David A. Spiller

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.

Effects of Top and Intermediate Predators in a Terrestrial Food Web

To determine the effects of lizards and web spiders on species in lower trophic levels, we manipulated their abundances within large field enclosures on Staniel Cay, Bahamas, from May 1989 to March 1992. The experimental design (2 x 2 factorial) measured the separate effects of lizards and spiders and compensatory predation (lizard x spider interaction). In treatments where web spiders were unaltered, mean number of web spider individuals was 1.4 times higher in enclosures with lizards removed than in those with lizards present at natural densities. Total biomass of aerial arthropods caught in sticky traps was 1.4 times higher in treatments with web spiders removed than in treatments with web spiders unaltered. Lizards had no significant effect on aerial arthropods. Total amount of herbivore damage on sea grape leaves was 3.3 times higher in treatments with lizards removed than in treatments with lizards unaltered. Web spiders had no significant effect on leaf damage. The lizard x spider interaction was not significant in each analysis, in- dicating that compensatory predation was weak. Our results support a model in which the interaction between top predators (lizards) and herbivores is strong, whereas the interaction between intermediate predators (web spiders) and herbivores is weak. Consequently, the net effect of top predators on producers is positive.

IS EXTINCTION RATE RELATED TO TEMPORAL VARIABILITY IN POPULATION SIZE? AN EMPIRICAL ANSWER FOR ORB SPIDERS

This study investigates the relationship between extinction rate and temporal variability in population size for 174 populations of seven orb spider species on 106 subtropical islands. Evidence for all population time series with at least two nonzero values supports either a negative (inverse) relationship or no relationship at all; this result is robust over a wide variety of statistical treatments. This perhaps unexpected result can be interpreted mainly as reflecting the inability of populations frequently going extinct ever to achieve large enough population sizes to attain even large relative variances (such as coefficient of variation), as well as reflecting the very erratic trajectories of boom-and-bust-type populations that seldom reach resource carrying capacities. Removal of zero counts from time series is also probably involved, and skewness of population-size values may have an effect as well. One type of data preparation, however-that including zero values of the population series and using arithmetic means and coefficients of variation-shows the opposite trend. Measures of temporal variability, coefficients of variation or standard deviations of log population sizes, are usually positively related to mean population size; the second derivative of this relationship is usually negative. Relation of extinction rate to mean population size is in all cases negative and highly significantly so; the second derivative of this relationship is usually positive. The latter relation is usually stronger than those involving variability, but taking into account relations with means in multiple regression still leaves a fair number of significantly negative relations of extinction rate to variability. Populations showing low temporal variabilities are mainly of two kinds: small populations with moderate to high extinction rates and large populations with low extinction rates. Thus, when only series with mean population size greater than or equal to eight are analyzed, the relation between extinction rate and temporal variability is, if anything, mildly positive. The entire analysis illustrates the great sensitivity of conclusions to seemingly biologically arbitrary conventions with respect to selection and transformation of data.

Rapid Temporal Reversal in Predator-driven Natural Selection

As the environment changes, will species be able to adapt? By conducting experiments in natural environments, biologists can study how evolutionary processes such as natural selection operate through time. We predicted that the introduction of a terrestrial predator would first select for longer-legged lizards, which are faster, but as the lizards shifted onto high twigs to avoid the predator, selection would reverse toward favoring the shorter-legged individuals better able to locomote there. Our experimental studies on 12 islets confirmed these predictions within a single generation, thus demonstrating the rapidity with which evolutionary forces can change during times of environmental flux.

An Experimental Study of the Effect of Lizards on Web‐Spider Communities

To determine the effect of lizards on web—spider populations, we conducted an 18—mo field experiment in the Bahamas. Densities of individuals of each common spider species were about three times as high in lizard—removal enclosures as in control enclosures with lizards or in unenclosed plots with lizards; spider densities in control enclosures and unenclosed plots were nearly identical. In the most common spider species, Metepeira datona, lizards reduced juvenile and adult abundance, as well as adult female survivorship and prey consumption. Numbers of spider species were higher where lizards were removed than where they were present; hence, lizards did not promote spider species coexistence in this system. Numbers and biomasses of aerial insects caught in sticky traps were higher in lizard—removal enclosures than in controls; hence, higher spider predation on insects where lizards had been removed did not completely compensate for the lack of lizards. Comparisons between control enclosures and unenclosed plots revealed that the enclosures reduced insect numbers and biomasses. This study and others have demonstrated that lizards play a major role in structuring web—spider communities in the West Indies. Several lines of evidence indicate that predation is the major interaction between lizards and spiders, although some evidence for competition also exists.

LIZARDS REDUCE SPIDER SPECIES RICHNESS BY EXCLUDING RARE SPECIES

To assess the impact of lizards on species richness and properties of individual species of web spiders, we conducted a 4.5-yr field experiment on Staniel Cay, Exumas, Bahamas. Spider populations were censused at ∼2-mo intervals in lizard-removal enclosures and in control enclosures with lizards present at natural densities. Lizards reduced total number of individuals, species richness (number of species), and composite diversity of web spiders. The differential absence of rare species was primarily responsible for the lower species richness in controls than in lizard-removal enclosures. The impact of lizards on the abundance of Metepeira datona, the numerically dominant spider species, was weaker than the impact on the abundance of all rarer species combined. Mean body lengths of Argiope argentata, a large, rare spider, were larger in removals than in controls, whereas mean body lengths of M. datona, a small, common spider, did not differ significantly in removals and controls. A. argentata were closer to the ground than two commoner species and thereby were potentially more vulnerable to lizard predation. The present mainland-enclosure experiment and an island-introduction experiment both demonstrated the same general pattern of lizard predation: exclusion of rare spider species. However, the impact of lizards on spiders was more devastating in the island experiment. Other experimental field studies that had terrestrial animals as subjects and that separately analyzed at least all common species in a prey assemblage demonstrated that predators reduced or had no effect upon prey species diversity. Each study in which predators reduced diversity indicated that local extinction of rare species in experimental areas with predators was common.

Predators increase the risk of catastrophic extinction of prey populations

There has been considerable research on both top-down effects and on disturbances in ecological communities; however, the interaction between the two, when the disturbance is catastrophic, has rarely been examined. Predators may increase the probability of prey extinction resulting from a catastrophic disturbance both by reducing prey population size and by changing ecological traits of prey individuals such as habitat characteristics in a way that increases the vulnerability of prey species to extinction. We show that a major hurricane in the Bahamas led to the extinction of lizard populations on most islands onto which a predator had been experimentally introduced, whereas no populations became extinct on control islands. Before the hurricane, the predator had reduced prey populations to about half of those on control islands. Two months after the hurricane, we found only recently hatched individuals—apparently lizards survived the inundating storm surge only as eggs. On predator-introduction islands, those hatchling populations were a smaller fraction of pre-hurricane populations than on control islands. Egg survival allowed rapid recovery of prey populations to pre-hurricane levels on all control islands but on only a third of predator-introduction islands—the other two-thirds lost their prey populations. Thus climatic disturbance compounded by predation brought prey populations to extinction.

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.

Effect of Lizards on Spider Populations: Manipulative Reconstruction of a Natural Experiment

Which species affect one another, how intensely, and the mechanisms of those effects are crucial data for understanding how ecological communities work. Tropical islands without lizards, the major top predators, have about ten times as dense web spider populations as those with lizards; processes responsible for this effect were experimentally simulated by removing lizards from randomly selected mainland plots. Spider densities in removal plots averaged 2.5 times as high as controls. Spider survival, prey abundance, and prey consumption were all negatively affected by lizards. Contrary to most studies, predator removal caused an increase in the number of spider species.

Founder Effects Persist Despite Adaptive Differentiation: A Field Experiment with Lizards

Random and Directed Natural selection drives populations to adapt to new environments; the raw material or “founder effects” provided by the first colonizing individuals can thus have a formative influence on the populations future. Kolbe et al. (p. 1086, published online 2 February; see the cover) tested the relative contributions of selection and founder effects in Bahamian lizards. Founders were taken from an island covered in forest: These lizards had long hindlimbs for sprinting across the broad expanses of tree trunks. Long-limbed lizards were introduced to seven smaller islands covered in scrub that, before hurricane Frances in 2004 swept them away, had been populated by lizards with short hindlimbs better suited for navigating a twiggy habitat. After several generations, all the new lizard populations had adapted to their new habitats by evolving shorter hindlimbs but they also retained other morphological and genetic signatures from their founding ancestors. Thus, evolution occurs by a combination of arbitrary events, as well as those shaped by selection. Introduced populations of anoles retain characteristics of their founders and acquire adaptations to their new environment. 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.