Field Studies Rick A. Relyea Department of Biological Sciences, University of Pittsburgh.
Ecologists have long appreciated the influence of predation on natural selection. Predators select prey based on their sizes and shapes, thereby acting as a form of natural selection that alters the range of phenotypes within the population. In doing so, predators alter the genetic composition of the population (gene pool), which determines the range of phenotypes in future generations. Through this process, many of the mechanisms of predator avoidance discussed in Section 14.10 are selected for in prey populations. In recent years, however, ecologists have discovered that predators can have a much broader influence on the characteristics of prey species through nonlethal effects. For example, presence of a predator can change the behavior of prey, causing them to reduce activity (or hide) to avoid being detected. This change in behavior can reduce foraging activity. In turn, changes in the rate of food intake can influence prey growth and development, resulting in shifts in their morphology (size and shape of body). This shift in the phenotype of individual prey, induced by the presence and activity of predators, is termed induction and represents a form of phenotypic plasticity (see Section 5.4).
The discovery that predators can influence the characteristics (phenotype) of prey species through natural selection and induction presents a much more complex picture of the role of predation in evolution. Although ecologists are beginning to understand how natural selection and induction function separately, little is known about how these two processes interact to determine the observed range of phenotypes within a prey population. Thanks to the work of ecologist Rick Relyea, however, this picture is becoming much clearer.
Relyea’s research is conducted in wading pools that are constructed to serve as experimental ponds. In one series of experiments, Relyea explored the nature of induced changes in behavior and morphology in prey (gray tree frog tadpoles, Hyla versicolor) by introducing caged predators (dragonfly larvae, Anax longipes) into the experimental ponds (Figure 1). The tadpoles can detect waterborne chemicals produced by the predators, allowing Relyea to simulate the threat of predation to induce changes in the tadpoles while preventing actual predation. By comparing the characteristics of tadpoles in control ponds (no predator present) and in ponds with caged predators, he was able to examine the responses induced by the presence of predators.
Results of the experiments reveal that induction by predatory chemical cues altered the tadpoles’ behavior. They became less active in the presence of predators (Figure 2). Reduced activity makes prey less likely to encounter predators and improves their probability of survival. The predators’ presence also induced a shift in the morphology of tadpoles—a form of phenotypic plasticity. Tadpoles raised in the experimental ponds in which predators were present have a greater tail depth and shorter overall body length than do individuals raised in the absence of predators (control ponds; Figure 3). Interestingly, previous studies showed that tadpoles with deeper tails and shorter bodies escape dragonfly predators better than tadpoles with the opposite morphology. Therefore, the induced morphological responses that were observed in Relyea’s experiments are adaptive; they are a form of phenotypic plasticity that functions to increase the survival of individual tadpoles. To assess the heritability of traits and trait plasticities, Relyea conducted artificial crosses of adults, reared their progeny in predator and no-predator environments, and then quantified tadpole behavior (activity), morphology (body and tail shape), and life history (mass and development). Results of the study found that predator-induced traits were heritable, however, the magnitude of heritability varied across traits and environments. Interestingly, several traits had significant heritability for plasticity, suggesting a potential for selection to act on phenotypic plasticity per se. Relyea’s experiments clearly show that predators can induce changes in prey phenotype and that the induced changes are heritable and result from natural selection.
The experiments discussed here focus on only one life stage in the development of the tree frog: the larval (tadpole) stage. But how might these changes in morphology early in development affect traits later in life? As the tadpoles metamorphose into adult frogs, they have drastically different morphologies and occupy different habitats. To answer this question, Relyea conducted an experiment to examine how differences in the morphology of wood frog tadpoles (Rana sylvatica), induced by the presence of predators, subsequently affected the morphology of the adult frog later in development.
As in previous experiments, tadpoles reared with caged predators developed relatively deeper tail fins and had shorter bodies, lower mass, and longer developmental times than did tadpoles reared without predators. Adult frogs that emerged from the tadpoles exposed to predators (and exhibiting these induced changes during the larval stage) exhibited no differences in mass but developed relatively large hindlimbs and forelimbs and narrower bodies as compared to individuals emerging from environments where predators were absent (Figure 4). These results clearly show that predator-induced shifts in traits early in development can subsequently alter traits later in development.
Plants respond to defoliation with a flush of new growth that drains nutrients from reserves that otherwise would go to growth and reproduction. For example, Anurag Agrawal of the University of Toronto found that herbivory by longhorn beetles (Tetraopes spp.) reduced fruit production and mass of milkweed plants (Asclepias spp.) by as much as 20–30 percent.
If defoliation of trees is complete (Figure 14.22a), as often happens during an outbreak of gypsy moths (Lymantria dispar) or fall cankerworms (Alsophila pometaria), leaves that regrow in their place are often quite different in form. The leaves are often smaller, and the total canopy (area of leaves) may be reduced by as much as 30–60 percent. In addition, the plant uses stored reserves to maintain living tissue until new leaves form, reducing reserves that it will require later. Regrown twigs and tissues are often immature at the onset of cold weather, reducing their ability to tolerate winter temperatures. Such weakened trees are more vulnerable to insects and disease. In contrast to deciduous tree species, defoliation kills coniferous species.
Browsing animals such as deer, rabbits, and mice selectively feed on the soft, nutrient-rich growing tips (apical meristems) of woody plants, often killing the plants or changing their growth form. Burrowing insects, like the bark beetles, bore through the bark and construct egg galleries in the phloem–cambium tissues. In addition to phloem damage caused by larval and adult feeding, some bark beetle species carry and introduce a blue stain fungus to a tree that colonizes sapwood and disrupts water flow to the tree crown, hastening tree death.
Some herbivores, such as aphids, do not consume tissue directly but tap plant juices instead, especially in new growth and young leaves. Sap-sucking insects can decrease growth rates and biomass of woody plants by as much as 25 percent.
Grasses have their meristems, the source of new growth, close to the ground. As a result, grazers first eat the older tissue and leave intact the younger tissue with its higher nutrient concentration. Therefore, grasses are generally tolerant of grazing, and up to a point, most benefit from it. The photosynthetic rate of leaves declines with leaf age. Grazing stimulates production by removing older tissue functioning at a lower rate of photosynthesis, increasing the light availability to underlying young leaves. Some grasses can maintain their vigor only under the pressure of grazing, even though defoliation reduces sexual reproduction. Not all grasses, however, tolerate grazing. Species with vulnerable meristems or storage organs can be quickly eradicated under heavy grazing.
