Comparative skeletal anatomy of salt marsh and western harvest mice in relation to locomotor ecology.

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.

Application of lidar to assess the habitat selection of an endangered small mammal in an estuarine wetland environment.

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.

Dietary characterization of the endangered salt marsh harvest mouse and sympatric rodents using DNA metabarcoding.

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.

Assessing small-mammal trapping design using spatially explicit capture recapture (SECR) modeling on long-term monitoring data.

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.

PARASITES OF AN ENDANGERED HARVEST MOUSE (REITHRODONTOMYS RAVIVENTRIS HALICOETES) IN A NORTHERN CALIFORNIA MARSH.

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.

Demography of the salt marsh harvest mouse (Reithrodontomys raviventris halicoetes) and associated rodents in tidal and managed wetlands.

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.

Effects of natural and anthropogenic change on habitat use and movement of endangered salt marsh harvest mice.

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.