Niche Partitioning Based on Diet Analysis of Three Introduced Rodents

CHAPTER THREE: NICHE PARTITIONING BASED ON DIET ANALYSIS OF THREE INTRODUCED RODENTS IN HAWAIIAN MONTANE FOREST Aaron B. Shiels Department of Botany University of Hawaii at Manoa 3190 Maile Way Honolulu, HI. 96822 93 Abstract Determining the diets of sympatric rodents can uncover patterns of resource partitioning and competitive interactions. Prey items that appear in the stomachs of introduced rodent predators can provide insight into trophic divisions and disruptions and help to assess the vulnerability of native prey. In the Hawaiian Islands, where rodents were absent prior to human arrival ca. 1000 years ago, three rodents (Rattus rattus or black rat, Rattus exulans or Pacific rat, Mus musculus or house mouse) are common to forests and are voracious predators of plants and animals. These three rodents were trapped in mesic montane forest from February 2007 to September 2009 to determine their short-term diet by analyzing stomach contents and their long-term (life-time) diets by extracting bone collagen for δ15N and δ13C isotopic analysis. For all three rodents > 75% of individuals had plants and > 90% had arthropods in their stomachs. Mean relative abundance of the major items in stomachs was 81% plant and 14% arthropod for black rats, 60% plant and 38% arthropod for Pacific rats, and 36% plant and 57% arthropod for mice. Rodents may be dispersing some native and non-native seeds, including the highly invasive Clidemia hirta, because intact seeds were found in some of the stomachs of all three species. Fruit pulp comprised 55% of the black rat diet, 41% of the Pacific rat diet, but only 11% of the house mouse diet. Caterpillars were particularly common in Pacific rats and mice, and aside from a native spider, a cricket, and two species of beetle, the majority of identifiable arthropods in all three rodents were non- native species. None of the stomachs contained evidence of birds, snails, or lizards, all of which are common at the study site. The δ15N and δ13C signatures revealed that the Pacific rat and house mouse occupy the same trophic level, whereas the slightly lower 94 δ15N values of black rats reflect a proportionally more vegetarian diet compared to the two smaller rodents. Therefore, the strongest evidence of food resource portioning among the three rodents is between the black rat and house mouse; the Pacific rat has an intermediate diet that partly overlaps with the two other rodent species. Introduction How closely related species coexist in a community has long intrigued ecologists. Numerous factors influence a species niche, including biotic and abiotic attributes, resource use, and competition (Elton 1927; Hutchinson 1957). Niche partitioning reflects competitive interactions among species and can be determined by diet analysis of sympatric animals (Biró et al. 2005; Purnell et al. 2006). Animals with similar life- history traits and close phylogenetic associations, such as different species of rodents in the same habitat, must partition resources across time and space in order to coexist (Gause 1934). Introduced animals can disrupt food webs by consuming native prey and by altering the niches of native competitors (Fritts and Rodda 1998; Fukami et al. 2006). Identifying prey consumed by introduced predators provides insight into native species‘ vulnerability and can help improve strategies of native and non-native species management (Stapp 2002; Caut et al. 2008a). Rodents (Rattus rattus or the black rat or ship rat, R. norvegicus or the Norway rat, R. exulans or the Pacific rat or Polynesian rat, and Mus musculus or the house mouse) are omnivorous predators that have been introduced to many ecosystems worldwide and are among the most widespread and problematic invasive animals affecting islands (Towns et al. 2006; Angel et al. 2009; 95 Drake and Hunt 2009). Introduced rodents may consume a wide variety of prey, including plants (e.g., fruits, seeds, vegetative material) and animals (e.g., arthropods, mollusks, birds; Sugihara 1997; Campbell and Atkinson 2002; Stapp 2002), and their diets can shift depending upon a number of factors, including the availability of food items, the chemical and nutritional quality of the food items, and the rodents‘ competitive ability relative to other animals that coexist in the environment (Clark 1982). Predation by introduced rodents is rarely observed directly, perhaps because they are nocturnal and often forage in the canopy or burrow belowground (Lindsey et al. 1999; Towns 2009). Consequently, field observations of partially consumed prey items (e.g., seeds, mollusks, arthropods; Norman 1970; Campbell et al. 1984; McConkey et al. 2003) or captive-feeding trials (Williams et al. 2000; Pérez et al. 2008; Meyer and Shiels 2009) have been used to determine the species suffering from predation by introduced rodents. Additionally, stomach content analysis has been used to identify rodent‘s prey and assess their diets (e.g., Clark 1982) despite this method reflecting one to a few meals. Stable isotopes (δ15N and δ13C) have been widely used to determine the trophic levels at which animals have fed during tissue development (Peterson and Fry 1987; Lajtha and Michener 1994); however, interpretations of diet using stable isotopes are restricted by the tissue type analyzed and tissue turnover rates. For example, liver tissue has a higher turnover rate than blood cells or muscle, and bone collagen is deposited and reworked during the lifetime of an animal, so its isotopic values represent a long-term average of an animal‘s diet (Lajtha and Michener 1994; Caut et al. 2008b). The difference in isotopic composition between a predator and its prey (discrimination values) is presumed to average ca. 3‰ and 1‰ for δ15N and δ13C, respectively; however, the 96 discrimination values can differ widely depending on the species of prey involved, as demonstrated by Post (2002) where the majority of the δ15N discrimination values in lake organisms were 2-4.5‰, and Caut et al. (2008c) determined from lab trials that the δ15N discrimination values for black rats ranged from -1.46‰ to 4.59‰. Applying isotope mixing models enables quantification of each prey item‘s contribution to a predator‘s diet (Phillips and Gregg 2003). However, without isotopic signatures for all prey items consumed by the predator, collected from the specific habitat of the predator (Flaherty and Ben-David 2010), interpretations of mixing models can be problematic (Martínez del Rio et al. 2009). Combining δ15N and δ13C to assign trophic-level feeding of coexisting predators and prey (Peterson and Fry 1987; Lajtha and Michener 1994) with stomach content analysis of predators can provide an understanding of the diet and trophic level occupancy of similar, coexisting predators. In the Hawaiian Islands the first rodents (the Pacific rat) arrived with humans ca. 1000 years ago (Athens et al. 2002), and later arrival of two additional rats (the Norwary rat and the black rat) and the house mouse occurred upon European settlement ca. 230 years ago (Tomich 1986). In contemporary Hawaii, the Norway rat has rarely been found in forests. The black rat appears to be the most common rat in forests, and both black rats and mice are distributed from sea level to nearly 3000 m (Amarasekare 1994; Lindsey et al. 1999; unpublished data). The Pacific rat is the smallest of the three introduced rats and may be outcompeted in many environments in Hawaii and other Pacific islands by the European-introduced rats (Russell and Clout 2004). Similarly, the house mouse may be suppressed by all three introduced rats (Russell and Clout 2004; Angel et al. 2009), such as in New Zealand where mice are rarely known to occur where Pacific rats are 97 present (Yom-Tov et al. 1999; Ruscoe and Murphy 2005). It has been established that these introduced rodents consume plants and animals in Hawaii, as evidenced by field trials (VanderWerf 2001; Shiels and Drake, in press), captive feeding trials (Pérez et al. 2008; Meyer and Shiels 2009; Shiels, in press), and two high elevation studies that analyzed stomach contents (Sugihara 1997; Cole et al. 2000). However, the short- and long-term diets and potential resource partitioning of three introduced rodent species has not been established in Hawaii or elsewhere. The objectives of this study are to 1) determine the short- and long-term diets of black rats, Pacific rats, and mice where they coexist in mesic montane forest in Hawaii, 2) identify some of the native and non-native prey species that are vulnerable to these three rodents, 3) determine if there is evidence of niche partitioning that may result from differential feeding and trophic level occupancy for each of the three rodent predators relative to their dominant prey. Methods Study site Rodents were obtained from Kahanahaiki Management Unit (21o 32′ N, 158o 11′ W), a 36 ha segment of mesic forest in highly dissected terrain (500-660 m a.s.l; Gagné and Cuddihy 1999) in the northern Waianae Mountains, on the island of Oahu, Hawaii. Kahanahaiki is managed for native species preservation by the U.S. Army, and the forest was fenced in 1996 to exclude feral goats and pigs. Daily air temperature at the site ranges from 16-24oC (unpublished data) and monthly rainfall varies from 50 mm to 170 mm (cited in Joe and Daehler 2008). 98 Two species of rats, the black rat (133 ± 3 g; mean ± SE) and Pacific rat (47 ± 2 g), and the house mouse (10 ± 1 g) are present at Kahanahaiki (Meyer and Shiels 2009; Shiels and Drake, in press). Average estimated relative abundance measures using bi- monthly mark-and-recapture sampling over 15 months during 2007-2008 were 17 indiv./100 trap nights for black rats and 1 indiv./100 trap nights for Pacific rats. No Norway rats were captured at the study site and the house mouse was captured at ca.

Load more