Published March 31, 2015

COMPANION ANIMALS SYMPOSIUM: Sustainable ecosystems: Domestic cats and their effect on wildlife populations1 S. E. Kitts-Morgan2 Department of Animal Science, Berry College, Mount Berry, GA 30149

ABSTRACT: Domestic cats are estimated to kill billions of small mammals and birds each year. In certain areas of the world, it is not uncommon for either feral or free-ranging cats to have high population densities, creating concern regarding their level of hunting. Many cats are considered to be subsidized predators, as they receive care and food from humans. Arguments abound regarding the presence of cats in the habitats of native small mammals and birds and whether or not local ecosystems can sustain this predator–prey relationship. The effects of cats on native wildlife can depend on several factors, including cat classification (feral vs. free ranging vs. indoor– outdoor), geographical location (islands vs. mainland), and type of habitat (rural vs. suburban vs. urban). Feral and free-ranging cats may have a greater impact on native species on islands because habitat is severely

limited. Continued urbanization and development of rural areas also creates fragmented habitats, and native species may struggle to survive with the added pressure of hunting by domestic cats. Additionally, cats in rural areas are frequently fed by humans, which can support high population densities and intensify pressure on native species. Species targeted by cats may also vary based on prey availability in different areas, but small mammals are generally preferred over birds, reptiles, or invertebrates. Domestic cats certainly have the potential to roam and hunt in very large areas inhabited by native species and loss of biodiversity is a major concern. Therefore, it is possible that ecosystems may not be able to sustain hunting by domestic cats. Because this predator–prey relationship is probably not sustainable, it is necessary to responsibly manage outdoor domestic cats.

Key words: feral cats, free-ranging cats, hunting, predation, sustainability, wildlife © 2015 American Society of Animal Science. All rights reserved. J. Anim. Sci. 2015.93:848–859 doi:10.2527/jas2014-8557 INTRODUCTION Felis catus, the modern day domestic cat, is the most widespread terrestrial carnivorous species on earth and can severely impact populations of small mammals, avian species, and insects (Konecny, 1987). Over the past 40 yr, the number of domestic cats in the United States has tripled (Lepczyk, 2008). Regardless of classification (e.g., indoor–outdoor, free ranging, feral), cats with outdoor access that hunt may negatively affect wildlife. Furthermore, 1Based on a presentation at the Companion Animals Symposium

titled “Companion animals and sustainability; Today’s impact on the future” at the Joint Annual Meeting, July 20–24, 2014, Kansas City, MO. 2Corresponding author: [email protected] Received September 26, 2014. Accepted December 18, 2014.

848

cats can reside in high densities and, when receiving food from humans, are described as subsidized predators. Regular access to food provided by humans does not suppress hunting behavior in cats, and they may continue to kill even when prey populations are low (Adamec, 1976; Turner and Meister, 1988). Cats prey on a wide variety of native mammals, and cats residing around human habitations hunt nonnative rodents, which are commonly associated with human activity (Langton et al., 2001). Depending on geographical location, season, and species availability, cats hunt various invertebrates, reptiles, amphibians, and birds, sometimes to complete or local extinction (Iverson, 1978; Nogales et al., 2004). In sustainable ecosystems, biological systems must remain diverse and productive, so major concern exists regarding the sustainability of a predator–prey relationship where the predator is subsidized and can exert tre-

Domestic cats and sustainable ecosystems

mendous pressure on prey. In many areas, prey hunted by cats may be endangered, and further decreasing the population threatens population viability and diversity. Whereas our understanding of the ecological impact of domestic cats has improved, much remains to be learned regarding how cats affect wildlife. The objective of this paper is to critically examine the effects of domestic cats on native and nonnative wildlife, including factors determining prey types targeted by cats. Additionally, sustainability of the predator–prey relationship will be discussed, with focus on management strategies to reduce hunting by domestic cats. EFFECTS OF CATS ON WILDLIFE Whereas it is unclear how many feral cats are in the United States, there are approximately 95.6 million pet cats (APPMA, 2013). Across Europe, there are approximately 17.3 million pet cats, and in the United Kingdom, there are estimated to be 8.5 million pet cats (FEDIAF, 2012; PFMA, 2013). The domestic cat has evolved with humans over thousands of years and is now present in most parts of the world (Fitzgerald, 1990; Brickner, 2003; Baker et al., 2010). Whereas domestic cats are genetically similar to their primary progenitor, Felis silvestris, they are now considered to be a distinct species (O’Brien and Johnson, 2007). Because they are a species distinct from their wild ancestors, they are classified as a nonnative species throughout the world (Fitzgerald, 1990; Lowe et al., 2000; Baker et al., 2010); consequently, native prey species usually have no evolved defenses against this invasive predator. Invasive species, particularly predators, have been implicated in the decline and extinction of native species throughout the world over the past centuries (Clavero and Garcia-Berthou, 2005). Domestic cats, in particular, are highly skilled predators and have been implicated in the extinction of numerous mammals, reptiles, and bird species (Iverson, 1978; Mellink, 1992; Lever, 1994; Mitchell et al., 2002; Tershey et al., 2002). They are listed among the 100 worst nonnative invasive species in the world (Lowe et al., 2000). Furthermore, evidence shows cats to be responsible for a significant proportion of wildlife mortality (Churcher and Lawton, 1987; Baker et al., 2008; Balogh et al., 2011). Beyond their direct hunting of wildlife, domestic cats also compete with native mesopredators such as skunks, opossums, raccoons, and foxes for prey. Cats are subsidized predators and have a distinct advantage over native predators because they receive food, water, and shelter from humans, which helps them to reach very high densities, sometimes 100 times greater than the density of native predators (Coleman and Temple, 1993; Hawkins,

849

1998). Research certainly shows that domestic cats have devastating effects on both native prey and predators. In fact, recent research estimates that annual mortality due to cats in the contiguous United States at between 6.9 and 20.7 billion mammals and between 1.4 and 3.7 billion birds (Loss et al., 2013). These estimates greatly exceed previous estimates of bird mortality due to cats (Banks, 1979; Gill, 1994; Dauphine and Cooper, 2009). It is likely impossible to determine the cumulative impact of domestic cats on wildlife, but research continues to further our understanding of how cats influence ecosystems through wildlife mortality. Different populations of cats contribute to wildlife mortality, and some contribute to a greater extent than others. Therefore, it is necessary to understand how cat populations are generally classified within the literature. Classification of Domestic Cat Ranging Behavior It is important to define the differences between various cat populations so as to attempt to understand the true impact domestic cats have on the environment, wildlife, and, ultimately, an ecosystem. It is not an easy task to clearly define cat populations, as individual cats can easily move from one category to another throughout the course of their lives. Furthermore, we can only estimate mortality of prey for different cat populations because we can only approximate the number of cats existing within a defined population. Domestic cats can be classified in several different ways according to degree of acclimation to humans, access to human habitations, and status as pets. Feral cats are generally unsocialized, unwanted, unconfined, and unowned cats. They are usually born in the wild and never socialized or are abandoned and become untrusting of humans. (Levy and Crawford, 2004). Feral kittens may sometimes be tamed, but rehabilitation of older feral cats may be difficult. Furthermore, feral cats are reproductively intact and contribute to overpopulation issues, therefore resulting in excessive killing of wildlife, which could reduce wildlife populations. Some areas do have trap–neuter–return programs in place to reduce feral cat numbers; however, the efficacy of these programs remains questionable (Lohr et al., 2013; Dombrosky and Wolverton, 2014). Freeranging or free-roaming cats could either be owned or stray and unconfined but at least partially socialized (Slater, 2001). Many owned cats fall into this category, as owners do not want indoor cats and simply keep the cats outside. These cats are most certainly subsidized predators, as owners of free-ranging cats provide food, water, and possibly shelter. Indoor (house) cats are not considered to be an invasive species or subsidized

850

Kitts-Morgan

predator because they are confined indoors and not allowed to hunt and kill wildlife. Indoor cats are owned, socialized, and confined. Domestic cats can also be classified according to ownership status, and the previously described categories of cats can fall within an ownership class. Owned cats usually (but not always) spend some time indoors and some research indicates that over 50% of owned cats spend time outdoors (APPMA, 1997; Loss et al., 2013). Owned cats that wander or become lost may become stray cats and it is possible for stray cats that live in the wild for an extended period of time to become feral (Levy and Crawford, 2004). On the other hand, unowned cats spend all of their time outdoors and could include free-ranging, feral, or stray cats (Loss et al., 2013). It is possible that domestic cats can occupy different categories at different periods in their lives and this fact makes it extremely difficult to accurately estimate cat populations within these categories. Furthermore, research studying these cats can define these terms differently. Regarding the impact of these cat populations on wildlife, cats within the aformentioned categories are managed differently, which can have serious consequences for wildlife. Native and Nonnative Mammals Hunted by Domestic Cats Whereas domestic cats are generalist predators that thrive in a variety of environmental conditions and hunt a wide variety of prey, research has shown they preferentially depredate mammals over other taxa (Loss et al., 2013). Individual unowned cats in the United States can reach predation rates of 200 mammals/yr (Nilsson, 1940; Hubbs, 1951; Llewellyn and Uhler, 1952; Parmalee, 1953). Of the annual mammal mortality rate previously mentioned, unowned cats are responsible for 89% (Loss et al., 2013). The mammals killed by cats include both native and nonnative species and the patterns of predation may be dependent on habitat. The prey of cats in suburban and particularly rural settings is dominated by native small mammals, such as native mice and rats, shrews, voles, squirrels, and rabbits (Errington, 1936; Llewellyn and Uhler, 1952; Kays and DeWan, 2004). Furthermore, other research indicates that rodent species are a primary prey of freeranging cats (Mitchell and Beck, 1992). A study that examined food habits of farm cats in Switzerland confirmed that whereas the diet of these cats was composed heavily of cat food provided by humans, the main prey item consisted of rodents such as voles and the wood mouse (Apodemus sylvaticus; Weber and Dailly, 1998). Another study examined predation by owned cats in an English village and also found their diets to contain pri-

marily small mammals, particularly rodents (Churcher and Lawton, 1987). These cats also targeted wood mice, various voles, and shrews, which are all native species. Interestingly, this study showed that as cat density increased, prey caught per cat decreased, which indicates the negative effect on wildlife of a high density of cats. Whereas these studies provide valuable information regarding specific prey targeted by domestic cats in Europe, these species are not necessarily the same as those found in the United States. In fact, only a few studies using domestic cats in the United States have attempted to identify native rodents and other small mammals hunted by cats. A study of suburban inside and outside cats in New York found mammals to be the predominate prey, and they identified deer mice (Peromyscus spp.), northern short-tailed shrew (Blarina brevicauda), eastern cottontail (Sylvilagus floridanus), eastern chipmunk (Tamias striatus), and the meadow vole (Microtus pennsylvanicus) as the major species targeted by these cats (Kays and DeWan, 2004). Another study of free-ranging cats in rural and urban Virginia found the woodland vole (Microtus pinetorum), white-footed mouse (Peromyscus leucopus), and northern short-tailed shrew to be the primary prey of these cats (Mitchell and Beck, 1992). A more recent study of free-roaming cats in a suburban area of Georgia used animal-borne video cameras to observe predation (Loyd et al., 2013). Native mammals hunted by these cats included mainly woodland vole and eastern chipmunk. Studies that identify specific native mammalian species hunted by cats in different geographical areas of the United States are important to further our understanding of patterns of predation within urban, suburban, and rural areas. Whereas many native mammals are found in rural habitats, certain species, such as woodland voles, have been documented in suburban areas (Loyd et al., 2013). As rural and suburban areas recede due to urbanization, it is crucial to understand the effects of habitat change (i.e., loss) on native small mammals. Additionally, with an increase in suburban and urban landscapes, cat density may increase, which increases the pressure on native small mammal populations. Another consideration may be the effects of cat predation in newer suburban developments close to unmodified natural areas, as prey species in these areas may be at greatest risk due to lack of previous exposure to cats as predators. Depredation of native small mammals by domestic cats is a major concern for at least 2 reasons: loss of biodiversity due to local or complete extinction and decreased prey for native predators. However, domestic cats’ hunting of nonnative small mammals, such as rodents, is generally a desired behavior, as these animals are considered pests. Nonnative rodents present in the

Domestic cats and sustainable ecosystems

United States include the Norway rat (Rattus norvegicus), black rat (Rattus rattus), and house mouse (Mus musculus). These species were introduced into the New World during colonization and have become well established over most of the United States (Whitaker and Hamilton, 1998). They have adapted well to life with humans and have moved with humans throughout the world. Their status as a pest has developed because they damage crops and buildings, and the Norway and black rats carry diseases, such as bubonic plague, typhus, Salmonella, and trichinosis (Whitaker and Hamilton, 1998). Whereas these nonnative pests are generally associated with human habitations, they are highly adaptive and can thrive in agricultural settings, not only in barns but in fields with abundant plant cover or crops (Stroud, 1982; Pocock et al., 2004; Klemann and Pelz, 2006). Norway rats, black rats, and house mice are all suitable prey for domestic cats living in urban, suburban, and rural areas. Cats will hunt these species as long as they are available and, in some urban settings, they may be the only rodent prey available. A study by Jackson (1951) estimated the impact of urban cats on rat populations in Baltimore and found that an individual cat would remove an average of 28 rats/yr. In other research, feral cats in rural areas fed extensively on black rats in New Zealand and Australia (Fitzgerald and Karl, 1979; Jones and Coman, 1981). In Auckland City, New Zealand, owned cats in a suburban area killed 486 rodents over the period of 1 yr, of which 61.5% were Norway and black rats. The remaining 38.5% were house mice (Gillies and Clout, 2003). On Mauna Loa in Hawaii, house mice were a major component of the diet of feral cats (Hess et al., 2007). It is clear from these studies that domestic cats will hunt and kill nonnative rodents, and regardless of the area being rural, suburban, or urban, removal of these pests is a desired behavior. However, cats will only limit hunting of mammals to nonnative mammals if native mammals are unavailable. A study by Molsher et al. (1999) indicated that domestic cats continued to hunt nonnative rabbits, most likely because they were an abundant prey. It is also possible that individual cats develop particular skills for hunting specific prey and they will continue to target that prey as long as it is available. Removal of rats and mice from buildings and barns by domestic cats is beneficial for humans, as reservoirs for disease and consumers of stored grain are eliminated. Many people keep free-ranging cats solely for this purpose, particularly in agricultural settings. Therefore, it is possible that farms may support high densities of cats due to providing a food source (hunting opportunities and supplemental cat food) and shelter. Indeed, a study evaluating the presence of free-ranging cats in various agricultural settings in Wisconsin found that livestock farms were more likely

851

to have cats than crop-only or nonfarm residences and that livestock farms had more cats than any other type of residence (Coleman and Temple, 1993). Additionally, people who had cats as predators to control pest species or as both pets and predators had more cats than people who had them for other reasons. This research reinforces the fact that having cats for pest control is very important in agricultural settings. However, having multiple cats in these situations artificially increases the density of cats, which may in turn negatively affect native wildlife due to hunting pressure by the cats. The study by Coleman and Temple (1993) showed that residences with cats had an average of 7.6 cats and the majority of these residences were farms. This value tends to agree with other research estimating number of rural cats per residence (Warner, 1985). Cat densities can sometimes reach the densities of other rural mammalian predators or even exceed them by several fold (Coleman and Temple, 1993). In the study by Coleman and Temple (1993), it was estimated that free-ranging cat densities could be as great as 40 to 44 cats/km2 in livestock-raising counties of Wisconsin, with an average density statewide of 10 to 14 cats/km2. It is likely that greater cat densities in rural areas are partially due to the availability of supplemental food particularly available on farms (Coleman and Temple, 1993). Furthermore, other studies have shown cats in rural areas are typically fed by their human caretakers (Liberg, 1984; Warner, 1985). Considering that people in rural areas intentionally keep cats as predators and they may not be neutered, cat density has the potential for an enormous increase and, thus, a negative effect on wildlife. Not only does an increase in cat density have the potential to increase hunting pressure on prey species, these cats may also compete with native predators. It may also be possible to have additive effects of cat predation along with predation by native predators, thus intensifying the impact on wildlife. Birds and Other Animals Hunted by Domestic Cats Using data from U.S. studies, Loss et al. (2013) estimated that cats in the contiguous United States kill between 1.4 and 3.7 billion birds/yr, with approximately 69% of this mortality caused by unowned cats. This estimate surpasses previous mortality estimates from other studies due to cats and other sources of anthropogenic mortality (Banks, 1979; Pimentel et al., 1991; Gill, 1994; Coleman and Temple, 1996; Erickson et al., 2005; Klem, 2009; Manville, 2009; Longcore et al., 2012). In Canada, there are estimated to be approximately 11.3 million cats, with 7.5 million of those cats living outdoors (Blancher, 2013). These cats are estimated to kill 204 million birds/yr

852

Kitts-Morgan

(Blancher, 2013). In Great Britain, a population of 9 million domestic cats has been estimated to kill 27 million birds/yr (Woods et al., 2003). Research has found that exotic predators, such as feral cats, are among the most significant threats to bird species (Butchart et al., 2006). Whereas mammals such as rodents and lagomorphs are generally the preferred prey taxons for domestic cats, birds will be hunted when small mammals are either less available or unavailable (Mitchell and Beck, 1992). Domestic cats are responsible for at least 33 bird extinctions and are probably a major cause of bird extinctions worldwide (Nogales et al., 2004). The devastating effects of cats on bird populations are likely due to these cats existing as subsidized predators and receiving supplemental food from humans. By feeding cats, providing shelter, and removing higher predators such as wolves and coyotes, humans enable predation of wildlife by cats (Dauphine and Cooper, 2009). Facilitating wildlife predation by cats is probably unintentional and most people may not even realize it occurs, but it is an important secondary effect that should be considered when caring for cats that do not dwell inside houses. A study conducted in a public park on California’s central coast compared an area where no cats were found to an area where cats were being fed by humans (Hawkins et al., 2004). In the “no-cat” area, they discovered almost double the number of birds compared with the area known to have cats. The general public remains unaware of the serious implications incurred on wildlife due to feeding and maintaining feral and free-ranging cat populations. Unfortunately, the effect of cat hunting on bird species is even more dramatic when it is considered that many bird species are restricted to certain ranges or habitats. Birds in these populations, particularly those that may already be endangered or threatened, are much more vulnerable to predators in general and are also likely to exhibit a dramatic population decline. As cats are an introduced species to islands, their impact on endangered or threatened birds can be devastating. This impact may be in addition to habitat loss caused by humans, size of the island, and history of no predators. Humans facilitate the creation of fragmented habitats on islands by splintering land into inhospitable areas (i.e., by buildings and roads) bordered by somewhat intact habitats. Whereas some bird species may adapt quite well to increasing urbanization, this loss of habitat may be treacherous for others, especially when combined with the hunting pressure of cats. Additionally, cats present on small islands and islands with a history of no predators present a further risk to birds. Islands typically have little diversification in plant and animal species and high rates of endemism, which increase their susceptibility to ecological

disturbances, particularly when exotic predators are introduced (Paulay, 1994). Furthermore, mammalian prey may be scarce on islands, in which case cats will begin hunting birds (Kirkpatrick and Rauzon, 1986). On the islands of Hawaii, domestic cats established a population in the 1840s and since then, feral cats have hunted various areas without a great deal of human intervention (Tomich, 1986; Hess et al., 2007). In lowland and coastal areas of Hawaii, cats depredate nesting colonial seabirds and in higher elevations, they target burrow-nesting seabirds, tree-nesting passerines, and ground-nesting waterfowl (Banko, 1992; Hodges and Nagata Sr., 2001; Smith et al., 2002; Hess et al., 2004). Cats have at least contributed to the global extinctions of some birds on islands, including the Socorro dove (Zenaida graysoni) in Mexico, the Stephens Island wren (Xenicus lyalli) in New Zealand, and the Guadalupe storm petrel (Oceanodroma macrodactyla) in Mexico (Nogales et al., 2004). Regional extinctions attributed at least partially to the domestic cat include Cassin’s auklet (Ptychoramphus aleuticus) from the Coronado Islands, Mexico, and the common diving petrel (Pelecanoides urinatrix) from Marion Island, South Africa (Nogales et al., 2004). Another approach to assessing the effects of cats on bird species is to evaluate how they hunt based on type of area: urban, suburban, or rural. Research has shown that the abundance of birds and other species varies between urban and rural areas (Mills et al., 1989; Blair, 1996; Chace and Walsh, 2006; van Heezik et al., 2008). Therefore, it is likely that cats will hunt different species, including a wide variety of bird species, depending on their habitat. Furthermore, the density of cats may vary based on area, and they may exist in greater densities in urban habitats (Paton, 1991; Lepczyk et al., 2004; Baker et al., 2008; Sims et al., 2008). Native bird species will likely exist in the intact vegetation bordering urban areas because there will be more resources to sustain them (Sewell and Catterall, 1998). As cats move into these natural areas, native birds are increasingly hunted. Research in New Zealand monitored the prey of cats in 2 suburban areas and found that more native birds were killed by cats in the urban-forest fringe area (fragmented habitat) than in the fully urban habitat (Gillies and Clout, 2003). It is unclear as to the level of preference cats have for hunting in these fragmented areas, but the potential for damage to native animals is greater when cats live within foraging distance of areas where these animals reside. The bird species hunted by cats in urban vs. suburban or rural areas may differ, as species such as the house sparrow (Passer domesticus) and European starling (Sturnus vulgaris) often represent over 70% of the birds in urban areas (Savard et al., 2000). Removal of

Domestic cats and sustainable ecosystems

these birds by cats can be beneficial because they are perceived as a nuisance when they reach high densities in urban ecosystems. Unfortunately, species such as the house sparrow and European starling have coevolved with cats in Europe over thousands of years and are probably more adept at evading them. Native species on islands and continents such as North America have had less time to adapt their behavior (only decades to 200 yr) and may be easier targets for cats (Jessup, 2004). Research indicates that when cats have a choice of prey, they tend to select native rodents and birds over introduced species (Hawkins et al., 1999). However, cats are also opportunistic hunters and will take prey in proportion to their availability, regardless of species (Fitzgerald and Turner, 2000; Lepczyk et al., 2004). A study in New Zealand evaluated specific urban areas for both the density of some native and exotic bird species as well as the number of kills of those species by cats (van Heezik et al., 2010). Within 3 urban areas, 2 nonnative species (house sparrows and blackbirds; Turdus merula) and 1 native species (silvereye; Zosterops lateralis) were found in the greatest densities per hectare. These same species were also killed in the greatest rates within those same urban areas, even when accounting for number of cats. Another study in New Zealand also evaluated the predation of these same species in suburban areas and also found house sparrows, silvereyes, and blackbirds to be the most commonly caught species (Gillies and Clout, 2003). Interestingly, whereas house sparrows and European starlings are invasive species in most of the world, there is actually conservation concern for these birds in urban areas of the United Kingdom where a substantial population of these birds exists (Baker et al., 2005). Whereas the house sparrow is one of the most common avian species in the United Kingdom, the species has been declining in urban areas (Howes, 2002; Siriwardena et al., 2002; Woods et al., 2003). There have been a few studies conducted in the United States where species of birds killed by cats were identified. In Virginia, a rural cat killed 8 different native bird species, including American goldfinch (Spinus tristis), white-throated sparrow (Zonotrichia albicollis), dark-eyed junco (Junco hyemalis hyemalis), and Carolina wren (Thryothorus ludovicianus; Mitchell and Beck, 1992). Urban cats in this study killed 6 different species and less than half the total number of birds compared with the rural cat. Most of the species killed included those that nest on or near the ground or feed on the ground, which likely subjected them to higher levels of predation (Wilcove, 1985). In another study of inside–outside cats around a suburban nature preserve in New York, prey included gray catbirds (Dumetella carolinensis) and ovenbirds

853

(Seiurus aurocapillus), which also prefer to nest and feed on or near the ground (Kays and DeWan, 2004). Carolina wrens, house wrens (Troglodytes aedon), and American robins (Turdus migratorius) were targeted less, most likely because these birds usually nest higher above the ground. Avian prey of suburban cats in Georgia included the American robin, hermit thrush (Catharus guttatus), and eastern phoebe (Sayornis phoebe; Loyd et al., 2013). Whereas none of the native species depredated in these U.S. studies are threatened or endangered, it is certainly possible that localized hunting pressure by cats, regardless of location, could reduce populations. Although a fair amount of research has been conducted on islands to evaluate the effects of cats on indigenous and endemic species, it is critical that more research be conducted to determine predation by cats on continental birds. We certainly know less regarding endangered or threatened birds targeted by cats, particularly in the United States. Whereas small mammals and birds are undeniably the most hunted vertebrates by domestic cats, if these taxa are present in low densities or unavailable, cats will shift to hunting reptiles, amphibians, and invertebrates, particularly on islands (Fitzgerald and Turner, 2000; Nogales and Medina, 2009; Bonnaud et al., 2011). A review by Medina et al. (2011) summarized the impacts of feral cats on vertebrates on 120 islands around the world and found that 25 threatened reptile species have been impacted by cats on islands. These threatened reptiles included 16 taxa that were endemic and 9 natives. This review also determined that most research regarding the effects of cats on reptiles occurred in the Caribbean, with little research in the Pacific (Medina et al., 2011). Examples of invertebrates hunted by cats include insects, spiders, woodlice, crayfish, or molluscs (Fitzgerald, 1988). Generally, invertebrates do not contribute significantly to the total biomass consumed by cats; therefore, many studies will simply list the most important ones and not attempt to identify all species (Fitzgerald, 1988). However, a study of the diet of feral cats in the Canary Islands did identify 28 different invertebrate species in the analysis of 500 cat scats (Medina and Garcia, 2007). They also found that consumption of invertebrates occurred less within a temperate forest habitat, which could reflect less abundance of invertebrates in this ecosystem (Medina and Garcia, 2007). Another study evaluating the diet of feral cats in Hawaii found that 86% of the digestive tracts contained invertebrates, including some intertidal marine species (Hess et al., 2007). In New Zealand, the prey of cats in 2 suburban areas included a significant number of invertebrates, including crickets (Teleogryllus commo-

854

Kitts-Morgan

dus), lepidopterans, and cicadas (Cicadidae; Gillies and Clout, 2003). Whereas some research in the United States has examined the effect of cat predation on reptiles and amphibians, more studies need to be conducted. Loss et al. (2013) used data from studies in Europe, Australia, and New Zealand to estimate that between 258 and 822 million reptiles and 95 to 299 million amphibians are killed by cats in the contiguous United States each year. Predation by cats in rural and urban Virginia demonstrated that cats in rural areas kill more reptiles, including lizards and snakes, as well as amphibians such as frogs (Mitchell and Beck, 1992). Similarly, prey hunted by suburban cats in Georgia included a large number of reptiles and amphibians as well as various invertebrates (Loyd et al., 2013). Both of these studies also found that predation of reptiles, amphibians, and invertebrates occurred primarily in the warm months of the year and greatly declined during the winter (Mitchell and Beck, 1992; Loyd et al., 2013). Because reptiles bask in sunlight during summer months, they become particularly visible and vulnerable to predators such as cats. In suburban areas, there could be a localized population impact on these animals by domestic cats. A study in Florida found a greater percentage of brown anoles (Anolis sagrei) with regenerated tails in areas known to have well-fed pet cats as compared with areas with feral cats (Bateman and Fleming, 2011). This was presumably due to feral cats completely consuming captured anoles, whereas pet cats “played” with their catch. Many anoles may escape from these cats through tail autotomy. Clearly, reptiles such as anoles are hunted by cats, whether for food or for sport. Outside the United States, research on Socorro Island in Mexico supports hunting of lizards by feral cats because they were found in up to 67% of the scat collected from the cats (Arnaud et al., 1993). Furthermore, a review by Medina et al. (2011) found that the most important groups of reptiles affected by cat predation on islands to be iguanas and lizards followed by turtles and snakes. In Australia, a study conducted over 22 yr observed the fauna present on a property and visitations by cats to the area (Bamford and Calver, 2012). In this study, 1 pet cat was observed hunting on the property daily and likely responsible for the local extermination of a small population (estimated at 40 to 50 animals) of lizards (Ctenotus fallens) over a 2-yr period. This study is important because it indicates a localized impact of cat hunting on 1 reptile species. Reptiles, amphibians, and invertebrates are vitally important in ecosystems. Reptiles and amphibians play vital roles in food webs and are known to be indicators of environmental health. Invertebrates dominate most ecosystems and provide food for mam-

mals, birds, reptiles, and amphibians. Threats to these groups by introduced species, such as cats, mean a serious loss of biodiversity. SUSTAINABILITY OF THIS PREDATOR–PREY RELATIONSHIP Natural ecosystems are sustainable only when native biodiversity and the functional basis of productivity are maintained. The ecological roles played by organisms within the ecosystem will influence biodiversity, productivity, and sustainability. Therefore, the role of domestic cats within an ecosystem can be described as a predator with the potential to decrease biodiversity and productivity. Therefore, by decreasing biodiversity and productivity through the action of overhunting a species, it is concluded that the presence of cats within an ecosystem may not be sustainable. If wildlife populations are to be sustained and remain intact, the delicate balance of relationships between all species must not be disturbed. Domestic cats certainly have the potential to disturb this balance. The dramatic effect domestic cats can have on wildlife through this predator–prey relationship cannot be overstated. The research evaluated in this review has clearly shown that domestic cats will hunt and kill small mammals, birds, reptiles, amphibians, and invertebrates regardless of geographic location (islands vs. mainland), type of habitat (rural, suburban, or urban) or cat classification (feral vs. free ranging vs. inside–outside). However, the impact of cat predation may vary based on the aforementioned factors. Clearly, cats have the potential to severely depredate native wildlife on islands, as these are typically small, confined areas with the additional pressure of habitat loss and a history of no predators. Domestic cats are an invasive species against which native wildlife on islands have little defense because they have not evolved with cats. In addition to the impact of cats on islands, cats may contribute to faunal decline on continents through predation, as illustrated by failed reintroduction attempts of several mammalian and reptilian species in South Australia (Moseby et al., 2011). Similarly, native wildlife inhabiting fragments of natural vegetation in urban landscapes are frequently hunted by urban cats, which is a serious issue as urbanization and habitat loss continues. Cats in rural areas maintained for the purpose of pest control are heavily subsidized by humans and usually present in high densities; therefore, the potential for wildlife damage by these cats is great as well. Removal of nonnative species (pests) such as the black rat, Norway rat, and house mouse is undoubtedly beneficial, as these animals are disease reservoirs that destroy crops and

Domestic cats and sustainable ecosystems

buildings. Additionally, nonnative small mammals and birds are quite flexible regarding the habitats in which they reside and create competition for native wildlife in terms of resources. On the other hand, cats remove the prey base for native predators, thereby negatively impacting them as well. Regardless of where cats are present, whether on islands or continents, in urban, suburban, or rural habitats, they have the potential to decrease biodiversity through hunting. Biodiversity Loss due to Hunting by Domestic Cats Based on the definition of ecological sustainability, one can easily argue that this predator–prey relationship is not sustainable. With domestic cats killing billions of mammals and birds and millions of reptiles and amphibians each year, ecosystems will only suffer a critical loss of biodiversity. Within an ecosystem, species vary in abundance, distribution, ecological function, and feeding habits (Savard et al., 2000). As native species provide services to the ecosystem, their disappearance can have catastrophic effects on the overall function of the system (Blake, 1986; Adams and Dove, 1989; Hawkins et al., 1999). As numbers within a population decline, species extinction may soon follow. Birds probably exhibit the most diverse range of ecological functions among vertebrates (Sekercioglu, 2006). Various species of birds scavenge, create soil, disperse seed, pollinate, deposit nutrients, and help to control insect populations (Sekercioglu, 2006). Insects consist of the most diverse group of multicellular organisms on Earth and they also contribute to essential ecological services such as pollination, decomposition, and pest control (Losey and Vaughan, 2006). New Zealand is an important case study for the potential impact of domestic cats on native invertebrate fauna because these animals have largely evolved in the absence of mammalian predators. Most native invertebrates in New Zealand are large bodied, long lived, flightless, ground dwelling, and nocturnal (Gibbs, 2010). Weta (Orthoptera) are important examples of invertebrates that may be affected by introduced mammals, such as domestic cats. Research has shown an increase in the weta population following mammal eradication on the New Zealand island of Maungatautari, which provides encouragement for the possibility of species recovery in areas where introduced mammals prey on invertebrate species (Watts et al., 2011). Small mammals such as rodents are important prey for specialist predators such as weasels and owls, whereas generalist predators such as foxes and badgers will prey on rodents when they are easily available (Watson, 1957; Erlinge, 1974; Englund, 1965). To halt a loss in biodi-

855

versity due to hunting by cats, plans need to be implemented to moderate the hunting of feral, free-ranging, and indoor–outdoor cats to preserve the ecosystem. Management Strategies to Reduce Hunting by Domestic Cats Cats have evolved with humans and, in the process, provided companionship and services such as pest control. Because of this relationship, humans have an obligation to care for cats and manage their outdoor presence in a responsible manner. Out of concern for native species, we should strive to minimize the impact of hunting by cats on wildlife. However, we also must recognize that all cats are predators and have an innate instinct to hunt. Hunting is simply part of a natural behavior and we can neither fault them for it nor change it. This natural behavior has been demonstrated in a study showing that cats supplemented with food would leave their food dish to kill a rat placed in an area with them and then return to their food dish and resume eating (Adamec, 1976). This research clearly demonstrates that for most cats, hunting is a result of instinct and behavior but not hunger. Furthermore, other research has indicated that feeding cats does not decrease their hunting (Hutchings, 2003; Tennent and Downs, 2008). For cats that are indoor–outdoor pets and possibly some free-ranging cats, there are devices available that have been shown to decrease successful hunting encounters with wildlife. In the United Kingdom, cats equipped with an electronic sonic device on a collar returned 38% fewer mammals and 51% fewer birds compared with cats wearing a plain collar (Nelson et al., 2005). A similar device called a Liberator cat collar (PetVision, Auckland, New Zealand) produces an audio and visual alarm, activated when the cat pounces toward prey. This collar was tested in Western Australia and found to decrease the number of prey caught by pet cats (Calver and Thomas, 2011). Other research using bells mounted on collars found variable results with regard to reduction of predation rates by domestic cats. Bell collars work by warning intended prey of a nearby cat, thus allowing it time to escape. Observational studies in Australia have found no effect of bell collars on predation rates, but another study in the United Kingdom found a reduction in predation of 50% of both mammals and birds for cats wearing bell collars (Paton, 1991; Barratt, 1998; Ruxton et al., 2002). Additionally, research in New Zealand also found predation of birds and rodents to be reduced by 50 and 61%, respectively, for cats wearing bell collars (Gordon et al., 2010). Other options include cat pounce protectors (CatBibs; Cat Goods, Inc., Springfield, OR;

856

Kitts-Morgan

https://catgoods.com). These devices attach to collars and are inexpensive, and research has shown them to reduce mean captures of birds and mammals by hunting cats (Calver et al., 2007). Whereas electronic sonic devices, bells, and pounce protectors may reduce hunting by cats, the public must be educated regarding the implications of cat hunting and be encouraged to either keep cats indoors or use these devices. SUMMARY AND CONCLUSIONS Through critical examination of available research, domestic cats residing primarily outdoors obviously have deleterious effects on native wildlife. As urbanization continues in all areas of the world and native species are forced to inhabit fragmented and fringe habitats, they face increasing pressure by feral, free-ranging, and indoor–outdoor cats that are simply following an innate instinct to hunt. Some geographical locations may face more pressure than others, as cats on islands have caused multiple extinctions of native birds and some mammals and reptiles. However, the fact that domestic cats provide an important service in removing nonnative rodents from agricultural, suburban, and urban areas must not be overlooked. In a world already facing numerous extinctions of species due to habitat loss, climate change, and anthropogenic mortality, further losses of biodiversity cannot be endured. Simply stated, the current predator–prey relationship of domestic cats and native wildlife may not be sustainable in certain habitats. Humans must intervene and manage these cat populations to reduce cat hunting to alleviate the effects of domestic cats on wildlife. Whereas a tremendous amount of knowledge and insight concerning the hunting behavior of domestic cats has been gained in recent years, there remain areas where information is lacking and more research needs to be conducted. For example, more needs to be learned regarding predation rates, the primary prey of cats in multiple geographic regions (particularly mainland prey), effect of food subsidies on hunting, whether impact on prey populations is compensatory or additive, and the effect of cat removal from sensitive habitats and the subsequent recovery of native species. Domestic cats are both companion animals and predators; the sheer number of cats present throughout the world implies that wildlife mortality will only continue to increase unless measures are implemented to decrease cat hunting. We need to better understand the impacts of cats on wildlife populations and effectiveness of methods to alleviate those impacts.

LITERATURE CITED Adamec, R. E. 1976. The interaction of hunger and preying in the domestic cat (Felis catus): An adaptive hierarchy? Behav. Biol. 18:263–272. doi:10.1016/S0091-6773(76)92166-0 Adams, W. L., and L. E. Dove. 1989. Wildlife reserves and corridors in the urban environment. National Institute for Urban Wildlife, Columbia, MD. American Pet Products Manufacturers Association (APPMA). 1997. APPMA national pet owners survey. APPMA, Inc., Greenwich, CT. American Pet Products Manufacturers Association (APPMA). 2013. APPMA national pet owners survey. APPMA, Inc., Greenwich, CT. Arnaud, G., A. Rodriguez, A. Ortega-Rubio, and S. AlvarezCardenas. 1993. Predation by cats on the unique endemic lizard of Socorro Island (Urosaurus auriculatus), Revillagigedo, Mexico. Ohio J. Sci. 93:101–104. Baker, P. J., A. J. Bentley, R. J. Ansell, and S. Harris. 2005. Impact of predation by domestic cats Felis catus in an urban area. Mammal Rev. 35:302–312. doi:10.1111/j.13652907.2005.00071.x Baker, P. J., S. Molony, E. Stone, I. C. Cuthill, and S. Harris. 2008. Cats about town: Is predation by free-ranging pet cats (Felis catus) likely to affect urban bird populations? Ibis 150(Suppl. 1):86–99. doi:10.1111/j.1474-919X.2008.00836.x Baker, P. J., C. D. Soulsbury, G. Iossa, and S. Harris. 2010. Domestic cat (Felis catus) and domestic dog (Canis familiaris). In: S. D. Gehrt, S. P. D. Riley, and B. L. Cypher, editors, Urban carnivores. John Hopkins Univ. Press, Baltimore, MD. p. 157–172. Balogh, A. L., T. B. Ryder, and P. P. Marra. 2011. Population demography of Gray Catbirds in the suburban matrix: Sources, sinks, and domestic cats. J. Ornithol. 152:717–726. doi:10.1007/ s10336-011-0648-7 Bamford, M. J., and M. C. Calver. 2012. Cat predation and suburban lizards: A 22 year study at a suburban Australian property. Open Conserv. Biol. J. 6:25–29. doi:10.2174/1874839201206010025 Banko, P. C. 1992. Constraints on productivity of wild nene or Hawaiian geese Branta sandvicensis. Wildfowl 43:99–106. Banks, R. C. 1979. Human related mortality of birds in the United States. Special Scientific Report – Wildlife no. 215. U.S. Fish and Wildlife Service, Department of the Interior, Washington, DC. Barratt, D. G. 1998. Predation by house cats. Felis catus (L.) in Canberra, Australia. II. Factors affecting the amount of prey caught and estimates of the impact on wildlife. Wildl. Res. 25:475–487. doi:10.1071/WR97026 Bateman, P. W., and P. A. Fleming. 2011. Frequency of tail loss reflects variation in predation levels, predator efficiency, and the behaviour of three populations of brown anoles. Biol. J. Linn. Soc. Lond. 103:648–656. doi:10.1111/j.10958312.2011.01646.x Blair, R. B. 1996. Land use and avian species diversity along an urban gradient. Ecol. Appl. 6:506–519. doi:10.2307/2269387 Blake, J. G. 1986. Species-area relationship of migrants in isolated woodlots in east central Illinois. Wilson Bull. 98:291–296. Blancher, P. 2013. Estimated number of birds killed by house cats (Felis catus) in Canada. Avian Conserv. Ecol. 8:3. doi:10.5751/ ACE-00557-080203 Bonnaud, E., F. M. Medina, E. Vidal, M. Nogales, B. Tershy, E. Zavaleta, C. J. Donlan, B. Keitt, M. Le Corre, and S. V. Horwath. 2011. The diet of feral cats on islands: A review and a call for more studies. Biol. Invasions 13:581–603. doi:10.1007/ s10530-010-9851-3

Domestic cats and sustainable ecosystems Brickner, I. 2003. The impact of domestic cat (Felis catus) on wildlife welfare and conservation: A literature review. With a situation summary from Israel. Tel Aviv University report. http:// www.tau.ac.il/lifesci/zoology/members/yom-tov/inbal/cats. pdf. (Accessed 15 September 2014.) Butchart, S. H. M., A. J. Sattersfield, and N. J. Collar. 2006. How many bird extinctions have we prevented? Oryx 40:266–278. doi:10.1017/S0030605306000950 Calver, M., S. Thomas, S. Bradley, and H. McCutcheon. 2007. Reducing the rate of predation on wildlife by pet cats: The efficacy and practicability of collar-mounted pounce protectors. Biol. Conserv. 137:341–348. doi:10.1016/j.biocon.2007.02.015 Calver, M. C., and S. R. Thomas. 2011. Effectiveness of the Liberator in reducing predation on wildlife by domestic cats. Pac. Conserv. Biol. 16:244–250. Chace, J. F., and J. J. Walsh. 2006. Urban effects on native avifauna: A review. Landsc. Urban Plan. 74:46–69. doi:10.1016/j.landurbplan.2004.08.007 Churcher, P. B., and J. H. Lawton. 1987. Predation by domestic cats in an English village. J. Zool. (Lond.) 212:439–455. doi:10.1111/j.1469-7998.1987.tb02915.x Clavero, M., and E. Garcia-Berthou. 2005. Invasive species are a leading cause of animal extinctions. Trends Ecol. Evol. 20:110. doi:10.1016/j.tree.2005.01.003 Coleman, J. S., and S. A. Temple. 1993. Rural residents’ free-ranging domestic cats: A review. Wildl. Soc. Bull. 21:381–390. Coleman, J. S., and S. A. Temple. 1996. On the prowl. Wisconsin Nat. Res. Mag. December issue. http://dnr.wi.gov/wnrmag/html/ stories/1996/dec96/cats.htm. (Accessed 25 September 2014.) Dauphine, N., and R. J. Cooper. 2009. Impacts of free-ranging domestic cats (Felis catus) on birds in the United States: A review of recent research with conservation and management recommendations. In: Proceedings of the Fourth International Partners in Flight Conference: Tundra to Tropics, Feb. 13–16, 2008, McAllen, TX. Partners in Flight – U.S. p. 205–219. Dombrosky, J. M., and S. Wolverton. 2014. TNR and conservation on a university campus: A political ecological perspective. PeerJ 2:e312 doi:10.7717/peerj.312 Englund, J. 1965. Studies on food ecology of the red fox (Vulpes vulpes) in Sweden. Viltrevy (Stockh.) 3:375–471. Erickson, W. P., G. D. Johnson, and D. P. Young Jr. 2005. A summary and comparison of bird mortality from anthropogenic causes with an emphasis on collisions. Tech. Rep. PSW-GTR-191. USDA, Forest Service. p. 1029–1042. Erlinge, S. 1974. Distribution, territoriality and numbers of the weasel Mustela nivalis in relation to prey abundance. Oikos 25:308–314. doi:10.2307/3543948 Errington, P. L. 1936. Notes on food habits of southern Wisconsin house cats. J. Mammal. 17:64–65. doi:10.2307/1374407 The European Pet Food Industry (FEDIAF). 2012. FEDIAF facts and figures 2012. FEDIAF, Brussels, Belgium. Fitzgerald, B. M. 1988. Diet of domestic cats and their impact on prey populations. In: The domestic cat: The biology of its behavior. D. C. Turner and P. Bateson, editors, 1st ed. Cambridge Univ. Press, Cambridge, UK. p. 123–147. Fitzgerald, B. M. 1990. Is cat control needed to protect urban wildlife? Environ. Conserv. 17:168–169. doi:10.1017/ S0376892900031970 Fitzgerald, B. M., and B. J. Karl. 1979. Foods of feral house cats (Felis catus L.) in forest of the Orongorongo Valley, Wellington. N. Z. J. Zool. 6:107–126.

857

Fitzgerald, B. M., and D. C. Turner. 2000. Hunting behavior of domestic cats and their impact on prey populations. In: D. C. Turner and P. Bateson, editors, The domestic cat: The biology of its behavior. 2nd ed. Cambridge Univ. Press, Cambridge, UK. p. 151–175. Gibbs, G.W. 2010. Do New Zealand invertebrates reflect the dominance of birds in their evolutionary history? New Zeal. J. Ecol. 34:152–157. Gill, F. B. 1994. Ornithology, 2nd ed. W.H. Freeman Publishers, Philadelphia, PA. Gillies, C., and M. Clout. 2003. The prey of domestic cats (Felis catus) in two suburbs of Auckland City, New Zealand. J. Zool. (Lond.) 259:309–315. doi:10.1017/S095283690200328X Gordon, J. K., C. Mattahei, and Y. Van Heezik. 2010. Belled collars reduce catch of domestic cats in New Zealand by half. Wildl. Res. 37:372–378. doi:10.1071/WR09127 Hawkins, C. C. 1998. Impact of a subsidized exotic predator on native biota: Effect of house cats (Felis catus) on California birds and rodents. PhD Thesis. Texas A&M Univ., College Station, TX. Hawkins, C. C., W. E. Grant, and M. T. Longnecker. 1999. Effects of subsidized house cats on California birds and rodents. Trans. West. Sect. Wildl. Soc. 35:29–33. Hawkins, C. C., W. E. Grant, and M. T. Longnecker. 2004. Effect of house cats, being fed in parks, on California birds and rodents. In: W. W. Shaw, L. K. Harris, and L. Vandruff, editors, Proceedings of the 4th International Urban Wildlife Symposium, University of Arizona, Tucson, AZ. p. 164–170. Hess, S. C., P. C. Banko, D. M. Goltz, R. M. Danner, and K. W. Brinck. 2004. Strategies for reducing feral cat threats to endangered Hawaiian birds. In: Proceedings of the 21st Vertebrate Pest Conference. p. 21–26. Hess, S. C., H. Hansen, and P. C. Banko. 2007. Ecology of an invasive predator in Hawai’i. In: G. W. Witmer, W. C. Pitt, and K. A. Fagerstone, editors, Managing vertebrate invasive species: Proceedings of an international symposium. USDA/ Animal and Plant Health Inspection Service/Wildlife Services, National Wildlife Research Center, Fort Collins, CO. p. 460– 468. Hodges, C. S. N., and R. J. Nagata, Sr. 2001. Effects of predator control on the survival and breeding success of the endangered Hawaiian Dark-rumped Petrel. Stud. Avian Biol. 22:308-318. Howes, C. A. 2002. Red in tooth and claw: 2. Studies on the natural history of the domestic cat Felis catus Lin. in Yorkshire. Naturalist 127:101–130. Hubbs, E. L. 1951. Food habits of feral house cats in the Sacramento Valley. Calif. Fish Game 37:177–189. Hutchings, S. 2003. The diet of feral house cats (Felis catus) at a regional rubbish tip, Victoria. Wildl. Res. 30:103–110. doi:10.1071/WR99067 Iverson, J. B. 1978. The impact of feral cats and dogs on populations of the West Indian rock iguana, Cyclura carinata. Biol. Conserv. 14:63–73. doi:10.1016/0006-3207(78)90006-X Jackson, W. B. 1951. Food habits of Baltimore, Maryland, cats in relation to rat populations. J. Mammal. 32:458–461. doi:10.2307/1375794 Jessup, D. A. 2004. The welfare of feral cats and wildlife. J. Am. Vet. Med. Assoc. 225:1377–1383. doi:10.2460/javma.2004.225.1377 Jones, E., and B. J. Coman. 1981. Ecology of the feral cat Felis catus (L.) in South Eastern Australia. I. Diet. Aust. Wildl. Res. 8:537–547. doi:10.1071/WR9810537 Kays, R. W., and A. A. DeWan. 2004. Ecological impact of inside/ outside house cats around a suburban nature preserve. Anim. Conserv. 7:273–283. doi:10.1017/S1367943004001489

858

Kitts-Morgan

Kirkpatrick, R. D., and M. J. Rauzon. 1986. Foods of feral cats Felis catus on Jarvis and Howland islands, central Pacific Ocean. Biotropica 18:72–75. doi:10.2307/2388365 Klem, D., Jr. 2009. Avian mortality at windows: The second largest human source of bird mortality on earth. In: Proceedings of the Fourth International Partners in Flight Conference: Tundra to Tropics, Feb. 13–16, 2008, McAllen, TX. Partners in Flight – U.S. p. 244–251. Klemann, N., and H. J. Pelz. 2006. The feeding pattern of the Norway rat (Rattus norvegicus) in two differently structured habitats on a farm. Appl. Anim. Behav. Sci. 97:293–302. doi:10.1016/j.applanim.2005.08.004 Konecny, M. J. 1987. Home range and activity patterns of feral house cats in the Galapagos Islands. Oikos 50:17–23. doi:10.2307/3565397 Langton, S. D., D. P. Cowan, and A. N. Meyer. 2001. The occurrence of commensal rodents in dwellings as revealed by the 1996 English House Condition Survey. J. Appl. Ecol. 38:699– 709. doi:10.1046/j.1365-2664.2001.00631.x Lepczyk, C. A. 2008. An overview of the natural history, human dimension, and management of outdoor cats. In: 126th Stated Meeting of the American Ornithologists’ Union, Portland OR. (Abstr.) Lepczyk, C. A., A. G. Mertig, and J. Liu. 2004. Landowners and cat predation across rural-to-urban landscapes. Biol. Conserv. 115:191–201. doi:10.1016/S0006-3207(03)00107-1 Lever, C. 1994. Naturalized animals: The ecology of successfully introduced species. T & AD Poyse Ltd., London, United Kingdom. Levy, J. K., and P. C. Crawford. 2004. Humane strategies for controlling feral cat populations. J. Am. Vet. Med. Assoc. 225:1354–1360. doi:10.2460/javma.2004.225.1354 Liberg, O. 1984. Food habits and prey impact by feral and housebased cats in a rural area in Southern Sweden. J. Mammal. 65:424–432. doi:10.2307/1381089 Llewellyn, L. L., and F. M. Uhler. 1952. The foods of fur animals of the Patuxent Research Refuge, Maryland. Am. Midl. Nat. 48:193–203. doi:10.2307/2422142 Lohr, C. A., L. J. Cox, and C. A. Lepczyk. 2013. Costs and benefits of trap-neuter-release and euthanasia for removal of urban cats in Oahu, Hawaii. Conserv. Biol. 27:64–73. doi:10.1111/j.15231739.2012.01935.x Longcore, T., C. Rich, P. Mineau, B. MacDonald, D. G. Bert, L. M. Sullivan, E. Mutrie, S. A. Gauthreaux Jr., M. L. Avery, R. L. Crawford, A. M. Manville II, E. R. Travis, and D. Drake. 2012. An estimate of mortality at communication towers in the United States and Canada. PLoS ONE 7:e34025 doi:10.1371/ journal.pone.0034025 Losey, J. E., and M. Vaughan. 2006. The economic value of ecological services provided by insects. Bioscience 56:311–323. doi:10.1641/0006-3568(2006)56[311:TEVOES]2.0.CO;2 Loss, S. R., T. Will, and P. P. Marra. 2013. The impact of freeranging domestic cats on wildlife of the United States. Nat. Commun. 4:1396. doi:10.1038/ncomms2380 Lowe, S., M. Browne, S. Boudjelas, and M. De Poorter. 2000. 100 of the World’s worst invasive alien species: A selection from the global invasive species database. Invasive Species Specialist Group, International Union for Conservation of Nature, Auckland, New Zealand. Loyd, K. A. T., S. M. Hernandez, J. P. Carroll, K. J. Abernathy, and G. J. Marshall. 2013. Quantifying free-roaming domestic cat predation using animal-borne video cameras. Biol. Conserv. 160:183–189. doi:10.1016/j.biocon.2013.01.008

Manville, A., II. 2009. Towers, turbines, power lines, and buildings – Steps being taken by the U.S. Fish and Wildlife Service to avoid or minimize take of migratory birds at these structures. In: Proceedings of the Fourth International Partners in Flight Conference: Tundra to Tropics, Feb. 13–16, 2008, McAllen, TX. Partners in Flight – U.S. p. 262–272. Medina, F. M., E. Bonnaud, E. Vidal, B. R. Tershy, E. S. Zavaleta, C. J. Donlan, B. S. Keitt, M. Le Corre, S. V. Horwath, and M. Nogales. 2011. A global review of the impacts of invasive cats on island endangered vertebrates. Glob. Change Biol. 17:3503–3510. doi:10.1111/j.1365-2486.2011.02464.x Medina, F. M., and R. Garcia. 2007. Predation of insects by feral cats (Felis sylvestris catus L., 1758) on an oceanic island (La Palma, Canary Island). J. Insect Conserv. 11:203–207. doi:10.1007/s10841-006-9036-7 Mellink, E. 1992. The status of Neotoma anthonyi (Rodentia, Muridae, Cricetinae) of Todos Santos Islands, Baja California, Mexico. Bull. South. Calif. Acad. Sci. 91:137–140. Mills, G. S., J. B. Dunning Jr., and J. M. Bate. 1989. Effects of urbanization on breeding bird community structure in southwestern desert habitats. Condor 91:416–428. doi:10.2307/1368320 Mitchell, J. C., and R. A. Beck. 1992. Free-ranging domestic cat predation on native vertebrates in rural and urban Virginia. Va. J. Sci. 43:197–207. Mitchell, N., R. Haeffner, V. Veer, M. Fulford-Gardner, W. Clerveaux, C. R. Veitch, and G. Mitchell. 2002. Cat eradication and the restoration of endangered iguanas (Cyclura carinata) on Long Cay, Caicos Bank, Turks and Caicos Islands, British West Indies. In: C. R. Veitch and M. N. Clout, editors, Turning the tide: The eradication of invasive species. World Conservation Union, Gland, Switzerland. Molsher, R., A. Newsome, and C. Dickman. 1999. Feeding ecology and population dynamics of the feral cat (Felis catus) in relation to the availability of prey in central-eastern New South Wales. Wildl. Res. 26:593–607. doi:10.1071/WR98058 Moseby, K. E., J. L. Read, D. C. Paton, P. Copley, B. M. Hill, and H. A. Crisp. 2011. Predation determines the outcome of reintroduction attempts in arid South Australia. Biol. Conserv. 144:2863–2872. doi:10.1016/j.biocon.2011.08.003 Nelson, S. H., A. D. Evans, and R. B. Bradbury. 2005. The efficacy of collar-mounted devices in reducing the rate of predation of wildlife by domestic cats. Appl. Anim. Behav. Sci. 94:273–285. doi:10.1016/j.applanim.2005.04.003 Nilsson, N. N. 1940. The role of the domestic cat in relation to game birds in the Willamette Valley, Oregon. MS Thesis, Oregon State College, Corvallis, OR. Nogales, M., A. Martin, B. R. Tershy, C. J. Donlan, D. Veitch, N. Puerta, B. Wood, and J. Alsonso. 2004. A review of feral cat eradication on islands. Conserv. Biol. 18:310–319. doi:10.1111/j.1523-1739.2004.00442.x Nogales, M., and F. M. Medina. 2009. Trophic ecology of feral cats (Felis silvestris f. catus) in the main environments of an oceanic archipelago (Canary Islands): An update approach. Mamm. Biol. 74:169–181. O’Brien, S. J., and W. E. Johnson. 2007. The evolution of cats. Sci. Am. 297:68–75. doi:10.1038/scientificamerican0707-68 Parmalee, P. W. 1953. Food habits of the feral house cat in east-central Texas. J. Wildl. Manage. 17:375–376. doi:10.2307/3797127 Paton, D. C. 1991. Loss of wildlife to domestic cats. In: C. Potter, editor, Proceedings of a workshop on the impact of cats on native wildlife. Australian National Parks and Wildlife Service, Canberra, Australia. p. 64–69. Paulay, G. 1994. Biodiversity on Oceanic islands: Its origin and extinction. Am. Zool. 34:134–144.

Domestic cats and sustainable ecosystems Pet Food Manufacturers Association (PFMA). 2013. Pet population report. PFMA, London, UK. Pimentel, D., A. Greiner, and T. Bashore. 1991. Economic and environmental costs of pesticide use. Arch. Environ. Contam. Toxicol. 21:84–90. doi:10.1007/BF01055561 Pocock, M. J. O., J. B. Searle, and P. C. L. White. 2004. Adaptations of animals to commensal habitats: Population dynamics of house mice Mus musculus domesticus on farms. J. Anim. Ecol. 73:878–888. doi:10.1111/j.0021-8790.2004.00863.x Ruxton, G. D., S. Thomas, and J. W. Wright. 2002. Bells reduce predation of wildlife by domestic cats (Felis catus). J. Zool. (Lond.) 256:81–83. doi:10.1017/S0952836902000109 Savard, J. L., P. Clergeau, and G. Mennechez. 2000. Biodiversity concepts and urban ecosystems. Landsc. Urban Plan. 48:131– 142. doi:10.1016/S0169-2046(00)00037-2 Sekercioglu, C. H. 2006. Increasing awareness of avian ecological function. Trends Ecol. Evol. 21:464–471. doi:10.1016/j. tree.2006.05.007 Sewell, S. R., and C. P. Catterall. 1998. Bushland modification and styles of urban development: Their effects on birds in southeast Queensland. Wildl. Res. 25:41–63. doi:10.1071/WR96078 Sims, V., K. L. Evans, S. E. Newson, J. A. Tratalos, and K. J. Gaston. 2008. Avian assemblage structure and domestic cat densities in urban environments. Diversity Distrib. 14:387–399. doi:10.1111/j.1472-4642.2007.00444.x Siriwardena, G. M., R. A. Robinson, and H. Q. P. Crick. 2002. Status and population trends of the house sparrow Passer domesticus in Great Britain. In: H. Q. P. Crick, R. A. Robinson, G. F. Appleton, N. A. Clark, and A. D. Rickard, editors, Investigation into the causes of the decline of starlings and house sparrows in Great Britain. British Trust for Ornithology, Thetford, UK. p. 33–52. Slater, M. R. 2001. The role of veterinary epidemiology in the study of free-roaming dogs and cats. Prev. Vet. Med. 48:273–286. doi:10.1016/S0167-5877(00)00201-4 Smith, D. G., J. T. Polhemus, and E. A. Vanderwerf. 2002. Comparison of managed and unmanaged wedge-tailed shearwater colonies on O’ahu: Effects of predation. Pac. Sci. 56:451–457. doi:10.1353/psc.2002.0044 Stroud, D. C. 1982. Population dynamics of Rattus rattus and R. norvegicus in a riparian habitat. J. Mammal. 63:151–154. doi:10.2307/1380682 Tennent, J., and C. T. Downs. 2008. Abundance and home ranges of feral cats in an urban conservancy where there is supplemental feeding: A case study from South Africa. Afr. Zool. 43:218– 229. doi:10.3377/1562-7020-43.2.218

859

Tershey, B. R., C. J. Donlan, B. S. Keitt, D. A. Croll, J. A. Sanchez, B. Wood, M. A. Hermosillo, G. R. Howald, and N. Biavaschi. 2002. Island conservation in north-west Mexico: A conservation model integrating research, education and exotic mammal eradication. In: C. R. Veitch and M. N. Clout, editors, Turning the tide: The eradication of invasive species. World Conservation Union, Gland, Switzerland. Tomich, P. Q. 1986. Mammals in Hawaii. Bishop Museum Press, Honolulu, HI. Turner, D. C., and O. Meister. 1988. Hunting behavior of the domestic cat. In: D. C. Turner and P. Bateson, editors, The domestic cat: The biology of its behavior. Cambridge Univ. Press, Cambridge, UK. van Heezik, Y., A. Smyth, A. Adams, and J. Gordon. 2010. Do domestic cats impose an unsustainable harvest on urban bird populations? Biol. Conserv. 143:121–130. doi:10.1016/j.biocon.2009.09.013 van Heezik, Y., A. Smyth, and R. Mathieu. 2008. Diversity of native and exotic birds across an urban gradient in a New Zealand city. Landsc. Urban Plan. 87:223–232. doi:10.1016/j.landurbplan.2008.06.004 Warner, R. E. 1985. Demography and movements of free-ranging domestic cats in rural Illinois. J. Wildl. Manage. 49:340–346. doi:10.2307/3801527 Watson, A. 1957. The behaviour, breeding, and food-ecology of the Snowy Owl Nyctea scandiaca. Ibis 99:419–462. doi:10.1111/ j.1474-919X.1957.tb01959.x Watts, C. H., D. P. Armstrong, J. Innes, and D. Thornburrow. 2011. Dramatic increases in weta (Orthoptera) following mammal eradication of Maungatautari – Evidence from pitfalls and tracking tunnels. N. Z. J. Ecol. 35:261–272. Weber, J. M., and L. Dailly. 1998. Food habits and ranging behavior of a group of farm cats (Felis catus) in a Swiss mountainous area. J. Zool. (Lond.) 245:234–237. doi:10.1111/j.1469-7998.1998. tb00096.x Whitaker, J. O., and W. J. Hamilton Jr. 1998. Mammals of the Eastern United States. 3rd ed. Cornell Univ. Press, Ithaca, NY. Wilcove, D. S. 1985. Nest predation in forest tracts and the decline of migratory songbirds. Ecology 66:1211–1214. doi:10.2307/1939174 Woods, M., R. A. McDonald, and S. Harris. 2003. Predation of wildlife by domestic cats Felis catus in Great Britain. Mammal Rev. 33:174–188. doi:10.1046/j.1365-2907.2003.00017.x