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Competitive exclusion of a burying beetle by mongoose

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Abstract

Competitive exclusion, a mechanism for local extinction of organisms, has been well established among taxonomically related species, including those within the same genus, family, or class in animal communities. This study, however, focuses on competitive exclusion that occurs across phyla, exemplified by the exclusion of a native insect by an invading exotic mammal, where food resources overlap. The hypothesis proposed in this study is that the small Indian mongoose (Urva auropunctata) has caused the local extinction of a burying beetle (Nicrophorus nepalensis) on Okinawa Is., Japan due to competition for carcasses of small vertebrates. To test this hypothesis, a comparison of beetle abundance was conducted between the area intensively controlled for mongoose and the area where mongoose control was weak or nonexistent. The former situated north of the boundary to prevent mongoose from crossing, and the latter located south of the boundary. To determine the user of carcasses on the forest floor, mouse carcasses were laid and their consumers were observed in each area. The results showed that the beetle abundance was clearly higher in the former than in the latter, and no beetles were collected where mongoose have never been controlled. The beetles often buried the mouse carcasses for their reproduction in the former, whereas in the latter, mongoose frequently consumed the mouse carcasses. These results provide evidence of competitive exclusion of the burying beetle by mongoose. This conclusion represents the first demonstration of competitive exclusion across phyla in an animal community.

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All data are available in Figshare at https://doi.org/10.6084/m9.figshare.22339693.

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References

  • Abe S (1992) What does mongoose feed on Amami-Oshima Is.? Chirimos 3:1–18 (in Japanese)

    Google Scholar 

  • Abernethy EF, Turner KL, Beasley JC et al (2016) Carcasses of invasive species are predominantly utilized by invasive scavengers in an island ecosystem. Ecosphere 7(10):1–15

    Article  Google Scholar 

  • Attisano A, Kilner RM (2015) Parental effects and flight behaviour in the burying beetle, Nicrophorus vespilloides. Anim Behav 108:91–100

    Article  PubMed  PubMed Central  Google Scholar 

  • Barun A, Simberloff D, Budinski I (2010) Impact of the small Indian mongoose on native amphibians and reptiles of the Adriatic islands, Croatia. Anim Conserv 13:549–555

    Article  Google Scholar 

  • Berentsen AR, Pitt WC, Sugihara RT (2017) Ecology of the small Indian mongoose (Herpestes auropunctatus) in North America. In: Pitt WC, Beasley J, Witmer GW (eds) Ecology and management of terrestrial vertebrate invasive species in the United States. CRC Press, Baca Raton, pp 251–267

    Chapter  Google Scholar 

  • Bøhn T, Amundsen PA, Sparrow A (2008) Competitive exclusion after invasion? Biol Invas 10:359–368

    Article  Google Scholar 

  • Branch TA, Lob AS, Purcell SW (2013) Opportunistic exploitation: an overlooked pathway to extinction. Trends Ecol Evol 28:409–441

    Article  PubMed  Google Scholar 

  • Brown JH, Davidson DW (1976) Competition between seed-eating rodents and ants in desert ecosystems. Science 196:880–882

    Article  Google Scholar 

  • Creighton JC, Schnell GD (1988) Short-term movement patterns of the endangered American burying beetle Nicrophorus americanus. Bio Conserv 86:281–287

    Article  Google Scholar 

  • Funakoshi K, Arai A, Yamasita K et al (2012) Food habits of the small Indian mongoose Herpestes auropunctatus in Kagoshima City, Japan. Mammal Sci 52(2):157–165 (in Japanese with English summary)

    Google Scholar 

  • Gause GF (1936) The principles of biocoenology. Quart Rev Biol 11:320–336

    Article  Google Scholar 

  • Grogan J, Blundell AG, Landis RM et al (2010) Over-harvesting driven by consumer demand leads to population decline: big-leaf mahogany in South America. Conserv Let 3:12–20

    Article  Google Scholar 

  • Hardin G (1960) The competitive exclusion principle: an idea that took a century to be born has implications in ecology, economics, and genetics. Science 131:1292–1297

    Article  PubMed  CAS  Google Scholar 

  • Hays WST, Conant S (2007) Biology and impacts of Pacific Island invasive species. 1. A worldwide review of effects of the small Indian mongoose, Herpestes javanicus (Carnivora: Herpestidae). Pacific Sci 61:3–16

    Article  Google Scholar 

  • Karatayev AY, Burlakova LE, Karatayev VA et al (2009) Introduction, distribution, spread, and impacts of exotic freshwater gastropods in Texas. Hydrobiologia 619:181–194

    Article  Google Scholar 

  • Kurosawa Y (1980) A first record of a silphid beetle in Japan (2). Coleopterists’ News 50:14 (in Japanese)

    Google Scholar 

  • Lowe S, Browne M, Boudjelas S et al (2000) 100 of the World’s worst invasive alien species: a selection from the global invasive species database. Invasive Species Specialist Group, Auckland

  • Mauerhofer V, Ichinose T, Blackwell BD et al (2018) Underuse of social-ecological systems: a research agenda for addressing challenges to biocultural diversity. Land Use Policy 72:57–64

    Article  Google Scholar 

  • Microsoft (2019) Microsoft Excel for Mac ver. 16.51

  • Ogura G, Sasaki T, Toyama M et al (2002) Food habits of the feral small Asian mongoose (Herpestes javanicus) and impacts on native species in the northern part of Okinawa Island. Mammal Sci 41(2):53–62 (in Japanese with English summary)

    Google Scholar 

  • Okinawa-Amami Natural Environment Office (2021) Information of results of mongoose control program in north area of Okinawa Island in 2020 and plan for 2021. https://kyushu.env.go.jp/okinawa/pre_2021/20202021.html Accessed 17 Feb 2023 (in Japanese)

  • Ozaki K, Baba T, Komeda S et al (2002) The declining distribution of the Okinawa rail Gallirallus okinawae. J Yamashina Inst Ornithol 34:136–144 (in Japanese with English abstract)

    Article  Google Scholar 

  • Parmesan C (1996) Climate and species’ range. Nature 382:765–766

    Article  CAS  Google Scholar 

  • Porter SD, Sagivnano DA (1990) Invasion of polygyne fire ants decimates native ants and disrupts arthropod community. Ecology 71:2095–2106

    Article  Google Scholar 

  • Pukowski E (1933) Okologische Untersuchungen an Necrophorus F. Zeit Morph Oecol 27:518–586

    Google Scholar 

  • Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Ann Rev Ecol Evol Syst 27:83–109

    Article  Google Scholar 

  • Russell RW, Hecnar SJ, Haffner GD (1995) Organochlorine pesticide residues in Southern Ontario spring peepers. Environ Toxicol Chem 14:815–817

    Article  CAS  Google Scholar 

  • SAS Institute (2009) JMP 8 ver 8.0.1

  • Schloegel LM, Berger L, Speare R (2006) The decline of the sharp-snouted day frog (Taudactylus acutirostris): the first documented case of extinction by infection in a free-ranging wildlife species? EcoHealth 3:35–40

    Article  Google Scholar 

  • Springett BP (1968) Aspects of the relationship between burying beetles, Necrophorus spp. and the mite, Poecilochirus necrophori Vits. J Anim Ecol 37:417–424

    Article  Google Scholar 

  • Ueda A (2019) Seasonal changes in beetles collected by carrion traps in Yambaru, Okinawa Island. Kyushu J Forest Res 72:43–46 (In Japanese)

    Google Scholar 

  • Ueda A, Sato S (2020) Preliminary study of assemblages of carrion silphid and dung beetles in a forest consisting of small, different-aged, different-tree species stands in Sapporo. Boreal Forest Res 68:11–15 (in Japanese)

    Google Scholar 

  • Ueda A, Tone T, Sano M (2016) Assemblages of carrion beetles (Silphidae and coprophagous group of Scarabaeoidea) in Okinawa City and Nago City and their seasonal changes. Kyushu J Forest Res 69:53–57 (in Japanese)

    Google Scholar 

  • Vayreda J, Martinez-Vilalta J, Gracia M et al (2016) Anthropogenic-driven rapid shifts in tree distribution lead to increased dominance of broadleaf species. Global Change Biol 22:3984–3995

    Article  Google Scholar 

  • Watari Y, Takatsuki S, Miyashita T (2008) Effects of exotic mongoose (Herpestes javanicus) on the native fauna of Amami-Oshima Island, southern Japan, estimated by distribution patterns along the historical gradient of mongoose invasion. Biol Invas 10:7–17

    Article  Google Scholar 

  • Williams NSG, Morgan JW, McCarthy MA et al (2006) Local extinction of grassland plants: the landscape matrix is more important than patch attributes. Ecology 87:3000–3006

    Article  PubMed  Google Scholar 

  • Wood C, Qiao Y, Ding PL et al (2010) Implications of rice agriculture for wild birds in China. Waterbirds 33:30–43

    Article  Google Scholar 

  • Yagihashi T, Seki SI, Nakaya T et al (2021) Eradication of the mongoose is crucial for the conservation of three endemic bird species in Yambaru, Okinawa Island, Japan. Biol Invas 23:2249–2260

    Article  Google Scholar 

  • Yamamoto K (2008) LIA32 ver.0.378. URL: http://www.agr.nagoya-u.ac.jp/~shinkan/LIA32 Accessed 12 Sep 2014 (in Japanese)

  • Yambaru Wildlife Conservation Center (2023) Protect the nature of Yambaru. https://www.ufugi-yambaru.com/save/alien Accessed 25 Jan 2023 (in Japanese)

  • Young OP (2014) Vertebrate predation on Silphidae (Coleoptera): a literature review. Coleopt Bull 68:221–234

    Article  Google Scholar 

Download references

Acknowledgments

I thank Rob Johns (Atlantic Forestry Centre, Canadian Forest Service) for his review of the manuscript. I would like to express my gratitude to the following organizations and individuals for their assistance with this study: the officials at Yambaru Nature Ranger Office of the Ministry of the Environ. (YN); the Yona Field of Ryukyu Univ. (RU); the Forest Resources Res. Ctr. (FRR) of Okinawa Pref. Gov. (OPG); Nago Branch of Agri. Res. Ctr. of OPG, Kenmin-no-Mori of OPG; the Fishery and Forestry Dept. of OPG; public offices of Kunigami, Ogimi, and Nago; the Forestry Union of Kunigami. Additionally, I would like to extend my thanks to Koji Ono, Katsushi Nakata (YN), Daijiro Kamiya (OPG), Takami Kudo, Takashi Takashima (RU), Takuya Aragaki, Hioroshi Furugen (FRR), Nobuyuki Asai (Kunigami), Koichi Tone, Masakazu Sano (Okinawa Municipal Museum), Noriaki Goto (Onna Village Museum), Nobuhiko Kotaka, Hideaki Goto (FFPRI), Masahiro Ohara, Mariko Shizuki (The Hokkaido Univ. Museum), Munetoshi Maruyama (The Kyushu Univ. Museum) for their contributions to the study. Finally, I would like to acknowledge the support of JSPS KAKENHI grant number 17K07864 for this study.

Funding

JSPS KAKENHI Grant Number 17K07864.

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Correspondence to Akira Ueda.

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Appendices

Appendix 1

See Fig. 6.

Fig. 6
figure 6

Fish-baited hanging trap to collect Nicrophorus nepalensis

The trap consisted of a plastic cup (95 mm in open diameter and 170 mm high) with four 2 mm diameter holes for drainage on the side (50 mm from the top). The cup contained 150 ml propylene glycol and a small plastic cup (42 mm in open diameter and 35 mm high) was fixed to its upper lip with steel wire. Another small plastic cup, containing 15 g of mackerel (Scomber spp.) meat with a perforated lid (having 25 holes, each 1 mm in diameter), was placed into the suspended cup. The trap was hung 100 mm beneath a white plastic plate (230 mm diameter and 20 mm high) using four steel wires to prevent rainwater from entering. The trap mechanism was hung from a tree branch, utilizing fishing line at an approximate height of 1.2 m. Three of the four wires that held the trap were fastened to nearby tree trunks using the fishing line to prevent the trap from rolling.

Appendix 2

See Fig. 7.

Fig. 7
figure 7

Mechanism for the observation of consumers of mouse carcasses

Two mouse carcasses were used for the observation, with one placed under a steel rack (405×250 mm, 30 mm high) weighed down with a concrete block (390×190 mm, 120 mm high, 11.3 kg) to prevent interference from animal scavengers. For the observations made south of the SF line, the mouse was placed at the center of a plastic bowl (265 mm diameter and 115 mm high), with the bottom of the bowl removed and the bowl buried in the ground, in order to prevent animals from digging to reach the mouse. The hind leg of the mouse was tied to the steel rack with dental floss measuring approximately 40 cm in length to track the position of the mouse buried by N. nepalensis. The other mouse was also tied to the steel rack and placed beside it without cover. An infrared sensor camera with interval photographing capabilities (Ltl-6210MC, Ltl Acorn®) was placed near the mouse carcasses, with the interval period set to every 60 min.

Appendix 3

See Fig. 8.

Fig. 8
figure 8

A mouse carcass buried and processed by Nicrophorus nepalensis (a), and the adult and larvae in a processed mouse carcass (b)

Appendix 4

See Fig. 9.

Fig. 9
figure 9

A mongoose shortly before consuming a mouse carcass without the cover (a) and another that is attempting to consume a mouse carcass with the cover (b)

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Ueda, A. Competitive exclusion of a burying beetle by mongoose. Biol Invasions 26, 605–617 (2024). https://doi.org/10.1007/s10530-023-03195-0

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