Introduction

Rats are a small species of mammals that occupy the lower trophic level of the food web, and are food sources for various predator species. Species of the genus Rattus living in Korea include R. norvegicus, R. rattus, and R. tanezumi (Jo et al., 2018). In particular, R. norvegicus (called the brown rat or Norway rat) is a relatively large species of the genus Rattus, with a total length of 302-355 mm, tail length of 140-167 mm, and weight of approximately 90-500 g. Brown rats are present nationwide, in habitats including islands, farmlands, and forests (Jo et al., 2018). Kang et al. (2008) and Oh et al. (2008) also observed them on islands. Brown rats are omnivorous and have a lifespan of four years in captivity or only 1-2 years in the wild.

According to the IUCN Red List, the Chinese crested tern (Thalasseus bersteini) is an extremely rare and globally critically endangered species. This species is listed as “Critically Endangered (CE)” on the IUCN Red List, and the surviving population is estimated to consist of approximately 30-49 individuals (BirdLife International, 2021). Prior to the discovery of a breeding site on the western coast of South Korea, the only known breeding sites were in China (Jiushan and Wuzhishan) and Taiwan (Matzu and Penghu Islands) (Chen et al., 2009). Currently, five described breeding sites remain (Song et al., 2017). Historically, the breeding populations in China have been pushed to the brink of extinction due to egg poaching, breeding failure due to typhoons, marine pollution, and hybridization with the Great crested tern (Chan et al., 2010). Yuksan Island, Korea, was declared a marine sanctuary (Natural Monument No. 389) to protect the breeding grounds of endangered marine bird species. Moreover, it was declared a Specified Island (No. 239) after Chinese crested tern breeding was confirmed during a census to investigate the natural habitats of uninhabited islands. In addition, the breeding period (late March-early July) of Chinese crested terns does not overlap with the typhoon season, which greatly reduces the risk of natural hazards (Ministry of Environment, National Institute of Ecology, 2019). Furthermore, the breeding colony of the Chinese crested terns being located close to breeding colonies of the distant Black-tailed gulls (Larus crassirostris) suggests a low risk of hybridization. Hybridization is known to be a great risk to Chinese and Taiwanese Chinese crested tern populations, but it does not seem to be significantly important to the South Korean population. However, Yuksan Island may have different risk factors for this species. Therefore, research and monitoring of the factors influencing the breeding of avian species on this island are of crucial importance.

Generally, goats, rabbits, felines, and rodents may threaten the breeding grounds of avian species (Russel & Le Corre, 2008). In particular, the impact of rodents has frequently been reported in the literature (Jones et al., 2008; Lee & Yoo, 2002). Previous censuses reported that the population size of brown rats (R. norvegicus) is approximately 50-100 (Cultural Heritage Administration, 2004) on Yuksan Island, the only breeding site of the Chinese crested tern in South Korea. Hence, the presence of brown rats may threaten the breeding of Chinese crested terns in South Korea. The impact of rodents on marine birds has been investigated from various perspectives (Howald et al., 2007; Møller, 1983; Towns et al., 2006). For example, on Sasu Island in South Korea, the presence of brown rats accounts for 85% of all hatching failures in the Streaked shearwater (Calonectris leucomelas) (Nam et al., 2014). However, it has also been reported that gulls (Larus spp.) may feed on rodents; thus, it is even more necessary to elucidate the prey–predator relationship between Chinese crested terns and brown rats on Yuksan Island. Moreover, Jones et al. (2008) reported that small species within the Hydrobatidae, or even smaller species, and especially burrow-nesting species, may be largely influenced by rodents, whereas larger species within the Laridae and ground-nesting species may be less influenced. The Chinese crested tern is a ground-nesting species, but it is smaller than many other species belonging to the Laridae family, making it potentially vulnerable to the presence of brown rats.

Atoms consist of neutrons, protons, and electrons, with neutrons and protons tending to exist in identical quantities. However, some atoms have one more neutron than protons, known as isotopes. There are two different types of isotopes: radioisotopes, with radioactivity, and stable isotopes, such as C, N, O, and P, which are used in stable isotope analyses and tend to have one more neutron than the number of protons. Owing to these characteristics, stable isotopes may accumulate within organisms during activity. Stable isotopes (e.g., ¹³C and ¹²C), which are constantly used during biological activities and are also absorbed from food sources, have been shown to have similar ratios across organisms that are in prey–predator relationships. Empirical studies using stable isotope analyses for food source analyses have been performed (Hong et al., 2016; Major et al., 2007; Tabak et al., 2016). In the case of ¹⁵N, which is depleted less during feeding activities than C and consequently accumulates, it has been shown that predators have higher nitrogen values than their prey; thus, it is a highly valuable stable isotope in studies on prey–predator relationships. In this study, we predicted the carbon sources of terrestrial and marine ecosystems would be different, and that we would be able to determine whether the brown rat feeds on birds or eggs through the ¹³C level.

This study aimed to assess the potential threats that brown rats may pose to the Chinese crested tern by investigating the population status and feeding behavior of brown rats on Yuksan Island, and determine the carbon source of the food sources of the brown rat by conducting stable isotope analysis.

Materials|Methods

Results

Discussion

This study analyzed factors that may threaten the breeding of avian species, including the globally endangered Chinese crested tern. In particular, brown rats inhabiting Yuksan Island may directly threaten the breeding of avian species; therefore, the breeding and feeding status of these brown rats should be thoroughly monitored for the management of Yuksan Island. For this purpose, we investigated the distribution of brown rat burrows in the field and sampled brown rat tissues, as well as edible plant and animal materials that may serve as food sources for brown rats, to conduct stable isotope analyses. We used the tail bones of the rats to determine their main food source. The avian species breeding on Yuksan Island stay for about half a year, while rats have a lifespan of 1-2 years; hence, about half of their lives overlaps with the avian species’ presence on the island. Thus, this duration may be considered sufficient for stable isotopes from avian species to accumulate in rat bones.

Additionally, we analyzed undigested food sources from the fecal samples under a microscope.

From the ¹³C values that provided information on the food source, which we separated into terrestrial and marine ecosystem sources, we deduced that brown rats mainly relied on food sources taken from the terrestrial environment, such as insects and flowering Indian goosegrasses, which had similar ¹³C values of –16‰ to –11‰. The ¹³C value of the Black-tailed gull, which we expected to feed on items obtained from the marine ecosystem, was approximately –22‰ to –18‰ (Table 2). Insects and flowering Indian goosegrasses are not in direct prey–predator relationships with Black-tailed gulls and Chinese crested terns, which feed on items obtained from the marine environment. A few rats had a similar carbon level to black-tailed gulls, but the possibility that they fed on similar food sources taken from the marine environment (e.g., stranded fish brought in by waves) is higher than the possibility that rats fed directly on Black-tailed gulls or Chinese crested terns. The stable isotope values from the bone of the tip of the tail in the rats were approximately –11.5‰ and –13.08‰. These values were even more different to those of Black-tailed gulls.

The ¹⁵N value of the plant material, which was supposed to be a producer at the bottom of the food chain, was even higher than that of the Black-tailed gull, which is a predator. This difference may have been due to the sampling period. The flowering period of Indian goosegrass is two months after Black-tailed gulls leave their breeding sites; hence, the guano is absorbed by the soil and the nitrogen level of the soil is the highest. The seeds of the plants were more nutritious than the bodies, and their constituents differed greatly. They accumulate nitrogen to sprout; therefore, it could be deduced that the nitrogen level of the plant material was the highest during this period. Generally, the ¹⁵N value of plant material from terrestrial ecosystems does not exceed 10 (Chahartaghi et al., 2005). In this study, we found that the ¹⁵N values of plants exceeded 18 (Craine et al., 2015; Xu et al., 2010; Yan et al., 2020). This may be due to external factors enriching the nitrogen of the soil on this island, such as the guano of Black-tailed gulls. The study site, Yuksan Island, is the breeding site of approximately 30,000 Black-tailed gulls that feed on items obtained from the marine environment over a relatively long period; hence, the guano of the Black-tailed gulls likely enriches the ¹⁵N values of the soil on this island. Plant material rarely leaves the island, but the external factors enriching nitrogen are maintained constantly, and very little nitrogen is washed away by rainwater.

To confirm the results obtained by our stable isotope analysis, we examined the undigested food sources within the fecal samples of brown rats (Fig. 3). Much of the undigested food consisted of plant material, such as plant seeds, and the proportion of animal matter, such as insects, was relatively low. Considering that food sources found in fecal samples are the remaining undigested, low-quality parts of the initial food consumed, this cannot be considered an absolute result, but is rather a supplement adding to the results of our stable isotope analysis. Feeding conditions of live organisms are determined by nutrition, handling time, and frequency (Pulliam, 1974). As high-quality food sources of animal matter are scarce on the island, brown rats seemed to have fed more frequently on the readily available plant materials. Moreover, due to the length of the gut and the short digestion time of the rat, they probably cannot digest and absorb all plant materials readily, which may explain the high content of undigested plant material in the feces.

Research on food sources and chains always entails certain types of errors. Regardless of whether the intake of certain food sources was high or not, if it was easily digested, it may not have been observed in fecal samples. In addition, even if the intake was low, hardy sources could pass through without being digested, and therefore may impart bias upon the main food source. To account for such limitations, we conducted stable isotope analysis, but it was not feasible to collect sufficient samples of all plant and animal species inhabiting the island due to its characteristics. A future study including sufficient samples of algae and fish species from the marine ecosystem will be able to provide a much clearer result.

In conclusion, contrary to our hypothesis that brown rats would feed on birds and eggs, which are excellent sources of protein, we found that there was no direct effect of brown rats on avian species. However, this study was limited to a small set of food sources, which may have imposed a bias. Therefore, future studies considering a wider array of samples, including plant and animal species inhabiting both the terrestrial and marine ecosystems of this island, will be necessary to assess the impact of brown rats on the breeding colony of avian species. Furthermore, environmental factors may push brown rats to change their feeding behavior, rendering it even more crucial to continue monitoring them.