Experimentally simulating the evolution-to-ecology connection: Divergent predator morphologies alter natural food webs.

The idea that changing environmental conditions drive adaptive evolution is a pillar of evolutionary ecology. But, the opposite-that adaptive evolution alters ecological processes-has received far less attention yet is critical for eco-evolutionary dynamics. We assessed the ecological impact of divergent values in a key adaptive trait using 16 populations of the brown anole lizard (Anolis sagrei). Mirroring natural variation, we established islands with short- or long-limbed lizards at both low and high densities. We then monitored changes in lower trophic levels, finding that on islands with a high density of short-limbed lizards, web-spider densities decreased and plants grew more via an indirect positive effect, likely through an herbivore-mediated trophic cascade. Our experiment provides strong support for evolution-to-ecology connections in nature, likely closing an otherwise well-characterized eco-evolutionary feedback loop.

Predator-induced collapse of niche structure and species coexistence.

Biological invasions are both a pressing environmental challenge and an opportunity to investigate fundamental ecological processes, such as the role of top predators in regulating biodiversity and food-web structure. In whole-ecosystem manipulations of small Caribbean islands on which brown anole lizards (Anolis sagrei) were the native top predator, we experimentally staged invasions by competitors (green anoles, Anolis smaragdinus) and/or new top predators (curly-tailed lizards, Leiocephalus carinatus). We show that curly-tailed lizards destabilized the coexistence of competing prey species, contrary to the classic idea of keystone predation. Fear-driven avoidance of predators collapsed the spatial and dietary niche structure that otherwise stabilized coexistence, which intensified interspecific competition within predator-free refuges and contributed to the extinction of green-anole populations on two islands. Moreover, whereas adding either green anoles or curly-tailed lizards lengthened food chains on the islands, adding both species reversed this effect-in part because the apex predators were trophic omnivores. Our results underscore the importance of top-down control in ecological communities, but show that its outcomes depend on prey behaviour, spatial structure, and omnivory. Diversity-enhancing effects of top predators cannot be assumed, and non-consumptive effects of predation risk may be a widespread constraint on species coexistence.

The Difficulty of Predicting Evolutionary Change in Response to Novel Ecological Interactions: A Field Experiment with Anolis Lizards.

AbstractDetermining whether and how evolution is predictable is an important goal, particularly as anthropogenic disturbances lead to novel species interactions that could modify selective pressures. Here, we use a multigeneration field experiment with brown anole lizards (Anolis sagrei) to test hypotheses about the predictability of evolution. We manipulated the presence/absence of predators and competitors of A. sagrei across 16 islands in the Bahamas that had preexisting brown anole populations. Before the experiment and again after roughly five generations, we measured traits related to locomotor performance and habitat use by brown anoles and used double-digest restriction enzyme-associated DNA sequencing to estimate genome-wide changes in allele frequencies. Although previous work showed that predators and competitors had characteristic effects on brown anole behavior, diet, and population sizes, we found that evolutionary change at both phenotypic and genomic levels was difficult to forecast. Phenotypic changes were contingent on sex and habitat use, whereas genetic change was unpredictable and not measurably correlated with phenotypic changes, experimental treatments, or other environmental factors. Our work shows how differences in ecological context can alter evolutionary outcomes over short timescales and underscores the difficulty of forecasting evolutionary responses to multispecies interactions in natural conditions, even in a well-studied system with ample supporting ecological information.

Consumer Responses to Experimental Pulsed Subsidies in Isolated versus Connected Habitats.

AbstractIncreases in consumer abundance following a resource pulse can be driven by diet shifts, aggregation, and reproductive responses, with combined responses expected to result in faster response times and larger numerical increases. Previous work in plots on large Bahamian islands has shown that lizards (Anolis sagrei) increased in abundance following pulses of seaweed deposition, which provide additional prey (i.e., seaweed detritivores). Numerical responses were associated with rapid diet shifts and aggregation, followed by increased reproduction. These dynamics are likely different on isolated small islands, where lizards cannot readily immigrate or emigrate. To test this, we manipulated the frequency and magnitude of seaweed resource pulses on whole small islands and in plots within large islands, and we monitored lizard diet and numerical responses over 4 years. We found that seaweed addition caused persistent increases in lizard abundance on small islands regardless of pulse frequency or magnitude. Increased abundance may have occurred because the initial pulse facilitated population establishment, possibly via enhanced overwinter survival. In contrast with a previous experiment, we did not detect numerical responses in plots on large islands, despite lizards consuming more marine resources in subsidized plots. This lack of a numerical response may be due to rapid aggregation followed by disaggregation or to stronger suppression of A. sagrei by their predators on the large islands in this study. Our results highlight the importance of habitat connectivity in governing ecological responses to resource pulses and suggest that disaggregation and changes in survivorship may be underappreciated drivers of pulse-associated dynamics.

Pulsed seaweed subsidies drive sequential shifts in the effects of lizard predators on island food webs.

Most prominent theories of food web dynamics imply the simultaneous action of bottom-up and top-down forces. However, transient bottom-up effects resulting from resource pulses can lead to sequential shifts in the strength of top-down predator effects. We used a large-scale field experiment (32 small islands sampled over 5 years) to probe how the frequency and magnitude of pulsed seaweed inputs drives temporal variation in the top-down effects of lizard predators. Short-term weakening of lizard effects on spiders and plants (the latter via a trophic cascade) were associated with lizard diet shifts, and were more pronounced with larger seaweed inputs. Long-term strengthening of lizard effects was associated with lizard numerical responses and plant fertilisation. Increased pulse frequency reinforced the strengthening of lizard effects on spiders and plants. These results underscore the temporally variable nature of top-down effects and highlight the role of resource pulses in driving this variation.

Predation-associated modulation of movement-based signals by a Bahamian lizard.

Signaling individuals must effectively capture and hold the attention of intended conspecific receivers while limiting eavesdropping by potential predators. A possible mechanism for achieving this balance is for individuals to modulate the physical properties of their signals or to alter the proportion of time spent signaling, depending upon local levels of predation pressure. We test the hypothesis that prey can alter their visual signaling behavior to decrease conspicuousness and potentially limit predation risk via modulation of signal properties or display rate. To do so, we conducted a manipulative experiment in nature to evaluate the possible effect of predation pressure on the physical properties of movement-based signals and on the proportion of time spent signaling by using a well-understood predator-prey system in the Bahamas, the semiarboreal lizard Anolis sagrei, and one of its main predators, the curly-tailed lizard Leiocephalus carinatus. We find that on islands onto which the predator was introduced, male anoles reduce the maximum amplitude of head-bob displays but not the proportion of time spent signaling, in comparison with control islands lacking the predator. This reduction of amplitude also decreases signal active space, which might alter the reproductive success of signaling individuals. We suggest that future studies of predator-prey interactions consider the risk effects generated by changes in signals or signaling behavior to fully determine the influence of predation pressure on the dynamics of prey populations.

Predators suppress herbivore outbreaks and enhance plant recovery following hurricanes.

Understanding processes that may stabilize ecological systems confronted with rapidly changing environmental conditions is a key issue in ecology. We studied a system of highly fluctuating populations, the moth Achyra rantalis feeding on the plant Sesuvium portulacastrum in a group of small subtropical islands of the Bahamas. The plant is a prostrate inhabitant of shorelines, and consequently moths are highly vulnerable to being consumed by the ground-foraging lizard Anolis sagrei. We measured the percent ground cover of Sesuvium and abundance of Achyra on 11 islands with lizards present and 21 islands without lizards annually for 10 consecutive years. Overall abundance of Achyra was 4.6 times higher on no-lizard islands than on lizard islands. The percent cover of Sesuvium exhibited lower temporal variability on lizard islands when the study site was undisturbed by hurricanes, and higher recovery rate on lizard islands following hurricanes. We suggest that both of these stabilizing phenomena are linked to a trophic cascade in which predatory lizards control herbivore populations, thereby suppressing outbreaks and enhancing plant recovery following physical disturbance.

The effect of chronic seaweed subsidies on herbivory: plant-mediated fertilization pathway overshadows lizard-mediated predator pathways.

Flows of energy and materials link ecosystems worldwide and have important consequences for the structure of ecological communities. While these resource subsidies typically enter recipient food webs through multiple channels, most previous studies focussed on a single pathway of resource input. We used path analysis to evaluate multiple pathways connecting chronic marine resource inputs (in the form of seaweed deposits) and herbivory in a shoreline terrestrial ecosystem. We found statistical support for a fertilization effect (seaweed increased foliar nitrogen content, leading to greater herbivory) and a lizard numerical response effect (seaweed increased lizard densities, leading to reduced herbivory), but not for a lizard diet-shift effect (seaweed increased the proportion of marine-derived prey in lizard diets, but lizard diet was not strongly associated with herbivory). Greater seaweed abundance was associated with greater herbivory, and the fertilization effect was larger than the combined lizard effects. Thus, the bottom-up, plant-mediated effect of fertilization on herbivory overshadowed the top-down effects of lizard predators. These results, from unmanipulated shoreline plots with persistent differences in chronic seaweed deposition, differ from those of a previous experimental study of the short-term effects of a pulse of seaweed deposition: while the increase in herbivory in response to chronic seaweed deposition was due to the fertilization effect, the short-term increase in herbivory in response to a pulse of seaweed deposition was due to the lizard diet-shift effect. This contrast highlights the importance of the temporal pattern of resource inputs in determining the mechanism of community response to resource subsidies.

Predators determine how weather affects the spatial niche of lizard prey: exploring niche dynamics at a fine scale.

Although abiotic and biotic factors can interact to shape the spatial niche of a species, studies that explore the interactive effects of both at a local scale are rare. We demonstrate that one of the main axes (perch height) characterizing the spatial niche of a common lizard, Anolis sagrei, varies according to the interactive effects of weather and the activity of a larger predatory lizard, Leiocephalus carinatus. Results were completely consistent: no matter how favorable the weather conditions for using the ground (mainly characterized by temperature, humidity, wind speed, rain), A. sagrei did not do so if the predator was present. Hence, great behavioral plasticity enabled A. sagrei to adjust its use of space very quickly. To the best of our knowledge, these results constitute the first field demonstration for anoles (and possibly for other animals as well) of how time-varying environmental conditions and predator presence interact to produce short-term changes in utilization along a major niche axis.

Marine subsidies have multiple effects on coastal food webs.

The effect of resource subsidies on recipient food webs has received much recent attention. The purpose of this study was to measure the effects of significant seasonal seaweed deposition events, caused by hurricanes and other storms, on species inhabiting subtropical islands. The seaweed represents a pulsed resource subsidy that is consumed by amphipods and flies, which are eaten by lizards and predatory arthropods, which in turn consume terrestrial herbivores. Additionally, seaweed decomposes directly into the soil under plants. We added seaweed to six shoreline plots and removed seaweed from six other plots for three months; all plots were repeatedly monitored for 12 months after the initial manipulation. Lizard density (Anolis sagrei) responded rapidly, and the overall average was 63% higher in subsidized than in removal plots. Stable-isotope analysis revealed a shift in lizard diet composition toward more marine-based prey in subsidized plots. Leaf damage was 70% higher in subsidized than in removal plots after eight months, but subsequent damage was about the same in the two treatments. Foliage growth rate was 70% higher in subsidized plots after 12 months. Results of a complementary study on the relationship between natural variation in marine subsidies and island food web components were consistent with the experimental results. We suggest two causal pathways for the effects of marine subsidies on terrestrial plants: (1) the "fertilization effect" in which seaweed adds nutrients to plants, increasing their growth rate, and (2) the "predator diet shift effect" in which lizards shift from eating local prey (including terrestrial herbivores) to eating mostly marine detritivores.

Predator-induced behaviour shifts and natural selection in field-experimental lizard populations.

The role of behaviour in evolutionary change has long been debated. On the one hand, behavioural changes may expose individuals to new selective pressures by altering the way that organisms interact with the environment, thus driving evolutionary divergence. Alternatively, behaviour can act to retard evolutionary change: by altering behavioural patterns in the face of new environmental conditions, organisms can minimize exposure to new selective pressures. This constraining influence of behaviour has been put forward as an explanation for evolutionary stasis within lineages and niche conservatism within clades. Nonetheless, the hypothesis that behavioural change prevents natural selection from operating in new environments has never been experimentally tested. We conducted a controlled and replicated experimental study of selection in entirely natural populations; we demonstrate that lizards alter their habitat use in the presence of an introduced predator, but that these behavioural shifts do not prevent patterns of natural selection from changing in experimental populations.

How is extinction risk related to population-size variability over time? A family of models for species with repeated extinction and immigration.

It is well known that for an isolated population, the probability of extinction is positively related to population size variation: more variation is associated with more extinction. What, then, is the relation of extinction to population size variation for a population embedded in a metapopulation and subjected to repeated extinction and recolonization? In this case, the extinction risk can be measured by the extinction rate, the frequency at which local extinction occurs. Using several population dynamics models with immigration, we find, in general, a negative correlation between extinction and variation. More precisely, with increasing length of the time series, an initially negative regression coefficient first becomes more negative, then becomes less negative, and eventually attains positive values before decreasing again to 0. This pattern holds under substantial variation in values of parameters representing species and environmental properties. It is also rather robust to census interval length and the fraction of missed individuals but fails to hold for high thresholds (population size values below which extinction is deemed to occur) when quasi extinction rather than true extinction is represented. The few departures from the initial negative correlation correspond to populations at risk: low growth rate or frequent catastrophes.

Recovery of food webs following natural physical disturbances.

The objective of our paper is to develop a mechanistic conceptual framework for how food webs recover from natural physical disturbances. We summarize our work on the effect of hurricanes on island food webs and review other studies documenting how other types of physical disturbances (including fires, floods, and volcanic eruptions) alter food-web interactions. Based on these case studies, we propose that four factors play an important role in food-web succession: (1) disturbance intensity, (2) sequential recovery/colonization of successively higher trophic levels, (3) tradeoffs between growth rate of organisms at different successional stages and susceptibility to consumers, and (4) detritus including autochthonous and allochthonous sources. Studies on river flooding and islands disturbed by hurricanes indicate that energy flow is higher and trophic cascades are stronger during recovery than when the food web is at a steady state. We suggest that as consumer species colonize during succession, they may change the species or phenotypic composition of their food supply from highly vulnerable to less vulnerable items, thereby weakening both bottom-up and top-down effects throughout the food web. High inputs of detritus caused by disturbances can amplify bottom-up effects during early succession, and subsequently alter top-down effects.

Alteration of island food-web dynamics following major disturbance by hurricanes.

Major abiotic disturbance can be an important factor influencing food-web dynamics, particularly in areas impacted by the recent increase in hurricane activity. We present a unique set of data on key food-web processes occurring on 10 small islands for three relatively calm years and then four subsequent years during which two hurricanes passed directly over the study site. Herbivory, as measured by leaf damage, was 3.2 times higher in the year after the first hurricane (2000) than in the previous year and was 1.7 times higher in the year after the second hurricane (2002) than in 2001. The effect of a top predator (the lizard, Anolis sagrei) on herbivory strengthened continuously after the first hurricane and overall was 2.4 times stronger during the disturbance period than before. Overall abundance of lizards was 30% lower during the disturbance period than before, and abundances of web spiders and hymenopteran parasitoids were 66% and 59% lower, respectively. We suggest that increased herbivory observed on all islands was caused, at least in part, by the overall reduction in predation by both lizards and arthropods, whereas magnification of the lizard effect on herbivory was caused by reduced compensatory predation by arthropods.

Marine subsidies change short-term foraging activity and habitat utilization of terrestrial lizards.

Resource pulses are brief periods of unusually high resource abundance. While population and community responses to resource pulses have been relatively well studied, how individual consumers respond to resource pulses has received less attention. Local consumers are often the first to respond to a resource pulse, and the form and timing of individual responses may influence how the effects of the pulse are transmitted throughout the community. Previous studies in Bahamian food webs have shown that detritivores associated with pulses of seaweed wrack provide an alternative prey source for lizards. When seaweed is abundant, lizards (Anolis sagrei) shift to consuming more marine-derived prey and increase in density, which has important consequences for other components of the food web. We hypothesized that the diet shift requires individuals to alter their habitat use and foraging activity and that such responses may happen very rapidly. In this study, we used recorded video observations to investigate the immediate responses of lizards to an experimental seaweed pulse. We added seaweed to five treatment plots for comparison with five control plots. Immediately after seaweed addition, lizards decreased average perch height and increased movement rate, but these effects persisted for only 2 days. To explore the short-term nature of the response, we used our field data to parametrize heuristic Markov chain models of perch height as a function of foraging state. These models suggest a "Synchronized-satiation Hypothesis," whereby lizards respond synchronously and feed quickly to satiation in the presence of a subsidy (causing an initial decrease in average perch height) and then return to the relative safety of higher perches. We suggest that the immediate responses of individual consumers to resource pulse events can provide insight into the mechanisms by which these consumers ultimately influence community-level processes.

Indirect Effects in an Experimentally Staged Invasion by a Major Predator.

We used a system of neighboring small islands with and without the lizard Anolis sagrei to stage a 7-yr experimental study of the effects of an invading species. Lizard propagules were introduced to four islands, randomly selected from eight that lacked lizards naturally. Four other islands where lizards occurred naturally constituted a third treatment. We examined possible lizard indirect effects on the commonest shrub (via its arthropod herbivores), two sizes of aerial arthropods, and hymenopteran parasitoids. Lizards reduced leaf damage; moreover, during the middle years of the experiment, damage was less on introduction islands than on islands having lizards naturally. Lizards increased the number of small aerial arthropods but had no effect on large aerial arthropods; the full effect on small arthropods was only evident near the end of the experiment. Lizard introduction increased the number of hymenopteran parasitoids at the end of the experiment; however, only islands having lizards naturally had significantly more parasitoids than no-lizard islands summed over the long term. In contrast to the indirect effects, the mostly direct effect of lizards on spiders was very strong; introduction transformed spider density to that on natural lizard islands relatively rapidly and monotonically. In addition to demonstrating how an introduced vertebrate predator can affect food webs even down to the producer level, this study illustrates the greater strength and regularity of direct as opposed to indirect effects.

Relationship between prey consumption and colony size in an orb spider.

I studied the relationship between prey consumption and colony size in the orb spiderPhiloponella semiplumosa. Observations of unmanipulated colonies showed that prey biomass per juvenile spider was positively correlated with colony size, indicating that prey consumption was highest in the largest colonies observed. In contrast, the relationship between prey biomass per adult female and colony size was curvilinear; prey consumption tended to be highest in intermediatesized colonies. Adult female cephalothorax width was positively correlated with colony size. Number of egg sacs per adult female tended to be highest in intermediate-sized colonies. Prey biomass per juvenile was lower in experimentally reduced colonies than in large control colonies. Aerial-arthropod abundance was not correlated with colony size, and experimental prey supplementation did not affect colony size. Thus, the relationship between prey consumption and colony size was influenced by coloniality directly, rather than by a correlation between prey abundance at a site and colony size.

Seasonal reversal of competitive advantage between two spider species.

To test for inter- and intraspecific competition between two common orb-weaving spiders, Metepeira grinnelli and Cyclosa turbinata, I conducted separate field experiments in the spring and summer. During the spring experiment, the prey-consumption rate of Metepeira was reduced at higher inter- and intraspecific densities, but Cyclosa was only affected by intraspecific density. During the summer experiment, Metepeira prey-consumption was not affected by inter- or intraspecific densities, while Cyclosa was affected by both inter- and intraspecific densities. In addition to competition for food, during the spring experiment Cyclosa was observed displacing Metepeira but not vice versa, whereas during the summer experiment Metepeira displaced Cyclosa but not vice versa. The seasonal reversal in the competitive advantage between the species was linked to their asynchronous phenologies; in the spring most Cyclosa were larger than Metepeira, whereas in the summer most Metepeira were larger than Cyclosa. I suggest that in this system, temporal variability in the competitive abilities may promote species coexistence.

Long-term variation in the effect of lizards on spider density is linked to rainfall.

The objective of this study was to ascertain whether the impact of lizards on spiders varies temporally, and if so, whether this variability is related to rainfall. We compared annual censuses of orb-spider populations on 24 islands with diurnal lizards present, and on 20 islands with diurnal lizards absent, to rainfall over a 10-year period. A strong positive correlation (Pearson r=0.877) was found between mean spider density on nolizard islands and the number of days of rain that occurred 2 months prior to spider censuses; correlation coefficients declined with longer and shorter time periods prior to censuses. Correlation coefficients between mean spider density on lizard islands and rainfall showed a similar pattern but were generally lower than those for no-lizard islands. The strength of the impact of lizards on spiders, measured as the ratio of mean spider density on no-lizard islands to mean spider density on lizard islands, varied considerably and was positively correlated with rainfall; the correlation was highest with number of rain days 6 months prior to spider censuses (r=0.741). Repeated-measures analysis of variance on the time series of spider densities showed that the lizard factor (present versus absent) varied significantly among years. Split-plot ANOVA with rainfall as a covariate indicated that spider density and the impact of lizards on spider density were both significantly correlated with rainfall. We discuss several hypotheses on the causal mechanisms that integrate abiotic and biotic factors.

Founder effects persist despite adaptive differentiation: a field experiment with lizards.

The extent to which random processes such as founder events contribute to evolutionary divergence is a long-standing controversy in evolutionary biology. To determine the respective contributions of founder effects and natural selection, we conducted an experiment in which brown anole (Anolis sagrei) lizard populations were established on seven small islands in the Bahamas, from male-female pairs randomly drawn from the same large-island source. These founding events generated significant among-island genetic and morphological differences that persisted throughout the course of the experiment despite all populations adapting in the predicted direction-shorter hindlimbs-in response to the narrower vegetation on the small islands. Thus, using a replicated experiment in nature, we showed that both founder effects and natural selection jointly determine trait values in these populations.