Lee B. Kats

The scent of death: Chemosensory assessment of predation risk by prey animals

AbstractIt is well documented that animals take risk of predation into account when making decisions about how to behave in particular situations, often trading-off risk against opportunities for mating or acquiring energy. Such an ability implies that animals have reliable information about the risk of predation at a given place and time. Chemosensory cues are an important source of such information. They reliably reveal the presence of predators (or their presence in the immediate past) and may also provide information on predator activity level and diet. In certain circumstances (e.g., in the dark, for animals in hiding) they may be the only cues available. Although a vast literature exists on the responses of prey to predator chemosensory cues (or odours), these studies are widely scattered, from marine biology to biological control, and not well known or appreciated by behavioural ecologists. In this paper, we provide an exhaustive review of this literature, primarily in tabular form. We highlight so...

Antipredator Defenses and the Persistence of Amphibian Larvae With Fishes

Communities of larval amphibians in fishless habitats often differ strikingly from those in habitats with fish. We surveyed larvae of 15 amphibian species to determine if presence or absence of specific defenses against fish was correlated with breeding habitat. Each species was tested for two key defenses: unpalatability and chemically mediated predator avoidance. In eight of nine cases, larvae of species that often encounter fish had at least one of these defenses. In contrast, larvae of seven species that breed in fishless pools consistently lacked defenses against fish. Lack of appropriate defenses appears to be a primary reason why temporary pool species cannot successfully coexist with predatory fishes in permanent habitats. Palatability and responses to chemical cues from fish often differed among closely related taxa and were correlated strongly with frequency of encounter with fish. Thus, natural selection rather than phylogeny best explains interspecific variation in antipredator defen- ses. Our data show that members of at least two orders and four families of amphibians use chemical cues to reduce predation risk from predatory fish.

Non-visual communication in freshwater benthos: an overview

This overview of non-visual communication in freshwater benthic animals emphasizes recent studies of the effect of chemical and mechanical signals on predator-prey interactions of benthic macroinvertebrates and amphibians. Prey species use chemical signals to modify their morphological development, life history strategy, feeding, and predator avoidance behavior. The advantages of chemical signals are that they can be used in dark or turbid environments by animals that do not have image-forming eyes. Chemical signals are more persistent than mechanical signals, and they allow species-level identification of predator species. In streams, prey species may use mechanical signals (hydrodynamic pressure waves or sound) to avoid predators approaching from downstream (a situation characteristic of streams and in which chemical signals are unreliable) and to initiate escape responses. Predators often depend on chemical signals to stimulate or inhibit feeding, and they use species-specific mechanical signals to locate or track prey or potential mates. The exact nature of non-visual signals depends on ecological constraints of both the sender and receiver. Responses to non-visual signals may be adapted to local predator conditions. Non-visual signals are effectively used over a wide range of temporal and spatial scales in all aquatic habitats. Organisms often adjust their responses as ontogenic development results in changing size, diet, and habitat.

Effects of predatory sunfish on the density, drift, and refuge use of stream salamander larvae

We addressed several controversial issues regarding the impact of predatory fish on prey in natural streams in Kentucky by experimentally adding predatory green sunfish, Lepomis cyanellus, to four stream pools that contained small—mouthed salamander larvae, Ambystoma barbouri, while leaving four other pools as fishless controls. We monitored the density, drift (in and out of pools), and habitat use of the larvae before and for 1 mo after fish addition (until larvae began to undergo metamorphosis). By quantifying larval density and drift, we were able to address two issues: (1) effect of prey exchange on predator impacts; and (2) relative contribution to total predator impact of predation per se vs. predator—induced emigration. Larval densities and behaviors were similar in experimental and control pools before fish addition. After fish addition: (1) density decreased more rapidly in fish pools than in control pools; (2) larvae in fish pools spent more time under rocks and less time in deep, central areas ...

The complexity of amphibian population declines: understanding the role of cofactors in driving amphibian losses

Population losses and extinctions of species are occurring at unprecedented rates, as exemplified by declines and extinctions of amphibians worldwide. However, studies of amphibian population declines generally do not address the complexity of the phenomenon or its implications for ecological communities, focusing instead on single factors affecting particular amphibian species. We argue that the causes for amphibian population declines are complex; may differ among species, populations, and life stages within a population; and are context dependent with multiple stressors interacting to drive declines. Because amphibians are key components of communities, we emphasize the importance of investigating amphibian declines at the community level. Selection pressures over evolutionary time have molded amphibian life history characteristics, such that they may remain static even in the face of strong, recent human‐induced selection pressures.

Oviposition Site Selection and Avoidance of Fish by Streamside Salamanders (Ambystoma barbouri)

The effect of fish (Lepomis cyanellus) on distribution of egg masses of the streamside salamander (Ambsytoma barbouri) was studied in a Kentucky stream. Although adult salamanders are not vulnerable to fish, larvae are extremely vulnerable; natural selection should favor adult oviposition behavior that minimizes contact between hatchling larvae and predators. In 1987, stream pools without fish had significantly higher densities of salamander eggs than did pools with fish. Between 1987 and 1988, fish in our study pools were killed by stream drying; this created a natural experiment addressing the effects of fish presence on adult oviposition behavior. In 1988, the new fishless pools had significantly more eggs in them than they had in 1987 when they contained fish. In contrast, a comparison of 1987 fishless pools with these same pools in 1988 did not show a similar increase in egg densities. Complete stream surveys in 1987 and 1988 indicated that fishless pools contained significantly greater densities of eggs and egg masses than did riffles or runs. Thus, pools without fish appear to be the preferred stream habitat for adult salamander oviposition. Competition for oviposition sites (rocks) did not appear to influence any of the comparisons. Because eggs are deposited such that fish cannot feed on them, our field surveys of egg masses suggest that selective oviposition by female streamside salamanders facilitates streamwide fish-salamander coexistence.

Aquatic invasive species: challenges for the future

Humans have effectively transported thousands of species around the globe and, with accelerated trade; the rate of introductions has increased over time. Aquatic ecosystems seem at particular risk from invasive species because of threats to biodiversity and human needs for water resources. Here, we review some known aspects of aquatic invasive species (AIS) and explore several new questions. We describe impacts of AIS, factors limiting their dispersal, and the role that humans play in transporting AIS. We also review the characteristics of species that should be the greatest threat for future invasions, including those that pave the way for invasions by other species (“invasional meltdown”). Susceptible aquatic communities, such as reservoirs, may serve as stepping stones for invasions of new landscapes. Some microbes disperse long distance, infect new hosts and grow in the external aquatic medium, a process that has consequences for human health. We also discuss the interaction between species invasions and other human impacts (climate change, landscape conversion), as well as the possible connection of invasions with regime shifts in lakes. Since many invaders become permanent features of the environment, we discuss how humans live with invasive species, and conclude with questions for future research.

Ontogenetic Changes in California Newts (Taricha torosa) in Response to Chemical Cues from Conspecific Predators

Many species of aquatic animals rely on chemical cues to assess the risk of predation. Although amphibians are known to have adaptations to avoid predatory fish, little is known about their adaptations that allow them to co-occur with other aquatic vertebrate and invertebrate predators. Adult California newts (Taricha torosa) prey on egg masses and larvae of conspecifics. Larvae use chemical cues to assess the risk of cannibalism. Laboratory studies showed that larvae that are two weeks post-hatching hid in response to chemical cues from adults. Larvae five weeks post-hatching did not respond to conspecific cues regardless of previous exposure to adult cues. Field surveys supported the prediction that small larvae would use refuges more than larvae that are only slightly older. Surveys of natural stream pools showed that newt larvae spent more time in refuge early in the summer than they did later in the summer. This behavioral shift also corresponds to the time of year when adults leave the streams and return to land. Thus, newt larvae showed an abrupt ontogenetic change in their response to conspecific chemical cues. Reduced sensitivity to conspecific risk suggests that large newt larvae are less vulnerable to conspecific adults than small larvae.

MODIFIED INTERACTIONS BETWEEN SALAMANDER LIFE STAGES CAUSED BY WILDFIRE-INDUCED SEDIMENTATION

A 1993 wildfire and subsequent landslides modified many streams in the Santa Monica Mountains of southern California (USA). Prior to the fire at Cold Creek Canyon, adult California newts (Taricha torosa) frequently preyed on conspecific eggs and larvae. Post-fire landslides increased the number of stream pools containing terrestrial earthworms. Earthworms were more common in adult newt diets after the fire, and conspecifics were absent. More earthworms and fewer conspecifics were present in the stomachs of adult newts in streams at burned sites than at unburned sites. In laboratory experiments, newt larvae used refuges significantly less in the presence of combined chemical cues from both newt adults and earthworms as compared to adult-newt cues alone. These data suggest that cannibalism is reduced in the presence of increased alternative prey items and that larvae can detect this reduced predation risk.

THE SCENT OF DANGER: TETRODOTOXIN (TTX) AS AN OLFACTORY CUE OF PREDATION RISK

Larvae of the California newt (Taricha torosa) exhibit striking predator-avoidance behavior, escaping to refuges in response to a chemical cue from cannibalistic adults. In laboratory flow-tank experiments, stream water collected near free-ranging adults induced hiding responses in 100% of the larvae tested. Solutions prepared by bathing adults (in field and laboratory) also evoked strong hiding behaviors. Insensitive to adult feeding status (fed or starved), and clearly not an excretory product, the chemical cue was released from adult skin (i.e., in swabs of adult backs, sides, and bellies). Tetrodotoxin (TTX) was found in skin swabs of adults and in bathwater at 1 × 10−7 mol/L using reversed-phase high-pressure liquid chromatography (HPLC). Concentrations of 1 × 10−7 to 1 × 10−9 mol/L TTX standard, and equivalent dilutions of bathwater, triggered hiding behaviors in larvae, with no subsequent sublethal toxicity. The presence of TTX-sensitive cells within larval olfactory epithelium was confirmed by beh...