Development of husbandry practices for the captive breeding of key largo woodrats (Neotoma floridana smalli)

The Key Largo woodrat is an endangered rodent endemic to the island of Key Largo in the Florida Keys. After several reports documented a steep decline in the population, the US Fish and Wildlife Service developed a recovery plan, including captive breeding and reintroduction. Captive breeding efforts were to be focused on providing animals for future reintroduction to protected areas on Key Largo. However, little was known about the husbandry needs or reproductive behavior of this elusive nocturnal species. In 2005, Disney's Animal Kingdom^® received 11 animals and began to systematically investigate methods of breeding Key Largo woodrats. Since the program's inception, 30 pups have been born and successfully parent reared. In this report, we describe some of the husbandry techniques that have contributed to the success of the Key Largo woodrat captive breeding program at Disney's Animal Kingdom^®. The results obtained may be of use to other facilities maintaining woodrats and other rodent species. Zoo Biol 30:318–327, 2011. © 2010 Wiley‐Liss, Inc.     

Evaluation of Factors Restricting Distribution of the Endangered Key Largo Woodrat

ABSTRACT We examined a suite of models in an information theoretic framework to identify factors restricting presence of the endangered Key Largo woodrat (Neotoma floridana smalli) throughout its remaining habitat. Models containing variables related to availability of nest sites and mammalian predator abundances were supported by our data. Abundance of natural (large overstory trees) and artificial (rock and debris piles) nest substrate were the most important predictor variables, followed by indices of feral cat and raccoon (Procyon lotor) abundance. We recommend increasing abundance of nest substrate in the short term through addition of artificial nest substrate and in the long term through continued protection of remaining forest habitat.     

Survey of raccoons on Key Largo, Florida, USA, for Baylisascaris procyonis

Numbers of the endangered Key Largo woodrat (KLWR; Neotoma floridana smalli) have been declining for at least 25 yr. The raccoon (Procyon lotor) roundworm, Baylisascaris procyonis, has been found to have an adverse effect on the survival of Alleghany woodrats (N. magister). High densities of raccoons can exacerbate this problem by increasing the amount of feces containing viable eggs of B. procyonis available to woodrats. In 2002, 64 fecal samples were collected and examined for eggs of B. procyonis from >32 raccoons within the KLWR's known range on Key Largo, Florida, USA. All samples were negative for eggs of B. procyonis. Raccoon density in this area was approximately 0.62 raccoons/ha. Despite this high density of raccoons, B. procyonis does not appear to be a threat to the KLWR population.     

Behavioral predictors of copulation in captive Key Largo woodrats (Neotoma floridana smalli)

The development of a captive breeding program for the endangered Key Largo woodrat (Neotoma floridana smalli) presents special challenges due to aggressive behavior toward conspecifics, a low reproductive rate, and limited information on estrous cycles. In an effort to identify behavioral predictors of copulation, we observed 17 Key Largo woodrats prior to and during 267 male-female pairing events, 76 of which resulted in copulation. Predictors of copulation include male-female interactions at the door of the tube connecting their enclosures, raspy vocalizations, pre-mounting lordosis, and chasing. A binary logistic regression model based on pre-pairing behaviors correctly predicted the outcome of 78.7% of observed pairing events, and a similar model based on intra-pairing behaviors correctly predicted the outcome of 86.1% of observed pairing events. Behavior-based models may be useful in the management of captive breeding programs for this and other endangered species.     

Pup development and maternal behavior in captive Key Largo woodrats (Neotoma floridana smalli)

This study describes the first systematic observations of maternal behavior and pup development of captive Key Largo woodrats (Neotoma floridana smalli) during the first 30 days of life. Data were collected on six litters of pups born to four dams between December 2006 and July 2007. Gestations for the six litters averaged 38 days and all dams exhibited adequate maternal care postpartum. Key Largo woodrat maternal and pup behavior was generally consistent with behavior observed in other woodrat species. We observed greater pup independence from the dam and a marked change in social interactions between days 13–22. No sex differences in pup development or maternal care were observed. Activity budgets were consistent across dams and across days within the observation period. Although dams spent much of their time inactive with pups attached to their teats, the average percent of intervals with at least one pup observed attached decreased steadily during the 30‐day observation period. Attachment of pups to the dams' teats did not interfere with dams' ability to forage. Feeding with pups attached and feeding following active detachment of pups were both common. Dams were observed to actively detach pups by performing a circular turning motion. This information has application for the future management of this endangered species in captivity and in the wild. Zoo Biol 27:394–405, 2008. © 2008 Wiley‐Liss, Inc.     

Breeding habitat and nest‐site selection by an obligatory “nest‐cleptoparasite”, the Amur Falcon Falco amurensis

The selection of a nest site is crucial for successful reproduction of birds. Animals which re‐use or occupy nest sites constructed by other species often have limited choice. Little is known about the criteria of nest‐stealing species to choose suitable nesting sites and habitats. Here, we analyze breeding‐site selection of an obligatory “nest‐cleptoparasite”, the Amur Falcon Falco amurensis. We collected data on nest sites at Muraviovka Park in the Russian Far East, where the species breeds exclusively in nests of the Eurasian Magpie Pica pica. We sampled 117 Eurasian Magpie nests, 38 of which were occupied by Amur Falcons. Nest‐specific variables were assessed, and a recently developed habitat classification map was used to derive landscape metrics. We found that Amur Falcons chose a wide range of nesting sites, but significantly preferred nests with a domed roof. Breeding pairs of Eurasian Hobby Falco subbuteo and Eurasian Magpie were often found to breed near the nest in about the same distance as neighboring Amur Falcon pairs. Additionally, the occurrence of the species was positively associated with bare soil cover, forest cover, and shrub patches within their home range and negatively with the distance to wetlands. Areas of wetlands and fallow land might be used for foraging since Amur Falcons mostly depend on an insect diet. Additionally, we found that rarely burned habitats were preferred. Overall, the effect of landscape variables on the choice of actual nest sites appeared to be rather small. We used different classification methods to predict the probability of occurrence, of which the Random forest method showed the highest accuracy. The areas determined as suitable habitat showed a high concordance with the actual nest locations. We conclude that Amur Falcons prefer to occupy newly built (domed) nests to ensure high nest quality, as well as nests surrounded by available feeding habitats.     

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

Pleistocene 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.     

Papers of interest in other journals

Abstract

Nonlithified, dome‐shaped deep‐water stromatolite analogs grow at a depth of 36 m and a light intensity of 100 Es^?1m^?2 off French Reef in the Key Largo National Marine Sanctuary. The only other modern deep‐water stromatolite analogs known to occur in the world are in antarctic freshwater lakes and these structures exist at light levels ≤ 1% of surface values (<1.0 Es^?1m^?2). Even though the two habitats are very dissimilar, they share the commonality of nonlithified, laminated stromatolite analogs growing in low‐light environments. The Key Largo formations exist on a carbonate sand substrate and have a low chlorophyll a:biomass ratio in comparison to the antarctic stromatolite analogs. The dominant cyanobacteria in the majority of antarctic habitats and in the Key Largo habitat are members of the genus Phormidium. The cyanobacterium in the Key Largo stromatolite analogs has been tentatively identified as Phormidium nov. sp. Reasons for the ability of the Key Largo structures to exist in areas of potential metazoan bioturbation present a biological enigma that remains to be explained.     

Conservation implications of past and present nesting habitat selection of the endangered Osprey Pandion haliaetus population of the Canary Islands

We studied nesting habitat selection of the endangered non‐migratory Osprey Pandion haliaetus population of the Canary Islands and evaluated the effect of human expansion in recent decades. Compared with randomly selected potential nest‐sites, Osprey nests were more frequently found on taller, southwest‐facing cliffs, characterized by lower human pressure and closer to Yellow‐legged Gull Larus michahellis colonies and Barbary Falcon Falco pelegrinoides breeding sites. Furthermore, changes in some breeding habitat features have been detected in recent decades. According to our predictive models, large areas of suitable habitat are available but unoccupied in the Canaries, and human activities are probably limiting the settlement and dispersion of new pairs.     

A suitable embankment mowing strategy for habitat conservation of the harvest mouse

The harvest mouse Micromys minutus (Pallas 1771), a small rodent, builds its nests on tall grasses such as Amur silvergrass Miscanthus sacchariflorus (Maxim.) Benth. This mouse species is endangered by grassland habitat loss worldwide. Although embankments are one of the mouse’s nest sites in Japan, these habitats are not stable because of regular mowing. To investigate ways of increasing the habitat suitability of embankments, research was carried out over a 2-year period in western Japan on an embankment where Amur silvergrass was dominant. Two to three divisions of the embankment were mowed at intervals in spring and autumn, and seasonal changes in nesting and vegetation were examined. Nest sites were evaluated using Manly’s index. In each year, the nesting period was extended and more nests were built compared to past years when phased mowing was not performed. The density of nests in each division increased in order of mowing in spring, but was low in autumn. Amur silvergrass was the preferred nesting plant and other perennial grasses were avoided. Annual grasses were preferred over Amur silvergrass in 2005. Nesting restarted when Amur silvergrass recovered to heights of >100 cm in all divisions, regardless of the mowing month. Each year, 120–160-cm-tall Amur silvergrass was preferred, while plants <80 cm high were avoided. Phased mowing, which allows annual grasses and Amur silvergrass sufficient time to recover, is clearly an effective method of maintaining stable nesting habitat for the harvest mouse on an embankment.     

Molecular phylogenetics of an endangered species: the Tamaulipan woodrat (<Emphasis Type="Italic">Neotoma angustapalata</Emphasis>)

Neotoma angustapalata (Tamaulipan woodrat) is a large cricetid rodent found only in southwestern Tamaulipas and northeastern San Luis Potosí, Mexico. This species currently is listed as endangered due to habitat alteration, its restricted distribution, and relative rarity. Previous taxonomic assessments have allied N. angustapalata with N. albigula (now encompassing N. leucodon), N. mexicana or N. micropus. We sequenced portions of the mitochondrial cytochrome b gene from two skin samples of the Tamaulipan woodrat, including one of two topotypes. We estimated genealogical relationships between N. angustapalata and other species of Neotoma using maximum likelihood and Bayesian inference. In general, our results confirm the phylogeny of woodrats as proposed previously but we also recovered major genetic differentiation within what currently is recognized as N. mexicana and N. albigula. Our data document that the Tamaulipan woodrat is genetically indistinguishable from geographically adjacent haplotypes of N. leucodon. However, mitochondrial introgression from N. leucodon cannot be ruled out inasmuch as we were not able to obtain nuclear sequence data for N. angustapalata. Morphological analyses document that both male and female Tamaulipan woodrats differ morphologically from N. leucodon. Given that the Tamaulipan woodrat is diagnosable morphologically and occurs in habitat that differs from N. leucodon, we recognize N. angustapalata as a species-level entity.     

Honey Buzzard Pernis apivorus nest‐site selection in relation to habitat and the distribution of Goshawks Accipiter gentilis

The selection of a suitable nest‐site is critical for successful reproduction. Species' preferences for nest‐sites have presumably evolved in relation to local habitat resources and/or interactions with other species. The importance of these two components in the nest‐site selection of the Eurasian Honey Buzzard Pernis apivorus was assessed in two study areas in eastern Austria. There was almost no difference in macro‐ and micro‐habitat features between nest‐sites and random plots, suggesting that Honey Buzzards did not base their choice of nest‐site on habitat characteristics. However, nests were placed significantly further from nests of Northern Goshawk Accipiter gentilis than would be expected if nest‐sites had been chosen at random. Furthermore, in one study area Honey Buzzards appeared to favour areas close to human settlements, perhaps indicating a mechanism to avoid Goshawks, which tend to avoid the proximity of humans. No habitat variable was significantly associated with the loss of Honey Buzzard young, but predation was higher in territories closer to breeding pairs of Goshawks at both study sites. Although Honey Buzzards are restricted to nesting in forests, their choice of nest‐site therefore appears to be largely dictated by the distribution of predators. Studies of habitat association may yield misleading results if the effects of predation risk on distribution are not considered.     

Efficacy of intervention to relieve nest box competition for Orange‐bellied Parrot Neophema chrysogaster

We use an experimental approach to evaluate the effectiveness of removing nests of a dominant competitor to create vacant nest boxes for a critically endangered parrot. We compared the number of times that Tree Martin (Petrochelidon nigricans – the dominant competitor at nest boxes) perched at or entered nest boxes intended for Orange‐bellied Parrot (Neophema chrysogaster – the subordinate nest competitor) over three time periods (before, immediately after and one week after experimental nest destruction). In the before period, rates of nest attendance by martins in treatment and control nests were not explained by treatment group. After experimental nest destruction, total attendance at boxes by martins rose to a mean of 6.1 visits over three five‐minute surveys in the treatment group, compared with 3.3 visits at control boxes. Within individual surveys, martins visited treatment boxes 4.4 times per survey one week after nest destruction, compared with only 1.6 visits in the control group. Martins in the treatment group rapidly rebuilt their nests and laid replacement clutches, and within a week, all boxes were reoccupied. Nest destruction did not increase nesting opportunities for the parrot, and increased vigilance of the dominant competitor may in fact reduce nesting opportunities in nearby boxes. Our study suggests that removing martin nests is an ineffective management action for alleviating nest competition for this parrot.     

Implications of Woodrats and Other Scavengers for Avian Telemetry Studies

Abstract: During 2 years of radiotelemetry research on chukars (Alectoris chukar) in western Utah, USA, we found 28% of retrieved radios (n = 78) in rubbish nests of woodrats (Neotoma spp.). Such movement and disturbance of carcasses and radios by woodrats and other species has implications for radiotelemetry studies. We evaluated spatio-temporal movement of 51 radiocollars attached to chukar carcasses in western Utah. Most (80%) carcasses were scavenged within one week and by the end of 3 weeks 25 (50%) had been retrieved from woodrat middens. Scavenging activity can both obscure important clues needed to identify causes of mortality and bias telemetry studies by delaying onset of mortality signals.     

Salt marsh elevation is a strong determinant of nest‐site selection by Clapper Rails in Georgia,USA

As sea levels rise, birds nesting in coastal marshes will be particularly vulnerable to increased tidal inundation. Understanding how marsh birds select their nesting habitat along the elevational gradient of these marshes will provide insight into how these species might be affected by rising sea levels. Clapper Rails (Rallus crepitans) are coastal marsh‐nesting birds whose nests are vulnerable to flooding, but it is not clear if they select for habitat along the elevational gradient or only use other habitat cues. Our objective was to determine if Clapper Rails select higher‐elevation nest sites, while also controlling for selection of other habitat variables at both landscape and territory levels, by comparing nest habitat to habitat in other areas of territories and at random points in the marsh landscape. At the landscape level, Clapper Rails did not exhibit selection for the elevational gradient, with nests and random points at similar elevations. At the territory level, however, nest‐site selection was most influenced by elevation and plant height, with Clapper Rails selecting nest sites with higher elevations and in areas with taller plants. However, the strength of the elevation effect was uncertain, suggesting the importance of precise elevation measurements in the field. Given this selection for higher‐elevation nest sites, Clapper Rails may be somewhat resilient to increased tidal inundation. However, the potential for increased intra‐ and interspecific competition for high‐elevation marshes should make conservation of these habitats a priority.     

Distance from riparian edge reduces brood parasitism of southwestern willow flycatchers,whereas parasitism increases nest predation risk

The southwestern willow flycatcher (Empidonax traillii extimus) is a federally endangered subspecies that breeds in increasingly fragmented and threatened habitat. We examined whether temporal and habitat characteristics were associated with risk of predation and probability of brood parasitism by brown-headed cowbirds (Molothrus ater) on flycatcher nests at 6 sites in southern Nevada and northwestern Arizona, USA. For nest predation, we found the most support for a model that included date and an interaction between parasitism status and nesting stage. Daily nest survival decreased from 0.87 (95% CI = 0.81–0.93) to 0.78 (95% CI = 0.72–0.84) through the season for parasitized nests but remained relatively constant for unparasitized nests (0.93, 95% CI = 0.91–0.95 to 0.92, 95% CI = 0.91–93). Parasitized nests had lower survival than non-parasitized nests during the incubation (0.85, 95% CI = 0.84–0.86 vs. 0.92, CI = 0.91–0.93) and nestling (0.79, 95% CI = 0.77–0.81 vs. 0.91, 95% CI = 0.90–0.92) stages. Of the variables included in our parasitism candidate models, model-averaged coefficients and odds ratios supported only distance to habitat edge; odds of parasitism decreased 1% for every 1 m from the habitat edge. Nests greater than 100 m from an edge were 50% less likely to be parasitized as those on an edge, however, only 52 of 233 nests (22%) were found at this distance. Where management and conservation goals include reducing nest losses due to parasitism, we recommend restoration of habitat patches that minimize edge and maximize breeding habitat further from edges. At sites where cowbirds have been documented as important nest predators, controlling cowbirds may be one option, but further study of the link between parasitism and nest predation and the identification of major nest predators at specific sites is warranted. © 2011 The Wildlife Society.     

Exclosure fences around nests of imperiled Florida Grasshopper Sparrows reduce rates of predation by mammals

Increasing nest survival by excluding predators is a goal of many bird conservation programs. However, new exclosure projects should be carefully evaluated to assess the potential risks of disturbance. We tested the effectiveness of predator exclosure fences (hereafter, fences) for nests of critically endangered Florida Grasshopper Sparrows (Ammodramus savannarum floridanus) at a dry prairie site (Three Lakes; 2015–2018) and a pasture site (the Ranch; 2015–2016) in Osceola County, Florida, USA. We installed fences at nests an average of 8 days after the start of incubation, and nest abandonment after fence installation was rare (2 of 149 installations). Predation was the leading cause of failure for unfenced nests at both sites (48–73%). At Three Lakes, nest cameras revealed that mammals and snakes were responsible for 61.5% and 38.5% of predation events, respectively, at unfenced nests. Fences reduced the daily probability of predation (0.016 for fenced nests vs. 0.074 for unfenced nests). The probability that a fenced nest would survive from discovery to fledging was more than double that of unfenced nests (60.4% vs. 27.7%). However, we found no difference in daily nest survival at the Ranch between the year before nests were fenced (2015; 0.874) and the year when all but one nest were fenced (2016; 0.867) because red imported fire ants (Solenopsis invicta) were responsible for 86% of predation events at fenced nests at the Ranch. The use of cameras at fenced nests revealed that site‐specific differences in nest predators explained variation in fence efficiency between sites. Our fence design may be useful for other species of grassland birds, but site‐specific predator communities and species‐specific response of target bird species to fences should be assessed before installing fences at other sites.     

Fine‐scale distribution modeling of avian malaria vectors in north‐central Kansas

Infectious diseases increasingly play a role in the decline of wildlife populations. Vector‐borne diseases, in particular, have been implicated in mass mortality events and localized population declines are threatening some species with extinction. Transmission patterns for vector‐borne diseases are influenced by the spatial distribution of vectors and are therefore not uniform across the landscape. Avian malaria is a globally distributed vector‐borne disease that has been shown to affect endemic bird populations of North America. We evaluated shared habitat use between avian malaria vectors, mosquitoes in the genus Culex and a native grassland bird, the Greater Prairie‐Chicken (Tympanuchus cupido), by (1) modeling the distribution of Culex spp. occurrence across the Smoky Hills of north‐central Kansas using detection data and habitat variables, (2) assessing the occurrence of these vectors at nests of female Greater Prairie‐Chickens, and (3) evaluating if shared habitat use between vectors and hosts is correlated with malarial infection status of the Greater Prairie‐Chicken. Our results indicate that Culex occurrence increased at nest locations compared to other available but unoccupied grassland habitats; however the shared habitat use between vectors and hosts did not result in an increased prevalence of malarial parasites in Greater Prairie‐Chickens that occupied habitats with high vector occurrence. We developed a predictive map to illustrate the associations between Culex occurrence and infection status with malarial parasites in an obligate grassland bird that may be used to guide management decisions to limit the spread of vector‐borne diseases.     

PVC nest boxes are less at risk of occupancy by feral honey bees than timber nest boxes and natural hollows

Feral European Honey Bee (Apis mellifera) has been identified as a potential nest competitor for Australian hollow nesting species, but few studies have investigated the impact of feral honey bee competition on Threatened species. Our study used data from Glossy Black‐cockatoo (Calyptorhynchus lathami halmaturinus) nests on Kangaroo Island, monitored and managed over an 11‐year period, and found 12% of nests became occupied by feral honey bees during that period. Our results indicate that feral honey bees were less likely to occupy nest boxes made of PVC (5%) compared with wooden nest boxes (24%) or natural hollows in Eucalyptus trees (14%). The removal of feral honey bee hives from nests is a priority for long‐term conservation of glossy black‐cockatoos on Kangaroo Island. We recommend that PVC nest boxes are chosen for future nesting habitat restoration, due to the more frequent use of wooden nest boxes by feral honey bees.