Termite (Isoptera) assemblages in some regions of the Goiás State, Brazil

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Termite (Isoptera) Assemblages in Some Regions of the Goiás State, Brazil

by

Hélida Ferreira da Cunha1, Diogo Andrade Costa2, Divino Brandão3

ABSTRACT

Termites are the dominant fauna in tropical soils, having an important role in nutrient cycling processes and soil formation. They are a dominant component of the Cerrado fauna, reaching high densities in some areas. Quantitative and qualitative assessment of the termite assemblages were carried out in natural (Riparian Forests, Mesophytic Interfluvial Forest, Cerrado and “Cerradão”) and impacted areas (pastures and plantations of sugar cane, banana, Eucalyptus trees, Bahia-coconut and Guariroba) in eleven municipalities of the Goiás state in Brazil. In each environment, 8 quadrats of 25 m2

were studied. The

quadrats were located 50 m apart from the habitat edge and 30 m between each other. Seventy-seven species belonging to the Families Rhinotermitidae (Subfamilies Coptotermitinae, Rhinotermitinae and Heterotermitinae) and Termitidae (Subfamilies Apicotermitinae, Nasutitermitinae and Termitinae) were collected. The species with the highest number of colonies were Ano-plotermes sp. 4 (68), Anoplotermes sp. 2 (57), Nasutitermes kemneri (46) and Ruptitermes sp. (34). Anoplotermes sp. 4 and N. kemneri were found in 10 of the 11 sampled municipalities while Anoplotermes sp. 2 was found in all of them. All the sampled localities have high equitability ranging form 0.85 to 0.94 because all the species were registered once or twice. Most of the species found feed upon decomposing organic matter and/or are litter foragers. Of the 77 species sampled, we were not able to identify 26 (designed as mor-phospecies). Some of them might be new species.

Keywords: Cerrado, diversity, Isoptera, pasture, plantation, termite.

INTRODUCTION

Termites (Order Isoptera) are social insects with ca. 2800 described species (Cancello & Schlemmermeyer 1999; Constantino 1998, 1999). Around 500 1Universidade Estadual de Goiás, Brazil, [email protected]

2Faculdade Araguaia, Goiânia-GO, Brazil, [email protected]

3Universidade Federal de Goiás, Goiânia-GO, Brazil, [email protected]

2 Sociobiology Vol. 47, No. 2, 2006

species occur in the Neotropics, a diversity only overcome by Oriental and Ethiopian regions where most studies are concentrated (Cancello & Schlem-mermeyer 1999; Constantino 1998, 1999). Well known by their economic importance as agricultural and wood pests, the termites are detritivorous and represent one of the dominant groups in the fauna of tropical ecosystems, having an important role in nutrient cycling processes and soil formation (Black & Okwakol 1997; Cancello & Schlemmermeyer 1999; Constantino 2002; Davies et al. 1999; Eggleton et al. 1996). According to Eggleton & Bignell (1995) and Overal (2001), the group represents almost 10% of the animal biomass at the tropics.

In tropical ecosystems, from open vegetation areas such as the Cerrado sensu sticto to rainforests, the ecological importance of termites has been poor studied (Cancello & Schlemmermeyer 1999), and the inventories that exist concentrate in few localities (Constantino in press). In Latin America, Brazil is the country where the termite fauna has been best studied, having ca. 280 described species (Constantino 1998, 1999).

Termites are a dominant and conspicuous component of the Cerrado fauna, reaching overwhelming densities in some areas. Considering only the open areas, termite richness in the Cerrado can reach ca. 150 species (Constantino in press). Some of the species, such as Cornitermes cumulans can be considered keystone species because of their great abundance and environmental impact (Redford 1984).

This work presents a quantitative and qualitative assessment of the termite fauna in some municipalities in Goiás state (Brazil), designed to represent the different meso-regions. The study intended to improve the knowledge on the termite fauna of the state, by collecting in regions where sampling was never carried out before.

Study AreaThe study area includes natural and disturbed habitats in 11 municipalities

of the state of Goiás (Fig. 1). This is the only Brazilian state that is totally embedded in the Cerrado Biome. The Cerrado is the second largest of Brazil’s major biomes, occupying 22% of the national territory (Oliveira Filho & Ratter 2002). The biome has altitudes varying from 300 m to 1800 m, with a predominance of latosols (Oliveira Filho & Ratter 2002). The climate is characterized by a rainy season from October to March followed by a dry period from April to September. Rain fall ranging from 800 to 2000 mm and

3 da Cunha, H.F. et al. — Termite Assemblages in Goiás

Fig. 1. Sampling Municipalities in Goiás State (Brazil).


annual temperature from 18ºC to 28ºC along the year (Dias 1992). Several vegetal formations occur at the Cerrado biome, including grass-

lands, savanna and forests (Eiten 1972; Coutinho 1978) like the cerrado sensu lato (represented by a physiognomic gradient that includes the campo limpo, campo sujo, the cerrado sensu stricto, and the cerradão), riparian forest, and the mesophytic interfluvial forest.

Sample collection in disturbed habitats was made in grasslands and in plantations of sugar cane, banana, Eucalyptus trees, Bahia-coconut and Guariroba trees, where available in each municipality, and sample collection in natural areas was made in the three vegetation types cited above, remnant in the legal protected area of private properties. Some of these areas presented light degrees of habitat alteration such as selective wood extraction, presence of cattle or trails. Areas with more heavy alterations were not used.

MATERIALS & METHODS

In each environment, 50 m away from the edge, eight 25 m2 quadrats were defined, 30 m apart from each other. In each quadrats, a one-hour exhaustive search was carried out in all the places where termites can be found (50 cm deep in the ground, soil surface, dead wood, hypogean nests, epigean nests, arboreal nests and foraging galleries).

Samples were identified to species or morphospecies level using taxonomic identification keys, taxonomic notes and revisions (Araujo 1954; Emerson & Banks 1957; Emerson & Banks 1965; Krishna & Araujo 1968; Mathews 1977; Fontes 1985; Cancello 1989; Constantino 1990; Constantino 1995; Cancello et al. 1996; Constantino & De Souza 1997; Constantino 1999; Cancello & Myles 2000; Constantino 2001), and by comparison with the Isoptera collections at the Federal University of Goiás (UFG) and the Zool-ogy Museum of the São Paulo University (MZUSP). Specimens from all the identified species and morphospecies were deposited at the termite collection of the UFG.

Richness estimates and diversity indexes were calculated for the sample as a whole and for each sampled municipality, using the software EstimatS (Colwell 2005) using 500 permutations. Parameters such as mean species richness, “uniques” (mean number of species that occur in one sample), “duplicates” (mean number of species that occur in two samples), Michaelis-


Menten (richness estimator that predicts the stabilization of the number of species using the observed richness), Bootstrap (richness estimator based on the species incidence) and Shannon-Wiener diversity index (H) were calcu-lated. Bootstrap is a non-parametric method (can be used in samples with different abundance distributions) that uses the total number of species to estimate the total richness, not being restricted to rare species (Santos 2003). The transformation eH

makes possible to analyze Shannon-Wiener diversity in

species richness units. The equitability was calculated from Shannon diversity (H) and species richness (S) using the formula E=H/ln(S) (Krebs 1989).

Cumulative species curves (collector’s curve) were done using mean rich-ness and number of species. To estimate the stabilization point of the curve, the Michaelis-Menten equation was used (Colwell 2005). This curve repre-sents the total number of species registered during data collection when new individuals or samples are added to the entire data set previously obtained (Gotelli & Colwell 2001).

Only the quadrats where termite species were found were included in the analysis because some of the methods can not be implemented when there are zero values. Thus, the total number of analyzed quadrants was 208 while the total number of quadrats studied was 244.

Colony number was interpreted as the abundance when used to calculate the diversity index. Total number of colonies in each municipality varied according to the habitat availability near sampling locations.

The species were classified according to the feeding habit registered for the genus, following Constantino (1999). Trophic guilds used were: humi-vorous, that feed on humus and soil organic matter; xylophagous, that feed mainly on wood; litter-feeders, for the ones that forage at the surface, cutting leafs from litter or grasses; and intermediate for the ones that do not have a specialized feeding habit.

RESULTS

Seventy-seven species were collected (Appendix 1) in 244 quadrats (the coconut plantation at the Matrinchã municipality had enough area for just four quadrats), for a total of 694 colonies belonging to the families Rhinotermitidae (Subfamilies Coptotermitinae, Rhinotermitinae and Heterotermitinae) and Termitidae (Subfamilies Apicotermitinae, Nasutitermitinae and Termitinae).


The species that had more colonies were: Anoplotermes sp.4 (68), Anoplotermes sp.2 (57), Nasutitermes kemneri (46) and Ruptitermes sp (34). Anoplotermes sp.2 was the only species that was present in all sampled municipalities, while Anoplotermes sp.4 and N. kemneri were present in ten out of eleven munici-palities. The mean number of colonies for a species was 9.01 ± 12.54 and for 40% of the species, there were just one or two colonies found (Fig. 2). In 225 quadrats (91%) one to five species were found (3.34 ± 1.8) and no termites were found in 38 of the sampled quadrants (15%) (Fig. 3).

The collector’s curve (Fig. 4) began to stabilize with one third of the samples. The stabilization of the richness was predicted to occur after 54 samples, when just 51 species were collected. Richness estimators of Mi-chaelis-Menten and Bootstrap overlapped when 80 species were collected in a total of 142 samples.

Richness and diversity estimates are found in Table 1. Comparing H with eH

it was verified that the expected diversity was higher than the observed

diversity. The equitability was high in all the municipalities since most of the species were registered only once or twice, rendering a more homogeneous distribution.

The number of unique and duplicate species together represented more than half of the total species richness in the majority of the sampled munici-palities (Table 1). This makes the termites a very particular group since most of the species have restricted distributions. For example, in Matrinchã and Alto Paraíso just three species presented more than two colonies.

The majority of the species in all the studied municipalities feed on soil and decomposing organic matter and/or foraged on the litter (Fig. 5).

DISCUSSION

This work is the first study carried in the Goiás State, with an extensive sampling that included eleven municipalities in different regions. Previous studies were all done in only one locality, generally in areas near Goiânia, the capital of the State. Compared to these previous works, the present study emerges as the greatest inventory of termite species (77) in Goiás, excluding the Federal District. Brandão & Souza (1998) collected 33 species in the Cerrado sensu stricto, mesophytic forest and grasslands in the Goiânia municipality, while in this same municipality Ferreira Junior (1999) registered 60 species


in 15 fragments of mesophytic forest. Oliveira (2003) found 22 species in an altitudinal gradient from Cerrado to Campo Rupestre at the Morro Feio, in the municipality of Hidrolândia. Freitas et al. (2004) collected 29 species in Cerrado, Campo Rupestre and riparian forests at the Serra de Caldas Novas State Park (PESCAN), in the Caldas Novas Municipality. Costa (2005) found 25 inquiline termite species of C. cumulans in 2.25 hectares of Campo Limpo at the Emas National Park (PNE) in the Mineiros municipality. Lima Filho (2005) collected 32 species in an altitude gradient from Cerrado to Campo Rupestre at the Serra dos Pirineus State Park in the Pirenópolis municipality. Most of the species collected by the authors cited above were also registered during the present work and only 24 previously registered species were not present at the eleven municipalities sampled.

In this work, from the 77 collected species, 26 morphospecies were not identified, some of them might even be new species. The Apicotermitinae are grouped in a genus because of identification limitations, thus, the real number of species found may be higher. Noirotitermes noiroti was recently described in the Cerrado of the Piauí State (Cancello & Myles 2000) so it does not appear in the New World Isoptera Catalog of Constantino (1998). This species was not collected in Goiás during previous studies.

Ferreira Junior (1999) was the only researcher that collected termites of the family Kalotermitidae at Goiás, generally underestimated in rapid inventories, because of their habit of using dry dead wood for shelter. If we consider all the lists in these studies, Nasutitermitinae is the dominant group in richness and abundance, and almost all the epigean and arboreal nests in the Cerrado are made by species from this subfamily.

An important characteristic of the Cerrado termite fauna is the great amount of humivorous litter-feeding species, confirming the ecological importance of these species in the processes of ecosystem maintenance, being respon-sible for the organic matter cycling. The great amount of litter produced at Cerrado areas and the existence of some selective extraction of wood where the species were collected, explain the abundance of humivorous and litter feeders found. A taxonomic revision will probably increase the humivorous proportion since almost all the members of the subfamily Apicotermitinae are characterized as humivorous species.


Constantino (1998, 1999) and Cancello & Schlemmermeyer (1999) highlighted that one of the main obstacles for neotropical termitology development has been the lack of taxonomic information. Few groups have been comprehensively revised and there are few well trained taxonomy spe-cialists, a fact that hampers the identification work. Thus, a lot of works with

Fig. 2. Number of species of termites by frequency of the colonies.

Fig. 3. Distribution of the number of quadrats by number of species of the termites.


erroneous or incomplete classifications have been published, hindering the process of production and storage of organized information, and making the comparisons between the results of different works difficult.

Fig. 4. Collector's curve of termites in eleven municipalities of the State of Goiás, Brazil.

Fig. 5. Distribution of species of termites according trophic guild.


In addition, the comparison of data from published studies is difficult be-cause there is a lack of standardized sampling protocols. The species richness obtained in an inventory is dependent on the local features but also on the sampling effort that can be defined by using the collector’s curve. But in most tropical ecosystems this curve rarely stabilizes (Santos 2003). Constantino (1992) and Ferreira Junior (1999) are some of the authors whose studies about diversity of termites presented the collector’s curve. Despite the fact that our curve presented a tendency to stabilization when considering the eleven municipalities together, more sampling would be needed to appropriately sample all kinds of habitats considered in this study.

There are regions and municipalities in Goiás state where inventories of the termites’ assemblages were never done. It is believed that the original fauna of these regions will never be completely known since most of them have been significantly disturbed. Most of the area of the state has been and continues to be cleared because of the expansion of the agricultural frontiers. Today’s rate of clearance for the Cerrado varies from 22.000 to 33.000 km2

per year and is believed that 55% of the original area of Cerrado was already converted into grasslands, agricultural fields, planted forests and urban areas, among others (Klink & Machado 2005).

ACKNOWLEDGMENTS

We are grateful to the colleagues that helped during data collection (Lorena, Kleber, Leandro, Gabriel, Guilherme, Danilo, Natália, Luiz). For the logistic

Table 1. Richness and diversity estimators for termite assemblages found in eleven municipalities of the State of Goiás, Brazil.

Municipalities quadrats colonies Richness “Uniques” “Duplicates” H eH

E

Aruanã 15 61 25 10 7 2.99 19.89 0.93Cocalzinho 22 76 30 17 3 3.09 21.98 0.91Cristalina 21 52 19 10 4 2.53 12.57 0.86Cristianópolis 13 61 30 18 5 3.14 23.10 0.92Hidrolândia 36 126 42 13 12 3.46 31.82 0.92Iporá 22 89 33 16 5 3.18 24.05 0.91Matrinchã 13 23 16 13 0 2.61 13.60 0.94Nova Crixás 17 53 25 12 8 2.97 19.49 0.92Pontalina 17 37 15 5 5 2.53 12.55 0.93Alto Paraíso 8 26 16 11 2 2.60 13.46 0.94Serranópolis 24 90 28 9 6 3.05 21.12 0.91All 208 694 77 13 18 3.69 40.04 0.85


support and permits granted to enter their properties, we thank Eduardo Luiz Mesquita, Reginaldo Freire, Mozart Martins de Araújo, Sandra, Paulo Roberto de Carvalho, Cacique Arumani of Karajás Indigenous Society, Car-los Alberto Guimarães, André Ferreira da Cunha, Ozório Vilela Neto, Paulo Henrique and Carol. Dr Eliana M. Cancello allowed us to access the MZUSP collection for material comparisons. We also wish to thank FUNAPE-UFG for the financial support. please spell out acronym

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Appendix 1. List of species of termite of the eleven municipalities in Goiás State (Brazil).

Family Rhinotermitidae Labiotermes longilabius Silvestri Subfamily Coptotermitinae Nasutitermes aff minor Holmgren Coptotermes sp Wasmann Nasutitermes corniger Motschulsky Subfamily Rhinotermitinae Nasutitermes ephratae Holmgren Dolichorhinotermes sp Emerson Nasutitermes kemneri Snyder & Emerson Subfamily Heterotermitinae Nasutitermes sp Dudley Heterotermes longiceps Snyder Nasutitermes unduliceps Mathews Heterotermes tenuis Hagen Noirotitermes noiroti Cancello & Myles Family Termitidae Paracornitermes emersoni Araújo Subfamily Apicotermitinae Paracornitermes hirsutus Araújo Anoplotermes sp1 Fr. Müller Paracornitermes orthocephalus Silvestri Anoplotermes sp2 Fr. Müller Parvitermes bachanalis Mathews Anoplotermes sp3 Fr. Müller Procornitermes araujoi Emerson Anoplotermes sp4 Fr. Müller Procornitermes triacifer (Silvestri) Aparatermes sp1 Fontes Rhynchotermes diphyes Mathews Aparatermes sp2 Fontes Rhynchotermes nasutissimus (Silvestri) Grigiotermes sp Mathews Subulitermes aff microsoma (Silvestri) Ruptitermes spp Mathews Syntermes molestus (Burmeister) Tetimatermes sp Fontes Syntermes nanus Constantino Subfamily Nasutitermitinae Syntermes wheeleri Emerson Agnathotermes glaber Snyder Velocitermes glabrinotus Mathews Angularitermes pinochio Cancello & Brandão Velocitermes heteropterus (Silvestri) Araujotermes sp Fontes Velocitermes paucipilis Mathews Armitermes cerradoensis Mathews Velocitermes velox (Holmgren) Armitermes euamignathus Silvestri Subfamily Termitinae Armitermes lanei Snyder Amitermes sp Silvestri Armitermes sp1 Wasmann Cylindrotermes sp1 Holmgren Armitermes sp2 Wasmann Cylindrotermes sp2 Holmgren Atlantitermes stercophilus Constantino & De Souza Dentispicotermes globicephalus (Silvestri) Coatitermes sp Fontes Dentispicotermes sp Emerson Constrictotermes cyphergaster Silvestri Dihoplotermes inusitatus Araújo Cornitermes bequaerti Emerson Microcerotermes sp Silvestri Cornitermes cumulans Kollar Microcerotermes exiguus (Hagen) Cornitermes pilosus Holmgren Microceroteremes strunckii (Sörensen) Cornitermes snyderi Emerson Neocapritermes araguaia Krishna & Araújo Cornitermes villosus Emerson Neocapritermes opacus (Hagen) Curvitermes minor Silvestri Neocapritermes talpa (Holmgren) Curvitermes odontognathus Silvestri Orthognatotermes sp Holmgren Cyranotermes timuassu Araújo Spinitermes sp1 Wasmann Diversitermes diversimiles Silvestri Spinitermes sp2 Wasmann Embiratermes festivellus Silvestri Spinitermes trispinosus (Hagen & Bates) Embiratermes silvestrii Emerson Termes sp Linnaeus Embiratermes sp Fontes

Termite (Isoptera) assemblages in some regions of the Goiás State, Brazil

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