Michael S. Mooring

Animal Grouping for Protection From Parasites: Selfish Herd and Encounter-Dilution Effects

Grouping has been widely accepted as a mechanism for protection from predation. Just as has been apparent with predation, there is now ample evidence that parasites (biting flies, warble flies and parasitoids) can impact an animals individual fitness. Some aspects of grouping, namely an encounter-dilution effect and the selfish herd effect, appear to apply as much to protection of animals from flying parasites as protection from predators. The encounter-dilution effect provides protection when the probability of detection of a group does not increase in proportion to an increase in group size (the encounter effect), provided that the parasites do not offset the encounter effect by attacking more members of the group (the dilution effect). The selfish herd effect provides protection from flying parasites to animals that are in the center of a group or more closely placed to other animals. Most of the quantitative evidence for the protection from flying parasites from grouping comes from studies on ungulates. Further investigation of these effects among a variety of taxa is needed for a full appreciation of the role of parasites in animal grouping and sociality.

Biological basis of grooming behaviour in antelope: the body-size, vigilance and habitat principles

Abstract Grooming in ungulates has been shown to be very effective in removing ectoparasites. Ectoparasites, especially ticks, may be costly to an animals resources in terms of blood removed and depression of appetite. There are two opposing models that address the parasite-control of function of grooming: (1) animals may groom in response to stimulation from parasite bites, whereupon those with the most parasites should groom the most; or (2) animals may groom prophylactically, removing parasites such as ticks before they attach, as a reflection of a central programming or timing mechanism. Based on behavioural observations of Thomsons gazelle, Gazella thomsonii , Grants gazelle, Gazella granti , impala, Aepyceros melampus , and wildebeest, Cannocheates gnu , in Kenya and at the San Diego Wild Animal Park (SDWAP), both models seemed to apply to different aspects of grooming. Presumably, as a reflection of their increased vulnerability to ectoparasites through a greater body surface to mass ratio (body-size principle), Thomsons gazelle were found to groom more frequently than wildebeest. This corresponds to a reportedly smaller number of ticks per m 2 surface area in Thomsons gazelle. Territorial males groomed less frequently than conspecific females and bachelor males, presumably relfecting their need to remain vigilant over females (vigilance principle). Within-species grooming was less in a low-parasite environment (SDWAP) than in a high-parasite environment (Kenya), reflecting both a decreased exposure to parasites (habitat principle) and a decrease in programmed grooming. Impala, which typically inhabit tick-infested woodland areas, orally groomed themselves more than the size-matched Grants gazelle comparison species, and also engaged in a unique form of reciprocal allogrooming of the head and neck. That the impala allogrooming may also have a tick-removal function was supported by the finding that impala scratch-groom the head and neck less than Grants gazelle.

Grooming in Impala: Role of Oral Grooming in Removal of Ticks and Effects of Ticks in Increasing Grooming Rate

In Experiment 1, five adult female impala were fitted with harnesses that restrained oral self-grooming of the anterior part of the body. At the same time, six cohoused female impala were fitted with control harnesses that allowed normal oral grooming. The impala were allowed to habituate to the harnesses for 10 days, and both groups were then exposed to larval ticks (Boophilus decoloratus) by herding them into a tick-seeding corral. During the third week following tick seeding, when female ticks were estimated to have developed into engorging adults, the impala were immobilized, tick numbers on the animals sampled by patch sampling, and the harnesses removed. Observations continued for 5 days following removal of the harnesses. Twenty-minute focal observations were conducted daily on each impala during the habituation, tick-seeded, and postharness phases. Restrained impala had a median of 20 times more adult female ticks (both engorged and unengorged) than control impala. Oral grooming, which had been suppressed in the restrained impala during habituation and tick-seeded phases, increased 10-fold once the harnesses were removed and occurred 2.5 times more frequently than in control impala during the postharness phase. In Experiment 2, 15 adult female impala were seeded with larval ticks as in Experiment 1; in week 3 after tick seeding all ticks were removed from animals by application of an acaricide. Grooming was recorded during 3 weeks of baseline observations prior to tick seeding, 3 weeks after tick seeding, and then for 3 weeks beginning 1 week after acaricide treatment. Oral grooming and scratch grooming significantly increased from baseline during tick seeding and significantly declined following removal of the ticks with acaracide. Taken together, the two experiments demonstrate that oral grooming is very effective and important in removing fitness-compromising ticks in free-ranging impala. Correspondingly, exposure to, and subsequent infestation by, ticks increases the rate of grooming.

VIGILANCE, PREDATION RISK, AND THE ALLEE EFFECT IN DESERT BIGHORN SHEEP

Abstract Knowledge of how predation risk affects population survivorship is important for understanding predator–prey relationships and designing effective conservation strategies. The Allee effect (inverse density dependence) can be generated when antipredator strategies become inefficient in small groups of prey, thus making the population more susceptible to catastrophic population collapse and extinction. Many populations of desert bighorn sheep (Ovis canadensis) are declining, and predation is, in many cases, a major mortality factor. We studied desert bighorns at the Red Rock Wildlife Area, New Mexico, USA, to assess predation risk in different group types (ram, ewe, mixed) and age–sex classes. Multiple regression analysis revealed that predation risk (as estimated by individual vigilance) increased with smaller group size and greater inter-individual distance for all bighorns, with groups of <5 individuals subject to the greatest risk. Although rugged terrain is thought to provide refuge from predators, habitat ruggedness did not influence vigilance. The biggest males in ram groups experienced the greatest predation risk in that they were in the smallest groups, were most likely to be solitary, and were spaced farther apart from conspecifics. Although big rams spent twice as much time vigilant as other age–sex classes, collective alertness was lowest for ram groups. The conclusion that big rams were most at risk from predation was partially supported by the recent predation history of the population and previous studies in which mountain lion (Felis concolor) kills were biased toward rams. We discuss the management implications of these results for small populations subject to Allee effects, including reintroduction and/or translocation practices and selective removal of problem predators. We suggest that the use of multivariate techniques to simultaneously explore the influence of multiple factors and the use of vigilance as a correlate of predation risk would be useful management tools for assessing seasonal and class-specific vulnerability to predation.

Testing the interspecific body size principle in ungulates: the smaller they come, the harder they groom

Tick removal grooming may be centrally regulated by an internal timing mechanism operating to remove ticks before they attach and engorge (programmed grooming model) and/or evoked by cutaneous stimulation from tick bites (stimulus-driven model). The programmed grooming model predicts that organismic and environmental factors that impact the cost-benefit ratio of grooming (e.g. body size and habitat) will influence the rate of tick removal grooming. The body size principle predicts that smaller-sized animals, because of their greater surface-to-mass ratio, should engage in more frequent tick removal grooming than larger-bodied animals in order to compensate for higher costs of tick infestation. The body size principle may be tested intraspecifically between young and adult animals, or interspecifically among species of contrasting body sizes. To rigorously test the interspecific body size prediction, we observed the programmed grooming (oral and scratch grooming) of 25 species (or subspecies) of bovids at a tick-free zoological park in which stimulus-driven grooming was ruled out. Multiple correlation analysis revealed highly significant negative correlations between species-typical mass and mean species grooming rates when habitat was controlled for in the model. Species-typical habitat type (classified along a gradient from most open to most closed) was positively correlated with mean oral grooming rate, indicating that species tended to groom at a higher rate in woodland and forest habitats (where typical tick density would be high) compared with more open environments. Species mass accounted for up to two-thirds of the variation in grooming rate across species, whereas habitat accounted for ca. 20% of variation in oral grooming. Similar results were obtained when the analysis was expanded to include 36 species/subspecies of six different families. The body size principle can therefore account for a large proportion of species-typical differences in programmed grooming rate among ungulates. However, to understand the tick defence adaptations of very large mammals that rarely or never engage in oral or scratch grooming (e.g. elephants, giraffes, rhinoceros), alternative tick defence strategies must be considered, such as thick skin, wallowing, rubbing and tolerance of oxpeckers and other tick-eating birds. Copyright 2000 The Association for the Study of Animal Behaviour.

The effect of tick challenge on grooming rate by impala

Grooming is among the most commonly performed parasite defence behaviour patterns and is eVective in removing ticks. Because both tick infestation and grooming activity have a cost, natural selection should favour individuals that match the current level of tick threat with an appropriate level of tick-defence grooming eVort. To test this notion, the relationship between seasonal tick challenge and grooming rate by wild, free-ranging impala, Aepyceros melampus, was investigated in Zimbabwe. Adult ticks in the vegetation showed a dramatic decrease from the warm/wet season to the hot/dry season, declining from 2·4 ticks per drag sample and 58 ticks per removal plot to virtually nil. This decline was mirrored by an associated decline in grooming rate by all impala in which self-oral and scratch grooming bouts per h decreased 30-45%. Allogrooming encounters per h (corrected for lying-down time) and total allogrooming delivered, as measured by bouts or episodes delivered per h, decreased for males but did not change for females. Overall percentage of time spent in all forms of grooming declined 37-57%. Multiple regression analysis revealed that, with the seasonal eVects of temperature and rainfall held constant, self-grooming rates were significantly and positively correlated with adult tick challenge, indicating that impala adjusted self grooming to seasonalfluctuations in adult tick threat. Allogrooming delivered was influenced by nymphal tick challenge; because the larvae and nymphs of the most abundant tick species favour the ear and neck region (where allogrooming is concentrated), allogroom- ing appears to function to remove immature ticks from body regions inaccessible to self-oral grooming. These results are what would be expected if grooming serves to remove ticks before they can attach and engorge, and supports the view that grooming is an evolved response to the threat of excessive tick burden in the impalas natural environment. ? 1995 The Association for the Study of Animal Behaviour

Role of sex and breeding status in grooming and total tick load of impala

Abstract The role of sex and breeding status constraints on grooming behavior and tick load in impala was examined among females, bachelor males (B males), and territorial males (T males) during the breeding season in Zimbabwe. T males orally groomed themselves much less than females or B males, whereas B males orally groomed themselves at a higher rate than, but not significantly different from, females. T males never engaged in allogrooming and B males allogroomed at a low rate that was not significantly different from that of T males; all males allogroomed much less than females. There was no difference in any of the grooming measures between T males with a breeding herd in residence, and solitary T males without a breeding herd on the territory. In conjunction with a management exercise, culled impala were examined for total tick burden using the digestion method, by which all ticks (larvae, nymphs, adults) are removed and counted. For all developmental stages, females harbored the fewest number of ticks and T males supported the most; tick loads of B males were intermediate to those of females and T males. When body surface area was taken into account, T males harbored a higher density of ticks than females and B males. All sex-breeding status groups supported a higher density of ticks on the head/neck region (inaccessible to self oral grooming) compared with accessible areas of the body. The results support the programmed grooming hypothesis, which predicts that those individuals that groom most will harbor fewest ticks, in contrast to the stimulus-driven model which predicts that those that groom most will harbor the most ticks. The lower grooming rates of males versus females can be attributed to competing behavioral demands on males for vigilance and rutting behavior during the breeding season, and/or to higher testosterone levels exerting a physiological suppression of oral grooming. The higher number and density of ticks harbored by T males indicates that lowered grooming rate is a significant cost to reproductively active impala males during the breeding season.

Amplitude of bison bellows reflects male quality, physical condition and motivation

Sound amplitude (measured as sound pressure level) is an acoustical parameter that has received little attention within communication research, especially in mammals. Although difficult to measure in the field, amplitude is a potentially important parameter of sexually selected signals. In North American plains bison, Bison bison, ‘bellows’ are low, guttural vocalizations made by bulls during the breeding season in the context of male–male contests. It has been hypothesized that bison use bellow amplitude to assess males during male–male competition or female mate choice. In this study, we tested the hypothesis that amplitude is significantly related to measures of bull competitive ability (quality, condition and motivation), and thus, could function as a sexually selected signal. During peak rut over 2 years, courtship and threat behaviours were recorded daily. During observation sessions, bellow amplitude was measured as peak sound pressure levels using a sound level meter. Subsequent genetic parentage analysis determined offspring sired by males. Based on aspects of signalling and game theory, we predicted positive associations between amplitude and mating and reproductive success, dominance, physical condition, motivation to retain females, age and weight. Our results supported a positive association between amplitude and both physical condition and motivation. Conversely, the results showed a negative association between amplitude and quality, as measured by mating and reproductive success. Supporting evidence and alternative hypotheses for these results are explored. Our findings provide support for the notion that bellow amplitude could be used as a sexually selected signal to assess rival males during male–male competition.

Acoustic cues to size and quality in the vocalizations of male North American bison, Bison bison

Source-filter theory provides a framework to interpret the acoustic structure of vertebrate vocalizations in relation to biophysical production, and it predicts that specific acoustic parameters can encode information about callers. Because formant frequencies are determined by vocal tract dimensions, with longer vocal tracts producing lower formants, they can be reliable indicators of body size, as well as other important traits. In polygynous species, reliable acoustic cues to fitness-related traits are expected to be under strong sexual selection pressure through male competition and/or female choice. This study investigates whether formant frequencies of male North American bison bellow vocalizations encode information about fitness-related caller attributes. Bison exhibit male-dominance female-defence polygyny, with dominance displays involving bellows. We hypothesized that physical attributes (mass, age) would predict formants and that formants would in turn predict quality indices (dominance, copulations, offspring sired). Our results showed that heavier bulls produced lower formants and that lower formants predicted higher mating success (copulations), even when controlling for mass. Given positive associations between mating success, dominance and reproductive success (offspring sired) in bison, we conclude that bellows with lower formants reflect greater fitness in bulls. We discuss the importance of reliable acoustic cues to size and quality indices in sexual selection contexts.

Fecal androgens of bison bulls during the rut

The influence of sex hormones is a key proximate factor underlying male reproductive behavior in mammals. Effective conservation policies for the remaining purebred plains bison (Bison bison bison) herds require knowledge of the physiology underlying bison reproductive biology. We used fecal steroid analysis to characterize androgen levels in adult bison bulls before, during, and after the rut, and to examine androgen levels of bulls differing in reproductive status, age, and mating success. Fieldwork was carried out at the Fort Niobrara National Wildlife Refuge in north-central Nebraska. All adult bison in the herd were individually known by unique brands. Fecal samples were collected during 2003 from bulls during pre-rut (June), rut (July-August), and post-rut (September), and behavioral observations focused on reproductive status and mating success during the rut. Matched sample data indicated that androgen levels (ng/g feces) of bulls peaked during the rut, doubling from pre-rut to rut and then declining by 75% during post-rut. Dominant bulls that tended (guarded) cows maintained higher androgen levels than bulls that were not tending. There was a positive correlation between bull age (associated with mating success) and androgens, with higher androgen levels in prime-aged bulls compared with younger bulls. Nonetheless, there was no correlation between mating success (measured by number of copulations observed) and androgen level. This suggests that while androgens may provide the proximate motivation to compete for matings, other factors determine the mating success of bison bulls.