The effects of predator odors in mammalian prey species: A review of field and laboratory studies

wPrey species show specific adaptations that allow recognition, avoidance and defense against predators. For many mammalian species this includes sensitivity towards predator-derived odors. The typical sources of such odors include predator skin and fur, urine, feces and anal gland secretions. Avoidance of predator odors has been observed in many mammalian prey species including rats, mice, voles, deer, rabbits, gophers, hedgehogs, possums and sheep. Field and laboratory studies show that predator odors have distinctive behavioral effects which include (1) inhibition of activity, (2) suppression of non-defensive behaviors such as foraging, feeding and grooming, and (3) shifts to habitats or secure locations where such odors are not present. The repellent effect of predator odors in the field may sometimes be of practical use in the protection of crops and natural resources, although not all attempts at this have been successful. The failure of some studies to obtain repellent effects with predator odors may relate to (1) mismatches between the predator odors and prey species employed, (2) strain and individual differences in sensitivity to predator odors, and (3) the use of predator odors that have low efficacy. In this regard, a small number of recent studies have suggested that skin and fur-derived predator odors may have a more profound lasting effect on prey species than those derived from urine or feces. Predator odors can have powerful effects on the endocrine system including a suppression of testosterone and increased levels of stress hormones such as corticosterone and ACTH. Inhibitory effects of predator odors on reproductive behavior have been demonstrated, and these are particularly prevalent in female rodent species. Pregnant female rodents exposed to predator odors may give birth to smaller litters while exposure to predator odors during early life can hinder normal development. Recent research is starting to uncover the neural circuitry activated by predator odors, leading to hypotheses about how such activation leads to observable effects on reproduction, foraging and feeding. (c) 2005 Elsevier Ltd. All rights reserved.

The response of native Australian rodents to predator odours varies seasonally: a by-product of life history variation?

Small mammals are subject to predation from mammalian, avian and reptilian predators. There is an obvious advantage for prey species to detect the presence of predators in their environment, enabling them to make decisions about movement and foraging behaviour based on perceived risk of predation. We examined the effect of faecal odours from marsupial and eutherian predators, and a native reptilian predator, on the behaviour of three endemic Australian rodent species (the fawn-footed melomys, Melomys cervinipes, the bush rat, Rattus fuscipes, and the giant white-tailed rat, Uromys caudimaculatus) in rainforest remnants on the Atherton Tableland, North Queensland, Australia. Infrared camera traps were used to assess visit rates of rodents to odour stations containing faecal and control odours. Rodents avoided odour stations containing predator faeces, but did not avoid herbivore or control odours. The responses of the three prey species differed: in the late wet season U. caudimaculatus avoided predator odours, whereas R. fuscipes and M. cervinipes did not. In contrast, in the late dry season all three species avoided odour stations containing predator odours. We speculate that these different responses may result from variation in life history traits between the species. (c) 2006 The Association for the Study of Animal Behaviour Published by Elsevier Ltd. All rights reserved.

Habitat-predator association and avoidance in rainbowfish (Melanotaenia spp.)

The ability to recall the location of a predator and later avoid it was tested in nine populations of rainbowfish (Melanotaenia spp.), representing three species from a variety of environments. Following the introduction of a model predator into a particular microhabitat, the model was removed, the arena rotated and the distribution of the fish recorded again. In this manner it could be determined what cues the fish relied on in order to recall the previous location of the predator model. Fish from all populations but one (Dirran Creek) were capable of avoiding the predator by remembering either the location and/or the microhabitat in which the predator was recently observed. Reliance on different types of visual cues appears to vary between populations but the reason for this variation remains elusive. Of the ecological variables tested (flow variability, predator density and habitat complexity), only the level of predation appeared to be correlated with the orientation technique employed by each population. There was no effect of species identity, which suggests that the habitat that each population occupies plays a strong role in the development of both predator avoidance responses and the cues used to track predators in the wild.

Predator-mediated phenotypic plasticity in tadpoles of the striped marsh frog, Limnodynastes peronii

We tested the phenotypic responses of larval striped marsh frogs (Limnodynastes peronii) to the odonate nymph predator, Aeshna brevistyla. When reared in the presence of dragonfly nymphs feeding upon conspecifics of L. peronii larvae the tadpoles showed a strong change in morphology. Morphological changes included an increase in total tail height, but also an unexpected marked change in head-body shape. In addition, we examined how tadpole development, as well as mass and length at metamorphosis, was affected by exposure to dragonfly nymphs. Larval development of L. peronii was strongly influenced by exposure to the predatory behaviour of dragonfly nymphs. Predator-induced tadpoles had significantly slower developmental rates than control larvae. Although metamorphs of non-exposed L. peronii were approximately 33% lighter than predator-exposed metamorphs and possessed lower jump distances, after adjusting for mass there was no difference in jump distance. The newly described morphological response may assist in more accurately relating morphological plasticity to fitness.

Predator-specific changes in the morphology and swimming performance of larval Rana lessonae

1. We investigated the morphological responses of larval Rana lessonae to the presence of two predators with substantially different prey-detection and capture techniques; larval dragonflies (Aeshna cyanea) and the Pumpkinseed Sunfish (Lepomis gibossus). 2. We also examined the functional implications of any predator-induced morphological variation on their swimming ability by assessing performance during the initial stages of a startle response. 3. We found the morphological responses of larval R. lessonae were dependent on the specific predator present. Tadpoles raised in the presence of dragonfly larvae preying upon conspecific tadpoles developed total tail heights 5.4% deeper and tail muscles 4.7% shallower than tadpoles raised in a non-predator environment, while tadpoles raised with sunfish possessed tails 2% shallower and tail muscles 2.5% higher than non-predator-exposed tadpoles. 4. Predator-induced morphological variation also significantly influenced swimming performance. Tadpoles raised with sunfish possessed swimming speeds 9.5 and 14.6% higher than non- and dragonfly predator groups, respectively. 5. Thus, the expression of these alternative predator-morphs leads to a functional trade-off in performance between the different environments.

Predator-induced phenotypic plasticity in tadpoles: extension or innovation?

Phenotypic plasticity, the ability of a trait to change as a function of the environment, is central to many ideas in evolutionary biology. A special case of phenotypic plasticity observed in many organisms is mediated by their natural predators. Here, we used a predator-prey system of dragonfly larvae and tadpoles to determine if predator-mediated phenotypic plasticity provides a novel way of surviving in the presence of predators (an innovation) or if it represents a simple extension of the way noninduced tadpoles survive predation. Tadpoles of Limnodynastes peronii were raised in the presence and absence of predation, which then entered a survival experiment. Induced morphological traits, primarily tail height and tail muscle height, were found to be under selection, indicating that predator-mediated phenotypic plasticity may be adaptive. Although predator-induced animals survived better, the multivariate linear selection gradients were similar between the two tadpole groups, suggesting that predator-mediated phenotypic plasticity is an extension of existing survival strategies. In addition, nonlinear selection gradients indicated a cost of predator-induced plasticity that may limit the ability of phenotypic plasticity to enhance survival in the presence of predators.

Encounter success of free-ranging marine predator movements across a dynamic prey landscape

Movements of wide-ranging top predators can now be studied effectively using satellite and archival telemetry. However, the motivations underlying movements remain difficult to determine because trajectories are seldom related to key biological gradients, such as changing prey distributions. Here, we use a dynamic prey landscape of zooplankton biomass in the north-east Atlantic Ocean to examine active habitat selection in the plankton-feeding basking shark Cetorhinus maximus. The relative success of shark searches across this landscape was examined by comparing prey biomass encountered by sharks with encounters by random-walk simulations of ‘model’ sharks. Movements of transmitter-tagged sharks monitored for 964 days (16754km estimated minimum distance) were concentrated on the European continental shelf in areas characterized by high seasonal productivity and complex prey distributions. We show movements by adult and sub-adult sharks yielded consistently higher prey encounter rates than 90% of random-walk simulations. Behavioural patterns were consistent with basking sharks using search tactics structured across multiple scales to exploit the richest prey areas available in preferred habitats. Simple behavioural rules based on learned responses to previously encountered prey distributions may explain the high performances. This study highlights how dynamic prey landscapes enable active habitat selection in large predators to be investigated from a trophic perspective, an approach that may inform conservation by identifying critical habitat of vulnerable species.

A late Pleistocene predator-accumulated avifauna from Kids Cave, West Coast, South Island, New Zealand

A fossil deposit excavated from the floor of Kids Cave, West Coast, South Island, New Zealand, is interpreted as having been primarily accumulated by New Zealand falcon Falco novaeseelandiae, with some contribution by Haast's eagle Harpagornis moorei. The fauna is rich: 3699 bones represented 41 bird species, two frog species, unspecified geckoes and skinks, and one bat species. Fossil deposition was mainly within the Last Glacial Maximum from about 22,000 cal yr bp to about 15,000 cal yr bp, with a marked change in sediment characteristics at the onset of the LGM's coldest period. Chronological control is given by three Uranium-series dates for a speleothem and radiocarbon AMS dating of four avian eggshell samples and one bone. The fauna is the first extensive predator accumulation of LGM age described from the West Coast of the South Island, and it indicates a palaeoenvironment of a mosaic of shrublands with forest patches. The onset of the coldest part of the LGM (Aurora 3 glacial advance, 19,500 - 19,000 cal yrs bp) saw marked climate cooling/drying affecting the site, but the avifauna indicates that although open-country taxa became more common in this period, some forest persisted nearby throughout the remainder of the LGM.

Observations on the diet and feeding habits of the epaulette shark, Hemiscyllium ocellatum (Bonnaterre), on Heron Island Reef, Great Barrier Reef, Australia

The diet and feeding habits of the epaulette shark, Hemiscyllium ocellatum, were investigated through stomach content analysis. Five groups of prey items were found. The index of relative importance showed worms and crabs,to be of greatest value at 51.3% and 40.1% respectively. The three minor prey groups were shrimps (7.7%), small fishes (0.7%) and amphipods (0.3%). Epaulette sharks tend to be crepuscular, although feeding bouts may occur at any time. They appear to be opportunistic predators, using olfaction and electroreception in prey capture. This species appears to be an important benthic predator in the reef flat environment on Heron Island Reef.

Bird responses at inherent and induced edges in the Murray Mallee, South Australia. 2. Nest predation as an edge effect

We assayed nest predation as an edge effect, using artificial ground nests, at inherent (naturally occurring) and induced (human-created) edges, in the Murray Mallee, South Australia. Nests were constructed at distances between 0-120 m away from habitat edges. The relative predation rate on nests generally increased close to induced edges with a significant difference (P < 0.05) recorded for two out of five experiments. Predation rate at inherent edges was similar from the edge to the interior, and was lower than that recorded at induced edges. Our results suggest that increased predator numbers, activity or efficiency at locating nests occurred close to the induced edges at our study sites.