Seeking the flowers for the bees: Integrating biotic interactions into niche models to assess the distribution of the exotic bee species Lithurgus huberi in South America
Introduction
The world is undergoing fast and intense environmental changes caused, directly or indirectly, by human activities (MEA, 2005, Sala, 2000). Habitat loss and fragmentation, deposition of anthropogenic fixed nitrogenous substances, and the increasing atmospheric CO2 concentration with its associated climatic changes, are considered to be worldwide drivers of environmental change (Tylianakis et al., 2008). Introduction of exotic species are also recognized as a major cause of environmental changes (Pejchar and Mooney, 2009, Tylianakis et al., 2008) and economic losses elsewhere (Pimentel et al., 2001, Pimentel et al., 2005). Therefore, practical tools to predict exotic species invasions are of the greatest importance for both science and society (Jiménez-Valverde et al., 2011, Thuiller et al., 2005), especially if we consider that human activities greatly increase species migratory abilities, allowing them to overcome their natural migratory barriers (Jiménez-Valverde et al., 2011).
The invasion of exotic species is often characterized by three stages (Richardson et al., 2000): species’ introduction, naturalization, and spread. In the first stage, the species arrive within its new ranges. In the second, some individuals from self-sustaining populations arrive and establish other populations in the new geographic range. Given the appropriate conditions, such populations will increase the species’ range, and eventually, in the third stage, they will spread, causing a new range expansion.
A wide array of environmental features may be changed after the establishment of exotic species in a new area, such as biogeochemical cycles (Ashton et al., 2005), which have inherent effects on important ecosystem processes (Bradley et al., 2010, Mangla et al., 2010, Pejchar and Mooney, 2009, Traveset and Richardson, 2006). Those changes may decrease the availability of important resources for native species (Asner et al., 2008, Iponga et al., 2008) and also affect species–specific interactions (Traveset and Richardson, 2006). Thus, cultural (e.g. tourism, aesthetic beauty), provisioning (e.g. food, fuel, water), and/or regulating ecosystem services (e.g. climate regulation, disease regulation, pollination) may be affected during the invasion process of exotic species.
In the context of pollination services, it is well known that many angiosperms rely on animal species for seed production (Herrera and Pellmyr, 2002, Traveset and Richardson, 2006). Depending on the degree of specialization, they may be generalists, which are visited by several pollinators, or extremely specialized species, which rely on a narrow suite of specific pollinators. In the latter case, the introduction of a pervasive exotic pollinator is expected to decrease the quantity and quality of pollen grains exchanged among different individuals, with subsequent fitness losses (Traveset and Richardson, 2006). Generalist invasive pollinators may easily become integrated to plant–pollinator systems in the exotic range (Traveset and Richardson, 2006) and may cause negative results for plant communities, given the establishment of fragile and loose interactions between invader pollinators and the plant species, but also for pollinator as well (Butz-Huryn, 1997, Santos et al., 2012).
When considering all factors determining either the success or failure of exotic species in new ranges, it is usually expected that the abiotic component of their ecological niche exerts a major effect on their distribution (Jiménez-Valverde et al., 2011, Soberón and Peterson, 2005, Soberón, 2007). However, while the biotic component of their niche is usually not considered in macroecological studies (Hortal et al., 2010, Pearson and Dawson, 2003), interspecific interactions with plant species are very important to pollinators, since they mainly depend on plants to survive in their environments. Therefore, the potential effects of such components, while determining the distribution of a given species, should be carefully considered whenever possible. Some attempts to contemplate interactions between pollinators and their specific host plants in macroecological scales have already been explored (Araújo and Luoto, 2007, Giannini et al., 2013a, Heikkinen et al., 2007, Meier et al., 2010, Preston et al., 2008, Rouget et al., 2001), however, as far as we know, no study has assessed the effects of the host plant species distribution on the distribution of an exotic species.
Other similar studies have already tried to include the biotic components of species niche while evaluating their distributions. Usually, biotic interactions between different species are considered by including them as predictor variables of the focus modeled species layers, corresponding to the modeled distribution of its interacting species (Giannini et al., 2013a, Heikkinen et al., 2007). Nonetheless, only the inclusion of known presence/absence data of interacting species (Araújo and Luoto, 2007, Giannini et al., 2013a), their abundances (Pellissier et al., 2010), or even land cover types (González-Salazar et al., 2013) may also be used as biotic predictor variables potentially determining the distribution of a species. Although such methods may seem simple at first, considering the broad spatial scale used in species distribution modeling, they can certainly provide us with a deeper understanding of important biological interactions occurring in local and/or regional scales, especially if we consider community ecology frameworks (Guisan and Rahbek, 2011, Meier et al., 2010, Pellissier et al., 2010). Considering the biotic portion of the species' niche, while dealing with their potential distributions, is of utmost importance, especially in a rapidly changing world (Adler and HilleRisLambers, 2008).
Herein, we constructed species distribution models to examine the potential distribution of the exotic bee species Lithurgus huberi Ducke (Apidae: Megachilinae: Lithurgini) in South America. Given the discovery of new occurrence records for this species (see below), the main goals in this study were: (1) to evaluate the capability of several species distribution modeling algorithms on predicting new occurrences using only the older ones; (2) to evaluate how the modeled distribution of its host plant species may affect the final distribution of L. huberi; and (3) to highlight unsurveyed but suitable areas for the occurrence of L. huberi in South America, with the aim of directing future studies.
Section snippets
The modeled species
L. huberi was described by Ducke (1907) from Maranhão, Brazil, and is the only representative of this Old World genus of solitary bees in the Americas. The nesting biology, cocoon, and floral associations of L. huberi have been documented by Camillo et al., 1994, Camillo et al., 1983, Mello et al. (1987), and Pick and Schlindwein (2011). The species is univoltine and, as in other members of the genus, L. huberi has a wood-nesting habit that facilitates dispersion across great distances. Nests
Results
In the first modeling experiment, TSS values for Envelope Score always showed the lowest values, independent of the species considered. The TSS values for all other modeling algorithms, for all species including L. huberi, were always higher than 0.5 (Fig. 3A), except for the modeled distributions of the host plants I. nil and I. purpurea obtained with Mahalanobis distance and GARP, which had TSS values below 0.5, under the ROC threshold. Despite a few exceptions (e.g. I. asarifolia, I.
Discussion
In this study, we attempted to integrate biotic interactions (plant–bee relationships) to our SDM procedures when predicting the potential distribution of L. huberi in its invaded range in South America. We also presented new occurrence records for L. huberi in Brazil (n = 17) and Argentina (n = 1). Of the five initial modeling algorithms, SVM and MaxEnt showed a good performance when predicting the occurrence of both, the host plant species and the bee. The inclusion of the host plant species
Conclusions
In this study we modeled the distribution of seven host plant species recorded in the literature for L. huberi and used them as a biotic variable in determining the potential distribution of this exotic pollinator in South America. We also presented new occurrence records for this species in Brazil and Argentina, some of which appear to support high population densities of L. huberi (DPS, pers. obs.). Although the modeled host plant distributions did not improve the algorithms’ ability to
Acknowledgements
DPS, VHG, ML, and LJA are grateful to Michael S. Engel, who initially introduced those authors to each other, and first evaluated the study viability. DPS and PDMJ would also like to thank CNPq – Conselho Nacional de Desenvolvimento Científico e Tecnológico (477639/2010-0), Fundação “O Boticário” de Proteção à Natureza (0880/2010-2), and Whitley Wildlife Conservation Trust for the resources which allowed them to execute field surveys in the Cerrado from the state of Goiás. Such resources
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