Neotoma Lepida Research Articles

A tale of two species: Extirpation and range expansion during the late Quaternary in an extreme environment

Death Valley, California is today the hottest hyperarid area in the western Hemisphere with temperatures of 57 °C (134 °F) recorded. During the late Quaternary, pluvial Lake Manly covered much of the Valley and contributed to a much more moderate climate. The abrupt draining of Lake Manly in the mid-Holocene and coincident dramatic shifts in temperature and aridity exerted substantial selection pressure on organisms living in this area. Our research investigates the adaptive response of Neotoma (woodrats) to temperature change over the late Quaternary along a steep elevational and environmental gradient. By combining fieldwork, examination of museum specimens, and collection of paleomiddens, our project reconstructs the divergent evolutionary histories of animals from the valley floor and nearby mountain gradients (− 84 to > 3400 m). We report on recent paleomidden work investigating a transition zone in the Grapevine Mountains (Amargosa Range) for two species of woodrats differing significantly in size and habitat preferences: N. lepida, the desert woodrat, and N. cinerea, the bushy-tailed woodrat. Here, at the limits of these species' thermal and ecological thresholds, we demonstrate dramatic fluctuations in the range boundaries over the Holocene as climate shifted. Moreover, we find fundamental differences in the adaptive response of these two species related to the elevation of the site and local microclimate. Results indicate that although N. cinerea are currently extirpated in this area, they were ubiquitous throughout the late Pleistocene and into the middle Holocene. They adapted to climate shifts over this period by phenotypic changes in body mass, as has been demonstrated for other areas within their range; during colder episodes they were larger, and during warmer intervals, animals were smaller. Their presence may have been tied into a much more widespread historical distribution of juniper ( Juniperus sp.); we document a downward displacement of approximately 1000 m relative to juniper's modern extent in the Amargosa Range. These results suggest a cooler and more mesic habitat association persisting for longer and at lower elevations than previously reported.

“Pharm‐Ecology” of Diet Shifting: Biotransformation of Plant Secondary Compounds in Creosote (Larrea tridentata) by a Woodrat Herbivore,Neotoma lepida

Diet switching in mammalian herbivores may necessitate a change in the biotransformation enzymes used to process plant secondary compounds (PSCs). We investigated differences in the biotransformation system in the mammalian herbivore, Neotoma lepida, after a radical shift in diet and secondary compound composition. Populations of N. lepida in the Mojave Desert have evolved over the past 10,000 years to feed on creosote (Larrea tridentata) from an ancestral state of consuming juniper (Juniperus osteosperma). This dietary shift represents a marked change in the dietary composition of PSCs in that creosote leaves are coated with phenolic resin, whereas juniper is high in terpenes but lacks phenolic resin. We quantified the enzyme activity of five major groups of biotransformation enzymes (cytochrome P450s, NAD(P)H:quinone oxidoreductase, glutathione conjugation, sulfation, and glucuronidation) recognized for their importance to mammalian biotransformation for the elimination of foreign compounds. Enzyme activities were compared between populations of Mojave and Great Basin woodrats fed control and creosote diets. In response to creosote, the Mojave population had greater levels of cytochrome P450s (CYP2B, CYP1A) and glutathione conjugation liver enzymes compared with the Great Basin population. Our results suggest that elevated levels of cytochrome P450s and glutathione conjugation enzymes in the Mojave population may be the underlying biotransformation mechanisms that facilitate feeding on creosote.

An Oak (Quercus agrifolia) Specialist (Neotoma macrotis) and a Sympatric Generalist (Neotoma lepida) Show Similar Intakes and Digestibilities of Oak

Dietary specialization is thought to be rare in mammalian herbivores as a result of either a limitation in their detoxification system to metabolize higher doses of plant secondary compounds or deficiencies in nutrients present in a diet composed of a single species of plant. Neotoma macrotis is an oak specialist, whereas Neotoma lepida is a dietary generalist when sympatric with N. macrotis. We hypothesized that N. macrotis would have a higher tolerance for and digestibility of oak. We determined the two species' tolerances for oak by feeding them increasing concentrations of ground oak leaves until they could no longer maintain body mass. The highest concentration on which both species maintained body mass was 75% oak. There were no differences between the species in their abilities to digest dry matter, nitrogen, or fiber in the oak diets. The species' similar tolerances for oak were probably due to their similar abilities to digest and potentially assimilate the ground oak leaves.

Dynamics of Rodent Populations in Semiarid Habitats in Lassen County, California

From 1996 to 2004, we studied population dynamics of a rodent assemblage in semiarid habitats in Lassen County, California. Abundances of rodents appeared affected by fluctuations in precipitation from a high in 1996 to average and slightly below-average levels in subsequent years; perhaps reflecting this, assemblage composition also changed dramatically during the study period. California kangaroo rats (Dipodomys californicus) declined from abun- dant to extremely rare, abundances of deer mice (Peromyscus maniculatus) fluctuated greatly during the study period, and, perhaps most notably, populations of dusky-footed woodrats (Neotoma fuscipes) appeared to decline to local extinction, possibly allowing for the subsequent colonization of desert woodrats (N. lepida). These changes appeared to represent natural variation in numbers and composition in an ecologically dynamic ecotonal region in response to multiyear changes in precipitation.

Characterization of 18 microsatellite loci for woodrats of the Neotoma lepida group (Rodentia, Cricetidae, Neotominae)

AbstractThe desert woodrat complex (Neotoma lepida group) is a set of four closely related species occupying the arid lands of western North America. We have developed 18 polymorphic microsatellite loci to analyse the population structure, mating patterns, and hybridization at points of contact between the contiguously allopatric species in the complex.

Assessment of mercury concentrations in small mammals collected near Las Vegas, Nevada, USA

Mercury concentrations in liver and hair tissue were determined for five species of small mammals captured near Las Vegas, Nevada, USA. These data were then used to evaluate the suitability of using hair as a noninvasive technique for determining body burdens of mercury. A total of 104 small mammals were captured and analyzed; four main species were examined and included: Dipodomys merriami, Chaetodipus penicillatus, Peromyscus eremicus, and Neotoma lepida. Mean mercury concentrations were highest in N. lepida, followed by D. merriami, C. penicillatus, and P. eremicus respectively. Positive associations were found between hair and liver taken from D. merriami (r = 0.647) and C. penicillatus (r = 0.533) indicating that hair may be a suitable indicator of body burdens in these two species.

Detoxification rates of wild herbivorous woodrats (Neotoma)

The detoxification systems of mammalian herbivores are thought to have evolved in response to the ingestion of plant secondary compounds. Specialist herbivores consume high quantities of secondary compounds and are predicted to have faster rates of Phase 1 detoxification compared to generalist herbivores. We tested this hypothesis by comparing the performances of a specialist (Neotoma fuscipes) and generalist (Neotoma lepida) herbivore using hypnotic state assays. Herbivores foraging in nature were live trapped and injected with hexobarbital (100 mg/kg). We measured the length of time in the hypnotic state as the time in which the animal was unable to right itself twice in 30 s. The specialist metabolized hexobarbital 1.7 times faster than the generalist (F(1, 19) = 9.31, P = 0.007) as revealed by its significantly shorter time spent in the hypnotic state (56+/-9 min vs. 87+/-8 min, respectively). The results are consistent with the hypothesis that specialists have faster rates of Phase 1 detoxification. This is the first evaluation of the detoxification capability of mammalian herbivores foraging under natural conditions. Hypnotic state assays have broad potential applications to the study of vertebrate-plant interactions.

MAMMAL AND FLEA RELATIONSHIPS IN THE GREAT BASIN DESERT: FROM H. J. EGOSCUE'S COLLECTIONS

Host-parasite association among 58 flea species parasitizing 40 mammal species in the Great Basin Desert of the western United States was investigated. Increased flea species richness was correlated with larger geographic ranges and stable locomotion of hosts. Hosts from habitats of moderately low productivity (sage and grass) and of Peromyscus maniculatus size, 10-33 g, had the highest flea species richness. Larger hosts had fewer flea species, but fleas were more prevalent. Increased host species richness correlated with flea species eye size. Mammals clustered into 3 major and 1 minor ecological groups, and fleas clustered into 2 major groups among rodents, and 6 minor groups, forming 12 host-parasite biocenoses. Factors producing biocenoses were shared burrows of mice and rats; food chains of hares, rabbits, squirrels, and their predators; keystone mammals: Lagurus curtatus, Neotoma lepida, Ochotona princeps, and Spermophilus townsendii; keystone fleas: Megabothris abantis, and Meringis hubbardi; or host isolation, Neotoma cinerea with Oropsylla montana, Sorex vagrans with Corrodopsylla curvata, and Tadarida brasiliensis with Sternopsylla distincta. Although host relatedness accounted for flea prevalence, host sociality explained the presence or absence of mammal-flea relationships.

Plant secondary metabolites alter the feeding patterns of a mammalian herbivore (Neotoma lepida)

Mammalian herbivores are predicted to regulate concentrations of ingested plant secondary metabolites (PSMs) in the blood by modifying the size and frequency of feeding bouts. It is theorized that meal size is limited by a maximum tolerable concentration of PSMs in the blood, such that meal size is predicted to decrease as PSM concentration increases. We investigated the relationship between PSM concentration in the diet and feeding patterns in the herbivorous desert woodrat (Neotoma lepida) fed diets containing phenolic resin extracted from creosote bush (Larrea tridentata). Total daily intake, meal size and feeding frequency were quantified by observing the foraging behavior of woodrats on diets containing increasing concentrations of creosote resin. Desert woodrats reduced meal size as resin concentration in the diet increased, resulting in an overall reduction in daily intake and regulation of resin intake. Moreover, desert woodrats were able to detect resin concentrations in the diet and regulate the intake of resin very rapidly. We suggest that the immediate and sustained ability to detect and regulate the intake of resin concentrations during each foraging bout provides a behavioral mechanism to regulate blood concentrations of resin and allows desert woodrats to make "wise" foraging decisions.

Within-taxon morphological diversity in late-Quaternary Neotoma as a paleoenvironmental indicator, Bonneville Basin, Northwestern Utah, USA

Ecological data indicate that as the amount of precipitation in an arid areas increases, so too does mammalian taxonomic richness. This correspondence has been found in two late-Quaternary mammalian faunas from Utah, one from Homestead Cave in the Bonneville Basin. We use the remains of two species of woodrat ( Neotoma cinerea and Neotoma lepida) from Homestead Cave to test the hypothesis that as the amount of precipitation in an arid area increases, so too does morphological diversity within individual mammalian taxa. Morphological diversity is measured as corrected coefficients of variation and as richness of size classes of mandibular alveolar lengths. Coefficients of variation for N. cinerea are few and coincide with moisture history if temporally successive small samples are lumped together. More abundant coefficients of variation for N. lepida coincide only loosely with moisture history, likely because such coefficients measure dispersion but not necessarily other aspects of variation. Richness of size classes of N. lepida is high during the early and late Holocene when moisture was high, and lowest during the middle Holocene when climate was most arid.

Creosote Bush (Larrea tridentata) Resin Increases Water Demands and Reduces Energy Availability in Desert Woodrats (Neotoma lepida)

Although many plant secondary compounds are known to have serious consequences for herbivores, the costs of processing them are generally unknown. Two potential costs of ingestion and detoxification of secondary compounds are elevation of the minimum drinking water requirement and excretion of energetically expensive metabolites (i.e., glucuronides) in the urine. To address these impacts, we studied the costs of ingestion of resin from creosote bush (Larrea tridentata) on desert woodrats (Neotoma lepida). The following hypotheses were tested: ingestion of creosote resin by woodrats (1) increases minimum water requirement and (2) reduces energy available by increasing fecal and urinary energy losses. We tested the first hypothesis, by measuring the minimum water requirement of woodrats fed a control diet with and without creosote resin. Drinking water was given in decreasing amounts until woodrats could no longer maintain constant body mass. In two separate experiments, the minimum drinking water requirement of woodrats fed resin was higher than that of controls by 18-30% (about 1-1.7 ml/d). We tested several potential mechanisms of increased water loss associated with the increase in water requirement. The rate of fecal water loss was higher in woodrats consuming resin. Neither urinary water nor evaporative water loss was affected by ingestion of resin. Hypothesis 2 was tested by measuring energy fluxes of woodrats consuming control vs. resin-treated diets. Woodrats on a resin diet had higher urinary energy losses and, thus, metabolized a lower proportion of the dietary energy than did woodrats on control diet. Fecal energy excretion was not affected by resin. The excretion of glucuronic acid represented almost half of the energy lost as a consequence of resin ingestion. The increased water requirement and energy losses of woodrats consuming a diet with resin could have notable ecological consequences.

Detection and characterization of Borrelia bissettii in rodents from the central California coast.

This is the first report of Borrelia burgdorferi sensu lato in rodents from San Luis Obispo county, with most isolates obtained from a previously unreported host, Neotoma lepida Thomas. B. burgdorferi sensu lato was identified in seven rodent species, including the California vole, Microtus californicus Peale; dusky-footed woodrat, Neotoma fuscipes Baird; desert woodrat, Neotoma lepida Thomas; brush mouse, Peromyscus boylii Baird; California mouse, Peromyscus californicus Gambel; deer mouse, Peromyscus maniculatus Wagner; and western harvest mouse, Reithrodontomys megalotis Baird. Ear punch biopsies were cultured in BSK-H medium from 179 rodents trapped at six different study sites. Overall, prevalence of rodent infection was 44/179 (24.6%), with 34 of these isolates from N. lepida. Spirochete isolates were obtained from rodents at all study sites, indicating widespread prevalence of B. burgdorferi sensu lato across rodent species and habitats. Nucleotide sequences for 14 of these isolates have been submitted to GenBank. Isolates from three N. lepida and one P. boylii had identical flagellin gene sequences, and phylogenetic analysis placed these spirochetes in B. burgdorferi sensu lato group DN127, now known as B. bissettii Postic, Marti Ras, Lane, Hendson & Baranton. Additional sequencing of the intergenic spacer regions between the 5S and 23S ribosomal genes was performed on three of these isolates. Phylogenetic analysis separated these isolates into two clusters that grouped with Colorado or California isolates. The role of B. bissettii and related species other than B. burgdorferi sensu stricto Johnson, Schmid, Hyde, Steigerwalt & Brenner as human pathogens in the United States warrants further investigation.

The effect of Holocene temperature fluctuations on the evolution and ecology of Neotoma (woodrats) in Idaho and northwestern Utah

Animals respond to climatic change by adapting or by altering distributional patterns. How an animal responds is influenced by where it is positioned within its geographic range; the probability of extirpation is increased near range boundaries. Here, we examine the impact of Holocene climatic fluctuations on a small mammalian herbivore, the bushy-tailed woodrat ( Neotoma cinerea), at five locations within south central Idaho and northwestern Utah. Previous work demonstrated that woodrats adapt to temperature shifts by altering body size. We focus here on the relationship between body mass, temperature, and location within the geographic range. Body mass is estimated by measuring fossil fecal pellets, a technique validated in earlier work. Overall, we find the predicted phenotypic response to climate change: animals were larger during cold periods, and smaller during warmer episodes. However, we also identify several time periods when changes in environmental temperature exceeded the adaptive flexibility of N. cinerea. A smaller-bodied species, the desert woodrat ( N. lepida) apparently invaded lower elevation sites during the mid-Holocene, despite being behaviorally and physically subordinate to N. cinerea. Analysis of contemporary patterns of body size and thermal tolerances for both woodrat species suggests this was because of the greater heat tolerance of N. lepida. The robust spatial relationship between contemporary body size and ambient temperature is used as a proxy to reconstruct local climate during the Holocene.

Small-Mammal Data on Early and Middle Holocene Climates and Biotic Communities in the Bonneville Basin, USA

Archaeological investigations in Camels Back Cave, western Utah, recovered a series of small-mammal bone assemblages from stratified deposits dating between ca. 12,000 and 500 14C yr B.P. The cave's early Holocene fauna includes a number of species adapted to montane or mesic habitats containing grasses and/or sagebrush (e.g., Lepus townsendii, Marmota flaviventris, Reithrodontomys megalotis, and Brachylagus idahoensis) which suggest that the region was relatively cool and moist until after 8800 14C yr B.P. Between ca. 8600 and 8100 14C yr B.P. these mammals became locally extinct, taxonomic diversity declined, and there was an increase in species well-adapted to xeric, low-elevation habitats, including ground squirrels, Lepus californicus and Neotoma lepida. The early small-mammal record from Camels Back Cave is similar to the 11,300–6000 14C yr B.P. mammalian sequence from Homestead Cave, northwestern Utah, and provides corroborative data on Bonneville Basin paleoenvironments and mammalian responses to middle Holocene desertification.

Current status of rodents on islands in the Gulf of California

On islands in the Gulf of California, many species and subspecies of rodents are relict species, restricted to the islands, and now considered extinct or verging on extinction. From 1991 to 1999, each island was surveyed and an average of 15 work-nights were spent on each island, for a total of 15,000 trap-nights. A Fourier series was used to estimate population density. Five native taxa are now considered extinct (C haetodipus baileyi fornicatus, Peromyscus guardia mejiae, P. g. harbinsoni, P. pembertoni, and Neotoma bunkeri). Two species are at risk of extinction ( Dipodomys insularis and Neotoma albigula varia). The most probable cause for extinction is the introduction of nonnative species, specifically cats. We believe that the most vulnerable rodent populations of the islands in the Gulf of California to non-native species are Neotoma lepida latirostra on Danzante island and Neotoma lepida abbreviata on San Francisco island, both in the state of Baja California Sur.

Detoxification in relation to toxin tolerance in desert woodrats eating creosote bush.

We studied the relationship between the use of three detoxification pathways and urine pH and the tolerance of desert woodrats from two populations to a mixture of naturally occurring plant secondary metabolites (mostly phenolics) in resin from creosote bush (Larrea tridentata). The two populations of desert woodrats came from the Mojave desert (Mojave woodrats), where woodrats consume creosote bush, and from the Great Basin desert (Great Basin woodrats), where the plant species is absent. We fed woodrats alfalfa pellets containing increasing levels of the phenolic resin and measured three detoxification pathways and urine pH that are related to detoxification of allelochemicals. We found that the excretion rate of two phase II detoxification conjugates, glucuronides and sulfides. increased with increasing resin intake, whereas excretion of hippuric acid was independent of resin intake, although it differed between populations. Urine pH declined with increasing resin ingestion. The molar proportion of glucuronides in urine was three times that of the other conjugates combined. Based on an evaluation of variation in the three detoxification pathways and urine pH in relation to resin intake, we rejected the hypotheses that woodrats' tolerance to resin intake is related to capacity for amination, sulfation, or pH regulation. However, Mojave woodrats had higher maximum glucuronide excretion rates, and we accepted the hypothesis that within and between populations woodrats tolerate more resin because they have a greater capacity for glucuronide excretion.

INTERPOPULATION DIFFERENCES IN TOLERANCE TO CREOSOTE BUSH RESIN IN DESERT WOODRATS (NEOTOMA LEPIDA)

Plant secondary metabolites (PSMs) can affect survival, reproduction, and distribution of herbivores. Individuals with a high capacity to tolerate PSMs will experience fewer and smaller adverse effects than less tolerant individuals. Theoretically, the capacity to tolerate PSMs can be acquired during development, modulated during adulthood, or genetically fixed. We studied tolerance to phenolic resin from creosote bush (Larrea tridentata) in two populations of desert woodrats as a first step in understanding phenotypic habituation and genetic adaptation of this species to creosote resin. One population was from Mojave desert habitat where woodrats eat creosote bush, and the other from the Great Basin desert, where creosote bush is not present and woodrats consume mainly juniper (Juniperus osteosperma). For >1 mo in the laboratory, woodrats from both populations were fed rabbit chow with increasing amounts of phenolic resin extracted from creosote bush until they lost body mass or showed any sign of sickness. Woodrats from the Mojave population maintained body mass at higher concentrations of resin and remained in the experiment longer. There were no differences between populations in food intake across all resin levels; however, maximum resin intake was 25% higher for the Mojave population. Food intake decreased with increasing resin intake. Glucuronic acid excretion in urine, one indicator of detoxification capacity, did not differ between populations. Water consumption increased with increased levels of creosote resin in the diet in woodrats from both populations. The results are consistent with the idea of differential tolerance to creosote bush phenolic resin in desert woodrat populations. Woodrats appear to be a promising natural system to study the developmental or genetic factors underlying vertebrate adaptation to plant secondary metabolites.

Arenavirus antibody in rodents indigenous to coastal southern California.

The purpose of this study was to extend our knowledge on the geographic and natural rodent host ranges of New World arenaviruses in California. Sera from 1,094 sigmodontine and 112 murine rodents were tested for antibody against Whitewater Arroyo and Amapari viruses. Antibody was found in 55 (4.6%) of the 1,206 rodents: 4 from northwestern San Diego County, 3 from Los Angeles County, and 48 from Orange County. The antibody-positive rodents included 8 (7.8%) of 103 Neotoma fuscipes, 1 (0.6%) of 180 Neotoma lepida, 1 (3.1%) of 32 Peromyscus boylii, 8 (11.0%) of 73 Peromyscus californicus, 1 (1.2%) of 85 Peromyscus eremicus, 30 (8.5%) of 353 Peromyscus maniculatus, and 6 (2.2%) of 268 Reithrodontomys megalotis. This study provides the first evidence that New World arenaviruses occur in Los Angeles and Orange counties and northwestern San Diego County, and the first evidence that Peromyscus and Reithrodontomys species are naturally infected with New World arenaviruses.

How isolated are Pleistocene refugia? Results from a study on a relict woodrat population from the Mojave Desert, California

AbstractPleistocene vicariance is often invoked to explain the disjunct populations of animals in habitat refugia throughout the southwestern United States. The combined effects of small population size and isolation from the rest of the contiguous range are thought to result in genetic differentiation of relict organisms.Here, we describe a relict population of dusky‐footed woodrats (Neotoma fuscipes Baird) found in a pinyon‐juniper‐oak community in a small mountain range within the Mojave Desert. We compare morphological and genetic data for these individuals with two populations within the contiguous range, and with another species of woodrat (Neotoma lepida). We also examine the distributional overlap between contemporary oak species and dusky‐footed woodrats, and estimate the potential oak woodland habitat available during the late Quaternary.As expected, both the morphological and genetic analysis confirm that the relict population is N. fuscipes. Within the limitations of our data, we detect no evidence of differentiation. Instead, the relict population forms a paraphyletic group with the nearest population within the contiguous range. This may be explained by the combined influences of a shorter period of isolation and a greater effective population size than was originally expected.The linkage between contemporary oak and dusky‐footed woodrat distributions is very tight, reinforcing the idea of an obligate relationship between the two.We estimate that at ~8000 ybp, pinyon‐juniper‐oak woodlands may have covered ~53% of the central Mojave, forming large contiguous areas of habitat. Although considerably more fragmented, at present ~12% of the area consists of relict woodlands.Our results suggest that there may be numerous other woodrat refugia, with a relatively high degree of connectiveness between the larger ones. Animals within them may effectively function as a single metapopulation, buffering against occasional stochastic extinction events.

Spring diet of the endemic ring-tailed cat (Bassariscus astutus insulicola) population on an island in the Gulf of California, Mexico

The spring diet of an endemic ring-tailed cat (Bassariscus astutus insulicola) population of Isla San José, Gulf of California, Mexico, is presented based on the analysis of 104 faeces. The ring-tailed cat is an opportunistic species, concentrating on the predation of mainly small prey, and has a richness of prey of 36 animal taxa and 12 plant species. The most important prey were found to be mainly Orthoptera, Tenebrionida, and Scorpionoidea, Chaetodipus spinatus and Neotoma lepida. Chilomeniscus cinctus, Cnemidophorus, and Sceloporus were the most important reptile species. Among the plant species, of particular importance were the fruits of Lycium,Solanum , Phaulothamnus, and ironwood leaves. The spring diet of the ring-tailed cats of Isla San José differs from the diet of all other mainland populations, in that the proportion of reptiles (50% of occurrence) and invertebrates (91%) were found to be of the highest ever reported, even when compared with other seasons.