Declines in rodent abundance and diversity track regional climate variability in North American drylands.

Regional long-term monitoring can enhance the detection of biodiversity declines associated with climate change, improving future projections by reducing reliance on space-for-time substitution and increasing scalability. Rodents are diverse and important consumers in drylands, regions defined by the scarcity of water that cover 45% of Earth's land surface and face increasingly drier and more variable climates. We analyzed abundance data for 22 rodent species across grassland, shrubland, ecotone, and woodland ecosystems in the southwestern USA. Two time series (1995-2006 and 2004-2013) coincided with phases of the Pacific Decadal Oscillation (PDO), which influences drought in southwestern North America. Regionally, rodent species diversity declined 20%-35%, with greater losses during the later time period. Abundance also declined regionally, but only during 2004-2013, with losses of 5% of animals captured. During the first time series (wetter climate), plant productivity outranked climate variables as the best regional predictor of rodent abundance for 70% of taxa, whereas during the second period (drier climate), climate best explained variation in abundance for 60% of taxa. Temporal dynamics in diversity and abundance differed spatially among ecosystems, with the largest declines in woodlands and shrublands of central New Mexico and Colorado. Which species were winners or losers under increasing drought and amplified interannual variability in drought depended on ecosystem type and the phase of the PDO. Fewer taxa were significant winners (18%) than losers (30%) under drought, but the identities of winners and losers differed among ecosystems for 70% of taxa. Our results suggest that the sensitivities of rodent species to climate contributed to regional declines in diversity and abundance during 1995-2013. Whether these changes portend future declines in drought-sensitive consumers in the southwestern USA will depend on the climate during the next major PDO cycle.

Ecological Traits Driving the Outbreaks and Emergence of Zoonotic Pathogens.

Infectious diseases that are transmitted from wildlife hosts to humans, such as the Ebola virus and MERS virus, can be difficult to understand because the pathogens emerge from complex multifaceted ecological interactions. We use a wildlife-pathogen system-prairie dogs (Cynomys ludovicianus) and the plague bacterium (Yersinia pestis)-to describe aspects of disease ecology that apply to many cases of emerging infectious disease. We show that the monitoring and surveillance of hosts and vectors during the buildup to disease outbreaks are crucial for understanding pathogen-transmission dynamics and that a community-ecology framework is important to identify reservoir hosts. Incorporating multidisciplinary approaches and frameworks may improve wildlife-pathogen surveillance and our understanding of seemingly sporadic and rare pathogen outbreaks.

Plague outbreaks in prairie dog populations explained by percolation thresholds of alternate host abundance.

Highly lethal pathogens (e.g., hantaviruses, hendra virus, anthrax, or plague) pose unique public-health problems, because they seem to periodically flare into outbreaks before disappearing into long quiescent phases. A key element to their possible control and eradication is being able to understand where they persist in the latent phase and how to identify the conditions that result in sporadic epidemics or epizootics. In American grasslands, plague, caused by Yersinia pestis, exemplifies this quiescent-outbreak pattern, because it sporadically erupts in epizootics that decimate prairie dog (Cynomys ludovicianus) colonies, yet the causes of outbreaks and mechanisms for interepizootic persistence of this disease are poorly understood. Using field data on prairie community ecology, flea behavior, and plague-transmission biology, we find that plague can persist in prairie-dog colonies for prolonged periods, because host movement is highly spatially constrained. The abundance of an alternate host for disease vectors, the grasshopper mouse (Onychomys leucogaster), drives plague outbreaks by increasing the connectivity of the prairie dog hosts and therefore, permitting percolation of the disease throughout the primary host population. These results offer an alternative perspective on plague's ecology (i.e., disease transmission exacerbated by alternative hosts) and may have ramifications for plague dynamics in Asia and Africa, where a single main host has traditionally been considered to drive Yersinia ecology. Furthermore, abundance thresholds of alternate hosts may be a key phenomenon determining outbreaks of disease in many multihost-disease systems.

Use of rodenticide bait stations by commensal rodents at the urban-wildland interface: Insights for management to reduce nontarget exposure.

BACKGROUND: Pest management professionals use anticoagulant rodenticides, usually placed in tamper-resistant bait stations, to control commensal rodents, but significant concerns remain about exposure of nontarget species, especially at the urban-wildland interface. We deployed digital cameras to monitor use of bait stations placed in 90 residential yards across Orange County, California, USA. Two bait stations, supplied with nontoxic bait, were monitored in each yard for approximately 30 consecutive days during two camera-trapping sessions between December 2017 and March 2019. One station was placed on the ground, while the other was elevated 1-1.5 m to determine if elevating stations could reduce nontarget exposure. RESULTS: Black rats (Rattus rattus L.) were present at 80% of sites, with mean activity ranging from 0 to 9.6 h each night. There were no significant differences between elevated and ground stations in the time to discovery, time to bait station entry, or nightly activity of rats. Rats discovered bait stations more quickly, and mean nightly activity was greater, in yards where rats were detected more frequently. Although native rodents visited and entered bait stations occasionally, they were relatively rare among our sites (13.3%), and were detected five times less often at elevated stations compared to those on the ground. Yards visited by these rodents were significantly nearer to areas of green open space and natural vegetation, and tended to have no significant barriers to entry, e.g. solid fences or walls. CONCLUSIONS: By elevating bait stations and avoiding placing rodenticides in yards that are likely to be visited by wildlife, pest management professionals may be able to reduce the risk of nontarget exposure, including secondary poisoning of predators and scavengers, while still providing effective control of commensal pests. © 2021 Society of Chemical Industry.

Inferring host-parasite relationships using stable isotopes: implications for disease transmission and host specificity.

Identifying the roles of different hosts and vectors is a major challenge in the study of the ecology of diseases caused by multi-host pathogens. Intensive field studies suggested that grasshopper mice (Onychomys leucogaster) help spread the bacterium that causes plague (Yersinia pestis) in prairie dog colonies by sharing fleas with prairie dogs (Cynomys ludovicianus); yet conclusive evidence that prairie dog fleas (Oropsylla hirsuta) feed on grasshopper mice is lacking. Using stable nitrogen isotope analysis, we determined that many blood-engorged O. hirsuta collected from wild grasshopper mice apparently contained blood meals of prairie dogs. These results suggest that grasshopper mice may be infected with Y. pestis via mechanisms other than flea feeding, e.g., early phase or mechanical transmission or scavenging carcasses, and raise questions about the ability of grasshopper mice to maintain Y. pestis in prairie dog colonies during years between plague outbreaks. They also indicate that caution may be warranted when inferring feeding relationships based purely on the occurrence of fleas or other haematophagous ectoparasites on hosts. Stable-isotope analysis may complement or provide a useful alternative to immunological or molecular techniques for identifying hosts of cryptically feeding ectoparasites, and for clarifying feeding relationships in studies of host-parasite interactions.

Evidence for the involvement of an alternate rodent host in the dynamics of introduced plague in prairie dogs.

1. The introduction of plague to North America is a significant threat to colonies of prairie dogs (Cynomys ludovicianus), a species of conservation concern in the Great Plains. Other small rodents are exposed to the causative agent, Yersinia pestis, during or after epizootics; yet, its effect on these rodents is not known, and their role in transmitting and maintaining plague in the absence of prairie dogs remains unclear. 2. We live-trapped small rodents and collected their fleas on 11 colonies before, during and after plague epizootics in Colorado, USA, from 2004 to 2006. Molecular genetic (polymerase chain reaction) assays were used to identify Y. pestis in fleas. 3. Abundance of northern grasshopper mice (Onychomys leucogaster) was low on sites following epizootics in 2004, and declined markedly following plague onset on other colonies in 2005. These changes coincided with exposure of grasshopper mice to plague, and with periods when mice became infested with large numbers of prairie dog fleas (Oropsylla hirsuta), including some that were infected with Y. pestis. Additionally, several Pleochaetis exilis, fleas restricted to grasshopper mice and never found on prairie dogs on our site, were polymerase chain reaction-positive for Y. pestis, indicating that grasshopper mice can infect their own fleas. No changes in abundance of other rodent species could be attributed to plague, and no other rodents hosted O. hirsuta during epizootics, or harboured Y. pestis-infected fleas. 4. In spring 2004, grasshopper mice were most numerous in colonies that suffered plague the following year, and the pattern of colony extinctions over a 12-year period mirrored patterns of grasshopper mouse abundance in our study area, suggesting that colonies with high densities of grasshopper mice may be more susceptible to outbreaks. We speculate that grasshopper mice help spread Y. pestis during epizootics through their ability to survive infection, harbour prairie dog fleas and, during their wide-ranging movements, transport infected fleas among burrows, which functionally connects prairie dog coteries that would otherwise be socially distinct.

Effects of weather and plague-induced die-offs of prairie dogs on the fleas of northern grasshopper mice.

Plague, the disease caused by the bacterium Yersinia pestis, can have devastating impacts on black-tailed prairie dogs (Cynomys ludovicianus Ord). Other mammal hosts living on prairie dog colonies may be important in the transmission and maintenance of plague. We examined the flea populations of northern grasshopper mice (Onychomys leucogaster Wied) before, during, and after plague epizootics in northern Colorado and studied the influence of host and environmental factors on flea abundance patterns. Grasshopper mice were frequently infested with high numbers of fleas, most commonly Pleochaetis exilis Jordan and Thrassis fotus Jordan. Flea loads changed in response to both environmental temperature and rainfall. After plague-induced prairie dog die-offs, flea loads and likelihood of infestation were unchanged for P. exilis, but T. fotus loads declined.

Resources from another place and time: responses to pulses in a spatially subsidized system.

As the theoretical bases for the dynamics of spatially subsidized communities emerge, ecologists question whether spatially subsidized communities exhibit similar structure or dynamics to communities that receive strongly pulsed resources. In both cases, communities may be structured by responses to resources that are potentially absent at any given point in time (pulsed communities) or space (subsidized communities), even if pulsed resources are part of the in situ productivity of the system or the subsidies arrive as a relatively constant input from a nearby system. The potential for significant spatial or temporal resource limitation, therefore, may be a key factor influencing in similar ways the persistence of populations, the structure and dynamics of communities, and the evolution of specific life history traits. In most complex systems, however, multiple resources may arrive for various trophic entities at various points in time and from various points in space, and thus it may be difficult to separate or compare the dynamics of spatially subsidized and pulsed systems. In this paper, we explore the effects of interactions between pulses and subsidies in plant and animal populations and communities on highly pulsed and variably subsidized islands in the Gulf of California. While many of the plant and animal communities on the unsubsidized islands in this system respond to pulses of rain in classic ways, responses to these rain pulses on islands subsidized by seabird guano or other marine resources are quite different and variable, and depend on a combination of life history characteristics, physiology, competitive interactions, and trophic relationships. These variable responses to rain pulses then translate into large differences in dynamics and community structure of subsidized vs. unsubsidized islands. Indeed, most systems experience both temporal pulses and spatial subsidies. When considered in tandem, complementary or synergistic effects of the multiple, temporally and spatially variable resources may emerge that help explain complex food web structure and dynamics.

No evidence of deer mouse involvement in plague (Yersinia pestis) epizootics in prairie dogs.

Plague, the disease caused by the bacterium Yersinia pestis, can have devastating impacts on black-tailed prairie dog (Cynomys ludovicianus) colonies. One suggested mechanism behind sporadic prairie dog die-offs involves an alternative mammal host, such as the deer mouse (Peromyscus maniculatus), which often inhabits prairie dog colonies. We examined the flea populations of deer mice to investigate the potential of flea-borne transmission of plague between deer mice and prairie dogs in northern Colorado, where plague is active in prairie dog colonies. Deer mice were predominantly infested with the flea Aetheca wagneri, and were rarely infested with prairie dog fleas, Oropsylla hirsuta. Likelihood of flea infestation increased with average monthly temperature, and flea loads were higher in reproductive animals. These results suggest that the deer mouse is an unlikely maintenance host of plague in this region.

Prevalence and abundance of fleas in black-tailed prairie dog burrows: implications for the transmission of plague (Yersinia pestis).

Plague, the disease caused by the bacterium Yersinia pestis, can have devastating impacts on North American wildlife. Epizootics, or die-offs, in prairie dogs (Cynomys ludovicianus) occur sporadically and fleas (Siphonaptera) are probably important in the disease's transmission and possibly as maintenance hosts of Y. pestis between epizootics. We monitored changes in flea abundance in prairie dog burrows in response to precipitation, temperature, and plague activity in shortgrass steppe in northern Colorado. Oropsylla hirsuta was the most commonly found flea, and it increased in abundance with temperature. In contrast, Oropsylla tuberculata cynomuris declined with rising temperature. During plague epizootics, flea abundance in burrows increased and then subsequently declined after the extirpation of their prairie dog hosts.

Exposure of small rodents to plague during epizootics in black-tailed prairie dogs.

Plague, caused by the bacterium Yersinia pestis, causes die-offs of colonies of prairie dogs (Cynomys ludovicianus). It has been argued that other small rodents are reservoirs for plague, spreading disease during epizootics and maintaining the pathogen in the absence of prairie dogs; yet there is little empirical support for distinct enzootic and epizootic cycles. Between 2004 and 2006, we collected blood from small rodents captured in colonies in northern Colorado before, during, and for up to 2 yr after prairie dog epizootics. We screened 1,603 blood samples for antibodies to Y. pestis, using passive hemagglutination and inhibition tests, and for a subset of samples we cultured blood for the bacterium itself. Of the four species of rodents that were common in colonies, the northern grasshopper mouse (Onychomys leucogaster) was the only species with consistent evidence of plague infection during epizootics, with 11.1-23.1% of mice seropositive for antibody to Y. pestis during these events. Seropositive grasshopper mice, thirteen-lined ground squirrels (Spermophilus tridecemlineatus), and deer mice (Peromyscus maniculatus) were captured the year following epizootics. The appearance of antibodies to Y. pestis in grasshopper mice coincided with periods of high prairie dog mortality; subsequently, antibody prevalence rates declined, with no seropositive individuals captured 2 yr after epizootics. We did not detect plague in any rodents off of colonies, or on colonies prior to epizootics, and found no evidence of persistent Y. pestis infection in blood cultures. Our results suggest that grasshopper mice could be involved in epizootic spread of Y. pestis, and possibly, serve as a short-term reservoir for plague, but provide no evidence that the grasshopper mouse or any small rodent acts as a long-term, enzootic host for Y. pestis in prairie dog colonies.

The potential role of swift foxes (Vulpes velox) and their fleas in plague outbreaks in prairie dogs.

Swift foxes (Vulpes velox) have been proposed as potential carriers of fleas infected with the bacterium Yersinia pestis between areas of epizootics in black-tailed prairie dogs (Cynomys ludovicianus). We examined antibody prevalence rates of a population of swift foxes in Colorado, USA, and used polymerase chain reaction (PCR) assays to examine their flea biota for evidence of Y. pestis. Fifteen of 61 (24%) captured foxes were seropositive, and antibody prevalence was spatially correlated with epizootic plague activity in prairie dog colonies in the year of, and previous to, the study. Foxes commonly harbored the flea Pulex simulans, though none of the fleas was positive for Y. pestis.

Effects of prolonged immunocontraception on the breeding behavior of American bison.

In late 2009, the Catalina Island Conservancy began using fertility control to replace periodic removals to manage an introduced population of American bison (Bison bison) on the island. Through the application of the immunocontraceptive vaccine porcine zona pellucida (PZP), population growth was slowed within 1 year, and halted over time. In response to lingering questions about the use of PZP to manage large, free-ranging wildlife populations, we sought to determine the reversibility of PZP by ceasing the annual application to a subset of 15 bison cows and monitoring for subsequent calf arrival, and to document changes in the timing and length of the breeding season in response to PZP by monitoring breeding behavior and assessing fecal progesterone (FP) levels for all 60 resident cows over a 13-month period. As of June 2017, no new calves had been observed on the island, suggesting that, following repeated annual treatment with PZP (3 or 4 years), bison do not resume normal reproduction for at least 4 or 5 years, and that fewer treatments would be advisable if a faster return to fertility is desired. Based on observations of bull and cow behavior, and FP levels, cows displayed estrous cycles consistently throughout the study period, indicating that bison may ovulate year-round when conception and its consequences, e.g., lactation and presence of calves, are blocked. Because there is little evidence that an extended breeding season would negatively impact the health of bulls or result in large numbers of out-of-season births on Catalina, PZP appears to be a highly effective tool for managing the population of introduced bison on the island. However, the extended period of contraception and breeding activity of both cows and bulls may make PZP less suitable in high-latitude, predator-rich environments where bison conservation remains a top priority.

Host usage and seasonal activity patterns of Ixodes kingi and I. sculptus (Acari: Ixodidae) nymphs in a Colorado prairie landscape, with a summary of published North American host records for all life stages.

We examined host usage and seasonal activity patterns of the nymphal stage of the ticks Ixodes kingi and I. sculptus within a prairie rodent community in north-central Colorado. Ixodes kingi was commonly encountered on both northern grasshopper mice (Onychomys leucogaster) and thirteen-lined ground squirrels (Spermophilus tridecemlineatus), whereas I. sculptus frequently infested S. tridecemlineatus but was absent from O. leucogaster. Low numbers of ticks of both species were collected from deer mice (Peromyscus maniculatus) and Ord's kangaroo rats (Dipodomys ordii). Nymphal loads of I. kingi and I. sculptus increased dramatically on commonly infested rodent species from spring (May-June) to summer (July-August). Further, rodents trapped on prairie-dog towns tended to experience increased nymphal loads of I. kingi (O. leucogaster, S. tridecemlineatus) but decreased loads of I. sculptus (S. tridecemlineatus) following plague epizootics among prairie dog populations. A summary of published North American host records revealed that I. kingi has been recorded from humans, domestic animals (cat, dog), 17 species of carnivores, 40 species of rodents, and four species of lagomorphs, and that I. sculptus has been recorded from humans, domestic animals (cat, dog, goat), 13 species of carnivores, 34 species of rodents, and three species of lagomorphs. In accordance with our observations from Colorado, I. kingi commonly has been found to infest heteromyid and murid rodents (such as grasshopper mice), whereas I. sculptus most frequently has been collected from ground-dwelling sciurid rodents, especially Spermophilus ground squirrels. The potential roles of I. kingi and I. sculptus as enzootic vectors of human pathogens, particularly the agents of tularemia (Francisella tularensis), Q fever (Coxiella burnetii), and Colorado tick fever (CTF virus), are discussed.

Community responses of arthropods to a range of traditional and manipulated grazing in shortgrass steppe.

Responses of plants to grazing are better understood, and more predictable, than those of consumers in North American grasslands. In 2003, we began a large-scale, replicated experiment that examined the effects of grazing on three important arthropod groups-beetles, spiders, and grasshoppers-in shortgrass steppe of north-central Colorado. We investigated whether modifications of the intensity and seasonality of livestock grazing alter the structure and diversity of macroarthropod communities compared with traditional grazing practices. Treatments represented a gradient of grazing intensity by cattle and native herbivores: long-term grazing exclosures; moderate summer grazing (the traditional regime); intensive spring grazing; intensive summer grazing; and moderately summer-grazed pastures also inhabited by black-tailed prairie dogs (Cynomys ludovicianus Ord). Beetles and spiders were the most common groups captured, comprising 60% and 21%, respectively, of 4,378 total pitfall captures. Grasshopper counts were generally low, with 3,799 individuals observed and densities <4 m(-2). Two years after treatments were applied, vegetation structure differed among grazing treatments, responding not only to long-term grazing conditions, but also to the short-term, more-intensive grazing manipulations. In response, arthropods were, in general, relatively insensitive to these grazing-induced structural changes. However, species-level analyses of one group (Tenebrionidae) revealed both positive and negative effects of grazing treatments on beetle richness and activity-density. Importantly, these responses to grazing were more pronounced in a year when spring-summer rainfall was low, suggesting that both grazing and precipitation-which together may create the greatest heterogeneity in vegetation structure-are drivers of consumer responses in this system.

Polymerase chain reaction (PCR) identification of rodent blood meals confirms host sharing by flea vectors of plague.

Elucidating feeding relationships between hosts and parasites remains a significant challenge in studies of the ecology of infectious diseases, especially those involving small or cryptic vectors. Black-tailed prairie dogs (Cynomys ludovicianus) are a species of conservation importance in the North American Great Plains whose populations are extirpated by plague, a flea-vectored, bacterial disease. Using polymerase chain reaction (PCR) assays, we determined that fleas (Oropsylla hirsuta) associated with prairie dogs feed upon northern grasshopper mice (Onychomys leucogaster), a rodent that has been implicated in the transmission and maintenance of plague in prairie-dog colonies. Our results definitively show that grasshopper mice not only share fleas with prairie dogs during plague epizootics, but also provide them with blood meals, offering a mechanism by which the pathogen, Yersinia pestis, may be transmitted between host species and maintained between epizootics. The lack of identifiable host DNA in a significant fraction of engorged Oropsylla hirsuta collected from animals (47%) and prairie-dog burrows (100%) suggests a rapid rate of digestion and feeding that may facilitate disease transmission during epizootics but also complicate efforts to detect feeding on alternative hosts. Combined with other analytical approaches, e.g., stable isotope analysis, molecular genetic techniques can provide novel insights into host-parasite feeding relationships and improve our understanding of the role of alternative hosts in the transmission and maintenance of disease.

Scavenging by mammalian carnivores on prairie dog colonies: implications for the spread of plague.

Plague causes mass mortality of prairie dogs (Cynomys ludovicianus) in shortgrass steppe. Although the pathogen, the bacterium Yersinia pestis, is spread within colonies by flea bites or contact between infected hosts, it is unclear how Y. pestis is transported over long distances between isolated colonies. One possibility is that wideranging, plague-resistant mammalian carnivores pick up fleas when scavenging prairie dog carcasses. Using guinea pigs as surrogates for prairie dogs, we compared how quickly scavengers discovered carcasses on active prairie dog colonies, on colonies recently extirpated by plague, and in grasslands without prairie dogs. In June-July 2007, we monitored the fates of 20 guinea pig carcasses for 4 consecutive days on each site type. Ten carcasses were placed in wire exclosures that restricted access only to arthropods and small rodents; the other 10 were exposed to all scavengers. Scavengers were identified by tracks, evidence of consumption, and/or remote cameras. Carnivores discovered carcasses more quickly on active and plague colonies (mean +/- 95% confidence interval [CI]: 1.6 +/- 0.7, 1.4 +/- 1.4 days, respectively) than on grasslands (3.1 +/- 0.7 days). By the end of the trials, all (100%) exposed carcasses were removed from active colonies, whereas 60% were removed from plague colonies and 30% were removed from grasslands. Rates of carcass discovery and removal on active colonies were significantly greater than in grasslands, which mirrored differences in carnivore activity recorded during earlier scat surveys. A small fraction (30%-40%) of carcasses in exclosures were eaten by rodents, but only on active and plague colonies, suggesting that small rodents, presumably grasshopper mice (Onychomys leucogaster), may also consume carcasses and pick up fleas if carcasses are not removed by carnivores first. These results, combined with observations that fleas remain alive on prairie dogs at least 1 day following their death, suggest that carnivores may encounter infectious fleas while scavenging, and they could transport them over long distances.

Marine resources subsidize insular rodent populations in the Gulf of California, Mexico.

Inputs of energy and nutrients from one ecosystem may subsidize consumers in adjacent ones, with significant consequences for local communities and food webs. We used stable isotope and faecal pellet analysis to quantify use of ocean-derived resources by small mammals on islands in the Gulf of California, Mexico. Rodents were live-trapped on grids originating near shore and extending 125-200 m inland to evaluate the extent to which rodents transport marine nutrients inland, and to determine whether marine foods subsidize island populations, permitting higher densities than would be possible based on terrestrial resources alone. Both faeces and stable carbon and nitrogen isotopes revealed that omnivorous mice (Peromyscus maniculatus) consume ocean-derived prey, including littoral and supralittoral invertebrates, and that their diets differed markedly from those of granivorous rodents (Chaetodipus rudinoris). On a small, seabird roosting island, marine prey were important in the diet of mice regardless of their proximity to shore, underscoring the pervasive influence of the ocean on small islands with relatively large coastline area. On a large island, however, consumption of marine foods declined sharply > or =50 m from shore, which suggests that mice are poor conduits of inland movement of energy and nutrients from the sea. Marine resources seemed to act as subsidies for omnivorous rodents: more P. maniculatus were captured near shore than farther inland and there was an inverse relationship between island area and rodent abundance, suggesting that small islands with large amounts of marine inputs support the highest population densities. Patterns of local and island-wide abundance of P. maniculatus are likely the result of several interacting factors, including frustrated dispersal, competition with C. rudinoris, and the absence of predators. We speculate, however, that the availability of marine resources allows P. maniculatus to reach high densities and to persist on small islands in the Gulf despite low and unpredictable terrestrial productivity. Spatial trophic subsidies thus provide a possible mechanistic explanation for the widely reported inverse relationship between population density and island or habitat area.