 100 150 200Sim

ilari

ty (

Mo

risi

ta-

Ho

rn)

Distance Km



CONCLUSION

To detect and describe the fauna of a given region, and interpret the data

obtained in the field, does not constitute an easy task, even for relatively

undiversified groups. The preparation of a list of any vertebrate or invertebrate

taxon is not a trivial task and involves, besides the use of specific and efficient

techniques to sample a particular group, a reasonable knowledge of their

systematics, taxonomy, ecology and natural history in general (Lewinsohn &

Prado 2005). Faunal inventories currently are the most direct way to access

and experience the diversity of the components of the biome or locality in a

given space and time; however, the biological diversity cannot be reduced to

knowledge of the taxa that occur in a given area. This limitation of the

approach renounces the background history of the evolution of the area. The

species abundance distribution (SAD) is one of the most studied patterns in

ecology due to its potential insights into commonness and rarity, community

assembly, and patterns of biodiversity. However, the distribution pattern of

species abundance found in this study revealed that the Hymenoptera fauna on

dry forests is strongly influenced by the rarity of the species, or else there are a

great number of species with low frequency of occurrence and a smaller

number of species with high frequency of occurrence in all Hymenoptera

groups presented in this study. It is well established that the Hymenoptera

community is composed of a few common and many rare species.

The low similarity between the sampled points suggests that the aculeate

species are randomly distributed over the region. There is a trend of the

similarity between the samples to decrease with increasing distance (r=-0.39).

Consecutive sampled sites suggest a strong formation effect and the influence

of adjacent areas, considering the Cerrado matrix where the dry formations are

encountered, which are evidenced by high beta diversity, with different

arrangements of this Hymenoptera fauna and a high turnover in species across

sample points.

Hanson and Gauld (1995) registered the Hymenoptera fauna in Costa Rica

with the following richness in the families: Apidae (700), Formicidae (620),

Spheciformes (400), Vespidae (180), Pompilidae (250), Mutillidae (300),

Tiphiidae (30), Scoliidae (15), and Rhopalosomatidae (8). The richness

sampled in the Brazilian dry forest was approximately 40% of the fauna

richness of the Tiphiidae, Scoliidae, Pompilidae and Formicidae found in

Costa Rica that can be considered interchangeable between the fauna of South

and North America.



Rasmussen and Asenjo (2009) reported species-group taxa of aculeate

wasps of Peru and presented the first checklist of the 225 genera and 1,169

species, including Chrysidoidea wasps, not considered here; in this work they

sampled 301 species of Spheciformes (Crabronidae 262, Sphecidae 38, and

Ampulicidae 1), and 691 species of Vespoidea (Vespidae 403, Pompilidae

158, Mutillidae 88, Tiphiidae 32, Scoliidae 8, and Rhopalossomatidae 2),

totaling 992 species/morphospecies sampled of these aculeate wasp families in

Peru. In our work we obtained 319 species/morphospecies of these wasps‟

families in a small region of dry forest localities in midwestern Brazil.

All Vespoidea families occurring in Brazil were sampled here; about 50 %

of the genera of Vespoidea recognized from Brazil were sampled in this dry

forest region. The diversity of species of Vespoidea recorded here is higher

than in other biomes in Brazil, although the methods used in those studies are

not standardized (Santos et al. 2014, Morato et al. 2008). When comparing

only species of social wasps (Polistinae), the diversity of the dry forest was

similar to the work carried out in the Atlantic Forest (Tanaka Jr. & Noll 2011,

Santos et al. 2007), but was much lower than that observed in the Amazon

region by Silveira et al. (2008).

The diversity of Mutillidae (20 species registered) is underestimated due

to the difficulty of determining species and association between males and

females. These wasps are more common in savannahs or semi-desert areas

(Hanson & Gauld 2006). Previous studies have reported that Ageniella

(Pompilidae) and Ephuta (Mutillidae) are the richest tropical forests in the

Vespoidea genera (Santos et al. 2014, Morato et al. 2008). In our work Pepsis,

Ageniella, and Notocyphus were the richest genera in number of species

between Vespoidea groups. Pepsis is the most diverse genus in open

environments (Vardy 2000), and Notocyphus is associated with the presence of

other genera, as its species are cleptoparasitic of other Pompilidae.

Due to the shortage of Spheciformes specialists in Brazil, knowledge of

the group is incipient. Large gaps are still found in the geographical

distribution of the species and information about their biology are still

presented in a fragmented way, whereby a small number of species, which are

generally more tolerant of anthropogenic presence, are better known than most

rare and sensitive organisms.

Ruiz et al. (2002) catalogued 615 Spheciformes species in Mexico, and

Rasmussen and Asenjo (2009) registered 301 species of these wasps in Peru.

Amarante (2002) recorded 633 species in Brazil, and in the Mato Grosso do

Sul he indicates 57 species. In this work we obtain 94 Spheciformes species.



In this work we observed a nearby association of certain species to the

physical structure of environments, such as in areas with exposed soil and

riverbanks, where we observed that species make their nests by digging the

soil; for example, Argogorytes umbratilis (R. Bohart 2000), and Penepodium

sp. were observed nesting in exposed soil areas. At these sites we also

observed the activity of collecting mud by Sceliphron asiaticum (Linnaeus,

1758) which uses clay to build grouped cells in protected sites, as in the bark

of trees, rocky outcrops, or in cave walls and often more tolerant species use

human buildings. Other species use pre-existing cavities in which to supply

food for their offspring, as observed with the genera Podium and Trypoxylon.

We also observed the nesting activity of digger sand wasps (Bembicini) in

open areas of exposed sandy soils, common in dry forests in this region.

The number of bee species presented in this study differs from sampling in

areas of dry forest made by other researchers in other Neotropical localities.

Osorio-Beristain et al. (1997) recorded the bee fauna of the Biological Station

of Chamela, Mexico, composed of 87 genera and 228 species. Vinson et al.

(1993) in Costa Rica (Tempisque dry forest) reported 250 species. The lowest

species richness found in this study is probably due to the smaller size of the

sampled area. However, our inventory compared to that performed by

Gonçalves & Brandão (2008 ) in 17 selected localities, using Malaise traps,

representing a gradient of almost 20° of latitude in evergreen pristine Atlantic

Forest, was superior in number of species and genera sampled (107 species

and 50 genera for Atlantic Forest).

Vergara (2002) in the Central Plateau of Mexico detected the same pattern

of distribution of abundance found in this work for bees. In contrast to

modified landscapes, such as agroecosystems, with intensive management it is

possible to create homogenous habitats which often indicate a loss of rare taxa

and keystone species and dominance of a few aggressive/opportunistic species

of aculeate Hymenoptera (Vinson et al. 1993; Gess & Gess, 1993). Batista-

Matos et al. (2013) consider the solitary bees, and conclude that the least

disturbed and oldest areas shelter a greater richness and rare species; while the

types of land use more intensively managed house the greatest abundance and

lower species diversity.

New records of ant distributions were obtained in this work for Brazilian

dry forest. Probolomyrmex brujitae Agosti, 1995 and Atta saltensis Forel,

1913 were previously reported only in Argentina and Uruguay, and Gracilidris

pombeiro Wild & Cuezzo, 2006 only in Paraguay. This ant inventory is

comparable to that made by Groc et al. (2013) in a Pristine Amazon Forest in

French Guiana in the number of genera sampled.



We verify for leaf litter ants a specificity of micro-environmental niche in

the samples, and that many species‟ population have geographical restrictions,

where many unpredictable filters may be operating. Many specialized species

with reduced amplitudes inserted into specific guilds were observed. There is a

strong selective pressure induced by the action of fragmentation both locally

and within the limits of the biome/region, which may cause effects of chaotic

vicariates.

The result of the model abundance distribution of Hymenoptera species in

dry forest areas presented here follows the expected pattern of most large

assemblies studied by ecologists who follow a log normal pattern of

abundance of species. The log normal model shows that diversity is influenced

by the rarity of the species; this indicates that there is also a better structure

and higher occupation of niches in ecosystems with more conserved

landscapes, consequently having a greater number of micro-habitats

(Magurran, 2004). One aspect is extremely important for the conservation of

aculeate Hymenoptera observed in the dry forest in this study, which is the

maintenance of the integrity of the environments in many localities near rivers

and hills are actually more preserved than plane areas where agriculture and

livestock alter the integrity of the landscape (Silva, 2009).

The study area has a high diversity and high anthropogenic pressure; it

harbors endemic species and has among the phytophysiognomic components

one of the largest continuous examples of this type of vegetation in South

America. The seasonal deciduous forests play a role key in the distribution of

various elements of the fauna and flora (Morrone 2006, Morrone et al. 2004,

Spichiger et al., 2004, Prado & Gibbs 1993). The studied sites are located

diagonally from open areas and have a great variety of species, including

endemic species (Souza 2005, Colli et al. 2002, Duellman 1999).

The assessment and identification of priority areas and actions for

biodiversity conservation in Brazilian Biomes (MMA, 2002) has been

identified through studies of invertebrate fauna, mammals, birds, reptiles,

amphibians, and fishes in Bodoquena Plateau and Brazilian Chaco, which are

considered to be sites of very high biological importance, being extremely

diverse; this needs to be urgently reflected as a hotspot.

ACKNOWLEDGEMENTS

We are thankful to the Brazilian Institution CAPES and CNPq, and to the

Instituto Chico Mendes de Biodiversidade- ICMBio in Bonito, MS. We would



like to thank the people who helped us in field: Vander Carbonari, Hadassa

Costa, Fabiola Oliveira, Tainá Greice Ensina, Murilo Moressi, Luna Carinyana

Silvestre, Guilherme Dalponti, Nelson Rodrigues da Silva, and Sr. Neil and

family in Pitangueiras farm. We are also grateful to the owners of RPPN, Cara

da Onça Edson and Gerson; to Eduardo F. Santos for Pompilidae species

confirmations; and Bolivar Garcete Barrett for Eumeninae, Sphecidae and

Crabronidae identifications. Collections permit IBAMA number 10674-

11/09/2007. This work is dedicated to Maria Alice Silvestre in memoriam.

APPENDIX

Checklist of Hymenoptera sampled in midwestern Brazilian dry forest

Species/Morphospecies

Formicidae Acanthostichus brevicornis Emery, 1894

Acanthostichus sp.

Acromyrmex crassispinus (Forel, 1909)

Acromyrmex rugosus

Acromyrmex subterraneus (Forel, 1893) Acromyrmex sp. 1

Acromyrmex sp. 2

Anochetus diegensis Forel, 1912 Apterostigma auriculatum Wheeler, 1925

Apterostigma manni Weber, 1938

Apterostigma pilosum Mayr, 1865 Apterostigma wasmanni Forel, 1892

Asphinctanilloides sp. n Atta sexdens Linnaeus, 1758

Atta sp. 1

Atta saltensis Forel, 1913 Azteca alfari Emery, 1893

Azteca chartifex Emery, 1896 Azteca constructor Emery, 1896

Azteca sp. 1

Azteca sp. 2 Basiceros disciger (Mayr, 1887)

Blepharidatta conops Kempf, 1967



Brachymyrmex patagonicus Mayr, 1868

Brachymyrmex sp. 1 Brachymyrmex sp. 2

Brachymyrmex sp. 3 Brachymyrmex sp. 4

Camponotus crassus Mayr 1862

Camponotus melanoticus Emery, 1894

Camponotus (Myrmaphaenus) blandus blandus (Smith, F. 1858)

Camponotus (Myrmobrachys) mus Roger, 1863

Camponotus (Myrmothrix) renggeri Emery, 1894

Camponotus (Myrmothrix) rufipes (Fabricius, 1775)

Camponotu s (Myrmobrachys) senex (Smith, F., 1858) Camponotus (Myrmepomis) sericeiventris Guérin-Méneville, 1838

Camponotus (Myrmocladoecus) sexguttatus (Fabricius, 1793)

Camponotus (Tanaemyrmex) termitarius Emery, 1902 Camponotus sp. 1

Camponotus sp. 2 Camponotus sp. 3

Camponotus sp. 4

Camponotus sp. 5 Camponotus sp. 6

Carebara sp. 1

Carebara sp. 2

Cephalotes atratus (Linnaeus, 1758)

Cephalotes borgmeieri (Kempf, 1951) Cephalotes clypeatus (Fabricius, 1804)

Cephalotes depressus (Klug, 1824)

Cephalotes eduarduli (Forel, 1921) Cephalotes guayaki De Andrade& Baroni Urbani, 1999

Cephalotes incertus (Emery, 1906) Cephalotes jheringi (Emery, 1894)

Cephalotes maculatus (Smith F., 1876)

Cephalotes minutus (Fabricius, 1804) Cephalotes pallens (Klug, 1824)

Cephalotes pellans De Andrade & Baroni Urbani, 1999 Cephalotes persimilis De Andrade & Baroni Urbani, 1999

Cephalotes pusillus (Klug, 1824)

Cephalotes sp. 1 Cephalotes sp. 2

Cerapachys splendens Borgmeier, 1957

Crematogaster acuta (Fabricius, 1804) Crematogaster bruchi Forel, 1912

Crematogaster crinosa Mayr, 1862



Crematogaster curvispinosa Mayr, 1862

Crematogaster quadriformis Roger, 1863 Crematogaster stollii Forel, 1885

Crematogaster sp. 1 Crematogaster sp. 2

Crematogaster sp. 3

Crematogaster sp. 4 Cryptomyrmex boltoni (Fernández, 2003)

Cylindromyrmex brasiliensis Emery, 1901

Cyphomyrmex (gr. rimosus) sp. 1


Cyphomyrmex (gr. rimosus) sp. 3 Cyphomyrmex (gr. rimosus) sp. 4


Cyphomyrmex (gr. rimosus) sp. 6 Cyphomyrmex (gr. rimosus) sp. 7

Cyphomyrmex (gr. rimosus) sp. 8 Cyphomyrmex (gr. strigatus) sp. 1

Cyphomyrmex (gr. strigatus) sp. 2

Cyphomyrmex lectus (Forel, 1911) Cyphomyrmex olitor Forel, 1893

Cyphomyrmex sp. 1

Dinoponera australis Emery, 1901

Dolichoderus bispinosus (Olivier, 1792)

Dolichoderus lutosus (F. Smith, 1858) Dolichoderus lujae Santschi, 1923

Dolichoderus sp.

Dorymyrmex bicolor Wheeler, 1906 Dorymyrmex brunneus Forel, 1908

Dorymyrmex thoracicus Gallardo, 1916 Dorymyrmex sp.

Eciton burchellii (Westwood, 1842)

Ectatomma brunneum Smith, 1858 Ectatomma edentatum Roger, 1863

Ectatomma opaciventre (Roger, 1861) Ectatomma permagnum Forel, 1908

Ectatomma suzanae Almeida, 1986

Ectatomma tuberculatum Olivier, 1792 Forelius sp. 1

Gnamptogenys (gr. striatula) sp.1

Gnamptogenys striatula Mayr, 1884 Gnamptogenys sulcata (Smith, F. 1858)

Gracilidris pombeiro Wild & Cuezzo, 2006



Heteroponera microps Borgmeier, 1957

Hylomyrma balzani (Emery, 1894) Hylomyrma sp. 1

Hypoponera sp. 1 Hypoponera sp. 2

Hypoponera sp. 3


Hypoponera sp. 6

Hypoponera sp. 7

Hypoponera sp. 8


Hypoponera sp. 11



Hypoponera sp. 16


Hypoponera sp. 19

Hypoponera sp. 20

Hypoponera sp. 21

Kalathomyrmex emeryi (Forel, 1907) Labidus coecus (Latreille, 1802)

Labidus mars (Forel, 1912)

Labidus praedator (Fr. Smith, 1858) Leptogenys sp.

Linepithema humile (Mayr, 1868) Linepithema micans (Forel, 1908)

Linepithema sp. 1

Linepithema sp. 2 Megalomyrmex silvestrii Wheleer, 1909

Megalomyrmex wallacei Mann, 1916 Monomorium floricola Jerdon, 1851

Monomorium sp.

Mycetarotes sp. Mycocepurus goeldii (Forel, 1893)

Mycocepurus smithi (Forel, 1893)

Mycocepurus sp. Myrmelachista sp.

Myrmicocrypta sp. 1



Myrmicocrypta sp. 2

Neivamyrmex carettei (Forel, 1913) Neivamyrmex sp. 1

Neivamyrmex sp. 2 Nomamyrmex esembecki (Westwood, 1842)

Nesomyrmex spininodis (Mayr, 1887)

Nylanderia fulva (Mayr, 1862) Nylanderia sp. 1

Nylanderia sp. 2

Nylanderia sp. 5

Octostruma balzani (Emery, 1894)

Octostruma iheringi (Emery, 1888) Octostruma rugifera (Mayr, 1887)

Octostruma stenognatha Brown & Kempf, 1960

Octostruma sp. 1 Octostruma sp. 2

Octostruma sp. 3 Octostruma sp. 4

Odontomachus bauri Emery, 1892

Odontomachus meinerti Forel, 1905 Odontomachus sp. 1

Oligomyrmex sp.

Oxiepoecus sp.

Pachycondyla apicalis (Latreille, 1802)

Pachycondyla bucki (Borgmeier, 1927) Pachycondyla constricta (Mayr, 1884)

Pachycondyla crassinoda (Latreille, 1802)

Pachycondyla ferruginea (Smith, F. 1858) Pachycondyla harpax (Fabricius, 1804)

Pachycondyla inversa (Smith, F. 1858) Pachycondyla lunaris (Emery, 1896)

Pachycondyla luteola (Roger, 1861)

Pachycondyla marginata (Roger, 1861) Pachycondyla mesonotalis (Santschi, 1923)

Pachycondyla obscuricornis Emery, 1890 Pachycondyla striata (Smith F., 1858)

Pachycondyla verenae (Forel, 1922)

Pachycondyla villosa (Fabricius, 1804) Pachycondyla sp. 1

Pachycondyla sp. 2

Paraponera clavata (Fabricius, 1775) Paratrechina longicornis (Latreille, 1802)

Paratrechina sp. 1



Paratrechina sp. 2

Paratrechina sp. 3 Paratrechina sp. 4

Paratrechina sp. 5 Pheidole (gr. flavens) sp.

Pheidole cornicula Wilson, 2003

Pheidole dinophila Wilson, 2003 Pheidole gertrudae Forel, 1886

Pheidole gigaflavens Wilson, 2003

Pheidole jelskii Mayr, 1884

Pheidole oxyops Forel, 1908

Pheidole radoskowiskii Mayr, 1884 Pheidole scapulata Santschi, 1923

Pheidole spininodis Mayr, 1887

Pheidole transversostriata Mayr, 1887 Pheidole vafra Santschi, 1923

Pheidole sp. 1 Pheidole sp. 2

Pheidole sp. 3


Pheidole sp. 6

Pheidole sp. 7

Pheidole sp. 8


Pheidole sp. 11



Pogonomyrmex abdominalis Santschi, 1929

Pogonomyrmex micans Forel, 1914 Pogonomyrmex uruguaiensis Mayr, 1887

Pogonomyrmex naegelli Emery, 1878 Prionopelta marthae Forel, 1909

Probolomyrmex boliviensis Mann, 1923

Probolomyrmex petiolatus Weber, 1940

Probolomyrmex brujitae Agosti, 1995

Procryptocerus attenuatus Smith, 1876

Procryptocerus montanus (Kempf, 1957) Procryptocerus sp.

Pseudomyrmex (gr. ferrugineus) sp. 1



Pseudomyrmex (gr. oculatus) sp. 1

Pseudomyrmex acanthobius (Emery, 1896) Pseudomyrmex denticolis (Emery, 1890)

Pseudomyrmex gracilis (Fabricius, 1804) Pseudomyrmex pallidus (Smith, 1855)

Pseudomyrmex termitarius (Smith F., 1855)

Pseudomyrmex sp. 1 Pseudomyrmex sp. 2

Rogeria alzatei Kugler, 1994

Rogeria lirata Kugler, 1994

Rogeria sp. 1

Rogeria sp. 2 Serycomyrmex (gr. amabilis) sp. 1

Serycomyrmex (gr. amabilis) sp. 2

Serycomyrmex sp. Solenopsis (gr. germinata) sp.

Solenopsis (gr. invicta) sp. 1 Solenopsis (gr. invicta) sp. 2

Solenopsis (gr. rimulus) sp. 1

Solenopsis invicta Burren, 1972 Solenopsis pusillignis Trager, 1991

Solenopsis sp. 1

Solenopsis sp. 2

Solenopsis sp. 3

Solenopsis sp. 4 Solenopsis sp. 5

Solenopsis sp. 6

Solenopsis sp. 7 Solenopsis sp. 8

Stigmatomma armigerum (Mayr, 1887) Stigmatomma sp. 1

Stigmatomma sp. 2

Stigmatomma sp. 3

Strumigenys elongata Roger, 1863

Strumigenys eggersi Emery, 1809 Strumigenys xenochelyna (Bolton, 2000)

Strumigenys sp. 1

Strumigenys sp. 2 Strumigenys sp. 3

Strumigenys sp. 4

Strumigenys sp. 5 Strumigenys sp. 6

Tapinoma melanochepalum (Fabricius, 1793)



Thaumatomyrmex contumax Kempf, 1975

Thaumatomyrmex mutilatus Mayr, 1887 Trachymyrmex urich (Forel, 1893)

Trachymyrmex sp. 1 Trachymyrmex sp. 2

Trachymyrmex sp. 3

Typhlomyrmex rogenhoferi Mayr, 1862 Typhlomyrmex sp.

Wasmannia auropunctata (Roger, 1863)

Wasmannia lutzi Forel, 1908

Wasmannia sp. 1

Wasmannia sp. 2 Wasmannia sp. 3

Total= 294

Apidae sensu lato

Agapostemon sp. 1

Alepidosceles hamata Moure, 1947

Ancyloscelis cfr. apiformis (Fabricius, 1793)

Anthodioctes cfr. camargoi Urban, 1999

Anthodioctes sp. 1

Apis mellifera Linnaeus, 1756

Arhysosage flava Moure, 1958

Augochlora sp. 1

Augochlora sp. 2

Augochlora sp. 3

Augochlora sp. 4

Augochlora sp. 5

Augochlora sp. 6

Augochlora sp. 7

Augochlora thusnelda (Schrottky, 1909)

Augochlorella neocorinora

Augochlorella sp. 1

Augochlorella sp. 2

Augochlorella sp. 3

Augochloropsis cfr. tupacamaru (Holmberg, 1884)

Augochloropsis sp. 1








Austrostelis zebrata (Schrottky, 1905)

Bombus (Fervidobombus) morio (Swederus, 1787)

Bombus (Fervidobombus) pauloensis Friese, 1913

Bothranthidium lauroi Moure, 1947

Centris (Aphemisia) mocsaryi Friese, 1899

Centris (Hemisiella) tarsata Smith, 1874

Centris (Hemisiella) vittata Lepeletier, 1841

Centris (Heterocentris) analis (Fabricius, 1804)

Ceratina (Ceratinula) sp. 1

Ceratina (Ceratinula) sp. 2

Ceratina (Crewella) sp. 1




Ceratina sp. 1

Ceratina sp. 2

Ceratina sp. 3

Coelioxys (Acrocoelioxys) tolteca Cresson, 1878

Coelioxys (Acrocoelioxys) sp. 1

Diadasia cfr. willineri (Moure, 1947)

Diadasina riparia (Ducke, 1907)

Dialictus sp. 1

Dichanthidium exile Moure, 1947

Epanthidium bolivianum Urban, 1995

Epanthidium tigrinum (Schrottky, 1905)

Epicharis (Epicharana) flava Friese, 1900

Epicharis (Epicharis) bicolor Smith, 1854

Epicharis (Hoplepicharis) fasciata Lepeletier & Serville, 1828

Eufriesea auriceps (Friese, 1899)

Eufriesea violacea (Blanchard, 1840)

Euglossa (Euglossa) fimbriata Moure, 1968

Euglossa (Euglossa) townsendi Cockerell, 1904

Euglossa (Glossura) annectans Dressler, 1982

Eulaema (Apeulaema) cingulata (Fabricius, 1804)

Eulaema (Apeulaema) nigrita Lepeletier, 1841

Eulonchopria psaenythioides Brèthes, 1909

Exaerete smaragdina (Guérin, 1844)



Exomalopsis (Exomalopsis) auropilosa Spinola, 1853

Exomalopsis (Phanomalopsis) sp. 1

Exomalopsis sp. 1

Exomalopsis sp. 2

Exomalopsis sp. 3

Habralictus sp. 1

Habralictus sp. 2

Habralictus sp. 3

Habralictus sp. 4

Hylaeus sp. 1

Hylaeus sp. 2

Hylaeus sp. 3

Hylaeus sp. 4

Hypanthidium obscurius Schrottky, 1908

Leiopodus trochantericus Ducke, 1907

Lestrimelitta chacoana Roig Alsina, 2010

Lophopedia pygmaea (Schrottky, 1902)

Megachile (Acentron) verrucosa Brèthes, 1909

Megachile (Austromegachile) fiebrigi Schrottky, 1908

Megachile (Chrysosarus) bella Mitchell, 1930

Megachile (Chrysosarus) diversa Mitchell, 1930

Megachile (Chrysosarus) guaranitica Schrottky, 1908

Megachile (Leptorachis) rubricrus Moure, 1948

Megachile (Melanosarus) brasiliensis Dalla Torre, 1896

Megachile (Melanosarus) nigripennis Spinola, 1841

Megachile (Moureapis) apicipennis Schrottky, 1902

Megachile (Neochelynia) brethesi Schrottky, 1909

Megachile (Pseudocentron) curvipes Smith, 1853

Megachile (Pseudocentron) inscita Mitchell, 1930

Megachile (Sayapis) planula Vachal, 1909

Megachile (Tylomegachile) orba Schrottky, 1913

Megachile (Zonomegachile) gigas Schrottky, 1908

Melipona orbignyi (Guérin, 1844)

Melipona quinquefasciata Lepeletier, 1836

Melissodes nigroaenea (Smith, 1854)

Melissodes sexcincta (Lepeletier, 1841)

Melissodes tintinnans (Holmberg, 1884)

Melissoptila paraguayensis (Brèthes, 1909)

Melitoma nudipes (Burmeister, 1876)



Melitoma sp. 1

Mesocheira bicolor (Fabricius, 1804)

Mesoplia rufipes (Perty, 1833)

Moureanthidium paranaense Urban, 1995

Nananthidium willineri Moure, 1947

Neocorynura sp. 1

Osiris sp. 1

Oxytrigona tataira (Smith, 1863)

Paratetrapedia connexa (Vachal, 1909)

Paratetrapedia flaveola Aguiar & Melo, 2011

Paratetrapedia fervida (Smith, 1879)

Paratetrapedia leucostoma (Cockrell, 1923)

Paratetrapedia lineata (Spinola, 1853)

Paratetrapedia lugubris (Cresson, 1878)

Partamona cupira (Smith, 1863)

Pereirapis sp. 1

Plebeia droryana (Friese, 1900)

Plebeia sp. 1

Plebeia sp. 2

Plebeia sp. 3

Protosiris sp. 1

Ptiloglossa sp. 1

Ptilotrix cfr. relata (Holmberg, 1903)

Ptilotrix cfr. scalaris (Holmberg, 1903)

Ptilotrix sp. 1

Rhathymus bicolor Lepeletier & Serville, 1828

Rhophitulus sp. 1

Scaptotrigona depilis Moure, 1942

Schwarziana mourei Melo, 2003

Schwarzula timida (Silvestri, 1902)

Temnosoma sp. 1

Tetragona clavipes (Fabricius, 1804)

Tetragonisca fiebrigi (Schwarz, 1938)

Tetrapedia garofaloi Moure, 1999

Tetrapedia sp. 1

Tetrapedia sp. 2

Tetrapedia sp. 3

Tetrapedia sp. 4

Triepeolus sp. 1



Trigona aff. fuscipennis Friese, 1900

Trigona hypogea Silvestri, 1902

Trigona spinipes (Fabricius, 1793)

Trigona truculenta Almeida,1984

Trophocleptria sp. 1

Xylocopa (Neoxylocopa) suspecta Moure & Camargo, 1988

Xylocopa (Schonnherria) muscaria (Fabricius, 1775)

Xylocopa (Stenoxylocopa) nogueirai Hurd & Moure, 1960

Xylocopa sp. 1

Total= 150

Pompilidae

Ageniella sp. 1

Ageniella sp. 2

Ageniella sp. 3

Ageniella sp. 4

Ageniella sp. 5

Ageniella sp. 6

Ageniella sp. 7

Ageniella sp. 8

Ageniella sp. 9

Ageniella sp. 10

Agenioideus sp. 1

Agenioideus sp. 2

Aimatocare sp. 1

Aimatocare sp. 2

Anoplius (Arachnophroctonus) taschenbergi (Brèthes)

Anoplius sp. 1

Anoplius sp. 2

Anoplius sp. 3

Anoplius sp. 4

Aplochares sp.

Aporus sp. 1

Aporus sp. 2

Auplopus sp. 1

Auplopus sp. 2

Auplopus sp. 3

Auplopus sp. 4

Auplopus sp. 5



Auplopus sp. 6

Auplopus sp. 7

Auplopus sp. 8

Caliadurgus sp. 1

Caliadurgus sp. 2

Caliadurgus sp. 3

Caliadurgus sp. 4

Caliadurgus sp. 5

Caliadurgus sp. 6

Caliadurgus sp. 7

Ceropales sp. 1

Ceropales sp. 2

Dicranopilus sp. 1

Dicranopilus sp. 2

Entypus sp. 1

Entypus sp. 2

Entypus sp. 3

Entypus sp. 6

Epipompilus aztecus (Cresson, 1869)

Epipompilus sp. 1

Epipompilus sp. 2

Epipompilus sp. 3

Epipompilus sp. 4

Episyron conterminus conterminus (Smith, 1855)

Episyron sp. n

Euplaniceps sp. 1

Euplaniceps sp. 2

Euplaniceps sp. 3

Euplaniceps sp. 4

Notocyphus sp. 1

Notocyphus sp. 2

Notocyphus sp. 3

Notocyphus sp. 4

Notocyphus sp. 5

Notocyphus sp. 6

Notocyphus sp. 7

Notocyphus sp. 8

Notocyphus sp. 9

Notocyphus sp. 10



Notocyphus sp. 11

Notoplaniceps sp.

Paracyphononyx sp. 1



Pepsis crassicornis Mócsary, 1885

Pepsis sp. 1

Pepsis sp. 2

Pepsis sp. 3

Pepsis sp. 4

Pepsis sp. 5

Pepsis sp. 6

Pepsis sp. 7

Pepsis sp. 8

Pepsis sp. 9

Poecilopompilus sp. 1







Priochilus (Foximia) opacifrons Banks, 1944

Priochilus captivum Fabricius, 1804

Priochilus gloriosum Cresson, 1869

Priochilus cf. gracile Evans, 1966

Priochilus gracillimus Smith, 1855

Priochilus nobilis (Fabricius, 1787)

Priochilus nubilis Banks, 1946

Priochilus rhomboideusBanks, 1944

Priochilus scrupulum (Fox, 1897)

Priochilus sericeifrons (Fox, 1897)

Priocnemella sp. n

Priocnemella sp. 1

Priocnemella sp. 2

Priocnemella sp. 3

Tachypompilus sp. 1

Total= 103



Vespidae

Agelaia multipicta (Haliday, 1836)

Agelaia pallipes (Oliver)

Ancistroceroides alasteroides (Saussure, 1852)

Ancistroceroides atripes (Fox, 1902)

Ancistroceroides conjunctus (Fox, 1902)

Ancistroceroides rufimaculatus (Fox, 1902)

Ancistroceroides venuustus (Brèthes, 1905)

Apoica flavissima van der Vecht, 1972

Apoica pallens (Fabricius)

Brachygastra lecheguana (Latreille, 1824)

Brachygastra moulae Richards, 1978

Brachymenes discherus (Sausurre, 1852)

Ceramiopsis paraguaensis Bertoni, 1921

Eumenes rufomaculatus Fox, 1899

Hypalastoroides brasiliensis (Saussure, 1856)

Hypalastoroides elongatus (Brèthes, 1906)

Hypalastoroides nitidus (Brèthes, 1906)

Hypalastoroides paraguayensis (Zavattari, 1911)

Hypancistrocerus advena (Saussure, 1856)

Minixi brasilianum (Saussure, 1875)

Minixi suffusum (Fox, 1899)

Monobia angulosa Saussure, 1852

Monobia apicalipennis (Saussure, 1852)

Monobia schrottkyi Bertoni, 1918

Montezumia azurescens (Spinosa, 1851)

Montezumia ferruginea brasiliensis Saussure, 1856

Montezumia infernalis (Spinosa, 1851)

Montezumia pelagica sepulchralis Saussure, 1856

Montezumia petiolata Saussure, 1856

Montezumia sp.

Myschocyttarus latior Fox

Myschocyttarus sp. 1













Omicron sp. 1

Omicron sp. 2

Omicron sp. 3

Omicron sp. 4

Omicron spegazzinii (Brèthes, 1905)

Omicron tuberculatum (Fox, 1899)

Pachodynerus brevithorax (Saussure, 1852)

Pachodynerus corumbae (Fox, 1902)

Pachodynerus grandis (Willink & Roig0Alsina, 1998)

Pachodynerus guadulpensis (Saussure, 1853)

Pachodynerus nasidens (Latreille, 1812)

Pachodynerus serrulatus (Brèthes)

Pachymenes ghilianii (Spinosa, 1851)

Pachymenes picturatus Fox, 1899

Parancistrocerus longicornutus (Dalla Torre, 1904)

Plagiolabra andina Brèthes, 1906

Plagiolabra nigra Schulthess, 1903

Polistes canadensis (Linnaeus, 1758)

Polistes ferreri Saussure, 1853

Polistes simillimus Zikan, 1951

Polistes versicolor (Olivier, 1791)

Polistes sp. 1

Polistes sp. 2

Polistes sp. 3

Polybia ignobilis (Haliday, 1836)

Polybia occidentalis (Oliver, 1791)

Polybia sericea (Oliver, 1791)

Polybia sp.

Protonectarina sylveirae (Saussure, 1854)

Protopolybia exigua exigua (Saussure, 1906)

Santamenes novarae (Saussure, 1867)

Stenodynerus suffusus (Fox, 1902)

Zeta argillaceum (Linnaeus, 1758)

Zethus cylindricus (Fox, 1899)

Zethus diminutus (Fox, 1899)



Zethus romandinus (Saussure, 1852)

Zethus sessilis Fox, 1899

Total= 79

Crabronidae

Alinia sp.

Argogorytes umbratilis Bohart, 2000

Astata lugens Tashenber, 1870

Bembecinus sp.

Bicyrtes angulata (F. Smith, 1856)

Bicyrtes discisa (Taschember, 1870)

Bicyrtes lilloi (Willink, 1947)

Bicyrtes variegata (Olivier, 1789)

Bothynostethus sp.

Cerceris sp. 1

Cerceris sp. 2

Cerceris sp. 3

Cerceris sp. 5

Cliteminestra brasilica Bohart, 2000

Cliteminestra paraguayana Bohart, 2000

Ectemnius carinatus (Smith, 1873)

Ectemnius semipunctatus (Lepeletier & Brullé, 1835)

Ectemnius sp. 1

Ectemnius sp. 2

Hoplisoides vespoides (F. Smith, 1873)

Incastigmus iphis (Finnamore, 2002)

Incastigmus neotropicus (Kohl, 1890)

Incastigmus sp.

Larra bicolor predatrix (Strand, 1910)

Liris sp. 1

Liris sp. 2

Liris sp. 3

Liris sp. 4

Liris spp.

Lyroda sp.

Megistommum procerus (Handlirsch, 1888)

Metanysson sp.

Microbembex uruguayensis (Holbery, 1884)

Nitela (Tenila) sp.



Nitela sp.

Oxybelus peruvicus R. Bohart, 1993

Pison (gr. cressoni) sp.

Pison delicatum Menke, 1988

Pison longicorne Menke, 1988

Pison sp.

Pluto axillaris van Lith, 1979

Pluto nitens van Lith, 1979

Podagritus sp.

Rhopalum sp.

Rubrica nasuta (Christ, 1791)

Sagenista brasiliensis (Shukard)

Sagenista cayennensis (Spinola)

Scapheutes laetus (Smith, 1860)

Solierella sp. 1

Solierella sp.2

Stenogorytes megalommiformis (Strand, 1910)

Stenogorytes specialis (F. Smith, 1873)

Stictia punctata (Fabricius, 1775)

Stigmus sp. ♂

Tachysphex inconspicuus (W. F. Kirby, 1890)

Tachysphex ruficaudis (Taschenberg, 1870)

Tachysphex sp.

Tachytes chrysopyga (Spinola, 1841)

Tachytes coloratus R. Bohart, 1979

Tachytes fraternus (Taschenberg, 1870)

Tachytes hades Schrottky, 1903

Trypoxylon duckei Richards, 1934

Trypoxylon marginatum Cameron, 1912

Trypoxylon nitidissimum Richards, 1934

Trypoxylon oculare Menke,1968

Trypoxylon spp.

Trypoxylon Trypargilum (gr. albititarse) sp.

Trypoxylon Trypargilum sp. 1




Trypoxylon Trypargilum spp.

Trypoxylon Trypoxylon sp.



Zannyson sp.

Total= 74

Mutillidae

Atillum sp.

Hoplocrates monacha (Gerstaecker, 1874)

Hoplocrates sp.

Mickelia sp.

Ptilomutilla pennata André, 1905

Sphinctopsis sp. 1

Sphinctopsis sp. 2

Sphinctopsis turnalia (Cresson, 1902)

Suareztilla sp.

Timulla sp. 1

Timulla sp. 2

Timulla sp. 3

Timulla spp. ♂

Traumatomutilla graphica (Gerstaecker, 1874)

Traumatomutilla manca (Cresson, 1902)

Traumatomutilla sp. 1






Total= 21

Sphecidae

Ammophila sp. 1

Ammophila sp. 2

Eremnophila binodis (Fabricius, 1798)

Eremnophila melanaria (Dahlbom, 1843)

Eremnophila opulenta (Guérin-Méneville, 1838)

Isodontia costipennis (Spinola, 1851)

Isodontia sp.

Penepodium haematogastrum (Spinola, 1851)

Penepodium sp. 1

Penepodium sp. 2

Penepodium sp. 3



Penepodium sp. 4

Podium sp. 1

Podium sp. 2

Prionyx thomae (Fabricius, 1775)

Sceliphron asiaticum Linnaeus, 1758

Sceliphron fistularium Dahlbom, 1843

Sphex dorsalis Lepeletier, 1845

Sphex ingens F. Smith, 1856

Sphex servillei Lepeletier, 1845

Total= 20

Typhiidae

Aelurus sp. 1

Aelurus sp. 2

Epomidiopteron sp.

Myzinum sp. 1

Myzinum sp. 2

Myzinum sp. 3

Myzinum sp. 4

Myzinum sp. 5

Myzinum sp. 6

Myzinum sp. 7

Pterombrus sp. 1

Pterombrus sp. 2

Thiphiodes sp.

Tiphia sp. 1

Tiphia sp. 2

Total= 15

Scoliidae

Campsomeris (Pygodases) terrestris (Saussure, 1858)

Campsomeris sp. 1

Campsomeris sp. 2

Campsomeris sp. 3

Campsomeris sp. 4

Campsomeris sp. 5

Total= 6



Rhopalosomatidae

Rhopalosoma sp.

Total= 1

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Chapter 3

THE BRAZILIAN "CAATINGA":

ECOLOGY AND VEGETAL BIODIVERSITY

OF A SEMIARID REGION

Heloisa Helena Gomes Coe1

and Leandro de Oliveira Furtado de Sousa2

1Departament of Geography,

Universidade Estadual do Rio de Janeiro, Brazil 2Department of Vegetal Sciences,

Universidade Federal Rural do Semiárido, Brazil

ABSTRACT

In this chapter we present the ecological characteristics and vegetal

biodiversity of a typical Brazilian biome; Caatinga. The name "Caatinga"

comes from a Tupi-Guarani term that means "white forest" or "clear

forest" in reference to the clear gray appearance of the vegetation during

the dry season. It is an exclusively Brazilian semi-arid ecosystem

covering about 11% of the country. It extends over all the states of the

Northeast region and the north of Minas Gerais State, comprising an area

of 800,000 km2. The caatinga area extends from 2º54'S in the states of

Ceará and Rio Grande do Norte to 17º21'S in Minas Gerais State.

Generally, Caatinga is recognized as low-growing forest with

discontinuous canopy, deciduous foliage during the dry season and

xeromorphic characteristics shared by the species. However, Caatinga

physiognomies are extremely variable, depending on the rainfall regime


Heloisa Helena Gomes Coe and Leandro de Oliveira Furtado de Sousa

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which, in general, does not exceed 1,000 mm/year and is concentrated in

three or four months of the year. They also depend on the characteristics

of soils of different geomorphological and geological origins, varying

from high dry forests up to 15-20 m tall, in more favorable soils in more

humid environments, to rocky outcrops with sparse low shrubs and

Cactaceae and Bromeliaceae in the crevices.

Caatinga stands out for presenting a large diversity of plant species,

currently having 4,478 recognized species in 8 eco-regions with 12

different types of vegetation, many of which are endemic to the biome,

and others that can exemplify biogeographical relationships which help to

clarify the historical vegetation dynamics of the Caatinga itself as well as

the entire eastern area of South America.

Caatinga has been highly modified by diverse human activities. The

northeastern soils are suffering an intense process of desertification due to

replacement of natural vegetation with crops, done mainly through slash

and burn. Deforestation and irrigated cultivation are leading to soil

salinization, further increasing the evaporation of the soil water and

accelerating the process of desertification. Only the presence of the

adapted vegetation of Caatinga has prevented the transformation of

northeastern Brazil into a vast desert. Despite threats to the biome, less

than 2% of the Caatinga is protected as conservation units under full

protection.

I. INTRODUCTION

Despite the fact that the diversity of plants and animals in arid and semi-

arid environments occurs to a much lesser extent than in tropical forests, these

environments have a number of plants and animals adapted to their extreme

conditions, making them environments with high rates of endemic fauna and

flora.

In Brazil there are no deserts, but there is a semi-arid region, with unique

species and features, called “Caatinga”. The name "Caatinga" has a Tupi-

Guarani origin and means white forest. This name aptly characterizes the

aspect of vegetation during the dry season, when the leaves fall and only the

white and shiny trunks of trees and shrubs remain in the dry landscape

(Albuquerque & Banner, 1995).

It is the only exclusively Brazilian ecosystem, composed of a mosaic of

dry forests and shrub vegetation (steppe savanna), with enclaves of montane

rainforests and “cerrado” (Brazilian savanna) (Tabarelli & Cardoso da Silva,

2003). Until the present moment about 5,000 plant species have been recorded,


The Brazilian "Caatinga"

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approximately 300 of which are endemic (Giulietti et al., 2002), along with

185 fish species, 154 reptiles and amphibians, 348 species of bird and 148

species of mammal, when considering the plant formations typical to Caatinga

( MMA 2002 ).

In these groups of organisms, the level of endemism varies between 4.3 %

(birds) and 57% (fish) and, as said by Pennington et al. (2000), the biota of the

Caatinga has borne witness to the huge dry forest that was once distributed as

far as northern Argentina, through central Brazil. Also affecting the

biodiversity of the region is the maintenance of human populations through the

exploitation of important natural resources, such as firewood and medicinal

plants, and the environmental services provided by this ecosystem on a

regional and global scale (Gil, 2002). Perennial water streams are very rare in

the area of caatinga, confirming the high water deficit responsible for this

vegetation type.

As it does not show the green exuberance of tropical rainforests, which are

of such great importance in Brazil, and due to the dry appearance of

physiognomies dominated by cacti and shrubs, the Caatinga vegetation

suggests, to a less trained eye, a low diversification of fauna and flora. Among

the Brazilian biomes, the Caatinga is probably the most undervalued and

poorly known scientifically. This situation is due to an unjustified belief,

which should no longer be accepted, that the Caatinga is the result of the

modification of another plant formation, is associated with a very low diversity

of plants, without endemic species and is highly modified by human actions

(Giulietti et al., 2002). Despite being really rather altered, particularly in the

lowlands, the Caatinga is a biome of wide biodiversity, with biological

relevance and peculiar beauty, especially in regard to the multiplicity of plant

communities, formed by a range of combinations of soil types and

microclimate variations, besides the significant proportion of rare and endemic

taxa, many of which are commonly used by the population for their

therapeutic properties.

The variety of strategies used by the species to survive during the periods

of lack of rainfall are numerous and of great interest. Many plants shed their

leaves to reduce water loss during periods of water stress; several herbs have

annual life cycles, growing and flowering in the rainy season; cacti and

bromeliads accumulate water in their tissues and there is a predominance of

shrubs and small trees in the landscape (Leal et al., 2003). The strongly

xerophytic character of the native plants of Caatinga demonstrates, beyond any

doubt, that the semi-aridity of the region does not come from centuries ago,

but probably from millions of years.



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II. LOCALISATION

The Caatinga is the only large natural Brazilian region whose boundaries

are entirely restricted to the national territory, occupying primarily the

Northeast region, with some areas in the state of Minas Gerais. It extends from

2º54' to 17°21' S, comprising an area of approximately 800,000 km2,

representing 70% of the Northeast region and 11% of the Brazilian territory.

The region includes the states of Ceará (CE), Rio Grande do Norte (RN), most

of Paraíba (PB) and Pernambuco (PE), southeast Piauí (PI), the west of

Alagoas (AL) and Sergipe (SE), the north and central region of Bahia (BA)

and a strip extending into Minas Gerais (MG) following the river São

Francisco and a dry valley enclave in the middle region of the Jequitinhonha

(Figure 1). The island of Fernando de Noronha should also be included

(Andrade-Lima, 1981).

Figure 1. Location of Caatinga in Brazil.



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III. GEOLOGY, GEOMORPHOLOGY AND SOILS

In northeastern Brazil most of the caatinga areas are located in depressions

between plateaus (Ab'Sáber, 1974). However, there are some exceptions, such

as the low plateau of Raso da Catarina in Bahia state, the mountain range of

Borborema in Paraíba, or the Apodi Plateau in Rio Grande do Norte (Figure

2), where savanna vegetation is found not only in the depressions, but also in

the highlands (Andrade - Lima, 1981).

Figure 2. Caatinga at the Apodi Plateau (Photo: Coe, 2013).

In general, this province extends over undulating pediplains (Andrade &

Lins, 1964), exposed from Cretaceous or Tertiary sediments covering the basal

Brazilian Precambrian shield. A great process of pediplanation occurred

during the lower Tertiary and Quaternary (Ab'Sáber, 1974) to uncover the

current surfaces of crystalline Precambrian rocks (gneisses, granites and

schists), leaving only isolated remnants of younger surfaces throughout the

Caatinga. These remnants are characterized as inselbergs, such as in Quixadá,

CE (Figure 3), and in Patos, PB, mountains or plateaus, in order of decreasing

erosion.



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Figure 3. Inselberg in Quixadá, CE (Photo: Coe, 2009).

The vegetation varies with topography, with savanna vegetation on top of

the tablelands, such as Chapada do Araripe and coastal tablelands, evergreen

or semi-deciduous rainforests on the tops of the mountains (such as the

marshes of Pernambuco) and dry forests or arboreal caatinga on the slopes and

inselbergs (Prado, 2003). There are some sedimentary areas within the

Caatinga, such as the coastal areas and the Mossoró river basin in Rio Grande

do Norte (Andrade - Lima, 1966) and Raso da Catarina, as well as the regions

under the influence of the São Francisco River in Bahia.

As a result of the origin of the substrate of the Caatinga, soils are stony

and shallow, with the bedrock depths sparsely decomposed and many outcrops

of massive rocks (Tricart, 1961; Ab'Saber, 1974). The geomorphological and

geological origin of the Caatinga has resulted in several complex mosaics of

soils, with varying characteristics even within small distances (Sampaio,

1995). Extensive outcrops of rocks are regionally called "lajedos" that act

ecologically as desert environments where only succulent plants are found

(Figure 4). Pediments covered by more or less continuous layers of stones

(desert pavement) are also common.



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Figure 4. Lajedo of Soledade, RN (Photo: Coe, 2013).

Santos et al. (1992) found a good relationship between vegetation

(physiognomy - flora) and soil types, confirming the observations of Andrade -

Lima (1981) as to the close relationship between vegetation and soil in semi-

arid regions. Rodal (1992) noted that geographical proximity and

geomorphology are important to the understanding of the floristic similarities

of caatinga areas. The author indicated that nearby areas, albeit with different

morphopedologic aspects, showed greater similarity to each other than to other

areas, and that the flora of the areas of the “sertaneja” depression (crystalline)

is distinct from that of the sedimentary plateaus. The west of Pernambuco has

a particular caatinga flora, possibly related to the large patch of red-yellow

latosol which occurs there. Undoubtedly, most of the vegetation of the

Borborema plateau, located in the semi -arid region of Pernambuco, consists

of caatinga of greater height and a sharp floristic richness, which may possibly

be explained by lower temperatures, especially at night (Jacomine et al.,

1973).

Cailleux & Tricart (1959 apud Prado, 2003) postulated that, during the

Quaternary, the Caatinga did not suffere the big climate changes that affected

other areas of Brazil. The only evidence of a Pleistocene fluctuation was

provided by certain localized pebble layers that seem to be products of a more

torrential regime. However, there is evidence indicating that the northeast of



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Brazil had a much drier climate during certain periods of the Quaternary,

giving rise to the fields of paleo-dunes in Xique-Xique, Bahia (Ab'Sáber,

1977; Tricart, 1985; Clapperton, 1993). These wind formations must have

originated when the allochthonous São Francisco River, the only major

perennial river crossing the Caatinga, dried completely at its middle course

and sandy alluvial sediments, previously scattered in the area, were modelled

into dunes, especially by east and southeast winds (Prado, 2003).

IV. CLIMATE

The weather does not always play a significant role in the establishment of

plant formations. However, in the case of the Caatinga, it is clear that the

climate has a major influence. The vegetation of the caatinga always appears

to be associated with high water stress, indicating a complex network of

vegetation types determined by climatic factors (Reis, 1976).

The climate of the Northeastern region, classified as semi-arid tropical, or

as type Bsh, according to the Köppen classification, is characterized by high

temperatures and scarce and irregular rainfall. Reis (1976) describes the

climate in the areas of Caatinga as one of the most extensive areas of semi-

aridity in South America, highlighting some of the most extreme

meteorological values in Brazil: the highest solar radiation, low cloud cover,

the highest average annual temperature, lower rates of relative humidity,

higher evapotranspiration, and, above all, lower irregular rainfall, limited, in

most of the area, to a very short period of the year (2-3 months). These rains,

often of great intensity, lead to floods in reservoirs and water courses, as well

as to high runoff, with little or no infiltration, accentuating and worsening soil

erosion each year. Catastrophic phenomena such as droughts and floods are

very common. However, what most characterizes the region is the complete

absence of rain in some years (Nimer, 1972).

The average absolute maximum temperatures of the region are rarely

above 40°C, and they are restricted to drier areas (Lower São Francisco river

and the Jequitinhonha River Valley in Minas Gerais), while in wetter areas

outside the Caatinga, such as the states of Goiás and Pará, temperatures higher

than 40º or 42º C are much more frequent. Very high average annual

temperatures are another important characteristic of the Caatinga, with values

between 26 and 28º C (Nimer, 1972). However, all the areas above 250 m high

have lower average temperatures (20-22°C).



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This area is characterized by a climatic heterogeneity that makes it the

most complex among the Brazilian regions, deriving primarily from its

geographical position in relation to the various atmospheric circulation

systems and, secondarily, although still of great importance, from the relief

and also latitude and continentality, among other factors. This climatic

heterogeneity can be observed by comparing meteorological data of

precipitation, insolation and evaporation among 34 stations scattered

throughout the area of caatinga (figures 5, 6, 7 and 8).

Figure 5. Map showing the location of the studied weather stations of the caatinga.

Figure 6. Histogram of the total annual rainfall in 34 stations of the caatinga, with

totals ranging from about 500 mm/ year (Cabrobó, PE) to over 1100 mm/ year (Bom

Jesus do Piaui, PI).



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Figure 7. Histogram of the total hours of insolation per year in 34 stations of the

caatinga, with totals ranging from about 1300 h/ year (Itaberaba, BA) to over 3000 h/

year (Apodi, RN).

Figure 8. Histogram of total annual evaporation in 34 stations of the caatinga, with

totals ranging from about 1000 mm/ year (Garanhuns, PE) to over 4000 mm/ year

(Paulistana, PI).

The air masses that act in northeastern Brazil are the Equatorial Atlantic

(Ea), the Equatorial Continental (Ec), the Polar (P), the Tropical Atlantic (Ta)

and Tropical Kalaariana (Tk). Ta has marine properties (warm and wet) and

Tk has desert properties (warm and dry). It is precisely this air of desert origin

that determines the dryness in the Northeast region. Both influence the

formation of the Atlantic Polar Front (APF), when they meet the P, which

originated in the Antarctic periglacial region, as well as the Inter-Tropical

Convergence (ITC), when they meet Ea, formed in the North Atlantic. The



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FPA bifurcates into two paths: the inner continental, which can lead it up to

the equator line, and the maritime or coastal, which reaches the entire eastern

coast of the Northeast, as far as the cape of São Roque, in Rio Grande do

Norte. When it meets Ta, which is warm and rich in moisture, the seafront

cools it, leading to storms along the northeastern coast during autumn and

winter. This effect is accentuated when it introduces itself as a wedge of cold

air beneath the Tk (which acquired some moisture on the way from Africa to

Brazil), refreshing it and causing it to rise, triggering the conditional

instability. This explains the existing wet zone on the eastern coastal strip of

the Northeastern region. However, the FPA loses energy on its journey, not

only from South to North, but also within the region. The Ec originates in the

Amazon region and presents marine features (hot and humid), because it

receives water vapor emanating from the forest. In the summer, it expands and

affects the western flank of the Northeast. The low and irregular rainfall is due

to 2 factors: 1) an area of encounter or ending of 4 atmospheric systems - Ec,

Ta, Ea and Pa. When these air masses reach the region, they have lost much of

their moisture; 2) the presence of the Borborema Plateau, a natural barrier to

the passage of the warm moist air mass coming from the ocean.

The semi-arid nature of this area results principally from the

predominance of stable air masses pushed into the southeast trade winds,

which have their origin in the action of the South Atlantic anticyclone. The

entire eastern coast of Brazil consists of a narrow strip of lowlands behind

which there is a mountain range, known as the “Serra do Mar” (Atlantic

Forest), stretching from the state of Rio Grande do Norte to Rio Grande do

Sul. When the Atlantic-Equatorial air masses, charged with water vapor, are

transported by trade winds against the northeast coast of Brazil, they are

adiabatically moistened and they precipitate annually about 2000 mm of rain.

This is the area of the Atlantic Forest where the Equatorial Atlantic system

loses most of its moisture, while in the areas of rain shadow of mountain

ranges, the Caatingais subject to the effect of stable dry air masses (Andrade &

Lins, 1964). It is only when these dry masses encounter the few elevations

resulting from the pediplanation process that swamps occur, like islands of

humid vegetation within the semi-arid region (Andrade-Lima, 1966; Andrade

& Lins, 1964), because the air mass is moistened and precipitates its remaining

water in these regions. The zone of low pressure known as the Intertropical

Convergence Zone occurs where there is the meeting of the trade winds of

both hemispheres, positioned almost parallel to the equator line, at a latitude of

about 10° N (Prado, 2003). During the summer, this meeting line moves to the

south of the equator, bringing high climatic instability to the northern half of



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the Caatinga from February to April, which is the rainy season in most of

northeastern Brazil. The humid Equatorial continental mass originates along

the Amazon, producing heavy convection rains, and it can reach the west side

of the Caatinga from November to January, particularly when it occurs in

conjunction with the displacement towards the south of the Intertropical

Convergence. Thus, the rainy season follows a sequence from November to

January in the west and southwest, until February or April in the north and

northeast, depending on the penetration of two unstable moist masses coming

from the north and west, as well as their ability to displace the stable dry mass

brought by the trade winds. Catastrophic droughts occur when the humid

masses are unable to reach Caatingas (Andrade & Lins, 1965; Reis, 1976).

In summary, we may say that the dry zone of the Northeast region is a

result of the predominance of stable air brought by the trade winds. This

condition can frequently persist, causing calamitous droughts in the region.

However, the most common situation is that the penetration of the continental

Equatorial mass to the west, combined with the undulations of the Intertropical

Convergence Zone, in the northwest, determine the rainy season in most areas

of the Northeast region, in the sequence summer, summer-autumn.

The generally accepted phytogeographic concept of Caatinga coincides

approximately with the isohyet of 1000 mm (Nimer, 1972; Reis, 1976;

Andrade-Lima, 1981). About 50 % of the area receives less than 750 mm,

while certain regions have less than 500 mm, such as the Raso da Catarina and

a large central area of Pernambuco and Paraiba (Figure 9). However, what is

most important is not the total amount of annual rainfall, but the annual

distribution. Although the Brazilian semi-arid region can be defined by isohyet

800 mm, this value is of little relevance. The complexity of the climatic

characterization of the region is great, being marked by major anticipations or

delays to the rainy season and its concentration in a few years. One major

consequence is the reduced availability of soil water to plants and the fragility

of social and economic systems that depend on these precipitations.

Nevertheless, the delimitation of the Caatinga zone presents an extraordinary

coincidence between the line demarcating the scrublands and the isohyet of

1,000 mm annually. This illustrates a dependency between the Caatinga and

the climatic conditions, especially rainfall (Figure 9).



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Figure 9. Isohyets in Northeast Brazil.



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Rainfall in the region is complex, since its annual totals range from 2,000

mm in coastal areas on the east coast to less than 500 mm in the Raso da

Catarina area, between Bahia and Pernambuco, and Patos Depression in

Paraíba. Overall, the average annual rainfall in the Northeast is less than 1.000

mm, and in Cabaceiras (Paraíba State), the lowest annual rainfall in Brazil,

278 mm/ year, has already been recorded. The northern part of the region

receives between 1,000 and 1,200 mm/ year. Moreover, in the hinterland of

this region, the rainy season is usually only two months a year, and may, in

some years, not even exist, causing the so called “regional droughts”.

Almost the entire area suffers a concentration of 50 to 70% of rainfall in

three consecutive months, characteristic of a very strong seasonal climate.

Across the region the duration of the dry season is very variable, ranging from

two to three months in the humid swamps, six to nine months in most of the

region and up to 10 or 11 months in the Raso da Catarina (Nimer, 1972). In

general, the dry period increases from the periphery to the center of the

hinterland (Nimer, 1972; Nishizawa, 1976). The most important feature of this

climate is the extremely irregular rainfall system from year to year. The

rainfall regime in the semi-arid Northeast can be characterized in non-

anomalous years by two well-defined periods: a rainy summer and a dry

winter, forming a unimodal oscillation; November, December and January

being the wettest months. The driest months are June, July and August. The

rainfall period starts in September, reaches its maximum in December and

ends in May. A curiosity is that, despite it happening during the months of

summer/fall, the rainy season in the Northeast region is named "winter" by the

local people.

V. VEGETATION

The Caatinga has about 5000 species of angiosperms with about 300

endemic species (Giulietti et al., 2002). The dry aspect of vegetation during

most of the year transforms so quickly and dramatically when the rains come

that the landscape changes almost overnight (Figure 10).

The interaction of factors such as soil type, altitude and rainfall index

allows us to recognize different landscape units, forming a vegetation mosaic

so diverse that it makes classification of the Caatinga vegetation difficult

(Figure 11). An analysis of the classifications already proposed for the

Caatinga shows an absence of well-defined characteristics, which results in



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conflicts of opinion among researchers and imprecise delimitation concepts.

Several attempts at classification of this biome have been made. Eiten (1983)

proposes an approach based on the distribution and density of herbaceous,

shrubby and tree species. Other authors have proposed floristic-ecological

classification systems, emphasizing the relationship between the floristic

composition and possible ecological conditioning factors (Luetzelburg, 1922-

23; Andrade-Lima, 1981; Prado, 2003). Velloso et al. (2002), using data of the

biota with the main abiotic factors, proposed the division of the biome into

eight ecoregions.

Figure 10. Aspects of the Caatinga in Açu National Forest (RN): a) in the dry season,

b) in the rainy season (Photos: Sousa, 2013).

In general, the Caatinga is characterized by a type of xeromorphic

vegetation composed of low-growing forests, often with discontinuous canopy,

deciduous foliage in the dry season and trees and shrubs commonly armed

with spines or prickles. The most common plant families are Fabaceae,

Euphorbiaceae, Malvaceae, Asteraceae and Cactaceae, among others

(Figure 12).

The vegetation presents unique strategies to survive in these extreme

weather conditions such as the absence of leaves or their transformation into

spines on Cactaceae ( Figure 12a), microfilia or compound leaves with leaflets

reduced in most Fabaceae (Fig. 12b), Anacardiaceae and Burseraceae.

Some woody species, such as Pseudobambax marginatum (A.St.-Hil.) A.

Robyns (Figure 12c) and Commiphora leptophloeos (Mart.) J.B. Gillett,

among others, present chlorophyllated bast allowing some photosynthetic

activity during the dry season, when the leaves are absent. Succulent species

such as Cactaceae and Bromeliaceae (Figure 12 d) have aquifer parenchyma



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for water supply and some plants have specific organs for storage, like the

swollen trunks of Ceiba glaziovii (Kuntze) K. Schum. and tuberous roots of

Spondias tuberosa Arruda (Figure 12e).

Figure 11. Physiognomies of the Caatinga: a) open shrub caatinga, Lajes, RN; b)

coastal caatinga, Icapuí, CE; c) arboreal caatinga, Martins, RN; d) tall arboreal

caatinga, Portalegre, RN; e) riparian vegetation with predominance of Copernicia

prunifera, Gov. Dix-sept Rosado, RN; f) dense shrub caatinga, Açu, RN (Photos:Coe

& Sousa, 2014).



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Figure 12. Conspicuous plants of the caatinga: a) Cactaceae Pilosocereus gounellei; b)

Fabaceae Anadenanthera colubrina; c) Malvaceae Pseudobombax marginatum; d)

Bromeliaceae Encholirium spectabile; e) Anacardiaceae Spondias tuberosa; f)

Fabaceae Amburana cearensis; g) Capparaceae Cynophalla flexuosa; h)

Chrysobalanaceae Licania rigida.

Trees and shrubs are the predominant forms of life and in most of the

biome the canopy does not exceed 8 meters in height, with the exception of

some species like Amburana cearensis (Allemão) A.C.Sm. (Figure 12f),

Anadenanthera colubrina (Vell.) Brenan, Pseudobombax marginatum (A.St.-

Hil.) A. Robyns and Cordia oncocalyx Allemão, among others. Falling leaves

during the dry season is a common feature among the tree and shrub species,

except for some species such as Ziziphus joazeiro Mart., Spondias sp. and

Cynophalla flexuosa (L.) J. Presl (Figure 12g). Common species along river

banks, such as Licania rigida Benth. (Figure 12h) and Parkinsonia aculeata

L., also maintain their evergreen leaves due to higher water availability during

the year. Still in the arboreal stratum, there are striking succulent species in the

landscape of Caatinga, such as Cactaceae Cereus jamacaru DC., Pilosocereus

gounellei (F.A.C. Weber) Byles & Rowley, Pilosocereus catingicola (Gürke)

Byles & Rowley and Pilosocereus pachycladus F. Ritter.



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The herbaceous stratum is mainly composed of annual plants and it is

absent for about seven months of the year, appearing more frequently in the

rainy season through seed germination in annual species or resprouting from

underground store structures in geophytes. Among the annual species, we

commonly found several species of Fabaceae (genera: Chamaecrista,

Stylosanthes, Zornia and Macroptilium, among others), Malvaceae (genera:

Sida, Waltheria, Herissantia and Pavonia among others), and Poaceae

(genera: Aristida, Eragrostis and Andropogon, among others). Geophyte

species are common among Monocotyledons. Perennial herbaceous species

such as Melocactus spp., Tacinga inamoena (K. Schum.) N.P. Taylor &

Stuppy and Bromeliaceae Encholirium spectabile Mart. ex Schult. & Schult.f.

and Neoglaziovia variegata (Arruda) Mez and Bromelia laciniosa Mart. ex

Schult. & Schult.f., are less common, but nonetheless striking on the

landscape.

CONCLUSION

The Caatinga is proportionally the least studied among Brazilian natural

regions. Historically some myths were created about its biodiversity, such as

the homogeneous environment, having a biota poor in species and endemism

and slightly altered vegetation. These myths are totally unfounded since the

biome has the most diverse of the Brazilian landscapes considering both

geomorphology and the types of vegetation (Queiroz et al., 2006).

Furthermore, much of its surface has been highly modified by human use and

occupation and continues to go through a long process of alteration and

environmental degradation caused by the unsustainable use of natural

resources, which is leading to the rapid loss of unique species, the elimination

of important ecological processes and the formation of large cores of

desertification in various sectors of the region (Leal et al., 2003).

Unlike other semi-arid areas of the world, the Brazilian one is quite

populous, with about 20 million people (about 10 % of Brazil's population), it

being the region with the lowest levels of human development in Brazil.

The Caatinga has been highly modified by man. Garda (1996) indicates

that the soils are suffering an intense process of desertification due to the

replacement of natural vegetation with crops, mainly through slash and burn.

Deforestation and irrigated crops are leading to salinization of the soils, further

increasing the evaporation of water contained in them and accelerating the



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process of desertification. These various effects of anthropogenic activities

include, for example, changes in the behavior of animals due to construction

and maintenance of roads, mortality from trampling, changes in vegetation, the

ease of fire spread, changes in the chemical and physical environment,

expansion of exotic species and changes in human use of land and water

(Trombulak & Frissell, 2000). According to Garda (1996), only the presence

of the adapted vegetation of Caatinga has prevented the transformation of

northeastern Brazil into a vast desert. Despite threats to its integrity, less than

2 % of the Caatinga is defined as fully protected conservation units (Tabarelli

et al., 2000).

Some actions have been taken in an attempt to preserve this unique

ecosystem. Areas of extreme biological interest have been selected through

overlaying information of different groups of organisms (Silva et al., 2004)

and eight natural ecoregions have been proposed for the Caatinga Biome,

combining biotic and abiotic data. Associated with these ecoregions, 57 areas

of high conservation concern were defined for the Caatinga Biome, including

27 of Extreme Biological Importance (Velloso et al., 2002).

Even with these efforts, the biome can be considered one of Brazil's most

endangered, with less than 2% under full protection. Studies on the fauna and

flora of caatinga regions are fundamental. Many areas of Caatinga have not

even been sampled. Complete information on the distribution of the organisms

is essential to efficiently understanding the evolution, ecology and

conservation of the biome (Primack, 1995).

Recently, the Caatinga was recognized as one of 37 major natural regions

of the planet, according to the study coordinated by Conservation International

(Tabarelli & Silva, 2003). Large natural areas are ecosystems that are still

home to at least 70 % of its original vegetation cover, occupy more than

100,000 km2 areas and, thus, are considered strategic in the context of major

global changes (Gil, 2002). More specifically, the conservation of the Caatinga

is important for the maintenance of regional and global climate patterns, the

availability of drinkable water and of arable land and is an important part of

biodiversity. Unfortunately, the Caatinga remains one of the least scientifically

known among South American ecosystems. Moreover, besides the lack of

scientific knowledge there is a small number of conservation units (Tabarelli

& Vincent, 2002) and increasing human pressure (Castelletti et al., 2003). The

result is that several species found in the Caatinga are threatened with global

extinction and a bird species, Cyanopsitta spixii, is officially extinct from

nature.. These indicators reflect unequivocally, the absence of policies aimed

at the conservation of biological diversity of the Caatinga and its other natural



100

resources. Strategies must be developed for more efficient use of altered areas

of the Caatinga for economic purposes, avoiding pressure on even slightly

altered areas.

ACKNOWLEDGMENTS

The authors would like to thank Wesley de Souza Paiva, Francisco

Ernesto de Souza Neto and Catia Pereira dos Santos for help in collecting

samples and Jenifer Garcia Gomes for the preparation of the figures.

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Universitária da UFPE, Recife, p. 777-796.

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Caatinga. TNC-Brasil, Associção Plantas do Nordeste, Recife.




Chapter 4

CHANGES IN THE LABILE AND

RECALCITRANT ORGANIC MATTER

FRACTIONS DUE TO TRANSFORMATION OF

SEMI-DECIDUOUS DRY TROPICAL FOREST

TO PASTURE IN THE WESTERN LLANOS,

VENEZUELA

A. González-Pedraza1* and N. Dezzeo

2

1Universidad Nacional Experimental Sur del Lago “Jesús María Semprum”

(UNESUR), Programa Ingeniería de la Producción Agropecuaria,

Laboratorio de Suelos, Santa Bárbara, Municipio Colón, Estado Zulia,

Venezuela

2Instituto Venezolano de Investigaciones Científicas (IVIC), Centro de

Ecología, Laboratorio de Ecología de Suelos, Altos de Pipe, Estado

Miranda, Venezuela

ABSTRACT

The changes of labile and recalcitrant organic matter fractions due to

transformation of semi-deciduous tropical forest to pasture were

evaluated in an area of tropical dry forest in the western Llanos of

* E-mail: [email protected].


A. González-Pedraza and N. Dezzeo

106

Venezuela. In this area, natural forest was converted to pasture by slash-

and-burn. Estrella grass (Cynodon nlemfuencis L) grows for cattle use.

For determining microbial activity, twelve soil samples were collected at

0-5 and 5-10 cm depth in natural forest and in two pastures of 5 and 18-

year-old (YP and OP, respectively) on three periods along the year: at the

beginning of the rainy season (May), at the end of the rainy season

(November) and during the dry season (March). To determine total soil

organic carbon (SOC) and total extractable carbon (TEC), 12 samples

were additionally collected at each site at 0-5, 5-10, 10-20, 20-30, and 30-

40 cm depth. SOC was determined by Walkley and Black method and

TEC was extracted with alkali solution. Cmic was determined according

to the CHCl3 fumigation-extraction method using K2SO4. The water

soluble carbon (WSC) was obtained by water extraction, and the basal

respiration (C-CO2) was carried out following the colorimetric method of

static incubations. The data sets were subjected to one-way analysis of

variance. Because clay content showed significant differences between

forest and pastures, it was used as a co-variable to adjust the data. Means

were separated with Tukey´s test when statistical differences (P < 0.05)

were observed. SOC increased with the change from forest to pasture. YP

showed the highest SOC content, which was positively correlated with

the clay percentage. TEC was significantly higher in pastures than in

forest. Cmic was higher in OP during March, which can indicate that the

organic matter there was easily decomposed and therefore allowed to

maintain a high microbial population. Cmic decreased in the pasture soils

in May, probably due to a slower response of microbial communities to

sudden changes in soil moisture. The pastures showed higher WSC

contents than the forest, probably due to a less efficient use of the labile

organic matter mineralized during the previous rains. The lowest C-CO2

value was found in YP in November, which can indicate lower efficiency

of microorganisms to decompose the organic matter. OP showed the

highest C-CO2 value, probably due to a higher content of labile organic

matter, evidenced by the higher values of Cmic, WSC and TEC in this

site.

Keywords: Soil organic matter fractions, dry tropical forest, pastures

INTRODUCTION

The variability in the soil organic matter (SOM) in different tropical

forests has been associated with the organic residue amount entering into the

soil and with the rate at which these residues are decomposed (Jaramillo &

Sanford 1995). It is known that the organic matter reserve in the soil has been


Changes in the Labile and Recalcitrant Organic Matter Fractions ...

107

divided into two parts, namely passive or stable and labile or active. Humus is

the most stable SOM fraction. It is composed of humic substances derived of

the decomposition, and it is often complexed with the clay particles

(Christensen 1992, Stevenson 1994, Barrios et al., 1996). The carbon

associated with humic substances is also known as total extractable carbon

(Sánchez et al., 2005). This fraction promotes the formation of stable

aggregates in the soil, improves the soil structure, exerts an important effect on

the chemical and biological soil properties and constitutes the largest reservoir

of C circulating to medium term on a global scale (Oades 1984, Stevenson &

Cole 1999).

The labile organic fraction is composed of fresh plant remains subjected to

rapid decomposition. This fraction is particularly important in nutrient cycling

in soils under forest and pastures (Tisdall & Oades 1982, Stevenson 1994). As

a result of disturbances, it is the first lost fraction (Stevenson 1994, Gregorich

et al., 1996). This labile fraction consists of the microbial biomass and the

water soluble carbon. The microbial biomass represents from 1 to 5% of the

organic carbon content (Powlson et al., 1987, Alef & Nannipieri 1995), and it

is a reservoir of labile nutrients like nitrogen (N) phosphorus (P) and sulfur (S)

(McGill et al., 1981). Moreover, the C water soluble is a good index of the

available soil C and it represents a quickly available energy source for the

microorganisms (Huang and Song 2010).

Similarly, the soil CO2 flux is a good indicator of the carbon distribution

in the subsurface soil and ecosystem productivity and it reflects the biological

activity into the soil (Raich & Nadelhoffer 1989).

The forests conversion to agricultural land and pastures is a topic of

considerable interest, particularly for the scientific community related to

biogeochemical cycles, global climate change and biodiversity (Houghton

1990, Kummer & Turner 1994, Fearnside 2000, Fearnside & Laurance 2004).

Most of the studies on land use change effects in the tropic have been

conducted in rainforest areas (Matson et al., 1987, Montagnini & Buschbacher

1989, Piccolo et al., 1994, Neill et al., 1997a, b), while for the dry forest there

is little information (Brown & Lugo 1990, García-Oliva et al., 1994, Johnson

& Wedin 1997, Ellingson et al., 2000), even when the latter has been

considered one of the most threatened ecosystems on the earth planet (Janzen

1988, Houghton et al., 1991, Murphy & Lugo 1986, Kennard 2002).

In tropical dry forest the marked seasonality of rainfall has a strong

influence in the growth, productivity and organic matter dynamics (Martínez-

Yrizar 1995, Murphy & Lugo 1986, 1995). However by this forest type there

is scarce information about the process of soil matter organic formation and



108

nutrient recycling (Lugo & Murphy 1986). When these forests are cut and

burned to be converted into pasture, much of the organic matter present in

living plants, plant debris and soil, including humus, is oxidized and emitted as

CO2 to the atmosphere (Houghton 1990), resulting in a decrease in the soil

organic C content (Ohta 1990, Luizão et al., 1992, Desjardins et al., 1994,

Veldkam 1994, Cerri et al., 2004).

Tropical dry forest in Venezuela represents the most important life zone in

terms of the land surface, and it includes large areas covered by dense seasonal

dry forests developed on relatively fertile soils. In the last decades these

forests have been subjected to a high pressure of use associated with

population growth and the expansion of the agricultural frontier. After the tree

cutting, one of the main uses has been the establishment of pastures. However,

for this important region of the country there is no detailed information about

the changes occurred in the soil once the forests have been cleared and

converted into pasture, particularly with respect to soil C stocks. This

information is needed to predict the deforestation consequences and to design

effective pasture management. Therefore, the objective of this research was to

evaluate the changes in the labile and recalcitrant organic matter fractions due

to transformation of semi-deciduous dry tropical forest into pasture with

different ages (5 and 18 years old) in the Western Llanos, Venezuela.

MATERIALS AND METHODS

Study Site

The study was carried out in the Western Llanos of Venezuela (Figure 1),

located at approximately 120 m asl. The average annual rainfall in this region

is 1243.7 mm (1998-2008), with a rainy season from April to December and a

dry season from January to March. The average annual temperature is 26.8ºC,

with a maximum of 28.9ºC between March and April and minimum of 25.5ºC

between December and January. The relief is plane with slope between 0 to

2% (Ewel et al., 1976, MARN 2005). According to Holdridge (1957), the area

belongs to tropical dry forest with dominant deciduous vegetation. The soil

parent material is from alluvial origin, consisting of a sandy-clay-loam texture,

with kaolinite as dominant clay mineral (Ewel et al., 1976). In this region,

large areas of natural forest were converted into pasture by slash-and-burn.

Estrella grass (Cynodon nlemfuencis L) grows for cattle use.



109

Figure 1. Study area in the Western Llanos of Venezuela (SIRA-INIA-CENIAP 2010).

Soil Sample Collection

Soils were sampled in natural forest and in two adjacent pastures of 5 and

18-year-old (YP and OP, respectively). At each site, soil samples were

systematically taken from a 600 m2 plot. For determining microbial activity

(microbial carbon, water soluble carbon and soil respiration), twelve soil

samples were collected at 0-5 and 5-10 cm depth with a 5 cm diameter soil

core on three periods along the year: at the beginning of the rainy season

(May), at the end of the rainy season (November) and during the dry season

(March). To determine total soil organic carbon (SOC) and total extractable

carbon (TEC), 12 samples were additionally collected at each site with the soil

core at 0-5, 5-10, 10-20, 20-30, and 30-40 cm depth. These last soil samples

were collected only once on November 2005.

Laboratory Analyses

Total soil organic carbon (SOC) was determined using the Walkley &

Black (1934) wet oxidation method. Total extractable carbon (TEC) was

measured using the methodology proposed by Ciavatta et al., (1990).

Microbial biomass carbon (Cmic) was determined according to the CHCl3

fumigation-extraction method in field-moist samples (Vance et al., 1987).

Study area



110

Cmic was extracted from both fumigated and non-fumigated samples with 0.5

K2SO4. It was calculated by subtracting the extracted C in non-fumigated

samples from that measured in fumigated samples and dividing it by a Kc

value of 0.45. Water soluble carbon (WSC) was determined by McGill et al.,

(1986) method using a 1:2.5 relationship of soil (< 2 mm) and distilled water.

SOC, TEC, Cmic and WSC values were corrected to dry soil and the

results were expressed in C g.m-2

based on the soil bulk density (kg m-3

) and

depth (m). Basal soil respiration (C-CO2) was determined following the

colorimetric method of static incubations of Alef (1995). With this method the

CO2 evolution from soil microbial activity was measured in specified and

controlled laboratory conditions. The calculations were based on the weight of

dry soil and the results were expressed in mg C-CO2 kg-1

24 hr-1

. The

Cmic/SOC ratio, also called soil microbial quotient (qCO2), was calculated by

the following formula: qCO2= Cmic*100/COT.

Statistical Analysis

Statistical analysis of the data was carried out by an analysis of variance

(ANOVA). Because the soil clay content showed significant differences

between forest and pastures, it is was used as a co-variable to adjust the data.

Means were separated with Tukey´s test when statistical differences (P < 0.05)

were observed. When necessary, the data was transformed in order to

homogenize variances, and when that did not meet this assumption (P > 0.05)

according to Levenne´s test, a non-parametric Mann-Whitney test was applied.

To relate variables at sites of interest, a simple linear regression analysis was

used. All statistics were computed using STATISTICA for Windows 6.0

(Statistica 2001).

Results and Discussion

Soil organic Carbon

The soil organic carbon (SOC) was significantly (P < 0.05) higher in the

pastures than in the forest, with the exception of the 0-5 and 30-40 cm soil

depths, where no significant differences (P < 0.05) were detected (Figure 2).

Between 5-10 cm depth, the SOC was 62 and 38% higher in YP and OP,

respectively, than in forest. From 10 cm depth SOC decreased with increasing

soil depth in the three study sites. The most significant differences between the



111

studied sites were observed at 10-20 cm depth, where YP had an increase of

83% and OP of 49% with respect to forest (Figure 2).

Figure 2. Soil organic carbon (SOC) in the forest and in the 5-year-old (YP) and 18-

year-old (OP) pastures. All points are mean values with standard error bars across

forest and pastures. Lower case letters indicate significant differences (P < 0.05)

between land use classes at the same depth. Capital letters indicate significant

differences (P < 0.05) between depths by the same site.

SOC values in this study were relatively higher than those reported by

Fassbender & Bornemisza (1987) for tropical regions. As shown in Figure 2, it

was clear that transformation of semi-deciduous tropical dry forest into pasture

caused an increase in the SOC, which is not consistent with some reported data

in the literature (Detwiler 1986, Detwiler & Hall 1988, Davidson & Akerman

1993, Fujisaka et al., 1998, Tiessen et al., 1998, Powers et al., 2004).

Several factors can influence the soil carbon increases in those pastures

established after cutting and burning of forest, but the most significant are the

change in the mode of carbon assimilation by the vegetation, and the age of

the pastures. When the forest vegetation is replaced by grasses, it is possible to

expect an increase in the isotope 13

C concentration in the soil, due to the fact

that the C4 plants of the pastures contain a δ13

C heavier than the C3 plants of

the forests (Reiners et al., 1994, Johnson & Wedin 1997). On this respect,

0

5

10

15

20

25

30

35

40

45

0 500 1000 1500 2000 2500

Dep

th,

cm

Soil organic carbon (SOC), g C m-2

Forest YP OP

Aa AaAa

BbBbAa

ACcAbBa

CbCaBa

DaDaCa



112

Lopez-Ulloa et al. (2005) found that most of the soil C in pastures

corresponded to a mixture of the original forest vegetation and grasses. They

also observed that in soils pasture the 13

C value increased with pasture age (>

11-year-old), showing a gradual replacement of the carbon in the vegetation

type C3 by the carbon present in C4 vegetation. Jaramillo et al. (2003) also

found that the soil C content was about 20% higher in the pasture than in the

forest. However, some of this carbon was provided by the decomposition of

remain roots of the original forest.

A similar trend was observed by García-Oliva et al. (1994), who found an

increase of 17% in the soil organic matter content in pastures with 3-year-old,

compared with the original forest. This increase was also attributed to the

decomposition of forest tree roots still present in the pasture. They also found

that in 7-year-old pastures, the 13

C value indicated the presence of forest

roots in the pasture, while in 11-year-old pastures the C from forest vegetation

had decreased 71%, thus indicating that the C contribution from C4 plants was

much higher in older pastures. Similarly, Veldkamp (1994) found that the soil

organic C decreased gradually up to 20 years after deforestation and that it was

replaced by the organic carbon produced by the grass.

The adsorption of organic matter to clay minerals is one of the

mechanisms responsible for the soil C stabilization under pastures originally

established in areas that were covered by forest (Lopez-Ulloa et al., 2005). The

soil organic matter may be retained on clay particles surface and, may also be

coated and/or trapped within the interlayer spaces and/or micro aggregates,

allowing it to be protected from degradation by microorganisms (Tisdall &

Oades 1982, Hassink 1994, Matus & Maire 2000). This organic matter in

closer contact with the fine soil fractions corresponds to a longer material in

the soil (Skjemstad et al., 1996).

In this study, the positive correlations between SOC and clay percentage

in the soils of forest (r = 0.39) and of YP (r = 0.69) indicate that clay

percentage is acting in the soil organic matter retention or protection,

especially in YP, where the soil clay content was significantly higher than in

forest and in OP (González-Pedraza & Dezzeo 2011). It is also probably that

some of the C present in the soils of YP could still match the original forest

vegetation. Similar results were reported by Matus & Maire (2000), who found

that over 80% of the SOC was associated with clay and silt fractions. Ochoa et

al. (1996) found also a significant positive correlation between SOC content

and the soil clay percentage.

The SOC accumulation also depends of the nature (quantity and

frequency) of the material incorporated into the soil (Matus & Maire 2000). In



113

that sense, the grass deep roots and their productivity should have a large

effect on soil C inputs after deforestation. For example, Brown and Lugo

(1990) pointed out that pastures are constantly covered by vegetation, which

provides abundant organic matter, particularly from its roots during periods of

increased productivity. In our case, the studied pastures were covered with star

grass (Cynodon nlemfuensis L.), a plant with stoloniferous growth and

abundant roots production that enhances the input of abundant organic

material into the soil profile (Guzmán 1996). According to observations made

during the field sampling, star grass forms a layer on the ground made up by

leaves and remnants stems, which could also contribute to the higher SOC

content in the pastures.

Total Extractable Carbon (TEC)

At 0-5 cm of soil depth, no significant differences in TEC were observed

between the three studied sites. At 5-10 cm, 10-20 cm, 20-30 cm and 30-40 cm

of soil depth TEC values were significantly (P < 0.05) higher in OP than in

YP. However, between YP and forest only differences (P < 0.05) were found

at the 10-20 cm, 20-30 cm and 30-40 cm of soil depth (Figure 3).

Figure 3 also shows an uneven distribution of TEC across the soil profile,

with decreases and increases through the soil profile. However, when the

changes are analyzed site by site along the soil profile, it was observed that the

TEC tend to decrease with depth, except between 10-20 cm, where significant

increases (P < 0.05) were detected in forest and in OP.

The TEC/SOC relationship in the three studied sites and in all considered

soil depths ranged between 9.3 and 58.9% (Table I). Along the soil profile, the

TEC/SOC values were very similar between forest and OP. However, in YP

the values were significantly lower (P < 0.05) than in forest and OP, except at

the soil depth of 0-5 cm, where no differences were observed.

TEC decreases with the soil depth have been explained by the decrease of

soil organic carbon with increasing of depth (Ruiz et al., 2000). The lower

TEC values in YP may be related to the higher clay percentage found in these

soils in comparison with the soils of forest and OP (González-Pedraza &

Dezzeo 2011). It has been found that the clay soil content contributes to the

retention of soil humic carbon by bridge linkages with divalent cations such as

Ca (Oades 1984, Ruiz et al., 2000), and it makes difficult the extraction of the

soil organic carbon (Matus & Maire 2000). The Ca content in the studied soils

was high (González-Pedraza & Dezzeo 2011) and the correlation analysis



114

between TEC and Ca content across the soil profile showed a significant (P <

0.05) and positive relationships in YP and in forest (r = 0.47 and 0.38,

respectively).

Figure 3. Total extractable carbon (g C m-2

) in the forest and in the 5-year-old and 18-

year-old pastures. All points are mean values with standard error bars across forest and

pastures. Lower case letters indicate significant differences (P < 0.05) between land

use classes at the same depth. Capital letters indicate significant differences (P < 0.05)

between depths at the same site. YP: 5-year-old pasture; OP: 18-year-old pasture.

Table I. Total extractable carbon percentage in the soil organic carbon in

the forest and in the 5-year-old and 18-year-old pastures

Depth

(cm)

TEC/SOC (%)

Forest YP OP

0-5 28.5±7.5ABa

26.9±7.9Aa

32.54±4.1Aa

5-10 18.9±3.8Aa

9.3±3.1BCb

19.1±4.2BDa

10-20 55.9±20.0BCa

16.4±3.1Bb

52.3±11.2Ca

20-30 38.5±21.2BCa

13.15±3.2CDb

32.9±13.7Aba

30-40 58.9±41.1Ca

20.9±4.2Db

46.8±18.4Da

TEC/SOC (%): Total extractable carbon percentage in the soil organic carbon. Mean

values ± standard deviation. Lower case letters indicate significant differences (P

< 0.05) between sites at the same depth. Capital letters indicate significant

differences (P < 0.05) between depths at the same site. YP: 5-year-old pasture;

OP: 18-year-old pasture.

0

5

10

15

20

25

30

35

40

45

0 100 200 300 400 500 600 700 800

Dep

th, c

m

Total extractable carbon (TEC), g m-2

Forest YP OP

ABa

Aa

Ba

ABa

Aa

Aa

BCa

Bb

CDb

Db

Aa

BDb

Cc

ABa

Da



115

TEC/SOC ratio represents the SOC proportion that may be involved in

mineralization process (Guggenberger & Zech 1994, Kalbitz et al., 2003). In

our case, the TEC proportion regarding to SOC represented 9 to 27% in YP,

19 to 52% in OP and 18 to 59% in the forest. These values are similar to those

reported by Sanchez et al. (2005) for tropical soils of savanna and gallery

forest, which ranged between 19.98 and 42.88%. Meanwhile, Figuera et al.

(2005) found relationships TEC/SOC slightly higher (53 and 63%) than those

found in this study. In soils of the Central Llanos of Venezuela, Ruiz et al.

(1997a & b) found that the TEC represented approximately 50% of the SOC,

and its distribution was influenced by the clay content and the drainage

conditions of the soils.

Although in this study YP showed the highest SOC content in a great part

of the soil profile, the TEC content and the TEC/SOC relationship were low,

which may indicate that only a small part of the SOC was in an available form

to perform the microbial processes involved in the soil organic matter

mineralization.

Soil Microbial Carbon (Cmic)

Cmic values are presented in the Table II. At the end of the rainy season,

no statistical differences (P > 0.05) were observed between the three studied

sites, both at the 0-5 and 5-10 cm of soil depth. However, during the dry

season the Cmic at the soil depth of 0-5 cm showed a significant increase (P <

0.05) of 78% in OP compared to forest. At the same depth, but at the

beginning of the rainy season, YP presented a significant decrease of the 52%

in relation to forest.

Table II shows also that Cmic in the first 0-5 cm of the forest soil was

significantly higher at the beginning of the rainy season in comparison to the

dry season. At 5-10 cm of soil depth, Cmic in the forest was lower at the

beginning of the rainy season. Cmic in the first 5 cm of YP soil was

significantly lower at the beginning of the rainfall, in relation to the end of the

rainy season. In OP no statistical differences were observed between seasons

and soil depths.

The values of Cmic found in this study are below those reported for other

areas of tropical dry forest (Saynes et al., 2005), but are relatively similar to

the values registered for other soils in different regions of Venezuela (Sánchez

et al., 2005, Ruiz & Paolini 2004, Hernández 1998). According to the results

of Table II, it is evident that the seasonality in the precipitation regime had



116

important effects on the microbial biomass in YP, OP and in the forest. These

results reveal that the microbial populations respond differently to changes in

soil moisture content throughout the year. Often the literature indicates that the

dynamics of soil microbial processes is greatly affected by changes in

moisture content (Sparling et al., 1994, Raich & Tufekcioglu 2000 Jangid et

al., 2008, Maharning et al., 2009).

Table II. Soil microbial carbon (Cmic) in the forest and in the 5-year-old

and 18-year-old pastures

Season Depth (cm) Cmic (g m-2)

Forest YP OP

End of the rainy season 0-5 31.1±10.0ABa(1) 31.8±12.8Aa(1) 35.2±13.2Aa(1)

5-10 24.7±7.8Aa(1) 21.6±16.7Aa(1) 20.4±10.6Aa(2)

Dry season 0-5 20.4±14.0Aa(1) 29.1±15.8ABab (1) 36.1±14.6Ab(1)

5-10 27.1±8.5Aa(1) 25.9±9.7Aa(1) 21.8±10.3Aa(2)

Beginning rainy season 0-5 34.0±15.7Ba(1) 17.7±11.6Bb(1) 31.0±16.2Aab(1)

5-10 15.6±8.3Ba(2) 17.2±11.3Aa(1) 16.3±11.2Aa(2)

Mean values ± standard deviation. Lower case letters indicate significant differences

(P < 0.05) between sites at the same depth. Capital letters indicate significant

differences (P < 0.05) between season at each site and depth. Different numbers

indicate significant differences (P < 0.05) between depth/site/season. YP: 5 year-

old pasture; OP: 18-year-old pasture.

The soil water moisture content in the three studied sites was statistically

lower (P < 0.05) during the dry season than at the beginning and at the end of

the rainy season (González-Pedraza & Dezzeo 2011). The sudden wetting of

the soil at the beginning of the rainy season probably stimulated the soil

organic matter mineralization and microbial activity in the forest soils, which

was evidenced by a higher Cmic content. When the soil is suddenly wet, the

osmotic shock induces the cells breakdown and the intracellular labile

substrate release is rapidly used by the new generations of microorganisms

(Kieft et al., 1987). Also, after the soil wetting, the microorganisms that died

during the dry season releases more C microbial and nutrients for the growth

of plants (Bottner 1985, Lodge et al., 1994, Sanford & Jaramillo 1995).

The low values of Cmic in the soils of YP at the beginning of the rainy

season are comparable to the results reported by García-Oliva et al. (2006)

under similar conditions. It is probably that in YP the microbial communities

were extremely stressed and therefore they took longer time to recover from



117

the sudden change in soil moisture, so they are less efficient in competing with

plants for the nutrients use released at the beginning of the rains. Schimel et al.

(1999) note that it is possible that after a prolonged drought period, the

microbial biomass is less able to respond to soil moisture increase, so that it

does not reach the activity levels obtained during the continuously wet period.

No differences were observed in the Cmic content of OP in the three

evaluated seasons. This suggests that the microorganisms present in this

systems are little sensitive to the changes in soil moisture throughout the year.

It is possible that in this pasture the soil moisture during the dry season and the

availability of labile substrate are enough to achieve their metabolic activities.

The results of this study suggest that seasonal fluctuations in the soils

moisture content exert some influence on the microbial communities of forest

and YP, while in OP this seems to have no effect. Although no specific data

are available, these results seem to indicate physiological differences between

YP, OP and forest microbial communities, such as it was mentioned by

Nüsslein & Tiedje (1999), who suggested that the change of forest to pasture

led to modifications in the soil microbial communities composition.

The higher content of Cmic in OP during the dry season could indicate

that the organic matter in this old pasture is of better quality to maintain a high

and more active microbial population in comparison with that of the forest

soils. According to Potthast et al. (2010), the forest vegetation has higher

values of lignin and higher C:N ratios in comparison with the pasture

vegetation, which resulted in a better microbial activity in pastures soil.

Paterson et al. (2008) suggested that the type and quality of the litter that

enter into the soil produce changes in the activity and composition of

microbial communities, even in areas with similar soils. Although the litter

quality in the forest and pastures was not assessed in this study, it is known

that the organic matter provided by grasses is generally more palatable by soil

microorganisms than that produced by forest vegetation (Sparling et al., 1994,

Maharning et al., 2009).

Microbial Quotient (Cmic/SOC)

Between sites, the Cmic/SOC ratio showed not significant differences

(P > 0.05) in the first 5 cm of the soil during three periods of the year. From 5-

10 cm depth, Cmic/SOC ratio was significantly lower (P < 0.05) in YP at the

end of the rainy season and during dry season. Between seasons, no statistical

differences were observed in the Cmic/SOC ratio. It was also observed that the



118

Cmic/SOC tended to decrease with increasing depth, but these differences

were only significant in the YP and OP soils (Table III).

The microbial quotient represents the C associated with the live organic

matter fraction and provides an idea of the level and quality of the soil

degradation state. This ratio has been proposed as a sensitive indicator of

changes in soil organic matter (Hart et al., 1989), and their decrease would

indicate soil C losses (Anderson & Domsch, 1989b).

According to Alef & Nannipieri (1995), the Cmic represents only 1 to 5%

of the SOC. The results of this study indicate that in relation to SOC, Cmic

comprised 1.1 to 2.5% in forest soils, 0.7 to 2.3% in YP soils and 0.9 to 2.4%

in OP soils. These values were higher than those reported by Saynes et al.

(2005) for dry tropical forest soils in both the rainy and dry season (0.49 and

1.85%, respectively).

The lower values of Cmic/SOC in YP and OP at the 5-10 cm depth (Table

III) seem to indicate SOC losses along the year. During the dry season, the

decrease of Cmic/SOC ratio in forest could be associated with less substrate

utilization efficiency by soil microorganisms in this period.

Table III. Microbial quotient (Cmic/SOC) in soil forest and in 5-year-old


Season Depth (cm) Cmic/SOC (%)

Forest YP OP

End of the

rainy

season

0-5 2.4±1.1Aa(1)

2.3±1.1Aa(1)

2.4±1.0Aa(1)

5-10 1.9±0.5Aa(1)

1.0±0.6Ab(2)

1.2±0.7Aab(2)

Dry

season

0-5 1.5±1.1Aa(1)

1.9±0.8Aa(1)

2.4±1.0Aa(1)

5-10 2.0±0.6Aa(1)

1.2±0.5Ab(2)

1.2±0.5Ab(2)

Beginning

rainy

season

0-5 2.5±1.1Aa(1)

1.4±1.4Aa(1)

2.2±1.4Aa(1)

5-10 1.1±0.8Ba(2)

0.7±0.5Aa(1)

0.9±0.7Aa(2)




indicate significant differences (P < 0.05) between depth/site/season. YP: 5-year-




119

Soil Carbon Water Soluble (SCW)

With few exceptions, no statistical differences (P > 0.05) in SCW were

observed at the 0-5 cm depth between the three studied sites, both at the

beginning and at end of the rainy season. During the dry season, the value of

SCW at 0-5 cm depth was statistically higher (P < 0.05) in YP than in forest.

At 5-10 cm depth, the values of SCW were significantly lower (P < 0.05) in

YP than in OP and in forest during the dry season and at the end of the rainy

season, while at the rainfall beginning these values in YP were higher.

Between seasons, the SCW content was higher in all studied sites during the

dry season at 0-5 cm depth, and decreased at the rainfall beginning. Between

depths, the SCW content tend to decrease with increasing soil depth (Table

IV).

Table IV. Soil carbon water soluble in the soil Forest and in 5-year-old


Season Depth

(cm)

Soil carbon water soluble (SCW), g m-2

Forest YP OP

End of the rainy season 0-5 8.6±1.1

Aa(1) 7.6±1.1

Aa(1) 9.0±1.3

Aa(1)

5-10 7.5±0.8Aa(1)

4.4±0.8Ab(2)

8.0±0.8Aa(1)

Dry season 0-5 11.5±0.9

Aa(1) 17.6±1.5

Bb(1) 14.1±0.9

Bab(1)

5-10 8.3±1.0Aa(2)

1.6±0.6Bb(2)

5.6±0.6ABc(2)

Beginning rainy season 0-5 5.1±0.4

Ba(1) 6.3±0.5

Aa(1) 5.8±0.6

Ca(1)

5-10 4.4±0.7Ba(1)

8.4±0.6Cb(2)

5.1±0.9Ba(1)






Similar results were found by Gomez et al. (2008) for tropical soil forests

of low fertility, especially during the dry season and in the first five soil

centimeters. The SCW content increase during the dry season has been

associated with lower efficiency used by plants and soil microorganisms of the

labile organic matter mineralized during the previous rains. Therefore, the C

labile can be accumulated in the soil during the dry period (Jiang et al., 2006).

The SCW is one of the largest and most accessible C sources for the soil

microbial activity (García-Oliva et al., 2006 Jiang et al., 2006, Gómez et al.,



120

2008). The significant decrease of this labile fraction at the beginning of the

rainy season can be probably associated with a strong microbial activity that

consumes a large amount of SCW from the mineralization of the many

microorganisms that usually die during the dry period, and which in turn serve

as a substrate for microbial populations developed with the rains onset

(García-Oliva et al., 2006, Jiang et al., 2006, Gómez et al., 2008). In addition,

with the precipitation onset can occur that some C labile will be leaching on

the ground, as noted by Jiang et al. (2006).

Soil Basal Respiration (C-CO2)

Seasonal changes in C-CO2 in the forest and pastures are presented in

Table V. At the end of the rainy season, the basal respiration was significantly

lower in YP and significantly higher in OP (P < 0.05) than that of the forest,

both at 0-5 and 5-10 cm depth. At the beginning of the rainfall no statistical

difference (P > 0.05) were observed between sites, while in the dry period the

value of C-CO2 in YP was significantly higher than those of the forest and OP

at the 5-10 cm soil depth.

Between depths, the C-CO2 increased significantly (P < 0.05) with

increasing soil depth at the beginning of the rainfall in all studied sites. A

similar increase was detected in YP during the dry period, while in OP the C-

CO2 decreased significantly at the end of the rainy season. Between seasons,

soil basal respiration decreased significantly (P < 0.05) in forest, YP and OP

during the dry period and increased again at the beginning of the rainfall

(Table V).

The land use change of forest to pasture significantly affected the

microbial activity at the end of the rainy season. With respect to the forest, the

soil basal respiration in YP decreased 40%. This can be associated with a

lower efficiency in the soil microorganism activity to decompose the organic

matter remnant from the original forest, and that from secondary woody

vegetation in regrowth and from the grasses. When the forest is cut and burnt

to establish pasture, changes related with humidity conditions, temperature and

organic matter inputs occur in the soil (Fearnside & Barbosa 1998), affecting

the biological activity and respiration rate.



121

Table V. Soil basal respiration (C-CO2) in the forest and in 5-year-old and

18-year-old pastures

Season Depth (cm)

Soil basal respiration (C-CO2)

(mg C-CO2/100 g soil/day)

Forest YP OP


Aa(1) 0.6±0.2

Ab(1) 1.9±0.2

Ac(1)

5-10 0.7±0.1Aa(1)

0.5±0.2Ab(1)

1.7±0.1Ac(2)

Dry season 0-5 0.3±0.1

Ba(1) 0.2±0.1

Ba(1) 0.3±0.2

Ba(1)

5-10 0.3±0.1Ba(1)

0.7±0.4Ab(2)

0.2±0.1Ba(1)


Aa(1) 1.0±0.3

Ca(1) 1.0±0.4

Ca(1)

5-10 1.2±0.5Ca(2)

1.4±0.1Ba(2)

1.5±0.1Ca(2)





old-pasture; OP: 18-year-old-pasture.

In a global analysis, Raich & Tufekcioglu (2000) found that the rate of

soil respiration under pasture was 20% higher than under forest, and suggested

that the conversion of forest into pasture can stimulate CO2 emissions to the

atmosphere, because the grasses may have more photo assimilates available in

belowground biomass than the forest trees, just as a mechanism of adaptation

to constant defoliation during grazing or burning. These authors concluded

that the soil respiration rate is mainly controlled by climatic factors,

particularly the interaction between the moisture availability and soil

temperature, and they also suggested that the interaction between climatic

conditions and availability substrate generate fundamental limitations on the

potential rate of soil respiration.

Sparling et al. (1994) found that pastures with a high proportion of

microbial carbon showed higher soil respiration than the native forest. This

was attributed to the huge differences between organic matter types in both

ecosystems. The organic matter of the pastures provides a substrate more

appropriate to maintain a persistent and active microbial population, because it

normally has high cellulose content and low C/N.

Our results showed also that soil respiration varied with the season of the

year. Decreases in the soil respiration rate from the dry to the wet period have

been reported for forests and pastures (Davidson et al., 2000). According to

these authors, soil respiration in the dry season was higher in the forest than in



122

the pasture, probably because in this period the grasses entered in a stage of

senescence and inactivity resulting in a soil respiration lower rate. Meanwhile,

Schimel et al. (1999) support the idea that highly active microbial

communities are not able to survive long periods of drought.

The soil moisture conditions affected the microbial activity, independently

of the vegetation type. According to Cook & Orchard (2008), there is a linear

correlation between the respiration of the microorganisms and the soil water

content. In this study, the correlation analysis between the C-CO2 and moisture

percentage was positive in all sites, seasons and depths (r = 0.60 to 0.88),

reflecting a positive and direct relationship between moisture content and soil

microbial activity. The high microbial activity and soil basal respiration at the

beginning of rainfall can be associated with the fact that at this period

microorganism are consuming and metabolizing the substrate that is released

from the cells rupture by osmotic shock (Kieft et at. 1987, Schimel et al.,

1999).

Metabolic Quotient (qCO2)

At 0-5 cm soil depth, the qCO2 at the end of the rainy season was

significantly lower in YP and higher in OP (P < 0.05) than that of the forest

(Table VI). With few exceptions, during the dry season and at the beginning of

rainfall no differences (P > 0.05) between sites were found. When comparing

the qCO2 between seasons at each site, it was observed that qCO2 increased

significantly (P < 0.05) in YP at the beginning of rainfall. In OP at 5-10 cm

soil depth the qCO2 increased significantly (P < 0.05) at the end of the rainy

season. Other increases were also observed in YP during the dry period and in

all studied sites at the beginning of the rainy season (Table VI).

The lowest qCO2 value found in YP at the end of the rainy season not

necessarily might be indicating greater microbial efficiency in the C labile use.

Although this pasture had the highest SOC content, it may be that the soil

organic matter is of lower quality, less labile and therefore less available to

soil microorganisms. In addition, such low value may also be associated with a

reduced activity of microorganisms due to a substrate deficiency (Anderson

1982). This aspect, coupled with the possible protection of organic matter by

soil clay in YP, could be influencing the low qCO2 found at the end of the

rainy season.



123

Table VI. Metabolic quotient (qCO2) in the soil Forest and in 5-year-old


Season Depth

(cm)

Metabolic quotient

qCO2 (mgC-CO2)/(mg Cmic/day)

Forest YP OP


Aab(1)

1.2±0.9Aa(1)

3.1±1.5ABb(1)

5-10 2.0±0.6Aa(1)

3.4±3.7Aab(1)

7.5±6.8Ab(1)

Dry season 0-5 1.6±2.0

Aa(1)

0.5±0.5Aa(1)

0.6±0.5Aa(1)

5-10 0.8±0.4Aa(1)

1.8±1.1Ab(2)

0.9±0.4Ba(1)


Aa(1)

3.9±2.2Ba(1)

2.3±2.7Ba(1)

5-10 7.0±7.9Ba(2)

10.2±12.4Ba(1)

8.7±6.9Aa(2)






The highest qCO2 in OP might indicate the presence of more labile and

readily available substrate for microbial activity. This was evidenced in the

slightly higher Cmic and SCW values found in OP. This could be indicating

that OP is reaching a steady state associated to the old age of this pasture. The

qCO2 decrease during the dry season is more related to low specific activity by

soil microorganisms because they enter an idle state and even many die due to

low moisture availability and shortage of substrate. With the rainfall beginning

the available C forms increased in the soil, affecting the microorganism

specific activity and increasing the microbial populations that will use these

substrate sources.

CONCLUSION

The land use change from forest to pasture resulted in increases in soil

SOC content. The SOC increase in the 5-year-old pasture is attributed to the

additional C inputs from the original forest vegetation, secondary forest

vegetation that continued regrowth, aerial and underground input from leaves

and roots of the pastures and by soil organic matter retention due to higher



124

clay content. The SOC increase in OP was related to the pasture age, which

allowed it to reach a more stable state in the biomass production.

The labile soil organic matter fraction and the soil basal respiration were

affected by vegetation type, seasonality of rainfall and pasture age. Cmic and

SCW behavior indicates physiological differences between microbial

communities in the three study sites, which can be associated with the fact that

each site responded differently to the changes in soil moisture content. During

the dry season the soil microorganisms present in the pastures are less efficient

in using labile organic matter provided by the grass. The SCW decreased in

the three sites at the beginning of the rainy season, is indicating that this

fraction is the main substrate used by microbial populations developed during

this season. YP soil microorganisms were apparently less efficient to

decompose the organic matter, while in OP the best quality of the substrate

stimulated the microbial activity. Also, the old age of this pasture allowed

greater stability of soil microbial activity.

ACKNOWLEDGEMENTS

We thank Alma Mater Program of the Planning Office Sector University

(OPSU) of Venezuela for the partial financing awarded to the Soil Laboratory

of the Venezuelan Institute for Scientific Research (IVIC) for the development

of this research.

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Chapter 5

ECOLOGY AND MANAGEMENT OF THE DRY

FORESTS AND SAVANNAS OF THE WESTERN

CHACO REGION, ARGENTINA

Carlos Kunst1, Sandra Bravo

2, Roxana Ledesma

1,

Marcelo Navall1, Analía Anríquez

3, Darío Coria

1,

Juan Silberman3, Adriana Gómez

1 and Ada Albanesi

3

1Instituto Nacional de Tecnología Agropecuaria (INTA),

Santiago del Estero Experimental Station, Santiago del Estero, Argentina. 2Universidad Nacional de Santiago del Estero (UNSE), Botany Chair,

Santiago del Estero, Argentina 3Universidad Nacional de Santiago del Estero (UNSE),

Ecology and Soil Microbiology Chairs,

Santiago del Estero, Argentina

INTRODUCTION

The Chaco region is a vast plain that extends into northwestern Argentina

and surrounding countries (Figure 1). Chaco is a quichua word meaning „a

place for hunting‟ or „a place where I am self-sufficient‟ (Metraux 1946,

Berton 2014, personal communication). Its northern limit is the Amazon. At

the southeast, it limits with the Pampas, and to the southwest with the Monte,

other key natural regions of Argentina. At the west, the Chaco borders the


Carlos Kunst, Sandra Bravo, Roxana Ledesma et al.

134

tropical jungles. Boundaries among those regions are gradual, and there are

many shared plant and wildlife species.

In this chapter, we will give an overview of the ecological features,

research concepts and field methods applied, and research results aimed to a

sustainable management of the forests, grassland and savannas of semiarid and

arid Chaco subregions of Argentina (Figure 1), based in findings and

publications from INTA, UNSE as well as other institutions.

Figure 1. The Chaco region in Argentina (Source: Morello, 1968).

ECOSYSTEM FEATURES

The Chaco climate is defined as „monzonic‟ because summers are hot and

wet, while winters are dry and cold (Boletta 1988, Figure 2). Freezing

temperatures as low as -10°/-15°C are common during winter, while they can

go up to 38-40°C in a spring-summer afternoon. Rain is quite variable within


Ecology and Management of the Dry Forests and Savannas …

135

and between seasons and tends to decrease from 700-800 mm in the east and

west to 200-300 mm toward the south (Boletta 1988). Average air

temperatures follows the same pattern, balancing in some way the diminishing

rainfall.

Figure 2. Climodiagram of Santiago del Estero.

The western Chaco is a vast plain, with a slight slope toward the southeast

and crossed by several rivers, such as the Salado and Dulce. Toward the south,

as rainfall decreases, rivers become semipermanent streams. Sediments

brought by rivers and streams from the mountains and sierras located in the

western side are the original material of soils. In the semiarid part soils belong

to the order Mollisol, and in the arid sector Aridisols and Entisols. Although

some are undeveloped (A – A/C horizons) they have usually no severe

limitations for root growth such as caliche layers. Toward the south, there are

areas with severe salt accumulations and problems with clay texture

(„barreales‟), that seriously restrict plant growth in the lowland sites.

The vegetation of the Chaco region is a mosaic of hardwood forests,

savannas and grasslands (Bucher, 1982; Morello and Adámoli, 1974, Bordón

1983). These vegetation types correspond to different soil and drainage

features related to the geomorphological processes associated with water

runoff (e. g. levees and flats, Bucher 1982). At a scale ~ 1:20,000, soil and

vegetation types of Chaco are located along a catena from the „upland‟ to the

„lowland‟.


Figure 3. Ecological sites, associated vegetation types and species in the Chaco region, at scale= 1:20,000 (modified from Kunst et al.

2006).

1

Range Sites

Good condition Poor condition

Features Upland Midland Lowland Upland Midland Lowland

Physiognomy Tall hardwood forest Woodland Savanna Low-Forest - Shrubland Shrubland Shrub-thicket

Tree species Schinopsis lorentzii

Aspidosperma

quebracho blanco

Prosopis nigra

Aspidosperma quebracho

blanco

Aspidosperma quebrachoblanco Prosopi snigra


blanco

Prosopisnigra


blanco

Aspidosperma quebrachoblanco

Shrub species Acacia furcaptispina Acacia aroma Acacia furcaptspina

Celtis spp

Larrea divaricata

Celtiss pp Acacia aroma

Aloyssia spp

Schinus spp

Aloyssia spp

Grass and forb

species

Trichloris pluriflora

T. crinita

Setaria leiantha

Digitaria californica

Pappophorum pappipherum


Paspalum spp

Elionorusmuticus

Heteropogon contortus

Paspalum spp

Schizachirium tenerum

Setaria leiantha

Setaria spp

Neoboutelua lophostachya

Forbs

Setaria leiantha

Setaria spp

Neoboutelua lophostachya


Digitaria insularis

Standing forage

(kg MS*ha-1)

600-1300 2000-3000 2000-5000 < 500 300 300-1000

Stocking rate

(ha*UG-1)

12-5 4-3 4-2 12 25 6

2



137

A vegetation model, using the ecological site concept, was provided by

Kunst et al., (2006b, Figure 3): hardwood forests occupy the upland sites,

while the woodlands and savannas are located on the intermediate and lowland

sites, respectively. The tree species Schinopsis lorentzii (quebracho colorado

santiagueño) and Aspidosperma quebracho-blanco (quebracho blanco)

dominate in upper layers of the forests (c. 15 m tall). Prosopis nigra

(algarrobo negro), Ziziphus mistol Griseb. (mistol), Cercidium praecox (brea),

Geoffroea decorticans (chañar) and Jodina rhombifolia(sombra de toro) are

common species in the mediumstrata. Acacia aroma, Acacia furcatispina,

Capparis atamisquea, Condalia microphylla (piquillín), and Porlieria

microphylla (cucharero) characterize the shrub strata (López de Casenave et

al., 1995). Natural grasslands occupying interfluvial homogeneous soils and

savannas are dominated by Elionurus muticus Spreng. (“aibe”, “espartillo”,

“paja amarga”), Heteropogon contortus, Schyzachirium spp., Trichloris

crinita, Trichloris pluriflora, Gouinia paraguariensis, Gouinia latifolia,

Setaria argentina, Setaria gracilis, Digitaria sanguinalis, Pappophorum

pappiferum, Papophorum mucronulatum (Herrera et al., 2003). Trees such as

A. quebracho-blanco, P. nigra, and shrub species such as A. aroma, Schinus

sp., Celtis sp. are scattered across the savannas in small patches or isolated

trees (Kunst et al., 2003). Currently dense shrub thickets and degraded

secondary forests are widespread in the region, caused by livestock

overgrazing, indiscriminate logging, changes in the fire regime, and fencing.

CHACO VEGETATION: THEN AND NOW

Descriptions of the original vegetation types of the Chaco are scarce. The

chronicles of European conquerors and scientists traveling along vast

territories of Chaco region described great grassland areas and dense forests

where indigenous people carried out their subsistence activities such as

hunting, raising animals, harvesting of fruits, among others. Comments as the

following have been provided by these old chronicles:

„There are large grasses and very good settlements for raising cattle

in big numbers such as those of Spain and to made windmills and other

homesteads which can make them prosperous..'1

Anonymous Relation, 1572, cited by Montes (2008).

1Free translation.



138

„…they are covered by extensive and thick forests, some with high

trees, some quite open in beautiful green meadows and fields‟2

Caamaño (1778)

„…In all this land and plains there is a large number of ostridges,

they are brown and big…they run very fast‟2

Lizarraga (circa 1600)

„Burning grasslands or the bush is a common hunting method

throughout the Chaco…The charred carcasses of animals overtaken by

the fire are gathered up and eaten on the spot. Later the Indians return to

the fired area to stalk the countless deer lured by the salty ashes or the

thick and tender new grass‟

Métraux (1946)

Old maps as well as the names of several places suggest that until the mid

XX century, grasslands and forests shared the Chaco landscape in an even

proportion (Figure 4). Fire was probably responsible of that fact, since it was

extensively used by the native for hunting and war (Bravo et al. 2001).

The part of the Chaco region located to the south of the Salado River was

settled by the Europeans since the Spanish conquest since ~ year 1500 AD.

Livestock breeding (cattle, mules, goats and horses) was the most important

productive activity. The area located to the north of this river was mostly

unexplored until to the late XIX Century. Intensive settlement of the Chaco

began in the earlier XX Century: timber operations based on native forests

became the most important trade, providing fence posts, firewood, charcoal

and railway ties. Early agricultural farms were developed in the east and west.

Timber operations declined around 1960, and in the next decade extensive

areas of land were cleared for agriculture, mostly sorghum and soybean

occupying the areas with the best edaphic and climate conditions (Grau et al.

2005). Today, cattle ranches alternate with large agricultural farms and areas

with small landowners.

DISTURBANCES AND PLANT ADAPTATIONS IN THE CHACO

Together with floods and droughts, fire was, and still is a common event

in the Chaco. It was used by the natives for hunting and war in pre-Columbian

times (Metraux 1946, Tortorelli 1947, Morello and Saravia Toledo 1959).

Today is mainly used as a tool for rangeland management and vegetation

clearing (Kunst et al. 2012).



139

Figura 4. Vegetation types of the Chaco in the late 1930‟s. (Frenguelli 1940).

Although fire is qualified as a „common event‟ in the Chaco, there are few

studies that address the fire regime of the Chaco ecosystems. There is evidence



140

that the savannas are a fire-prone community: E. muticus, the dominant grass,

contains citral terpenes in its foliage, making the species very flammable

(Burkart 1969).

Fire usually starts in the savannas as high intensity headfires, but they

often show low severity on soils because its fast speed (Kunst et al., 2000).

The fire regime of ecotones between an E. muticus savannas and forests has

been studied by dendrochonological techniques on native woody species,

estimating a mean fire free interval 3-5 years during the last century (Bravo et

al., 2001b). There is no information about the fire regime of the forests,

although there are empiric evidences as oral communication from rural

inhabitants and studies about fire resistance in tree species of the genus

Prosopis, mentioning fire scars in branches until 7 m height, suggesting that

crown fires can occur under extreme climatic conditions (Bravo et al., 2001a;

Bravo et al., 2008). Grass species of the forests recover quickly after fires and

in the savannas environments fire is associated to an increase in herbaceous

diversity during 3- 6 years after fire event (Kunst et al., 2003). The unusual

intense fires that occurred in the Chaco forests probably originated the „fire

grasslands‟ (`quemados‟) due to all aboveground structure of the native

vegetation was eliminated and replaced immediately by an homogeneous

herbaceous stratum. These “fire grassland” were maintained by recurrent fires

performed by the aborigines (Morello y Saravia Toledo 1959).

Studies about fire tolerance of the native hardwood tree and shrub species

composing the medium and high strata of the forests and savannas suggest

both high fire resistance and fire tolerance, as related to traits such as barks

thickness, bud features, resprouting pattern and phenology among others

(Bravo et al. 2001b; 2006; 2008, 2001a).

The dominant species of the upper stratum of Chaco forests; A.

quebracho-blanco and S. lorentzii are remarkably resistant to fire at the mature

state and reestablish damaged aerial structures by profuse resprouting (basal

and epicormic Figure 5). Both species have thick bark, a trait allowing them to

effectively protect the cambium tissue of the bole, branches and buds.

Therefore, this great ability to resprout after fires produces some arquithectural

changes such as an increase of plant cover and multi-stemmed forms

principally on sapling and pole-sized trees (Bravo et al., 2011, 2012, Figure 5).

Secondary tree and shrub species of the medium and lower strata of the

forests and savannas have a differential fire resistance according to bark

thickness, plant height and foliage features.



141

Figure 5. Response to fire in native woody species of Argentine Chaco region. A- Fire

scars in S. lorentzii, B. Basal resprouts in A. quebracho-blanco, C. Basal resprouts in

C. atamisquea, D. Bark exfoliation in G. decorticans.

Fire usually eliminates aerial structures of shrub species such as Acacia

aroma, A. furcatispina, Capparis atamisquea, Celtis sp. and Schinus sp.,

because of their lower plant height and thin bark thickness than the tree



142

species. These species recover mainly by basal resprouts, and the initial plant

cover could even increase after a fire depending of fire severity, their aerial

bud bank and reserve levels (Kunst et al. 2000, 2009). Secondary tree species

of Chaco forests such as Prosopis nigra, P. alba, Ziziphus mistol, Geoffroea

decorticans, and Cercidium praecox have different fire resistance according to

different combination of thickness and density of their barks, which allow

them keeping alive the main bole and buds. The main bark feature related to

fire resistance is thickness but a higher bark density may contribute to delay

the time to reach ignition (Bravo et al., in press). Thick bark species as A.

quebracho-blanco and P. alba resist to high severity fires due to the greater

isolation of cambial tissues and buds. Other species, with lower bark thickness

can resist to medium and low severity due to greater bark density, a fact that

delays the time to reach ignition. Bark protection, however, could be

insufficient in high severity fires. This has been observed in P. nigra and Z.

mistol. Other thin bark species, like G. decorticans and C. praecox

continuously exfoliate the bark tissues becoming very susceptible yet in low

intensity fires (Figure 5). High severity fires, or a high fire frequency could

overwhelm the bark protection, and to produce the loss of epicormic buds of

stem and branches. Even in these cases, the species showed a high ability to

differentiate adventitious buds from collar zone producing vigorous basal

resprouts (Kunst et al., 2000; 2012).

The stress caused by fire usually adds to the dryness and cold typical of

autumn and winter in Chaco region and this synergism influences also the fire

tolerance of native vegetation. The mortality after medium to high intensity

prescribed fires reached until 10 % of individuals (Bravo et al., 2014, in press)

and these values could diminish if fire occur at late fire season (late spring and

early summer) when better environmental conditions promote fast recovery of

vegetation.

The effect of fires on the sexual propagation and dispersion of native

woody species is an interesting future research line because will allow to

comprise its relationship with forest dynamic in spatial and temporal scale.

VEGETATION MANAGEMENT: FOREST AND SAVANNAS

During the European conquest, cattle and goat breeding was the main

productive activity in the Chaco. The native vegetation was used as the main

source of forage. From the late XIX until the middle XX century, colonizers



143

produced the greatest change in the native vegetation through intensive

deforestation to provide railway sleepers, the exploitation of the “quebracho”

for the tannic acid industry, and the use of fire for clearing the land for

agriculture and grazing (Soares 1990).

In the late 1940‟s, livestock activities were remarkably reduced by

overgrazing of grasslands and savannas (Adámoli et al., 1990). The decrease

in fine fuel load in open areas reduced the fire frequency and facilitated the

invasion of Acacia, Prosopis, Mimosa and Mimoziganthus shrub species

(Morello y Adámoli, 1973). Currently, savannas and grasslands of Chaco are

maintained by recurrent fires performed by cattle ranchers. The implantation

of tropical grass species belonging to the genus Panicum, such as P. maximum

cv Gatton is the most common strategy to increase to livestock production in

Chaco (Kunst et al., 2014). Since these exotic species have a greater biomass

production potential than native pastures therefore, changes in the fire regime

should be expected.

Historically, due to climatic, soil and technological restrictions,

agriculture was viable as an economic alternative in Argentina in the central

and southern subregions of the Chaco (Figure 1). From 1975 on,

approximately, it occurred an intensive deforestation in Chaco region

increasing the agricultural areas at the expense of native forest (Grau et al.,

2005; Boletta et al., 2006). The traditional crops as cotton; bean and chikpea

were replaced by sorghum and soybean (Morello et al. 2004). Within the

native forests the fire is used as tool for land clearing and elimination of

residues of forest operations (Boletta et al., 2006). The silvopastoral systems

can also use fire as a tool management of the shrub strata and some recent

studies give information about resistance of native woody species to

prescribed fires (Kunst et al., 2012; Bravo et al., 2014).

Silviculture in the Chaco

One of the main productive uses of Chaco forests is logging. Native

hardwood species are highly valued in the whole country as fuel (charcoal or

firewood), for building livestock management facilities (fences) or as railway

sleepers. The dominant species A. quebracho-blanco and S. lorentzii are

locally named “quebracho”, from “quiebra hacha” (axe breaker), which tells

about their wood hardness (density 0,8 and 1,2 kg.dm3-1, respectively) (Kryn

1954). S. lorentzzi wood yield up to 24% on tannin extraction (Luna 2012),

which gives a great suitability to use it outdoors, in direct contact with soil and



144

water, standing for decades without any preservation treatment. Railway

sleepers have been reported to be as sound as when installed, after more than

40 years in service (Kryn 1954). Charcoal of A. quebracho-blanco is valuated

as the best, both at home and in foreign countries where is exported.

Considering the whole country, these products have a great participation in the

productivity of the Chaco native forests, Almost 80% of national production of

the native forests (4 million Mg.year-1

) comes from Chaco region, and 80% of

it is firewood (for charcoal and other uses).

The structure of western Chaco forests is uneven-aged, which high

densities in smaller size classes, and a decreasing density in higher ones. A

well conserved forest usually presents more than 7 m2.ha-1

of basal area of

“quebrachos” (Brassiolo, 2005), and present near 170 trees.ha-1

with DBH >

10cm, and less than 7 trees.ha-1

with DBH > 45 cm. In the size range from

saplings to DBH = 10cm, Gómez and Navall (2008) found more than 2000

individuals.ha-1

. In the Chaco forests the size classes and species are

completely mixed, and no groups can be clearly identified, except in the lower

size classes of Schinopsis lorentzii (DBH < 10cm).

The diameter growth for both dominant species in the western Chaco

forests is highly variable. In selected individuals, growth rates around 0.3 – 0.4

cm.year-1

have been reported (Gimenez and Ríos, 1999). However, when

considering the whole plot and all DBH classes, other researchers reported

smaller values (0,1 to 0,3 cm.year-1

) (Araujo 2003, Cid Londínez et al., 2013).

Volumetric growth is estimated around 1 to 1,5 m3.ha

-1.yr

-1 (Unique 2007).

The traditional harvesting approach of hardwood forests in the western

Chaco has been the harvest of the best individuals of selected species, without

considerations on forest sustainability, remaining structure or cover (Morello

et al., 2005; Unique, 2007). Additionally, uncontrolled grazing and burning

caused that currently, a high proportion of the western Chaco forests are in a

“regeneration” state (Brassiolo, 2005). This state is characterized by a lower

proportion of commercial species, and a higher proportion of small diameter

trees and shrubs than those observed in well conserved forests.

It has been recommended that the sustainable management of western

Chaco forests could be performed by selective cutting, combined with the

management of remaining trees selected by applying the “future-tree” concept

(Brassiolo et al., 2007). In this approach, mature individuals are harvested, and

thinning is applied on the remaining individuals in the same operation.

Preferred individuals are selected as “future trees”, and some of their

competitors are removed by thinning. To be sustainable, the overall cutting

should be less or equal than the product of cutting rate and annual growth of



145

the stand. The return interval recommended for western Chaco forests is

usually 20 yr. Additionally, conditions to favor natural regeneration are

needed. It has been recommended to apply regeneration protection intervals of

5 yr after forest harvesting. At least, 100 trees.ha-1 should reach a “safe

height” (>2m to avoid grazing damage) 5 years after each cutting event

(Brassiolo, 1997; Brassiolo and Pokorny, 2000).

Range and Grassland Management in the Chaco

Standing forage in the upland site in good condition is estimated around

700 -1000 kg*ha-1

, while in the lowland site is 5000-6000 kg*ha-1

(Kunst et

al., 2006). Grass species belonging to the genera Trichloris, Setaria and

Digitaria dominate in the upland site, while Elionorus, Botriochloa,

Heteropogon, Pennisetum and Aristida are abundant in the lowland site.

Broadleaf species of the genus Justicia, Lantana and Zexmenia are also quite

common, the first two in the upland site, while the third is abundant in the

midland site. Preference of grass species by cattle was reported by Kunst et al.,

(1995). In forests, the most preferred species are D. californica and C. ciliata.

T.pluriflora and crinita are of intermediate preference. Appropriate stubble

height for native grass species for the forest spcies is around 15 cm, as

reported by Renolfi et al., (1987). In the savannas, the most preferred species

is Heteropogon contortus, followed by Pappophorum caespitosum (Kunst

1982).

Trees and shrubs belonging to the genus Prosopis and Acacia provide

foliage and edible fruits of high quality, they are quite considered by ranchers

and cattlemen of the Chaco (Diaz). The genus Prosopis in the Chaco comprise

several native species such as P. alba, P. kuntzei and P. ruscifolia, that are

quite important in the Chaco, as sources of hardwood of high quality that can

be used for furniture and building construction, fruits and shadow in

silvopastoral systems. The Santiago del Estero Experimental Station is testing

P. alba consociated with pastures of Panicum and Chloris in order to develop

a system than can ameliorate saline soils.

Silvopastoral Systems: A New Approach

Intensive land use has converted large areas of the Chaco in dense shrub

thickets and secondary forests, whose „suitability‟ for livestock and timber



146

operations is low. Herbaceous standing biomass is insignificant due to either

low plant density and/or small plant size. The high density of woody plants

and their thorny stems also decrease forage accessibility and hamper livestock

and personnel movements (Nai Bregaglio et al., 1999). Current stocking rates

are negligible, a fact that negatively influences the economy of ranching

operations in areas with woody states (Fumagalli et al., 1997, Kunst et al.,

2006). These problems are shared with other arid and subhumid regions of the

world, creating complex management situations (Gifford and Howden 2001;

Burrows 2002, Van Auken 2009).

From the point of view of forest management, the excess of shrubs and

young tree individuals (advance regeneration) decrease the availability of

resources for tree growth, thus the community requires thinning.

Figure 6. Yield (standing crop) of native grass species and Panicum maximum after a

Low Intensity Roller Chopping treatment. Average 1997-2002. “La Maria”

Experimental Ranch, Santiago del Estero Experimental Station. References: RC:

roller-chopping only, native grass species. RC+seeding: roller-chopping plus seeding

of Panicum maximum cv Green panic.



147

LOW INTENSITY ROLLER-CHOPPING (RBI)

A „roller-chopper‟ is an iron drum with diameter =1.4 m and width = 2.5

m, filled with 3000 kg of water, armed with blades, usually pulled by a 4-

wheel articulate tractor or by a D4 Caterpillar bulldozer. Nowadays, „roller

chopping‟ is widely used in the Chaco region. Reasons are a lack of fine fuel

for carrying out a prescribed fire, high cost of chemical products and

ecological concerns. Roller chopping is a mechanical disturbance aimed at

creating a park-like vegetation structure, which is more suitable for livestock

operations than the current dense, homogeneous „woody state‟ (Kunst et al.,

2003). Woody individuals –especially trees- with DBH > 10-15 cm are left

standing in different patterns and densities, while at the same time the rest,

especially shrubs, are crushed and left as residues that can degrade naturally or

be burnt. The latter practice should be carefully practiced because fire is

extremely soil degrading due to the high density of the wood of the woody

Chaco species. Forage yields and stocking rates usually increase due to the

seeding of a grass species simultaneously with the roller chopping. Exotic

species of the genus Panicum (Poaceae) are commonly used (Ledesma 2006).

They are summer growth perennials which possess the C4 syndrome, and are

adapted to shadow. Average P. maximum yield in under tree cover is estimated

5000-8000 kg DM*ha-1

, a magnitude higher than the standing crop of native

pastures, increasing stocking rates significantly (Kunst et al., 2012, 2014).

Tree thinning and roller-chopping have one thing in common: they are

disturbances, defined here as an event that kills or partially destroys biomass

in a site, creating new after-disturbance environmental conditions (Sousa

1984, Platt and Connell 2003). Parameters of a disturbance such as intensity

and severity can be used to manage their outcomes (White and Jentsch 2001,

Norkko et al., 2006, Buhk et al., 2007). By proper handling the tractor and

roller-chopper sizes, and the number of passes over the standing vegetation,

intensity and severity of the mechanical disturbance could be properly

planned. This is the main principle of the „Low Intensity roller-chopping‟

(RBI) technique developed by research personnel of the Santiago del Estero

Experimental Station to establish a silvopastoral system in the Chaco region.

The mechanical disturbance serves several purposes: (a) to create site

availability by specifically reducing the aboveground structure of shrubs and

decreasing their competence for resources (also called thinning or clearing in

literature); (b) to increase sunlight availability, (c) to facilitate forage

accessibility and livestock movements, and (d) to thin the tree population to an



148

acceptable density. Roller chopping should be aimed at controlling shrub

plants, since they are the main source of „problems‟ instead of trees. The top

soil horizon is slightly disturbed so to seed germination is enhanced.

Severity of the disturbance aimed to create a silvopastoral system could be

assessed by the amount of woody biomass crushed and left as a residue.

SOILS IN SILVOPASTORAL SYSTEMS CREATED BY RBI

Soil is an essential part of any production system. In this section, we will

address the effect of silvopastoral systems on the soil organic matter, and the

structure and functions of soil microbial community. Mollisols, entisols and

alfisols occupy 38 %, 28 % and 16,5 % of the region, respectively. The first

soil order have a better productive capacity than the other two, while the

entisols are less evolved and shallow, mainly showing an ochric epipedon

(Morello et al., 2012). The resilience and buffering capacity of these soils is

limited when faced to an unsustainable management (Sanzano et al., 2005).

However, homogenization of the vegetation (shrub physiognomy) does not

mean that soils also behave in the same way, and could confuse managers.

Figure 7. Annual dynamics of mean shrub volume as percent of the initial volume in

plots with a silvopastoral system established with Low intensity roller chopping.



149

Research conducted by the Santiago del Estero National University in

roller-chopped forests using a medium intensity and severity approach has

shown that the mechanical treatment and rotational grazing does not affect

bulk density 5 years after the initial disturbance (Table 1). Therefore, water

and air movement in the soilis not reduced. In upland sites, the soil total

organic carbon (TOC), particulate organic carbon (POC), microbial carbon

biomass (MBC), and the ratio MBC:TOC are not modified either. These

results are attributed to the brush residues left and crushed by the roller

chopper, mainly composed by twigs and leaves. Roots of Panicum are quickly

degraded and incorporated into the soil. However, cattle grazing, even

rotational (grazing in winter+ rest in early summer) decreases TOC, POC and

the ratio MBC:TOC, likely due to the export of plant residues taken away by

the animals (Taddese et al., 2002). However, the level of total nitrogen (TN)

increases, a fact attributed to addition of Nitrogen and Phosporus via faeces, as

it has been reported by silvopastoral systems in other world ecosystems

(Nyakatawa et al., 2011)

Tree cover has a significant effect: TOC and POC decrease as the distance

to the main bole of a tree increases, probably due to a litter accumulation

gradient (Figure 8). In silvopastoral systems, litter play a significant role in the

dynamics of soil carbon because of litter and soil retain more C than the plants

(Kumada et al., 2008). It is essential that in a silvopastoral system crown

canopies overlap because this cover provides litter rich in carbon. Tree effect

depends on the species: under Ziziphus mistol, TOC content is higher than

under A. quebracho blanco and S. lorentzii canopy cover because of the first

species produce between 16 – 64 % more litter than the other two species.

Effects on Soil Functions

In an upland site, the creation of a silvopastoral system that keeps the

majority of the tree individuals standing, maintain a higher magnitude of the

fractions of soil carbon of fast mineralization, the mineralization rate (kc) of

the soil as well as the activity of the microbial population involved in the

initial degradation of SOM. The high activity of dehydrogenase also supports

this finding. In lowland sites, enzymatic activity increases, because soil water

availability stimulate microbial activity and hence enzyme production

(Albanesi et al., 2003, Table 2).


Table 1. Soil bulk density, total organic carbón(TOC), particulate organiccarbón (POC), total nitrogen (TN),

microbial biomass carbon, ratio MBC:TOC and metabolic quotient (qCO2) at a depth 0-15 cm, in a roller-chopper

experiment

BA

(gr soil cm-3)

TOC

(g C kg-1 soil)

POC

(g C kg-1 soil)

TN

(g N kg-1 soil)

MBC

(ug C g suelo-1)

MBC:TOC

(%) qCO2

Control 0,84 a1 30,10 b 25,37 b 2,24 a 226,07b 0,58 a 0,26 ab

Roller-chopped 0,84 a 28,77 b 24,14 b 2,72 a 167,63 b 0,55 a 0,28 ab

Roller- chopped plus

cattle grazing 0,87 a 22,94 a 18,91 a 2,11 a 91,84 a 0,37 a 0,46 b

Table 2. Potential mineralizable Carbonl (C0), mineralization rate (kc), and dehidrogenase activity (Dh-asa) at 0-15

cm soil depth in a roller-chopper experiment bterween 1999-2003. Roller chopping applied in 2000. „La María‟

Experimental Ranch INTA Santiago del Estero. Referencias: Ecological sites: UP, upland; MD: Midland; LL,

lowland. Treatments: Control, no treatment; RBI: low intensity roller chopping with seeding of Panicum

C0

(mg C kg-1 soil)

kc

(mg C kg-1 soil day-1)

Dh-asa

(mg TPF kg-1 de suelo h-1)

Sitios ecológicos

UP MD LL UP MD LL UP MD LL

Control 384,4 344,2 338,7 0,040 0,054 0,019 96,8 103,9 119,3

RBI 454,1 290,1 386,7 0,027 0,064 0,025 96,1 95,2 134,2


Figure 8. Soil organic carbon (black bars) and particulate organic carbon (grey bars) in g C kg-1

of dry soil at a depth = 0-15 cm, average

2007-2012. „La María‟ Experimental Ranch, INTA Santiago del Estero. References: RBI. two roller-chopperpasses plus seeding of

Panicum; „RBI con pastoreo‟, ídem RBI plus grazing Control: no treatment. 1. 0,50 m from the tree bole; 2. crown center, and 3, crown

border.

Control

0

10

20

30

40

1 2 3 1 2 3 1 2 3

M Qb Qc

RBI

0

10

20

30

40

1 2 3 1 2 3 1 2 3

M Qb Qc

RBI con pastoreo

0

10

20

30

40

1 2 3 1 2 3 1 2 3

M Qb Qc



152

However, in grazed silvopastoral systems located in the upland site the

microbial metabolic quotient (qCO2) increases, a fact suggesting some stress

that decreases the water use efficiency of soil microorganisms (Table 1).

In the midland site, RBI and the seeding of tropical grasses decrease the

carbon stock available for mineralization in the short term (C0) and the

mineralization rate (kc) increase (Table 2). The midland site has usually less

TOC and POC of fast mineralization. These facts suggest that the grazing

management of tropical grasses in a silvopastoral system in this site should be

carefully planned because small magnitude of C0 and a fast mineralization rate

could increase the loss of SOC.

RBI Effects on the Structure and Composition of Soil Microbial

Communities

Research conducted during five years in the semiarid and humid Chaco

regions using terminal restriction fragment lengthpolymorphism (TRFP)

suggest that in the upland and midland sites, roller chopping and the seeding of

tropical species modify the composition of soil microbial communities a year

after the initial treatment (Figure 8). This result agrees with research that

indicates that soil bacterial communities change as the production system

changes, a fact that includes modification of the plant community and soil

features (Lupatini et al., 2013). In the case of RBI, the change in communities

may reflect the significant input of C through the incorporation of plant

residues as a result of the roller-chopping treatment. The microbial population

re-establish after five years of the initial disturbance, agreeing with Vallejo et

al., (2012) that found similar results in a Prosopis juliflora silvopastoral

systems when compared with the control. These results suggest that RBI has

low impact on soil microorganisms, and that they present high resilience to the

environmental alterations caused by production systems (Vallejo et al., 2012).

Forage Yields and Stocking Rates in Silvopastoral Systems

Created by RBI

After the roller-chopper treatment, grass yields increase up to 1000 % or

more, considering native or tropical exotic species (Figure 6, Kunst et al.,

2012, 2014). These yields represent a concomitant increase of stocking rate.



153

Roller chopping plus seeding of P.maximum decreases herbaceous diversity,

but woody plant diversity is not affected when the disturbance is of medium to

low intensity (Kunst et al., 2012).

Shrub Control in a Silvopastoral Systems Created by RBI

Native woody plants, especially shrubs, „return‟ because most are

sprouters: mechanical treatments and/or fire rarely kill them (Bond and

Midgley 2001, Van Auken 2009, Bravo 2008). An important aspect in

silvopastoral systems is their „longevity‟ related to the shrub stratum, referred

in literature as persistence, duration of the treatment, treatment life, or

thickening (Heitchmidt and Pieper 1983, Noble et al., 2005; Gifford and

Howden 2001), since shrub regrowth severely hampers the transit of livestock

and personnel. „Longevity‟ estimates how long the „disruption‟ caused by the

disturbance used to create the silvopastoral system will last. Naveh (1990,

2004), based on the Prygogyne dissipation equation, stated that the main issue

of a management program is to establish the regime of disturbance, defined by

the longevity (~„return interval‟) of treatments. Concerns are both economical

(treatment amortization, Teague et al., 2008) and ecological, since the

disturbance cannot have a return interval that may endanger the sustainability

of the population of a desirable woody or wildlife species (Navall 2008).

Cattlemen in the Chaco have reported that the average longevity of a

severe roller chopper treatment is 3 years (Casas et al., 1978), an interval at

odds with the conservation of forest species, especially their advance

regeneration. Research in the Santiago del Estero Experimental Station has

showed that when a disturbance of intermediate severity is used, longevity of

the treatment could at least 6 years (Figure 7), a more appropriate return

interval for a sustainable silvopastoral system.

The genus Prosopis comprise several native species such as P. alba, P.

kuntzei and P. ruscifolia, that are quite important in the Chaco, as sources of

hardwood of high quality that can be used for furniture and building

construction, fruits and shadow in silvopastoral systems. The Santiago del

Estero Experimental Station is testing P. alba consociated with pastures of

Panicum and Chloris in order to develop a system than can ameliorate saline

soils.



154

WILDLIFE

Hábitats

There are several wildlife habitats in the Chaco: rivers, swamps and

lagoons; cultivated lands and exotic pastures, saline flats, savannas and

grasslands, forests and shrublands. However, for habitat management the

ecosystem classification based on ecological sites and state and transitions is

more specific and detailed (Figure 9). The most significant modifications in

wildlife habitat the Chaco are the disappearance of savannas and grasslands,

the increase of woody component of the vegetation and the transformation of

the upland tall forest in a dense shrub thicket (Bucher, 1980). These

modifications have been caused by overgrazing, indiscriminate logging and

changes of the fire regime. In order to successfully manage wildlife either for

conservation or commercial purposes it is essential to classify vegetation types

using as criteria the quality of these types for wildlife habitat.

Figure 9. Dendrogram build using TRFLP profiles, Ward method and euclidean

dsitance. References: INTA: semiarid environment; Herrero: subhumid environment.

T. Control; SP1. 1 year after roller-chopping treatment; SP5. 5 years after roller-

chopping treatment; Qb, cover of Aspidosperma quebracho blanco; Qc cover of

Schinopsis lorentzii, M cover of Zizyphus mistol.



155

Limiting factors

Critical factors for wildlife in the Chaco are (Bucher, 1980):

Annual dry season that affects primary production and causes the

vanishing of water bodies.

Highly variable rainfall pattern, annual and seasonally.

Extreme oscillations of air temperatures, between 49ºC and -10ºC in

the extremes.

Two environmental pulses, fire and floods.

Bucher (1980) indicate that when confronted with the limiting factors,

wildlife has to adapt by maintaining an appropriate thermal and water balance,

and by building a protection for wildfires and floods, and irregular hunting.

This author summarizes the ethological and physiological adaptations to cope

with these limiting factors.

Species list (not exhaustive, see Table 3):

Mammals: Mazama gouazoubira, small deers, „guasuncha‟.

Tayas supecari, Catagonus wagneriand Pecari tajacu, wild oars,

Tapirus terrestres, tapir,

Puma concolor, puma

Panthera onca, yaguareté,

Herpailurus yaguarondi and Leoparduspardalis (wildcats)

Canidae, foxes

Several species of Dasypodidae, armadillos.

Lagostomus maximus, vizcacha

Pumas and yagueretes are hunted because they conflict with livestock and

other farm animals.

Birds: Myopssi tamonachu, cotorra, Amazona aestiva, parrot

Zenaida auriculata, torcaza,

Columba maculosa and C. picazur, doves, paloma grande.

Emberizidae, Turdidae

Ducks, Anatidae

Tinamidae, quail

Ophidia: Micruruspyrrhocryptus, coral snake, dangerous for men.

Crotalus durissus terrificus, rattlesnake, cascabel

Bothropoides diporus, Rhinocerophis alternatus and Rhinocerophis

ammodytoides, Yararás.



156

Reptiles:

Lizards: Tupinambis merianae and Tupinambis rufescens, looked after

because their skins,

Emblematic species for conservation are Myermeco phagatridactyla, ant

bear, and Priodontes maximus, a large armadillo.

Other information about Chaco wildlife could be found in Canevari &

Vaccaro, 2007; Parera, 2002; Ares, 2007; Naroski & Izurieta, 2003; Short,

1975, Cabrera, 2009), Cabrera, 2010; Leynaud & Bucher, 1999, Heredia,

2008; Gallardo, 1987;and Cabrera, 1998).

Use Values

According to Primack & Ros (2002), the values of use of the Chaco

wildlife are:

Consumption: Hunting for food is very common in the Chaco,

practiced by the aborigines and small farmers (Bucher, 1980). Meat is

the first objective, but skins and eggs are also used.

Commercial hunting. Hunting for sport and recreation is also quite

common. Zenaida auriculata, a dove species declared „agricultural

plague‟ could be hunted without restriction in some Chaco provinces.

Indirect Values

Non consumptive, environmental services. It is assumed that

dispersion of native plant species and the regulation of insect

populations are among the services brought by wildlife.

Existence values. There is an increasing concern about these values of

the Chaco wildlife by people.

Threats

According to Bucher (1980) main wildlife threats are: hunting, habitat

modification such loss of plant cover, loss of wetlands, croplands, overuse of

rivers, and fencing, a practice that limit wildlife movement.

Several mammalian species have decreased their population sizes and

distributions areas dramatically, such as Blastocerus dichotomus, ciervo de los

Pantanos, swamp deer; Ozotoceros bezoarticus, ciervo de las pampas, pampas

deer; and Lama guanicoe, guanaco (Canevari & Vaccaro, 2007; Parera, 2002).


Table 3. List of some wildlife species of the western Chaco of economic importance (not exhaustive)

Species Food Hunting Commercial hunting Control hunting

Mammalians

Mazama gouazoubira X X X (hide, meat)

Tayassu pecari and T. tajacu X X X (hide, meat)

Catagonus wagneri X X

Tapirus terrestris X X X (meat)

Dasypodidae X

Puma concolor X X X (hide) X (damage to livestock)

Panthera onca X X X (hide) X (damage to livestock)

Herpailurus yaguarondi X (hide) X (damage to farm animals)

Leopardus pardalis X (hide) X (damage to farm animals)

Lycalopex griseus X X X (hide) X (damage to livestock and farm animals)

Birds

Myopssita monachus X X (pets) X (damage to crops)

Zenaida auriculata X X X (meat) X (damage to crops)

Columba maculosa and C. picazuro X X X (damage to crops)

Diverse Anatidae X X X (meat) X (damage to crops)

Diverse Tinamidae X X X (meat)

Diverse Emberizidae y Turdidae X (singing birds)

Amazona aestiva X (pets)

Reptiles

Boa constrictor occidentalis X X (hide, pets)

Chelonoidis petersi X X (hide, pets)

Tupinambis merianae and T. rufescens X X (hide)



158

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Chapter 6

PREDICTING PASTURE SECURITY IN

RANGELAND DISTRICTS OF KENYA USING

1 KM RESOLUTION SPOT VEGETATION

SENSOR NDVI DATA

Mwangi J. Kinyanjui Department of Resource Surveys and Remote Sensing,

Nairobi, Kenya

ABSTRACT

Ten day interval Normalized Difference Vegetation Index (NDVI)

data recorded from 1 km resolution SPOT VEGETATION sensor for the

period 2000 – 2011 was used to show variations in vegetation health in

the northern rangeland counties of Kenya to advise on pasture availability

over time and space. Using FAO land cover classification categories,

three land cover types were selected for pasture areas; Herbaceous,

Herbaceous with shrub and Open shrubs. The NDVI data was

summarized for each vegetation type in 8 counties in the northern

rangelands of Kenya. Yearly trends of vegetation were plotted and

polynomial regression used to predict vegetation indices at different times

of the year. Results show that pasture specific vegetation in the study

areas cover over 17 million ha, a significant portion of the total 59 million

hectares of Kenya‟s land area making them very potential for grazing and

the national economic planning. The vegetation health was very

dependent on the hydrological fluxes and regression models for


Mwangi J. Kinyanjui

166

predicting vegetation indices at specific periods of the year gave near

perfect fit in Garissa, Mandera and Wajir counties with coefficients of

Determination (R2) higher than 0.9 in all cases. ANOVA indicated no

differences in vegetation among areas, seasons and years implying that

effects of climate change and increased human activities have not

compromised vegetation in the study period. The study proposes

enhancement of the pasture by promoting nutritious and palatable grasses.

Keywords: Range lands, pasture availability, vegetation indices

INTRODUCTION

Rangelands, defined as vast natural landscapes largely comprising of

grasslands, shrublands, woodlands, wetlands, and deserts, cover almost half of

the Earth‟s land surface (Tal, 2009). In Kenya, they comprise up to 80% of the

total land cover (Rao and Mathuva, 2000). and support the livelihoods of

pastoral communities characterized by large herds of livestock that often

compete for scarce pasture with wild ungulates (Oba et al., 2003). Most of the

rangeland counties of Kenya occur in the northern parts of the country and

David (2010) described them as areas with low rainfall and elongated

droughts. The pastoral communities living here are largely nomadic since they

have to relocate their animals from time to time in search of better pasture

(Berger, 2003). As such pasture availability is a prime issue and is often a

cause of conflict in Kenyan rangelands (Fratkin, 2001 and Otuoma et al,

2009).

If pasture is managed well in the rangelands, they become sustainable

ecosystems (Majule et al., 2009). Management entails availing pasture of the

right quality to meet the demands of all the grazers all the time (Prins and

Beekman, 2008). In these dry areas of Kenya, Berger (2003) has detailed

requirements for a good rangeland management programme. It would ensure

that the carrying capacity is not exceeded through culling and stock reduction,

provision of alternative food during the dry season and implementation of

policies that protect the natural resources. Management also includes proper

prediction of drought seasons which would aid relocation of livestock to areas

of better pasture and would aid communities in coping with changing climatic

patterns (Anyamba et al, 2002).

Methods of pasture prediction range from traditional systems (Berger,

2003) to remote sensing techniques (Zhao et al., 2007) and soil potential

measurement methods (Kusumo et al., 2010). For vast areas, remote sensing


Predicting Pasture Security in Rangeland Districts of Kenya …

167

has been used to compare vegetation data from season to season (Anyamba et

al, 2002) and also among areas (Kinyanjui, 2011). Since pasture availability is

a cyclic event influenced by climatic conditions, hydro-ecological fluxes and

anthropological factors (Otuoma et al, 2009) it may be possible to predict

pasture availability based on the season of the year. This study sought to

predict pasture availability in rangeland counties of northern Kenya and

develop tools for pasture prediction. Using 10 day interval vegetation health

Index data from the Endeleo project (Endeleo, 2013), the variation of

vegetation health from season to season and spatially would help advise

communities on “danger seasons” when they would need to relocate herds or

cull and optimal relocation sites.

METHODS

Study Area and Land Cover Mapping

The study area comprised the northern arid counties of Kenya namely

Marsabit, Mandera, Wajir, Samburu, Garissa, Baringo, Laikipia and Isiolo

(Figure 1). From the FAO land cover map (FAO, 2003) which has 29 land

cover types for Kenya, areas of herbaceous vegetation designated in class A12

(Natural and Semi natural Terrestrial Vegetation) of the Africover legend were

clipped. The specific cover types relevant to pasture were; Open low shrubs

(65-40% crown cover), Open shrubs (45-40% crown cover), Open to closed

Herbaceous vegetation, Shrub savannah and Sparse shrubs. However, using an

image enhancement method (Eastman, 2003), Endeleo project (Endeleo, 2013)

has merged the 29 FAO classes to give 11 classes and provides vegetation

index data based on the 11 classes. The merged pasture specific land cover

classes in the Endeleo data set are referred to Herbaceous, Herbaceous with

shrub and Open shrubs.

NDVI Tools

Using the 11 land cover classes, Endeleo project (Endeleo, 2013) provides

10 day (dekadal) interval data on changes in vegetation health and density all

over Kenya using two indices namely; the Normalised Difference Vegetation

Index (NDVI) and the Dry Matter Productivity (DMP). The data is received


http://endeleo.vgt.vito.be/help.html

Mwangi J. Kinyanjui

168

through the African Monitoring of the Environment for sustainable

Development (AMESD) server in the Department of Resource Surveys and

Remote Sensing (DRSRS). The indices are calculated to show variations from

spectral characteristics of the vegetation as recorded by the 1 km resolution

SPOT VEGETATION sensor. An average of 10 day data is smoothed to

remove possible dips related to bad values, with an algorithm based on Best

Index Slope Extraction (Viovy et al., 1992) which inspects each pixel‟s profile

and removes all abrupt local minima.

Figure 1. Location of the range land districts studied.



169

The NDVI which has been used to indicate vegetation health and density

(Anyamba, et al., 2002 and Kinyanjui 2011) was selected for this study. Ten

day interval data for each vegetation type in each county was summarized into

excel tables cover the period January 2000 and December 2011. This data was

used for analyzing vegetation conditions over time, among seasons and among

counties. This illustrates varying vegetation conditions would be used as a

proxy to show pasture availability (Tucker and Sellers, 1986).over space and

time.

Data Analysis

Trends of vegetation changes were plotted to show low and high seasons

and predict changes over the study period. ANOVA and the Normal Deviate

(Zar, 1999) were used to show differences in NDVI among counties and

among seasons and illustrate seasons with extremely low values. Polynomial

regression (Zar 1999) was used to develop equations that predict the

vegetation conditions of a county area at a time. Using the forward stepwise

procedure in Data Fit 9.0.59 Statistical Software the best “polynomial of fit

“with the coefficient of multiple determination (R2), Adjusted Coefficient of

Multiple determination (Ra2), the Durbin-Watson statistic and standard error of

estimate (SEE) the best polynomial was selected.

RESULTS AND DISCUSSION

The Vegetation Conditions of Kenya

Areas Available for Pasture

There were over 17 million hectares with pasture related vegetation in the

8 counties studied (Table 1). Marsabit and Wajir counties had the most

extensive vegetation of interest with 4.9 million and 4.6 million hectares

respectively as compared to the counties of Laikipia and Baringo which are

dominated by other vegetation types (Figure 2). Shrub savannah was dominant

with about 7 million hectares but mainly restricted to Marsabit, Wajir and

Garissa counties. Although abundance of grasses may not imply availability of

pasture (Ali and Tomrat, 2009), the extensive grasslands show the potential for

grazing in these rangelands described as supporting over 4% of Kenya‟s

human population (Berger, 2003) and availing up to 70% of Kenya‟s land

cover for pastoral activities (Tal, 2009).


Mwangi J. Kinyanjui

170

Table 1. The extent of the herbaceous vegetation types among the districts

County Open low

shrubs

(65-40%

crown

cover)

Open

shrubs (45-

40% crown

cover)

Open to

closed

herbaceous

Shrub

savannah

Sparse

shrubs

Total

Marsabit 1,069,470 159,913 641,176 1,864,835 1,180,578 4,915,972

Wajir 885,977 828,135 510,644 1,857,359 615,082 4,697,197

Garissa 772,869 104,916 114,004 1,029,771 42,112 2,063,671

Isiolo 604,969 96,963 301,631 832,154 167,379 2,003,097

Mandera 695,421 169,392 47,033 336,091 280,010 1,527,947

Samburu 463,499 132,976 215,700 424,477 122,407 1,359,059

Baringo 184,333 67,089 66,449 210,116 36,695 564,681

Laikipia 158,121 11,868 33,540 276,806 2,405 482,740

Total 4,834,659 1,571,252 1,930,177 6,831,609 2,446,668 17,614,365

Figure 2. Vegetation distribution in the selected counties.



171

Vegetation Trends within the Year

Averages of NDVI calculated for the study period indicated that

vegetation had a similar trend among the seasons of the year for all counties

(Figure 3). The vegetation was healthy in November – January season but

gradually decreased towards March. There was a minor peak in April – June

followed by an elongated period of poor vegetation between June and October.

The differences in vegetation health for all the counties and in all vegetation

types were significant (P < 0.05) between the dry and wet periods. However,

there were no significant differences (P < 0.05) among counties except that

Laikipia had a slightly higher average than the other counties. It was noted that

Laikipia County has some artificial grasses which could have enhanced the

vegetation Index. In all cases, open shrub vegetation type was healthier

(Figure 2) with an average Index of over 0.3 which is described as normal for

shrublands and grasslands (Endeleo, 2013). Herbaceous vegetation was

poorest with values of the Index going below 0.2 which Endeleo (2013)

describes as poor. The difference in health of the herbaceous and open shrub

vegetation may be attributed to the presence of shrubs on pasture lands. These

shrubs might have enhanced the spectral characteristics of the vegetation and

may not imply better pasture. However, this may also be an indication of the

improvement of grasses that grow below shrubs as they are protected from the

direct sunlight (Lamprey and Yussuf, 1981).

The trend of vegetation changes among seasons of the year illustrates its

strong dependence on the hydrological fluxes (Otuoma et al, 2009) making it

easy to predict based on the rainfall patterns. In all the vegetation types, 6th

order polynomials were selected as best predictors of the vegetation health in

the seasons of the year (Table 2). Garissa County had the best trends with the

three polynomials selected for herbaceous with shrub, open shrub and

herbaceous vegetation types giving Ra² values over 0.94 which indicates high

level of agreement between predicted and real values (Zar, 1999). Mandera

and Wajir counties also had vegetation with good predictability and in all

cases agreement between predicted and real values was over 90%. The 6th

order polynomial assumes a trend of rising and falling values (Zar, 1999) and

would best predict vegetation that follows a bimodal and trimodal patterns as

described for the rainfall patterns of the study area (David, 2010). Laikipia, the

county where artificial grasses were identified on the ground had the lowest

predictability with two polynomials giving about 60% agreement between

predicted and real values. The vegetation of Laikipia County is therefore less

influenced by hydrological patterns.


Mwangi J. Kinyanjui

172

Figure 3. The trend of vegetation in sampled counties.

Table 2. Models for estimating vegetation indices for selected districts

District

Vegetation

Type Relationship (y = NDVI, x = dekad) Ra²

Baringo

Herbaceous

with shrub

y = -3.05x6 +2.38x5 - 2.73x4 - 1.99x3 +5.84x2

- 4.23x +0.41 0.78

Open shrub

y = -4.30x6 + 3.79x5 - 8.60x4 - 9.24x3 + 5.14x2

- 4.26x + 0.48 0.77

Herbaceous

y = 9.49x6 - 1.53x5 + 1.07x4 - 3.82x3 + 6.57x2

- 4.21x + 0.39 0.71

Garissa

Herbaceous

with shrub

y = -1.15x6 + 9.13x5 - 1.84x4 - 1.50x3+ 7.75x2

- 6.62x + 0.41 0.95

Open shrub

y = -1.36x6 + 1.10x5 - 2.42x4 - 9.55x3 + 8.04x2

- 7.14x - 0.45 0.95

Wajir Laikipia

Isiolo Marsabit

Garissa Mandera

0.15

0.2

0.25

0.3

0.351

0-J

an

10

-Fe

b

10

-Mar

10

-Ap

r

10

-May

10

-Ju

n

10

-Ju

l

10

-Au

g

10

-Se

p

10

-Oct

10

-No

v

10

-De

c

ND

VI

Time of the year

Herbacious Herbacious with shrub Open shrub

0.3

0.35

0.4

0.45

0.5

10

-Jan

10

-Fe

b

10

-Mar

10

-Ap

r

10

-May

10

-Ju

n

10

-Ju

l

10

-Au

g

10

-Se

p

10

-Oct

10

-No

v

10

-De

c

ND

VI

Time of the the yearherbacious with shrub herbacious open shrubs

0.1

0.15

0.2

0.25

0.3

0.35

10

-Jan

10

-Fe

b

10

-Mar

10

-Ap

r

10

-May

10

-Ju

n

10

-Ju

l

10

-Au

g

10

-Se

p

10

-Oct

10

-No

v

10

-De

c

ND

VI

Time of the yearherbacious herbacious with shrubs open shrubs

0.1

0.15

0.2

0.25

0.3

10

-Jan

10

-Fe

b

10

-Mar

10

-Ap

r

10

-May

10

-Ju

n

10

-Ju

l

10

-Au

g

10

-Se

p

10

-Oct

10

-No

v

10

-De

c

ND

VI

Time of the yearherbacious herbacious with shrub open shrubs

0.15

0.2

0.25

0.3

0.35

0.4

10

-Jan

10

-Fe

b

10

-Mar

10

-Ap

r

10

-May

10

-Ju

n

10

-Ju

l

10

-Au

g

10

-Se

p

10

-Oct

10

-No

v

10

-De

c

ND

VI

Time of the yearherbacious herbacious with shrub open shrub

0.15

0.2

0.25

0.3

0.35

10

-Jan

10

-Fe

b

10

-Mar

10

-Ap

r

10

-May

10

-Ju

n

10

-Ju

l

10

-Au

g

10

-Se

p

10

-Oct

10

-No

v

10

-De

c

ND

VI

Time of the yearherbacious herbacious with shrubs open shrubs



173

District

Vegetation

Type Relationship (y = NDVI, x = dekad) Ra²

Herbaceous

y = -8.36x6 + 6.36x5 - 1.07x4 - 2.00x3+ 7.02x2

- 5.80x + 0.36 0.94

Laikipia

Herbaceous

with shrub

y = -8.43x6 + 7.82x5 - 2.29x4 + 1.43x3 +

3.41x2 - 4.38x + 0.49 0.61

Open shrub

y = -1.24x6 + 1.17x5 - 3.69x4 + 3.72x3 +

1.65x2 - 0.04x - 0.51 0.73

Herbaceous

y = -8.36x6 + 6.90x5 - 1.49x4 - 1.13x3 + 6.82x2

- 0.06x + 0.51 0.62

Mandera

Herbaceous

with shrub

y = -1.29x6 + 1.09x5 - 2.76x4 + 9.62x3 +

4.46x2 - 4.52x + 0.34 0.92

Open shrub

y = -1.30x6 + 1.03x5 - 2.22x4 - 7.74x3 + 6.70x2

- 5.54x +0.36 0.91

Herbaceous

y = -1.30x6 +1.17x5 - 3.50x4 - 3.45x3 - 8.65x2

- 2.56x + 0.28 0.94

Marsabit

Herbaceous

with shrub

y = -6.04x6 + 4.83x5 - 9.72x4 - 8.69x3 + 4.34x2

- 0.04x + 0.27 0.84

Open shrub

y = -8.14x6 + 6.32x5 - 1.18x4 - 1.41x3 + 5.87x2

- 4.75x + 0.33 0.87

Herbaceous

y = -3.06x6 + 2.33x5 - 3.62x4 - 9.49x3 + 3.00x2

- 2.30x + 0.19 0.76

Wajir

Herbaceous

with shrub

y = -1.12x6 + 9.71x5 - 2.59x4 + 1.34x3 +

3.44x2 - 4.06x + 0.32 0.93

Open shrub

y = -1.18x6 + 9.64x5 - 2.23x4 - 1.01x3 + 5.55x2

-5.18x + 0.36 0.93

Herbaceous

y = -1.18x6 + 1.07x5 - 3.18x4 + 2.95x3 +

1.46x2 - 0.03x + 0.29 0.94

Vegetation Trends over Time

Vegetation conditions for the June – July period denoted as the season of

poor vegetation and October – November season denoted as season of good

vegetation indicated differences among years in the 2000 – 2011 study period.

In all the years, vegetation indices of the herbaceous vegetation type decreased

gradually from the first dekad of June to the first dekad of July (Figure 4).

Conversely, the indices increased gradually from the last dekad of October to

the last dekad of November. There were no significant differences (P < 0.05)

in vegetation indices for the low vegetation seasons in all the vegetation types.

However, differences were noted for the high vegetation season attributed to

years 2006 and 2011 in Wajir and Isiolo Counties and 2004, 2006 and 2011 in


Mwangi J. Kinyanjui

174

Mandera County. In these years, the vegetation indices show enhanced values

tending towards 0.5 which is characteristic of spectral indices in forest

vegetation (Endeleo, 2013). These results imply that the vegetation of the

rangelands may be improving in the period 2000 to 2011 and the seasons have

not been altered. This finding agrees with Anyamba et al. (2002) who

predicted a shrinking of the Sahelian vegetation using data sets from 1980s to

1990s. the findings therefore predict better vegetation for the study areas in

future.

Figure 4. The trend of vegetation in the June July and October November season.

Wajir

Marsabit

Mandera

Isiolo

Garissa

0

0.1

0.2

0.3

0.4

0.5

YEAR 2000

YEAR 2001

YEAR 2002

YEAR 2003

YEAR 2004

YEAR 2005

YEAR 2006

YEAR 2007

YEAR 2008

YEAR 2009

YEAR 2010

YEAR 2011

ND

VI

30-Oct 10-Nov 20-Nov 30-Nov

0

0.1

0.2

0.3

0.4

0.5

YEAR 2000

YEAR 2001

YEAR 2002

YEAR 2003

YEAR 2004

YEAR 2005

YEAR 2006

YEAR 2007

YEAR 2008

YEAR 2009

YEAR 2010

YEAR 2011

ND

VI


0

0.1

0.2

0.3

0.4

0.5

YEAR 2000

YEAR 2001

YEAR 2002

YEAR 2003

YEAR 2004

YEAR 2005

YEAR 2006

YEAR 2007

YEAR 2008

YEAR 2009

YEAR 2010

YEAR 2011

ND

VI


0

0.1

0.2

0.3

0.4

0.5

YEAR 2001

YEAR 2002

YEAR 2003

YEAR 2004

YEAR 2005

YEAR 2006

YEAR 2007

YEAR 2008

YEAR 2009

YEAR 2010

YEAR 2011

ND

VI

30-Oct noplot 10-Nov noplot 20-Nov noplot 30-Nov noplot

0

0.1

0.2

0.3

0.4

0.5

YEAR 2000

YEAR 2001

YEAR 2002

YEAR 2003

YEAR 2004

YEAR 2005

YEAR 2006

YEAR 2007

YEAR 2008

YEAR 2009

YEAR 2010

YEAR 2011

ND

VI


0

0.1

0.2

0.3

0.4

0.5

YEAR 2000

YEAR 2001

YEAR 2002

YEAR 2003

YEAR 2004

YEAR 2005

YEAR 2006

YEAR 2007

YEAR 2008

YEAR 2009

YEAR 2010

YEAR 2011

ND

VI

10-Jun 20-Jun 30-Jun 10-Jul

0

0.1

0.2

0.3

0.4

0.5

YEAR 2000

YEAR 2001

YEAR 2002

YEAR 2003

YEAR 2004

YEAR 2005

YEAR 2006

YEAR 2007

YEAR 2008

YEAR 2009

YEAR 2010

YEAR 2011

ND

VI


0

0.1

0.2

0.3

0.4

0.5

YEAR 2000

YEAR 2001

YEAR 2002

YEAR 2003

YEAR 2004

YEAR 2005

YEAR 2006

YEAR 2007

YEAR 2008

YEAR 2009

YEAR 2010

YEAR 2011

ND

VI


0

0.1

0.2

0.3

0.4

0.5

YEAR 2001

YEAR 2002

YEAR 2003

YEAR 2004

YEAR 2005

YEAR 2006

YEAR 2007

YEAR 2008

YEAR 2009

YEAR 2010

YEAR 2011

ND

VI

10-Jun noplot 20-Jun noplot 30-Jun noplot 10-Jul noplot

0

0.1

0.2

0.3

0.4

0.5

YEAR 2000

YEAR 2001

YEAR 2002

YEAR 2003

YEAR 2004

YEAR 2005

YEAR 2006

YEAR 2007

YEAR 2008

YEAR 2009

YEAR 2010

YEAR 2011

ND

VI




175

SUMMARY AND CONCLUSION

The rangeland districts of Kenya have vast areas that comprise pasture

potential areas. The areas can be enhanced to make them sustainable to meet

the demand of the growing pastoral population. Some of the management

activities that would make the rangelands sustainable are proper prediction of

pasture availability. This study has demonstrated that it is possible to predict

pasture availability in the districts using vegetation indices that show the

health of vegetation.

The study found out that the vegetation patterns of the selected counties

are largely similar. They are highly dependent on the rainfall and therefore a

dry season indicates poor vegetation in all the counties. As such there is no

option for relocation of the livestock since all the counties experience similar

conditions. This implies that in the July - October period when an elongated

low pasture season is anticipated, culling and stock reduction should be

proposed as an alternative to translocating the animals. Moreover, the study

has proposed models that can be used to predict vegetation indices. For

example, using the models, the effects of climate change on the vegetation can

be tested for specific periods and advice on mitigation methods. This would be

very relevant in extreme droughts which severely affect the vegetation.

Similarly the models can be used to test effects of natural and anthropogenic

effects like fires that can totally eliminate vegetation.

The study found no evidence of a decrease in vegetation health in the

period 2000 – 2011. As such there is no negative effect to the vegetation due

to climate change or the increasing human population in the study area.

Therefore the sustainability of these ecosystems has not been compromised. It

would be necessary to establish the specific carrying capacities of the specific

vegetation types to be able to advise pastoralists on the optimal number of

livestock to keep. As in the case of Laikipia County, it is possible to enhance

the pasture through artificial means which would improve the potential of

these lands to support grazers.

The study used vegetation indices as a proxy for pasture availability. This

may not imply presence of quality pasture. The nutrient content of the various

grasses and their palatability should be assessed and proposals made to

enhance the grazing potential of the study areas.


Mwangi J. Kinyanjui

176

ACKNOWLEDGMENT

This study was part of the resource surveys carried out by the Department

of Resource surveys and Remote Sensing in the Ministry of Environment. We

wish to thank Endeleo project for image analysis, specifically Delrue Josefien

of VITO who guided us on data processing methods.

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INDEX

A

access, 47

accessibility, 146, 147

acid, 132, 143

activity level, 117

adaptation(s), 12, 19, 121, 155

adsorption, 112

adults, 34

Africa, 2, 74, 91, 176

age, 23, 111, 124

agriculture, 50, 78, 138, 143

air temperature, 135, 155

algorithm, 168

amortization, 153

amphibians, 10, 18, 50, 73, 83

anatomy, 3

angiosperm, 27

ANOVA, xi, 110, 166, 169

Argentina, v, vii, viii, x, xi, 5, 6, 8, 12, 30,

31, 38, 49, 83, 133, 134, 143, 159, 160,

161, 162, 163

aromatic compounds, 39

arthropods, 34

Asia, 128

assessment, 50, 75

assimilation, 111

atmosphere, 108, 121

Austria, 23, 76

average longevity, 153

B

banks, 39, 97

barriers, 7, 10, 17, 23

base, 3

beetles, 34

behaviors, 34

biochemistry, 124

biodegradation, 128

biodiversity, ix, 19, 25, 31, 33, 35, 47, 50,

77, 79, 81, 83, 98, 99, 107

biogeography, viii, 9, 15, 20, 22, 23, 27, 28,

30

biological activity, 107, 120

biomass, 107, 109, 116, 117, 121, 124, 125,

126, 127, 128, 129, 130, 132, 143, 146,

147, 148, 149, 150, 162, 177

biotic, 26, 27, 99

birds, 10, 21, 22, 27, 50, 83, 157

Bolivia, 5, 6, 8, 12, 16, 38, 128

Brazil, vii, viii, x, 1, 5, 6, 12, 19, 20, 29, 30,

31, 32, 33, 34, 35, 36, 37, 38, 40, 41, 48,

72, 73, 75, 77, 78, 81, 82, 83, 84, 85, 87,

88, 90, 91, 93, 94, 98, 99, 100, 101

Brazilian dry forests, vii, 31

breakdown, 116

breeding, 138, 142

buffalo, 177

burn, ix, x, 82, 98, 106, 108, 129


Index

180

C

caatinga, vii, ix, 24, 81, 83, 85, 86, 87, 88,

89, 90, 96, 97, 99, 100, 101, 102

cambium, 140, 158

carbon, x, 106, 107, 109, 110, 111, 112,

113, 114, 116, 119, 121, 125, 126, 127,

128, 129, 130, 131, 132, 149, 150, 151,

152, 160, 162

carbon emissions, 126

Caribbean, 10, 23, 24, 28, 75, 129

Caribbean Islands, 10, 24, 28, 75

cattle, x, 106, 108, 125, 137, 138, 142, 143,

145, 149, 150

C-C, x, 106, 110, 120, 121, 122

cellulose, 121

chemical, 99, 107, 147, 162

Chile, 158

China, 127, 128

chopping, 146, 147, 148, 150, 152, 153, 154

circulation, 89

classes, 40, 77, 111, 114, 144, 167

classification, xi, 32, 88, 94, 154, 165, 176

clay minerals, 112

climate(s), vii, xi, 9, 13, 16, 22, 25, 31, 87,

88, 94, 99, 102, 134, 138, 166, 175

climate change, xi, 9, 16, 22, 25, 87, 166,

175

climatic factors, 88, 121

close relationships, 33

closure, 9, 10, 24

CO2, x, 106, 107, 108, 110, 120, 121, 123

cocoa, 73

Colombia, 8, 28, 71, 72, 73, 74, 77, 162

colonization, 8, 10, 17, 25

commercial, 144, 154

communication, 140

community(s), viii, ix, 21, 30, 40, 47, 74,

75, 78, 83, 102, 107, 117, 129, 130, 131,

140, 146, 152, 161, 166, 167

competitors, 144

complexity, 7, 19, 92

composition, 10, 22, 33, 40, 95, 117, 152,

161

compounds, 125

computing, 76

conditioning, 95

configuration, 31

conflict, 155, 166, 176

conflict resolution, 176

Congress, 159

conservation, viii, x, 21, 28, 30, 50, 73, 78,

82, 99, 101, 153, 154, 156

construction, 35, 99, 145, 153

Continental, 23, 26, 90

corolla, 3

correlation, 11, 14, 40, 45, 112, 113, 122

correlation analysis, 113, 122

cost, 33, 147

Costa Rica, 47, 49, 74, 126, 130

cotton, 143

covering, ix, 8, 14, 39, 81, 85

criticism, 18

crop(s), ix, 82, 98, 126, 143, 146, 147, 157

crown, 140, 149, 151, 167, 170

crown fires, 140

crystalline, 85, 87

CT, 26

cultivation, ix, 82, 125, 126

cycles, 107

cycling, 107, 128, 129

D

danger, 167

data analysis, 78

data processing, 176

data set, x, 40, 106, 167, 174

database, 76

decomposition, 107, 112, 126

deficiency, 122

deficit, 83

deforestation, 108, 112, 113, 125, 126, 127,

128, 130, 132, 143

degradation, 38, 112, 118, 127, 149, 177

deposition, 10

depression, 87

depth, x, 106, 109, 110, 111, 113, 114, 115,

116, 117, 118, 119, 120, 121, 122, 123,

150, 151


Index

181

deviation, 11

diet, 34, 177

digestion, 132

dispersion, 11, 142, 156

displacement, 92

distilled water, 110

distribution, vii, viii, 2, 5, 10, 11, 12, 13, 16,

17, 21, 25, 28, 30, 31, 33, 35, 40, 45, 47,

48, 49, 50, 75, 76, 92, 95, 99, 101, 107,

113, 115, 129, 170

divergence, 3, 7, 9

diversification, 19, 25, 26, 83

diversity, vii, viii, ix, 1, 2, 11, 14, 15, 22,

23, 26, 28, 30, 33, 34, 35, 37, 38, 40, 45,

47, 48, 49, 50, 73, 75, 76, 82, 83, 99,

140, 153, 161, 176

DNA, 3, 4, 18, 27

DOI, 159, 161, 162

dominance, 49

drainage, 8, 15, 115, 135

drought, 37, 117, 122, 166, 176

dry forests, vii, viii, ix, 5, 6, 12, 22, 25, 26,

30, 31, 35, 47, 49, 76, 82, 86, 101, 108,

129

E

ecological processes, 98

ecology, vii, 28, 47, 76, 99

economic systems, 92

ecosystem, ix, 32, 81, 82, 83, 99, 107, 128,

154, 160

Ecuador, 5, 6, 15, 20, 27, 28, 130

EEA, 161

egg, 32

endangered, 99, 128

energy, 91, 107

England, 73

environment(s), ix, 4, 5, 7, 8, 9, 11, 12, 13,

14, 16, 17, 18, 26, 33, 38, 48, 49, 50, 76,

86, 98, 140, 154

environmental change, 3, 100

environmental conditions, 7, 19, 142, 147

environmental degradation, 98

environmental services, 83, 156

enzymatic activity, 149

enzyme, 149

equilibrium, 177

erosion, 85

evaporation, ix, 82, 89, 90, 98

evapotranspiration, 28, 88

evidence, 3, 8, 10, 11, 12, 18, 19, 22, 87,

139, 175

evolution, 6, 7, 19, 20, 21, 22, 34, 47, 72,

73, 74, 76, 99, 110

exile, 59

exploitation, 83, 143

extinction, 9, 99

extraction, x, 39, 106, 109, 113, 125, 132,

143

F

families, ix, 2, 30, 32, 34, 41, 47, 48, 72, 74,

95

farmers, 156

farms, 138

fauna, viii, 18, 29, 31, 33, 36, 41, 47, 49, 50,

73, 75, 82, 83, 99

fencing, 137, 156

fertility, 119

fertilization, 127, 128

filters, 50

fire event, 140

fire resistance, 140, 142

fires, 140, 142, 143, 175

fish, 22, 83

flank, 91

floods, 88, 138, 155

flora, 18, 26, 27, 50, 82, 83, 87, 99, 102

flowers, 14, 39

fluctuations, 19, 22

food, 32, 35, 49, 156, 166, 177

food chain, 32

forest ecosystem, 130, 161

forest fragments, viii, 16, 30, 78

forest management, 146

formation, viii, 30, 35, 37, 39, 47, 83, 90,

98, 107

formula, 110


Index

182

fossils, 8, 32

fragility, 92

fragments, 15

frequency distribution, 40

fruits, 12, 20, 137, 145, 153

fungi, 130

G

genetic diversity, 35

genus, vii, 1, 2, 4, 5, 6, 7, 10, 11, 13, 14, 17,

21, 23, 25, 26, 34, 41, 48, 78, 140, 143,

145, 147, 153

germination, 98, 148

glacial period, vii, 16, 31

global climate change, 107

global scale, 83, 107

Google Earth, 40

gracilis, 57, 137

grass(es), x, 106, 108, 112, 111, 113, 117,

120, 121, 122, 124, 137, 138, 140, 143,

145, 146, 147, 152, 166, 169, 171, 175,

177

grasslands, 129, 135, 137, 138, 140, 143,

154, 166, 169, 171

grazers, 166, 175

grazing, xi, 121, 143, 144, 145, 149, 150,

151, 152, 162, 165, 169, 175, 177

Great Britain, 124, 128, 129

greenhouse, 126

greenhouse gas, 126

greenhouse gas emissions, 126

growth, vii, 1, 107, 113, 116, 144, 146, 147,

160

growth rate, 144

H

habitat(s), vii, viii, 1, 2, 4, 6, 7, 9, 11, 15,

16, 17, 18, 19, 24, 26, 49, 50, 154, 156,

177

hair, 33

harbors, 50

hardness, 143

hardwood forest, 135, 137, 144

harvesting, 137, 144, 145

health, xi, 165, 167, 169, 171, 175

heat loss, 14

height, 87, 97, 140, 141, 145

herpetofauna, 21, 72

heterogeneity, 89

highlands, 85, 162

history, viii, 2, 3, 11, 18, 19, 20, 23, 24, 26,

47

Holocene, 24

horses, 138

host, 32, 33, 34

human, ix, xi, 35, 49, 82, 83, 98, 99, 128,

166, 169, 175, 177

human actions, 83

human development, 98

humidity, 37, 88, 120

humus, 108

hunting, xi, 38, 133, 137, 138, 155, 156, 157

hymenoptera aculeate, vii

hypothesis, 5, 8, 9, 10, 17, 18

I

identification, 50, 72, 74

image, 167, 176

image analysis, 176

in transition, 6, 176

income, 177

Indians, 138

individuals, 41, 142, 144, 146, 147, 149

industry, 143

inferences, 18, 20

insects, 31, 32, 35, 39

institutions, xi, 134

integrity, 50, 99

intron, 3

iron, 37, 147

islands, 6, 10, 31, 91

isolation, 15, 17, 26, 142

isotope, 111


Index

183

K

Kenya, vi, vii, xi, 165, 166, 167, 169, 175,

176, 177

kill, 153

L

landscape, 8, 50, 82, 83, 94, 97, 98, 127,

130, 138

landscapes, 49, 50, 98, 128, 166

larvae, 34

Late Pleistocene, 24

Latin America, 24, 75, 127

leaching, 120

lead, 11, 88, 91

legend, 167

legume, 15, 125

levees, 135

lianescent clade, vii, viii, 1, 2, 3, 4, 11, 18

life cycle, 34, 83

light, 3, 10, 27, 127

lignin, 117

limestone, 37

livestock, 50, 137, 143, 145, 147, 153, 155,

157, 166, 175, 177

logging, 137, 143, 154

logistics, 177

longevity, 153

low temperatures, 14

M

magnitude, 147, 149, 152

majority, 32, 149

Malaysia, 75

mammal(s), 26, 50, 83

man, 98

management, vii, xi, 49, 108, 127, 130, 134,

138, 143, 144, 146, 148, 152, 153, 154,

159, 160, 162, 166, 175

mangroves, 9

Maryland, 75

mass, 91, 92

materials, 35

matrix, 31, 40, 47, 78

matter, x, 74, 106, 107, 112, 118, 120, 121,

122, 124, 125, 132

measurement, 75, 166, 176

meat, 157

media, 160

median, 13

Mediterranean, 159, 161

Metabolic, 122, 123

metabolizing, 122

meter, 39, 40

methodology, 4, 33, 109

Mexico, 5, 9, 21, 28, 48, 49, 79, 126, 131

microbial communities, x, 106, 116, 117,

122, 124, 130, 152, 162

microbial community, 127, 148, 162

microclimate, 83

micronutrients, 131

microorganism(s), x, 106, 107, 112, 116,

117, 118, 119, 120, 122, 123, 124, 152

Microsoft, 40

migration, 8, 10, 16

mineralization, 115, 116, 120, 127, 129,

130, 149, 150, 152

Miocene, 3, 8, 9, 15, 19, 20, 23, 26

Missouri, 20, 22, 26, 76

MMA, 50, 75, 78, 79, 83, 101

models, 8, 46, 175

modifications, 32, 117, 154

moisture, x, 91, 106, 116, 117, 121, 122,

123, 124, 125

moisture content, 116, 117, 122, 124

morphogenesis, 21

morphology, 2, 11

mortality, 99, 142

mosaic, 8, 9, 82, 94, 135

mountain ranges, 91

N

National Academy of Sciences, 25, 27

national product, 144

native species, 145, 153


Index

184

natural resources, 83, 98, 100, 166, 176

Neotropical Dry Forests, vii

Neotropical region, vii, 30, 32, 34, 35, 41,

75

New Zealand, 127

nitrification, 129, 130

nitrogen, 107, 125, 126, 128, 129, 130, 131,

149, 150, 162

nodes, 22

North America, 3, 28, 47

null, 9

nutrient(s), 32, 107, 108, 116, 117, 128, 175

O

oceans, 23

old age, 123, 124

operations, 138, 143, 146, 147

organic matter, vii, x, 105, 106, 107, 108,

112, 113, 115, 116, 117, 118, 119, 120,

121, 122, 123, 124, 125, 127, 128, 129,

130, 132, 148

organs, 14, 96

oscillation, 94

overgrazing, 38, 137, 143, 154

overlap, 149

oxidation, 109

P

Pacific, 23

Panama, 9, 10, 23, 24, 26

Paraguay, 6, 12, 38, 49, 78

parallel, 91

parenchyma, 95

pathogens, 14

pathways, 8

permit, 51

personal communication, xi, 133

Peru, 5, 6, 15, 16, 20, 21, 23, 27, 28, 48, 76

Philippines, 130

phosphorus, 107, 131, 162

phylogenetic tree, 4

physical characteristics, 127

physical environment, 99

physical structure, 49

physiological correlates, 20

pistil, 14

plant growth, 135

plants, 9, 10, 12, 14, 15, 16, 20, 25, 26, 33,

35, 37, 77, 82, 83, 86, 92, 96, 97, 98,

108, 111, 112, 116, 117, 119, 146, 148,

149, 153

plasticity, 19

plastid, 3, 4, 27

Pleistocene, vii, 7, 8, 9, 10, 22, 23, 24, 26,

31, 87, 102

Pliocene, 8, 9, 10

pollen, 9, 33

pollinators, 34, 35, 78

pools, 128

population, x, 7, 34, 50, 83, 98, 106, 108,

117, 121, 147, 149, 152, 153, 156, 169,

175

population growth, 108

population size, 156

positive correlation, 112

positive relationship, 114

precipitation, 89, 115, 120

predation, 34

predators, 32, 34

predictability, 171

preparation, 47, 100

preservation, 144

primate, 22

productive capacity, 148

project, 19, 76, 167, 176

propagation, 142

protection, x, 14, 82, 99, 112, 122, 142, 145,

155

Puerto Rico, 125

R

radiation, 14, 21, 27, 88

radius, 36, 45

rain forest, 9, 26, 28, 129, 130


Index

185

rainfall, ix, 37, 81, 83, 88, 89, 91, 92, 94,

101, 107, 108, 115, 119, 120, 122, 123,

124, 135, 155, 166, 171, 175

rainforest, 74, 107, 128

rangeland, vii, xi, 138, 160, 165, 166, 167,

175, 176, 177

reading, 19

recognition, viii, 1

reconstruction, 3, 18

recovery, 142

recreation, 156

recycling, 108

regeneration, 144, 145, 146, 153

regions of the world, 2, 146

regression, xi, 165, 169

regression model, xi, 165

regrowth, 120, 123, 153

regulations, 177

relatives, 27

relevance, 83, 92

relief, 31, 89, 108

remote sensing, 166, 177

requirements, 166

researchers, 49, 95, 144

residues, 106, 143, 147, 149, 152

resilience, 148, 152

resistance, 142, 143

resolution, vii, xi, 4, 18, 165, 168

resources, 33, 100, 146, 147

respiration, x, 106, 109, 110, 120, 121, 122,

124, 125, 130

response, x, 14, 106, 128, 176

restrictions, 50, 143

root(s), 96, 112, 113, 123, 130, 135, 176

root growth, 135

rotations, 129

Royal Society, 25, 26

runoff, 88, 135

S

salt accumulation, 135

salt tolerance, 9

savannah, 167, 169, 170

savannas, vii, xi, 101, 132, 134, 135, 137,

140, 143, 145, 154

science, 15, 23, 26

scientific knowledge, 99

scrublands, 92

SEA, 73

sea level, 38

Seasonal Deciduous Forests, vii

seasonal flu, 117

seasonal forests, vii, 6, 26, 31

seasonality, 107, 115, 124

security, vii

sediments, 3, 9, 85, 88

seed, 2, 11, 14, 98, 148

seeding, 146, 147, 150, 151, 152, 153

semi-deciduous dry tropical forest, vii, 108

senescence, 122

sensing, 166, 177

sensitivity, 33

services, 156

settlements, 137

sexual dimorphism, 33

shape, 11, 14

shelter, 49

shock, 116, 122

shoreline, 10

shortage, 48, 123

showing, 89, 112, 148

shrubs, vii, ix, xi, 1, 2, 82, 83, 95, 97, 144,

145, 146, 147, 153, 165, 167, 170, 171

signals, 33

simple linear regression, 110

skeleton, 22

social behavior, 34, 35, 75

software, 40, 78

soil erosion, 88

soil type, 83, 87, 94, 128

solution, x, 106

South America, viii, ix, 2, 4, 5, 7, 8, 9, 10,

12, 19, 21, 22, 25, 26, 27, 28, 30, 31, 37,

41, 50, 73, 76, 78, 82, 88, 99, 100, 102,

160

South Pacific, viii, 1, 2, 11, 12

Spain, 137

specialists, 48


Index

186

speciation, 8, 17, 20, 23, 25

species richness, viii, 20, 28, 30, 33, 35, 49,

72, 162

spiders, 34, 35

stability, 124, 130, 131

stabilization, 112, 128

standard deviation, 114, 116, 118, 119, 121,

123

standard error, 111, 114, 169

state(s), ix, 5, 6, 12, 16, 31, 81, 84, 85, 88,

91, 118, 123, 124, 140, 144, 146, 147,

154, 161

statistics, 110

stock, 152, 166, 175

storage, 96

storms, 91

stratification, 159

stress, 38, 83, 88, 142, 152

stretching, 91

structure, vii, viii, 7, 12, 29, 30, 31, 35, 39,

50, 74, 107, 127, 131, 140, 144, 147,

148, 161, 162

Styria, 23

subsistence, 137

substrate, 86, 116, 117, 118, 120, 121, 122,

123, 124

succession, 125, 128, 129

sulfur, 107, 131

sustainability, 144, 153, 175

syndrome, 147

synthesis, 22

T

taxa, viii, 2, 3, 4, 6, 8, 12, 16, 17, 18, 33, 45,

47, 48, 49, 83

taxonomy, 47

techniques, 39, 47, 140, 166

temperature, 14, 24, 37, 88, 108, 120, 121

terpenes, 140

terrestrial ecosystems, 35

territory, 38, 84

testing, 145, 153

texture, 108, 127, 135

thinning, 100, 144, 146, 147

thorax, 32

threats, x, 82, 99, 156

time series, 177

tissue, 140

topology, 4, 6

trade, 91, 92, 138

traits, 2, 19, 140

transformation(s), vii, x, 82, 95, 99, 105,

108, 111, 129, 154

translation, 137

treatment, 25, 144, 146, 149, 150, 151, 152,

153, 154

tropical dry forest, x, 76, 105, 107, 108,

111, 115, 126, 128, 129

tropical forests, 22, 32, 35, 48, 76, 82, 106,

128, 129, 131

tropical rain forests, 21

turnover, 47, 74, 132

U

United Kingdom (UK), 22, 28

United Nations, 77

United States (USA), 19, 25, 27, 28, 77,

124, 162

Uruguay, 6, 49

V

Valencia, 21, 24

variables, 110

variations, xi, 83, 165, 168

velvet, 33

Venezuela, v, vii, x, 105, 106, 108, 109,

115, 124, 126, 127, 130

vertebrates, 15

violaceae, vii

vouchers, 4

W

war, 138

Washington, 71, 128


Index

187

water, viii, ix, x, 2, 9, 10, 11, 12, 14, 75, 82,

83, 88, 91, 92, 96, 97, 98, 99, 106, 107,

109, 116, 119, 122, 125, 127, 128, 129,

132, 135, 144, 147, 149, 152, 155

water vapor, 91

watershed, 37

western llanos, vii

Wet Forests, vii

wetlands, 156, 166

wetting, 116

wildlife, xi, 134, 153, 154, 155, 156, 157,

177

Wisconsin, 124

wood, 3, 35, 143, 147

worldwide, 32, 33, 34

X

xylem, 27

Y

Yale University, 26

yield, 143, 147


Dry Forests: Ecology, Species Diversity and Sustainable Management

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