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The critical agenda for mammalian ecologists over this century is to obtain a synthetic and predictive understanding of the factors that limit the distribution and abundance of mammals on Earth. During the last 100 years, a start has been made on this agenda, but only a start. Most mammal species have been described, but there still are tropical areas of undisclosed species richness. We have been measuring changes in distribution and abundance of many common mammals during the last century, and this monitoring agenda has become more critical as climate change has accelerated and habitat destruction has increased with human population growth. There are a small number of factors that can limit the distribution and abundance of mammals: weather, predation, food supplies, disease, and social behavior. Weather limits distribution and abundance mostly in an indirect manner by affecting food supplies, disease, and predation in the short term and habitat composition and structure in the longer term. A good starting point for all studies of mammals is to define them within a well-structured trophic web, and then quantify the major linkages within that web. We still are far from having data on enough model systems to develop a complete theory and understanding of how food webs are structured and constrained as climate shifts and humans disturb habitats. We have many of the bits and pieces for some of our major ecosystems but a poor understanding of the links and the resilience of our mammalian communities to changes in trophic webs driven by climate change and human disturbances.
Within populations, individual males adopt different courtship tactics due to differences in their competitive ability, which may vary depending on the animal's age and size. To test the hypothesis that mule deer (Odocoileus hemionus) and white-tailed deer (O. virginianus) males vary their courtship behavior based on their size, we conducted focal observations of 144 mule deer and 85 white-tailed males that varied in size, at a large grassland site in southern Alberta. The smallest mule deer males devoted more time to feeding, were less likely to engage in late-stage courtship than larger males and were less likely to move among female groups. Other males, including small white-tailed males, appeared to use a roving strategy to search for estrous females in different groups, which is consistent with recent research on male movements. Both medium and large males increased the time they spent in one-male groups, and specifically isolated pairs, as courtship advanced, presumably to reduce competition with other males. However, this trend was most pronounced for medium mule deer males, and for all size classes of white-tailed deer. In contrast, large mule deer males spent a similar proportion of time tending females in all group types. Our results identified potential size-dependent tactics for mule deer males. In contrast, white-tailed males of all sizes appeared to rely on a tactic of finding and tending estrous females in isolation from other males.
Bighorn sheep (Ovis canadensis) can live in extremely harsh environments and subsist on submaintenance diets for much of the year. Under these conditions, energy stored as body fat serves as an essential reserve for supplementing dietary intake to meet metabolic demands of survival and reproduction. We developed equations to predict ingesta-free body fat in bighorn sheep using ultrasonography and condition scores in vivo and carcass measurements postmortem. We then used in vivo equations to investigate the relationships between body fat, pregnancy, overwinter survival, and population growth in free-ranging bighorn sheep in California and Nevada. Among 11 subpopulations that included alpine winter residents and migrants, mean ingesta-free body fat of lactating adult females during autumn ranged between 8.8% and 15.0%; mean body fat for nonlactating females ranged from 16.4% to 20.9%. In adult females, ingesta-free body fat > 7.7% during January (early in the second trimester) corresponded with a > 90% probability of pregnancy and ingesta-free body fat > 13.5% during autumn yielded a probability of overwinter survival > 90%. Mean ingesta-free body fat of lactating females in autumn was positively associated with finite rate of population increase (λ) over the subsequent year in bighorn sheep subpopulations that wintered in alpine landscapes. Bighorn sheep with ingesta-free body fat of 26% in autumn and living in alpine environments possess energy reserves sufficient to meet resting metabolism for 83 days on fat reserves alone. We demonstrated that nutritional condition can be a pervasive mechanism underlying demography in bighorn sheep and characterizes the nutritional value of their occupied ranges. Mountain sheep are capital survivors in addition to being capital breeders, and because they inhabit landscapes with extreme seasonal forage scarcity, they also can be fat reserve obligates. Quantifying nutritional condition is essential for understanding the quality of habitats, how it underpins demography, and the proximity of a population to a nutritional threshold.
Knowledge of a species' visual system has far reaching implications that affect our understanding of a species' ecology and evolutionary history. As a model taxon, the heteromyid rodent genus Dipodomys has been valuable in elucidating patterns and mechanisms in biomechanics, ecology, adaptive physiology, biogeography, and more. Although studied extensively, the visual system of Dipodomys has not been described beyond anecdotal mention of their large eyes. Here, the transmittance parameters of the cornea and lens of Ord's kangaroo rat (Dipodomys ordii) were analyzed and photoreceptor proteins (opsins) expressed in the retina were identified with immunohistochemical (IHC) labeling. Retina maps were constructed to illustrate the relative densities of photoreceptor cells expressing short wavelength (SWS1) opsins, middle/long wavelength (MW/LW) opsins, and rhodopsin (RH1). The retina of D. ordii has variable densities of SWS1 opsin with the highest density being ventral to the optic nerve, high density of MW/LW opsin, and uniform distribution and high density of RH1 across the retina. Our results suggest that D. ordii has a UV-sensitive visual system. Composition and densities of MW/LW- and SWS1-expressing cells resemble that of a crepuscular/diurnal species thereby supporting previous authors who have reported such activity patterns. Uniform retinal distribution of RH1 indicates visual acuity at night, also confirming the paradigm of D. ordii as primarily a nocturnal species and suggesting visual acuity at all times of the day in the species. These results demonstrate not only that the species is capable of UV vision and has a retina characteristic of a diurnal mammal, but that many previously unknown photic niche selective advantages likely have shaped the evolution and ecology of this model taxon.
The Asian golden cat (Catopuma temminckii) occurs in small, declining, and highly fragmented populations throughout Southeast Asia, whereas the smaller leopard cat (Prionailurus bengalensis) is common and widespread. In contrast to leopard cats, little is known about the ecology of Asian golden cats, and resource partitioning between these species has not been studied. We used DNA-confirmed scats, camera-trap data, and prey surveys, to determine the diet, prey selection, and activity, of Asian golden cats and leopard cats in a protected area in northern Laos. The two felids had different diets: Asian golden cats consumed mostly ungulates (35% biomass consumed), murid rodents (23%), and carnivores (15%), whereas leopard cats consumed mostly murid rodents (79%). Asian golden cats were not random in their consumption of ungulates, because muntjac (Muntiacus spp.) were selectively consumed over larger ungulates, indicating muntjac were preyed upon rather than scavenged. Dietary overlap between the two felid species was moderate (R0 = 0.60), and the dietary niche breadth of Asian golden cats (B = 8.44) was nearly twice as high as that of leopard cats (4.54). The mean (± SD) scat diameter was greater for Asian golden cats (2.1 ± 0.3 cm) than leopard cats (1.8 ± 0.2 cm), although diameters of leopard cat scats were considerably larger than previously assumed for this species. The felid species differed in their activity patterns, because Asian golden cats were diurnal, whereas leopard cats were nocturnal, although they did not differ in their use of elevation, suggesting there was no habitat segregation. Overall, leopard cats appeared to coexist with Asian golden cats, a potential predator and competitor, by exhibiting dietary and temporal partitioning. Our results showed that muntjac were important prey of Asian golden cats, suggesting the management of muntjac might be important for conserving populations of Asian golden cats.
Increases in apex predator abundance can influence the behavior of sympatric species, particularly when the available habitat and/or resources are limited. We assessed the temporal and spatiotemporal interactions between Florida panthers (Puma concolor coryi) and six focal sympatric species in South Florida, where Florida panther abundance has increased by more than 6-fold since the 1990's. Using camera trap data, we quantified species' diel activity patterns, temporal overlap, and time-to-encounter (i.e., time between consecutive visits of a Florida panther and a focal species and vice versa). The Florida panther and bobcat (Lynx rufus) displayed a nocturnal activity pattern; the black bear (Ursus americanus), white-tailed deer (Odocoileus virginianus), wild boar (Sus scrofa), and wild turkey (Meleagris gallopavo) were mostly diurnal; and the raccoon (Procyon lotor) was cathemeral. Prey species and black bears minimized encounters with Florida panthers by being active during the day and displaying longer time-to-encounter, whereas Florida panthers visited a site after a prey species at higher probabilities than after competitor species, and were more likely to visit an elevated site or upland habitat. Our results suggest that interactions between Florida panthers and sympatric species in our study system are driven by species-specific behavioral responses. Gaining a better understanding of the crucial interactions driving species coexistence is important for a better understanding of the structure and function of ecological communities and help manage the potential expansion of the Florida panther into Central Florida.
Robust abundance estimates of wild animal populations are needed to inform management policies and are often obtained through mark–recapture (MR) studies. Visual methods are commonly used, which limits data collection to daylight hours and good weather conditions. Passive acoustic monitoring offers an alternative, particularly if acoustic cues are naturally produced and individually distinctive. Here we investigate the potential of using individually distinctive signature whistles in a MR framework and evaluate different components of study design. We analyzed signature whistles of common bottlenose dolphins, Tursiops truncatus, using data collected from static acoustic monitoring devices deployed in Walvis Bay, Namibia. Signature whistle types (SWTs) were identified using a bout analysis approach (SIGnature IDentification [SIGID]—Janik et al. 2013). We investigated spatial variation in capture by comparing 21 synchronized recording days across four sites, and temporal variation from 125 recording days at one high-use site (Aphrodite Beach). Despite dolphin vocalizations (i.e., echolocation clicks) being detected at each site, SWTs were not detected at all sites and there was high variability in capture rates among sites where SWTs were detected (range 0–21 SWTs detected). At Aphrodite Beach, 53 SWTs were captured over 6 months and discovery curves showed an initial increase in newly detected SWTs, approaching asymptote during the fourth month. A Huggins closed capture model constructed from SWT capture histories at Aphrodite Beach estimated a population of 54–68 individuals from acoustic detection, which overlaps with the known population size (54–76 individuals—Elwen et al. 2019). This study demonstrates the potential power of using signature whistles as proxies for individual occurrence and in MR abundance estimation, but also highlights challenges in using this approach.
The timing of life-history traits may have strong influences on the evolution of life cycles and on population demography. This is especially true of the age at which females first reproduce (Cole's principle). We examined whether the age at which females first reproduce influences fitness in Columbian ground squirrels (Urocitellus columbianus), for which females varied in the age at which they initially produce weaned offspring, from ages 1 through 5 years. With 148 females with complete known life spans in a 28-year data set, we examined four fitness measures: individual fitness (λind), individual fitness relative to the pattern of growth of the population (λrel), lifetime reproductive success (LRS), and LRS relative to the total LRS for each female's cohort (LRSrel). These metrics were calculated for offspring produced at the time of weaning and offspring that survived to emerge after their first hibernation period. Individual fitness (λind) was significantly associated with population growth during a female's lifetime (λLeslie; R2 = 0.523, P < 0.0001), indicating the need to adjust individual fitness for demonstrated changes in population growth and thus producing a relative individual fitness index (λrel). We regressed λrel on age at first reproduction, and found significant selection favoring earlier reproductive success (β ± SE = –0.20 ± 0.06; R2 = 0.306, P < 0.0001). When using an earlier (offspring at weaning) versus later (those that survived their first hibernation) measure of fecundity, we found that the latter introduced considerable variation, likely environmental, into the estimate of selection. This greatly weakened the regression of relative fitness on the age at first successful reproduction. LRS and LRSrel exhibited nonsignificant changes with age at first reproduction. Finally, those females that reproduced successfully at younger ages had similar litter sizes but significantly shorter life spans than females that matured when older, perhaps reflecting costs to early reproduction.
Ryan T. Botts, Amy A. Eppert, Timothy J. Wiegman, Abner Rodriguez, Steven R. Blankenship, Ellen M. Asselin, Wyatt M. Garley, Abigail P. Wagner, Sierra E. Ullrich, Gabrielle R. Allen, Michael S. Mooring
Temporal niche shifts can shape predator–prey interactions by enabling predator avoidance, enhancing feeding success, and reducing competition among predators. Using a community-based conservation approach, we investigated temporal niche partitioning of mammalian predators and prey across 12 long-term camera trap surveys in the Pacific slope and Talamanca Cordillera of Costa Rica. Temporal overlap and segregation were investigated between predator–prey and predator–predator pairs using overlap analysis, circular statistics, and relative abundance after accounting for differences in habitat, season, and human impact among sites. We made the assumption that predators select abundant prey and adjust their activity to maximize their temporal overlap, thus we predicted that abundant prey with high overlap would be preferred prey species for that predator. We also predicted that similar-sized pairs of predator species with the greatest potential for competitive interactions would have the highest temporal segregation. Our results supported the existence of temporal niche separation among the eight species of predators—the smaller Leopardus felids (ocelot, margay, oncilla) were primarily nocturnal, the largest felids (jaguar and puma) and coyote were cathemeral, and the smaller jaguarundi and tayra were mostly diurnal. Most prey species (67%) were primarily nocturnal versus diurnal or cathemeral (33%). Hierarchical clustering identified relationships among species with the most similar activity patterns. We discuss the primary prey and competitor species predicted for each of the eight predators. Contrary to our prediction, the activity pattern of similar-sized intraguild competitors overlapped more than dissimilar-sized competitors, suggesting that similar-sized predators are hunting the same prey at the same time. From this we conclude that prey availability is more important than competition in determining circadian activity patterns of Neotropical predators. Our results indicate the presence of a delicate balance of tropical food webs that may be disrupted by overhunting, leading to a depauperate community consisting of ubiquitous generalists and endangered specialists. With Central America a hotspot for hunting-induced “empty forests,” community-based conservation approaches may offer the best road to reduce illegal hunting and maintain the biodiversity and community structure of tropical forest systems.
Carbon and nitrogen stable isotope ratios are used widely to describe wildlife animal diet composition and trophic interactions. To reconstruct consumer diet, the isotopic differences between consumers and their diet items—called the trophic discrimination factor (TDF)—must be known. Proxies of diet composition are sensitive to the accuracy of TDFs. However, specific TDFs are still missing for many species and tissues because only a few controlled studies have been carried out on captive animals. The aim of this study was to estimate TDFs for hair and blood for carbon and nitrogen stable isotopes for caribou, moose, white-tailed deer, eastern coyote, and black bear. We obtained stable isotope ratios for diet items, hair, and blood samples, of 21 captive adult mammals. Diet–tissue discrimination factors for carbon in hair (Δ13CLE) ranged from 0.96‰ to 3.72‰ for cervids, 3.01‰ to 3.76‰ for coyote, and 5.15‰ to 6.35‰ for black bear, while nitrogen discrimination factors (Δ15N) ranged from 2.58‰ to 5.95‰ for cervids, 2.90‰ to 3.13‰ for coyote, and 4.48‰ to 5.44‰ for black bear. The Δ13CLE values in coyote blood components ranged from 2.20‰ to 2.69‰ while Δ15N ranged from 3.30‰ to 4.41‰. In caribou serum, Δ13CLE reached 3.34 ± 1.28‰ while Δ15N reached 5.02 ± 0.07‰. The TDFs calculated in this study will allow the evaluation of diet composition and trophic relationships between these five mammal species and will have important implications for the study of endangered caribou populations for which the use of noninvasive tissue sampling is highly relevant.
Predators and parasites have synergistic effects on the phenotype of the species they share as prey and host. Experimental studies that incorporate the interactions between predation and parasitism are, however, scarce in small-mammal populations. Our previous work has shown that the combined effects of predation and coccidian infection reduce overwinter survival and population density in root voles (Microtus oeconomus). Here, we examined the separate and combined effects of these two drivers on the population growth of root voles during the breeding season. We carried out a two-level factorial experiment, in which we manipulated predator exclusion and the removal of parasites in enclosures and measured survival, fecal corticosterone metabolite (FCM) concentration, recruitment, and population density. An expected synergistic effect of predators and parasites on vole population was not found, due to no effect of parasites on FCM level and recruitment rate during the period of the experiment. Instead, we found phase-related effects of predation on demography. Predation reduced the survival rate of voles in spring, which was intensified by parasite infection. Predation risk reduced recruitment rate in early summer by elevating FCM levels. Consequently, both direct and indirect effects of predation lowered population density during the experimental period. In addition, for populations free of predators, the peak density that occurred in early autumn elevated FCM level of adult voles, which reduced recruitment rates and halted population growth. Moreover, predation, parasites, and density affected the quality of the offspring. Our study suggests that multiple regulation processes influence population fluctuations during the breeding season. We conclude that a population experiencing stress acts as a common interface through which interactions between intrinsic and extrinsic factors can be important determinants of fluctuations. We propose a new hypothesis of integrative stress effects to explain small-mammal population fluctuations.
Moonlight intensity influences the activity patterns of bats. Some bat species reduce their activity levels during brighter nights, a phenomenon known as “lunar phobia.” While lunar phobia of bats has been extensively studied in tropical regions, the same is not the case of bats in temperate regions. By using acoustic detectors, we examined differences in the activity of insectivorous bats on nights with different moonlight intensity in an agricultural landscape of central Chile. We also examined the hourly activity patterns throughout the night and how these varied between full and new moon nights. All bat species modified their activity based on the moonlight intensity; however, their effects were species-specific. The activity of Lasiurus varius, L. villosissimus, Myotis chiloensis, and Histiotus montanus was lower during bright nights, while Tadarida brasiliensis was the only species whose activity was higher during bright nights. Hourly activity throughout the night differed between full moon nights and new moon nights in most bat species. During full moon, bats concentrated their activities in the early hours of the nights; a more homogeneous activity pattern was exhibited during new moon night. Our study demonstrates that moonlight affects the activity of bats in Chile, a factor that should be considered when studying bats.
Viscacha rats (genus TympanoctomysYepes, 1942) are ecologically, physiologically, and behaviorally unusual octodontid rodents endemic to the Monte and Patagonian desert biomes of Argentina. The geographic ranges of the different species of Tympanoctomys have been described in general terms but have not been associated with spatial and climate data. Within species, populations are patchily distributed and genetically distinct. We investigated the predicted distribution of Tympanoctomys and the influence of climate fluctuations on their geographic range in historical, current, and future, scenarios. Our objectives were to characterize the environmental niche of the genus, propose a paleoclimatic context for the oldest fossils, characterize the environmental niches for T. barrerae and T. kirchnerorum, and forecast potential future distributions for these taxa. Ecological niche models were constructed using occurrence records from 1941 to the present wherein we identified several precipitation and temperature variables as important predictors of the geographic distributions of the genus, and the species T. barrerae and T. kirchnerorum. Based on our models' results, we hypothesize that the distribution of Tympanoctomys has contracted from historical to modern times. At the species level, T. kirchnerorum likely experienced the most dramatic change, suffering a large contraction of its historical distribution resulting in its limited present distribution. Given these findings, projected future climate fluctuations and global warming are expected to affect the distributions and persistence of these species.
Population viability and metapopulation dynamics are strongly affected by gene flow. Identifying ecological correlates of genetic structure and gene flow in wild populations is therefore a major issue both in evolutionary ecology and species management. Studying the genetic structure of populations also enables identification of the spatial scale at which most gene flow occurs, hence the scale of the functional connectivity, which is of paramount importance for species ecology. In this study, we examined the genetic structure of a social, continuously distributed mammal, the European badger (Meles meles), both at large spatial scales (among populations) and fine (within populations) spatial scales. The study was carried out in 11 sites across France utilizing a noninvasive hair trapping protocol at 206 monitored setts. We identified 264 badgers genotyped at 24 microsatellite DNA loci. At the large scale, we observed high and significant genetic differentiation among populations (global Fst = 0.139; range of pairwise Fst [0.046–0.231]) that was not related to the geographic distance among sites, suggesting few large-scale dispersal events. Within populations, we detected a threshold value below which badgers were genetically close (< 400 m), highlighting that sociality is the major structuring process within badger populations at the fine scale.
Africa hosts a high number of bat species, many of which have been poorly studied. Among African vesper bats (Vespertilionidae), some species are morphologically similar to each other, hampering identification in the field. Consequently, basic information on these species' population dynamics, distributions, or behaviors is vague and/or incorrectly documented. Among some Vespertilionidae, variation in flaccid penis shape enables species identification. This variation in morphology is thought to have resulted from sexual selection operating on the erect penis. Furthermore, in the context of strong postcopulatory competition, divergence in sperm traits may have evolved among closely related species. These male reproductive characters have hitherto not been investigated in southern African vespertilionid bats. In this study, we present the morphology of flaccid penis, erect penis, and sperm, of six small vesper species, based on the prediction that these characters have evolved sufficiently toward different optima to allow species discrimination. Species identification based solely on the morphological characters of the penis entirely matched species identification based on traditional (craniodental) characters. We illustrate penis morphology of these species to assist with field identifications for future ecological, conservation, or behavioral studies. Sperm morphology was sufficient to discriminate between the different genera, but could not reliably separate Neoromicia nana, Ne. zuluensis, and Ne. capensis. Hence, we demonstrate that these difficult to identify species can be readily distinguished based on traits directly observable in the field and on living animals, which will lead to more focused field studies on these otherwise morphologically cryptic species. Finally, our comparisons of penis morphology support the suggestion that Hypsugo anchietae is better placed within the genus Neoromicia.
Northern yellow bats (Dasypterus intermedius) are tree-roosting bats in the family Vespertilionidae comprised of two subspecies: D. intermedius intermedius and D. intermedius floridanus. The two subspecies are thought to be geographically separated. Due to their cryptic morphology, this hypothesis has never been tested and can benefit from being examined within a molecular framework. In this study, mitochondrial sequence data from 38 D. intermedius and nuclear sequence data from 14 D. intermedius from across their range were used to test the hypothesis that genetically defined groups correspond geographically with the two morphologically defined subspecies. Although high levels of divergence of the mitochondrial sequence (11.6%) suggest genetically distinct clusters sympatric in southern Texas, no genetic structure was recovered with the nuclear marker. Moreover, the mitochondrial sequence data recovered a paraphyletic relationship between the two subspecies of D. intermedius with the Cuban yellow bat (D. insularis), whereas no such paraphyly was recovered from analysis of the nuclear marker. Divergence time based on analyses of mitochondrial sequence for the two subspecies was approximately 5.5 Ma. The patterns observed are hypothesized to be the result of past isolation of lineages and secondary contact that is currently contributing to gene flow.
The subspecies concept is one of the most controversial in Linnean taxonomy. In the past, subspecies were described without a clear conceptual framework, triggering confusion and motivating criticism of the very concept of a subspecies. At present, subspecies are conceived as aggregates of populations that are geographically isolated, are composed of interfertile individuals, and are morphologically diagnosable. The tayra, Eira barbara, was described in 1758 and has had a stable taxonomic history at the species level. However, below the species level, 16 subspecies have been named, with from two to seven subspecies recognized as valid by different authors. None of the subspecies were, however, described within a clear conceptual framework. Using the modern concept of a subspecies, I analyzed subspecies of E. barbara recognized by recent authors. I gathered morphometric data from 155 specimens in mammal collections, georeferenced each specimen, and recorded membership to subspecies assigned by different references and by its location. I gathered climate and geographic data for each location. I analyzed data using Principal Components Analysis (PCA) and analysis of variance (ANOVA). Specimens exhibited sexual dimorphism in size but not in skull shape. I used regression analysis to test for associations between skull shape and size and climate data. Geographic analyses documented that subspecies are not allopatric, violating one of the main properties of the subspecies concept. ANOVA showed significant differences in skull morphology between some pairs of recognized subspecies but not others. However, none of the subspecies segregated in the PCA. Thus, the recognized subspecies could not be diagnosed from morphological data, violating another property of the subspecies concept. Size varied greatly between the sexes using different schemes for recognized subspecies. Climate variables explained between 4% and 6% of size variation for males and females. Skull shape proved not to be geographically variable.
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