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We define a genetic species as a group of genetically compatible interbreeding natural populations that is genetically isolated from other such groups. This focus on genetic isolation rather than reproductive isolation distinguishes the Genetic Species Concept from the Biological Species Concept. Recognition of species that are genetically isolated (but not reproductively isolated) results in an enhanced understanding of biodiversity and the nature of speciation as well as speciation-based issues and evolution of mammals. We review criteria and methods for recognizing species of mammals and explore a theoretical scenario, the Bateson–Dobzhansky–Muller (BDM) model, for understanding and predicting genetic diversity and speciation in mammals. If the BDM model is operating in mammals, then genetically defined phylogroups would be predicted to occur within species defined by morphology, and phylogroups experiencing stabilizing selection will evolve genetic isolation without concomitant morphological diversification. Such species will be undetectable using classical skin and skull morphology (Morphological Species Concept). Using cytochrome-b data from sister species of mammals recognized by classical morphological studies, we estimated the number of phylogroups that exist within mammalian species and hypothesize that there will be >2,000 currently unrecognized species of mammals. Such an underestimation significantly affects conclusions on the nature of speciation in mammals, barriers associated with evolution of genetic isolation, estimates of biodiversity, design of conservation initiatives, zoonoses, and so on. A paradigm shift relative to this and other speciation-based issues will be needed. Data that will be effective in detecting these “morphologically cryptic genetic species” are genetic, especially DNA-sequence data. Application of the Genetic Species Concept uses genetic data from mitochondrial and nuclear genomes to identify species and species boundaries, the extent to which the integrity of the gene pool is protected, nature of hybridization (if present), and introgression. Genetic data are unique in understanding species because the use of genetic data 1) can quantify genetic divergence from different aspects of the genome (mitochondrial and nuclear genes, protein coding genes, regulatory genes, mobile DNA, microsatellites, chromosomal rearrangements, heterochromatin, etc.); 2) can provide divergence values that increase with time, providing an estimate of time since divergence; 3) can provide a population genetics perspective; 4) is less subject to convergence and parallelism relative to other sets of characters; 5) can identify monophyly, sister taxa, and presence or absence of introgression; and 6) can accurately identify hybrid individuals (kinship and source of hybrid individuals, F1s, backcrosses, direction of hybridization, and in concert with other data identify which hybrids are sterile or fertile). The proposed definition of the Genetic Species Concept is more compatible with a description of biodiversity of mammals than is “reproductively isolated species.” Genetic profiles of mammalian species will result in a genetic description of species and mammalian diversity, and such studies are being accelerated by technological advances that reduce cost and increase speed and efficiency of generating genetic data. We propose that this genetic revolution remain museum- and voucher specimen–based and that new names are based on a holotype (including associated tissues) deposited in an accredited museum.
The oldest known species of the genus Didelphis (Mammalia, Marsupialia, Didelphidae) is described here. The holotype and only known specimen comes from the late Miocene deposits of the Solimões Formation at Patos, Acre River, Brazil. The new species is one of only a few marsupials known from this assemblage. The new species differs from other known species by its smaller size, low mandibular ramus, smaller molars relative to premolars, and p3 with inflated crown. The last feature suggests more frugivorous habits than in other species of the genus.
Complete DNA sequences obtained from the mitochondrial cytochrome-b gene were examined in 41 individuals representing 11 currently recognized species of Geomys. Similar tree topologies were obtained from parsimony, genetic distance, likelihood, and Bayesian methods of data analyses. Phylogenetic relationships indicated 4 major clades that are referred to as species groups (bursarius, breviceps, personatus, and pinetis). The results also suggest the existence of several cryptic species that warrant further investigation.
The islands of the Gulf of California are considered protected natural areas by the Mexican government. However, mammals in these islands face major threats and possible extinction because of the introduction of exotic species. Dipodomys insularis is endemic to San José Island, and has been declared a critically endangered species by the World Conservation Union. Surveys undertaken since 1989 had been unsuccessful in documenting the presence of this species, leading to the conclusion that extinction may have occurred because of the presence of feral cats on the island. After 15 years of unsuccessful surveys, we rediscovered D. insularis in 2005. Kangaroo rats were captured at 5 locations on the island within a total area of less than 30 km2. Fecal analyses showed that D. insularis is not a usual prey item of feral cats. A discriminant function analysis allocated 99.29% of the heteromyid upper incisors recovered from scats to Chaetodipus spinatus (P > 0.97), whereas only 2 incisors (0.71%) were allocated to D. insularis. The actual extent of damage to the native biota caused by the introduction of cats remains unknown.
In this study we provide data on morphological and morphometric variation in specimens of Peromyscus zarhynchus from 6 different geographically isolated localities in Chiapas, Mexico. We found significant differences in the mean greatest skull length in all specimens examined of P. zarhynchus, but we did not find differences in other cranial and external variables related to age, sex, and individual variation. The individuals examined from different populations of P. zarhynchus showed distinctive morphometric characters correlated with their distribution, and probably to feeding changes related to different types of vegetation and weather in Chiapas.
The southern hairy-nosed wombat (Lasiorhinus latifrons) is a cryptic, primarily nocturnal marsupial, for which behavioral information is notably lacking. Animals that are difficult to observe can be identified and tracked by individual-specific genotypes obtained from remotely collected DNA sources; wombats are excellent candidates for such an approach because freshly plucked hair is easily captured at burrow entrances. Twice a year during 1999–2001, we employed an intensive remote hair-collection regime coupled with individual-resolution genetic analysis to sample a South Australian population in a 63.3-km2 protected conservation reserve. Individuals were identified using 5 highly polymorphic microsatellite markers and further examined using another 10 markers to resolve ambiguities, enabling assessment of burrow- and space-use patterns. Analyses of rate of discovery of new individuals indicated that nearly all wombats inhabiting the study area were detected (102); there were >1,000 “capture” events, and 90% of individuals were detected multiple times. Surprisingly, a female sex bias existed despite females being the dispersing sex. Space use was conservative and likely a reflection of adaptations enabling energy conservation. Transits between the northern and southern sections of the study area were nearly nonexistent. No sex or consistent seasonal differences were found in burrow, warren, or space use, other than in interaction with other factors. However, a strong increase in activity and space use in September 2001 relative to other sampling periods may be attributed to activities associated with mating. The thoroughness and evenness of this study's sampling strategy was markedly effective for this species, as, with appropriate modification and optimization, it will likely be for other shy and cryptic organisms.
Soricine shrews are typified by the presence of reddish pigment in their tooth enamel. This coloration is caused by iron and is thought to make the enamel more resistant to wear. Ten specimens of Blarina brevicauda were examined for percentage iron concentration using a scanning electron microscope in conjunction with an energy-dispersive spectrometer. Substantial iron variation was found between individual molar cusps and between different tooth positions. Specifically, the cusps associated with crushing and grinding, as opposed to shearing, had more iron incorporated into their enamel. In addition, the enlarged m1 exhibits higher iron density than the more-posterior teeth. These results suggest that increased iron density is expressed on teeth, and parts of teeth, that are subject to greatest stresses and are most prone to fracture and excessive wear.
Although interactions between behavior, demography, and genetic diversity have been studied extensively for neutral molecular markers, relationships among these variables remain poorly understood for loci that are subject to selection. The genes of the major histocompatibility complex (MHC) provide a particularly appropriate opportunity to examine the impact of selection on genetic structure; the high levels of polymorphism characteristic of these loci are thought to be maintained by selective pressures arising due to pathogen exposure and inbreeding depression, both of which may be influenced by behavior and demography. To explore interactions among population structure, selection, and genetic diversity, we compared levels and patterns of MHC variability in 2 demographically distinct populations of the Talas tuco-tuco (Ctenomys talarum), a subterranean rodent that occurs in eastern Argentina. Specifically, we tested the prediction that selection on 2 class II loci (DRB and DQA) should be greater in the more dense, more inbred Mar de Cobo population. At both loci, allelism and heterozygosity were greater for Mar de Cobo than for Necochea. Similarly, for both loci, estimates of the intensity of selection (corrected for differences in effective population size) were greater for Mar de Cobo, as predicted based on demographic and behavioral differences between the study populations. Interlocus differences in variability are examined with respect to the apparent function(s) of these genes, whereas interpopulation differences in intensity of selection are evaluated with regard to the demonstrated behavioral and demographic differences between Necochea and Mar de Cobo.
Body condition directly affects survival and reproduction by animals, so its effects on fitness represent an important component of animal ecology. Traditionally, ecologists have relied on direct chemical analysis or morphometric indices to assess body condition. We examined the ability of morphometric indices and bioelectrical impedance analysis to estimate body condition of raccoons (Procyon lotor) and assessed the need for species-specific models. Morphological indices were poor estimators of body condition; the best model explained 62% of the variation of fat and had a high SE (r2 = 0.62, SE = 0.52, P < 0.001). Bioelectrical impedance analysis proved to be a reliable way to noninvasively estimate body condition. Models for lean dry mass and total body water were used to accurately estimate body fat (r2 = 0.94, SE = 0.16, P < 0.001). Body fat estimates derived through models for a similar species performed better than morphometric indices but did not achieve the accuracy of the species-specific model. Examination of our data highlights the need to validate models used to estimate body condition before use.
In a 2-year study of the bush dog (Speothos venaticus), a small canid from Central and South America, we examined the reproductive physiology of mature females and the effect of male presence on the incidence and timing of ovulation. Fecal hormones, vulvar measurements, and mating behavior were used to characterize reproductive cycle dynamics. As described for all other canids, female bush dogs have an obligate pseudopregnancy after an infertile mating or ovulation without mating. However, the female cycle is not fixed to a single rigid breeding season each year, as in most canids. Unlike other canids, the presence of a male was associated with shortened interestrous intervals and increased number of estrous cycles. Examination of preliminary testosterone data from males showed a nonseasonal pattern suggesting that males have year-round, not seasonal, sperm production. The results from this study, including the validation of the noninvasive fecal hormone monitoring technique used, can provide managers of captive animals with tools for optimizing breeding potential of this species.
We investigated daily activity patterns of the long-nosed mouse (Oxymycterus nasutus) in a high-elevation grassland field in southern Brazil. We censused the animals every other month from June 2001 to May 2002, determining capture time with digital timing devices attached to traps. Activity patterns were markedly diurnal and did not differ between sex or age classes. Captures were more frequent just after sunrise and just before sunset. Daily activity was strongly influenced by ambient light, with animals showing seasonal changes in their activity time according to day length but with some activity at night. Nocturnal captures were positively related with night brightness measured in log lm/m2 (logistic regression; odds ratio = 1.76, P < 0.001). Temperature positively influenced the probability of capture of O. nasutus during daylight hours (quadratic regression; r2 = 0.76, d.f. = 11, P < 0.001), with the highest predicted capture probability at 3–6°C and a sharp reduction above 21°C. Although diurnal activity has been reported for other Oxymycterus species this is the 1st study to rigorously quantify diurnal activity of a neotropical rodent in the field. O. nasutus apparently showed a more strictly diurnal pattern than described for other congeners.
The river otter (Lontra canadensis) has a complex social system, which varies widely across its range. We examined patterns of space use and social interactions for a native population of river otters in southeastern Minnesota. We radiomarked 28 river otters and monitored annual home ranges and core areas, static and dynamic interactions, and site fidelity. We compared these characteristics and interactions between sexes and age classes. Annual home ranges of male river otters were 3.2 times greater than those of females (P = 0.042), and annual core areas of males were 2.9 times greater than those of females (P = 0.083). The static interactions among river otters were extensive, with 69% of the individuals exhibiting core-area overlap. Overall dynamic interactions were positive (i.e., animals were closer together than expected). Males used 74% of their year 1 home range during year 2, and females used 75%. Females on average used only 39% of their core area from year 1 during year 2, whereas males used 65%. In general, conspecifics were not excluded from home ranges or core areas and signs of cooperation were evident, suggesting that river otters in southeastern Minnesota were social rather than territorial.
We studied the home-range and core-area size and overlap of Tehuantepec jackrabbits (Lepus flavigularis) by radiotracking 32 individuals between May 2001 and April 2003 in savanna habitat in the Isthmus of Tehuantepec, Oaxaca, Mexico. Annual home-range and core-area sizes averaged 55 ha ± 8 SE and 8 ± 1 ha for 10 adults of both sexes using the 95% and 50% fixed-kernel isopleths, respectively. Seasonal home ranges varied widely for adults, from 15 to 111 ha for females and from 24 to 166 ha for males. Juvenile males had larger seasonal home ranges than did juvenile females (X̄ = 80 and 24 ha). For adult jackrabbits, seasonal home ranges were larger during the 1st year compared to those of the 2nd year of study (X̄ = 87 and 49 ha), particularly for females. Home ranges and core areas of Tehuantepec jackrabbits were comparable in size and overlapped between active periods (nocturnal and crepuscular hours) and inactive periods (diurnal hours). Adults overlapped their home ranges with 1–10 individuals. Home-range overlap among females was greater than among males. Females shared portions of their ranges with other females more frequently than did males with other males. Home-range and overlap analysis suggests that Tehuantepec jackrabbits have polygamous mating behavior and nonterritorial social organization.
Using standardized small mammal surveys at 26 Atlantic Forest sites, we evaluated the efficiency and compared the weight of captured species and individuals between large pitfall traps and Sherman traps. We also investigated the effects of climatic variables on daily capture success of pitfalls. Pitfalls were clearly more efficient than Sherman traps, capturing 29 species, of which 16 were captured exclusively with this method, mostly represented by rare species. In contrast, Sherman traps captured 14 species, of which just 1 was not captured with pitfall traps. Compared to Sherman traps, pitfalls captured (per site) 3 times the number of species, 2 times the number of individuals, and significantly more individuals of 7 species. Despite differences in sampling efficiency, positive correlations suggest that at least coarse-scale variation among sites for several assemblage parameters are congruent between the 2 trapping methods. Sherman traps tended to capture adults, whereas pitfalls captured individuals over a broader range of weight classes or tended to capture more juveniles. Total daily capture rates in pitfall traps increased with precipitation. Our results suggest that large pitfall traps are effective at capturing rare species and juveniles, probably because they are less selective, and are thus essential for inventorying the rich and poorly known small mammal fauna of the tropics and for demographic studies.
Previous studies in tropical rain forests suggest that most small mammal species reach their highest densities in disturbed habitats; however, only a few sites have been examined. Consequently, habitat and resource use for many species is poorly understood. This is especially true in the Amazon Basin, where no studies of microhabitat associations of small mammals have been undertaken. We studied relationships with habitat variables and resource abundances for 5 species of marsupials and 9 species of rodents at a site in southeastern Amazonia. Small mammals were sampled with traps placed both on the ground and in the understory. Eight habitat variables were measured to quantify habitat structure. Measures of insect biomass were collected by the use of sticky traps, and fruit abundance was quantified. Patterns of habitat use were examined using logistic regression, multiple regression, and ordinations. Many species showed increased abundances with habitat features indicative of edge-affected or disturbed habitats, showing negative relationships with understory openness, understory woody-stem density, tree density, and tree size; and positive relationships with number of vines per tree, mean log size, number of logs, and volume of downed wood. We obtained support for the hypothesis that the cause of this pattern is increased resource abundances in these areas, because both insect biomass and number of fruiting trees showed similar relationships. However, for many species, measures of resource abundance were not important once habitat features were entered into the models, indicating that the relationship to resources is an indirect one.
We used published data to calculate small-mammal species richness at 43 sites in North America to examine the response of species richness to increasing primary productivity. We estimated species richness for the entire community and for each of 4 functional groups (insectivore, granivore, herbivore, and omnivore). Total richness exhibited a significant unimodal relationship to increasing amounts of annual precipitation and was driven by granivores; this functional group exhibited the most pronounced decline in richness with high precipitation. We suggest that the decline in granivore richness is due to increased litter associated with increased productivity.
To test the association between body size and degree of folivory and to examine the different food habits in sympatric arboreal herbivorous mammals, we investigated diets of 2 flying squirrel species (Petaurista petaurista and Eoglaucomys fimbriatus) sympatrically distributed in the Himalayan moist temperate forest of northern Pakistan. P. petaurista and E. fimbriatus used 27 and 28 tree species, respectively. Both flying squirrel species used the same 27 tree species. However, frequency of tree species used by P. petaurista was significantly different from that used by E. fimbriatus. P. petaurista was significantly more folivorous than was E. fimbriatus. Preference of P. petaurista for leaves may be an important factor preventing competition for resources between these species. We conclude that larger body size in flying squirrels is associated with the tendency toward a foliage diet.
The slow loris (Nycticebus coucang; Lorisidae) is a slow-moving, arboreal mammal with a very low metabolism relative to other eutherian species of its body mass. A slow pace of life has been causally linked to a low intake rate of usable energy due to a diet that is generally low in energy, is unpredictably periodically scarce, and contains high amounts of toxins or digestion inhibitors. To assess whether the slow loris faces any of these limitations, we studied its dietary habits in an area of West Malaysia (Manjung District, Perak State) by direct observations of radiocollared individuals and by fecal analysis. The diet was composed of 5 distinct types of food: floral nectar and nectar-producing parts, phloem sap, fruits, gum (another group of plant exudates), and arthropods. The largest proportion of feeding time was spent on phloem sap (34.9%), floral nectar and nectar-producing parts (31.7%), and fruits (22.5%). These foods should provide high amounts of easily digestible sugars, indicating that slow lorises did not face an energy-poor diet. Dietary habits were indistinguishable between rainy and dry seasons, even though most dry-season data were collected during periods of extreme drought induced by the 1997–1998 El Niño Southern-Oscillation event. However, many genera of food plants contain secondary compounds that are toxic or reduce digestibility. We suggest that low metabolism in slow lorises is at least partly related to the need to detoxify secondary compounds in high-energy plant diet.
Focal observations of sea otter (Enhydra lutris kenyoni) foraging patterns and prey selection were collected in coastal Washington between 1993 and 1999. Records consisted of 13,847 individual dives from 841 feeding bouts ranging from 1 min to >4 h. Average dive time was 55 s ± 0.9 SE and average surface time was 45 s ± 2.3 SE, irrespective of dive success. At least 77% of all dives (n = 10,636) were successful prey captures (dives in low light or of undetermined success were excluded). Prey capture success was significantly lower for subadults (63% ± 5 SE) than adults (82% ± 1 SE; P < 0.001). Sea otters occupying the established population range on the outer coast of Washington fed heavily on bivalves (63%) and had a diverse diet consisting of several prey groups (n = 10). In contrast, sea otters occupying new habitat in the Strait of Juan de Fuca had a restricted diet dominated by >60% red urchins (Strongylocentrotus franciscanus), with only 2 other prey species comprising >10% of their diet. Prey size and prey category were dominant predictor variables in generalized linear models of dive duration and postdive surface duration on successful dives. Significant increases in areal extent of surface canopy of giant kelp (Macrocystis integrifolia) and bull kelp (Nereocystis leutkeana) were found both in the outer coast and the Strait of Juan de Fuca (0.4–0.5 km2 per year, P < 0.05) and suggest increasing suitable habitat for a growing population. The growth and expansion of a small and isolated sea otter population provides a unique opportunity to examine the relationship between dietary diversity and population status and explore similarities and differences between trophic paradigms established for sea otter populations at other localities.
We used fecal analyses to document the diet of ocelots (Leopardus pardalis) and puma (Puma concolor) at 2 sites in central Panama. We detected puma on Barro Colorado Island (BCI) nearly every month during the study but never found evidence of jaguars (Panthera onca) at either site. Both ocelots and puma fed predominantly on mammalian prey, but consumed a diversity of species. Collared peccaries (Pecari tajacu) and Central American red brocket (Mazama temama) were the most important food items for puma, whereas Central American agoutis (Dasyprocta punctata) and sloths (Choloepus hoffmanni and Bradypus variegatus) were the most important for ocelots. Considerable overlap in diet was found between populations and species, but the diet of puma on BCI was significantly different from the 2 ocelot populations in containing more large prey, suggesting that dietary differences between these predator species are chiefly related to their relative body size. Comparing across larger scales, both populations of ocelots in our study ate larger prey than elsewhere in their range, suggesting that their fundamental niche includes more medium-sized prey than their realized niche in other sites. Puma on BCI ate proportionally more peccaries and deer than in most other populations. These unusual diets in the wake of a recent decline or local extinction of jaguars are consistent with a prey shift in response to competitive release.
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