Search

Herbivores that forage on chemically defended plants consume complex mixtures of plant secondary metabolites (PSMs). However, the mechanisms by which herbivores tolerate mixtures of PSMs are relatively poorly understood. As such, it remains difficult to predict how PSMs, singly or as complex mixtures, influence diet selection by herbivores. Although relative rates of detoxification of PSMs have been used to explain tolerance of PSMs by dietary specialist herbivores, few studies have used the rate of detoxification of individual PSMs to understand dietary preferences of individual herbivores for individual versus mixtures of PSMs. We coupled in vivo experiments using captive feeding trials with in vitro experiments using enzymatic detoxification assays to evaluate the dietary preferences and detoxification capacities of pygmy rabbits (Brachylagus idahoensis), dietary specialists on sagebrush (Artemisia spp.), and mountain cottontails (Sylvilagus nuttallii), dietary generalists. We compared preference for five single PSMs in sagebrush compared to a mixture containing those same five PSMs. We hypothesized that relative preference for individual PSMs would coincide with faster detoxification capacity for those PSMs by specialists and generalists. Pygmy rabbits generally showed little preference among individual PSMs compared to mixed PSMs, whereas mountain cottontails exhibited stronger preferences. Pygmy rabbits had faster detoxification capacities for all PSMs and consumed higher concentrations of individual PSMs versus a mixture than cottontails. However, detoxification capacity for an individual PSM did not generally coincide with preferences or avoidance of individual PSMs by either species. Cottontails avoided, but pygmy rabbits preferred, camphor, the PSM with the slowest detoxification rate by both species. Both species avoided β-pinene despite it having one of the fastest detoxification rate. Taken together our in vivo and in vitro results add to existing evidence that detoxification capacity is higher in dietary specialist than generalist herbivores. However, results also suggest that alternative mechanisms such as absorption and the pharmacological action of individual or mixtures of PSMs may play a role in determining preference of PSMs within herbivore species.

Understanding habitat use by animals requires understanding the simultaneous tradeoffs between food and predation risk within a landscape. Quantifying the synergy between patches that provide quality food and those that are safe from predators at a scale relevant to a foraging animal could better reveal the parameters that influence habitat selection. To understand more thoroughly how animals select habitat components, we investigated tradeoffs between diet quality and predation risk in a species endemic to sagebrush Artemisia spp. communities in North America, the pygmy rabbit Brachylagus idahoensis. This species is a rare example of a specialist herbivore that relies almost entirely on sagebrush for food and cover. We hypothesized that pygmy rabbits would forage in areas with low food risk (free of plant secondary metabolites, PSMs) and low predation risk (high concealment). However, because of relatively high tolerance to PSMs in sagebrush by pygmy rabbits, we hypothesized that they would trade off the...

Summary Small herbivores face risks of predation while foraging and are often forced to trade off food quality for safety. Life history, behaviour, and habitat of predator and prey can influence these trade‐offs. We compared how two sympatric rabbits (pygmy rabbit, Brachylagus idahoensis; mountain cottontail, Sylvilagus nuttallii) that differ in size, use of burrows, and habitat specialization in the sagebrush‐steppe of western North America respond to amount and orientation of concealment cover and proximity to burrow refuges when selecting food patches. We predicted that both rabbit species would prefer food patches that offered greater concealment and food patches that were closer to burrow refuges. However, because pygmy rabbits are small, obligate burrowers that are restricted to sagebrush habitats, we predicted that they would show stronger preferences for greater cover, orientation of concealment, and patches closer to burrow refuges. We offered two food patches to individuals of each species during three experiments that either varied in the amount of concealment cover, orientation of concealment cover, or distance from a burrow refuge. Both species preferred food patches that offered greater concealment, but pygmy rabbits generally preferred terrestrial and mountain cottontails preferred aerial concealment. Only pygmy rabbits preferred food patches closer to their burrow refuge. Different responses to concealment and proximity to burrow refuges by the two species likely reflect differences in perceived predation risks. Because terrestrial predators are able to dig for prey in burrows, animals like pygmy rabbits that rely on burrow refuges might select food patches based more on terrestrial concealment. In contrast, larger habitat generalists that do not rely on burrow refuges, like mountain cottontails, might trade off terrestrial concealment for visibility to detect approaching terrestrial predators. This study suggests that body size and evolutionary adaptations for using habitat, even in closely related species, might influence anti‐predator behaviors in prey species.

When selecting habitats, herbivores must weigh multiple risks, such as predation, starvation, toxicity, and thermal stress, forcing them to make fitness trade-offs. Here, we applied the method of paired comparisons (PC) to investigate how herbivores make trade-offs between habitat features that influence selection of food patches. The method of PC measures utility and the inverse of utility, relative risk, and makes trade-offs and indifferences explicit by forcing animals to make choices between two patches with different types of risks. Using a series of paired-choice experiments to titrate the equivalence curve and find the marginal rate of substitution for one risk over the other, we evaluated how toxin-tolerant (pygmy rabbit Brachylagus idahoensis) and fiber-tolerant (mountain cottontail rabbit Sylviagus nuttallii) herbivores differed in their hypothesized perceived risk of fiber and toxins in food. Pygmy rabbits were willing to consume nearly five times more of the toxin 1,8-cineole in their diets to avoid consuming higher levels of fiber than were mountain cottontails. Fiber posed a greater relative risk for pygmy rabbits than cottontails and cineole a greater risk for cottontails than pygmy rabbits. Our flexible modeling approach can be used to (1) quantify how animals evaluate and trade off multiple habitat attributes when the benefits and risks are difficult to quantify, and (2) integrate diverse risks that influence fitness and habitat selection into a single index of habitat value. This index potentially could be applied to landscapes to predict habitat selection across several scales.

Small mammals in habitats with strong seasonal variation in the thermal environment often exhibit physiological and behavioral adaptations for coping with thermal extremes and reducing thermoregulatory costs. Burrows are especially important for providing thermal refuge when above-ground temperatures require high regulatory costs (e.g., water or energy) or exceed the physiological tolerances of an organism. Our objective was to explore the role of burrows as thermal refuges for a small endotherm, the pygmy rabbit (Brachylagus idahoensis), during the summer and winter by quantifying energetic costs associated with resting above and below ground. We used indirect calorimetry to determine the relationship between energy expenditure and ambient temperature over a range of temperatures that pygmy rabbits experience in their natural habitat. We also measured the temperature of above- and below-ground rest sites used by pygmy rabbits in eastern Idaho, USA, during summer and winter and estimated the seasonal thermoregulatory costs of resting in the two microsites. Although pygmy rabbits demonstrated seasonal physiological acclimatization, the burrow was an important thermal refuge, especially in winter. Thermoregulatory costs were lower inside the burrow than in above-ground rest sites for more than 50% of the winter season. In contrast, thermal heterogeneity provided by above-ground rest sites during summer reduced the role of burrows as a thermal refuge during all but the hottest periods of the afternoon. Our findings contribute to an understanding of the ecology of small mammals in seasonal environments and demonstrate the importance of burrows as thermal refuge for pygmy rabbits.

For herbivores, nutrient intake is limited by the relatively low nutritional quality of plants and high concentrations of potentially toxic defensive compounds (plant secondary metabolites [PSMs]) produced by many plants. In response to phytochemical challenges, some herbivores selectively forage on plants with higher nutrient and lower PSM concentrations relative to other plants. Pygmy rabbits (Brachylagus idahoensis) are dietary specialists that feed on sagebrush (Artemisia spp.) and forage on specific plants more than others within a foraging patch. We predicted that the plants with evidence of heavy foraging (browsed plants) would be of higher dietary quality than plants that were not browsed (unbrowsed). We used model selection to determine which phytochemical variables best explained the difference between browsed and unbrowsed plants. Higher crude protein increased the odds that plants would be browsed by pygmy rabbits and the opposite was the case for certain PSMs. Additionally, because pygmy rabbits can occupy foraging patches (burrows) for consecutive years, their browsing may influence the nutritional and PSM constituents of plants at the burrows. In a post hoc analysis, we did not find a significant relationship between phytochemical concentrations, browse status, and burrow occupancy length. We concluded that pygmy rabbits use nutritional and chemical cues while making foraging decisions.

A quarter of all lagomorph species worldwide are threatened with extinction. Captive breeding programs, such as that developed for the Columbia Basin (CB) pygmy rabbit (Brachylagus idahoensis), sometimes are implemented as emergency conservation measures to restore small, genetically distinct populations. However, small source populations also may have low genetic diversity, which may influence attributes related to fitness, including growth, survival, and reproduction. We used mixed-effects regression models to explore the influence of genetic pedigree (% CB) on pairing success, growth, and survival during the 10-year captive breeding program at Washington State University, which included controlled pairings and outbreeding with pygmy rabbits from Idaho. Pairing success, juvenile growth, and juvenile survival declined with increasing CB pedigree of 1 or both parents, suggesting inbreeding depression among the small number of related founders. Demographic variables such as age, sex, and previous pregnancies, and environmental variables such as month and temperature at birth also were associated with production of pygmy rabbits. Our study illustrates the difficulty of retaining a unique genome of a small source population while simultaneously producing enough rabbits for restoration into natural habitat as part of endangered species recovery programs.

The objective of this study was to determine if housing conditions, specifically pen size and soil enrichment, had an effect on faecal glucocorticoid concentrations in the endangered pygmy rabbit (Brachylagus idahoensis). The success of the captive breeding programme has been limited, so one hypothesis is that chronic stress due to sub-optimal housing conditions may be responsible for poor fecundity. Faecal glucocorticoid concentrations were assessed in 50 females housed among several pen types at two breeding facilities. The highest glucocorticoid concentrations were found in females housed in 0.37 m2 crates as compared to enclosures ranging from 0.96 to 75 m2 in size. Results also indicated that enrichment of enclosures with soil had a significant influence on adrenal activity, based on a reduction in glucocorticoid excretion for females moved from non-soil pens to those with soil. Last, a significant facility effect on glucocorticoid concentrations was observed, suggesting that factors other than housing influenced adrenal activity in these rabbits. In conclusion, based on measurements of faecal glucocorticoids, pygmy rabbits are best managed in enclosures that contain soil for digging burrows. Pen size had little effect on stress hormones, except for crates where limited space and/or absence of soil was associated with higher glucocorticoid concentrations. These results underline the importance of monitoring glucocorticoid concentrations in captive breeding programmes to identify optimal husbandry and management practices.

An animal’s ability to avoid predation likely depends on its ability to detect approaching predators, conceal itself, and seek refuge or protection from predators. Habitat, especially vegetation structure, can influence all of these factors concurrently. Binary categorical assessments of habitat as ‘open’ or ‘closed’, however, confound at least two functions of habitat structure that could influence the perceived risk of predation: concealment, which functions to hide an individual, and visibility, which enhances detection of a potential predator. Both can influence predation risk independently and simultaneously. In this study, we decoupled these functional properties of vegetation and studied the effects of concealment, visibility, and proximity to a refuge on the distance at which pygmy rabbits (Brachylagus idahoensis) fled from an approaching threat (flight initiation distance; FID). Concealment by vegetation decreased perceptions of risk; however, pygmy rabbits exhibited elevated risk at high levels of visibility, regardless of the amount of concealment. Proximity to burrow entrances also influenced perceptions of risk, such that risk was significantly lower when rabbits were on or near burrow systems. Disentangling the functional properties of habitat can provide a more comprehensive understanding of the factors that influence perceived risk and escape behaviors of prey and provide insight into how habitat structure mechanistically relates to predation risk.

The Columbia Basin pygmy rabbit (Brachylagus idahoensis) is critically endangered and the focus of a captive-breeding program. However, reproductive success in captivity to date has not been sufficient to sustain reintroduction efforts. The goal of this study was to investigate patterns of fecal progestagen and glucocorticoid excretion in females during mating, gestation, and lactation and identify hormonal relationships to reproductive success. Fresh fecal samples were collected from 48 adult, female rabbits over 3 breeding seasons at a frequency of 4–7 samples per week. Results showed that a large (17-fold) increase in progestagen concentrations 1 day after mating provides a reliable means of determining if a successful mating occurred. In general, higher glucocorticoid concentrations during the breeding season, specifically during mating and gestation, were associated with lower reproductive success. Females that failed to conceive during the breeding season had higher glucocorticoid and lower...

As part of a captive-breeding program to restore extirpated Columbia Basin pygmy rabbits (Brachylagus idahoensis) to their native habitat in Washington, we documented mating and parental care behavior of these lagomorphs, which was previously unknown. Pygmy rabbits bred from late February through early June, and mating behavior consisted of chasing and brief copulations. Although presented with 1–4 mating partners and 1–6 mating opportunities annually, only 74% of females became pregnant each year. Unlike other lagomorphs, females dug a 16- to 35-cm natal burrow, usually separate from the residential burrow system, an average of 13 days after a successful copulation. Twenty-four days after copulation, females gave birth to 2–7 young at the entrance of the natal burrow and then covered the entrance. Females returned to nurse 1 or 2 times per day, until young emerged from burrows about 15 days after birth. Females averaged 1.3 litters per year, rarely (2%) producing 4 litters. Except for digging a natal burrow, mating and parental care in pygmy rabbits is similar to that of other lagomorphs. Understanding reproductive behavior is critical for captive breeding and reintroduction of pygmy rabbits, and efforts to reduce the consequences of genetic bottlenecks and inbreeding in captivity.

Dramatic declines in the endangered Columbia Basin pygmy rabbit, a genetically unique population of small, burrowing rabbits in Northwestern United States, are likely the combined results of habitat degradation and fragmentation, disease, and predation. A critical component of pygmy rabbit habitat includes big sagebrush (Artemisia tridentata), which constitutes 82–99% of their winter diet and 10–50% of their summer diet. Sagebrush also forms the bulk of hiding cover around burrow sites. Across the range of pygmy rabbits, sagebrush habitat is grazed extensively by cattle. However, grazing has unknown effects on pygmy rabbits inhabiting the remaining, fragmented shrub-steppe habitat. We evaluated the effects of four grazing treatments on the distribution of pygmy rabbit burrows, diets of pygmy rabbits, and quality and quantity of vegetation at Sagebrush Flat in central Washington. Ungrazed areas contained significantly more burrows per unit area than did grazed areas. Vegetation composition and structure differed little among treatments in early summer before annual grazing by cattle. However, cattle grazing in late summer through winter removed about 50% of the grass cover, and reduced the nutritional quality (e.g., increased fiber and decreased protein) of the remaining grass. Although pygmy rabbits ate

In 2001, the sudden collapse of the Columbia Basin population of pygmy rabbits prompted the initiation of a captive breeding program to facilitate reintroduction, but reproductive success in captivity has not met expectations. Therefore, the objective of this study was to characterize the reproductive and adrenal endocrinology of this endangered rabbit species so that appropriate management strategies could be developed to monitor animal welfare and increase reproduction. Fecal samples were collected from 27 female pygmy rabbits over three breeding and non-breeding seasons. HPLC analyses verified the presence of progesterone in the excreta of pygmy rabbits, but the majority of progestagen metabolites were unidentified polar compounds. By contrast, >70% of glucocorticoid immunoactivity was associated with cortisol. Longitudinal fecal hormone profiles during pregnancy were characterized by a large spike in progestagens shortly after mating, a gradual increase in progestagen and glucocorticoid concentrations throughout gestation and a return of hormones to baseline soon after birth (Day 24). The spike in progestagens 1 day after mating was a significant discovery for this species and appears to provide a reliable means of determining if a successful mating has occurred. Seasonal analyses of hormone excretion found that progestagen baselines did not vary between the breeding and non-breeding seasons, but, as expected, were highest during the breeding season in association with pregnancy. Across seasons, the lowest concentrations of glucocorticoids were associated with the highest rates of offspring production and survival, suggesting a possible link between heightened adrenal activity and lowered reproductive fitness in pygmy rabbits.

Sagebrush (Artemisia tridentata) comprises up to 99% of the winter and 50% of the summer diets of pygmy rabbits (Brachylagus idahoensis). Few animals specialize on such plants as sagebrush, which contain high levels of plant chemicals that can be toxic. We investigated the nutritional requirements of pygmy rabbits and their ability and propensity to consume sagebrush alone and as part of a mixed diet. We compared diet choices of pygmy rabbits with that of a generalist forager, the eastern cottontail (Sylvilagus floridanus). Pygmy rabbits had a moderately low nitrogen requirement (306.5 mg N/kg(0.75)/d), but a relatively high energy requirement, needing 750.8 kJ digestible energy/kg(0.75)/d to maintain their body mass while residing in small cages. They digested fiber in pelleted diets similarly to other small hindgut fermenters, but both cottontails and pygmy rabbits digested the fiber in sagebrush better than expected based on its indigestible acid detergent lignin content. Pygmy rabbits consumed more sagebrush than cottontails, regardless of the amount and nutritional quality of supplemental pellets provided. When consuming sagebrush alone, they ate barely enough to meet their energy requirements, whereas cottontails ate only enough sagebrush to meet 67% of theirs. Both rabbit species ate more sagebrush as the quality and quantity of supplemental pellets declined, and more greenhouse-grown sagebrush than sagebrush grown outside. Urine was more acidic when consuming sagebrush than when consuming pellets, indicating detoxification by the liver. Pygmy rabbits do not require sagebrush to survive, but seem to tolerate terpenes and other plant chemicals in sagebrush better than cottontails do.

Ultraviolet-B (UV-B) radiation has been increasing in temperate latitudes in recent decades and is expected to continue rising for some time. Enhanced UV-B radiation can change plant chemistry, yet the effects of these changes on mammalian herbivores are unknown. To examine the influence of enhanced UV-B radiation on nutrition of a specialist and generalist hindgut fermenter, we measured nutritional and chemical constituents of three common North American range plants, big sagebrush (Artemisia tridentata), yarrow (Achillea millefolium), and bluebunch wheatgrass (Pseudoregneria spicata), and how these changes influenced in vitro dry matter digestibility and in vivo digestibility by pygmy rabbits (Brachylagus idahoensis) and eastern cottontails (Sylvilagus floridanus). Forages were irradiated for 3 mo with ambient (1×) or supplemental (1.6×) UV-B radiation representing a 15% ozone depletion for Pullman, WA, USA. Enhanced UV-B radiation had minimal effects on the nutritional content and the tannin-binding capacity of forages. Similarly, the terpene concentration in sagebrush and yarrow was not affected by higher UV-B irradiances. Flavonoid compounds increased in sagebrush but decreased in yarrow. Rabbit preference and intake was not affected by treatment levels for any forage species and no differences were found between treatments for dry matter, fiber, protein digestibility, and apparent digestible energy.

Livestock grazing is one of the primary uses of sagebrush rangelands in western North America; therefore, an understanding of the ecological implications of grazing on habitat quality for sagebrush-dependent wildlife is needed to help land managers balance multiple objectives for land use. We studied effects of cattle grazing on components of habitat for an uncommon sagebrush habitat specialist, the pygmy rabbit (Brachylagus idahoensis), which has been petitioned for endangered or threatened status in the USA. We evaluated multiple components of habitat before and after grazing in replicated control and treatment plots in a mesic, high-elevation sagebrush-steppe environment in south-western Montana, USA. We predicted that grazing would decrease the biomass of herbaceous forage, alter security cover, and increase rate of collapse of rabbit burrows, and we expected that these effects would be more pronounced during summer than spring. As expected, cattle grazing reduced the biomass of perennial grasses available to pygmy rabbits after grazing that occurred during either spring or summer, and the biomass of forbs after spring grazing. In contrast, grazing did not markedly influence the functional properties of vegetation related to predation risk or the integrity of rabbit burrow systems. In the context of the stocking rate of the allotments in our study (7.3 acres/Animal Unit Month, 2.95 ha/Animal Unit Month), annual cattle grazing did not seem to markedly change habitat for pygmy rabbits in our study area; however, longer-term and higher intensity grazing might result in more pronounced habitat changes. Understanding the ecological implications of cattle grazing on habitat quality for pygmy rabbits and other sagebrush-dependent wildlife can guide conservation strategies for these species on sagebrush rangelands managed under multiple-use policies.