Biology and Impacts of Pacific Island Invasive Species. 11. Rattus Rattus, the Black Rat (Rodentia: Muridae)

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USDA National Wildlife Research Center - Staff U.S. Department of Agriculture: Animal and Publications Plant Health Inspection Service

2014

Biology and Impacts of Pacific Island Invasive Species. 11. Rattus rattus, the Black Rat (Rodentia: Muridae)

Aaron B. Shiels USDA, [email protected]

William C. Pitt

Robert T. Sugihara

Gary W. Witmer USDA-APHIS-Wildlife Services, [email protected]

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Shiels, Aaron B.; Pitt, William C.; Sugihara, Robert T.; and Witmer, Gary W., "Biology and Impacts of Pacific Island Invasive Species. 11. Rattus rattus, the Black Rat (Rodentia: Muridae)" (2014). USDA National Wildlife Research Center - Staff Publications. 1404. https://digitalcommons.unl.edu/icwdm_usdanwrc/1404

This Article is brought to you for free and open access by the U.S. Department of Agriculture: Animal and Plant Health Inspection Service at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in USDA National Wildlife Research Center - Staff Publications by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Biology and Impacts of Pacific Island Invasive Species. 11.Rattus rattus, the Black Rat (Rodentia: Muridae)1

Aaron B. Shiels,2,4 William C. Pitt,2 Robert T. Sugihara,2 and Gary W. Witmer3

Abstract: The black rat, roof rat, or ship rat (Rattus rattus L.) is among the most widespread invasive vertebrates on islands and continents, and it is nearly ubiq- uitous on Pacific islands from the equatorial tropics to approximately 55 degrees latitude north and south. It survives well in human-dominated environments, natural areas, and islands where humans are not present. Rattus rattus is typically the most common invasive rodent in insular forests. Few vertebrates are more problematic to island biota and human livelihoods than R. rattus; it is well known to damage crops and stored foods, kill native species, and serve as a vector for human diseases. Rattus rattus is an omnivore, yet fruit and seed generally domi- nate its diet, and prey items from the ground to the canopy are commonly at risk and exploited as a result of the prominent arboreal activity of R. rattus. Here we review the biology of this invasive species and its impacts on humans and the insular plants and animals in the Pacific. We also describe some of the past ­management practices used to control R. rattus populations on islands they have invaded.

Few undomesticated animals are as wide- ments across the planet is intriguing, espe- spread and well known as the black rat, Rattus cially when considering that rodents compose rattus L. (Figure 1). This rat’s behavior results over 40% of the world’s mammal species (Al- in countless negative interactions with hu- derton 1996); thus there must be some char- mans in most parts of the world, including acteristics facilitating the success of R. rattus consuming and spoiling foods, causing fires that further separate this species from the and electrical interruptions by gnawing wir- other 2,000 or more rodent species on the ing in buildings, nesting in and around human planet. Perhaps the most important charac- dwellings, and carrying diseases such as the teristic for success is that R. rattus is highly bubonic plague that has killed millions of commensal. The ability of black rats to live people ( Wilson 1968, Twigg 1978, Alderton closely and successfully with humans has fa- 1996). Human impacts and associated costs in cilitated their transport to, and establishment attempts to control or eradicate this species on, most islands in the Pacific, as well as into have continued for centuries. The success of most of the world’s biomes (Alderton 1996). R. rattus in such a range of different environ- In addition to affecting human health and economies, R. rattus is well known for its neg- ative effects on a large suite of native biota 1 Manuscript accepted 17 July 2013. and ecosystems. Rattus rattus has been identi- 2 U.S. Department of Agriculture ( USDA), Animal fied as the most damaging invasive rodent to and Plant Health Inspection Service (APHIS), National island ecosystems (Ruffino et al. 2009, Trave- Wildlife Research Center, Hawai‘i Field Station, P.O. set et al. 2009, Banks and Hughes 2012); and Box 10880, Hilo, Hawai‘i 96721. 3 USDA, APHIS, National Wildlife Research Center, globally, R. rattus is associated with the 4101 Laporte Avenue, Fort Collins, Colorado 80521. ­greatest number of declines or extinctions of 4 Corresponding author (e-mail: ashiels@hawaii.edu). native island biota (Towns et al. 2006). Be- cause most of the islands in the Pacific lacked native land mammals, native flora and fauna Pacific Science (2014), vol. 68, no. 2:145 – 184 doi:10.2984/68.2.1 are particularly at risk to the negative effects © 2014 by University of Hawai‘i Press of introduced rodents such as R. rattus. Unlike All rights reserved most other introduced mammals on Pacific

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Figure 1. Adult black rats (Rattus rattus) with (A) a black pelt and (B) a brown pelt, shown climbing a tree in native forest, O‘ahu, Hawai‘i. Note the shiny metal ear tags in both photos. (Photographs by A. B. Shiels.) islands (e.g., ungulates, dogs, cats, ­mongooses, and based on molecular evidence there are al- or stoats), R. rattus was unintentionally intro- most certainly multiple species within what duced to islands. has historically been identified asRattus rattus (e.g., five to seven species in the R. rattus name ­complex described by Robins et al. [2007] and Pagès et al. [2010], respectively). In the Mari- Rattus rattus Linnaeus, 1758 (Rodentia: Muri- dae), is commonly called the black rat, roof ana Islands, Wiewel et al. (2009) reported that rat, or ship rat. Past synonyms have included all species in their sampling that had been previously believed to be or Mus rattus Linnaeus, 1758; Mus alexandrines R. rattus R. tane- were most closely related to the Geoffroy, 1803; Musculus frugivorus Rafin- zumi R. diar- group described by Robins et al. (2007). esque, 1814; Mus novaezelandiae Buller, 1870; dii Without molecular analysis of individuals plus numerous others (Innes 2005a). In evolu- within the complex, it is very difficult tionary terms, the genus Rattus originated R. rattus about 2 – 3 million years ago (Aplin et al. to separate the species, and R. rattus and R. 2003). tanezumi are almost impossible to distinguish morphologically (Aplin et al. 2003). In addi- Rattus rattus has been separated into two subgroups based on chromosome numbers tion, three interbreeding color morphs of R. ( Yoshida et al. 1974). The Oceania group of rattus have been described in the Pacific (Tomich 1986, Innes 2005 ): R. rattus generally has 2n = 38 chromosomes a R. r. rattus (Musser and Carleton 2005), and it was this (black individuals), R. r. frugivorous (white- species that was thought to have originated in bellied), and R. r. alexandrinus (gray-bellied). the Indian Peninsula and reached Britain by For simplicity, we have not distinguished among species or color morphs within the the 3rd century A.D. (Innes 2005a). The sec- R. complex and therefore consider all of ond group of R. rattus is an Asian form that rattus those species within the complex as the black has 2n = 42 chromosomes and is indigenous to Southeast Asia; today it is also found in Ja- rat, R. rattus. pan, Taiwan, the Philippines, New Guinea, Fiji, and other islands (Robins et al. 2007). description and account of variation This Asian group is potentially multiple spe- Species Description cies and called R. tanezumi (syn. R. diardii ) by Musser and Carleton (2005). Phylogenetic re- The black rat, R. rattus, is an arboreal, ground- structuring of the “R. rattus complex” (Oce- active, and fossorial rodent that is not always anic and Asian groups) continues to progress, black in pelage (Figure 1). A recent review of Pacific Island Invasive Species:Rattus rattus, the Black Rat · Shiels et al. 147

Figure 2. Frequency of average adult body mass of Rattus rattus on Pacific island sites n( = 85 sites, representing 59 islands; latitudinal range of islands was 0 – 55 degrees).

R. rattus body sizes from islands extending sexes (Innes 2005a) or slightly greater in across the Pacific basin reveals that mean males than in females (Shiels 2010). (±SE) adult body mass is 153 ± 3 g (range, Black rats, like most nocturnal rodents, 76 – 243 g; n = 85 sites, 59 islands) (Figure 2) have well-developed senses of touch, smell, (A.B.S., J. Russell, and W.C.P., unpubl. data), and hearing. Both their whiskers and guard whereas the mean adult head-body length hairs (on their pelt) are very sensitive to touch, (measured from snout to base of tail) is 175 ± 2 and they are used in orientation and move- mm (range, 134 – 207 mm; n = 71 sites, 53 is- ment in the dark. Their keen sense of smell lands) (A.B.S., J. Russell, and W.C.P., unpubl. allows them to find food and water, detect data). These Pacific-wide R. rattus body size sexually active individuals, and distinguish measurements were similar to those summa- foreign and familiar individuals and locations rized across New Zealand (Innes 2005a). (Mallick 1992, Innes 2005a,b). They have ­Unlike other invasive Rattus species ( Yom- round, dark eyes that are specialized for noc- Tov et al. 1999, Atkinson and Towns 2005), turnal vision; their eyes are very sensitive to there does not appear to be a Pacific-wide light, but their vision is not acute (Innes pattern of greater body size with increasing 2005a). latitude for R. rattus ( Yom-Tov et al. 1999; The fur of black rats is smooth, and the A.B.S., J. Russell, and W.C.P., unpubl. data). guard hairs on their back are longer than any Adult male R. rattus are larger in both mass other hair on their body. As a result of their and body length than adult females (Innes frequent grooming, they incidentally swallow 2005a, Shiels 2010), whereas average tail some of their hair and it may compose an length has been recorded as similar between ­average of 5% by volume of their stomach 148 PACIFIC SCIENCE · April 2014 contents (Shiels et al. 2013). All four feet are (Innes 2005a, Shiels 2010), whereas R. exu- dorsally hairy and ventrally bare, and each lans, R. norvegicus, and M. musculus all have foot has clawed toes that are essential for tails approximately equal to or shorter than climbing: the forefeet have four clawed toes their body length exclusive of the tail (Atkin- and the hind feet have five. Unlike R. exulans son and Towns 2005). The longer tail and (Pacific or Polynesian rat), the dorsal hair on sleek body shape of R. rattus may be adapta- the hind feet is uniformly colored in R. rattus, tions related to their arboreal activity (Figure and the hind feet measure 3 – 7 mm longer on 1), which is more frequent than that of other R. rattus (28 – 30 mm) than on R. exulans introduced Rattus spp. and mice (Shiels 2010, (Atkinson­ and Towns 2005). Female R. rattus Foster et al. 2011, King et al. 2011a). Ear generally have 10 nipples (range, 10 – 12), length of R. rattus (19.0 – 26.0 mm) is gener- consisting of two pectoral pairs and three in- ally the largest among the four main invasive guinal pairs (Atkinson and Towns 2005). rodents introduced to Pacific islands, includ- Like R. exulans and R. norvegicus ( Norway ing R. exulans (15.5 – 20.5 mm), R. norvegicus rat), R. rattus has 16 teeth, which are com- (14.0 – 22.0 mm), and M. musculus (12.0 – 15.0 prised of four incisors (two on the top and two mm). The ears of R. exulans, like those of R. on the bottom) and six molars on each side of rattus, cover the eyes when pulled forward, the mouth (Innes 2005a). All teeth grow con- and the fine ear hairs do not extend beyond tinuously throughout life, and the large inci- the edges of the ears, which is unlike those of sors, which are specialized for gnawing and R. norvegicus and M. musculus (Atkinson and grinding, must be kept to a usable length by Towns 2005). The fur on the back of all four grinding and self-sharpening (Innes 2005a). invasive rodents can be brown (agouti); how- The skull is also specialized for gnawing, and ever, the only species of the four invasive ro- the average length of R. rattus skulls in the dents in the Pacific that includes some indi- ­Pacific region is 40 – 43 mm ( Yom-Tov et al. viduals with black fur on their backs is R. 1999). Because of the size variability across rattus (Tomich 1986, Atkinson and Towns ages, the size of R. rattus droppings (6.8 – 13.8 2005). mm) cannot always be used to distinguish the species from other species of common inva- diet sive rats (Atkinson and Towns 2005). The diet of R. rattus in the Pacific has been well studied using a variety of methods, in- Distinguishing Features cluding examination of stomach contents Body mass is a characteristic that can occa- ( Kami 1966, Yabe 1979, Clark 1981, Sugihara sionally be used to distinguish R. rattus from 1997, Cole et al. 2000, Sweetapple and Nu- other invasive rodents, but it is often unreli- gent 2007, Caut et al. 2008a), field observa- able given that rat body size varies depending tions of chewed food items ( Norman 1970, on location of capture and level of maturity Meyer and Shiels 2009, Pender et al. 2013), (Miller and Miller 1995, Shiels 2010) (Figure field trials measuring food item removal 2). For example, when adult body masses were ( Norman 1970, Abe 2007, Shiels and Drake reviewed in New Zealand, R. rattus ­individuals 2011), captive-feeding trials (Amarasakare were 52 – 295 g (Innes 2005a), which overlaps 1994, Williams et al. 2000, Pérez et al. 2008, with the smaller R. exulans (30 – 187 g) (Atkin- Gregory and Macdonald 2009, Meyer and son and Towns 2005) and the larger R. nor- Shiels 2009, Shiels 2011), and stable isotope vegicus (103 – 422 g) (Innes 2005b). Instead of analysis (Harper 2006, Caut et al. 2008a,b, body size, features that distinguish R. rattus Shiels et al. 2013). As a whole, these dietary from other coexisting rodents (e.g., R. exulans, assessments confirm that R. rattus is highly R. norvegicus, and Mus musculus [house mouse]) omnivorous, eating a wide variety of plants, include tail length and ear length. The tail of invertebrates, vertebrates, and fungi (Figure 3). R. rattus is approximately 27 ± 2 mm (or Based on literature reviewed from Pacific 16% ± 1%) longer than the rest of its body islands, Figure 3 summarizes the relative im- Pacific Island Invasive Species:Rattus rattus, the Black Rat · Shiels et al. 149

Figure 3. Organisms that Rattus rattus are known to consume on Pacific islands. The arrows’ thickness indicates the average diet of R. rattus on Pacific islands, measured by the relative proportion of the food item in stomach contents and in some cases other indicators of diet (see text); dashed lines indicate items that have been recorded but are least common in diets. In general, thickened solid arrows = common consumption of food item; thinnest solid arrows = generally infrequent by volume but commonly consumed on some islands (i.e., snail, forest bird, seabird); dashed ­arrows = uncommon consumption of food item (i.e., infrequent in most studies and islands). The vegetative category includes stems and leaves. All categories and relationships are based on reviewed literature (see text and Figure 4). portance of various food items in the diet of R. latitudes sampled (47° S) and one at 38° S rattus. The most frequent food items con- (Figure 4). sumed by R. rattus are plants (fruit, seed, veg- Plant material often composes 75% – 80% etative), insects, and spiders; yet most of the of the diet of R. rattus in the insular Pacific terrestrial food web may be vulnerable to R. ( Kami 1966, Norman 1970, Yabe 1979, Clark rattus consumption. By collating available 1981, Cole et al. 2000, Beard and Pitt 2006, stomach content analyses of R. rattus across Sweetapple and Nugent 2007, Shiels et al. the insular Pacific n( = 20 sites) and determin- 2013), and fruit and seed are the most com- ing the ratio of plant to animal contents in mon plant items in their diet (see review by their diets (based on mass or volume), we Grant-Hoffman and Barboza [2010] and found that plant material dominated the diet ­Figure 3). After a literature review, Grant- of R. rattus at 17 of 20 sites (Figure 4), and Hoffman and Barboza (2010) found that 36 plants were generally nine times more fre- plant families have been documented contain- quent in its diet than animals (i.e., average ing species consumed by R. rattus, and the ­ratio in Figure 4 is 9 : 1). The three sites where majority of these families had the fruit as animals were proportionally more frequent the plant part that rats consumed. Clark than plants in the diet of R. rattus (i.e., ratio (1982) found that one population of R. rattus was <1.0) included two sites at the highest in the Galápagos Islands consumed at least 22 150 PACIFIC SCIENCE · April 2014

Figure 4. Ratio of plant to animal contents in the diet of R. rattus trapped on Pacific islands. The dashed horizontal line represents the 1 : 1 line where the plant component of the rat diet is equal to the animal component (i.e., a diet of 50% plant, 50% animal). Diets are based on mass or volumetric quantities from stomach content analyses. Twenty entries from 14 islands in the Pacific are shown. The three points below the 1: 1 line (latitudes 38.8° S, 47.0° S, and 47.2° S, each from New Zealand) indicate the only studies where R. rattus diets contained proportionally greater amounts of animal than plant contents. Data are from Strecker and Jackson (1962), Kami (1966), Norman (1970), Fall et al. (1971), Daniel (1973), Clout (1980), Clark (1981), Gales (1982), Tobin et al. (1994), Sugihara (1997), Robinet et al. (1998), Cole et al. (2000), Beard and Pitt (2006), Harper (2007), Sweetapple and Nugent (2007), Yabe et al. (2009), Shiels et al. (2013). species of vascular plants. In Hawai‘i, the rela- most commonly eaten by rats; however, green tive abundance of fruit in R. rattus stomachs (immature) fruit of a variety of coastal species was 55% in mesic forest (Shiels et al. 2013), including coconut (Cocos nucifera) and some 23% – 53% in wet forest (Sugihara 1997), and high-elevation legume fruits and seeds (So- 44% in arid shrubland (Cole et al. 2000). phora chrysophylla) are often consumed by R. Fruit fragments of Clidemia hirta, Rubus rosifo- rattus in the Pacific (Marshall 1955, Fall et al. lius, and Psidium cattleianum, which are all in- 1971, Amarasekare 1994). vasive species on many Pacific islands, were Seed consumption by R. rattus is generally found in R. rattus trapped on O‘ahu (Shiels et an antagonistic relationship (seed predation), al. 2013), and Clidemia hirta and Rubus rosifo- yet some intact seeds are found in stomach lius were found in R. rattus trapped on Hawai‘i contents (see Shiels et al. 2013) and can sur- Island ( Beard and Pitt 2006). Fruit composed vive gut passage and therefore represent a 26% of the stomach contents of R. rattus mutualistic relationship (seed dispersal) with trapped in a New Zealand forest, which in- plants ( Williams et al. 2000, Shiels 2011, cluded 12 native species, and Eleaocarpus Shiels and Drake 2011) (see subsection on hookerianus was the most abundant species, Impact on Plant Communities). Seeds of composing 13% of the stomach contents ­multiple species of the native Hawaiian palm (Sweetapple and Nugent 2007). Ripe fruit is Pritchardia are commonly depredated by R. Pacific Island Invasive Species:Rattus rattus, the Black Rat · Shiels et al. 151 rattus (Pérez et al. 2008), and several other na- leaves, stems, roots, and rhizomes could com- tive trees in Hawai‘i also suffer R. rattus seed pose 2% – 28% of R. rattus diet on Maui, and predation (Shiels and Drake 2011). In a New the greatest abundance of these vegetative Zealand forest, seed fragments were the dom- components occurred in rat stomachs during inant food item in adult R. rattus stomach the summer. Clark (1982) found that fern rhi- contents, composing 48% of their total diet zomes (Blechnum sp.) were a frequent compo- (Sweetapple and Nugent 2007), whereas in a nent in most R. rattus stomachs from montane Hawaiian forest approximately 25% of the forest in the Galápagos Islands; and leaves stomach contents were seed fragments (Shiels from 24 species were found in stomachs ana- et al. 2013). Many seeds of economically im- lyzed across eight R. rattus populations (Clark portant species (e.g., macadamia nuts [Maca- 1981). Moss was also present in R. rattus diets damia integrifolia and M. tetraphylla] and coco- in Hawaiian macadamia nut orchards and in nuts) are consumed by R. rattus in the Pacific New Zealand forests, although it accounted and can form the dominant parts of their diets for a very small (1% – 4%) portion of their diet (Fall et al. 1971, Twibell 1973, Tobin et al. (Tobin et al. 1994, Sweetapple and Nugent 1994, Sugihara 2002, Elmouttie and Wilson 2007). In general, vegetative parts are most 2005). Flowers are not commonly consumed commonly consumed by R. rattus when other by R. rattus (Sweetapple and Nugent 2007), food types are limited. yet in arid habitats in the Galápagos Islands Fungus is an additional component of R. flowers were occasionally found in R. rattus rattus diet, and it has generally been identified stomachs (Clark 1981); in southern Tasmania in stomachs from cool and moist temperate R. rattus foraged on Acrotriche serrulata ­flowers islands, such as North Island, New Zealand, ( Johnson et al. 2011), and rats (probably R. and Stewart Island, New Zealand, where it rattus) in Hawai‘i consumed Freycinetia arbo- composed <2% of R. rattus diet (Daniel 1973, rea inflorescenses (Drake et al. 2011) and de- Gales 1982, Sweetapple and Nugent 2007), stroyed some Clermontia fauriei flowers while and on offshore islands of Tasmania where presumably accessing nectar (D. Drake, un- partly eaten Agaricus campestris and Lepiota publ. data). rhacodes were documented ( Norman 1970). In general, vegetative material (e.g., seed- Winter sampling of R. rattus stomachs re- lings, leaves, and shoots) is less abundant than vealed relatively high (12%) fungi content in fruit and seed in R. rattus diet. However, in pine (Pinus radiata) plantation forest in New some environments and seasons, vegetative Zealand (Clout 1980). In montane forest in material can account for a substantial portion the tropical Galápagos Islands, fungi com- (20% – 30%) of a fruit-dominated diet ( Kami posed up to 12% of the R. rattus seasonal diet 1966, Norman 1970, Clark 1981, Cole et al. (Clark 1981). In addition, fungi dispersal may 2000). The pith tissue in twigs of 23 plant be enhanced by gut passage of fungal spores species is consumed by R. rattus when fruit ( Vernes and Dunn 2009, Vernes and Mc- production is low in the Ogasawara Islands, Grath 2009). Japan ( Yabe et al. 2010, Abe and Umeno Arthropods, particularly insects, are an im- 2011). Rats (probably R. rattus) also wound portant dietary component of most R. rattus legume trees (Acacia koa) in Hawai‘i in young individuals, but they typically compose a (<6 yr old) but not old (7- to 11-yr-old) plan- smaller component of the R. rattus diet rela- tations by stripping the bark (Scowcroft and tive to plant material ( Kami 1966, Norman Sakai 1984); they also eat Clermontia fauriei 1970, Yabe 1979, Clark 1981, Cole et al. bark in wet forest on Kaua‘i (D. Drake, un- 2000, Sweetapple and Nugent 2007, Shiels publ. data). In addition, Campbell (1978) et al. 2013) (Figures 3, 4). For example, ar- found that R. rattus ate the bark on two spe- thropods composed 14% – 16% of R. rattus cies of Araliaceae (Pseudopanax arboreus and stomach contents in Tasmania, Maui, and Schefflera digitata), and they ate leaves, stems, O‘ahu ( Norman 1970, Cole et al. 2000, Shiels and roots of a third species in this family et al. 2013) and just 2% in stomachs in ­lowland (­Stilbocarpa lyallii). Sugihara (1997) found that wet forest in Hawai‘i ( Beard and Pitt 2006). 152 PACIFIC SCIENCE · April 2014

However, insects dominated R. rattus diets on native invasive snails, Achatina fulica and Eug- some high-latitude islands, such as Stewart Is- landina rosea, were readily consumed by R. land and Taukihepa Island ( Big South Cape rattus during captive feeding trials (Meyer and Island), New Zealand (47° S latitude) (Gales Shiels 2009). Introduced slugs were also con- 1982, Harper 2007). In addition, seasonality sumed by R. rattus in New Zealand (Miller and rat age and sex can influence the abun- and Miller 1995) and in captive feeding trials dance of arthropods eaten (Clark 1982, Miller in Hawai‘i, yet not to the extent observed in and Miller 1995, Sugihara 1997, Caut et al. consumption of introduced snails (A.B.S. and 2008a). Clout (1980) attributed the domi- S. Joe, unpubl. data). Several studies indicate nance of arthropods (particularly Lepidoptera that various bird eggs (seabirds and forest and weta [Rhaphidophoridae]) in R. rattus birds) are consumed by R. rattus, and the sizes diet to winter scarcity of fruit and seed. The of the eggs appear to influence the likelihood tree weta, Hemideina thoracica, was a year- of consumption ( Norman 1970, Amarasekare round prey item for R. rattus in New Zealand 1994, Igual et al. 2006, Zarzoso-Lacoste et al. broadleaf forest and composed 26% of their 2011). Because rats generally consume little if annual diet (Daniel 1973). Clark (1982) in the any of the shell when eggs or snails are eaten Galápagos and Gales (1982) on Stewart Island (Amarasekare 1993, Caut et al. 2008a, Meyer found that young rats ate more arthropods and Shiels 2009) or exoskeletons when crabs than did adult rats, which may indicate a are eaten (Fall et al. 1971), captive feeding greater protein demand for growing animals. ­trials are often needed to complement other Similarly, Gales (1982) found that mature fe- means of assessing the importance of such males consumed more birds and arthropods prey in diets of R. rattus. than did males, which may reflect a protein In addition to bird eggs, feathers in R. rat- demand for reproduction. Beetles (Coleop- tus stomachs are evidence that either juvenile tera) and crickets (Orthoptera) were common or adult birds have been consumed directly or components of R. rattus diets in New Zealand scavenged (Clark 1981, Harper 2007, Sweet- (Innes 2005a, Ruscoe and Murphy 2005, St. apple and Nugent 2007). Caut et al. (2008a) Clair 2011) and Hawai‘i, and 11% – 42% of found that approximately half of the R. rattus the R. rattus stomachs sampled in Hawai‘i also stomachs analyzed (n = 9 of 16 stomachs) had contained spiders (Araneae) (Cole et al. 2000, seabird feathers on an isolated New Caledo- Shiels et al. 2013). Caterpillars appear to be nian island during the seabird nesting season; an attractive food item for R. rattus, but their yet there was no evidence of seabirds in rat proportion of total stomach contents can dif- stomachs during the nonnesting season. On fer widely among sites (e.g., 25% in montane Higashijima, Ogasawara Islands, 28% of the Maui [Cole et al. 2000]; 3% in montane O‘ahu stomach contents of R. rattus were seabirds, [Shiels et al. 2013]). particularly the Bulwer’s Petrel (Bulweria bul- Earthworms ( Norman 1970, Clark 1980, werii, 78 – 130 g [Yabe et al. 2009]). Forest Copson 1986, Sugihara 1997), terrestrial birds typically compose <9% of R. rattus ­mollusks (St. Clair 2011), and crabs (Fall et al. stomach contents (Gales 1982, Harper 2007, 1971, Wegmann 2009) (Figure 5) are compo- Sweetapple and Nugent 2007), and birds may nents of the R. rattus diet on some Pacific is- be absent from R. rattus stomach contents lands (Figure 3). Because some food items even in forests where both native and nonna- (e.g., egg yolk, blood, nectar, soft tissues) are tive birds are present (Sugihara 1997, Shiels not easily identifiable via standard stomach et al. 2013). It should be noted that some ani- content analyses, captive feeding trials pro- mals, such as large seabirds ( Norman 1970; vide another useful technique for determining e.g., Sula spp. in Caut et al. 2008a), goats (Capra rat diets. Under captive feeding conditions, R. hircus), burros (Equus asinus), and other rodents, rattus fed on ghost crabs (Ocypode sp.), which appear in R. rattus stomachs from scavenging occupy sandy shorelines on many tropical rather than direct predation (Clark 1981). ­Pacific islands ( Jackson and Carpenter 1966 Rattus rattus has been observed killing cited in Fall et al. 1971). In Hawai‘i, two non- hatchlings of the giant Galápagos tortoise Pacific Island Invasive Species:Rattus rattus, the Black Rat · Shiels et al. 153

Figure 5. Rattus rattus interacting with a strawberry hermit crab (Coenobita perlatus) on Palmyra Atoll. (Photograph courtesy of A. S. Wegmann.)

(Geochelone elephantopus [Clark 1981]) and potential food items of R. rattus, but studies green sea turtle (Chelonia mydas [Caut et al. documenting consumption of these food 2008a]), even though there was no evidence of types in the Pacific are largely lacking. The these vertebrates in the rat stomachs analyzed Pacific boa Candoia( bibroni) coexists with R. at those sites. Gnawed eggshells of Royal rattus in Southwest Pacific forests, yet R. rat- Penguin (Eudyptes schlegeli ) were found in tus stomach contents did not reveal any evi- coastal tussock grasslands of Macquarie Island dence of snakes (Robinet et al. 1998). How- where R. rattus occur (Pye et al. 1999). Skinks ever, the milk snake (Lampropeltis triangulum) were found in <10% of R. rattus stomachs in “reappeared” 2 yr after R. rattus removal from New Caledonia (Caut et al. 2008a) and Tas- San Pedro Mártir Island off Baja Peninsula, mania ( Norman 1970), and remnants of a liz- Mexico (Samaniego-Herrera et al. 2011), and ard were uncovered in a R. rattus stomach in there is reference to R. rattus in the Caribbean Borneo (Harrison 1954 cited in Fall et al. nearly causing the extinction of an endemic 1971). Both lizards (Tropidurus duncanensis) racer snake (Towns 2009). Beard and Pitt and geckos (Phyllodactylus galapagensis) were (2006) did not find any evidence of Eleuthero- found in R. rattus stomachs in arid habitats in dactylus coqui frogs in R. rattus stomachs in the Galápagos, but they never accounted for Hawaiian rain forest, yet R. rattus has been more than 3% of the average stomach con- observed consuming E. coqui in Puerto Rican tents (Clark 1981). Bats, frogs, and snakes are rain forest (Stewart and Woolbright 1996). 154 PACIFIC SCIENCE · April 2014

Two species of bats (greater short-tailed, valuable to know why some birds and plants Mystacina robusta, and lesser short-tailed, M. are highly at risk to predation by R. rattus tuberculata) went extinct on Taukihepa Island, when other species appear to be unaffected. New Zealand, after R. rattus was introduced (Daniel 1990), yet documentation of bats in R. Direct and Indirect Impacts rattus dietary studies across the Pacific is ­absent. Rattus rattus has been documented Rattus rattus can have both direct and indirect foraging in the intertidal zone in several effects on native biota. Many of the direct im- ­locations in the Pacific, including Chile and pacts have been reported in the preceding diet Midway Atoll, but the types of marine organ- section. A growing body of evidence of indi- isms and the extent to which they prey upon rect effects of rats on island ecosystems is re- them is unknown (Carlton and Hodder 2003). ported from a group of 18 offshore islands in Although some prey species are infrequent or northern New Zealand, where half of the is- minimally represented in R. rattus diets, it is lands were rat-free at the time of the study possible that such prey may still suffer (Fukami et al. 2006, Wardle et al. 2007, 2009, ­population-level changes from R. rattus that Mulder et al. 2009, Towns et al. 2009, Peay result from relatively rare consumption (e.g., et al. 2013). The main conclusions from these VanderWerf 2001). studies were that islands with rats (R. rattus, R. exulans, and R. norvegicus) had few seabirds economic importance and present (presumably because the rats ate the environmental impacts seabirds), which caused reduced inputs of ­seabird-transferred marine nutrients and sub- Much of the economic impact resulting from sequent changes in soil fauna, fungi, decom- R. rattus populations relates to agricultural position, and plant nutrient concentrations and horticultural damage; they can destroy up (Fukami et al. 2006, Wardle et al. 2007, 2009, to 30% of crops annually (Hood et al. 1971, Mulder et al. 2009, Towns et al. 2009, Peay Elmouttie and Wilson 2005) and spoil foods et al. 2013). The extent to which R. rattus that result in millions of dollars of losses each (versus other rodent species) was involved in year for islands or island chains (Sugihara these ecosystem-level changes to New Zea- 2002, Pimentel et al. 2005). Disease transfer land islands is unclear, yet R. rattus is certainly to humans and alteration of native habitats are capable of such changes given direct evidence additional negative aspects of R. rattus inva- of predation on burrowing seabirds on islands sions. It can be difficult to determine impacts ( Jones et al. 2008). Additional indirect effects of R. rattus unambiguously without experi- of rats include competition for various food mental studies because additional rodent spe- items. For example, birds that rely on either cies and/or other animals with overlapping arthropods or fruit may suffer from resource diets are often sympatric with R. rattus. competition by R. rattus in areas where these Therefore, studies that have implicated R. animals have overlapping diets. rattus in damaging species and habitats by use of correlative factors should be interpreted Impact on Plant Communities with caution. Knowing the breadth of organ- isms that R. rattus consumes (e.g., from di- The impacts of R. rattus on plant communi- etary studies) is an important first step toward ties can be difficult to determine because of determining their environmental impacts or the substantial time lag between effects on the ecosystem changes that result from R. rat- seeds and seedlings and the responses of adult tus behaviors. However, all interested parties plant populations. Such lag times are particu- (e.g., agriculturalists, academics, conserva- larly relevant for longer-lived plants like trees. tionists, natural historians, or land managers) Some responses to R. rattus impacts may mask will benefit greatly if causal factors can be others, particularly over extended periods, identified and linked to R. rattus’ environ- which makes the species composition of the mental impacts. For example, it would be community potentially important for assess- Pacific Island Invasive Species:Rattus rattus, the Black Rat · Shiels et al. 155 ing rat impacts. For these reasons, assess- lands that include R. rattus as part of the ro- ments of plant community change as a result dent community, but the particular rodent of R. rattus are generally restricted to their species responsible for such removals were ­effects on seeds and seedlings (Shaw et al. not identified (e.g., Moles and Drake 1999, 2005, Abe 2007, Wegmann 2009, Auld et al. Uowolo and Denslow 2008, Meyer and Bu- 2010, Shiels and Drake 2011). taud 2009, Erwin and Young 2010, Grant- Seed removal in field trials is an important Hoffman et al. 2010, Chimera and Drake step in determining seed fate, and several 2011). characteristics of the seeds (e.g., size, nutri- Evidence of rat-gnawed seeds is commonly tional value, and defense chemicals) can affect found in habitats where R. rattus has invaded; seed removal by rodents (Forget et al. 2005). the spatial distribution of such rat-gnawed Rattus rattus individuals remove and eat fruit, seeds is often clumped due to their presence including seed, on the ground and in the can- in “husking stations,” which are sheltered opy (Auld et al. 2010, Shiels and Drake 2011, ­areas where rats process food items after col- Pender et al. 2013). As indicated by a recent lection (McConkey et al. 2003, Elmouttie and literature review of plant reproductive parts Wilson 2005, Wegmann 2009) (Figure 6). (i.e., fruit, cone, seed) consumed by R. rattus, Rats may use husking stations to hide from the small parts (<15 mm, but especially 5 – 10 predators or competitors while they consume mm) were the most frequently consumed food items (Campbell et al. 1984). Rattus rat- (Grant-Hoffman and Barboza 2010). Shiels tus generally does not cache or store foods; and Drake (2011) found that the three largest however, excess cereal bait was cached by R. seeds (17.9 – 30.3 mm longest axial length) rattus held in 5 × 5 × 2 m pens (Morriss et al. monitored in the field were among the 2012), and at the edge of their latitudinal most unattractive to R. rattus, whereas ­distribution (55° S [Macquarie Island]) Shaw ­intermediate-sized seeds (5.2 – 17.7 mm) suf- et al. (2005) found that on average 30 g of fered the highest level of predation (>50%), fruit (equivalent to 20,000 – 30,000 fruit and and the smallest seeds (0.5 – 1.2 mm) were in- seed) of the megaherb Pleurophyllum hookeri gested but not destroyed. On Lord Howe Is- were frequently stored by R. rattus in small land, Auld et al. (2010) found that R. rattus (20 × 20 cm) piles on the surface just before removed 94% of Lepidorrhachis mooreana palm winter. The number of seedlings and adult fruit from trees, but a sympatric palm (Hedys- plants that originate from intact seeds depos- cepe canterburyana) that has fruits 18 times ited in husking stations is rarely known. How- larger in dry mass suffered much less (54%) ever, due to the characteristic substrates of removal by R. rattus. Pender et al. (2013) husking stations (e.g., rock piles, root and tree showed that trapping R. rattus in a Hawaiian bases), they are often unsuitable sites for ger- forest resulted in the reduction of fruit con- mination and plant establishment from intact sumption and seed predation from 46% to seeds that are left by rats. just 4% for the endangered tree Cyanea su- Kukui nut (Aleurites moluccana) is a com- perba. In Hong Kong, Hau (1997) concluded mon tree in tropical Pacific island forests, and that forest restoration by direct seeding would the hard seed coats are often found in husking not be feasible due to rat (R. rattus and Nivi- stations and valley bottoms with distinct venter fulvescens) predation of 12 plant species. markings of rat gnawing (McConkey et al. Yamashita et al. (2003) suggested that R. rat- 2003, Shiels and Drake 2011). It is interesting tus may be facilitating the invasion of the non- that both field and laboratory trials in which native tree Bischofia javanica in the Ogasawara A. moluccana fruit and seed were offered to R. Islands because R. rattus depredates the seeds rattus revealed that it was not an attractive of the dominant native tree Elaeocarpus food item (Shiels 2011, Shiels and Drake ­photiniae-folius both before dispersal (27% – 2011). One explanation for this enigma is that 33% of the seed crop) and after dispersal consumption of A. moluccana in the field may (41% – 100%). Several other studies of fruit be overestimated because the stony seed coats and seed removal have occurred on Pacific is- of the chewed seeds persist indefinitely on the 156 PACIFIC SCIENCE · April 2014

Figure 6. Rattus rattus processing the fruit and seed of Terminalia catappa in a husking station at the base of a tree on Palmyra Atoll. Note the many discarded husks (seed coverings) on the ground surrounding the rat. Food items are typically discarded at individual husking stations over a period of many days. (Photograph courtesy of A. S. Wegmann.)

forest floor (Shiels 2011). An additional expla- 2011, Shiels and Drake 2011), New Zealand nation for the presence of chewed A. moluc- ( Williams et al. 2000), and the Ogasawara Is- cana seeds may be that rats target the very lands (Abe 2007). The majority of the seeds hard and readily available A. moluccana seeds that are dispersed by R. rattus are small to grind or sharpen their teeth. Extending (<1.5 – 2.2 mm) and survive ingestion and gut prior captive feeding trials with R. rattus and passage ( Williams et al. 2000, Shiels 2011). A. moluccana (Shiels 2011, Shiels and Drake In addition, larger-seeded species (>2.5 mm 2011) showed that several R. rattus gnawed long) may also be dispersed by R. rattus by the seed coats without penetrating them transporting collected seeds and then failing (A.B.S., unpubl. data). Thus, seeds of A. mo- to eat them (Abe 2007, Shiels and Drake luccana do not appear to be a favored food for 2011). Such dispersal of native species could rats (particularly R. rattus [Shiels 2011, Shiels be particularly important for plant ­community and Drake 2011]); it may be a “famine food” change if there are no longer native frugivores or simply a hard item that enables rats to to disperse large-seeded, fleshy fruited spe- grind their incisor teeth to sharpen and main- cies, such as the Hawaiian forest species Plan- tain them. chonella sandwicensis (syn. Pouteria ­sandwicensis), Rattus rattus disperses some seeds of both which has seeds that are 18 mm in length and native and nonnative species, as demonstrated are sometimes dispersed by R. rattus (Shiels in the Galápagos (Clark 1980), Hawai‘i (Shiels and Drake 2011). Pacific Island Invasive Species:Rattus rattus, the Black Rat · Shiels et al. 157

Future studies that will extend our under- birds on Lord Howe Island went extinct dur- standing of R. rattus effects at the seed stage to ing the years after a shipwreck occurred and the seedling stage will also help clarify the R. rattus colonized the island (Towns 2009). ­ultimate impacts of R. rattus on plant commu- Rattus rattus is thought to be the primary fac- nities. For example, on subantarctic Macqua- tor in the extinction of the translocated popu- rie Island, Shaw et al. (2005) found that R. lations of Laysan Rail (Porzana palmeri) and rattus reduced initial seedling establishment Laysan Finch (Telespiza cantans) on Midway and seedling survival of the megaherb Pleuro- Atoll (Fisher and Baldwin 1946, Seto and phyllum hookeri, yet high seedling mortality in Conant 1996). Similarly, translocating an areas protected from R. rattus for 1 yr resulted ­endangered parakeet (Eunymphicus cornutus in an absence of sustained impacts on seedling uvaeensis) was deemed unfeasible in New densities. It is more common for R. rattus to Caledonian islands because of R. rattus nest consume seeds than seedlings (Grant-­ predation of eggs (Robinet et al. 1998). Rattus Hoffman and Barboza 2010). However, on rattus predation of robin (Petroica australis) Palmyra Atoll where both R. rattus and land- eggs and chicks was observed directly by auto- crab densities were particularly high (>50 mated cameras on North Island, New Zea- ­individuals/ ha), R. rattus killed 63% of land ( Brown 1997); in Australia, cameras ­monitored seedlings of five native species linked 96% of predation events at artificial ( Wegmann 2009). nests and eggs to R. rattus (Major and Gowing 1994), and R. rattus was also documented re- moving chicks from nests (Major 1991). Simi- Impact on Vertebrate Communities larly, photographic evidence revealed that R. Vertebrate species, such as turtles, tortoises, rattus was the only nest predator of an endan- lizards, and bats, are prey items of R. rattus, as gered flycatcher (the ‘elepaio, Chasiempis evidenced by diet assessments or observations sandwichensis) on O‘ahu Island, Hawai‘i, where (Clark 1981, Daniel 1990, Caut et al. 2008a it reduced nest success by 45% – 55% ( Vander- [see section on Diet]); however, the Werf 2001). In high elevations (2,100 – 2,500 ­community-level impacts of this consumption m) in Hawai‘i, nest predation by R. rattus was have yet to be investigated. The threat of just 4% (n = 500 artificial nests), which may ­predation by rats on birds seemingly attracts be due to low rat densities (<1 individual/ ha) more attention than threats posed to any or high abundance of alternative foods (plants ­other type of rat prey. With the strong climb- and arthropods [Amarasekare 1993]). Ama- ing capabilities of R. rattus, few predators pose rasekare (1994) offered captive R. rattus a greater threat to insular forest birds. Some ­different-sized bird eggs as proxies for native seabirds are also at risk from R. rattus, particu- Hawaiian bird eggs. All but the largest eggs larly at the egg and chick life stages, yet many ( Japanese quail, Coturnix coturnix; 25 × 40 other vertebrate predators also threaten sea- mm) were eaten by the rats, implying that birds of all life stages and these other species some native bird eggs (e.g., endangered palila, can be more successful seabird predators than Loxioides bailleui; 16.8 × 25 mm) would be rats (see Mulder et al. 2011). consumed by R. rattus. Using rat-control Forest and wetland birds have suffered methods to reduce R. rattus abundance, ‘ele- substantial predation and extinction from R. paio reproduction increased 112%, and the rattus (Towns et al. 2006). Five species of population growth rate (lambda) increased birds (saddleback, Philesturnus carunculatus; from 0.76 to 1.00 ( VanderWerf and Smith robin, Petroica australis; fernbird, Bowdleria 2002). Furthermore, long-term (15 yr) nest punctate; banded rail, Rallus philippensis; snipe, monitoring of ‘elepaio in Hawaiian forests re- Coenocorypha iredalei; and bush wren, Xenicus vealed the importance of nest height in forest longipes) went extinct following R. rattus inva- invaded by R. rattus; nests ≤3 m in height pro- sion of Taukihepa Island, New Zealand ( Bell duced offspring less often than nests posi- 1978, Atkinson 1989, Towns et al. 2006). Also tioned higher in the canopy ( VanderWerf in the southern Pacific, five endemic forest 2012). Nesting height may therefore be one 158 PACIFIC SCIENCE · April 2014 useful factor for determining forest bird vul- of sooty terns chicks (90 – 150 g), and about nerability to R. rattus. 40% of their stomach contents was sooty The effects of R. rattus on seabirds are terns, whereas predation by R. rattus was more variable than those on native forest much lower, and <9% of their stomach con- birds; some seabirds are highly vulnerable, tents was sooty tern and forest bird combined whereas others appear largely unaffected by (Harper 2007). Norman (1970) experimen- presence of R. rattus ( Jones et al. 2008, Ruf- tally determined that R. rattus does not kill fino et al. 2009). In a Mediterranean-wide Short-Tailed Shearwater (Puffinus tenuirostris) analysis of historical data sets that included adults (ca. 425 g) or 3-week-old juveniles in four seabird species (three shearwaters that Tasmania but does remove and consume were each >350 g, and one petrel weighing ­unattended eggs (46 – 47 mm length) and eats 25 – 29 g), only the smallest species (the Storm dead chicks. Chicks of Cory’s Shearwater Petrel, Hydrobates pelagicus) appeared to have (Calonectris diomedea) that were 2 – 7 days old its abundance limited by R. rattus (Ruffino were commonly eaten by R. rattus, but chicks et al. 2009). Jones et al. (2008) conducted a ≥3 weeks old (equivalent to 2/3 of the adult global meta-analysis on the effects of intro- body mass) were never depredated (Igual et al. duced rats on seabirds and found that R. rattus 2006). In addition, Igual et al. (2006) ­suggested was the invasive rat that had the largest nega- that egg consumption by R. rattus occurs only tive effect on seabirds, thus surpassing R. nor- when eggs are abandoned and likely broken vegicus and R. exulans in frequency of seabird by the adult; the large size of the Cory’s predation. Furthermore, R. rattus had the Shearwater likely enables them to fend off R. largest effect on burrowing seabirds (22 rattus and protect their eggs. Zarzoso-Lacoste ­species preyed upon), followed by ground- et al. (2011) offered different-sized bird eggs nesting (12 species), those nesting in holes to captive wild R. rattus and found that only and crevices (six species), and branch-nesting the small eggs (14 × 18 mm) and not the (one species) ( Jones et al. 2008). One caution 27 × 35 mm or the 43 × 56 mm eggs were with global generalizations about seabird vul- consumed; however, when eggs were dam- nerability to R. rattus is that most knowledge aged by puncturing before being offered to R. about the impacts of introduced rats on sea- rattus all egg sizes were consumed. Most birds is from temperate ecosystems (e.g., only ­nocturnal burrow-nesting species periodically five of 115 studies in Jones et al. [2008] were leave their offspring unattended once the from tropical regions). chick is only a few days old (Igual et al. 2006), Examples of seabird mortality on Pacific which enables R. rattus the opportunity to ac- islands are also largely limited to temperate cess unattended eggs and chicks. On Midway regions. On Anacapa Island, California, R. Atoll (28° N), 79% of Bonin Petrel (Pterodroma­ rattus removal resulted in pronounced artifi- hypoleuca, 180 – 200 g adults) nests failed due cial nest success of Xantus’ Murrelet (Synthli- to R. rattus predation of both abandoned eggs boramphus hypoleucus scrippsi); 96% of artificial (size 38 × 50 mm) and those being incubated eggs that mimicked eggs of this small seabird (Seto and Conant 1996). There were no adult (148 – 167 g) were depredated before eradica- Bonin Petrels consumed by R. rattus, and tion, and just 3% of eggs were depredated chicks were unlikely to suffer R. rattus preda- (probably by gulls and ravens) after eradica- tion (Seto and Conant 1996). In the tropics, tion ( Jones et al. 2006). Harper (2007) moni- the number of Galápagos Petrel (Pterodroma tored nests of a burrowing seabird, the Sooty phaeopygia) chicks that fledged during two sea- Tern (Puffinus griseus; 800 g), on Taukihepa, sons increased 50% – 100% following R. rattus New Zealand, in areas where R. rattus and control (Cruz and Cruz 1996). weka (an introduced large rail, Gallirallus Seabird characteristics that are associated ­australis) were trapped and in sites where they with vulnerability to R. rattus appear to in- were not trapped to determine the effects of clude burrowing and ground-nesting habits, each of these predators on nest successes of small adult or chick body sizes (i.e., <170 g, sooty terns. Weka were the primary predators which is within the average R. rattus body size Pacific Island Invasive Species:Rattus rattus, the Black Rat · Shiels et al. 159 range [Figure 2]), leaving eggs or young off- the recorded impacts have been population spring unattended while foraging, and possi- suppressions, which commonly involve bee- bly small egg sizes (e.g., ≤50 mm longest tles (Coleoptera), crickets/ katydids (Orthop- length [Norman 1970, Amarasekare 1994, tera), and mollusks (especially large terrestrial Seto and Conant 1996, Zarzoso-Lacoste et al. snails). Additional arthropods that are com- 2011]). Procellariiformes (e.g., petrels and monly at risk from R. rattus include spiders shearwaters) may be particularly vulnerable to (Araneae) and caterpillars (Lepidoptera) (Cole population-level impacts of R. rattus because et al. 2000, Towns 2009, St. Clair 2011, Shiels they lay just one egg per year, have delayed et al. 2013). Towns (2009) suggested that the maturity and long reproductive cycles, and nocturnally active invertebrates are also par- ­often leave their offspring unattended to ticularly vulnerable to R. rattus predation. ­forage when the chick is only a few days old One generalization that was apparent from ( Warham 1990, Seto and Conant 1996). the St. Clair (2011) review was that larger- Native and nonnative rodent communities bodied invertebrates, relative to smaller-­ have also been altered by R. rattus invasion of bodied ones, tend to be more vulnerable to Pacific islands. Harris (2009) conducted a local extinction and suppression by invasive R. ­review of the negative impacts of invasive rattus. Large beetles, weta (large flightless Or- ­rodents on native mammals and found that R. thoptera), giant land snails (Gastropoda), and rattus has been implicated in at least six ex- large millipedes and centipedes (Arthropoda) tinctions in the Pacific, including four from are common prey items for introduced ro- the Galápagos Islands (Nesoryzomys spp. rats), dents in New Zealand islands, and giant stick one from New Zealand (Mystacina robusta insects (Phasmatodea) are preyed upon by R. bat), and one from the Marías Islands in rattus on Lord Howe Island (St. Clair 2011). ­Mexico (Oryzomys nelsoni rat). Stokes et al. Terrestrial snails are at risk of predation by (2009) in Australia, and Harris and Macdon- R. rattus in the Pacific (Clark 1980, St. Clair ald (2007) in the Galápagos demonstrated 2011). Snails that reside in trees, such as many that native rats (Rattus fuscipes and Nesoryzomys of those native to Pacific islands, are often swarthi, respectively) suffered from interfer- depredated by arboreal R. rattus; damaged ence competition with nonnative R. rattus. shell remains from snail predation by R. rattus Furthermore, removal of R. rattus can result have closely correlated with declines in native in population increases in coexisting nonna- tree snails in both the Hawaiian Islands (Had- tive rodents on Pacific islands, which has been field et al. 1993, Hadfield and Saufler 2009) observed with M. musculus in New Zealand and the Ogasawara Islands (Chiba 2010a). (Ruscoe et al. 2011) and in the Galápagos Most sizes of snails are at risk of predation by (Harper and Cabrera 2010). R. rattus, including egg masses (Clark 1981) and 11 – 59 mm nonnative snails (Achatina and Euglandina rosea [Meyer and Shiels Impact on Invertebrate Communities ­fulica 2009]). However, in the Ogasawara Islands, Population- and community-level impacts of larger native snails (>10 mm) are at greater R. rattus on invertebrates have rarely been risk of R. rattus predation than smaller snails studied, despite the importance of terrestrial (<10 mm) (Chiba 2010a). In addition, native invertebrates as detritivores, primary con- snails that occupy the ground are at risk of sumers, predators, prey, and pollinators. In a predation by R. rattus, particularly if they do global review of the impacts of invasive ro- not reside deeply within the leaf litter (Chiba dents on island invertebrates, St. Clair (2011) 2010a,b). highlighted cases in which invertebrate popu- The general traits most useful for predict- lations may have been driven to extinction ing invertebrate vulnerability to R. rattus ap- by invasive R. rattus (e.g., flightless beetles pear to be large body size, nocturnal activity, Hadramphus stillborcarpae [Kuschel and Wor- flightless nature, and residence or activity at thy 1996] and Dorcus helmsi [Ramsay 1978]) in shallow leaf litter depths or exposed surfaces southern New Zealand), but the majority of (Towns 2009, Chiba 2010a,b, St. Clair 2011). 160 PACIFIC SCIENCE · April 2014

Future research on R. rattus – invertebrate in- including cauliflower Brassica( oleracea), sweet teractions is clearly needed on islands outside orange (Citrus sinenis), mango (Mangifera in- temperate New Zealand and tropical Hawai‘i, dica), grape (Vitis vinifera), and apple (Malus where the majority of our generalizations pumilla) (Ahmad et al. 1993). have originated (St. Clair 2011). Introduced rats have been a major threat to agriculture in Hawai‘i for at least the past 170 yr (Tobin et al. 1990). In 1990, it was Agricultural Impacts ­estimated that annual revenues from sugar- Rodents cause substantial losses to food pro- cane (Saccharum spp.) alone in Hawai‘i ex- duction in all regions of the world ( Witmer ceeded $350 million, with annual losses from and Singleton 2010). In fact, Meerburg et al. rat destruction of sugarcane averaging about (2008) estimated that 280 million malnour- 11% (Tobin et al. 1990); however, it was not ished people worldwide could benefit from uncommon to lose about 30% of a sugarcane pre- and postharvest rodent control. Pimentel crop to invasive rodents (Hood et al. 1971). et al. (2005) estimated that annual economic The timing of crop damage was critical for losses due to nonnative rats (including R. rat- planning control strategies for rat impacts, tus) in the United States are approximately and damage to sugarcane became appreciable $19 billion, and the majority of such losses re- at 14 months and peaked at 19 – 21 months. sult from consumption of grain and spoiling The edges of the sugarcane fields suffered the foods. Further estimates described in Pimen- most damage, despite trapping showing uni- tel et al. (2005) include a cost of $15/yr of form rat abundance across the fields (Hood grain or other material for each rat in the et al. 1971). Rattus rattus damages tropical United States, and they estimated that ­roughly fruit (e.g., rambutans [Nephelium lappaceum], 250 million rats are in the United States. Of bananas [Musa spp.]) and seed crops (e.g., the 60 or more species in the genus Rattus, at corn [Zea mays], soybeans [Glycine max] [Pitt least 14 are substantial agricultural pests, and et al. 2011a]), and such damage may be more R. rattus is likely to be the most damaging to common in modern Hawai‘i than in the past agricultural crops globally (Aplin et al. 2003). because of the increased tropical fruit and Most types of fruits and vegetables can be seed crop acreage following the demise of the damaged by R. rattus in the field and in stor- sugarcane industry (R.T.S., unpubl. data). age. Coconuts are well known as desired food Much increased labor and costs due to neces- items for rats in tropical countries, and in sary R. rattus control strategies are required to Tonga R. rattus was the sole cause of the 20% protect crops on Pacific islands, including loss of the coconut crop during one study control efforts in crop fields, adjoining non- (Twibell 1973). Rattus rattus has pronounced crop areas, and in storage and transportation negative effects on rice (Oryza sativa), particu- units (Hood et al. 1971, Ahmad et al. 1993, larly in the Philippines and Southeast Asia Elmouttie and Wilson 2005). (Fall and Sumangil 1980, Aplin et al. 2003, Miller et al. 2008). The macadamia nut indus- Human Health Impacts try in both Australia and Hawai‘i suffers 5% – 30% crop losses from nut consumption Meerburg et al. (2009) reviewed the large by R. rattus (Tobin et al. 1990, 1994, 1996, number of pathogens that rodents can ­directly Elmouttie and Wilson 2005). Rattus rattus or indirectly transmit to humans. Rattus rattus consumes most macadamia nuts by foraging is a carrier of a number of diseases that are in the canopy (Tobin et al. 1996), yet in the serious threats to humans. Such diseases are rows that are adjacent to crop edges R. rattus typically transferred to humans via urine and removes numbers of nuts that drop to the droppings or through hosts that interact with ground equivalent to those that are consumed both R. rattus and humans. We describe some in the canopy (Elmouttie and Wilson 2005). of the most problematic human-threatening Seeds, fruits, and vegetables that are stored in diseases that are carried by R. rattus, including bags and boxes are also damaged by R. rattus, those resulting from bacteria (e.g., bubonic Pacific Island Invasive Species:Rattus rattus, the Black Rat · Shiels et al. 161 plague, leptospirosis) and nematodes (rat lung ( Banks and Hughes 2012). Symptoms of these worm disease); we then describe some infec- bacterial infections in humans can include tions that are much less threatening to hu- headaches and muscle aches, nausea, vomit- mans but can be relatively common within R. ing, mental confusion, rash, pneumonia, rattus in the Pacific. ­encephalitis, and heart failure ( Banks and More than 200 species of mammals may Hughes 2012). Streptobacillus moniliformis, or host fleas that harbor the bubonic plague rat-bite fever or Haverhill fever, can be trans- (Yersinia pestis). Although most mammalian mitted to humans through rat bites or species can suffer from the impacts of Y. pestis, ­scratches, as well as via contact with infected both R. rattus and R. norvegicus show moder- rat urine or feces. Symptoms from human ate levels of resistance (Aplin et al. 2003), and contraction of the bacteria generally include R. rattus was the main host of this disease that fever and arthritis (Singleton et al. 2003). Sal- historically affected humans (Alderton 1996). monella spp. are also carried by R. rattus, and By the 1800s, the bubonic plague, or Black although they do not appear to have any ill Death, had wiped out more than 25 million effects on R. rattus, they can be transferred to people in Europe and an additional estimated humans and livestock ( Lapuz et al. 2008). 50 million in Asia and Africa; by the early Leptospirosis is a worldwide zoonotic in- 1900s the plague had reached many Pacific fection that occurs from Leptospira bacteria islands and popular ports (Twigg 1978, Al- transferred to humans through exposure to derton 1996). In an effort to arrest the plague water or soil contaminated with urine or feces outbreak in Hawai‘i, the Chinatown district from infected mammalian hosts, such as R. of Honolulu was burned and strict quarantine rattus ( Wong et al. 2012). The Leptospira bac- measures were practiced (Tomich 1986). The teria become concentrated in the rats’ kidneys plague in Hawai‘i caused at least 370 human and are passed out of the rat via their urine. fatalities, and the last reported case of human These bacteria survive well in water and can infection in Hawai‘i occurred in 1949 (Sugi- enter humans through any damaged skin, hara 2002). Rattus rattus was also the likely ­mucous membranes, or the conjunctiva of the source of the plague outbreak in Australia in eye. Infection by Leptospira ­icterohaemorrhagiae, the early 1900s, where about 180 people died, which results in the human illness called mainly in the densely populated cities of Weil’s disease, is the most serious form of ­Sydney, Brisbane, and Melbourne (Curson ­human infection. Dogs are also at risk from a and McKracken 1989). Improved sanitation, strain called L. canicola, and they may spread mechanized agriculture, and natural and/or this to their owners, but a vaccine for dogs has human-mediated control of the reservoir (rat) led to dramatic declines in the incidence of and vector (flea) populations have likely re- this disease (Alderton 1996). In Hawai‘i, ap- duced outbreaks of the plague (Tomich et al. proximately 13% of R. rattus are carriers of 1984). However, even today bubonic plague is Leptospira spp. ( Wong et al. 2012). a potential killer; antibiotics can help over- Rattus rattus (as well as R. exulans and R. come the bacterium and a vaccine is available, norvegicus) are definitive hosts of the nema- yet the infection can spread around the world tode Angiostrongylus cantonensis, or rat lung at frightening rates due to our modern means worm ( Wang et al. 2008). Human infections of transportation (Alderton 1996). of rat lung worm can result in the main ­clinical In addition to the fleas that harborYersinia manifestation of eosinophilic meningitis, and pestis, ticks and mites carried by R. rattus can human infection generally arises from con- harbor bacteria that can infect humans. In sumption of the intermediate host (typically eastern Australia and Tasmania some of the slugs and snails). Thus, to complete its life bacterial infections that have resulted from R. cycle, the nematode needs both the rat host rattus include Rickettsia spp., which causes tick and a gastropod intermediate host. Humans, typhus or spotted fever (Singleton et al. 2003); birds, and other mammal hosts can suffer Orientia tsutsugamushi, or scrub typhus; and from meningitis symptoms and death from A. Coxiella burnetii, which may cause Q fever cantonensis infection (Prociv et al. 2000). Since 162 PACIFIC SCIENCE · April 2014

1945, more than 2,800 human cases have been Regulatory Aspects reported in over 30 countries; symptoms of the infection range from headaches and neck On all islands in the Pacific R. rattus is gener- ally consider a pest, and therefore importa- stiffness to numbness, coma, and death ( Wang tion of (accidentally or intentionally) et al. 2008). Screening of R. rattus for A. canton­ R. rattus is unwanted. However, inhabits most ensis infection during the last 70 yr in the Pa- R. rattus cific has revealed infection rates ranging from island groups in the Pacific, so movement of 3% (Taiwan) to 20% – 30% (Australia, Fiji, rats probably has little impact on established populations in most situations beyond the po- ­Japan) to 100% ( Thailand) ( Wang et al. 2008). tential for rats to spread diseases. One notable Calodium hepatica is another nematode that exception is islands and areas that have never is found in R. rattus, and it can infect humans had rats or have eradicated rats and main- through ingestion of the C. hepatica eggs. ­Human infection is rare (37 cases reported tained biosecurity measures to prevent rees- tablishment. Formal regulations against globally) despite R. rattus infection rates R. reaching 79% in some Pacific regions ( Wad- rattus transport and establishment are lacking for most Pacific islands (Moors et al. 1992). dell 1969, Banks and Hughes 2012). Rattus However, the International Health Regula- rattus may also act as reservoirs for the proto- tions of 1969 states that all ships containing zoan Toxoplasma gondii, which requires cats to complete its life cycle. Humans can obtain overseas goods must have a certificate stating that their vessel is maintained as rodent-free Toxoplasma oocytes through contact with cat or is “periodically deratted”; certificates are feces. Some species of Cryptosporidium are a threat to human health, particularly in urban issued by the health authority at approved ports and they are valid for 6 months ( World areas, and R. rattus is known to be a carrier of Health Organization 1995). It is unlikely that the protozoa ( Banks and Hughes 2012). such certification prevents rodent movements There are several types of parasites that among landmasses, although some reductions ­infect R. rattus that are much less likely to be may result. Aircraft and ships are vectors for transferred to, or infect, humans. Rattus rattus can be carriers of a number of blood parasites, repeated introductions of stowaway species like because of routine routes trav- such as Trypanosoma lewisi and Grahamella sp., R. rattus eled and regularity of transport schedules. which occurred in 10% – 25% of R. rattus ­examined in Hawai‘i ( Kartman 1954). Also in Ship personnel control rodents aboard air- craft and ships, and some countries require Hawai‘i, ear mites (Notoedres muris) that cause routine inspection of ships in their ports and ear lesions can infect 26% of the R. rattus population in some forests but other popula- also require biosecurity measures for ships tions suffer very little (<2%) infection (Shiels docking to reduce the risk of importing ro- 2010). Intestinal worms (helminths), likely dents. Such ship-to-shore measures may in- clude rat guards on mooring lines, separation the nematode Mastophorus muris, are common of gangways and cargo nets from piers at in wild R. rattus on many Pacific islands (Fall et al. 1971, Sugihara 1997, Shiels 2010), and night and when not in active use, and main- taining rodent control with rodenticide bait- the majority of the R. rattus captured were parasitized by this worm on Palmyra Atoll ing and trapping on ships and 200 m distant from the wharf (Moors et al. 1992). On is- ( Lafferty et al. 2010) and on Rangitoto Island, New Zealand (Miller and Miller 1995). Be- lands where rats have been eradicated, addi- tional biosecurity measures are typically re- cause the nematodes M. muris and Physolop- quired (Moors et al. 1992, Russell et al 2008). tera getula have obligate life cycles involving arthropods as intermediate hosts, R. rattus is likely infected directly by eating its arthropod Beneficial Aspects prey (Miller and Miller 1995). In addition, parasitic mites cause mange in R. rattus in Despite its remarkable adaptability, R. rattus both the tropical North Pacific (Shiels 2010) is highly destructive and is generally unpop­ and South Pacific (Caut et al. 2008a). ular with people. There are few beneficial im- Pacific Island Invasive Species:Rattus rattus, the Black Rat · Shiels et al. 163 pacts of R. rattus, and its destructive impacts tion of R. rattus can result in relatively large on island ecosystems seem to far outweigh financial gains in some urban and natural set- any positive ones. One potentially positive tings (e.g., Scofield et al. 2011). impact of R. rattus is its possible functional re- In the early and mid-1900s rats became placement of extinct island fauna, such as tak- popular pets, especially with young women, ing a role in seed dispersal (Abe 2007, Shiels who often kept them in squirrel cages. and Drake 2011) or possibly pollination (Cox ­Breeders would develop strains with new 1983, Innes 2001). Additional benefits related ­colors and patterns. Although most modern to R. rattus may include personal financial pet rats are descendants of R. norvegicus, there gain through rat catching and control, as well were several color variants of R. rattus bred as a source of food and entertainment (at least during the early 1920s; the most unusual of historically). these was a bizarre greenish-colored strain Many species of rodents are popular cui- (Alderton 1996). sine in many parts of the world, and rats are often hunted in Africa and Asia as a readily geographic distribution in the pacific available source of protein. Early Polynesian region voyagers in the Pacific may have purposefully kept R. exulans on their ships as an emergency Rattus rattus is distributed globally outside the food source, and R. exulans was trapped and polar regions, with perhaps the highest lati- eaten as an esteemed food source during tude of occurrence at 63° N in Sweden ( J. E. Mäori ceremonial feasts in New Zealand Brooks and F. P. Rowe, 1987, unpubl. report (­Atkinson and Towns 2005). The degree to on commensal rodent control, WHO/VBC/ which R. rattus was consumed on islands or 87.949 [cited in Innes 2005a]). In the Pacific, historical voyages in the Pacific is unknown, R. rattus extends from the Queen Charlotte yet news reports from the 1940s indicated Islands, British Columbia (53° N) (Golumbia that men survived in part by eating rats on 2000) to subantarctic Macquarie Island (55° Wake Atoll (Fisher and Baldwin 1946), and at S) (Copson 1986). Of the 30 archipelagos in least one entry from Captain Cook’s journal the Pacific that were identified by Carvajal noted that a midshipman on the Resolution and Adler (2005), which included those be- cleaned, roasted, and consumed part of a rat tween 25° N and 25° S and from 120° W that the ship cat had caught ( Beaglehole westward through the Bismarck and Palau 1969). ­archipelagos, R. rattus occurs on at least 27 of Rat capture and removal have been a major the archipelagos (A.B.S., J. Russell, and income source in many countries. During the W.C.P., unpubl. data); those that R. rattus are Victorian Era in Britain (1837 – 1901) when potentially absent from include Rotuma, Pit- rats were particularly widespread pests, cairns, and Tokelau, which may harbor R. ex- ­money was to be gained by using live rats for ulans or other invasive rodents (A.B.S., J. Rus- entertainment purposes. In public houses, rat sell, and W.C.P., unpubl. data). pits were often established where pet dogs Island colonization by R. rattus in the Pa- were encouraged by their owners and specta- cific varied greatly during the past 300 yr (see tors to kill as many rats as possible within a set Atkinson [1985] for a review). From Britain it period. One dog, a terrier, killed a record 500 was spread throughout the world along ship- rats in just 5.5 min (Alderton 1996). Because ping routes and probably reached the Pacific of the great supply of rats needed for this type by the 1850s (Atkinson 1985). Of course many of entertainment, many rat-catchers (as many islands in the Pacific were first discovered by as 20 per public house) were employed for Europeans before 1850 (e.g., the Galápagos this purpose. Rats from sewers were avoided in the late seventeenth century and most ­other because they would most likely cause the dogs Pacific islands in the late eighteenth century). to become ill (Alderton 1996); therefore some However, Atkinson (1985) pointed out that of the rats used in rat pits would probably have the European ships that first landed on been R. rattus. Today, control and extermina- most of the Pacific islands would have been 164 PACIFIC SCIENCE · April 2014 carrying R. norvegicus stowaways rather than rattus above 2,837 m, which is approximately R. rattus; the reasoning behind this is that R. the vegetation boundary in the alpine desert rattus was the only nonnative rat in Britain ecosystem; R. rattus generally occurs in low until R. norvegicus was introduced about 1716, abundances near those upper elevations (less and it competitively displaced R. rattus from than one individual/ ha at 2,100 – 2,500 m the wharfs and thereby the ships traveling to [Amarasekare 1993]; 0.2 individuals/trap- the Pacific. Records indicate that R. rattus night at 1,785 – 2,600 m [Banko et al. 2002]). suddenly reappeared on European ships dur- Poa foliosa tussock grassland is the principal ing the 1850s, which is a change that still re- habitat for R. rattus on Macquarie Island (55° mains unexplained (Atkinson 1985). Never- S), probably because it provides year-round theless, the first R. rattus that arrived on most food, shelter, and a slightly warmer micro- Pacific islands are believed to have arrived habitat than outside the tussock canopy (Pye from this British stock (Atkinson 1985). et al. 1999). Black rats have not been found in Once R. rattus was established in the Pa- the windswept uplands of Macquarie Island, cific, islands that are relatively close to one where lichens and cushion-forming plants another (i.e., 300 – 750 m) could be colonized dominate, including Azorella and bryophytes by swimming rats (Innes 2005a). Russell and (Pye et al. 1999). The upper latitudes and el- Clout (2004) determined some of the predic- evations may reflect the boundaries of cool tive factors that influence whether or not New temperatures that R. rattus can withstand, yet Zealand islands are colonized by R. rattus. food scarcity and lower ambient oxygen levels The factors that positively influence the pres- may also be factors contributing to distribu- ence of R. rattus on New Zealand islands tional limitations in such cool environments. ­included island area, presence of a landing Rattus rattus does not seem to be limited by an structure (wharf), and whether or not the is- upper temperature level, or at least this has land was inhabited by humans. Factors shown not been investigated. Thus, R. rattus is abun- to negatively influence the presence of R. rat- dant and spans most terrestrial communities, tus included elevation, distance to nearest is- from arid lowland and montane ecosystems land, and the number of rock types. Finally, (Tamarin and Malecha 1971, Clark 1981, the factors that had no significant effect onR. Amarasekare 1994, Harris and Macdonald rattus presence included number of seabirds, 2007, Chimera and Drake 2011) to lowland number of nonnative land birds, number of and montane rain forests (Daniel 1973, Sugi- introduced rodents, number of introduced hara 1997, Lindsey et al. 1999, Wegmann mammals, and the number of abandoned set- 2009). Even in highly disturbed environ- tlements (Russell and Clout 2004). ments, such as Eniwetok Atoll, which suffered numerous nuclear explosions, R. rattus sur- vived in densities of ­approximately 20 indi- habitat viduals/ ha 10 yr after the last nuclear test (Fall et al. 1971). Climate Requirements, Limitations, and Rattus rattus survives on islands that do not Ecosystems Invaded contain bodies of fresh water (e.g., many Rattus rattus is widely distributed throughout atolls, dry forests). Unlike M. musculus, R. rat- tropical, alpine, and subpolar climates, and tus appears incapable of concentrating its the species has invaded ecosystems from urine, and R. rattus was unaccepting of seawa- shorelines to mountain peaks. The only ­places ter when offered it ( Norman and Baudinette where R. rattus is not found in the Pacific 1969). Therefore, much or all of black rat seem to be within the highest latitudes (those ­water requirements for survival probably >55°) (A.B.S., J. Russell, and W.C.P., unpubl. comes from foods consumed (e.g., fleshy fruits, data) and the highest elevations (in most cases vegetative material), yet dew and ­rainfall are >3,000 m) (Amarasekare 1994). On Hawai‘i other sources of water to fill survival require- Island, ­Amarasekare (1994) did not find R. ments for R. rattus (Alderton 1996). Pacific Island Invasive Species:Rattus rattus, the Black Rat · Shiels et al. 165

Habitat Resource Requirements and Limitations erford et al. 2009, Shiels 2010). In Hawaiian montane rain forests, Lindsey et al. (1999) Rattus rattus commonly utilizes belowground, used radio tracking to determine that R. rattus ground, and aboveground habitats. Relative (n = 9) nested in trees or treeferns, whereas to other invasive Rattus spp. and Mus muscu- Shiels (2010) found that R. rattus (n = 24) used lus, R. rattus uses a much greater proportion a mixture of aboreal and belowground den of the arboreal habitat ( Lindsey et al. 1999, sites and nearly half of the monitored indi- Shiels 2010), and R. rattus prefers forests over viduals switched their den site uses between open, heath, and scrub macrohabitats in Aus- tree cavities and burrows. Larger trees (in tralia (Cox et al. 2000). Preference of R. rattus height and girth) were the most common for arboreal habitats is further supported by trees in which R. rattus denned in Hawaiian its numeric dominance over other coexisting forests, and these included nonnative Aleurites rodents in most insular forests in the Pacific moluccana and Grevillea robusta, and native (Tamarin and Malecha 1971, Daniel 1973, Acacia koa and Metrosideros polymorpha ( Lind- Clark 1981, Sugihara 1997, Yabe et al. 2010). sey et al. 1999, Shiels 2010). In New Zealand However, R. rattus does not require forest or forest, Hooker and Innes (1995) found that all substantial vertical structure, as evidenced by of the R. rattus radio-collared in their study its high abundance in savannahs (Clark 1981) had dens in trees and that the den sites were and on atolls with low scrub vegetation (Fall too high (>2 m) to pinpoint from the ground. et al. 1971). Unlike other studies where R. rattus was typi- Unlike its high abundance in most insular cally found denning only in trees, all of the 14 forests, R. rattus is not always the dominant R. rattus followed on a 797 ha offshore island rodent species in agricultural settings. Tobin in southern New Zealand (Taukihepa) had and Sugihara (1992) examined the relative dens belowground despite the presence of a abundances of three species of sympatric rats short-statured forest; many of the dens were in sugarcane fields in Hawai‘i. They found in seabird burrows, beneath logs and ­branches, that either R. norvegicus or R. exulans was the and in fern cover (Rutherford et al. 2009). On most numerous within any given field and Macquarie Island, where trees are absent, Pye that R. rattus was captured mainly near field et al. (1999) documented extensive tunneling edges where trees were present. During that connected entrances to R. rattus den sites 11,200 trap-nights, Tobin and Sugihara in coastal tussock habitat. (1992) captured 526 R. norvegicus, 335 R. exu- Habitat partitioning, which can reduce lans, and 139 R. rattus in four sugarcane plan- competition, has been previously observed for tations that regularly experienced pronounced R. rattus when it is sympatric with other intro- rat damage. The importance of arboreal habi- duced rodents (Shiels 2010). Experimental tat availability for R. rattus is evident histori- evidence of habitat partitioning between R. cally in the United Kingdom, where R. rattus rattus and R. exulans was demonstrated by was not able to coexist with R. norvegicus be- Strecker and Jackson (1962), where several cause of interference competition (R. nor­ rats of each species were confined in 3 × 3 m vegicus is larger than R. rattus) coupled with enclosures for 14 days and then examined for the presence of an arboreal rodent (the native signs of conflict and weight loss. The authors red squirrel Sciurus vulgaris) that already oc- concluded that if food and available micro- cupied the arboreal niche ( King et al. 2011a). sites were present, these rats could coexist in a Den sites are important habitat features for confined space. However, when smaller cages black rats because roughly half of their lives limited space and microhabitats to a greater are spent in them. Common den sites for R. extent or arrival times of different rat species rattus include cavities in trees or rocks, be- into the cage were altered, then there was neath woodpiles or dense vegetation cover, strong evidence of interference competition fern and stick-lined arboreal nests, and in bur- that resulted in fighting and high death rates rows belowground ( Lindsey et al. 1999, Ruth- ( Barnett 1964, Norman 1970). In Australia, 166 PACIFIC SCIENCE · April 2014

Stokes et al. (2012) experimentally deter- in intraspecific communication. Scent mark- mined that the resident species (R. rattus or ings from other animals do not always affect native R. fuscipes) were dominant in their be- R. rattus behavior. Stokes et al. (2012) experi- havior relative to intruders 88% of the time, mentally determined that R. rattus does not irrespective of the rodent species that was the appear to respond to traps scented with a intruder. competing rat species (Rattus fuscipes) in Aus- tralia. However, scents of predators, such as physiology and behavior mongooses, were avoided by R. rattus (Tobin et al. 1995). Rattus rattus also follows scents to The physiological and behavioral adaptations revisit locations and to find prey; rats are con- of R. rattus have likely aided in its successful stantly, or nearly so, sniffing the air and are establishment in Pacific island ecosystems. well attuned to foreign sounds (Innes 2005a). Rattus rattus has a relatively high metabolic In New Zealand, R. rattus located some bird rate and keen sense of smell. Black rats are nests before eggs were laid, then returned ­agile, move beneath vegetation cover rather regularly to the nests during the egg-laying than in exposed areas, use aboveground habi- period, and finally depredated several eggs tat (trees) more than other introduced rodent (Innes 2001). Exposed and concealed nests species, and typically move food items upon were equally vulnerable to predation, suggest- collection but generally do not store (cache or ing that rats do not readily rely on visual cues hoard) them (see section on Impact on Plant to locate nests (Innes 2001). Selvaraj and Arc- Communities under Economic Importance hunan (2006) determined that male R. rattus and Environmental Impacts). An important scent provided by both cheek cells and urine point for rat control and eradication programs increased the acceptance of poison bait by fe- is that rats typically suffer from “neophobia,” male R. rattus. which is fear of new objects; it occurs when Black rats are agile, good climbers, excel- there is a change in an otherwise familiar situ- lent jumpers, and adept swimmers (Meehan ation ( Barnett 1963, Clapperton 2006). 1984, Innes 2005a, Foster et al. 2011, King Rodents have large surface areas relative to et al. 2011a). They have been documented their volume, which results in greater heat jumping higher than 150 cm (Meehan 1984), losses from their bodies when compared with and all 20 adults of various body sizes (range, larger mammals. Thus, to maintain their body 87 – 173 g) that were tested in Hawai‘i were temperatures, rodents have high metabolic able to jump at least 40 cm high (Pitt et al. rates. Some rodents must find and eat up to 2011d ). When R. rattus was compared with R. 70% of their body weight each day to support norvegicus in New Zealand pen trials, Foster et their metabolic requirements (Alderton al. (2011) determined that R. rattus was faster 1996). Captive R. rattus consumed 14 – 18 g of moving and more agile, more easily overcame pellet bait and a slice of apple each day (Clap- obstacles, was less dependent on footholds, perton 2006). Rattus rattus does not hibernate, was less likely to fall, and could more easily and in winter and early spring months on reach unsupported ends of small branches. Macquarie Island (55° S) black rats retrieved Rattus rattus can also fit through small holes, seeds from established surface caches to sus- and all 16 adults tested of various body sizes tain themselves until natural seedling recruit- (range, 85 – 162 g) were able to pass through ment commenced in the spring (Shaw et al. 35 mm diameter holes to access food (Pitt 2005). et al. 2011d ). Black rats have been known to Rattus rattus has a keen sense of smell that swim 300 – 750 m to colonize adjacent islands is readily used during foraging and communi- (Innes 2005a). cation with other individuals (Mallick 1992, Rodents are often in areas of relatively Innes 2005a,b). Mallick (1992) found that high vegetation cover presumably to limit both sexes of R. rattus mark substrates with their exposure to predators (Alderton 1996, urine at equal rates, and that urine marking Cox et al. 2000, Atkinson and Towns 2005). probably contains olfactory cues that are used Using spool-and-line tracking in the Wai‘anae Pacific Island Invasive Species:Rattus rattus, the Black Rat · Shiels et al. 167

Mountains on O‘ahu, R. rattus was observed Hakalau Forest on Hawai‘i Island ( Lindsey under vegetation ground cover an average of et al. 1999), three to five times in the Rotoehu 88% of the monitoring time when rats were Forest, North Island, New Zealand (Hooker out of their dens and active on the ground and and Innes 1995), two to nine times in Puketi aboveground (Shiels 2010). In eastern Austra- Forest, North Island, New Zealand (Dowd- lia, Cox et al. (2000) found that R. rattus pre- ing and Murphy 1994), and one to 11 times in ferred densely vegetated understories and Kahanahäiki Forest on O‘ahu (Shiels 2010). showed a significant attraction to habitats Determining R. rattus home ranges helps with increased leaf litter when their popula- elucidate rat distribution and habitat prefer- tion density was relatively high. The direc- ence and assists with rat control strategies tions of rat movements are often unpredict- such as trap and bait-station spacing (Howald able because their exploratory behavior is et al. 2007). Home ranges of R. rattus in two influenced by both scents and other features montane mesic forests on O‘ahu (1.5 – 9.1 ha that are encountered in the environment [Shiels 2010]) were nearly as variable as those ( Barnett 1963). Often a R. rattus individual in a South Island, New Zealand, beech forest doubles back over its same pathway by cir- (0.3 – 11.4 ha [Pryde et al. 2005]). Other New cling or moving a few decimeters in one di- Zealand studies in North Island forests found rection, then returns to a point that it had al- that R. rattus home ranges were much smaller ready traveled before it quickly changes paths (e.g., 0.3 – 1.8 ha in a study by Dowding and and explores a new direction ( Key and Woods Murphy [1994], and 0.3 – 2.2 ha in Hooker 1996, Shiels 2010). The average height R. rat- and Innes [1995]). When 55 R. rattus were tus was observed active aboveground was 2.8 monitored in Hawaiian macadamia nut or- m (Shiels 2010), yet black rats can spend an chards, average home-range sizes were 0.2 ha average of 30% – 90% of their night activity (Tobin et al. 1996). Lindsey et al. (1999) de- on the ground (Dowding and Murphy 1994, termined that R. rattus home range averaged Hooker and Innes 1995, Lindsey et al. 1999, 4.2 ha for three males and was 1.8 ha for one Shiels 2010). female in montane wet forest on Hawai‘i Is- Rattus rattus typically leaves its den just land. Male R. rattus often have larger home ­after sunset and returns just before sunrise ranges than females (two times larger in (Hooker and Innes 1995, Shiels 2010); how- Whisson et al. [2007]; three times larger in ever, some rats return to their den partway Hooker and Innes [1995]; more than nine through the night and then resume foraging times larger in Pryde et al. [2005]), yet aver- (Dowding and Murphy 1994). One female rat age home range sizes do not always differ in the study by Shiels (2010) left her den site ­between sexes (Dowding and Murphy 1994, at sundown (three nights) or 17 min before Shiels 2010). Movements between captures sundown (one night). In macadamia nut or- can range from 18 to 174 m (Clapperton chards, black rats left their dens 1 – 2 hr after 2006), and in Hawaiian mesic forest the maxi- sunset and returned 1 – 2 hr before sunrise mum distances that R. rattus (n = 12) was re- (Tobin et al. 1996). Rattus rattus is rarely ac- corded from den sites during nighttime forag- tive during the day unless densities are high ing averaged 45 m (Shiels 2010). (>50 individuals/ ha) and predators are absent, such as previously documented on Palmyra reproduction and population Atoll ( Wegmann 2009). As evidence of their dynamics pronounced social behavior, multiple R. rattus individuals den together, and they do not typ- Owing to the prolific nature of rodents, rapid, ically occupy just one den site during the pe- exponential increases in populations are com- riod that they are monitored (Dowding and mon ( Krebs et al. 1973), especially on islands Murphy 1994, Lindsey et al. 1999, Ruther- (Martin et al. 2000). The female R. rattus re- ford et al. 2009). Over a range of monitoring productive biology includes an estrous cycle periods (1 – 20 weeks), R. rattus changed den of 4 – 6 days, a 20- to 22-day gestation period, sites to different trees one to three times at and 21 – 29 days to complete weaning (Innes 168 PACIFIC SCIENCE · April 2014

2005a). According to laboratory studies, R. New Zealand, Alterio et al. (1999) found that rattus reaches sexual maturity at 2 – 4 months abundances of R. rattus ranged from 1.8 to 5.6 ( Watts and Aslin 1981). Rattus rattus is capa- individuals/100 trap-nights. In a 5-yr study of ble of having litters every 32 days (range, R. rattus in North Island, New Zealand, Innes 27 – 38 [Innes 2005a]), and four to six litters et al. (2001) found that abundances were 1 – 20 per year is common (Tobin et al. 1994, Efford individuals/100 trap-nights (mean ca. 8 – 10). et al. 2006). Each litter typically averages Other studies of R. rattus from North Island, 3 – 6.5 individuals (Tobin et al. 1994), yet in New Zealand, found that abundances ranged laboratory trials the litter size ranges from from 5 to 35 individuals/100 trap-nights three to 10 and averages five to eight (Innes (Dowding and Murphy 1994, Wilson et al. 2005a). On a small New Zealand island, 2007). Moller and Craig (1987) found that female R. Determining the causes of pronounced rattus produced 19 – 21 young per year (in population fluctuations and density differ- three litters). Rattus rattus is not monoga- ences among sites has been one of the greatest mous, and multiple paternity in a single litter challenges in animal ecology ( Krebs et al. has been demonstrated for wild R. rattus 1973). Availability of resources, rainfall, pred- (Miller et al. 2010). ator abundance, and disease are all factors that Rattus rattus density can vary greatly among can potentially influence population dynamics sites and islands in the Pacific. For example, of R. rattus. For example, dramatic seasonal density estimates for R. rattus in Hawai‘i increases in rat and mouse populations in ­include 0.7 individuals/ ha in high-elevation New Zealand were explained by several cor- shrubland (Amarasekare 1994), 3.6 related factors including litter arthropods, ­individuals/ ha in lowland wet forest ( Beard beech (Northofagus truncata) flowers (Fitzger- and Pitt 2006), 7.1 rats/ ha in montane mesic ald et al. 1996), fruit and seed availability forest (Shiels 2010), and 8 – 15 individuals/ ha (Alley­ et al. 2001), and predator populations in lowland dry forest (Tamarin and Malecha (Efford et al. 2006). Studies in New Zealand 1971). In New Zealand, R. rattus density esti- have suggested that stoats and cats are key mates in forests ranged from 0.5 to 6.8 rats/ ha predators that may partly regulate R. rattus (Dowding and Murphy 1994, Hooker and populations (Innes et al. 2001, Blackwell et al. Innes 1995, Brown et al. 1996, Innes et al. 2003, Efford et al. 2006), and cats and mon- 2010). Rattus rattus populations on Pacific is- gooses are rodent predators in Hawai‘i that lands have densities comparable with those may influence R. rattus populations (Tamarin within its native range in India, which in- and Malecha 1971, Shiels 2010). Food avail- cludes 14.5 individuals/ ha in tropical forest ability may be an important factor influencing (elevation 340 – 2,400 m) (Chandrasekar-Rao rodent reproduction and abundance ( Black- and Sunquist 1996) and 2 – 36 individuals/ ha well et al. 2003). Juvenile R. rattus abundance in tropical forest and savannah (elevation in mesic montane forests on O‘ahu was 1,800 – 2,500 m) (Shanker and Sukumar 1999); ­highest in June – December, which coincides however, density comparisons should be with the seasonal timing of the heaviest ­interpreted cautiously because of the wide ­fruiting and seed fall of Psidium cattleianum range of factors that are dissimilar among rat- ( June – October) and may influence the repro- trapping studies (e.g., habitat, trapping re- ductive timing and juvenile abundance of R. gime, rodent species composition, abundance rattus (Shiels 2010). Psidium cattleianum is a and density calculation). common tree in most wet and mesic forests in Estimates of R. rattus abundances based on Hawai‘i that produces high seed rain, and it is the number of individuals per 100 trap-nights a highly desired food item for R. rattus (Shiels were 8 – 17 in montane wet forest on Maui and Drake 2011, Shiels et al. 2013). Late sum- (Sugihara 1997), 8 – 14 in montane mesic mer and autumn are also seasons when juve- ­forest on O‘ahu (Shiels 2010), and 11 – 25 in nile R. rattus abundance is highest in lowland montane wet forest on Hawai‘i Island ( Lind- dry forest on O‘ahu (Tamarin and Malecha sey et al. 1999). In a study on South Island, 1971) and in New Zealand (Innes et al. 2001). Pacific Island Invasive Species:Rattus rattus, the Black Rat · Shiels et al. 169

There are typically more male rats in a given brown tree snakes in Guam (R.T.S., unpubl. population than females (Sugihara 1997, data). In Tasmania, Tasmanian devils (Sar- Innes 2005a,b), and peak R. rattus densities cophilus harrisii) and quolls (Dasyurus spp.), (all age classes and both sexes) occurred from which are carnivorous marsupials, introduced October through January (autumn and win- foxes (Vulpes vulpes), feral cats, and raptors are ter) in montane and coastal forest on O‘ahu predators of R. rattus (H. Stephens, pers. (Tamarin and Malecha 1971, Shiels 2010). comm.). Skua (Stercorarius spp. [a predatory Similarly, in a 27 yr snap-trap study in Oron­ seabird]) are capable of consuming R. rattus, gorongo Valley, New Zealand, autumn and but there have not been any such reports for winter were also the peak seasons for R. rattus Pacific islands. density (Efford et al. 2006). Maximum survival of is about 2 yr R. rattus response to management in the wild, but mean survival is usually 1 yr or less ( Weinbren et al. 1970, Shiels 2010). In Much interest in Pacific island rodent man- the laboratory, however, mean longevity for agement occurred during the late 1800s and R. rattus is much longer, and Bentley and early 1900s as a result of expanding plantation Taylor (1965) recorded average life spans of agriculture and associated rodent damage. An 3.9 yr for males and 3.4 yr for females. An- additional period of increased interest in ro- nual disappearance rates for R. rattus during a dent research and management in the Pacific 2 yr live-trapping study exceeded 90% for occurred during the 1940s – 1950s, and it was both sexes in the Orongorongo Valley, New associated with increased military operations Zealand. Few rats survived more than a year in the Pacific and heightened incidences of in the field, and the maximum longevity rodent-borne diseases ( Wilson 1968). Such ­recorded was 11 months for males and 17 interests initiated several multiyear research months for females (Daniel 1972). In Hawai- projects that focused on rat ecology and con- ian montane forest, R. rattus individuals that trol in the Pacific; perhaps the most substan- were recaptured at the end of a 2 yr study had tial ones were in Ponape (Pohnpei) from 1955 lived 10.9 ± 1.4 months (mean ± SE), and four to 1958 (Storer 1962), Enewetak (Eniwetok) of 18 individuals were alive at 19 months of Atoll from 1964 to the late 1970s (Devaney age (Shiels 2010). et al. 1987), the Philippines from 1967 to 1983 (Fall and Sumangil 1980, Singleton and natural enemies Petch 1984), Malaysia during the late 1970s (Dubock 1984, Richards and Ku 1987), and Cats (Felis catus) and owls (particularly the Hawai‘i from 1960 to the 1970s for bubonic Barn Owl Tyto alba) are the most ubiquitous plague monitoring research (Tomich et al. predators of R. rattus on most Pacific islands, 1984) and 1966 to the present for ecology, and these predators are generally nocturnally crop damage evaluation, toxicant screening active like R. rattus. Other raptors, primarily and registration, and conservation (Sugihara hawks and eagles, also consume R. rattus on 2002, Pitt et al. 2011a). Pacific islands. MongoosesHerpestes ( auro- The longest-standing and most common punctatus) consume R. rattus on several Pacific control measures that have been implemented islands (Hays and Conant 2007). In New Zea- are chemical control using rodenticides, phys- land, Mustela spp. (stoats, weasels, and ferrets) ical control, and exclusion. Biological control are predators of R. rattus. Several species of has been unsuccessfully attempted several civets ( Viverridae), which are nocturnal mam- times with often unexpected and negative mals, are predators of R. rattus in the Philip- ­secondary effects. Often there are multiple pines (Rickart et al. 1993). Monitor lizards control measures used simultaneously, woven (Varanus indicus) and the brown tree snake into an integrated pest management strategy (Boiga irregularis) are predators of R. rattus in to control rodents ( Witmer 2007). The man- the Mariana Islands ( Wiewel et al. 2009), and agement of rodents can be broadly separated R. rattus has been found in the gut of several into two distinct operational approaches: 170 PACIFIC SCIENCE · April 2014

­control and eradication. Rodent control (pop- ­Witmer et al. (2007) reviewed the use of ro- ulation and damage reduction) has historically denticides for conservation efforts. Hawaiian been used to protect agricultural crops, sugarcane growers began using a myriad of ­human health, and natural resources. Control mostly acute rodenticides (e.g., strychnine projects attempt to minimize the effects of ­alkaloid, 1080) in the late 1800s, but due to ­rodents but require ongoing operations. environmental health and human safety con- ­Efforts to eradicate rodents from islands or cerns these acute rodenticides were replaced fenced areas attempt to remove all rodents in agricultural settings by first- and second- from an area over a short period and then generation anticoagulant products like those maintain the area as rodent free using quaran- containing warfarin or diphacinone (Sugihara tine methods. Although eradicating rodents 2002). Anticoagulants became the toxicants of from small areas has been accomplished using choice for controlling rats beginning in the ground-based trapping and persistent control 1950s and were applied by placing the poison methods, techniques developed over the last in plastic baggies and tossing them into agri- 20 yr to effectively aerially broadcast rodenti- cultural fields and surrounding habitat ( Lind- cides have enabled much larger areas to be sey et al. 1971). Threats to nontarget animals, targeted (Howald et al. 2007). Since eradica- including humans eating feral pigs (Sus scrofa) tion programs began on small islands in the that were contaminated with rodenticides early 1960s, rats have been removed from such as diphacinone, prompted the use of over 300 islands around the world (Howald tamperproof bait stations (Tobin et al. 1990, et al. 2007, Towns 2009, Witmer et al. 2011). Pitt et al. 2011c). Bait stations are used in ag- Gaining local community support for rat ricultural, urban, and natural areas in contem- control or eradication, particularly when it porary Pacific islands to help control rodents. ­involves the use of toxicants (rodenticides), is Bait degradation by fungi (especially in wet an important yet often difficult procedure. habitats) and consumption by ants, slugs, and Ogden and Gilbert (2009) identified three other invertebrates reduces bait availability reasons why gaining local support for rat and palatability (Tobin et al. 1990, Mosher eradications is typically challenging: (1) a lack et al. 2010). In addition, prolonged use of a of appreciation of the ecological damage re- single type of rodenticide decreases its effec- sulting from rats, and therefore a low priority tiveness (Doty 1945). placed on their elimination, (2) suspicion by Pitt et al. (2011a) tested the efficacy and community members that conservationists palatability of nine commercial rodenticide want access to private lands and island-wide bait formulations; second-generation antico- biosecurity, and 3) numerous regulatory bar- agulants (e.g., brodifacoum) generally had the riers that delay decisions and actions and ulti- highest efficacy on R. rattus. Several types of mately result in disinterest in such projects. toxicant baits require multiple feedings by Witmer et al. (2011) discussed many other each individual rat (e.g., diphacinone), challenges to invasive rodent eradication on ­whereas others are more toxic and typically islands. require fewer feedings for a lethal dose (e.g., brodifacoum). Witmer et al. (2011) identified 40 islands or archipelagos in the United States Chemical Control where rodent (primarily Rattus spp.) eradica- tion has been attempted, of which approxi- Rodenticides, such as those containing the mately half were Pacific islands, and almost all anticoagulants diphacinone or brodifacoum, of them had used diphacinone; approximately have been used on many Pacific islands to 75% of these eradication attempts were suc- control R. rattus; one benefit over trapping is cessful. The larger islands where eradication that rodenticide bait can simultaneously affect has been attempted in the Pacific include Rat many rats over longer periods than a single Island (2,900 ha) in Alaska where R. norvegicus baited trap. Rodenticide baiting is also gen­ was the target rodent species (Howald et al. erally less labor-intensive than trapping. 2007), and most recently Macquarie Island Pacific Island Invasive Species:Rattus rattus, the Black Rat · Shiels et al. 171

(128,860 ha) where R. rattus and M. musculus costs decreased to about $2000/ km2 ($20/ ha). were the target rodents (Springer 2011). The authors’ main conclusion from the study Natural and artificial scents have been was that it is feasible to reduce rat abundance ­tested for their effectiveness in deterring R. during a 4-month period each year during the rattus from particular food items. Synthetic forest bird breeding season ( Nelson et al. scents were unsuccessful at deterring R. rattus 2002). from macadamia nut trees in Hawai‘i ( Bur- Howald et al. (2007) collated economic wash et al. 1998); yet mongoose urine and costs for 47 eradication campaigns that used ­feces deterred R. rattus from traps in Hawai‘i toxicant bait; costs varied widely by island (Tobin et al. 1995). Capsaicin from chili fruits even when standardized by size ( US$3000 – (Capsicum annuum) helped reduce Rattus spp. $20,000/ ha [adjusted to 2005 prices]) and bait predation of bird eggs in New Zealand (Baylis delivery method (aerial broadcast, hand et al. 2012). Price and Banks (2012) recently broadcast, bait station). Minimizing impacts tested the effectiveness of pre-exposing R. rat- of rodenticides to nontarget animals while en- tus to scents of native species to potentially suring that enough bait remains to expose all protect them before reintroducing such na- of the rats is important for successful rodent tive species into areas with R. rattus. When R. eradication programs ( Witmer et al. 2007, rattus had encountered the prey odor (quail Witmer et al. 2011). feces and feathers) before encountering the prey (quail eggs, which were used as surro- Physical Control gates to native bird eggs), there was a 62% reduction in quail egg predations relative to Physical control methods (e.g., trapping, areas where the prey and odor were intro- fencing) are frequently used to manage R. rat- duced simultaneously (Price and Banks 2012). tus because they do not require the use of It is unlikely that use of odors would be an ef- toxicants. Both live- and kill-trapping tech- fective long-term rat deterrent because indi- niques have been used to control R. rattus viduals become accustomed to foreign scents throughout the Pacific (see Sugihara et al. and objects over time (Clapperton 2006). 1977). Continuous trapping campaigns al- Campaigns to sterilize wild rats were also most certainly increases trap shyness, thereby attempted where the chemosterilant was ad- affecting the degree to which rat populations ministered in bait. Despite the successful ster- are reduced and desired resources are pro­ ilization of male rats in the laboratory, field tected (Tobin et al. 1990, Mosher et al. 2010). trials failed as evidenced by many female rats Many other factors may cause failure in rat impregnated in populations containing “ster- control programs, and such factors may not ile” males (Bowerman and Brooks 1971). Fu- always be obvious. For example, between migating rat dens with poison gas has been 1914 and 1922, averages of 141,000 rats were attempted to reduce R. rattus populations, but removed annually using trapping methods it was also unsuccessful (Doty 1945). from sugarcane plantations on Hawai‘i Island, Nelson et al. (2002) measured the costs and yet there was no apparent effect on the popu- effectiveness of rat control (R. rattus and R. lations of the rats, and sugarcane continued to exulans) over 3 yr ( January – April each year) be damaged (Pemberton 1925). using toxic bait and snap-traps in a remote Most trapping regimes place traps on the Hawaiian montane rain forest. A 48 ha treat- ground for ease of maintenance. However, in ment area was monitored before, during, and macadamia nut orchards in Hawai‘i, Tobin after control. The cost was about US$7000/ et al. (1994) established snap-traps (41 – 49 km2 ($70/ ha) to reduce the rat population traps/ ha) in 8 to 11 ha blocks by attaching the 58% – 90% during 1 yr, yet the rat population traps to lower lateral branches in the trees. rebounded from incursion from the perimeter New Zealand and Hawai‘i have both estab- each year such that rat numbers had returned lished large trapping grids in natural areas to pretreatment levels by the beginning of the to control R. rattus and other rodents. In subsequent treatment. After the first year, the these large trapping grids, traps are checked, 172 PACIFIC SCIENCE · April 2014 rebaited, and reset approximately every 2 make economic sense over other methods of weeks for several years or decades ( King et al. predator control. However, for animals that 2011b, Pender et al. 2013). In Hawai‘i, such rely upon particular areas for annual repro- large-scale (26 ha, 440 traps) snap-trapping duction (e.g., seabird nesting sites) or endan- grids have reduced R. rattus abundance and gered animals that do not migrate great dis- subsequently their fruit removal and seed pre- tances (e.g., tree snails), predatorproof fencing dation of an endangered plant (Pender et al. may be a particularly useful conservation 2013). However, Ogden and Gilbert (2009) technique. found that trapping alone was not enough to reduce rat (primarily R. rattus) numbers for Biological Control successful avian reintroductions on Great Barrier ­Island, New Zealand. After determin- Predators of R. rattus have been intentionally ing that ground-based rodent control was introduced to some Pacific islands in attempts ­ineffective for improving nest success of the to reduce the negative effects of rats. The endangered cavity-nesting Kaua‘i Thrush, small Indian mongoose is currently found in puaiohi (Myadestes palmeri), Pitt et al. (2011b) eight Pacific islands, including four in the Ha- developed a ratproof artificial nest box, using waiian Islands, two in Fiji, and two in Japan a design that was essentially a 36 cm length of (Hays and Conant 2007). Although rodents 15 cm diameter plastic pipe with an entrance were the dominant part of the mongoose diet cut at an angle of 49 degrees. Multiple tech- in some Hawaiian sugarcane fields (Baldwin niques are often needed to conserve and re- et al. 1952), rodents continued to thrive after store native species that are vulnerable to R. mongoose introduction. In 1958, Hawai‘i’s rattus. Commissioners of Agriculture and Forestry Predatorproof fencing has been used in approved the introduction of the Barn Owl to New Zealand for over a decade to wall-off help control rodents (Tomich 1962), but this problematic mammals (Scofield et al. 2011). measure largely failed despite Barn Owls con- More recently (within the last 3 yr), other Pa- suming many rats. Failed biocontrol attempts cific islands have begun to use predatorproof are worsened when the species introduced fencing to keep predators that are the size of ­becomes problematic for native species or M. musculus and larger out of natural and con- ­human health and safety (Pitt and Witmer servation areas. At Ka‘ena Point Natural Area 2007). For example, in contemporary Hawai‘i, Reserve on O‘ahu, the number of breeding the Barn Owl and mongoose are predators of pairs of some seabirds, such as the Laysan Al- some native birds (Funasaki et al. 1988, Hays batross (Phoebastria immutabilis), has appar- and Conant 2007; F. Duvall, pers. comm.). In ently increased by 15%, and Wedge-tailed addition, it is important to consider the eradi- Shearwater (Puffinus pacificus) chicks have tri- cation or control of introduced R. rattus from pled since the installation of the predator- a multitrophic-level perspective (e.g., ­Zavaleta proof fencing and the removal of introduced et al. 2001, Caut et al. 2009) because these rats R. rattus, M. musculus, mongoose, cats, and are highly integrated into the food web (Fig- dogs (Pala 2012). Often the individual im- ure 3) and consume both native and nonnative pacts of R. rattus are unknown or cannot be (in some cases highly invasive) organisms. In easily determined because methods of control some situations, removal of rats can have neg- (e.g., trapping, toxicants, rodentproof fences) ative repercussions by benefitting coexisting can apply to multiple invasive rodent species nonnative species (e.g., M. musculus, which is (e.g., mice, rats) and in many cases nonrodent often a competitor with R. rattus), and these species (e.g., mongoose, stoats). The cost-­ may include (1) extensive population growth, effectiveness of predatorproof fencing in New (2) equivalent or larger impacts than those of Zealand is commonly debated, and Scofield introduced R. rattus, and (3) greater difficulty et al. (2011) described the areas enclosed by of eradication relative to R. rattus (e.g., Cour- predatorproof fencing as large zoos that do champ et al. 1999, Zavaleta et al. 2001, Caut not allow population expansion and do not et al. 2007, Meyer and Shiels 2009). Pacific Island Invasive Species:Rattus rattus, the Black Rat · Shiels et al. 173

Dogs (Canis lupus familiaris) can be used to ing of the local food web will help reduce the detect rats on islands. To prevent rodent rein- chances of unexpected or negative conse- vasion of islands, parts of New Zealand utilize quences resulting from R. rattus removal (e.g., specially trained rat dogs to find introduced M. musculus population increases, which is Rattus spp. and M. musculus in conservation ­often a more difficult species to eradicate than areas and on cargo transported between ports R. rattus [Harper and Cabrera 2010]), as well and islands (Towns 2009, Gsell et al. 2010). as help guide actions that will minimize both Additional rat control methods that have been nontarget impacts and pollution from toxi- historically attempted to reduce rat popula- cants (Bowie and Ross 2006). Second, gaining tions include destroying habitat around agri- social acceptance for the campaign is often an cultural fields (Sugihara et al. 1977, Sugihara underestimated barrier to success; outreach 2002) and introducing viral diseases (Doty and education early in the campaign as well as 1945). clear articulation of the goals and expected ­responses of the local species should therefore be disclosed (Moors et al. 1992, Ogden and prognosis Gilbert 2009). Finally, it is critical to secure When R. rattus arrived on most Pacific is- posteradication funding and operational com- lands, there was probably at least one other mitments for biosecurity and reinvasion re- nonnative rat species present (most likely R. sponse. To ensure success, posteradication exulans); therefore, the magnitude of ecosys- monitoring and prevention of R. rattus rein- tem change resulting from R. rattus introduc- vasions must occur indefinitely. tion may have been less than if no other ­rodents had been present. However, contem- porary studies have indeed depicted R. rattus acknowledgments as the rodent species responsible for the most detrimental impacts on islands (Towns et al. We thank the following people for providing 2006, Jones et al. 2008, Ruffino et al. 2009, Rattus rattus body size data from islands Traveset et al. 2009). With a highly omnivo- throughout the Pacific: D. Balete, J. Baudat- rous diet (Figure 3), few organisms are safe Fanceschi, D. Buden, S. Caut, P. Dilks, R. from possible predation and/or indirect con- Dowler, F. Duvall, L. Faulquier, R. Fewster, S. Gregory, A. Gupta, G. Harper, D. Harris, sequences of R. rattus invasion. There are many factors that may affect the future distri- N. Holmes, K. Ishida, C.-C. Kuo, J. Lacoste, J. Lavers, L. Matisoo-Smith, G. McCormack, bution of R. rattus, including changes in land uses, climate, and additional ecological factors K. Nakata, M. Pascal, J. Penniman, R. Pierce, such as the changes in densities, distributions, R. Powlesland, O. Robinet, J. Russell, A. ­Samaniego-Herrera, K. Springer, H. Ste- and dominance of other invasive rodents, par- phens, D. Watling, A. Weiwel, A. Wegmann, ticularly M. musculus and R. norvegicus. Rattus and T. Yabe. We are also grateful for helpful rattus will almost certainly continue to nega- comments by D. Clements, D. Drake, D. tively affect the human food supply, spread Duffy, M. Fall, and M. Tobin on early ver- disease, and alter native ecosystems. sions of the manuscript. Increased rat control and eradications across larger insular areas are expected in the future as tools and technology continue to Literature Cited improve. To ensure that such control and eradication campaigns are of value and will Abe, T. 2007. Predator or disperser? A test of succeed, we first suggest that the conserva- indigenous fruit preference of alien rats tion, human health, or economic goals are (Rattus rattus) on Nishi-jima (Ogasawara clear and feasible before initiation of the Islands). Pac. Conserv. Biol. 13:213 – 218. ­campaign. Local field research is necessary to Abe, T., and H. Umeno. 2011. Pattern of twig identify species or ecosystem functions that cutting by introduced rats in insular cloud suffer impacts from R. rattus. An understand- forests. Pac. Sci. 65:27 – 39. 174 PACIFIC SCIENCE · April 2014

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