Species Diversity and Habitat Fragmentation Per Se: The Influence of Local Extinctions and Species Clustering.

AbstractAnthropogenic fragmentation of habitat is considered to be a critical factor contributing to the decline of species. However, a general consensus on the degree to which habitat loss and what has been called "habitat fragmentation per se" contribute to the loss of species diversity has not yet emerged. For empirical and theoretical reasons the topic has recently attracted renewed attention, thus reviving the "single large or several small" (SLOSS) debate. To study the effect of fragmentation per se, we use a spatially explicit and continuous, competitively neutral simulation model with immigration from a regional pool. The model accounts for the influence of ecological drift and intrafragment species clustering (due to limited dispersal) on local (plot) and global (landscape) diversity. We find that fragmentation increases global diversity but decreases local diversity, prominently so if fragments become more isolated. Cluster formation is a key mechanism reducing local diversity. By adding external disturbance events that lead to the occasional extinction of entire communities in habitat fragments, we show that the combined effect of such extinctions and cluster formation can create nonlinear interactive effects of fragmentation and fragment isolation on diversity patterns. We conclude that while in most cases fragmentation will decrease local and increase landscape diversity, universal predictions concerning the SLOSS debate should be taken with care.

Explaining the variability in the response of annual eusocial insects to mass-flowering events.

Empirical studies of annual eusocial insects in agricultural landscapes report contrasting findings with regard to colony responses to mass-flowering of crops such as oilseed rape. In particular, total sexual production is often unaffected by such events, whereas worker number responds with a prominent increase. To resolve these conflicting observations, we model-using an established approach-the expected change in worker and sexual numbers in response to an increased worker productivity induced by mass-flowering events at different times of the season. We find that the predicted response pattern is mainly shaped by the degree to which individual worker productivity is reduced by an increasing number of workers in the colony. Different environmental conditions and colony characteristics result in different levels of interference of workers, for example, during foraging or nest construction. Reduction in individual productivity is low, when worker interference is negligible ("weak limitation") and high when an increasing number of workers substantially decreases per-capita efficiency ("strong limitation"). For weak limitation, any mass-flowering event that ends before the production of sexuals starts has a strong multiplicative impact on both worker and sexual numbers. The magnitude of the effect is quite independent of the precise timing of such an event. After the onset of sexual production, mass-flowering has a weaker effect, as the added resource supply is only linearly transferred into production of additional sexuals. For colonies under strong limitation, the predicted impact of mass-flowering events is generally weaker, especially on the production of sexuals, and the timing of mass-flowering events becomes more influential: Production of sexuals profits more from late than from early mass-flowering events. Consequently, early mass-flowering events are predicted to have a prominent effect on worker numbers but a negligible one on the output of sexuals. The model presented provides a mechanistic explanation of why increased worker abundances do not necessarily translate into increased production of sexuals. The model is also applicable to other eusocial insects such as paper wasps whenever brief pulses of massive resource availability shortly elevate resource intake rates above the "normal" levels.

Information use during movement regulates how fragmentation and loss of habitat affect body size.

An individual's body size is central to its behaviour and physiology, and tightly linked to its movement ability. The spatial arrangement of resources and a consumer's capacity to locate them are therefore expected to exert strong selection on consumer body size. We investigated the evolutionary impact of both the fragmentation and loss of habitat on consumer body size and its feedback effects on resource distribution, under varying levels of information used during habitat choice. We developed a mechanistic, individual-based, spatially explicit model, including several allometric rules for key consumer traits. Our model reveals that as resources become more fragmented and scarce, informed habitat choice selects for larger body sizes while random habitat choice promotes small sizes. Information use may thus be an overlooked explanation for the observed variation in body size responses to habitat fragmentation. Moreover, we find that resources can accumulate and aggregate if information about resource abundance is incomplete. Informed movement results in stable resource-consumer dynamics and controlled resources across space. However, habitat loss and fragmentation destabilize local dynamics and disturb resource suppression by the consumer. Considering information use during movement is thus critical to understand the eco-evolutionary dynamics underlying the functioning and structuring of consumer communities.

The Adequate Use of Limited Information in Dispersal Decisions.

Several theoretical studies predict that informed (e.g., density-dependent) dispersal should generally result in lower emigration probabilities than uninformed (random) dispersal. In a 2012 publication, Bocedi et al. surprisingly come to the opposite conclusion. For most scenarios investigated, they found that noninformed and, particularly, less precisely informed dispersers evolve lower dispersal propensity than dispersers following "fully informed" strategies. Further, they observed that fully informed individuals evolved a steplike dispersal response-a response to local density that contradicts theoretical predictions for organisms with nonoverlapping generations. Replicating the individual-based simulations of Bocedi et al. we find that these conclusions are not justified and are based on a misinterpretation of simulation results: their controversial findings result from (i) a misleading use of the term "population density," (ii) a misconception concerning the true informative value of the different decision criteria they compared, and (iii) arbitrary constraints on the evolution of the dispersal response that prevented the evolution of strategies that allow for a fitness-enhancing utilization of available information.

Annual dynamics of wild bee densities: attractiveness and productivity effects of oilseed rape.

Mass-flowering crops may affect long-term population dynamics, but effects on pollinators have never been studied across several years. We monitored wild bees in oilseed rape fields in 16 landscapes in Germany in two consecutive years. Effects on bee densities of landscape oilseed rape cover in the years of monitoring and in the previous years were evaluated with landscape data from three consecutive years. We fit empirical data to a mechanistic model to provide estimates for oilseed rape attractiveness and its effect on bee productivity in comparison to the rest of the landscape, and we evaluated consequences for pollinator densities in consecutive years. Our results show that high oilseed rape cover in the previous year enhances current densities of wild bees (except for bumble bees). Moreover, we show a strong attractiveness of and dilution on (i.e., decreasing bee densities with increasing landscape oilseed rape cover) oilseed rape for bees during flowering in the current year, modifying the effect of the previous year's oilseed rape cover in the case of wild bees (excluding Bombus). As long as other factors such as nesting sites or natural enemies do not limit bee reproduction, our findings suggest long-term positive effects of mass-flowering crops on bee populations, at least for non-Bombus generalists, which possibly help to maintain crop pollination services even when crop area increases. Similar effects are conceivable for other organisms providing ecosystem services in annual crops and should be considered in future studies.

Evolutionary responses to climate change in parasitic systems.

Species may respond to climate change in many ecological and evolutionary ways. In this simulation study, we focus on the concurrent evolution of three traits in response to climate change, namely dispersal probability, temperature tolerance (or niche width), and temperature preference (optimal habitat). More specifically, we consider evolutionary responses in host species involved in different types of interaction, that is parasitism or commensalism, and for low or high costs of a temperature tolerance-fertility trade-off (cost of generalization). We find that host species potentially evolve all three traits simultaneously in response to increasing temperature but that the evolutionary response interacts and may be compensatory depending on the conditions. The evolutionary adjustment of temperature preference is slower in the parasitism than in commensalism scenario. Parasitism, in turn, selects for higher temperature tolerance and increased dispersal. High costs for temperature tolerance (i.e. generalization) restrict evolution of tolerance and thus lead to a faster response in temperature preference than that observed under low costs. These results emphasize the possible role of biotic interactions and the importance of 'multidimensional' evolutionary responses to climate change.

Gender-specific emigration decisions sensitive to local male and female density.

Increasing interest is directed on understanding how individuals utilize information to come to dispersal decisions. We assume individuals base emigration decisions on male and female density in their natal patches. We derive gender-specific functions for emigration probability of species with discrete generations and polygynous mating under the premise that dispersal strategies equalize fitness expectations of emigrants and philopatric individuals: migration decisions should then always depend on a critical threshold density of the own gender. Whether density of the opposite sex affects emigration depends on details of resource competition: (1) Without competition, females should never emigrate, while males should emigrate in response to local sex ratio. (2) Under extreme competition among females or offspring, females and males should respond to the local density of their own gender only. (3) If both sexes compete over resources, emigration responds to the density of both sexes, but the dependence differs quantitatively between females and males. (4) Male-biased dispersal is the general expectation for polygynous species, but the model allows specifying conditions under which more females than males might nonetheless emigrate. The model provides guidelines for implementing density-dependent dispersal in simulations and specifies principal patterns that should emerge in empirical data.

Specialization and phenological synchrony of plant-pollinator interactions along an altitudinal gradient.

One of the most noticeable effects of anthropogenic climate change is the shift in timing of seasonal events towards earlier occurrence. The high degree of variation in species' phenological shifts has raised concerns about the temporal decoupling of interspecific interactions, but the extent and implications of this effect are largely unknown. In the case of plant-pollinator systems, more specialized species are predicted to be particularly threatened by phenological decoupling, since they are assumed to be less flexible in the choice of interaction partners, but until now this hypothesis has not been tested. In this paper, we studied phenology and interactions of plant and pollinator communities along an altitudinal gradient in the Alps as a model for the possible effects of climate change in time. Our results show that even relatively specialized pollinators were much more flexible in their use of plant species as floral resources than their local flower visitation suggested. We found no relationship between local specialization of pollinators and the consistency of their visitation patterns across sites, and also no relationship between specialization and phenological synchrony of pollinators with particular plants. Thus, in contrast to the conclusions of a recent simulation study, our results suggest that most pollinator species included in this study are not threatened by phenological decoupling from specific flowering plants. However, the flexibility of many rarely observed pollinator species remains unknown. Moreover, our results suggest that specialized flower visitors select plant species based on certain floral traits such as the length of the nectar holder tube. If that is the case, the observed flexibility of plant-pollinator interactions likely depends on a high degree of functional redundancy in the plant community, which may not exist in less diverse systems.

Evolutionary ecology of dispersal in biodiverse spatially structured systems: what is old and what is new?

Dispersal is a well-recognized driver of ecological and evolutionary dynamics, and simultaneously an evolving trait. Dispersal evolution has traditionally been studied in single-species metapopulations so that it remains unclear how dispersal evolves in metacommunities and metafoodwebs, which are characterized by a multitude of species interactions. Since most natural systems are both species-rich and spatially structured, this knowledge gap should be bridged. Here, we discuss whether knowledge from dispersal evolutionary ecology established in single-species systems holds in metacommunities and metafoodwebs and we highlight generally valid and fundamental principles. Most biotic interactions form the backdrop to the ecological theatre for the evolutionary dispersal play because interactions mediate patterns of fitness expectations across space and time. While this allows for a simple transposition of certain known principles to a multispecies context, other drivers may require more complex transpositions, or might not be transferred. We discuss an important quantitative modulator of dispersal evolution-increased trait dimensionality of biodiverse meta-systems-and an additional driver: co-dispersal. We speculate that scale and selection pressure mismatches owing to co-dispersal, together with increased trait dimensionality, may lead to a slower and more 'diffuse' evolution in biodiverse meta-systems. Open questions and potential consequences in both ecological and evolutionary terms call for more investigation. This article is part of the theme issue 'Diversity-dependence of dispersal: interspecific interactions determine spatial dynamics'.

When can plant-pollinator interactions promote plant diversity?

In the light of rapid losses of biodiversity worldwide, it has become more important than ever to study the factors that ensure the continued existence of diverse ecological communities. Whereas the diversity-enhancing effects of antagonistic interactions are relatively well understood, much less is known about the contribution of mutualistic interactions to biodiversity maintenance. This study assesses the influence of mutualistic interactions with pollinators on the diversity of plant communities with alternative means of reproduction besides animal pollination. In contrast to a recent more general model of plant-animal mutualisms, the results of our simulations suggest that interactions with pollinators do not generally promote plant diversity, irrespective of the structure of the interaction network. Despite a potential for increased plant species richness through the positive effect of pollinators on plant birth rates, species richness was mostly negatively affected by the presence of pollinators because existing abundance asymmetries were amplified by animal pollination. Our results imply that for plant communities with alternative means of reproduction, the loss of pollinators will usually not lead to decreased diversity. However, whereas the immediate effects of pollinator loss on plant community composition may be negligible, the long-term population genetic consequences are likely to be severe.

Kin competition as a major driving force for invasions.

Current theory explains accelerating invasions with increased levels of dispersal as being caused by "spatial selection." Here we argue that another selective force, strong kin competition resulting from high relatedness due to subsequent founder effects at the expanding margin, is of at least comparable importance for dispersal evolution during invasions. We test this hypothesis with individual-based simulations of a spatially structured population invading empty space. To quantify the relative contribution of kin competition to dispersal evolution, we contrast two scenarios, one including kin effects and one excluding them without influencing spatial selection. We find that kin competition is a major determinant for dispersal evolution at invasion fronts, especially under environmental conditions that favor a pronounced kin structure (i.e., small patches, low environmental stochasticity, and high patch isolation). We demonstrate the importance of kin competition and thus biotic influences on dispersal evolution during invasions.

Prey density, value, and spatial distribution affect the efficiency of area-concentrated search.

Searching individuals need to take decisions on where and how long to search. When food is spatially aggregated, detection of a food item signals a probability for the presence of further prey items in its surrounding. Organisms can thus intensify search effort upon detecting a prey item, but after unsuccessfully searching for a while, return to the previous, extensive search, this strategy is known as 'area-concentrated-search' (ACS). Here we present results of simulations where individuals perform ACS employing a correlated random walk with variable directional persistence. Switching between intensive and extensive search (with respectively low and high directional persistence) is a function of searcher's internal state represented as 'satiety' level depending on preceding consumption of prey items. We explore the effect of this function's control parameters ('switching level' i.e., the satiety at which the switching occurs, and the switchover shape parameter) on searching efficiency in dependence of (1) prey items' spatial distribution ranging from randomly uniform to highly contagious, (2) the overall prey density, and (3) prey 'caloric' value. Our main conclusions: (1) the form of the adopted switchover exerts an effect on searching efficiency, and this effect is most pronounced in landscapes with highly aggregated resources. Except for the most homogeneous prey distributions, there was a clear optimum area within the movement parameter space, yielding highest efficiency. (2) The optimal switching level is larger in heterogeneous landscapes, but optimum switchover shape is little affected by any of the landscape attributes. In most landscapes, it is most profitable to switch gradually rather than abruptly. (3) The success and optimal switching level depend not only on the prey's spatial distribution but also on average prey density while the value of prey items has little effect on the optimal movement parameters.

Effects of compositional heterogeneity and spatial autocorrelation on richness and diversity in simulated landscapes.

Landscape structure plays a key role in mediating a variety of ecological processes affecting biodiversity patterns; however, its precise effects and the mechanisms underpinning them remain unclear. While the effects of landscape structure have been extensively investigated both empirically and theoretically from a metapopulation perspective, the effects of spatial structure at the landscape scale remain poorly explored from a metacommunity perspective. Here, we attempt to address this gap using a spatially explicit, individual-based metacommunity model to explore the effects of landscape compositional heterogeneity and per se spatial configuration on diversity at the landscape and patch levels via their influence on long-term community assembly processes. Our model simulates communities composed of species of annual, asexual organisms living, reproducing, dispersing, and competing within grid-based, fractal landscapes that vary in their magnitude of spatial environmental heterogeneity and in their degree of spatial environmental autocorrelation. Communities are additionally subject to temporal environmental fluctuations and external immigration, allowing for turnover in community composition. We found that compositional heterogeneity and spatial autocorrelation had differing effects on richness, diversity, and the landscape and patch scales. Landscape-level diversity was driven by community dissimilarity at the patch level and increased with greater heterogeneity, while landscape richness was largely the result of the short-term accumulation of immigrants and decreased with greater compositional heterogeneity. Both richness and diversity decreased in variance with greater compositional heterogeneity, indicating a reduction in community turnover over time. Patch-level richness and diversity patterns appeared to be driven by overall landscape richness and local mass effects, resulting in maximum patch-level richness and diversity at moderate levels of compositional heterogeneity and high spatial autocorrelation.

Population dynamics of plant and pollinator communities: stability reconsidered.

Plant-pollinator networks are systems of outstanding ecological and economic importance. A particularly intriguing aspect of these systems is their high diversity. However, earlier studies have concluded that the specific mechanisms of plant-pollinator interactions are destabilizing and should lead to a loss of diversity. Here we present a mechanistic model of plant and pollinator population dynamics with the ability to represent a broad spectrum of interaction structures. Using this model, we examined the influence of pollinators on the stability of a plant community and the relationship between pollinator specialization and stability. In accordance with earlier work, our results show that plant-pollinator interactions may severely destabilize plant coexistence, regardless of the degree of pollinator specialization. However, if plant niche differentiation, a classical stabilizing mechanism, is sufficiently strong to overcome the minority disadvantage with respect to pollination, interactions with pollinators may even increase the stability of a plant community. In addition to plant niche differentiation, the relationship between specialization and stability depends on a number of parameters that affect pollinator growth rates. Our results highlight the complex effects of this particular type of mutualism on community stability and call for further investigations of the mechanisms of diversity maintenance in plant-pollinator systems.

Unexpected benefit of a social parasite for a key fitness component of its ant host.

Numerous invertebrates inhabit social insect colonies, including the hoverfly genus Microdon, whose larvae typically live as brood predators. Formica lemani ant colonies apparently endure Microdon mutabilis infections over several years, despite losing a considerable fraction of young, and may even produce more gynes. We present a model for resource allocation within polygynous ant colonies, which assumes that whether an ant larva switches development into a worker or a gyne depends on the quantity of food received randomly from workers. Accordingly, Microdon predation promotes gyne development by increasing resource availability for surviving broods. Several model predictions are supported by empirical data. (i) Uninfected colonies seldom produce gynes. (ii) Infected colonies experience a short-lived peak in gyne production leading to a bimodal distribution in gyne production. (iii) Low brood : worker ratio is the critical mechanism controlling gyne production. (iv) Brood : worker ratio reduction must be substantial for increased gyne production to become noticeable.

Why are metapopulations so rare?

Roughly 40 years after its introduction, the metapopulation concept is central to population ecology. The notion that local populations and their dynamics may be coupled by dispersal is without any doubt of great importance for our understanding of population-level processes. A metapopulation describes a set of subpopulations linked by (rare) dispersal events in a dynamic equilibrium of extinctions and recolonizations. In the large body of literature that has accumulated, the term "metapopulation" is often used in a very broad sense; most of the time it simply implies spatial heterogeneity. A number of reviews have recently addressed this problem and have pointed out that, despite the large and still growing popularity of the metapopulation concept, there are only very few empirical examples that conform with the strict classical metapopulation (CM) definition. In order to understand this discrepancy between theory and observation, we use an individual-based modeling approach that allows us to pinpoint the environmental conditions and the life-history attributes required for the emergence of a CM structure. We find that CM dynamics are restricted to a specific parameter range at the border between spatially structured but completely occupied and globally extinct populations. Considering general life-history attributes, our simulations suggest that CMs are more likely to occur in arthropod species than in (large) vertebrates. Since the specific type of spatial population structure determines conservation concepts, our findings have important implications for conservation biology. Our model suggests that most spatially structured populations are panmictic, patchy, or of mainland-island type, which makes efforts spent on increasing connectivity (e.g., corridors) questionable. If one does observe a true CM structure, this means that the focal metapopulation is on the brink of extinction and that drastic conservation measures are needed.

Emergence of spatially structured populations by area-concentrated search.

The idea that populations are spatially structured has become a very powerful concept in ecology, raising interest in many research areas. However, despite dispersal being a core component of the concept, it typically does not consider the movement behavior underlying any dispersal. Using individual-based simulations in continuous space, we explored the emergence of a spatially structured population in landscapes with spatially heterogeneous resource distribution and with organisms following simple area-concentrated search (ACS); individuals do not, however, perceive or respond to any habitat attributes per se but only to their foraging success. We investigated the effects of different resource clustering pattern in landscapes (single large cluster vs. many small clusters) and different resource density on the spatial structure of populations and movement between resource clusters of individuals. As results, we found that foraging success increased with increasing resource density and decreasing number of resource clusters. In a wide parameter space, the system exhibited attributes of a spatially structured populations with individuals concentrated in areas of high resource density, searching within areas of resources, and "dispersing" in straight line between resource patches. "Emigration" was more likely from patches that were small or of low quality (low resource density), but we observed an interaction effect between these two parameters. With the ACS implemented, individuals tended to move deeper into a resource cluster in scenarios with moderate resource density than in scenarios with high resource density. "Looping" from patches was more likely if patches were large and of high quality. Our simulations demonstrate that spatial structure in populations may emerge if critical resources are heterogeneously distributed and if individuals follow simple movement rules (such as ACS). Neither the perception of habitat nor an explicit decision to emigrate from a patch on the side of acting individuals is necessary for the emergence of such spatial structure.

The rising moon promotes mate finding in moths.

To counteract insect decline, it is essential to understand the underlying causes, especially for key pollinators such as nocturnal moths whose ability to orientate can easily be influenced by ambient light conditions. These comprise natural light sources as well as artificial light, but their specific relevance for moth orientation is still unknown. We investigated the influence of moonlight on the reproductive behavior of privet hawkmoths (Sphinx ligustri) at a relatively dark site where the Milky Way was visible while the horizon was illuminated by distant light sources and skyglow. We show that male moths use the moon for orientation and reach females significantly faster with increasing moon elevation. Furthermore, the choice of flight direction depended on the cardinal position of the moon but not on the illumination of the horizon caused by artificial light, indicating that the moon plays a key role in the orientation of male moths.

A metapopulation paradox: partial improvement of habitat may reduce metapopulation persistence.

The adverse influence of habitat degradation on the survival of populations may sometimes be amplified by rapid evolution over ecological timescales. This phenomenon of "evolutionary suicide" has been described in theoretical as well as empirical studies. However, no studies have suggested that habitat improvement could possibly also trigger an evolutionary response that would result in a decline in population size. We use individual-based simulations to demonstrate the potential for such a paradoxical response. An increase in the quality, size, or stability of only a fraction of the habitat patches in a metapopulation may result in an evolutionary decline in the dispersal propensity of individuals, followed by a decrease in recolonization, a reduction in the number of patches occupied, a decline in overall population size, and even extinction. Thus, well-intended conservation efforts that ignore potential evolutionary consequences of habitat management may increase the extinction risk of populations.

The ability of individuals to assess population density influences the evolution of emigration propensity and dispersal distance.

We analyze the simultaneous evolution of emigration and settlement decisions for actively dispersing species differing in their ability to assess population density. Using an individual-based model we simulate dispersal as a multi-step (patch to patch) movement in a world consisting of habitat patches surrounded by a hostile matrix. Each such step is associated with the same mortality risk. Our simulations show that individuals following an informed strategy, where emigration (and settlement) probability depends on local population density, evolve a lower (natal) emigration propensity but disperse over significantly larger distances - i.e. postpone settlement longer - than individuals performing density-independent emigration. This holds especially when variation in environmental conditions is spatially correlated. Both effects can be traced to the informed individuals' ability to better exploit existing heterogeneity in reproductive chances. Yet, already moderate distance-dependent dispersal costs prevent the evolution of multi-step (long-distance) dispersal, irrespective of the dispersal strategy.