Cranial variation in species and subspecies of kangaroo rats (Dipodomys, Dipodomyinae, Rodentia) according to geometric morphometrics.

Traditional Dipodomys (sub)species identification uses geography, phenotype, and external/skull measurements. Such measurements are correlated with size and thus redundant. I assessed the value of scaled cranial shape, based on two-dimensional landmarks (analyzed using geometric morphometric methods) in distinguishing Dipodomys taxa, and in summarizing their variation. My dataset includes 601 adult specimens from 20 species (49 operational taxonomic units - OTUs) across 190 localities. Cranial shape was highly useful in classifying Dipodomys taxa without considering geography. The auditory bulla was the most variable region-taxa differed in its hypertrophy, accompanied by different degrees of nearby structure crowding. Cranial shape was weakly allometric, with no significant sexual dimorphism. Weak size dimorphism was detected. (Sub)specific taxonomy is not reflective of shape variation, as the number of subspecies per species is not associated with disparity. Shape had significant phylogenetic signal, but subspecies did not always cluster with conspecifics and species did not always cluster according to phylogenetic relationship/taxonomy. Shape variation was correlated with climate, and species differed in morphological disparity and degree of specialization, which may contribute to divergence in shape variation patterns from phylogeny. D. deserti was the most specialized species, diverging greatly from the genus mean; D. heermanni was the least specialized. This study provides new insights into morphological variation of North American keystone species, several of conservation interest, for example, D. heermanni berkeleyensis, D. h. dixoni, D. nitratoides brevinasus, and D. n. nitratoides.

The earliest dipodomyine heteromyid in North America and the phylogenetic relationships of geomorph rodents.

Dipodomyine heteromyids (kangaroo rats and mice) are a diverse group of arid-adapted ricochetal rodents of North America. Here, a new genus and species of a large dipodomyine is reported from early Miocene-aged deposits of the John Day Formation in Oregon that represents the earliest record of the subfamily. The taxon is known from a single specimen consisting of a nearly complete skull, dentary, partial pes, and caudal vertebra. The specimen is characterized by a mosaic of ancestral and highly derived cranial features of heteromyids. Specifically, the dental morphology and some cranial characteristics are similar to early heteromyids, but other aspects of morphology, including the exceptionally inflated auditory bullae, are more similar to known dipodomyines. This specimen was included in a phylogenetic analysis comprising 96 characters and the broadest sampling of living and extinct geomorph rodents of any morphological phylogenetic analysis to date. Results support the monophyly of crown-group Heteromyidae exclusive of Geomyidae and place the new taxon within Dipodomyinae. The new heteromyid is the largest known member of the family. Analyses suggest that large body size evolved several times within Heteromyidae. Overall, the morphology of the new heteromyid supports a mosaic evolution of the open-habitat adaptations that characterize kangaroo rats and mice, with the inflation of the auditory bulla appearing early in the group, and bipedality/ricochetal locomotion appearing later. We hypothesize that cooling and drying conditions in the late Oligocene and early Miocene favored adaptations for life in more open habitats, resulting in increased locomotor specialization in this lineage over time from a terrestrial ancestor.

Niche partitioning in an assemblage of granivorous rodents, and the challenge of community-level conservation.

Coexistence of competing species in the same foraging guild has long puzzled ecologists. In particular, how do small subordinate species persist with larger dominant competitors? This question becomes particularly important when conservation interventions, such as reintroduction or translocation, become necessary for the smaller species. Exclusion of dominant competitors might be necessary to establish populations of some endangered species. Ultimately, however, the goal should be to conserve whole communities. Determining how subordinate species escape competitive exclusion in intact communities could inform conservation decisions by clarifying the ecological conditions and processes required for coexistence at local or regional scales. We tested for spatial and temporal partitioning among six species of native, granivorous rodents using null models, and characterized the microhabitat of each species using resource-selection models. We found that the species' nightly activity patterns are aggregated temporally but segregated spatially. As expected, we found clear evidence that the larger-bodied kangaroo rats drive spatial partitioning, but we also found species-specific microhabitat associations, which suggests that habitat heterogeneity is part of what enables these species to coexist. Restoration of natural disturbance regimes that create habitat heterogeneity, and selection of translocation sites without specific competitors, are among the management recommendations to consider in this case. More generally, this study highlights the need for a community-level approach to conservation and the usefulness of basic ecological data for guiding management decisions.

Effects of artificial light at night on the foraging behavior of an endangered nocturnal mammal.

Modification of nighttime light levels by artificial illumination (artificial light at night; ALAN) is a rapidly increasing form of human disturbance that affects natural environments worldwide. Light in natural environments influences a variety of physiological and ecological processes directly and indirectly and, as a result, the effects of light pollution on species, communities and ecosystems are emerging as significant. Small prey species may be particularly susceptible to ALAN as it makes them more conspicuous and thus more vulnerable to predation by visually oriented predators. Understanding the effects of disturbance like ALAN is especially important for threatened or endangered species as impacts have the potential to impede recovery, but due to low population numbers inherent to at-risk species, disturbance is rarely studied. The endangered Stephens' kangaroo rat (SKR), Dipodomys stephensi, is a nocturnal rodent threatened by habitat destruction from urban expansion. The degree to which ALAN impacts their recovery is unknown. In this study, we examined the effects of ALAN on SKR foraging decisions across a gradient of light intensity for two types of ALAN, flood and bug lights (756 vs 300 lumen, respectfully) during full and new moon conditions. We found that ALAN decreased probability of resource patch depletion compared to controls. Moreover, lunar illumination, distance from the light source and light type interacted to alter SKR foraging. Under the new moon, SKR were consistently more likely to deplete patches under control conditions, but there was an increasing probability of patch depletion with distance from the source of artificial light. The full moon dampened SKR foraging activity and the effect of artificial lights. Our study underscores that ALAN reduces habitat suitability, and raises the possibility that ALAN may impede the recovery of at-risk nocturnal rodents.

The Contributions of Individual Muscle-Tendon Units to the Plantarflexor Group Force-Length Properties.

The combined force-length (F-L) properties of a muscle group acting synergistically at a joint are determined by several aspects of the F-L properties of the individual musculotendon units. Namely, misalignment of the optimal lengths of the individual muscles will affect the group F-L properties. This misalignment, which we named [Formula: see text], arises from the properties of the muscles (i.e., optimum fiber length and pennation angle) and of their tendons (i.e., compliance and slack length). The aim of this study was to measure the F-L properties of kangaroo rat plantarflexors as a group and individually and determine the effects of [Formula: see text] on the group F-L properties. Specifically, we performed a sensitivity analysis to quantify how [Formula: see text] influences the tradeoff between maximizing the peak force vs. having a wider group F-L curve. In the kangaroo rat, we found that the optimal lengths of two bi-articular musculotendon units, the plantaris and the gastrocnemius, were misaligned by 1.8 mm, but this amount favored maximal peak force rather than increasing F-L curve width. Because we measured the misalignment in situ, we could directly assess the tradeoff between maximizing peak force vs. a wider F-L curve without making modeling assumptions about the individual muscle or tendon properties.

Functional connectivity and home range inferred at a microgeographic landscape genetics scale in a desert-dwelling rodent.

Gene flow in animals is limited or facilitated by different features within the landscape matrix they inhabit. The landscape representation in landscape genetics (LG) is traditionally modeled as resistance surfaces (RS), where novel optimization approaches are needed for assigning resistance values that adequately avoid subjectivity. Also, desert ecosystems and mammals are scarcely represented in LG studies. We addressed these issues by evaluating, at a microgeographic scale, the effect of landscape features on functional connectivity of the desert-dwelling Dipodomys merriami. We characterized genetic diversity and structure with microsatellites loci, estimated home ranges and movement of individuals using telemetry-one of the first with rodents, generated a set of individual and composite environmental surfaces based on hypotheses of variables influencing movement, and assessed how these variables relate to individual-based gene flow. Genetic diversity and structure results evidenced a family-induced pattern driven by first-order-related individuals, notably determining landscape genetic inferences. The vegetation cover and soil resistance optimized surface (NDVI) were the best-supported model and a significant predictor of individual genetic distance, followed by humidity and NDVI+humidity. Based on an accurate definition of thematic resolution, we also showed that vegetation is better represented as continuously (vs. categorically) distributed. Hence, with a nonsubjective optimization framework for RS and telemetry, we were able to describe that vegetation cover, soil texture, and climatic variables influence D. merriami's functional connectivity at a microgeographic scale, patterns we could further explain based on the home range, habitat use, and activity observed between sexes. We describe the relationship between environmental features and some aspects of D. merriami's behavior and physiology.

Uterine Receptivity in Merriam's Kangaroo Rat (Dipodomys merriami).

The uterine surface undergoes significant remodeling, termed the "plasma membrane transformation," during pregnancy to allow for implantation of the blastocyst and formation of the placenta in viviparous amniote vertebrates. Unlike other species within the superorder Euarchontoglires, which have a hemochorial (highly invasive) placenta, kangaroo rats (Dipodomys spp.) exhibit a less invasive endotheliochorial placenta. We characterized the changes that occur to membrane molecules and the cellular ultrastructure of the uterine epithelium during early pregnancy in Merriam's kangaroo rat, Dipodomys merriami using electron microscopy and immunofluorescence microscopy. Epithelial cadherin (E-cadherin) is an adhesion protein that forms the adherens junction and is localized to the lateral plasma membrane of uterine epithelium during the nonreproductive state but localizes nonspecifically in the uterine epithelium immediately preceding implantation. Desmosomes are a type of cadherin that form junctional complexes along the lateral plasma membrane of epithelium. Dsg-2, a marker for desmosomes, is localized along the lateral plasma membrane in non-pregnant animals but redistributes to the apical region of the lateral plasma membrane during early pregnancy. The shift in desmosome and cadherin distribution before implantation suggests that there is a reduction in lateral adhesion between epithelial cells to allow for invasion by the blastocyst. Surprisingly, although Kangaroo rats form a less invasive placenta, these same changes occur during pregnancy in species with highly invasive placentation, such as the laboratory rat and human. These commonalities suggest that it is not through the retention of lateral adhesion that the blastocyst is prevented from further invasion in this rodent species. Anat Rec, 301:1928-1935, 2018. © 2018 Wiley Periodicals, Inc.

A multispecies test of source-sink indicators to prioritize habitat for declining populations.

For species at risk of decline or extinction in source-sink systems, sources are an obvious target for habitat protection actions. However, the way in which source habitats are identified and prioritized can reduce the effectiveness of conservation actions. Although sources and sinks are conceptually defined using both demographic and movement criteria, simplifications are often required in systems with limited data. To assess the conservation outcomes of alternative source metrics and resulting prioritizations, we simulated population dynamics and extinction risk for 3 endangered species. Using empirically based habitat population models, we linked habitat maps with measured site- or habitat-specific demographic conditions, movement abilities, and behaviors. We calculated source-sink metrics over a range of periods of data collection and prioritized consistently high-output sources for conservation. We then tested whether prioritized patches identified the habitats that most affected persistence by removing them and measuring the population response. Conservation decisions based on different source-sink metrics and durations of data collection affected species persistence. Shorter time series obscured the ability of metrics to identify influential habitats, particularly in temporally variable and slowly declining populations. Data-rich source-sink metrics that included both demography and movement information did not always identify the habitats with the greatest influence on extinction risk. In some declining populations, patch abundance better predicted influential habitats for short-term regional persistence. Because source-sink metrics (i.e., births minus deaths; births and immigrations minus deaths and emigration) describe net population conditions and cancel out gross population counts, they may not adequately identify influential habitats in declining populations. For many nonequilibrium populations, new metrics that maintain the counts of individual births, deaths, and movement may provide additional insight into habitats that most influence persistence.

A mast-seeding desert shrub regulates population dynamics and behavior of its heteromyid dispersers.

Granivorous rodent populations in deserts are primarily regulated through precipitation-driven resource pulses rather than pulses associated with mast-seeding, a pattern more common in mesic habitats. We studied heteromyid responses to mast-seeding in the desert shrub blackbrush (Coleogyne ramosissima), a regionally dominant species in the Mojave-Great Basin Desert transition zone. In a 5-year study at Arches National Park, Utah, USA, we quantified spatiotemporal variation in seed resources in mast and intermast years in blackbrush-dominated and mixed desert vegetation and measured responses of Dipodomys ordii (Ord's kangaroo rat) and Perognathus flavescens (plains pocket mouse). In blackbrush-dominated vegetation, blackbrush seeds comprised >79% of seed production in a mast year, but 0% in the first postmast year. Kangaroo rat abundance in blackbrush-dominated vegetation was highest in the mast year, declined sharply at the end of the first postmast summer, and then remained at low levels for 3 years. Pocket mouse abundance was not as strongly associated with blackbrush seed production. In mixed desert vegetation, kangaroo rat abundance was higher and more uniform through time. Kangaroo rats excluded the smaller pocket mice from resource-rich patches including a pipeline disturbance and also moved their home range centers closer to this disturbance in a year of low blackbrush seed production. Home range size for kangaroo rats was unrelated to seed resource density in the mast year, but resource-poor home ranges were larger (P < 0.001) in the first postmast year, when resources were limiting. Blackbrush seeds are higher in protein and fat but lower in carbohydrates than the more highly preferred seeds of Indian ricegrass (Achnatherum hymenoides) and have similar energy value per unit of handling time. Kangaroo rats cached seeds of these two species in similar spatial configurations, implying that they were equally valued as stored food resources. Blackbrush mast is a key resource regulating populations of kangaroo rats in this ecosystem.

The complete mitochondrial genome of the Dipodomys ordii (Ord's kangaroo rat).

Ord's kangaroo rat is a kangaroo rat native to western North America. In this study, we first reported the complete mitochondrial genome of Dipodomys ordii that the first has the complete mitochondrial genome in the genus of Heteromyidae. The mitogenome is a circular molecule of 16 257 bp in length, containing 13 protein-coding genes, 2 ribosomal RNAs, 22 transfer RNAs and a putative displacement loop region. All protein-coding genes started with a traditional ATN codon and terminated with the mitochondria stop codon (TAA/TAG/AGA) or a single T base. The gene order and composition of mitogenome was similar to that of most other Sciurognathi species and its GC content was 36.73%. Thirteen protein-coding genes of D. ordii together with eight other closely species were used to construct the species phylogenetic tree for verification of the accuracy of new determined mitogenome sequences.

Natural selection and the genetic basis of osmoregulation in heteromyid rodents as revealed by RNA-seq.

One adaptation of ecological and evolutionary interest is the extraordinary ability of desert rodents to retain water during waste production. Much is known regarding the unique kidney physiology of kangaroo rats (Dipodomys spp.) and their ability to retain water during waste production, yet the genetic basis of these physiological adaptations is relatively unknown. Herein, we utilized RNA-seq data to conduct a comparative study to identify osmoregulatory genes expressed in heteromyid rodents. We sequenced kidney tissue from two temperate desert species (Dipodomys spectabilis and Chaetodipus baileyi) from two separate subfamilies of the Heteromyidae and compared these transcriptomes to a tropical mesic species (Heteromys desmarestianus) from a third subfamily. The evolutionary history of these subfamilies provided a robust phylogenetic control that allowed us to separate shared evolutionary history from convergence. Using two methods to detect differential expression (DE), we identified 1890 genes that showed consistent patterns of DE between the arid and mesic species. A three-species reciprocal BLAST analysis revealed 3511 sets of putative orthologues that, upon comparison to known Mus musculus sequences, revealed 323 annotated and full-length genic regions. Selection tests displayed evidence of positive selection (dn/ds > 1) on six genes in the two desert species and remained significant for one of these genes after correction for multiple testing. Thus, our data suggest that both the coding sequence and expression of genes have been shaped by natural selection to provide the genetic architecture for efficient osmoregulation in desert-adapted heteromyid rodents.

Using imputation and mixture model approaches to integrate multi-state capture-recapture models with assignment information.

In this article, we first extend the superpopulation capture-recapture model to multiple states (locations or populations) for two age groups., Wen et al., (2011; 2013) developed a new approach combining capture-recapture data with population assignment information to estimate the relative contributions of in situ births and immigrants to the growth of a single study population. Here, we first generalize Wen et al., (2011; 2013) approach to a system composed of multiple study populations (multi-state) with two age groups, where an imputation approach is employed to account for the uncertainty inherent in the population assignment information. Then we develop a different, individual-level mixture model approach to integrate the individual-level population assignment information with the capture-recapture data. Our simulation and real data analyses show that the fusion of population assignment information with capture-recapture data allows us to estimate the origination-specific recruitment of new animals to the system and the dispersal process between populations within the system. Compared to a standard capture-recapture model, our new models improve the estimation of demographic parameters, including survival probability, origination-specific entry probability, and especially the probability of movement between populations, yielding higher accuracy and precision.

Effects of bannertail kangaroo rat mounds on small-scale plant community structure.

The effects of bannertail kangaroo rat (Dipodomys spectabilis) mounds and associated soil-surface disturbance on plant species composition and diversity in the Chihuahuan Desert were examined with multivariate analysis. Kangaroo rat mounds created disturbance gaps and contributed to local species diversity by creating microhabitats that supported unique plant communities. These microhabitats supported populations of species that were relatively rare in surrounding areas. The diversity observed at the whole habitat level resulted from (1) local spatial heterogeneity, because the mounds offered microenvironments with distinctive nutrient, water, and light conditions; and (2) local patterning of disturbance, because the digging and traffic of the kangaroo rats maintained high levels of soil disturbance at and near the mounds. At a finer scale, species diversity was highest in the area immediately adjacent to active and inactive mounds, and was lower on both the highly disturbed soil of the mounds and in the relatively undisturbed area between mounds. Lowest species diversity occurred on inactive mounds. Annual plant biomass was much greater on mounds than in inter-mound areas. The results support the predictions that intermediate levels of disturbance and small-scale environmental heterogeneity contribute to supporting high species diversity.

The influence of seed apparency, nutrient content and chemical defenses on dietary preference in Dipodomys ordii.

Physical, nutritional and defensive qualities of seeds differ in the extent to which they influence granivore preference. In a study aimed to quantifying those differences, Ord's kangaroo rats (Dipodomys ordii) were found to prefer the seeds of just three of twenty-nine species: Cryptantha crassisepala, Oryzopsis hymenoides and Salsola kali. Oryzopsis hymenoides was most preferred during the early plant growth season (April-July); preference for S. kali peaked during late (August-November) and dormant (December-March) seasons; and greatest preference for C. crassisepala occurred during dormant and early seasons. Regression of forage ratios, averaged across seasons, against seed length, mass, abundance, patchiness, percent nitrogen, energy content, and chemical defenses showed seed length to be the most important predictor of seed preference. Seed length combined with nitrogen (protein) content and levels of two defensive compounds, saponins and non-protein amino acids, to account for 68% of the variation in seed preference. The importance of seed length rather than biomass indicated that there are limits to the ability of D. ordii to detect small seeds and that small size facilitated escape of dispersed seeds. Seasonality in preference suggested, however, that seed escape was encountered by predispersal harvesting of newly maturing seeds still on plants. Maximization of protein intake contradicted previously published observations, but presumably reflected low nitrogen availability. In addition to small size, the presence of saponins or non-protein amino acids in seeds was sufficient to negate the positive influence of higher protein content.