Bradley R. Anholt

Interaction Between Food Availability and Predation Mortality Mediated by Adaptive Behavior

Increased activity rates in larval anurans rates are associated with both higher growth rates and higher predation mortality. Models of adaptive foraging behavior in the face of predation risk predict that at higher resource levels, foraging activity should be reduced. Thus, at higher resource levels predation mortality should also be reduced. We manipulated the resources available to Rana catesbeiana tadpoles and then measured the activity of tadpoles in the presence of caged dragonfly larvae and the mortality rate of the tadpoles when the dragonflies were free to forage. At low food levels the tadpoles moved more often and more quickly. Similarly, at low food levels the tadpoles suffered higher predation mortality. The dependence of predation mortality on resources available to prey underlines the futility of characterizing population regulation as being due to predation or resources. Adaptive variation in behavior responds to both pressures simultaneously. These results suggest the possibility that adaptive variation in behavior may lead to density—dependent population regulation. Density—dependent depletion of resources by prey should lead to increased activity levels, which will result in higher per capita predation rates. The generality of the trade—off between growth rate and mortality rate argues that this mechanism may be widespread. If adaptive variation in behavior is as widespread as it appears, incorporating this variation into population dynamic modelling may improve our ability to predict the outcome of interactions within ecological communities.

Predator-Induced Behavioral Indirect Effects: Consequences to Competitive Interactions in Anuran Larvae

This study examines the non-lethal effects of an odonate predator (Anax junius) on the competitive interactions among several size classes of anuran larvae. In an outdoor experiment using cattle watering tanks, we estimated the effects of both large and small bullfrogs (Rana catesbeiana) on themselves, on each other, and on small green frogs (R. clamitans) in the absence and non-lethal (caged) presence of Anax. The presence of Anax depressed both growth and survivorship of small bullfrogs and green frogs. In contrast, the presence of Anax had positive effects on growth rates and size at metamorphosis of the large bullfrogs. Increasing density of competitors also decreased survivorship of small classes, and growth rates of all classes. The per-unit-biomass competitive effects of the small bullfrogs on target classes were much greater than those of large bullfrogs. The presence of Anax significantly altered the per-unit-biomass competitive effects of small bullfrogs but not large bullfrogs, presumably because individuals in the small class reduced their activity rates in the presence of Anax. Overall production of new tadpole biomass was quite similar across experimental units, with decreases in production of small size classes in the presence of Anax compensated for by increases in production of the large size class. Thus the non-lethal presence of Anax had substantial effects on the nature of competitive interactions in this system, and we discuss the implications of such behavioral indirect effects in the study of ecological communities. Our results also illustrate the futility-of attempting to partition the effects of competitors and predators, as both competitors and the non-lethal presence of predators significantly affected growth rates and death by star- vation of small larvae. Finally, our results illustrate how individual behavioral responses may be translated to community and ecosystem properties.

Measuring selection on a population of damselflies with a manipulated phenotype

The estimation of the relationship between phenotype and fitness in natural populations is constrained by the distribution of phenotypes available for selection to act on. Because selection is blind to the underlying genotype, a more variable phenotypic distribution created by using environmental effects can be used to enhance the power of a selection study. I measured selection on a population of adult damselflies (Enallagma boreale) whose phenotype had been modified by raising the larvae under various levels of food availability and density. Selection on body size (combination of skeletal and mass at emergence) and date of emergence was estimated in two consecutive episodes. The first episode was survival from emergence to sexual maturity and the second was reproductive success after attaining sexual maturity. Female survival to sexual maturity was lower, and therefore opportunity for selection greater, than males in both years. Opportunity for selection due to reproductive success was greater for males. The total opportunity for selection was greater for males one year and for females the other. Survival to sexual maturity was related to mass gain between emergence and sexual maturity. Females gained more mass and survived less well than males in both years but there was no linear relationship between size at emergence and survival for females in either year. However, females in the tails of the phenotype distribution were less likely to survive than those near the mean. In contrast, small males consistently gained more mass than large males and survived less well in one year. There was significant selection on timing of emergence in both years, but the direction of selection changed due to differences in weather; early emerging females were more successful one year and late emerging males and females the other. The number of clutches laid by females was independent of body size. Because the resources used to produce eggs are acquired after emergence and this was independent of size at emergence, female fitness did not increase with size. Small males may have had lower survival to sexual maturity but they had higher mating success than large males. Resources acquired prior to sexual maturity are essential for reproductive success and may in some species alter their success in inter‐ and intrasexual competition. Therefore, ignoring the mortality associated with resource acquisition will give an incomplete and potentially misleading picture of selection on the phenotype.

Density Dependence Resolves the Stream Drift Paradox

The downstream displacement of individuals by drifting in the current is a prominent feature in the population biology of stream invertebrates. To compensate for the loss of individuals it has been proposed that adults of aquatic insects preferentially fly upstream to oviposit and thereby maintain populations. The observation of adult flight biased in the upstream direction has been advanced as confirmation of the hypothesis. I argue here that upstream-biased dispersal is not sufficient for population persistence nor is it necessary. Population persistence can only be explained on the basis of density depen- dence at some point in the life cycle. Computer simulations showed that density dependence by itself is not sufficient for population persistence. Infrequent dispersal by randomly flying adults coupled with density dependence does allow population persistence. Upstream-biased dispersal can be explained by increased individual fitness. If upstream reaches are depopulated by drift, these reaches provide more rapid growth to successful colonists. Computer simulations of competition for space by two genotypes that differ only in the directionality of dispersal showed that genotypes with upstream-biased dispersal always drove random dispersers to extinction.

MATRIX MODEL INVESTIGATION OF INVASIVE SPECIES CONTROL: BULLFROGS ON VANCOUVER ISLAND

Invasive species control is now a conservation priority in many parts of the world. Demographic modeling using population matrix models is a useful tool in the design of these control efforts as it identifies the life stages with the strongest influence on pop- ulation dynamics. As a case in point, American bullfrogs (Rana catesbeiana) have been introduced around the world and have negative effects on native fauna. We studied de- mography of four populations on southern Vancouver Island, Canada, using field obser- vations and capture-mark-recapture methods to estimate survival, growth, and fecundity. The life cycle of these introduced bullfrogs progressed in yearly increments through the following stages: eggs/small tadpoles, first-year tadpoles, second-year tadpoles, meta- morphs/juveniles, and adults. Some bullfrog tadpoles were able to skip the second-year tadpole stage and metamorphosed one year after hatching. With tadpole survival estimates from the literature and field estimates of the remaining parameters we constructed a matrix population model. Prospective demographic perturbation analysis showed that bullfrog population growth rate ( l) was most influenced by the proportion of tadpoles metamor- phosing early (tadpole development rate), and by early postmetamorphic survival rates. Most current control efforts for bullfrogs have focused on removing tadpoles and breeding adults, and our modeling suggests that these efforts may not be optimal. Partial removal of tadpoles may lead to higher tadpole survival and development rates and higher postmeta- morphic survival due to decreased density-dependent competition. Removal of adults leads to higher survival of early metamorphic stages through reduced cannibalism. Our modeling suggests that culling of metamorphs in fall is the most effective method of decreasing bullfrog population growth rate. Our study shows how demographic information can be used to maximize the efficacy of control efforts, and our results are likely directly applicable to other invasive species with complex life cycles.

Functional responses modified by predator density.

Realistic functional responses are required for accurate model predictions at the community level. However, controversy remains regarding which types of dependencies need to be included in functional response models. Several studies have shown an effect of very high predator densities on per capita predation rates, but it is unclear whether this predator dependence is also important at low predator densities. We fit integrated functional response models to predation data from 4-h experiments where we had varied both predator and prey densities. Using an information theoretic approach we show that the best-fit model includes moderate predator dependence, which was equally strong even at low predator densities. The best fits of Beddington–DeAngelis and Arditi–Akçakaya functional responses were closely followed by the fit of the Arditi–Ginzburg model. A Holling type III functional response did not describe the data well. In addition, independent behavioral observations revealed high encounter rates between predators. We quantified the number of encounters between predators and the time the focal predator spent interacting with other individuals per encounter. This time “wasted” on conspecifics reduced the total time available for foraging and may therefore account for lower predation rates at higher predator densities. Our findings imply that ecological theory needs to take realistic levels of predator dependence into account.

An Experimental Separation of Interference and Exploitative Competition in Larval Damselfly

Density-dependent reduction in survival, growth, and development rates of larval damselflies can be the result of depletion of food resources or increased interference costs (energy or time) associated with behavioral interactions. While interference has been implicated in several studies, no direct test of this hypothesis by manipulating interaction frequency or intensity has been attempted. To separate these mechanisms, I simultaneously manipulated habitat complexity (number of perches) to alter the frequency of behavioral interactions, larval density, and food supply. Damselflies became more evenly distributed among available perches as the density per perch increased, demonstrating that there were behavioral responses to the manipulation of habitat complexity. Food supply and damselfly density strongly affected survival, timing of emergence, and mass at emergence. However, the proportion of the variation in these performance variables attributable to the habitat complexity manipulation was tiny. In spite of the overt nature of the interactions among individuals, the costs appear to be very low. Future work that implicates behavioral mech- anisms in population processes will have to attempt more direct manipulations of the behavior itself to test the hypothesis before concluding that behavior is the cause of an observed pattern.

OVERWINTER SURVIVAL OF RANA LESSONAE AND ITS HEMICLONAL ASSOCIATE RANA ESCULENTA

In central Europe, the hybridogenetic water frog Rana esculenta is a sexual parasite that only persists in the presence of the parental species, R. lessonae, with which it must mate in order to reproduce. R. esculenta is a superior larval competitor, and adult females are about three times more fecund than R. lessonae. This suggests that, in the absence of some balancing advantage to R. lessonae, R. esculenta should drive the parental species locally extinct, closely followed by itself. We measured annual survival rates over six years at two widely separated ponds using modern capture–mark–recapture methods to test whether differences in adult survival might contribute to the persistence of the water frog system. We marked 856 adult frogs and recovered 182 at least once. The data did not deviate significantly from the assumptions of the Cormack-Jolly-Seber model at either pond. There were no detectable differences in recapture probabilities between taxa, but females were, overall, less likely to be recaptured. Survival was higher for R. esculenta in all but one year. Therefore, some mechanism other than adult survival must be invoked to explain the persistence of this unusual breeding system. There was considerable year-to-year variation in survival, ranging from 6% over the winter of 1996–1997, to 98% over the winter of 1995–1996. Although the two ponds are separated by 35 km, pond identity did not contribute to the minimum models. A composite measure of winter severity constructed from a principal components analysis of weather data during the course of the study had a very close relationship with survival (R. lessonae, r = 0.905; R. esculenta, r = 0.889). Survival was lowest in winters with low minimum temperatures coupled with high and variable maximum temperatures. Corresponding Editor: B. Sinervo.

SPECIES DIVERSITY MODULATES PREDATION

Predation occurs in a context defined by both prey and non-prey species. At present it is largely unknown how species diversity in general, and species that are not included in a predators diet in particular, modify predator-prey interactions. Therefore we studied how both the density and diversity of non-prey species modified predation rates in experimental microcosms. We found that even a low density of a single nonprey species depressed the asymptote of a predators functional response. Increases in the density and diversity of non-prey species further reduced predation rates to very low levels. Controls showed that this diversity effect was not due to the identity of any of the non-prey species. Our results establish that both the density and diversity of species outside a predators diet can significantly weaken the strength of predator-prey interactions. These results have major implications for ecological theory on species interactions in simple vs. complex communities. We discuss our findings in terms of the relationship between diversity and stability.

The Effect of Assortative Mating on the Coexistence of a Hybridogenetic Waterfrog and Its Sexual Host.

In central Europe, the hybridogenetic waterfrog Rana esculenta, a hybrid between Rana ridibunda and Rana lessonae, lives in sympatry with one of its parental species, the poolfrog Rana lessonae. As R. esculenta has to backcross constantly with R. lessonae in order to produce viable offspring, this coexistence is obligatory for R. esculenta. Since R. esculenta has a higher primary fitness than R. lessonae, a mechanism is required that prevents the hybrid from driving the parental species, and hence itself, to extinction. Here, we present an analytical model and a computer simulation that investigate whether assortative mating can operate as a such a control mechanism. Our results show that assortative mating is very effective in regulating coexistence in such a hybrid‐host system. This is particularly true when choice is affected by the proportion of the two male types in the population. Furthermore, we could show that even if the species composition in a mixed hybrid‐host population may be largely influenced by differences in life‐history parameters, assortative mating still plays a very important role by stabilizing coexistence. Thus, mating behavior turns out to be more important for the populations dynamics of hybridogenetic waterfrog systems than previously assumed.