Accounting for abundance makes multivariate dispersion less sensitive to rare species, which often make up a large fraction of the total species richness in bee assemblages but may contribute little to the pollination services rendered to plants . For these reasons, multivariate dispersion is superior to the traditional approach of using multiplicative or additive partitioning for investigating bee temporal beta diversity with respect to characterizing individual-level bee assemblage composition, as well as temporal turnovers in ecosystem function. To calculate multivariate dispersion, we performed a non-metric multidimensional scaling ordination based on a dissimilarity matrix of abundance-weighted bee assemblages in all possible pairs of samples across all plots . From this ordination, we calculated the multidimensional centroid of the samples from each plot, and then computed the mean distance between each plot’s centroid and its constituent samples. The resulting dispersion score for each plot thus measures the degree to which the species composition of each plot’s bee assemblage turns over through time. Dispersion scores of reserve and fragment plots were then compared using Welch’s two sample t-tests. As with our analyses of temporal gamma and alpha diversity, we repeated all analyses with the temporal beta diversity of native plants as an added independent variable . Models that included plant temporal beta diversity yielded poorer AICc scores in all cases; thus, we did not include plant temporal beta diversity in our final models.Across our two years of sampling, we found consistent differences in bee assemblages occurring in reserves and fragments, despite the known tendency for bee faunas to exhibit considerable inter-annual variation at a given locality . Compared to reserves, big plastic pots fragments harbored bee assemblages that were less diverse with respect to all three components of temporal diversity .
While all metrics of bee diversity and abundance varied with time, differences in bee diversity between reserves and fragments were remarkably constant through time . Individually scrutinizing the three components of temporal diversity allowed for a high resolution characterization of the temporal structure of bee assemblages in intact and fragmented habitats; these analyses also yielded further insights into the potential consequences of bee diversity loss for ecosystem function in fragmented habitats in our system. Reduced species richness is one of the most commonly reported effects of habitat fragmentation on bee assemblages . Though our reserve and fragment plots did not differ systematically with respect to the composition of floral resources , it is possible that decreased availability of nest sites within foraging distance of key host plants or increased vulnerability to demographic stochasticity due to isolation or small population size may have contributed to reduced bee species richness in fragments. Analyses of the temporal gamma and temporal alpha components of bee species richness yielded qualitatively similar results; however, the impact on each of the two temporal diversity components may have distinct implications for the conservation of bees andecosystem function. The temporal gamma component of bee richness provides information on the habitat conditions and locations that support the greatest total number of bee species or species of particular conservation concern; as such, it is the most useful metric for developing conservation strategies aimed at bees. On the other hand, the pollination effectiveness of a particular bee species for a particular plant species may depend upon the timing during which the interaction between bees and plants takes place or upon the bee species’ functional complementarity with other, temporally co-occurring pollinator species .
Detecting potential impacts of climate change on the phenological matching between bee species and the plants they pollinate also requires examining the composition of bee assemblages at discrete points in time. Thus, in the face of a changing climate, effective strategies aimed at conserving bees and the ecosystem function they perform should account for both the temporal alpha and gamma components of bee richness. As with patterns of bee species richness, patterns in the temporal gamma and alpha components of bee assemblage evenness are in qualitative agreement with each other. Assemblage evenness is an important driver of ecosystem function , including pollination , but remains an under-appreciated aspect of pollinator assemblage dynamics . Reductions in the temporal alpha component of bee assemblage evenness in fragments may result in decreased frequencies of interspecific encounters among bee species; such encounters have been shown to enhance pollination efficiency via altering bee foraging behavior . On the other hand, reductions in the temporal gamma component of bee assemblage evenness may result in a stronger reliance by plant assemblages on a small subset of numerically dominant bee species, and consequently, reduced stability of pollination services . In contrast to patterns of bee species richness and assemblage evenness, overall bee abundance did not differ between reserves and fragments. This pattern was caused by reserves having higher bee abundance in spring and fragments having higher bee abundance in summer . This treatment-by-sample interaction appears to be driven by the higher relative abundance of generalist bees in fragments ; many generalist species in our system reach peak abundance between late June and August. Generalist bees may be more tolerant of habitat fragmentation compared to specialists and have been hypothesized to replace the ecosystem function formerly performed by extirpated specialists .
However, even though generalists in our study numerically compensated for absent specialists when considering the temporal gamma component of bee abundance , reduced bee abundance in fragments early in our study period may threaten the pollination of spring blooming plant species. Temporal beta diversity represents another under-appreciated metric in ecology , and reports on the effects of anthropogenic disturbance on intra annual turnover of biological assemblages remain rare . In our system, decreased temporal beta diversity in fragments may explain how modest reductions in the temporal alpha component of species richness and assemblage evenness in fragments translate into more pronounced reductions in the temporal gamma component . More broadly, decreasing seasonal turnover in an assemblage may result in increasing temporal niche overlap among its constituent species , which may in turn decrease the number of distinct temporal niches created by the assemblage. Decreases in the seasonal turnover of bee assemblages may be especially consequential in cases where bee species tend to interact with a set of preferred host plants throughout their activity season even when new plant species begin to bloom as time progresses . If temporal host-switching is likewise rare in our system, reduced bee assemblage turnover in fragments may jeopardize the reproduction of certain plant species that occupy specific temporal niches with respect to pollination . Examining the temporal beta diversity of bee assemblages thus appears crucial for understanding mechanisms underlying the impact of anthropogenic disturbance on pollination services. Novel selection forces in altered habitats often create ecological filters —environmental or biotic processes that determine which species can establish or persist. The strength of ecological filters depends on the form of disturbance, the natural history of organisms in question, and the strength of other forces shaping community assembly such as dispersal, competition, and natural disturbance regimes . Understanding the extent to which ecological filters shape community assembly represents a central goal of community ecology , and can be used to predict the long-term implications of habitat modifications . Assessing the strength of ecological filters is especially important when evaluating the long-term ecological consequences of habitat fragmentation, one of the leading causes of ecosystem change and biodiversity loss worldwide . Many studies have found strong evidence that ecological filtering drives diversity loss in habitat fragments, both at the local scale and landscape scale . On the other hand, community assembly in fragmented landscapes may also be shaped by stochastic colonization and extinction events typical of island biogeography , or by underlying heterogeneity among habitat patches . While habitat fragmentation could reduce local species richness through different combinations of the above mentioned processes, effective conservation practices will need to account for the degree to which ecological filtering drives species loss . One powerful approach to assess the strength of ecological filters in fragmented habitats is to examine functional diversity, since ecological filters, by definition, black plant pots plastic act on functional traits rather than species . Functional diversity is related to taxonomic diversity in complex ways , and the relationship between the two metrics can provide insight into the mechanisms that drive biodiversity loss in fragmented habitats. For instance, when habitat fragmentation results in strong ecological filtering, functional diversity may decline even if species richness and abundance remains little altered, as may be the case when taxa that thrive in fragmented habitats replace those that are extirpated .
On the other hand, if species loss in habitat fragments mainly results from stochastic extinction events associated with small population size and isolation, functional diversity may be relatively unaffected by the loss of taxonomic diversity, especially in systems with sufficient functional redundancy among species .Here, we evaluate the contribution of ecological filters to diversity loss by taking advantage of an extensive survey of native bees in a species rich ecosystem where we have documented profound reductions in bee species richness associated with urbanization-induced habitat fragmentation . Bees are ecologically important pollinators known to exhibit non-random species loss in fragmented habitats, where specialist species appear particularly vulnerable . Ecological filtering of bees may occur in habitat fragments when fragments experience reductions in the diversity or abundance of plant species that serve as food resource for bees, exhibit altered abiotic conditions due to influences from the surrounding matrix , or fail to contain the correct spatiotemporal configuration of food and nesting resources . Habitat fragmentation may also reduce bee diversity via processes not related to ecological filtering; for instance, when the isolation of habitats disrupts dispersal processes crucial in buffering bee populations from year-to-year variation in the local and temporal distribution of floral resources . We assess the strength of ecological filters by addressing four questions. First, to what extent does fragmentation impact bee functional diversity? Loss of functional diversity more severe than that predicted by a null model of random species loss would lend support for the importance of ecological filters . Second, do bee assemblages in fragments exhibit distinct taxonomic or functional compositions compared to those in reserves, as would be expected when ecological filtering causes the assembly of novel communities ? Third, do bee assemblages in fragments exhibit lower taxonomic or functional beta diversity among plots, as would be expected when ecological filters select for or remove common sets of functional traits in altered habitats ? Lastly, are bee assemblages in fragments composed of taxa with larger range sizes relative to those in reserves? Given that range size tends to be positively related to niche breadth , a shift to more cosmopolitan species in fragments is expected if ecological filtering precludes the persistence or colonization of species more specialized to the local ecosystem . Answering these questions will yield insights into the mechanisms that drive bee species loss in our study system as well as provide information on the potential conservation value of scrub habitat fragments .Study system: Field data were collected between April and August of 2011 and 2012 in coastal sage scrub habitat in San Diego County, California, USA, and are detailed in Chapter 1 of this dissertation. We surveyed one-hectare study plots belonging to two categories: large natural reserves , and habitat fragments surrounded by urban development. This is the same system of reserves and fragments previously used to study the ecological effects of urbanization-induced habitat fragmentation . In 2011, we surveyed eight study plots ca. every 2-4 weeks; in 2012, we surveyed 17 study plots ca. every 3-5 weeks. During each survey at each study plot, the first author deployed 30 bowl traps between ca. 0900 h and 1500 h, and collected free-flying wild bees via aerial netting . Concurrently, we also documented the identities of native, insect-pollinated plant species in bloom at each study plot by walking through pre-planned paths that allowed an observer to visually survey the entire study plot . All collected bees were individually mounted and identified to species or morphospecies within genus, hereafter referred to collectively as “species” . This sampling effort resulted in a dataset of 11,037 native bees belonging to 216 species in 52 genera and 6 families, after the exclusion of bee specimens not identifiable beyond genus .