Forest Ecology and Management 258 (2009) 1830–1837
Contents lists available at ScienceDirect
Forest Ecology and Management
journal homepage: www.elsevier.com/locate/foreco
The complex responses of social stingless bees (Apidae: Meliponini) to tropical deforestation
Berry J. Brosi *
Department of Biology, Stanford University, 385 Serra Mall, Stanford, CA 94305, USA
ARTICLE INFO ABSTRACT
Article history: Despite concern over a putative ‘‘global pollination crisis’’, we still have an incomplete understanding of Received 26 November 2008 how bee communities respond to land-use change. I studied the responses of social stingless (or Received in revised form 22 February 2009 ‘‘meliponine’’) bees (Hymenoptera: Apidae: Meliponini) to surrounding forest cover and floral resources Accepted 25 February 2009 in 35 sites in a largely deforested landscape in Costa Rica over three years, sampling bees with a standardized netting protocol. I recorded a diverse fauna of meliponines, comprised of 20 species and Keywords: nine genera. I found that meliponine species richness and abundance are strongly related to forest cover, Pollinator but not floral resource variables (blooming plant species richness and abundance). The effect of forest on Land-use change meliponine abundance, but not diversity, disappeared when the most common meliponine species, Deforestation Bee communities Trigona fulviventris (which comprised 45% of sampled individuals), was excluded from analyses. Biodiversity Meliponine community composition, by contrast, was related most strongly to plant species richness, only weakly to forest cover, and not related to blooming plant abundance. This work differs from past work in the same landscape, which did not find evidence of changes in species richness or abundance of meliponines and forest-related variables (distance to forest or forest fragment size), but did find shifts toward meliponine-dominated communities near forests, especially larger ones. The larger true sample size (i.e. number of sample sites) of the present work likely improved the statistical power to detect these relationships. While meliponines are forest dependent, I recorded some species in the smallest forest fragments in the landscape, and as a group they respond strongly to overall forest cover in the landscape (i.e. including both small and large patches of forest). Both of these observations support arguments for preserving even small fragments of forest in agricultural landscapes. Given the ecological and economic importance of meliponine bees, it is imperative that we better understand their long-term conservation needs in the changing tropical landscapes of the world. ß 2009 Elsevier B.V. All rights reserved.
1. Introduction 1992). All meliponine bees are eusocial, with perennial hives consisting of a single queen and thousands of workers. Meliponine Despite ongoing controversy over pollinator declines and a workers recruit foragers to rich sources of floral forage, thus concomitant increase in studies on the effects of anthropogenic allowing them to efficiently pollinate tropical plants whose environmental change on pollinators (e.g. Ghazoul, 2005; Steffan- blooming period is brief, including crops such as coffee (Klein Dewenter et al., 2005), we still do not have a comprehensive view et al., 2003a; Ricketts, 2004). This efficient exploitation of floral of how bee communities respond to land use change. This problem resources, along with their high densities, means that they are also is particularly acute in the tropics, where most tropical forest trees major players in the cycling of nutrients in tropical forests (Roubik, are animal-pollinated (Bawa, 1990), where pollination limitation is 1989: p. 354). most severe (Vamosi et al., 2006) and where land-use change is the This importance carries over to the human enterprise as well, largest driver of biodiversity loss (Sala et al., 2000). since meliponines contribute to the pollination of >60 tropical The meliponine, or social stingless, bees (Apidae: Meliponini) crops. They are the primary wild pollinators of coffee (Klein et al., are a critically important group of tropical bees. They are the most 2003b); and contribute to the effective pollination of avocado, diverse group of eusocial tropical bees (Michener, 2000: p. 779), sweet pepper, tomato, cucumber, strawberry, and rambutan (Slaa and may be the most abundant clade of bees on earth (Roubik, et al., 2006); as well as coconut, mango, macadamia nuts, chayote, carambola (‘‘star fruit’’), and achiote (Heard, 1999) among many other crops. These meliponine-mediated pollination services likely * Tel.: +1 650 450 3715; fax: +1 650 723 5920. contribute billions of dollars to tropical economies ever year E-mail address: [email protected]. (Kearns et al., 1998; Ricketts et al., 2004b; Klein et al., 2007). The
0378-1127/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2009.02.025 B.J. Brosi / Forest Ecology and Management 258 (2009) 1830–1837 1831 importance of meliponines as pollinators of tropical crops is likely bees (Brosi et al., 2007, 2008). With data from both studies and to increase given the ongoing problems of honey bees, including with restrictions I imposed on sites (detailed below), I used 35 sites Africanization (Schneider et al., 2004) and parasites and disease in the Las Cruces landscape in this analysis. The results presented (e.g. Oldroyd, 2007). here are distinct from those in Brosi et al. (2007, 2008) in that While the Maya and other indigenous peoples have managed analyses combine both datasets (though only including sites that meliponine bees for millennia (Chemas and Rico-Gray, 1991), and were sampled in a minimum of two full field seasons), along with some efforts have been made to modernize techniques and several new analyses. The sites used in Brosi et al. (2007) fell along promote the husbandry of meliponines, also known as ‘‘melipo- a gradient of distance to forest and were sampled in the rainy niculture’’ (Cortopassi-Laurino et al., 2006), wild colonies account season (July-September) of 2003 and in the dry season (February- for the vast majority of crop pollination activities that are May) of 2005. The sites from Brosi et al. (2008) were along a conducted by meliponines. Thus, nearly all meliponine pollination gradient of forest fragment size, with sample sites situated in activity can be considered a true ecosystem service, rather than a pastures at the edges of the forest fragments. These sites were managed human activity. sampled in the rainy season (June-September) of 2004, and the dry Given the central place of meliponine bees in provisioning season (February–May) of 2005, with the dry season samples being tropical crop pollination services, it is critically important to taken concurrently with those from Brosi et al. (2007). Sites ranged understand how they respond to ongoing land-use changes. This from 500 m to 13 km in geographic distance from one another and is particularly true given that studies of bee communities in Central from 900 to 1300 m in elevation above sea level. America and Southeast Asia have found that meliponine bees are strongly associated with native forest habitat (Klein et al., 2002; 2.3. Bee and plant sampling Ricketts, 2004; Brosi et al., 2007; Brosi et al., 2008). On one hand, this association with forest is not surprising given that many (but not all) In each site, two field team members netted bees in a meliponines are tree-cavity nesters that may rely on tropical forests 20 m 20 m square plot for a 15-minute period, focusing their for nesting habitats (Roubik, 1989). On the other hand, many efforts on flowering plants within the plot. The netting team caught meliponine species will forage and even nest in human-dominated bees in the order that they were seen, and thus would not pursue a habitats that have experienced high degrees of deforestation (Klein relatively rare species at the expense of a common species seen et al., 2002; Ricketts, 2004; Brosi et al., 2007, 2008). first. The netting trials were focused across all bees in the bee This tendency of meliponines to forage in human-dominated community; in the analyses presented here, we include only the habitats is a positive attribute when considering crop pollination— meliponine bees from these samples. We did not net bees in and also makes for a direct linkage between forest cover and conditions of fog, precipitation, or high winds. For more on the meliponine-mediated crop pollination. For example, Ricketts et al. sampling, see Brosi et al. (2007, 2008). Specimens were pinned, (2004a) found that two patches of tropical forest near a large coffee labeled, and identified to species using Roubik (1992). V. Gonzalez farm in southern Costa Rica supported meliponine bees which and I. Hinojosa, University of Kansas, evaluated and corrected contributed approximately $60,000 a year to the value of the coffee species determinations. Specimens are housed in the Biology harvest, through increases in both the quantity and quality of Department, Stanford University. coffee beans produced. Blooming plants were counted along 5 parallel 20 m transects In order to improve understanding the responses of meliponine in each site, counting and identifying all plants in bloom within bees to land use change, I sampled meliponines over 3 years in a 50 cm of either side of the transect line. See Brosi et al. (2007, 2008) largely deforested landscape in southern Costa Rica, along for more details on plant sampling. gradients of both distance to forest and also forest fragment size. I hypothesized that meliponines would be more diverse and 2.4. Data analysis abundant in sites with more forest cover surrounding them, and in sites with greater density and diversity of floral resources. I also I analyzed two responses (dependent variables) of meliponine hypothesized that meliponine species would respond differently to communities to landscape structure and plant resource avail- land use change, and that these differences would be reflected in ability: (1) the species richness and abundance of meliponines measures of community composition. (across all species, and also species-specific abundances for those species with >20 individuals recorded); and (2) meliponine 2. Methods community composition (similarity matrices between sites). I analyzed data using the R statistical programming language (R 2.1. Study region Core Development Team, 2006); additional R packages I used are cited with the details of specific analyses. Sample size was 35 (i.e. I conducted this study in the Valle de Coto Brus, Puntarenas the number of sites), except for analyses on forest fragment size, province, southern Costa Rica, in the landscape surrounding the Las where N = 19. Cruces Biological Station (88 470 N, 828 570 W), near the town of San I assessed the effects of (1) landscape structure and (2) local floral Vito. The landscape was converted in the 1960s from mid-elevation resources on meliponine species richness, abundance, and commu- tropical forest to a mosaic of pastures, coffee fields, rural dwellings, nity composition. The primary measure of landscape structure used and subsistence plots of crops like corn, beans, and bananas. Locally in the analyses was ‘‘forest cover’’, or the proportional area of forest collected pollen records, however, show a history of forest clearing surrounding sample sites at a radius of 400 m. I used 400 m because and agriculture by indigenous people spanning several thousand earlier work showed this radial distance to have a consistently years (Clement and Horn, 2001). Remnant tracts of forest comprise strong relationship with meliponine diversity and abundance (Brosi about 15% of land cover in the region, with the largest fragment the et al., 2007, 2008). In secondary analyses, I also looked at two 230 ha tract at the Las Cruces Biological Station. additional measures of landscape structure: ‘‘distance’’, i.e. whether a site was at the edge of a forest fragment or located in open
2.2. Study sites countryside; ‘‘fragment size’’, the log10 of forest fragment area (for those sites at forest edges). Forest cover, distance to forest, and forest The sites and samples—and thus the data presented here—come fragment area were all highly correlated with one another. I used from one of the larger systematically collected datasets on tropical forest cover in multivariate analyses because it is continuous (unlike 1832 B.J. Brosi / Forest Ecology and Management 258 (2009) 1830–1837 the categorical ‘‘distance’’ measure) and is available for all sites Table 1 (unlike fragment size, which is only available for a subset). To assess Species list. Species presented in alphabetical order by genus. if fragment area or distance to forest behaved differently than forest Genus Species Abundance cover, I conducted separate univariate analyses for these variables. Melipona fasciata 24 The other major independent variable was the floral resource Nogueirapis sp 1 base in each site, specifically blooming plant abundance and Oxytrigona sp 4 species richness (per 100 m2). Because of uneven sampling in sites, Paratrigona isopterophila 1 I used a bootstrapped estimate of the mean (Efron, 1981) for both Paratrigona ornaticeps 26 Partemona orizabaienses 250 plant richness and abundance. To generate the bootstrapped Plebeia frontalis 7 means, I sampled with replacement from the set of sample dates, Plebeia jatiformis 49 repeated this 1,000 times, and took the mean estimate. Scaptotrigona c.f. pectoralis 10 To assess the effects of forest cover (proportional area of forest Scaptotrigona mexicana 42 surrounding sample sites) and flowering plant richness and Trigona sp. 1 5 Trigona sp. 2 6 abundance on meliponine diversity and abundance, I used Trigona almathea 38 multivariate mixed-effects models. I chose this class of model Trigona angustula 32 because it allows for the use of all individual samples while Trigona c.f. ferricauda 2 correcting for the temporal pseudoreplication, i.e. different Trigona corvina 118 Trigona dorsalis 7 samples from the same site are not independent from one another Trigona fulviventris 512 (Crawley, 2002: pp. 670–671). I used generalized linear models Trigona perangulata 1 (GLM) with Poisson errors in the mixed-effects model, because the Trigonisca sp 6 samples are count-based, and because variance increased with the mean for both meliponine richness and abundance (e.g. Olofsson and Shams, 2007). I conducted the mixed-effects models using the significantly spatially autocorrelated (p = 0.00031). Abundance LME4 package for R (Bates, 2008), with site as a random variable. I and richness were both significantly altitudinally autocorrelated repeated this analysis both with and without Trigona fulviventris, (abundance: p = 0.0031; richness: p = 0.0011). Community simi- the most abundant species in the samples. larity, however, showed no significant relationship with either To assess species-specific responses, I also separately ran geographic distance (p = 0.22) or altitudinal differences between multivariate mixed-effects models with the abundance of each of sites (p = 0.52), as assessed with Mantel tests. In subsequent the nine most common species (those with >20 individuals) as analyses, I assumed sites were independent. response variables. I also conducted univariate tests on the effects of distance to forest and forest fragment size on meliponine species 3.3. Meliponine diversity and abundance richness and abundance with mixed-effects models, again with site as a random variable. Multivariate mixed-effects models showed that both melipo- To evaluate the impact of forest characteristics (isolation, size, nine abundance and species richness are strongly related to forest and cover) and floral resources on meliponine community cover, but not to the abundance or richness of plants in bloom composition, I calculated pairwise meliponine community simi- (Table 2; Fig. 2). When I re-analyzed these models without larity between sites using the Morisita-Horn similarity index. including Trigona fulviventris, the most common species, these Because of the very uneven number of samples between sites, I results changed somewhat. Meliponine abundance was no longer calculated the similarity index as the average of 50 replicates of a significantly related to forest cover, though it remained unrelated bootstrapped collection of 11 sample dates (the minimum number to blooming plant richness or abundance. In contrast, meliponine of times each site was sampled), sampling with replacement. I used richness was still related to forest cover, though more weakly, and multivariate matrix permutation tests, with the ADONIS function showed marginal relationships with both plant richness and plant in the VEGAN package for R (Oksanen et al., 2006) to test the abundance (Table 3; Fig. 3). Thus, T. fulviventris appears to be a relationship between community similarity and forest cover and floral resources. To assess spatial and altitudinal autocorrelation between sites, I used Moran’s I for meliponine abundance and diversity, and Mantel tests for pair-wise community similarity, using the aforementioned bootstrapped Morisita-Horn similarity matrix.
3. Results
3.1. Overview
I sampled 1141 meliponine individuals representing 9 genera and 20 species (species list, Table 1). The rank abundance profile of the meliponine community in the Las Cruces landscape is highly uneven. One species, Trigona fulviventris, accounted for 45% of all sampled individuals; the next-most common species, Partamona orizabaensis, represented 22% of all individuals (rank abundance curve, Fig. 1).
3.2. Spatial and altitudinal autocorrelation
Meliponine abundance was not spatially autocorrelated as assessed by Moran’s I (p = 0.13), but meliponine richness was Fig. 1. Rank abundances of meliponine species. B.J. Brosi / Forest Ecology and Management 258 (2009) 1830–1837 1833
Table 2 Mixed-effects model results for meliponine abundance and species richness.
Abundance Species richness
Estimate Std. error z value p value Estimate Std. error z value p value
(Intercept) 0.272 0.411 0.662 0.508 0.498 0.230 2.168 0.030* Forest cover 1.791 0.674 2.658 0.008** 1.091 0.355 3.071 0.002** Plant abund 0.000 0.001 0.394 0.693 0.001 0.001 1.118 0.264 Plant spp. rich 0.036 0.038 0.972 0.331 0.020 0.021 0.965 0.335
Significance levels are: .p < 0.1; *p < 0.05; **p < 0.01; ***p < 0.001.
Fig. 2. Relationships between forest cover, floral resources, and meliponine species richness and abundance. These graphs are not constructed from the multivariate mixed- effects models, but rather show site-based averages with linear regression fit lines to show basic relationships. Solid regression lines depict significant relationships in the mixed-effects models, with dashed lines for non-significant relationships. driver of the results, particularly with regard to meliponine in the species-specific analyses. At this level, I found only three abundance and forest cover. significant associations between landscape or flowering-plant Separate univariate analyses showed strong positive relation- variables and species-specific abundances of meliponines. Two ships with meliponine richness and abundance and both distance species showed positive relationships with forest cover (T. to forest (abundance: z = 3.26, p = 0.0011; richness: z = 3.31, fulviventris z = 3.55, p = 0.00039; Plebeia jatiformis z = 8.40, p = 0.00094) and forest fragment size (abundance: z = 2.40, p = 8.69 10 15). The abundance of Paratrigona orniticeps was p = 0.016; richness: z = 3.13, p = 0.0017). positively related to plant species richness (z = 3.65, p = 0.00027).
3.4. Species-specific abundance 3.5. Community composition
Because I separately analyzed the abundances of nine species, I The results of the multivariate matrix permutation tests were used a Bonferroni-corrected significance cut-off p-value of 0.0005 highly dependent on variable order, so I re-ran them for all possible
Table 3 Mixed-effects model results for meliponine abundance and species richness, excluding Trigona fulviventris.
Abundance Species richness
Estimate Std. error z value p value Estimate Std. error z value p value
(Intercept) 1.044 0.472 2.214 0.027* 1.185 0.305 3.886 0.000*** Forest cover 1.146 0.769 1.491 0.136 0.975 0.473 2.061 0.039* Plant abund 0.001 0.001 0.835 0.404 0.002 0.001 1.796 0.072. Plant spp. rich 0.073 0.043 1.694 0.090. 0.050 0.028 1.773 0.076.
Significance levels are: *p < 0.05; ***p < 0.001. 1834 B.J. Brosi / Forest Ecology and Management 258 (2009) 1830–1837
Fig. 3. Relationships between forest cover, floral resources, and meliponine species richness and abundance, excluding Trigona fulviventris. These graphs are not constructed from the multivariate mixed-effects models, but rather show site-based averages, excluding Trigona fulviventris (the most common species in the samples) using linear regression fit lines to show basic relationships. Solid regression lines depict significant relationships in the mixed-effects models, with dashed lines for non-significant relationships. order combinations (15 combinations total for all three-way, all cover. I also found species-specific responses: abundance of T. two-way, and all one-way combinations). This order specification fulviventris and Plebeia jatiformis was significantly positively dependency could be due in part to correlations between variables. related to forest cover, while abundance of Paratrigona orniticeps Forest cover and plant variables were not significantly correlated was positively related to plant species richness. None of the six with one another, though plant abundance and species richness other species analyzed showed any relationship with forest cover were significantly correlated. Plant species richness had a or plant resources. Meliponine community composition was most consistently significant relationship with meliponine community strongly related to plant species richness, weakly related to forest composition, in all but two of the 11 trials (univariate: F = 3.18, cover, and not related to plant abundance. p 0.001). Forest cover was significant in the univariate test, in two of four bivariate tests, and in two of the six trivariate tests 4.2. Meliponine species richness and abundance (univariate: F = 1.72, p < 0.001). Thus, forest is likely playing some role in the relationship, but not as strongly or consistently as plant The results related to species richness and abundance are richness. Plant abundance, on the other hand, was not significant in largely consistent with the few landscape-scale studies that have univariate tests or any bivariate tests, and was only significant in considered meliponine bees. Brown and Albrecht (2001), working one of the six trivariate tests. Therefore, plant abundance overall in Brazil, found a strong relationship between the species richness does not seem to be an important factor in shaping meliponine of bees in the genus Melipona and forest cover, and further showed community composition (univariate: F = 0.48, p = 0.8). Univariate species-specific responses in that two Melipona species were not tests showed no relationship between meliponine community associated with the degree of forest cover, while another two similarity and forest fragment size (F = 0.76, p = 0.6) or distance species showed a very strong association with forest. In Indonesia, category (F = 0.87, p = 0.4). Klein et al. (2002) demonstrated a negative relationship between land-use intensity and the diversity and abundance of social bees, 4. Discussion which there included meliponines as well as two species Apis.In southern Costa Rica, about 100 km NW of my study region, Ricketts 4.1. Overview (2004) showed significantly greater visitation to coffee flowers by meliponine bees, as well as enhanced bee species richness, near Meliponine species richness and abundance are strongly and two large forest fragments, but not near a thin riparian strip of positively related to the proportion of forest surrounding sample trees. Finally, earlier work in the same landscape did not directly sites, but are not correlated with blooming plant density or plant show effects of distance to forest (Brosi et al., 2007) or forest species richness. Much of the effect of meliponine abundance (but fragment size (Brosi et al., 2008) on meliponine species richness not species richness) is driven by the most common species, and abundance. Both studies, however, did show a positive Trigona fulviventris. In analyses that omitted this species, relationship between forest size and proximity and the proportion abundance was no longer significantly related to forest cover, of the total bee community represented by meliponines. Compar- but species richness remained significantly correlated with forest ing the results presented here with those from Brosi et al. (2007, B.J. Brosi / Forest Ecology and Management 258 (2009) 1830–1837 1835
2008), it is likely that in the present work, the larger true sample show any significant effects, as was expected given the correlation size (increased number of sites), as well as the larger number of of those values with forest cover. Thus, there is only very weak samples considered within some individual sites, contributed to evidence to support my hypothesis that meliponine species would greater statistical power to detect trends within the meliponine be grouped into sets of species that are more or less resilient to community. deforestation. I did not find a relationship between meliponine species The result that meliponine community composition is driven richness and abundance and the availability of floral resources primarily by blooming plant diversity is somewhat surprising, within a site. While all meliponines in this region are dependent on given the complex relationship between bee and plant commu- nectar and pollen for essentially 100% of their dietary require- nities discussed previously. One potential mechanism that could ments, the relationship between the species richness and cause plant richness to structure bee communities is the abundance of plants and bees is not straightforward, for several interference competition and dominance hierarchy that melipo- reasons. One factor is that different plant species have distinct nines display, which is thought to contribute to resource pollen and nectar rewards, both in terms of quantity and quality, as partitioning (e.g. Hubbell and Johnson, 1978). Such a mechanism well as access to those rewards, through both morphological (floral may lead, for example, to an increased likelihood of some structure) and chemical (nectar and pollen chemistry) means (e.g. ‘‘submissive’’ bee species appearing in species-rich plant commu- Chittka et al., 1999). It was beyond the scope of this study to nities, where they can exploit floral resources that are not being quantify these rewards, and thus by necessity I used somewhat used by more dominant species. coarse measures of the availability of floral resources. Second, Potts et al. (2004) showed that nectar resource diversity, which meliponines and many other pollinators, by virtue of their ability is strongly related to plant species richness, is a major factor to fly, have large areas over which they can forage, and quantifying structuring pollinator community composition. They also found a the floral resource base over the entire study area, let alone over a significant relationship, however, between nectar resource diver- larger area in each study site, was beyond the scope of the study. sity and bee diversity. Perhaps quantifying the species-specific Finally, there can be lag effects in the responses of bee floral rewards in the flowering plant community would strengthen communities to changes in floral resources. Due to the time the association between plants and bees, both in terms of diversity constraints of provisioning larval cells, larval and pupal develop- and abundance and also in terms of community composition. ment, and (in some species) periods of dormancy, bee abundance can take several weeks to a year to respond to increases in the floral 4.4. Meliponine foraging behavior and land use change resource base (e.g. Tepedino and Stanton, 1981). Meliponines as a group are associated with the quantity of Meliponine foraging strategies are extremely diverse and are a forest cover, as evidenced by both the results presented here as major driver of the distribution of workers of a given species on the well as those reported by others, from a range of disparate and landscape. In the context of this study, this is a particularly distant locations (Brazil, Brown and Albrecht, 2001; Indonesia, important point because some the strategy of some meliponine Klein et al., 2003a,b; and Costa Rica, Ricketts, 2004; Brosi et al., species is geared toward the efficient exploitation of ‘‘bonanza’’- 2007, 2008). This pattern is likely driven by two primary life- type resources, by having a few scouts locate resources, followed history requirements: nesting and feeding needs. While melipo- by massive recruitment. Foraging workers of such species are not nines have diverse nesting habits and substrates, many species distributed evenly across the landscape, which means that my prefer to nest in tree cavities, as is befitting of their evolution in sampling strategy would not have detected such species propor- tropical forest habitats (Roubik, 1989). In addition, while many tionally to their abundance. By contrast, other meliponine species meliponine species will forage both within tropical forests and also forage in a primarily or exclusively solitary manner, and others are in deforested areas, some of the rich floral resources within forests facultative recruiters, which forage in a solitary mode but will (such as mass-blooming tropical trees) likely help support sometimes recruit nestmates to high-density floral resources (e.g. meliponine species richness and abundance. Measuring floral Hubbell and Johnson, 1978; Roubik et al., 1986; Slaa et al., 2003). resources within tropical forests is logistically daunting and was Foraging strategy, however, is closely tied to the distribution of beyond the scope of this study. flowering plant resources (Johnson and Hubbell, 1975), which is in Another factor that could have contributed to the association turn strongly associated with land cover. Forested and deforested between meliponines and forest is human exploitation and habitats contrast strongly in the spatiotemporal distributions of destruction of stingless bee nests. In many parts of the tropics, flowering plant resources in many places in the tropics. In including southern Costa Rica, stingless bee honey is valued for its particular, tropical forest trees often bloom in intense, short medicinal properties and carries a high price (Souza et al., 2006); bursts, leading to an extremely patchy distribution of floral nests are often destroyed in the process of harvesting this honey. resources in both space and time (Bawa, 1990). By contrast, many Additionally, meliponine nest defense mechanisms (hair pulling; deforested habitats, such as the rustic pastures I sampled flying in the eyes, ears, and mouth; etc.) can present a nuisance to meliponines in, have low densities of flowering herbs and shrubs, people (Roubik, 1989: p. 196), and nests near human habitation are many of which are in bloom for much of the year (Brosi et al., 2007, often purposefully destroyed for this reason. 2008). Thus, it is likely that meliponine species that employ a solitary 4.3. Community composition or facultative-recruiting foraging style will fare better in defor- ested habitats, and forage more in those habitats, than will species The community composition of meliponines was consistently that use intensive forager recruitment. For example, Trigona related only to the species richness of blooming plants in the fulviventris, by far the most commonly sampled bee in this study, is sampled pastures, and consistently not related to plant abundance. a facultative recruiter that conducts a great deal of solitary foraging There was a more complex response of forest cover, which showed (Johnson and Hubbell, 1975; Hubbell and Johnson, 1978; Slaa et al., inconsistent evidence of being an important factor in shaping 2003). While T. fulviventris can apparently efficiently utilize the meliponine communities. In about half of the combinations of low-density floral resources of the deforested habitats in the study variable order, it was significant, whereas it was not in the other region, its distribution is also strongly linked to forest habitat. Its half. Univariate tests on the effects of forest fragment size and need for relatively large tree cavities for nesting sites (Hubbell and proximity to forest on meliponine community composition did not Johnson, 1977) likely drives this pattern. 1836 B.J. Brosi / Forest Ecology and Management 258 (2009) 1830–1837
Considering foraging patterns in meliponines, the sampling of land use change on different species of meliponines. For strategy that I used is appropriate for the deforested habitats I example, do mass-recruiting meliponines fare worse in deforested sampled in due to their relatively consistent, low-density floral habitats? Will crop fields near very large tracts of tropical forest resources. At the same time, this sampling strategy would not receive higher levels of crop pollination services, due to a greater serve well for understanding the meliponine community in abundance of meliponine species that exhibit mass-recruitment? tropical forest habitats with a much patchier distribution of floral In addition to questions on meliponine species traits, we also resources; such a goal was beyond the scope of this study. know little about the particular attributes of tropical forest that Foraging strategy is also a very important aspect of meliponine support their foraging and nesting. In particular, there is little biology in the context of crop pollination services. Crops with information on how meliponines respond to re-growth forest, or mass-blooming phenology, particularly those with a short flower- how to design ecological restoration programs to support ing duration, should theoretically be particularly well pollinated by meliponine bees and the crop pollination services they provide. meliponines with strong recruitment behavior. Coffee (Coffea arabica L.), a cornerstone of tropical export agriculture, fits this 5. Conclusion exact profile with a typical blooming period of three days (e.g. Drinnan and Menzel, 1995). In a study of coffee pollination near Meliponine bees are important both ecologically and economic- San Isidro del General, Costa Rica (about 100 km north-northwest ally, and more work is needed to both understand their complex of my study site), Ricketts (2004) found that ten species of responses to habitat change, and to conserve their populations, meliponines, along with feral honey bees (Apis mellifera) were the over the long term. Given the increasing concern over the status of most common visitors to coffee flowers. While foraging-strategy pollinators worldwide, conserving this critically important group data are not available for all species, of the four most common of bees in the most biodiverse habitats on Earth should be meliponines in the Ricketts (2004) study, one is a solitary forager prioritized. (Plebeia frontalis, the second-most common floral visitor) and another is a facultative group forager (T. fulviventris, the fourth Acknowledgements most common floral visitor). Thus, while foraging recruitment can play a role in meliponine-mediated crop pollination services, it is I thank the many Costa Rican families who allowed me to work not the only factor in determining the density of flower visitors. It on their land. G. Daily contributed crucial support, advice, and is possible that land-use change, and the concomitant change in funding at all stages of this work. V. Gonzalez and I. Hinojosa, the distribution of floral resources, reduced the abundance of University of Kansas, confirmed my species determinations. L. mass-recruiting meliponines in the San Isidro landscape. Billadello, E. Brosi, J. DeNoyer, K. Frangioso, B. Graham, J. Ilama, F. Oviedo, and T. Shih provided superb field assistance. The staff of 4.5. Management recommendations the Las Cruces Biological Station and the Organization for Tropical Studies (especially R. Quiro´ s, E. Ramirez, and Z. Zahawi) provided Based on my results and those of others, several recommenda- cheerful field research support. G. Dura´n of Las Cruces provided tions for landscape management to support meliponine bees and key spatial data. J. Ranganathan provided GIS advice, data, and their crop pollination services can be made: assistance. I am grateful for funding from the Anne M. and Robert T. Bass Stanford Graduate Fellowship in Science and Engineering, a Preserve even small patches of forest near pollination-dependent Teresa Heinz Scholarship for Environmental Research, and the crops to support meliponine nesting. I recorded meliponines in Moore Family Foundation; the Stanford University Field Studies fragments as small as 0.25 ha. and Human Biology Research Experiences for Undergraduates (HB- Consider conserving forest even when not adjacent to pollina- REX) Programs; and grants to the Center for Conservation Biology tion-dependent crops, for their option value if land use were to at Stanford University from the Koret, McDonnell, Sherwood, and change. This is particularly important given ongoing problems Winslow Foundations and Peter and Helen Bing. with honey bee declines. Work to re-connect isolated forest patches. While I did not find References an effect of forest isolation on meliponine communities, the maximum isolation distance between forest fragments in this Bates, D. 2008. LME4: linear mixed-effects models using S4 classes.
Drinnan, J.E., Menzel, C.M., 1995. Temperature affects vegetative growth and Ricketts, T., Daily, G., Ehrlich, P., Michener, C., 2004a. Economic value of tropical flowering of coffee (Coffea-arabica L.). J. Horticult. Sci. 70, 25–34. forest to coffee production. Proc. Natl. Acad. Sci. U.S.A. 101, 12579–12582. Efron, B., 1981. Nonparametric estimates of standard error—the jackknife, the Ricketts, T.H., Daily, G.C., Ehrlich, P.R., Michener, C.D., 2004b. Economic value of bootstrap and other methods. Biometrika 68, 589–599. tropical forest to coffee production. Proc. Natl. Acad. Sci. U.S.A. 101, 12579– Ghazoul, J., 2005. Buzziness as usual? Questioning the global pollination crisis. 12582. Trends Ecol. Evol. 20, 367–373. Roubik, D.W., 1989. Ecology and Natural History of Tropical Bees. Cambridge Gross, M., 2008. Pesticides linked to bee deaths. Curr. Biol. 18, R684. University Press, Cambridge, New York. Heard, T.A., 1999. The role of stingless bees in crop pollination. Ann. Rev. Entomol. Roubik, D.W., 1992. Stingless bees. A guide to Panamanian and Mesoamerican species 44, 183–206. and their nests (Hymenoptera:Apidae:Meliponinae. In: Quintero, D., Aiello, A. Hubbell, S.P., Johnson, L.K., 1977. Competition and nest spacing in a tropical (Eds.), Insects of Panama and Mesoamerica—Selected Studies. Oxford University stingless bee community. Ecology 58, 949–963. Press, Oxford, UK, pp. 495–524. Hubbell, S.P., Johnson, L.K., 1978. Comparative foraging behavior of 6 stingless bee Roubik, D.W., Moreno, J.E., Vergara, C., Wittmann, D., 1986. Sporadic food competi- species exploiting a standardized resource. Ecology 59, 1123–1136. tion with the African honey bee: projected impact on Neotropical social bees. J. Johnson, L.K., Hubbell, S.P., 1975. Contrasting foraging strategies and coexistence of Trop. Ecol. 2, 97–111. 2 bee species on a single resource. Ecology 56, 1398–1406. Sala, O.E., Chapin, F.S., Armesto, J.J., Berlow, E., Bloomfield, J., Dirzo, R., Huber- Kearns, C.A., Inouye, D.W., Waser, N.M., 1998. Endangered mutualisms: the con- Sanwald, E., Huenneke, L.F., Jackson, R.B., Kinzig, A., Leemans, R., Lodge, D.M., servation of plant–pollinator interactions. Ann. Rev. Ecol. Systemat. 29, 83–112. Mooney, H.A., Oesterheld, M., Poff, N.L., Sykes, M.T., Walker, B.H., Walker, M., Klein, A., Steffan-Dewenter, I., Buchori, D., Tscharntke, T., 2002. Effects of land-use Wall, D.H., 2000. Biodiversity—global biodiversity scenarios for the year 2100. intensity in tropical agroforestry systems on coffee flower-visiting and trap- Science 287, 1770–1774. nesting bees and wasps. Conserv. Biol. 16, 1003–1014. Schneider, S.S., Hoffman, G.D., Smith, D.R., 2004. The African honey bee: factors Klein, A., Steffan-Dewenter, I., Tscharntke, T., 2003a. Bee pollination and fruit set of contributing to a successful biological invasion. Annu. Rev. Entomol. 49, 351– Coffea arabica and C-canephora (Rubiaceae). Am. J. Bot. 90, 153–157. 376. Klein, A., Steffan-Dewenter, I., Tscharntke, T., 2003b. Fruit set of highland coffee Slaa, E.J., Wassenberg, J., Biesmeijer, J.C., 2003. The use of field-based social increases with the diversity of pollinating bees. Proc. R. Soc. Lond. Ser. B: Biol. information in eusocial foragers: local enhancement among nestmates and Sci. 270, 955–961. heterospecifics in stingless bees. Ecol. Entomol. 28, 369–379. Klein, A.M., Vaissiere, B.E., Cane, J.H., Steffan-Dewenter, I., Cunningham, S.A., Kre- Slaa, E.J., Sanchez Chaves, L.A., Malagodi-Braga, K.S., Hofstede, F.E., 2006. Stingless men, C., Tscharntke, T., 2007. Importance of pollinators in changing landscapes bees in applied pollination: practice and perspectives. Apidologie 37, 293– for world crops. Proc. R. Soc. Biol. Sci. Ser. B 274, 303–313. 315. Michener, C.D., 2000. The bees of the world. Johns Hopkins University Press, Souza, B., Roubik, D., Barth, O., Heard, T., Enriquez, E., Carvalho, C., Villas-Boas, J., Baltimore, Md. Marchini, L., Locatelli, J., Persano-Oddo, L., Almeida-Muradian, L., Bogdanov, S., Oksanen, J., Kindt, R., Legendre, P., O’Hara, R., 2006. Vegan: Community Ecology Vit, P., 2006. Composition of stingless bee honey: setting quality standards. Package. http://cc.oulu.fi/ jarioksa/, p. Ordination methods and other useful Interciencia 31, 867–875. functions for community and vegetation ecologists. Steffan-Dewenter, I., Potts, S.G., Packer, L., 2005. Pollinator diversity and crop Oldroyd, B.P., 2007. What’s killing American honey bees? PLoS Biol. 5, 1195–1199. pollination services are at risk. Trends Ecol. Evol. 20, 651–652. Olofsson, J., Shams, H., 2007. Determinants of plant species richness in an alpine R Development Core Team, R.D.C., 2006. R: a language and environment for meadow. J. Ecol. 95, 916–925. statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Potts, S.G., Vulliamy, B., Roberts, S., O’Toole, C., Dafni, A., Ne’eman, G., Willmer, P.G., Tepedino, V.J., Stanton, N.L., 1981. Diversity and competition in bee-plant commu- 2004. Nectar resource diversity organises flower–visitor community structure. nities on short-grass prairie. Oikos 36, 35–44. Entomol. Exp. Appl. 113, 103–107. Vamosi, J.C., Knight, T.M., Steets, J.A., Mazer, S.J., Burd, M., Ashman, T.L., 2006. Ricketts, T.H., 2004. Tropical forest fragments enhance pollinator activity in nearby Pollination decays in biodiversity hotspots. Proc. Natl. Acad. Sci. U.S.A. 103, coffee crops. Conserv. Biol. 18, 1262–1271. 956–961.