Losers in the ‘Rock-Paper-Scissors’ game: The role of non-hierarchical competition and chaos as biodiversity sustaining agents in aquatic systems

Processes occurring within small areas (patch-scale) that influence species richness and spatial heterogeneity of larger areas (landscape-scale) have long been an interest of ecologists. This research focused on the role of patch-scale deterministic chaos arising in phytoplankton assemblages characteristic of “Rock-Paper-Scissors” population dynamics (i.e., competitively non-hierarchical). We employed a simple 2-patch model configuration with lateral mixing and through-flow, and tested the robustness of species richness at the scale of the landscape and spatial heterogeneity. Three different assemblages were used that in a dimensionless box model configuration exhibited chaotic behavior. Our results showed that when a spatial dimension was added to the model configuration, and when all species were shared between patches (i.e., no invading populations), chaos-induced species richness and spatial heterogeneity were quickly reduced with the onset of mixing. While assemblages in each patch were comprised of exactly the same species, they differed in their proportional population densities due to differing stages of succession and the incidence of alternative assemblage structures. Even at very low mixing rates (0.001 d⁻¹), which produced low passive migration rates (0.1% of the total biomass per day), the incidence of high richness and heterogeneity decreased by ∼80%. Interestingly, this sensitivity was not the same for the three assemblages tested. Declines in species richness and spatial heterogeneity associated with mixing were greater in assemblages comprised of competitively dissimilar species (based on the area occupied in the resource-tradeoff space defined by the R* model). The underlying mechanisms may involve the degree to which nutrient dynamics are altered with the arrival of immigrants. Our findings suggest that in partially to well-mixed aquatic systems, the roles of patch-scale non-hierarchical competition and chaos as factors maintaining species richness and spatial heterogeneity may be limited. However, in aquatic systems that experience periods of very low mixing, or even disconnection, non-hierarchical competition and chaos might indeed contribute significantly to biodiversity.     

Reproductive conflicts and egg discrimination in a socially polymorphic ant

The ability to discriminate against competitors shapes cooperation and conflicts in all forms of social life. In insect societies, workers may detect and destroy eggs laid by other workers or by foreign queens, which can contribute to regulate reproductive conflicts among workers and queens. Variation in colony kin structure affects the magnitude of these conflicts and the diversity of cues used for discrimination, but the impact of the number of queens per colony on the ability of workers to discriminate between eggs of diverse origin has so far not been investigated. Here, we examined whether workers from the socially polymorphic ant Formica selysi distinguished eggs laid by nestmate workers from eggs laid by nestmate queens, as well as eggs laid by foreign queens from eggs laid by nestmate queens. Workers from single- and multiple-queen colonies discriminated worker-laid from queen-laid eggs, and eliminated the former. This suggests that workers collectively police each other in order to limit the colony-level costs of worker reproduction and not because of relatedness differences towards queens’ and workers’ sons. Workers from single-queen colonies discriminated eggs laid by foreign queens of the same social structure from eggs laid by nestmate queens. In contrast, workers from multiple-queen colonies did not make this distinction, possibly because cues on workers or eggs are more diverse. Overall, these data indicate that the ability of F. selysi workers to discriminate eggs is sufficient to restrain worker reproduction but does not permit discrimination between matrilines in multiple-queen colonies.     

Using an individual-based model to quantify scale transition in demographic rate functions: Deaths in a coral reef fish

Scientifically informed population management requires quantitatively accurate demographic rate functions that apply at the spatial scale at which populations are actually managed, but practical constraints confine most field measurements of such functions to small study plots. This paper employs an individual-based population growth model to extrapolate the death rate function in a well-studied coral reef fish, the bridled goby Coryphopterus glaucofraenum, from the scale of coral reef “cells” at which it was measured to the larger scale of an entire coral reef. Density dependence in the whole-reef function actually proves stronger than in the local function because high goby density occasionally arises in local patches with few refuges from predators, producing very high mortality there. This IBM-based approach extends the reach of scale transition theory by examining considerably more realistic models than standard analytical methods can presently handle.     

A novel method for investigating the collective behaviour of fish: introducing ‘Robofish’

Collective animal behaviour has attracted much attention recently, but cause-and-effect within interaction sequences has often been difficult to establish. To tackle this problem, we constructed a robotic fish (‘Robofish’) with which three-spined sticklebacks (Gasterosteus aculeatus L.) interact. Robofish is a computer-controlled replica stickleback that can be programmed to move around a tank. First, we demonstrated the functioning of the method: that the sticklebacks interacted with Robofish. We examined two types of interaction: recruitment and leadership. We found that Robofish could recruit a single fish from a refuge and could initiate a turn in singletons and in groups of ten, i.e. act as a leader. We also showed that the influence of Robofish diminished after the first 30 min that fish spent in a new environment. Second, using this method, we investigated the effects of metric and topological inter-individual distance on the influence that Robofish had on the orientation of fish in a shoal of ten. We found that inter-individual interactions during this turn were predominantly mediated by topological, rather than metric, distance. Finally, we discussed the potential of this novel method and the importance of our findings for the study of collective animal behaviour.     

Dynamic response to danger in a parasitoid wasp

Despite the multitude of work on patch time allocation and the huge number of studies on patch choice in the face of danger, the patch leaving response of foragers perceiving cues of danger has received relatively little attention. We investigated the response of parasitoid insects to cues of danger both theoretically and experimentally. Using stochastic dynamic theory, we demonstrate that patch-leaving responses in response to the detection of danger should be seen as a dynamic decision that depends upon reproductive options on the current host patch and on alternative patches that might be found after leaving the current patch. Our theory predicts a sigmoidal response curve of parasitoids, where they should accept the danger and stay on the patch when patch quality is high and should increasingly avoid the risk and emigrate from the patch with decreasing patch quality and decreasing costs of traveling to an alternative host patch. Experiments with females of the drosophilid parasitoid Asobara tabida that were exposed to a puff of formic acid (a danger cue) at different times through their patch exploitation confirmed the theoretical predictions (i.e., a sigmoid response curve); however, the predicted curve was significantly steeper than observed. We discuss the impact of dynamic patch-exit decisions of individual foragers on population and community dynamics.     

Coexistence of intraguild predators and prey in resource-rich environments

The prevalence of intraguild predation (IGP) in productive environments has long puzzled ecologists. Theory predicts the exclusion of intraguild prey from such environments, but data consistently defy this expectation. This suggests that coexistence mechanisms at high resource productivity may differ from those at lower productivity. Here I present a mathematical model that investigates multiple coexistence mechanisms. I incorporate two biological features widely observed in IGP communities: intraspecific interference via cannibalism or superparasitism, and temporal refuges arising from differential sensitivities to abiotic variation. I develop predictions based on three aspects of the IG prey-IG predator interaction: mutual invasibility, transient dynamics, and long-term abundances. These predictions specify the conditions under which coexistence mechanisms reinforce vs. deter one another: when a competition-IGP trade-off allows coexistence at intermediate productivity a temporal refuge for the intraguild prey always allows coexistence at high productivity, but intraspecific interference does so only at a net fitness cost to the intraguild predator. Intraspecific interference that benefits the intraguild predator not only reduces tradeoff-mediated coexistence at intermediate productivity, but also undermines the refuge's coexistence-enhancing effect at high productivity. Different mechanism combinations yield characteristic signatures in time series data during transient dynamics. By judicious measurement of parameters and examining time series for critical signatures, one can elucidate the mechanisms that allow IGP to prevail in resource-rich environments.     

Evolution of polyploidy and the diversification of plant-pollinator interactions

One of the major mechanisms of plant diversification has been the evolution of polyploid populations that differ from their diploid progenitors in morphology, physiology, and environmental tolerances. Recent studies have indicated that polyploidy may also have major effects on ecological interactions with herbivores and pollinators. We evaluated pollination of sympatric diploid and tetraploid plants of the rhizomatous herb Heuchera grossulariifolia (Saxifragaceae) along the Selway and Salmon Rivers of northern Idaho, USA, during four consecutive years. Previous molecular and ecological analyses had indicated that the tetraploid populations along these two river systems are independently derived and differ from each other in multiple traits. In each region, we evaluated floral visitation rate by all insect visitors, pollination efficacy of all major visitors, and relative contribution of all major pollinators to seed set. In both regions, diploid and tetraploid plants attracted different suites of floral visitors. Most pollination was attributable to several bee species and the moth Greya politella. Lasioglossum bees preferentially visited diploid plants at Lower Salmon but not at Upper Selway, queen Bombus centralis preferentially visited tetraploids at both sites, and worker B. centralis differed between sites in their cytotype preference. Hence, diploid and autotetraploid H. grossulariifolia plants act essentially as separate ecological species and may experience partial reproductive isolation through differential visitation and pollination by their major floral visitors. Overall the results, together with recent results from other studies, suggest that the repeated evolution of polyploidy in plants may contribute importantly to the structure and diversification of ecological interactions in terrestrial communities.     

Female aggressive response and hormonal correlates—an intrusion experiment in a free-living passerine

The optimal mating system is rarely the same for males and females—whereas males usually benefit from attracting additional females to the territory, this could incur costs for the resident female. Females should therefore prevent prospecting females from settling on the territory. We studied the male and female behavioral and hormonal responses to simulated female territorial intrusions in free-living bluethroats during the pre-laying period. In the study population, polygyny occurs with potential fitness costs for the resident female. We recorded different aspects of aggressive behavior before and after presentation of a live female decoy and playback of female song. These behaviors were compared with a set of intrusions using a male decoy. At the end of a trial, the birds were captured, and blood samples were analyzed for androstenedione, testosterone, estradiol and corticosterone. During the pre-intrusion period, none of the females were observed. Females generally responded strongly to the female decoy by increased flight rate, vocalizations, and by conspicuous perching. Nearly half of the males displayed to the female decoy but never while the resident female was present. We suggest that resident female aggression in bluethroats prevents courtship by her mate and signals her mating status to the female intruder. Female aggression could therefore prevent additional females to settle on the territory and shape the mating system. Females that responded with song had higher levels of estradiol. These findings suggest that estradiol may support aggression in breeding female birds.     

Elemental Conservation Units: Communicating Extinction Risk without Dictating Targets for Protection

Abstract:  Conservation biologists mostly agree on the need to identify and protect biodiversity below the species level but have not yet resolved the best approach. We addressed 2 issues relevant to this debate. First, we distinguished between the abstract goal of preserving the maximum amount of unique biodiversity and the pragmatic goal of minimizing the loss of ecological goods and services given that further loss of biodiversity seems inevitable. Second, we distinguished between the scientific task of assessing extinction risk and the normative task of choosing targets for protection. We propose that scientific advice on extinction risk be given at the smallest meaningful scale: the elemental conservation unit (ECU). An ECU is a demographically isolated population whose probability of extinction over the time scale of interest (say 100 years) is not substantially affected by natural immigration from other populations. Within this time frame, the loss of an ECU would be irreversible without human intervention. Society's decision to protect an ECU ought to reflect human values that have social, economic, and political dimensions. Scientists can best inform this decision by providing advice about the probability that an ECU will be lost and the ecological and evolutionary consequences of that loss in a form that can be integrated into landscape planning. The ECU approach provides maximum flexibility to decision makers and ensures that the scientific task of assessing extinction risk informs, but remains distinct from, the normative social challenge of setting conservation targets.     

Impact of cannibalism on predator-prey dynamics: size-structured interactions and apparent mutualism

Direct and indirect interactions between two prey species can strongly alter the dynamics of predator-prey systems. Most predators are cannibalistic, and as a consequence, even systems with only one predator and one prey include two prey types: conspecifics and heterospecifics. The effects of the complex direct and indirect interactions that emerge in such cannibalistic systems are still poorly understood. This study examined how the indirect interaction between conspecific and heterospecific prey affects cannibalism and predation rates and how the direct interactions between both species indirectly alter the effect of the cannibalistic predator. I tested for these effects using larvae of the stream salamanders Eurycea cirrigera (prey) and Pseudotriton ruber (cannibalistic predator) by manipulating the relative densities of the conspecific and heterospecific prey in the presence and absence of the predator in experimental streams. The rates of cannibalism and heterospecific predation were proportional to the respective densities and negatively correlated, indicating a positive indirect interaction between conspecific and heterospecific prey, similar to "apparent mutualism." Direct interactions between prey species did not alter the effect of the predator. Although both types of prey showed a similar 30% reduction in night activity and switch in microhabitat use in response to the presence of the predator, cannibalism rates were three times higher than heterospecific predation rates irrespective of the relative densities of the two types of prey. Cumulative predation risks differed even more due to the 48% lower growth rate of conspecific prey. Detailed laboratory experiments suggest that the 3:1 difference in cannibalism and predation rate was due to the higher efficiency of heterospecific prey in escaping immediate attacks. However, no difference was observed when the predator was a closely related salamander species, Gyrinophilus porphyriticus, indicating that this difference is species specific. This demonstrates that cannibalism can result in the coupling of predator and prey mortality rates that strongly determines the dynamics of predator-prey systems.