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.

Eusociality outcompetes egalitarian and solitary strategies when resources are limited and reproduction is costly.

Explaining the evolution and maintenance of animal groups remains a challenge. Surprisingly, fundamental ecological factors, such as resource variance and competition for limited resources, tend to be ignored in models of cooperation. We use a mathematical model previously developed to quantify the influence of different group sizes on resource use efficiency in egalitarian groups and extend its scope to groups with severe reproductive skew (eusocial groups). Accounting for resource limitation, the model allows calculation of optimal group sizes (highest resource use efficiency) and equilibrium population sizes in egalitarian as well as eusocial groups for a broad spectrum of environmental conditions (variance of resource supply). We show that, in contrast to egalitarian groups, eusocial groups may not only reduce variance in resource supply for survival, thus reducing the risk of starvation, they may also increase variance in resource supply for reproduction. The latter effect allows reproduction even in situations when resources are scarce. These two facets of eusocial groups, resource sharing for survival and resource pooling for reproduction, constitute two beneficial mechanisms of group formation. In a majority of environmental situations, these two benefits of eusociality increase resource use efficiency and lead to supersaturation-a strong increase in carrying capacity. The increase in resource use efficiency provides indirect benefits to group members even for low intra-group relatedness and may represent one potential explanation for the evolution and especially the maintenance of eusociality and cooperative breeding.

Biased dispersal of Metrioptera bicolor, a wing dimorphic bush-cricket.

In the highly fragmented landscape of central Europe, dispersal is of particular importance as it determines the long-term survival of animal populations. Dispersal not only secures the recolonization of patches where populations went extinct, it may also rescue small populations and thus prevent local extinction events. As dispersal involves different individual fitness costs, the decision to disperse should not be random but context-dependent and often will be biased toward a certain group of individuals (e.g., sex- and wing morph-biased dispersal). Although biased dispersal has far-reaching consequences for animal populations, immediate studies of sex- and wing morph-biased dispersal in orthopterans are very rare. Here, we used a combined approach of morphological and genetic analyses to investigate biased dispersal of Metrioptera bicolor, a wing dimorphic bush-cricket. Our results clearly show wing morph-biased dispersal for both sexes of M. bicolor. In addition, we found sex-biased dispersal for macropterous individuals, but not for micropters. Both, morphological and genetic data, favor macropterous males as dispersal unit of this bush-cricket species. To get an idea of the flight ability of M. bicolor, we compared our morphological data with that of Locusta migratoria and Schistocerca gregaria, which are very good flyers. Based on our morphological data, we suggest a good flight ability for macropters of M. bicolor, although flying individuals of this species are seldom observed.

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.

Dispersal Timing: Emigration of Insects Living in Patchy Environments.

Dispersal is a life-history trait affecting dynamics and persistence of populations; it evolves under various known selective pressures. Theoretical studies on dispersal typically assume 'natal dispersal', where individuals emigrate right after birth. But emigration may also occur during a later moment within a reproductive season ('breeding dispersal'). For example, some female butterflies first deposit eggs in their natal patch before migrating to other site(s) to continue egg-laying there. How breeding compared to natal dispersal influences the evolution of dispersal has not been explored. To close this gap we used an individual-based simulation approach to analyze (i) the evolution of timing of breeding dispersal in annual organisms, (ii) its influence on dispersal (compared to natal dispersal). Furthermore, we tested (iii) its performance in direct evolutionary contest with individuals following a natal dispersal strategy. Our results show that evolution should typically result in lower dispersal under breeding dispersal, especially when costs of dispersal are low and population size is small. By distributing offspring evenly across two patches, breeding dispersal allows reducing direct sibling competition in the next generation whereas natal dispersal can only reduce trans-generational kin competition by producing highly dispersive offspring in each generation. The added benefit of breeding dispersal is most prominent in patches with small population sizes. Finally, the evolutionary contests show that a breeding dispersal strategy would universally out-compete natal dispersal.

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.

Spatially correlated extinctions select for less emigration but larger dispersal distances in the spider mite Tetranychus urticae.

Dispersal is a central process to almost all species on earth, as it connects spatially structured populations and thereby increases population persistence. Dispersal is subject to (rapid) evolution and local patch extinctions are an important selective force in this context. In contrast to the randomly distributed local extinctions considered in most theoretical studies, habitat fragmentation or other anthropogenic interventions will lead to spatially correlated extinction patterns. Under such conditions natural selection is thought to lead to more long-distance dispersal, but this theoretical prediction has not yet been verified empirically. We test this prediction in experimental spatially structured populations of the spider mite Tetranychus urticae and supplement these empirical results with insights from an individual-based evolutionary model. We demonstrate that the spatial correlation of local extinctions changes the entire distribution of dispersal distances (dispersal kernel) and selects for overall less emigration but more long-distance dispersal.

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.

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.

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.

Diaspore trait preferences of dispersing ants.

Elaiosomes of myrmecochorous plant seeds are known to enhance the attraction of diaspore-dispersing ants by serving as a nutritional reward. However, it remained unclear which (nutritional) compounds affect diaspore preferences of ants. We hypothesized that apart from elaiosome/seed-size ratio, volume, and physical surface of diaspores, the quantity and the composition of fatty acids, amino acids, and sugars strongly influence the diaspore preferences of different species. Chemical (nutritional) profiles as well as structural properties of seeds with and without elaiosomes were analyzed and correlated with observed seed choice behavior of ants. Cafeteria experiments in the field confirmed the enhanced attractiveness of elaiosome-bearing seeds for all three ant species tested (Lasius fuliginosus, Myrmica ruginodis, and Temnothorax nylanderi), although seeds lacking elaiosomes also were transported. In multiple-choice cafeteria experiments with simultaneously offered diaspores of 16 plant species with and without elaiosome and with highly varying structural and chemical properties, all three ant species showed distinct preferences for certain diaspore species. Correlation analyses confirmed that the presence of an elaiosome represents the crucial factor that favors ant diaspore dispersal. In addition, the composition and the content of free amino acids, and to varying degrees fatty acids, were found to significantly affect preferences of each ant species, whereas the effect of single fatty acids acting as chemical triggers for diaspore transport by ants, as supposed by several studies, was not confirmed. In conclusion, although at least some diaspore species lacking elaiosomes attract ants for diaspore removal services by presenting nutritional seed coats, the production of elaiosomes seems to provide a worthwhile investment. Elaiosomes ensure rapid diaspore detection and removal due to chemical cue compounds and by offering a highly nutritional food supply, probably fitting the nutritional demands of ants.

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.

Assortative mating counteracts the evolution of dispersal polymorphisms.

Polymorphic dispersal strategies are found in many plant and animal species. An important question is how the genetic variation underlying such polymorphisms is maintained. Numerous mechanisms have been discussed, including kin competition or frequency-dependent selection. In the context of sympatric speciation events, genetic and phenotypic variation is often assumed to be preserved by assortative mating. Thus, recently, this has been advocated as a possible mechanism leading to the evolution of dispersal polymorphisms. Here, we examine the role of assortative mating for the evolution of trade-off-driven dispersal polymorphisms by modeling univoltine insect species in a metapopulation. We show that assortative mating does not favor the evolution of polymorphisms. On the contrary, assortative mating favors the evolution of an intermediate dispersal type and a uni-modal distribution of traits within populations. As an alternative, mechanism dominance may explain the occurrence of two discrete morphs.

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.

On the elasticity of range limits during periods of expansion.

Dispersal is known to play a crucial role in the formation of species' ranges. Recent studies demonstrate that dispersiveness increases rapidly during the range expansion of species due to a fitness increase for dispersers at the expanding front. R. D. Holt concluded, however, that emigration should decline after the period of invasion and hence predicted some range contraction following the initial expansion phase. In this study, we evaluate this hypothesis using a spatially explicit individual-based model of populations distributed along environmental gradients. In our experiments we allow the species to spread along a gradient of declining conditions. Results show that range contraction did emerge in a gradient of dispersal mortality, caused by the rapid increase in emigration probability during invasion and selection disfavoring dispersal, once a stable range is formed. However, gradients in growth rate, local extinction rate, and patch capacity did not lead to a noticeable contraction of the range. We conclude, that the phenomenon of range contraction may emerge, but only under conditions that select for a reduction in dispersal at the range edge in comparison to the core region once the expansion period is over.

Predator-induced dispersal and the evolution of conditional dispersal in correlated environments.

It is widely accepted that organisms adjust their dispersal propensity to local population density, but there has been no analysis of how they should react to changes in environmental conditions that reduce local density. We take the case of delayed predator-induced dispersal (PID) in aphids to explore in which way current environmental conditions may be utilized as an appropriate signal for dispersal decisions. In aphids, the presence of predators triggers the production of winged offspring that may later leave the plant and shift their center of activity permanently. Using individual-based simulations as well as analytical approximations, we explore under which conditions PID is likely to evolve. We demonstrate that this requires substantial temporal correlation in predation risk and weak competition among prey; these conditions may be fulfilled in the aphid system. We discuss the analogy between the specific case of PID and the evolution of conditional emigration in the face of spatiotemporally correlated deterioration in reproduction or survival.

The effect of translocation on movement behaviour--a test of the assumptions of behavioural studies.

Animal movement behaviour is intensively investigated with capture-mark-recapture studies. For the analysis of such experiments, the influence of marking technique, handling and translocation of marked animals on movement pattern is of crucial importance since it may mask or overrule the effects of the main research question. Here we present a capture-mark-recapture experiment on the movement behaviour of the blue-winged grasshopper Oedipoda caerulescens. We analyzed the influence of translocation of individuals from familiar to unfamiliar sites. Our study clearly demonstrates a significant influence of translocation to unfamiliar sites on the movement behaviour of O. caerulescens. Translocated individuals moved longer distances, showed smaller daily turning angles, and thus movements were more directed than those of resident individuals. The effect of translocation on daily moved distances was most pronounced on the first day of the experiment. We thus conclude that at least for the first day after translocation, movement behaviour is significantly influenced by translocation itself. Data ignoring this influence will be unsuitable for the prediction of dispersal behaviour, habitat detection capability or habitat preference.

Sex-specific spatio-temporal variability in reproductive success promotes the evolution of sex-biased dispersal.

Inbreeding depression, asymmetries in costs or benefits of dispersal, and the mating system have been identified as potential factors underlying the evolution of sex-biased dispersal. We use individual-based simulations to explore how the mating system and demographic stochasticity influence the evolution of sex-specific dispersal in a metapopulation with females competing over breeding sites, and males over mating opportunities. Comparison of simulation results for random mating with those for a harem system (locally, a single male sires all offspring) reveal that even extreme variance in local male reproductive success (extreme male competition) does not induce male-biased dispersal. The latter evolves if the between-patch variance in reproductive success is larger for males than females. This can emerge due to demographic stochasticity if the habitat patches are small. More generally, members of a group of individuals experiencing higher spatio-temporal variance in fitness expectations may evolve to disperse with greater probability than others.

Sex-specific dispersal and evolutionary rescue in metapopulations infected by male killing endosymbionts.

BACKGROUND: Male killing endosymbionts manipulate their arthropod host reproduction by only allowing female embryos to develop into infected females and killing all male offspring. Because the resulting change in sex ratio is expected to affect the evolution of sex-specific dispersal, we investigated under which environmental conditions strong sex-biased dispersal would emerge, and how this would affect host and endosymbiont metapopulation persistence. RESULTS: We simulated host-endosymbiont metapopulation dynamics in an individual-based model, in which dispersal rates are allowed to evolve independently for the two sexes. Prominent male-biased dispersal emerges under conditions of low environmental stochasticity and high dispersal mortality. By applying a reshuffling algorithm, we show that kin-competition is a major driver of this evolutionary pattern because of the high within-population relatedness of males compared to those of females. Moreover, the evolution of sex-specific dispersal rescues metapopulations from extinction by (i) reducing endosymbiont fixation rates and (ii) by enhancing the extinction of endosymbionts within metapopulations that are characterized by low environmental stochasticity. CONCLUSION: Male killing endosymbionts induce the evolution of sex-specific dispersal, with prominent male-biased dispersal under conditions of low environmental stochasticity and high dispersal mortality. This male-biased dispersal emerges from stronger kin-competition in males compared to females and induces an evolutionary rescue mechanism.