Jeffrey E. Lane

Delayed phenology and reduced fitness associated with climate change in a wild hibernator

The most commonly reported ecological effects of climate change are shifts in phenologies, in particular of warmer spring temperatures leading to earlier timing of key events. Among animals, however, these reports have been heavily biased towards avian phenologies, whereas we still know comparatively little about other seasonal adaptations, such as mammalian hibernation. Here we show a significant delay (0.47 days per year, over a 20-year period) in the hibernation emergence date of adult females in a wild population of Columbian ground squirrels in Alberta, Canada. This finding was related to the climatic conditions at our study location: owing to within-individual phenotypic plasticity, females emerged later during years of lower spring temperature and delayed snowmelt. Although there has not been a significant annual trend in spring temperature, the date of snowmelt has become progressively later owing to an increasing prevalence of late-season snowstorms. Importantly, years of later emergence were also associated with decreased individual fitness. There has consequently been a decline in mean fitness (that is, population growth rate) across the past two decades. Our results show that plastic responses to climate change may be driven by climatic trends other than increasing temperature, and may be associated with declines in individual fitness and, hence, population viability.

The functional response of a hoarding seed predator to mast seeding.

Mast seeding involves the episodic and synchronous production of large seed crops by perennial plants. The predator satiation hypothesis proposes that mast seeding maximizes seed escape because seed predators consume a decreasing proportion of available seeds with increasing seed production. However, the seed escape benefits of masting depend not only on whether predators are satiated at high levels of seed production, but also on the shape of their functional response (type II vs. type III), and the actual proportion of available seeds that they consume at different levels of seed production. North American red squirrels (Tamiasciurus hudsonicus) are the primary vertebrate predator of white spruce (Picea glauca) mast seed crops in many boreal regions because they hoard unopened cones in underground locations, preempting the normal sequence of cone opening, seed dispersal, and seed germination. We document the functional response of cone-hoarding by red squirrels across three non-mast years and one mast year by estimating the number of cones present in the territories of individual red squirrels and the proportion of these cones that they hoarded each autumn. Even though red squirrels are not constrained by the ingestive and on-body (fat reserves) energy reserve limitations experienced by animals that consume seeds directly, most squirrels hoarded < 10% of the cones present on their territories under mast conditions. Cone availability during non-mast years also reached levels that satiated the hoarding activity of red squirrels; however, this occurred only on the highest-quality territories. Squirrels switched to mushroom-hoarding when cone production was low and mushrooms were abundant. This resulted in type III functional response whereby the proportional harvest of cones was highest at levels of cone availability that were intermediate within non-mast years. Overall, more cones escaped squirrel cone-hoarding during a mast event than when cone production was low in non-mast years, which supports the predator satiation hypothesis. However, the highly variable seed escape in non-mast years may help to explain why all spruce cone production is not concentrated into fewer, larger, mast years.

Energetic costs of male reproduction in a scramble competition mating system.

1. The assumption that the primary limitations on reproductive success differ between the sexes is inherent in traditional sexual selection theory. Although the energy that can be allocated to reproduction is assumed to be the main limitation to females, the ability to attract and defend oestrous females is assumed to be the primary limitation to males. 2. Estimates of the energetic costs of reproduction in male mammals are, however, limited and have largely been obtained from sexually dimorphic species exhibiting female defence mating systems. These studies often reveal that the energetic cost of male reproduction is similar to or even exceeds that of females, and therefore challenge long-held assumptions of inter-sexual reproductive limitations, but their generality is little known. 3. We coupled measurements of energy expenditure with detailed behavioural observations of reproductive male North American red squirrels (Tamiasciurus hudsonicus). This species displays minimal sexual dimorphism and exhibits a scramble competition mating system, under which sexual selection favours enhanced mate searching effort by males. 4. We conducted the study over 2 years characterized by a substantial variation in upcoming natural food availability and across two study populations that experienced either natural food abundance or an ad libitum food-supplementation to investigate the influence of resource availability on male reproductive energy expenditure. 5. Under natural conditions, mean energy expenditure of males across the 2 years was high, approximating that of females during lactation. Furthermore, in the anticipation of high upcoming natural food availability and resultant offspring survival, expenditure approximately doubled (from 290 +/- 7 to 579 +/- 73 kJ day(-1)). When current food availability (and consequently the density of receptive females) was experimentally elevated, males displayed the highest levels of energy expenditure we recorded (873 +/- 98 kJ day(-1)). 6. Our results provide compelling evidence that the energy available for reproductive allocation places a strong limitation on reproduction in male North American red squirrels and contribute to previous work suggesting that high and limiting energetic costs of male reproduction may be a general feature of mammalian reproduction.

Climate change and mammals: evolutionary versus plastic responses

Phenotypic plasticity and microevolution are the two primary means by which organisms respond adaptively to local conditions. While these mechanisms are not mutually exclusive, their relative magnitudes will influence both the rate of, and ability to sustain, phenotypic responses to climate change. We review accounts of recent phenotypic changes in wild mammal populations with the purpose of critically evaluating the following: (i) whether climate change has been identified as the causal mechanism producing the observed change; (ii) whether the change is adaptive; and (iii) the relative influences of evolution and/or phenotypic plasticity underlying the change. The available data for mammals are scant. We found twelve studies that report changes in phenology, body weight or litter size. In all cases, the observed response was primarily due to plasticity. Only one study (of advancing parturition dates in American red squirrels) provided convincing evidence of contemporary evolution. Subsequently, however, climate change has been shown to not be the causal mechanism underlying this shift. We also summarize studies that have shown evolutionary potential (i.e. the trait is heritable and/or under selection) in traits with putative associations with climate change and discuss future directions that need to be undertaken before a conclusive demonstration of plastic or evolutionary responses to climate change in wild mammals can be made.

Plasma DHEA levels in wild, territorial red squirrels : Seasonal variation and effect of ACTH

In many species, territorial behavior is limited to the breeding season and is tightly coupled to circulating gonadal steroid levels. In contrast, both male and female red squirrels (Tamiasciurus hudsonicus) are highly aggressive in both the breeding and non-breeding seasons in defense of food stores on their individual territories throughout the boreal and northern forests of North America. Dehydroepiandrosterone (DHEA), an androgen precursor, is secreted from the adrenal cortex in some mammals, and DHEA has been linked to aggression in non-breeding songbirds. Here, we examined plasma DHEA levels in a natural population of red squirrels in the Yukon, Canada. Plasma DHEA levels in both males and females reached high concentrations (up to 16.952 ng/ml in males and 14.602 ng/ml in females), markedly exceeding plasma DHEA concentrations in laboratory rats and mice and similar to plasma DHEA concentrations in some primates. Circulating DHEA levels showed both seasonal and yearly variation. Seasonal variation in male plasma DHEA levels was negatively correlated with testes mass. Yearly variation in male DHEA levels was positively correlated with population density. In both males and females, circulating DHEA rapidly increased after ACTH treatment, implying an adrenal origin. This is the first examination of plasma DHEA concentrations in a wild rodent and the first field experiment on the regulation of plasma DHEA in any wild mammal. These data lay the foundation for future studies on the role of DHEA in non-breeding territoriality in this species and other mammals.

Sexually selected behaviour: red squirrel males search for reproductive success

1. Differential male reproductive success is commonplace in mammals and frequently attributed to variation in morphological traits that provide individuals with a competitive advantage in female defence mating systems. Other mammalian mating systems, however, have received comparatively little attention and correlates of male reproductive success in them are less well understood. 2. We studied a free-ranging population of North American red squirrels (Tamiasciurus hudsonicus Erxleben) exhibiting year-round individual territoriality. Males must temporarily vacate their territories to locate spatially dispersed receptive females, thereby setting the stage for a scramble competition mating system. 3. We predicted that both male annual mating success (measured as the number of females copulated with) and annual reproductive success (measured as the number of offspring sired) would be positively correlated with both search ability (measured as the number of oestrous females located over the mating season) and effort (measured as mating season home range size), generating directional sexual selection on these two metrics. 4. Mating season home ranges of males showed, on average, an almost 10-fold increase relative to those measured during the nonmating season, while those of females showed a more moderate twofold increase and both annual mating and reproductive success of males was positively correlated with search ability and search effort. 5. The spatial dispersion of females, resulting from the strict territorial social structure of red squirrels, gave rise to a predicted scramble competition mating system. Furthermore, the strength of sexual selection on behavioural traits in this mating system equalled previous estimates for morphological traits in female defence mating systems.

Daily Torpor in Free‐Ranging Whip‐Poor‐Wills (Caprimulgus vociferus)

The use of heterothermy is well documented in the order Caprimulgiformes, but there is conflicting information regarding whether whip‐poor‐wills are heterothermic. Consequently, we sought to rigorously examine the thermoregulatory abilities of this species. Our study was conducted in southeast South Dakota (42°47′N, 97°0′W), where 35 individuals were captured and outfitted with external, temperature‐sensitive radio transmitters. We found evidence that whip‐poor‐wills used daily torpor during the autumn of 2000 and the spring of 2001 (n = 12 torpor bouts, based on 346 bird‐nights of observation). The average minimum skin temperature of two torpid whip‐poor‐wills (n = 5 torpor bouts) in spring 2001 was 20.1° ± 2.6°C, and bouts of reduced skin temperature lasted an average of 360.0 ± 93.7 min. The distribution of heterothermy within the Caprimulgiform phylogeny suggests that the trait is ancestral in the order. Specific heterothermic parameters, however, differ among the different species. In particular, the frequency of torpor use in whip‐poor‐wills is lower than for other species. These data suggest that several factors, including weather conditions and gender‐specific reproductive ecology, influence the propensity of whip‐poor‐wills and other Caprimulgiformes to enter torpor.

Reproductive phenology of a food-hoarding mast-seed consumer: resource- and density-dependent benefits of early breeding in red squirrels.

The production of offspring by vertebrates is often timed to coincide with the annual peak in resource availability. However, capital breeders can extend the energetic benefits of a resource pulse by storing food or fat, thus relaxing the need for synchrony between energy supply and demand. Food-hoarding red squirrels (Tamiasciurus hudsonicus) breeding in the boreal forest are reliant on cones from a masting conifer for their nutrition, yet lactation is typically completed before the annual crop of cones is available for consumption such that peaks in energy supply and demand are not synchronized. We investigated the phenological response of red squirrels to annual variation in environmental conditions over a 20-year span and examined how intra- and inter-annual variation in the timing of reproduction affected offspring recruitment. Reproductive phenology was strongly affected by past resource availability with offspring born earlier in years following large cone crops, presumably because this affected the amount of capital available for reproduction. Early breeders had higher offspring survival and were more likely to renest following early litter loss when population density was high, perhaps because late-born offspring are less competitive in obtaining a territory when vacancies are limited. Early breeders were also more likely to renest after successfully weaning their first litter, but renesting predominantly occurred during mast years. Because of their increased propensity to renest and the higher survival rates of their offspring, early breeders contribute more recruits to the population but the advantage of early breeding depends on population density and resource availability.

The heritability of multiple male mating in a promiscuous mammal.

The tendency of females to mate with multiple males is often explained by direct and indirect benefits that could outweigh the many potential costs of multiple mating. However, behaviour can only evolve in response to costs and benefits if there is sufficient genetic variation on which selection can act. We followed 108 mating chases of 85 North American red squirrels (Tamiasciurus hudsonicus) during 4 years, to measure each females degree of multiple male mating (MMM), and used an animal model analysis of our multi-generational pedigree to provide what we believe is the first estimate of the heritability of MMM in the wild. Female red squirrels were highly polyandrous, mating with an average of 7.0 ± 0.2 males on their day of oestrus. Although we found evidence for moderate levels of additive genetic variation (CVA = 5.1), environmental variation was very high (CVE = 32.3), which resulted in a very low heritability estimate (h2 < 0.01). So, while there is genetic variation in this trait, the large environmental variation suggests that any costs or benefits associated with differences among females in MMM are primarily owing to environmental and not genetic differences, which could constrain the evolutionary response to natural selection on this trait.

Cavity roost site availability and habitat use by bats in different aged riparian cottonwood stands

ABSTRACT Riparian forests provide important roosting habitat, abundant prey and access to drinking water for many bat species but to date there has been little research on the differential quality of habitats within riparian areas. We quantified the density of potential roost cavities in three age classes (i.e., young: ca. 20 years, mature: ca. 60 years, and old: ca. 100 years) of riparian cottonwood (Populus deltoides) forest stands. Bat activity was also sampled using acoustic detectors in one representative stand of each age class. Stands were situated along an 80 km stretch of the Missouri River in southeastern South Dakota and northwestern Iowa, USA. We predicted the highest density of potential roosts and the highest activity of bats to occur in the oldest age class. Contrary to our predictions, and previous work in aspen dominated upland sites, we found that the density of potential roosts was not significantly different between mature and old stands. However, there were no potential roosts in young stands. Data from guano traps verified the use of a number of cavities in both mature and old stands. Both commuting and foraging activities were highest in the mature, relative to the old and young stand. In total, our data indicate that mature and old stands represent high quality roosting habitat, with the mature being used preferentially for commuting and foraging. Trees in the oldest stands, however, are nearing the end of their lifespan and falling. Younger cohorts must therefore be retained for future recruitment of natural cavities.