The salt marsh harvest mouse (Reithrodontomys raviventris) is an endangered species, endemic to the San Francisco Bay Estuary, that co-occurs with the more broadly distributed species, the western harvest mouse (Reithrodontomys megalotis). Despite their considerable external morphological similarities, the northern subspecies of salt marsh harvest mice have relatively longer and thicker tails than do western harvest mice, which may be related to their abilities to climb emergent marsh vegetation to avoid tidal inundation. We used micro-CT to compare post-cranial skeletal anatomy between the salt marsh and western harvest mouse, to examine whether the salt marsh harvest mouse's restriction to brackish marshes is associated with skeletal adaptations for scansorial locomotion. We found that salt marsh harvest mice exhibited a deeper 3rd caudal vertebra, a more caudally located longest tail vertebra, craniocaudally longer tail vertebrae, and a longer digit III proximal phalanx than western harvest mice. These phalangeal and vertebral characteristics are known to decrease body rotations during climbing, increase contact with substrates, and decrease fall susceptibility in arboreal mammals, suggesting that the salt marsh harvest mouse may be morphologically specialized for scansorial locomotion, adaptive for its dynamic wetland environment.

Abstract Light detection and ranging (lidar) has emerged as a valuable tool for examining the fine‐scale characteristics of vegetation. However, lidar is rarely used to examine coastal wetland vegetation or the habitat selection of small mammals. Extensive anthropogenic modification has threatened the endemic species in the estuarine wetlands of the California coast, such as the endangered salt marsh harvest mouse (Reithrodontomys raviventris; SMHM). A better understanding of SMHM habitat selection could help managers better protect this species. We assessed the ability of airborne topographic lidar imagery in measuring the vegetation structure of SMHM habitats in a coastal wetland with a narrow range of vegetation heights. We also aimed to better understand the role of vegetation structure in habitat selection at different spatial scales. Habitat selection was modeled from data compiled from 15 small mammal trapping grids collected in the highly urbanized San Francisco Estuary in California, USA. Analyses were conducted at three spatial scales: microhabitat (25 m2), mesohabitat (2025 m2), and macrohabitat (~10,000 m2). A suite of structural covariates was derived from raw lidar data to examine vegetation complexity. We found that adding structural covariates to conventional habitat selection variables significantly improved our models. At the microhabitat scale in managed wetlands, SMHM preferred areas with denser and shorter vegetation and selected for proximity to levees and taller vegetation in tidal wetlands. At the mesohabitat scale, SMHM were associated with a lower percentage of bare ground and with pickleweed (Salicornia pacifica) presence. All covariates were insignificant at the macrohabitat scale. Our results suggest that SMHM preferentially selected microhabitats with access to tidal refugia and mesohabitats with consistent food sources. Our findings showed that lidar can contribute to improving our understanding of habitat selection of wildlife in coastal wetlands and help to guide future conservation of an endangered species.

ContextThe area-isolation paradigm of metapopulation theory predicts that larger and more connected patches have a higher probability of occupancy. Although it may be too simplistic for generalist terrestrial mammals, the area-isolation paradigm may be an effective tool for assessing patch-occupancy for habitat specialists.ObjectivesWe tested predictions of the area-isolation paradigm for the endangered salt marsh harvest mouse (Reithrodontomys raviventris), a habitat specialist living in highly fragmented salt marsh habitat in the San Francisco Estuary (California, USA).MethodsWe surveyed for salt marsh harvest mice at 47 marsh patches throughout their range using a non-invasive genetic survey technique. We used occupancy modeling to estimate the effects of patch size, patch connectivity, matrix urbanization, and several habitat characteristics on occupancy probabilities. We evaluated occupancy at both coarse (e.g., among patches) and fine (e.g., within patches) spatial scales.ResultsPatch size, connectivity, and matrix urbanization had significant effects on patch-occupancy. Within patches, occupancy was positively related to the presence of high-tide escape vegetation. Our data also revealed the extirpation of several geographically distinct populations, consistent with expectations due to reduced patch sizes and connectivity over the past century.ConclusionsPatterns of salt marsh harvest mouse patch-occupancy were consistent with the area-isolation paradigm. In addition, our models provide important guidelines of patch size and connectivity that can inform habitat conservation and restoration for this endangered species. Specifically, our data suggests that selecting restoration sites that are well-connected may be more beneficial than selecting larger, isolated sites.

Coastal wetland ecosystems support unique biodiversity and are imminently threatened by climate change-driven sea level rise. However, the impact of climate change on their demographic and evolutionary histories is poorly understood. To improve our understanding, we examined how past climatic events have shaped the evolutionary history of the salt marsh harvest mouse ( Reithrodontomys raviventris ), an endangered species and a salt marsh habitat specialist, completely restricted to coastal wetlands in the San Francisco Estuary (SFE). We used whole mitochondrial genome sequences of 102 salt marsh harvest mice to characterize phylogeography and demographic history. Then, we predicted the ancient distribution of salt marsh habitat and examined correspondence between divergence, demographic history, and changes in ancient marsh habitat caused by sea level rise. A Bayesian Skyline Plot revealed demographic expansions during periods of sea level rise, particularly during the formation of the modern SFE (~ 10 kya), and rapid decline consistent with recent anthropogenic landscape change. Bayesian estimates of divergence time were consistent with subspecies divergence ~ 10 kya, and subpopulation divergence ~ 5 kya, consistent with multiple episodes of vicariance caused by Holocene sea level rise. Spatial Analysis of Molecular Variance and Φ ST revealed a mismatch between the morphological and molecular subspecies assignment of two populations. Our study implicates sea level rise as a force of demographic change and evolutionary divergence in coastal marsh ecosystems. Our study also aids conservation of an endangered species by clarifying genetic subspecies boundaries and highlighting the unique nature of isolated populations that are increasingly threatened by modern sea level rise.

The salt marsh harvest mouse (Reithrodontomys raviventris; RERA) is an endangered species endemic to the coastal wetlands of the San Francisco Estuary, California. RERA are specialized to saline coastal wetlands, and their historical range has been severely impacted by landscape conversion and the introduction of non-native plant and rodent species. A better understanding of their diet is needed to assess habitat quality, particularly in relation to potential competitors. We investigated three questions using DNA metabarcoding with ITS2 and trnL markers: (1) Do RERA specialize on the native plant, pickleweed (Salicornia pacifica), (2) Do RERA consume non-native plants, and (3) What is the dietary niche breadth and overlap with three sympatric native and non-native rodents? RERA diet was dominated by two plants, native Salicornia and non-native salt bush (Atriplex spp.), but included 48 plant genera. RERA diet breadth was narrowest in fall, when they consumed the highest frequencies of Salicornia and Atriplex, and broadest in spring, when the frequencies of these two plants were lowest. Diet breadth was slightly lower for RERA than for co-occurring species in pairwise comparisons. All four species consumed similarly high frequencies of wetland plants, but RERA consumed fewer grasses and upland plants, suggesting that it may be less suited to fragmented habitat than sympatric rodents. Diet overlap was lowest between RERA and the native California vole (Microtis californicus). In contrast, RERA diet overlapped substantially with the native western harvest mouse (R. megalotis) and non-native house mouse (Mus musculus), suggesting potential for competition if these species become sufficiently abundant.

Noninvasive genetic surveys, often conducted by collecting fecal samples, have become a popular tool for surveying wildlife, but have primarily been applied to species with large and conspicuous scat. Although many small mammals are threatened, endangered, or data deficient, noninvasive genetic surveys have rarely been applied due to the challenges of detecting their inconspicuous fecal pellets. As part of a broader study of the endangered salt marsh harvest mouse (Reithrodontomys raviventris), we developed a noninvasive genetic survey technique for the community of small mammals in their putative range. We designed bait stations to passively collect fecal samples from rodents, and developed a multiplex primer set that amplified unique fragment sizes for salt marsh harvest mice and four other sympatric species. We tested the primer set on positive controls and on fecal pellets collected from bait stations at two regularly monitored field sites known to have very different densities of salt marsh harvest mice. The multiplex amplified DNA from all five species, even when all five species were present in a single sample. A positive species identification was made for all field-collected samples, and 43% of these field-collected samples had multispecies detections. The combination of bait stations and genetic species identification proved to be an effective means of noninvasively surveying small mammals in potential salt marsh harvest mouse habitat. The sampling technique should be applicable to a wide variety of small mammals in other systems.

Preserving the genetic diversity of endangered species is fundamental to their conservation and requires an understanding of genetic structure. In turn, identification of landscape features that impede gene flow can facilitate management to mitigate such obstacles and help with identifying isolated populations. We conducted a landscape genetic study of the endangered salt marsh harvest mouse ( Reithrodontomys raviventris ), a species endemic to the coastal marshes of the San Francisco Estuary of California. We collected and genotyped > 500 samples from across the marshes of Suisun Bay which contain the largest remaining tracts of habitat for the species. Cluster analyses and a population tree identified three geographically discrete populations. Next, we conducted landscape genetic analyses at two scales (the entire study area and across the Northern Marshes) where we tested 65 univariate models of landscape features and used the best supported to test multivariable analyses. Our analysis of the entire study area indicated that open water and elevation (> 2 m) constrained gene flow. Analysis of the Northern Marshes, where low elevation marsh habitat is more continuous, indicated that geographic distance was the only significant predictor of genetic distance at this scale. The identification of a large, connected population across Northern Marshes achieves a number of recovery targets for this stronghold of the species. The identification of landscape features that act as barriers to dispersal enables the identification of isolated and vulnerable populations more broadly across the species range, thus aiding conservation prioritization.

Few studies have evaluated the optimal sampling design for tracking small mammal population trends, especially for rare or difficult to detect species. Spatially explicit capture-recapture (SECR) models present an advancement over non-spatial models by accounting for individual movement when estimating density. The salt marsh harvest mouse (SMHM; Reithrodontomys raviventris) is a federal and California state listed endangered species endemic to the San Francisco Bay-Delta estuary, California, USA; where a population in a subembayment has been continually monitored over an 18-year period using mark-recapture methods. We analyzed capture data within a SECR modeling framework that allowed us to account for differences in detection and movement between sexes. We compared the full dataset to subsampling scenarios to evaluate how the grid size (area) of the trap design, trap density (spacing), and number of consecutive trapping occasions (duration) influenced density estimates. To validate the subsampling methods, we ran Monte Carlo simulations based on the true parameter estimates for each specific year. We found that reducing the area of the trapping design by more than 36% resulted in the inability of the SECR model to replicate density estimates within the SE of the original density estimates. However, when trapping occasions were reduced from 4 to 3-nights the density estimates were indistinguishable from the full dataset. Furthermore, reducing trap density by 50% also resulted in density estimates comparable to the full dataset and was a substantially better model than reducing the trap area by 50%. Overall, our results indicated that moderate reductions in the number of trapping occasions or trap density could yield similar density estimates when using a SECR approach. This approach allows the optimization of field trapping efforts and designs by reducing field efforts while maintaining the same population estimate compared to the full dataset. Using a SECR approach may help other wildlife programs identify sampling efficiencies without sacrificing data integrity for long term monitoring of population densities.

Disease may limit recovery of endangered species. We surveyed parasites in the federally endangered salt marsh harvest mouse (SMHM; Reithrodontomys raviventris halicoetes) and sympatric rodents in Suisun Marsh (Solano County, California, USA) from April 2018 through March 2019. We investigated individual SMHM risk factors (age, sex, reproductive status, and body condition) for infection and relationships among the estimated parasite prevalence and season and habitat management (natural tidal habitats versus diked, nontidal habitats). We captured 625 individual rodents, including 439 SMHM, and tested these for infection with Bartonella spp., Borrelia spp., Rickettsia spp., Francisella tularensis, Leptospira spp., Cryptosporidium spp., Giardia spp., and Toxoplasma gondii by PCR. Over one-third (34.6%, confidence interval [CI], 30.2-39.3%) of SMHM tested positive for at least one parasite. Four percent (CI, 2.8-6.3%) of SMHM were infected with F. tularensis holarctica, a virulent bacterium that causes mortality in rodents shortly after infection. Additionally, we detected three species of Bartonella (B. henselae, B. rochalimae, B. vinsonii arupensis), Leptospira borgpetersenii serovar Ballum, Cryptosporidium sp. (deer mouse [Peromyscus maniculatus] genotype), Cryptosporidium parvum, Giardia intestinalis, and an unidentified Borrelia sp. The only parasite that was associated with habitat management was Bartonella spp., which was more prevalent in diked than tidal areas. Male SMHM were more likely to be parasitized than females, and individuals in modestly poor body condition were most likely to be infected with Bartonella spp. The estimated sample prevalence of multiple parasites varied by season and by host species. This is the first major parasite assessment in a long-endangered species, and these results will assist managers to incorporate parasitic disease into recovery planning and provide a critical baseline for future investigations, including how climatically induced habitat and species composition changes could alter disease dynamics.

Did you know that one of the most unique and incredible mammals in the world is found only in the San Francisco Bay-Estuary? The salt marsh harvest mouse is an endangered species because over 90% of its coastal marsh habitat has been lost due to human development. This species can swim for over 2h, can climb using its tail like a fifth limb, can eat salty foods, and can even drink water saltier than the ocean! For decades, people thought this animal could live only in tidal marshes dominated by salt-loving plants. However, in the past few years, we have learned many new things about the salt marsh harvest mouse. For example, we now know it can live in non-tidal marshes and forage on freshwater plants. Unfortunately, the superhero abilities of this mouse will not protect it from all the threats it faces in the future, such as sea-level rise.

The salt marsh harvest mouse (SMHM; Reithrodontomys raviventris) is a state and federally listed endangered species endemic to the coastal marshes of the San Francisco Estuary of California.Of two subspecies, the southern (R. r. raviventris) is most endangered and lacks reliable morphological field tools to distinguish from the sympatric western harvest mouse (WHM; R. megalotis).We trapped and collected genetic samples and morphological data from 204 harvest mice from 14 locations from across the range of the southern SMHM.Genetic species identification indicated these to be composed of 48 SMHM and 156 WHM, which we compared at ten morphological characters.Most continuous characters overlapped between species.Color characters were significantly differentiated and we identified a number of species-specific diagnostic pelage categories in both species.A random forest analysis indicated that ventral coloration of the abdomen and the ventral tail hair color were the most useful for differentiating between species.We used these two morphological characters to develop a decision tree which correctly classified 94% of harvest mice to species with 99% accuracy.These findings suggest that our decision tree can be used to reliably identify the species of most harvest mice in the range of the southern SMHM, with a small proportion (6% in our study) needing genetic confirmation.The decision tree should be tested on additional harvest mice that were not used in its development, particularly from novel locations across the range.

Suisun Marsh (Solano County, California) is the largest contiguous marsh remaining on the West Coast of the United States, and makes up approximately 10% of the wetlands remaining in the San Francisco Estuary. Suisun Marsh has been safeguarded from development through the operation of over 100 privately owned waterfowl hunting clubs, which manage for diked waterfowl habitat. However, this management—and the subsequent loss of tidal influence—has been considered harmful for some species, including the endangered salt marsh harvest mouse (SMHM; Reithrodontomys raviventris). To determine the value of tidal wetlands relative to those managed for waterfowl, we performed periodic surveys for rodents in managed and tidal wetlands over 5 years, and used capture-mark-recapture analyses to estimate demographic parameters and abundance for the three most common rodents—the northern SMHM (R. r. halicoetes), the western harvest mouse (a sympatric native species; R. megalotis, WHM), and the house mouse (a sympatric invasive species; Mus musculus). Wetland type had no effect on detection, temporary emigration, or survival for any of these species. However, fecundity and population growth for all three species were affected by an interaction of season and wetland type, although none of these parameters was consistently superior in either habitat type. Estimated abundance of SMHM and Mus was similar in both wetland types, whereas WHM were more abundant in managed wetlands. Salt marsh harvest mice also showed no affinity for any microhabitat characteristics associated with tidal wetlands. Managed wetlands in Suisun Marsh support SMHM and Mus equally, and abundances of WHM were greater than in tidal wetlands, suggesting managed wetlands may be superior in terms of supporting native rodents. As climate change and sea level rise are predicted to threaten coastal marshes, these results suggest the recovery strategy for SMHM could incorporate managed wetlands.

Author(s): Smith, Katherine R.; Riley, Melissa K.; Barthman–Thompson, Laureen; Statham, Mark J.; Estrella, Sarah; Kelt, Douglas | Abstract: [Abstracts are not presented for essays. -The SFEWS Editors.]

ABSTRACTThe northern subspecies of the salt marsh harvest mouse (Reithrodontomys raviventris halicoetes) is morphologically similar to the western harvest mouse (R. megalotis) with which it co‐occurs in the Suisun Marsh, California, USA, and therefore they are difficult to distinguish in the field. The salt marsh harvest mouse is a federal and California state‐listed endangered species, whereas the western harvest mouse has no special status. Thus, our objective was to identify the most effective field metrics that distinguish the species. First we identified a barcode of life and restriction fragment length polymorphism approach for genetically distinguishing between the species. Then we performed univariate tests to examine variation in standard external morphological traits within and between species, and found that differences between species were confounded by sex and age. We then used discriminant function analysis and multiple logistic regression (MLR) to find combinations of characters that resulted in the highest percentages of correct classification based on a data set of individuals with genetically verified species identity. The best model (MLR) correctly classified 90.1 ± 3.5% ( ± SD) of individuals, though all approaches performed relatively poorly with smaller, ostensibly younger, mice. Therefore, tail length, body length, and tail diameter, if treated in a comprehensive multivariate context, can yield substantial accuracy for distinguishing between coexisting northern salt marsh and western harvest mice. © 2018 The Wildlife Society.

The northern salt marsh harvest mouse (Reithrodontomys raviventris halicoetes) is an endangered species endemic to the San Francisco Bay Estuary. Using a conservation behavior perspective, we examined how salt marsh harvest mice cope with both natural (daily tidal fluctuations) and anthropogenic (modification of tidal regime) changes in natural tidal wetlands and human-created diked wetlands, and investigated the role of behavioral flexibility in utilizing a human-created environment in the Suisun Marsh. We used radio telemetry to determine refuge use at high tide, space use, and movement rates to investigate possible differences in movement behavior in tidal versus diked wetlands. We found that the vast majority of the time salt marsh harvest mice remain in vegetation above the water during high tides. We also found no difference in space used by mice during high tide as compared to before or after high tide in either tidal or diked wetlands. We found no detectable difference in diurnal or nocturnal movement rates in tidal wetlands. However, we did find that diurnal movement rates for mice in diked wetlands were lower than nocturnal movement rates, especially during the new moon. This change in movement behavior in a relatively novel human-created habitat indicates that behavioral flexibility may facilitate the use of human-created environments by salt marsh harvest mice.

We undertook a 2-year (2002-2004) mark-recapture study to investigate demographic performance and habitat use of salt marsh harvest mice (Reithrodontomys raviventris halicoetes) in the Suisun Marsh. We examined the effects of different wetland types and microhabitats on 3 demographic variables: density, reproductive potential, and persistence. Our results indicate that microhabitats dominated by mixed vegetation or pickleweed (Salicornia spp.) supported similar salt marsh harvest mouse densities, reproductive potential, and persistence throughout much of the year, whereas few salt marsh harvest mice inhabited upland grass-dominated microhabitats. We found that densities were higher in diked wetlands, whereas post-winter persistence was higher in tidal wetlands, and reproductive potential did not differ statistically between wetland types. Our results emphasize the importance of mixed vegetation for providing adequate salt marsh harvest mouse habitat and suggest that, despite their physiognomic and hydrological differences, both diked and tidal wetlands support salt marsh harvest mouse populations by promoting different demographic attributes. We recommend that habitat management, restoration, and enhancement efforts include areas containing mixed vegetation in addition to pickleweed in both diked and tidal wetlands. (c) 2011 The Wildlife Society.