ORIGINAL PAPER

Bee diversity on nectarful and nectarless honey mesquites

Jordan Golubov • Maria C. Mandujano •

Armando J. Martınez • Jorge Lopez-Portillo

Received: 10 June 2009 / Accepted: 26 October 2009 / Published online: 10 November 2009

� Springer Science+Business Media B.V. 2009

Abstract Nectar production has been proposed as an

adaptation to attract pollinators that benefit from this

resource. Energetic investments may be expensive, so

some species such as Prosopis glandulosa have developed

a dimorphic system of nectar production, which is expected

to affect floral visitor behaviour and then plant fitness. We

quantified bee diversity during a 2 year period in a popu-

lation of the honey mesquite in order to determine changes

in bee diversity due to the presence of nectar, bee prefer-

ences to collect either nectar of pollen, and to determine

between year variations of bee faunas. Floral visitors were

captured at three different times of the day during the

flowering seasons of 1994 and 1995, in a population of

Prosopis glandulosa which has a 1:1 proportion of nectar:

nectarless individuals. Pollinators were clearly distinct

between nectar morphs, bee species diversity and relative

abundance of visits were significantly greater on nectarful

than on nectarless plants, with species on nectarless indi-

viduals being a subset of those in the nectarful morph. Our

results suggest differences in the function of floral rewards

(i.e., nectar and pollen) to attract floral visitors. For the

Chihuahuan arid environment, mesquite provides floral

rewards with ease, quantity and quality for close to 10% of

all bee fauna making them important components of these

communities.

Keywords Bee diversity � Diversity profiles �Floral rewards � Floral visitors � Deceit pollination

A large number of studies that aim to estimate bee diversity

include the number of species, subgenera, and genera

(Michener 2006), associated to a particular plant species

and to a lesser extent for plant communities (Minckley and

Roultson 2006). In general, studies compare bee faunas

between plant communities, at the species or genera-sub-

genera level. For example, biogeographically the bee fauna

in equivalent neartic regions appears more diverse in Cal-

ifornia, USA, than in Spain, apparently because the former

includes more climatic and floral zones (Michener 2006).

Unfortunately as Freitas et al. (2009) clearly state, ‘‘The

main problem faced in Latin America is the lack of

information on richness, diversity, taxonomy, distribution,

population dynamics and impact of human activities on

most bee species’’, so inferences on diversity are difficult to

obtain in the Neotropics.

Several studies have concluded that xeric habitats are

the regions that have the highest bee diversity (Michener

2006; Minckley 2008). Such diversity has been attributed

to soil characteristics that enable bees to dig nests, the less

J. Golubov

Departamento del Hombre y su Ambiente, Laboratorio de

Ecologıa, Taxonomıa y Fisiologıa Vegetal, Universidad

Autonoma Metropolitana-Xochimilco, Calzada del Hueso 1100,

Colonia Villa, Quietud, 04960 Mexico, D. F., Mexico

e-mail: gfjordan@correo.xoc.uam.mx

M. C. Mandujano (&)

Departamento de Ecologıa de la Biodiversidad, Instituto de

Ecologıa, UNAM, Apartado Postal 70-275, Ciudad

Universitaria, 04510 Mexico, D.F., Mexico

e-mail: mcmandu@ecologia.unam.mx

A. J. Martınez

Instituto de Neuroetologıa, Universidad Veracruzana, Apartado

Postal 566, 91190 Xalapa, Veracruz, Mexico

e-mail: armartinez@uv.mx

J. Lopez-Portillo

Red de Ecologıa Funcional, Instituto de Ecologıa A. C.

(INECOL), Apartado Postal 63, 91070 Xalapa, Veracruz,

Mexico

e-mail: jorge.lopez.portillo@inecol.edu.mx

123

J Insect Conserv (2010) 14:217–226

DOI 10.1007/s10841-009-9248-8

humid conditions inside the ground-nests increases pres-

ervation of pollen and nectar, the absence of water reduces

flooding and competition seems to be avoided between

solitary and social bees (Michener 2006). Specifically for

Mexico, detailed studies also suggest that the bee fauna is

more diverse in xeric than in temperate areas (Ayala et al.

1996). Of the few studies of bee diversity in arid envi-

ronments, oligolecty is predominant (Waser et al. 1996;

Minckley and Roultson 2006) and specialization is not as

common as once thought. In addition, Minckley and

Roultson (2006) in a study in the arid southwest suggest

that most bee species are rare and unevenly distributed,

with little cospecialization, and use readily available

resources irrespective of plant species. In addition, tem-

poral and spatial variation in bee fauna seems to be rather

high (Herrera 1988, 1995; Minckley et al. 1999) in xeric

environments, especially for solitary bees which can be

partly attributed to short bee life cycles and the temporal

and spatial variation of rainfall limiting the potential for the

evolution of mutualisms (Minckley 2008; Minckley and

Roultson 2006).

Flowers and their attributes such as color, shape, size

and the presence of nectar and/or pollen, fragrances and

oils have been considered characteristics that attract and

influence floral visitors (Sprengel 1793; Proctor et al.

1996). Temporal and spatial variation in the expression,

quantity and quality of each of these attributes are deter-

minants of plant fitness as they affect the number of visits

received (Gori 1989; Ohashi and Yahara 1998), the quality

of visitation, the foraging pattern (Heinrich 1983; Keasar

2000), and pollen carry-over. In addition, the variation in

foral traits has been considered an important component of

coexistence and diversity in pollinator guilds (Palmer et al.

2003). Although the expression of floral attributes enhan-

ces plant fitness, increasing their allocation necessarily

involves an energetic investment for the plant, because

they are rich in nitrogen and phosphorus, two elements

often in growth-limiting short supply in natural habitats,

which may ultimately lead to a reproductive cost (South-

wick 1984; Pyke 1991; Proctor et al. 1996). However,

some species or individuals within populations have

evolved strategies that avoid the cost incurred by floral

attributes such as nectar (Rust et al. 2003; Thakar et al.

2003; Renner 2006), some of which have led to deceit

pollination systems with common occurrence of nectarless

individuals intermingled with nectar produces (e.g. the

Orchidaceae; Cozzolino and Widmer 2005). Plant deceit

pollination systems apparently evolved to cheat floral vis-

itors while achieving the same fitness among mimic (i.e.,

cheaters) and model plants (Renner 2006). Few studies

describe the effect of the presence of some resource on the

visitors’ performance (Zimmerman 1988), in general the

benefits are evaluated for the plant point of view, and its

effect on pollinators is often neglected. Interactions

between insects and plants are an important component of

biodiversity and with the current debate about pollinator

declines, information about plants and their floral visitors is

urgently needed. We documented bee diversity on nectarful

and nectarless mesquites (Prosopis) in Mexico and provide

information about bee diversity, visitation rates and spe-

cialization of native and exotic bee species.

Prosopis (Fabaceae) is a common genus in the arid and

semi arid environments of North and South America and

has a typical bee pollinator syndrome (Simpson et al. 1977)

characterized by a large number of inflorescences consist-

ing of 100? tiny yellow hermaphrodite florets per inflo-

rescence. Trees are visited by a large number of polylectic

as well as oligolectic bees (Simpson and Neff 1987) and

constitute mating sites, areas where predator–prey interac-

tions occur, as well as growth sites for different animal taxa

(Simpson et al. 1977). Although it has not been described

yet in other Prosopis species, Prosopis glandulosa var.

torreyana has a dimorphic system of nectar production

among plants of the same population (Lopez-Portillo et al.

1993; Golubov et al. 1999). This dimorphic system involves

a 1:1 proportion of nectarful: nectarless individuals that are

intermingled, in dense scrublands and vegetation stripes in

the Southern Chihuahuan desert. Previous studies showed

similarities in floral morphology, flowering time, seed mass

and germination success between nectarful and nectarless

individuals (Golubov et al. 1999; Golubov et al. 2004).

Differences between nectar morphs were found in fruit set

which is higher in nectarful individuals, while nectarless

plants produce more pollen (Golubov et al. 1999), and just

considering floral visitors, nectarful individuals were visited

by one order of magnitude more than nectarless individuals

(Golubov et al. 1999).

Our goal was to compare bee faunas (diversity) in a

small scale, among nectar versus nectarless trees and also

between years. The comparison will aid to determine the

effect of floral rewards on bee visitation patterns and

diversity. To do this, several authors have proposed that

diversity profiles (Kindt et al. 2006; Ricotta 2002) are a

useful technique when comparing different communities as

single indices may have different sensitivities to rare or

common species (Liu et al. 2007). We chose Renyi

diversity profiles (Tothmeresz 1995) as they are equivalent

to a large number of what Liu et al. (2007) categorize as

information related methods (namely Hill’s diversity

number of order a, Daroczy’s entropy of type a, Tsalli’s

generalized entropy, among others). When the diversity

values of one community throughout the profile is greater

than the other, we can then state that the former is more

diverse than the latter (they are separable). When the

curves intersect at some point in the profile we cannot say

that one community is more diverse than the other

218 J Insect Conserv (2010) 14:217–226

123

(i.e., they are non separable). In addition, specific values of

the scale parameter a of the Renyi profile at 0, 1, 2 and ?are related to species richness S, the Shannon diversity

index H, the Simpson diversity index D-1 and the Berger–

Parker diversity index d-1 respectively (Legendre and

Legendre 1998; Kindt et al. 2006).

The dimorphic system of nectar production in the honey

mesquite is a suitable natural experiment to assess the effect

of nectar production on pollinator diversity. The specific

aim of this study was to compare the guild of pollinators

visiting the honey mesquite focusing on what effect nectar

production has on species diversity and gender of bee vis-

itors between nectar morphs and between years.

Methods

Study area

This research was conducted in the Mapimı Biosphere

Reserve (hereafter MBR), in the Southern Chihuahuan

desert (26�N 104�W, 1,100 m altitude, 264 mm yearly

average rainfall, 21�C mean temperature) during the 1994

and 1995 mesquite flowering season. Yearly rainfall was

138.5 mm in 1994 and 198.4 mm in 1995 (MBR climatic

station). Field work was concentrated in a 1 ha plot of

desert scrubland where P. glandulosa var. torreyana sur-

rounds a temporary (only during the rainy season) water-

catchment site. Within the plot, all reproductive individuals

were tagged and their nectar condition determined initially

in 1994 (Golubov et al. 1999). Prosopis glandulosa var.

torreyana is a desert perennial tree or shrub common to the

arid environments of Southern United States and Northern

Mexico.

Visitor surveys

During the 1994 and 1995 flowering season, we performed

fixed-time capture efforts on 12 trees (6 per nectar morph) at

three times of day (0800–1000, 1200–1400 and 1600–

1800 hours) every other day. The sample size (12 trees) was

conditioned by the sampling effort, which included 5 min

captures on the selected plants. Since thorns precluded the

use of nets and bees remain in the inflorescences regardless

of the observer, bees were captured with 15 9 20 cm

plastic bags or directly with the aid of lethal chambers

containing ethyl acetate. Captured individuals were identi-

fied, sexed and deposited at the Museo de Zoologıa, Fac-

ultad de Ciencias, UNAM, Mexico (see Yanez-Ordonez and

Hinojosa-Dıaz 2004 for a preliminary list). We only

assessed bees of the Apoidea even though other visitors

were also found visiting P. glandulosa inflorescences at

MBR. Identification of families followed Michener (2006)

and those of genera followed the classification of Michener

et al. (1994). A preliminary list of visiting species on both

nectar morphs was previously published for the 1994

flowering season (Golubov et al. 1999).

Bee diversity estimations

We calculated the relative dominance (RD) of individual

bee species as the mean of their relative abundance (species

abundance/total abundance) 9 100 plus their relative fre-

quency (species frequency/total frequency) 9 100 to obtain

values between 0 and 100%.

To estimate our collection effort, we used species

accumulation functions which are non-decreasing curves

that represent the expected accumulated number of dif-

ferent species encountered within a certain geographical

area as a function of a measure of the collection effort,

usually time or person-hour units (Soberon and Llorente

1993; Dıaz-Frances and Soberon 2005). We used captured

bee data to estimate the number of floral visitors that could

be expected to be found visiting mesquite inflorescences

during a single season. Species accumulation functions

were fitted with the program Species Accumulation Func-

tions developed at CIMAT (www.cimat.mx). The database

consisted of the accumulated number of new species found

during each sampling date, pooling all samples taken

during a single day (including nectar and nectarless

individuals).

Diversity profiles were obtained for data sets between

nectar morphs and years, and we then subdivided the data

set into nectar morph, bee gender and year. Renyi diversity

profiles are one of the techniques that rank communities

using a collection of diversity indices. The values of the

Renyi diversity profiles (Ha) are calculated from the fre-

quencies of each component species and a scale parameter

(a) that ranges from 0 to infinity, such that

Ha ¼lnP

pai

� �

1� a:

The Renyi profile provides species richness S (when

H = 0), the Shannon diversity index H (when H = 1), the

Simpson diversity index D-1 (when H = 2) and the

Berger–Parker diversity index d-1 (when H = ?) as

follows (Legendre and Legendre 1998):

H0 ¼ lnðSÞH1 ¼ H ¼ �

Xpi logpi

H2 ¼ ln D�1� �

¼ lnX

p2i

� ��1� �

H1 ¼ ln d�1� �

¼ lnX

p�1max:

We calculated Bray-Curtis similarity coefficients for the

whole data set (nectar morph, year and bee gender).

J Insect Conserv (2010) 14:217–226 219

123

Diversity analyses were made with Biodiversity R (Kindt

and Roe 2005) and vegan packages (Oksanen et al. 2005)

in R (R Development Core Team 2005).

Pollen deposition

To assess differences in the amount of pollen received by

each nectar morph, we tagged three fresh inflorescences of

each of six trees while immature during the same sampling

period as above. Once the inflorescences matured, we

collected one tagged inflorescence (sequence of collection

determined at random) on three consecutive days. The

styles of at least 10 florets per inflorescence were separated,

stained with methylene blue, and the number of pollen

grains was counted on each stigma.

Results

During the blooming period, the number of flowering

individuals of P. glandulosa was similar for both nectar

morphs, resulting in an equal proportion of nectarful to

nectarless morphs in the study site that did not change

among years (Table 1; v2 = 0.02, df = 2). However,

individuals not always flower each year.

Visitor surveys

During the 2-year study period, a total of 64 bee species

were collected on flowers of the honey mesquite. These

consisted of 20 genera, 55 species and 728 individuals

collected in the first year and 17 genera, 44 species and 598

individuals in the second year. During the second year,

nine new species visited Prosopis flowers and 20 species

found on the previous year were not collected (Table 2).

The total number of species expected from adjusting the

species accumulation functions showed that we would

expect 78 species for 1994 (with an interval 64–117 species

using a likelihood level of 0.05) and 45 species for 1995

(interval 44–47 species). For the 1994 sampling season

there was no best model suggesting that a more exhaustive

sampling effort was needed, but for the 1995 flowering

season the best model (Exponential) was 11 times better

than other models (Clench and logarithmic).

Relative dominance differed between genera, the

Megachilidae (RD = 47.02%) having the highest followed

by Colletidae (RD = 23.71%), Apidae (RD = 11.63%),

Andrenidae (RD = 9.74%) and finally Halictidae (RD =

5.89%). Bee relative abundance was strongly biased

towards the Megachilidae in both 1994 and 1995 (47 and

54% of all individuals captured, respectively) and Collet-

idae (36 and 31%) followed by Apidae (7.9 and 5.7%),

Andrenidae (6.2 and 9.4%), and Halictidae (3.3 and 1.2%).

Bee relative abundance was dominated by 13 species

(RD [ 2%) for both nectar morphs and years (Table 2)

even though the relative importance of the less abundant

families changed between years (Table 3). During 1994,

Colletes was the most common genus (31%) followed by

Ashmeadiella (22%), while during 1995, the relative

abundance was reversed (24 vs. 30%, for Colletes and

Ashmeadiella, respectively). The relative abundance of

Megachile was similar in both years (19 vs. 18%). Perdita

followed in abundance with less than 10% and the rest of

the genera (N = 19) accounted for less than 5% of the

captures. Relative abundance in 1994 was clearly charac-

terized by more genera and species with few individuals,

which were not captured in 1995 (30 vs. 24 species,

respectively). Only eight species were consistently abun-

dant in both years (Table 1). The ANOVA (visits were

square root transformed) indicated there are greater relative

abundances of bees in nectarful, than in nectarless trees

(F1, 252 = 70.42, P \ 0.001). The number of species that

visited the nectarful morph accounted for more than 50%

of total species diversity found within a given year.

Bee diversity differed between nectar morphs (Fig. 1).

In nectarful individuals the most common species was

Ashmeadiella luecozona that accounted for 13.4% (1994)

and 17.8% (1995) of total yearly captures (Table 1). In the

nectarless morph, the most abundant species was Colletes

algarobiae during 1994 and Megachile newberryae in

1995. Species richness as well as all diversity indices

summarized in the diversity profile (Shannon, Simpson and

Berger-Parker) was higher in nectarful than nectarless tress

(Table 4, Fig. 1). Within nectar morphs, the 1994 season

was more diverse for nectarful individuals (i.e. they were

separable), but were non-separable for the nectarless morph

(the curves intersect). This only reflects the large differ-

ences in total captures in which nectarful trees had 97% of

total captures and nectarless trees had only 3% of total

captures during 1994, even though this changed slightly in

1995, where nectarful trees had 93% of total captures and

nectarless trees had 7%.

Table 1 Number of nectarful and nectarless individuals over a 3 year

period in a 1 ha scrubland site within the Southern Chihuahuan desert

Tree morph Year

1994 1995 1996

Nectarful 140 129 109

Nectarless 170 160 135

Non flowering 48 69 114

All individuals within the hectare (n = 358) were assessed for nectar

production every year, but there were always non-flowering trees,

which are also indicated

220 J Insect Conserv (2010) 14:217–226

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Table 2 Number of individuals and relative dominance (RD) of each bee species captured on nectarful (NF) and nectarless (NL) trees of

Prosopis glandulosa var. torreyana in a scrubland within the Southern Chihuahuan desert during the flowering seasons of 1994 and 1995

Family Genus Species Number of bees RD

1994 1995

NF NL NF NL

Andrenidae Perdita Callicerata Ckll 0 0 1 0 0.43

Andrenidae Perdita Sp. 1 4 0 10 0 1.31

Andrenidae Perdita Sp. 2 3 0 0 0 0.5

Andrenidae Perdita Sp. 3 2 0 3 0 0.97

Andrenidae Perdita Sp. 4 30 0 11 3 2.83

Andrenidae Perdita Sp. 5 3 2 24 0 2.26

Andrenidae Perdita Sp. 6 0 0 2 0 0.47

Andrenidae Perdita Sp. 7 3 0 2 0 0.97

Apidae Apis Mellifera L 2 1 0 0 0.89

Apidae Centris Pallida Fox 0 0 1 0 0.43

Apidae Centris Rhodopus Ckll 1 0 0 0 0.43

Apidae Ceratina Sp. 1 0 0 4 0 0.54

Apidae Diadasia Sphaeralcearum Ckll 8 1 0 0 1.12

Apidae Epeolus Mesillae Ckll 5 0 11 2 1.85

Apidae Epeolus Sp. 1 2 0 3 0 0.97

Apidae Epeolus Sp. 2 5 0 4 2 1.59

Apidae Melissodes Tristis Ckll 26 1 6 0 2.42

Apidae Nomada Sp. 1 1 0 0 0 0.43

Apidae Xeromelecta Larreae Ckll 0 0 1 0 0.43

Apidae Zacosmia Maculata Cr 4 0 0 0 0.54

Colletidae Colletes Aff. perileucus 78 0 26 1 5.13

Colletidae Colletes Aff. scopiventer 0 0 1 0 0.43

Colletidae Colletes Algarobiae Ckll 91 4 54 2 7.25

Colletidae Colletes Deserticola Timb 3 0 0 0 0.5

Colletidae Colletes Louisae Ckll 1 0 8 1 1.55

Colletidae Colletes Prosopidis Ckll 1 0 0 0 1.43

Colletidae Colletes Salicicola Ckll 41 1 40 2 4.73

Colletidae Colletes Wickhami Timb 3 0 11 0 1.31

Colletidae Hylaeus Asininus Ckll&Casad 34 0 38 2 3.96

Colletidae Hylaeus Sp. 1 1 0 0 0 0.43

Halictidae Agapostemon Cockerelli Crawford 4 0 2 0 1.01

Halictidae Agapostemon Sp. 1 6 0 0 0 0.62

Halictidae Agapostemon Sp. 2 1 0 0 0 0.43

Halictidae Agapostemon Tyleri Ckll 0 0 0 1 0.43

Halictidae Lasioglossum Sp. 1 0 1 0 0 0.43

Halictidae Lasioglossum Sp. 2 1 0 0 0 0.43

Halictidae Lasioglossum Sp. 3 1 0 0 0 0.43

Halictidae Lasioglossum Sp. 4 8 2 4 1 2.13

Megachilidae Anthidium Cochimi Snell 23 0 1 1 2.11

Megachilidae Anthidium Cockerelli Schwarz 1 0 0 0 0.43

Megachilidae Anthidium Paroselae Ckll 7 0 0 0 0.65

Megachilidae Ashmeadiella Bigeloviae Ckll 6 0 1 0 1.05

Megachilidae Ashmeadiella Breviceps Mich 10 0 13 0 1.65

Megachilidae Ashmeadiella Clypeodentata Mich 23 1 5 1 2.69

Megachilidae Ashmeadiella Gillettei Titus 8 0 5 0 1.27

J Insect Conserv (2010) 14:217–226 221

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When we considered the gender of bees, male bees were

not found on nectarless individuals, while both genders

were found on nectarful individuals. When we subdivided

bee diversity by gender, nectar morph and year, female bee

diversity in nectarful individuals during 1994 was the

highest followed by males on nectarful individuals during

1995 and finally males on nectarful individuals during

1994 (Fig. 2). The lowest diversity was found for female

diversity on nectarless individuals during 1995. Bee

diversity between female individuals on nectarful trees

Table 3 Relative abundance of bee families corresponding to the five

bee families collected in two consecutive years on inflorescences of

nectarful and nectarless individuals of Prosopis glandulosa var. tor-reyana in a locality within the Southern Chihuahuan desert

1994 1995

Nectarful Nectarless Nectarful Nectarless

Megachilidae 47.2 38.1 51.9 62.8

Colletidae 35.8 23.8 32.1 18.6

Apidae 7.6 14.3 5.4 9.3

Andrenidae 6.4 9.5 9.5 7.0

Halictidae 3.0 14.3 1.1 2.3

D 12.8 9.8 11.5 10.7

n 707 21 555 43

D indicates Simpson’s dominance index, which is the ‘‘apparent’’

number of species accounting for at least 80% of the total number of

collected individuals, indicated by n for each morph and year

Fig. 1 Renyi diversity profiles of bees during the 1994 and 1995

flowering seasons, visiting nectarful (NF) and nectarless (NL)

inflorescences of Prosopis glandulosa var. torreyana in a locality

within the Southern Chihuahuan desert

Table 2 continued

Family Genus Species Number of bees RD

1994 1995

NF NL NF NL

Megachilidae Ashmeadiella Leucozona Ckll 95 3 99 7 9.25

Megachilidae Ashmeadiella Meliloti Ckll 1 0 1 2 1.32

Megachilidae Ashmeadiella Prosopidis Ckll 1 0 3 0 0.93

Megachilidae Ashmeadiella Rhodognatha Ckll 12 1 41 4 3.75

Megachilidae Coelioxys Aff. hunteri 2 0 2 0 0.93

Megachilidae Coelioxys Menthae Ckll 0 0 2 0 0.47

Megachilidae Dioxys Productus Ckll 1 0 0 1 0.86

Megachilidae Dolichostelis Perpulchra Crawford 1 0 0 0 0.43

Megachilidae Megachile Chilopsidis Ckll 7 0 0 0 0.65

Megachilidae Megachile Discorhina Ckll 6 0 2 0 1.08

Megachilidae Megachile Lippiae Ckll 11 0 2 0 1.27

Megachilidae Megachile Newberryae Ckll 95 1 84 8 8.65

Megachilidae Megachile Odontostoma Ckll 7 0 5 2 1.7

Megachilidae Megachile Sidalceae Ckll 7 2 2 0 1.59

Megachilidae Megachile Spinotulata Mich 1 0 0 0 0.43

Megachilidae Osmia Subfasciata Cresson 1 0 0 0 0.43

Megachilidae Stelis Elongativentris Parker 5 0 15 1 1.96

Megachilidae Stelis Aff. xerophila 3 0 4 0 1.05

Megachilidae Trachusa Larreae Ckll 0 0 1 0 0.43

Total 23 64 705 21 555 43

222 J Insect Conserv (2010) 14:217–226

123

during 1995 could not be separated from female diversity

on nectarless individuals during 1994 (Fig. 2a).

Similarity coefficients showed that the nectarful condi-

tion differs markedly from the nectarless condition

(Fig. 3). Within the nectarless group, the bee fauna of both

genders had the highest similarity (low values of B) and

was also similar to the males during the 1995 flowering

season. The bee fauna between bee genders differed during

1995 (Fig. 3). Species abundance was independent of the

specific year (v2 = 0.076, P [ 0.01), which was reflected

in the similar abundances of 23 species between years,

although richness was 1994 NF [ 1995 NF [ 1995

NL [ 1994 NL (Fig. 1). There were four species that had

high relative abundance in both years, two species with

intermediate and seventeen species with low relative

abundance (Table 2). The rest of the species differed in

their abundance between years. In both years, the species

that visited nectarless individuals in the majority of the

cases corresponded to a subset of those that visited nec-

tarful individuals (Table 2) except for three species that

were only found on nectarless individuals: Lasioglossum

sp. 1, Agapostemon tyleri and Dioxys productus.

Pollen deposition

The sampled stigmas of nectarful individuals accumulated

more pollen grains (mean ± SE 14.9 ± 1.4) than those of

nectarless individuals (9.1 ± 0.9; F1, 60 = 10.9, P \ 0.01),

a trend that increased over time (F2, 60 = 2.8, P = 0.067),

suggesting that visitation is affecting the number of pollen

grains received by each nectar morph.

Discussion

In the honey mesquite, a hermaphrodite species, nectar

production positively affected bee visitation. The relatively

larger number of bee visitors on P. glandulosa var. torre-

yana could increase pollen export, as has been found for

other plant species (Zimmerman 1988; Rush et al. 1995;

Smithson and Gigord 2001) but also increases pollen grain

deposition on nectarful trees. However, even with very low

visitation, the number of pollen grains that are deposited on

nectarless stigmas is surprisingly high suggesting that

Table 4 Specific values of the scale parameter a and evenness in

nectarful and nectarless individuals during the 1994 and 1995 flow-

ering season

Scale

parameter

1994 NF 1994 NL 1995 NF 1995 NL

H0 3.99 2.56 3.74 2.89

H1 3.02 2.43 2.87 2.63

H2 2.55 2.28 2.43 2.37

H? 2.01 1.66 1.72 1.68

Evenness 0.381 0.870 0.421 0.768

NL nectarless, NF nectarful

H0 species richness S, H1 Shannon diversity index H, H2, Simpson

diversity index D-1 and H? Berger–Parker diversity index d-1

Fig. 2 Renyi diversity profiles of bees visiting for nectarful (NF) and

nectarless (NL) individuals of Prosopis glandulosa var. torreyanaduring the1994 (closed symbols) and 1995 (open symbols), according

to bee gender

Fig. 3 UPGMA using the distance matrix from Bray–Curtis similar-

ities of male and female bees visiting nectarful and nectarless

individuals of P. glandulosa during the 1994 and 1995 flowering

seasons

J Insect Conserv (2010) 14:217–226 223

123

visitation and pollen transport is carried out quite effi-

ciently by the few visitors of nectarless individuals. In

nectarful individuals pollinators benefit from the presence

of nectar and pollen in the same plant and this would

reduce foraging time but may increase competition. How-

ever, bees can also exclusively collect pollen on nectarless

individuals, maybe to avoid competition or benefit from a

relatively abundant uncollected source. Therefore, nectar

production seems to be favouring male more than female

bees. The dimorphic system of nectar production in

P. glandulosa var. torreyana may on one hand provide

resources for a wide range of visitors (nectarful morph),

and on the other, provide resources (i.e. pollen by the

nectarless morph) to a limited number of visiting species,

mainly females bees. The data suggest that the dimorphic

system is not driven by deceipt pollination mechanisms but

rather by successful pollen carryover by floral visitors.

Morphologically, the flowers of mesquite are easily

accessible to a variety of visitors seeking both nectar and

pollen (Simpson et al. 1977). Unlike other floral resources

in arid environments, mesquites usually have a predictable

flowering time as blooming is independent of rainfall

(Simpson et al. 1977). In addition, the morphology of

mesquite inflorescences and individual florets does not

preclude visitation. Mesquite is particularly rich in pollen

and nectar (Simpson et al. 1977) which makes it a readily

available and predictable resource for bees in arid envi-

ronments. Of the 396 bee species found in the xeric envi-

ronments of Chihuahua (Ayala et al. 1996), mesquite

seems to be visited by at least 10% of total bee fauna

making it a very important resource for bee species,

probably of the most visited species in North American

deserts (Simpson and Neff 1987). Mesquites are widely

distributed in the arid and semi arid environments of North

and South America and have been shown to be a widely

used resource for a large group of species (Golubov et al.

2001). Mesquites therefore offer a wide range of resources

being a key factor in xeric communities (Golubov et al.

2001) and may have a main role in maintaining the polli-

nator guild contributing to overall bee diversity by pro-

viding a high density of resources that are patchy in space

and time (Palmer et al. 2003).

One of the first comprehensive studies of insects found

on mesquite is that of Ward et al. (1977) in which the

authors compiled 28 species of bees (mainly Andrenidae)

on North American species of mesquite. A few years later,

Simpson and Neff (1987) found 64 species of solitary bees

during a single season on P. velutina, and Minckley and

coworkers have identified 83 species on P. velutina

and P. juliflora http://www.rochester.edu/College/BIO/labs/

Minckley/minckley_table.php (accessed May 07 2009).

During the two year period, we were able to identify 64

species of bees. Of the 83 identified by Minckley in

Arizona, 28 species were also found in this study of those

that could be assigned taxonomically to the species level.

Many species of Perdita and Lasioglossum could quite

possibly also be the same between these two sites, however

we lack more specific taxonomic identities. Of these,

probably the only monolectic species is Colletes prosopi-

dis, the rest are either oligoleles (or mesoleles as defined by

Cane and Sipes 2006) that visit Larrea and a small number

of other species such as Opuntia (which starts flowering

just after Prosopis at our study sites) a characteristic

common in arid environments (Waser et al. 1996) and a

few are broadly polylectic (sensu Cane and Sipes 2006)

such as the introduced A. mellifera, and other native spe-

cies, namely Osmia subfasciata, species of Ashmeadiella

and Agapostemon. Other species such as Diadasia spp. are

generally considered to be specific to the Malvaceae (e.g.

D. sphaeralcearum) but were found visiting P. glandulosa

and have been found also foraging on Cactaceae and As-

teraceae (Cane and Sipes 2006). Even though these species

are thought to be specific to other species the lack of

resources during the period when P. glandulosa offers

nectar and pollen may be causing the visitation by species

that require the energetic resources provided during the

spring dry period.

Bee guilds varied between both morphs and slightly

between years. On one hand, nectarless individuals were

only visited by the most abundant pollinators and on the

other, greater resource availability in nectarful individuals

increased visitation rates. Of all species studied, 8 genera

seem to be abundant and constant year to year visitors of

Prosopis glandulosa at Mapimı BR, while only 5 genera

(all females) were found on nectarless morphs during the

two studied years. When we consider the species accu-

mulation curves, in 1994 we clearly undersampled the

possible bee diversity found at the site. As both the 1994

and 1995 methods were the same, the lack of an adequate

model for 1994 and a reasonable model for 1995 (in which

diversity was lower) is attributed to the fact that the number

of species changes from year to year i.e. species turnover is

relatively high. It is possible that the higher bee diversity in

1994 could be a consequence of a significant amount of

rainfall (MBR climatic station) during 1993 (239.4 mm)

and a close to 40% decrease in rainfall in 1994

(138.5 mm). The data suggest that the abundance of the

main species on Prosopis flowers was constant over time

(at least during these two study periods), and Prosopis may

quite possibly depend on these main species for pollination.

However, Simpson and Neff (1987) suggest that the spe-

cialized bees may not play an important role in mesquite

pollination and the medium- to large-sized bees appear to

be the main pollinators of P. velutina, species that visit

other species as well. Detailed studies on pollinator

effectiveness could provide more insight on the role played

224 J Insect Conserv (2010) 14:217–226

123

by each species for the honey mesquite such as those made

by Keys et al. (1996). The rest of the species differed in

their abundance between years, making them unpredictable

pollinators. The presence of rare species, uneven distribu-

tions and temporal variation seems to the rule rather than

the exception in arid environments (Herrera 1988, 1995;

Minckley et al. 1999), which can potentially be attributed

to the patchiness of resources in space and time.

Deceit pollination systems are usually based on naıve

pollinators that visit flowers until they are able to dis-

criminate rewardless flowers (Cozzolino and Widmer

2005). In the case of mesquite, the dimorphic system of

nectar production may not be depending on naıve pollin-

ators as only females visitors were found on nectarless

individuals. In this case there is no deceit pollination. Other

cues may be affecting insect in such a way that visitors can

clearly differentiate nectar from nectarless individuals. It is

clear that mesquites are offering different rewards to

the bees, and other visitors, as well as cues that cause the

differences in visitation. The key to the maintenance of the

dimorphic system in natural conditions may well be med-

iated by the different rewards and the cues that regulate

insect cognition.

How important is mesquite for bee diversity?

Many conservation biologists are concerned about the

spread of invasive species (Gross 2001) and the loss of bee

species in may parts of the world (Brown and Paxton

2009). This means that we must find the resources that are

sought by bee species in order to maintain bee diversity,

and ultimately ecosystem function through mutualisms

provided by the plant pollinator interaction. Ayala et al.

(1996) estimated approximately 1,800 species of bees for

Mexico, half of which are in the Neotropics (Freitas et al.

2009). This leaves close to 900 species or close to half are

found in xeric habitats. The number of species recorded on

mesquite has been as high as 160 species (Simpson et al.

1977) which means visitors to mesquite make up a little

less than 10% of total bee diversity in Mexico, and 20% of

total bee diversity expected in xeric environments. Mes-

quite species together with Larrea (Minckley 2008) may

quite probably constitute one the most important resources

for bees in xeric environments. Even though we do not

know of the dimorphic system of nectar production is

extensive top other species of mesquite, it is clear that

mesquite and especially nectar producing mesquites are an

essential component of bee species in xeric habitats. The

widespread distribution of mesquite makes it a vital

resource for bee communities in North American Deserts

(as well as for those in South America). Management of

mesquite stands in agroforestry programmes (Fagg and

Stewart 1994) could consider the removal of nectarless

individuals which would dramatically mitigate the possible

impact on bee species.

Acknowledgments The authors thank the Herrera family at the

Mapimı BR facilities for support during field work. Rocıo Lopez

Mendoza and Luis Manuel Godınez at the Museo de Zoologıa, Fac-

ultad de Ciencias, UNAM identified bee specimens. L.E. Eguiarte and

C. Montana read previous versions of the manuscript. Access to MBR

and facilities was kindly provided by the Instituto de Ecologıa A. C.

This research was partially financed by PROMEP (2115-32637),

CONACyT (#83790 and #62390) and Fundacion UNAM fellowships

to JG.

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