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Tonic immobility in a marine isopod: the effects of body size, sex, and colour morph

Published online by Cambridge University Press:  01 March 2024

Koichi Igarashi Open the ORCID record for Koichi Igarashi [Opens in a new window]  and
Satoshi Wada Open the ORCID record for Satoshi Wada [Opens in a new window]
Koichi Igarashi*
Affiliation:
Laboratory of Marine Biology, Graduate School of Fisheries Sciences, Hokkaido University, Minato-cho 3-1-1, Hakodate, Hokkaido 041–8611, Japan
Satoshi Wada
Affiliation:
Laboratory of Marine Biology, Graduate School of Fisheries Sciences, Hokkaido University, Minato-cho 3-1-1, Hakodate, Hokkaido 041–8611, Japan
*
Corresponding author: Koichi Igarashi; Email: igapi.xxx@gmail.com
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Abstract

Tonic immobility is considered an anti-predator defence, wherein prey adopts a motionless state in a characteristic posture elicited by external stimuli. The marine isopod Cleantiella isopus exhibits tonic immobility with an arch-like posture and motionless state lasting several seconds or minutes in response to external stimuli such as predatory attacks by fish. In this study, we describe tonic immobility by wild-caught C. isopus and examine the influence of body size, sex, and colour morph on the frequency and duration of tonic immobility. All individuals exhibited tonic immobility regardless of body size, sex, or colour morph, suggesting that the behaviour plays a major role in predator avoidance following detection by a predator. In males, smaller individuals exhibited more prolonged tonic immobility than larger individuals, whereas the relationship between the duration of tonic immobility and body size was unclear in females. Colour morph had no effect on the duration of tonic immobility. These findings provide a detailed documentation of tonic immobility in C. isopus and suggest that the factors affecting tonic immobility differ between males and females.

Keywords

anti-predator behaviourbody sizedeath feigningmarine isopodthanatosistonic immobility
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 104 , 2024 , e17
Copyright
Copyright © The Author(s), 2024. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

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References

Aguilera, MA, Weiß, M and Thiel, M (2019) Similarity in predator-specific anti-predator behavior in ecologically distinct limpet species, Scurria viridula (Lottiidae) and Fissurella latimarginata (Fissurellidae). Marine Biology 166, 1–13.Google Scholar
Bach, C and Hazlett, B (2010) Individuality in the predator defense behaviour of the crab Heterozius rotundifrons. Behaviour 147, 587–597.Google Scholar
Bergey, L and Weis, JS (2006) Immobility in five species of fiddler crabs, genus Uca. Journal of Crustacean Biology 26, 82–84.Google Scholar
Brooks, ME, Kristensen, K, van Benthem, KJ, Magnusson, A, Berg, CW, Nielsen, A, Skaug, HJ, Maechler, M and Bolker, BM (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. The R Journal 9, 378–400.Google Scholar
Cazzolla Gatti, R, Messina, G, Tiralongo, F, Ursino, LA and Lombardo, BM (2020) Learning from the environment: how predation changes the behavior of terrestrial Isopoda (Crustacea Oniscidea). Ethology Ecology & Evolution 32, 29–45.Google Scholar
Christy, JH, Goshima, S, Backwell, PR and Kreuter, TJ (1997) Nemertean predation on the tropical fiddler crab Uca musica. Hydrobiologia 365, 233–239.Google Scholar
Coutinho, C, Ayres-Peres, L, Araujo, PB, Jara, CG and Santos, S (2013) Thanatosis in freshwater anomurans (Decapoda: Aeglidae). Journal of Natural History 47, 2623–2632.Google Scholar
Endler, JA (1986) Defense against predation. In Federand, ME and Lauder, GV (eds), Predator-Prey Relationships: Perspective and Approaches From the Study of Lower Vertebrates. Chicago: University of Chicago Press, pp. 109–134.Google Scholar
Farkas, TE (2016) Body size, not maladaptive gene flow, explains death-feigning behaviour in Timema cristinae stick insects. Evolutionary Ecology 30, 623–634.Google Scholar
Field, LH (1990) Aberrant defense displays of the big-handed crab, Heterozius rotundifrons (Brachyura: Belliidae). New Zealand Journal of Marine and Freshwater Research 24, 211–220.Google Scholar
Fox, J and Weisberg, S (2019) An R Companion to Applied Regression. Thousand Oaks CA: Sage Publications.Google Scholar
Franke, HD, Gutow, L and Janke, M (2007) Flexible habitat selection and interactive habitat segregation in the marine congeners Idotea baltica and Idotea emarginata (Crustacea, Isopoda). Marine Biology 150, 929–939.Google Scholar
Hazlett, BA and McLay, C (2000) Contingencies in the behaviour of the crab Heterozius rotundifrons. Animal Behaviour 59, 965–974.Google Scholar
Hazlett, BA and McLay, C (2005) Responses to predation risk: alternative strategies in the crab Heterozius rotundifrons. Animal Behaviour 69, 967–972.Google Scholar
Hazlett, BA, Bach, CE, McLay, C and Thacker, RW (2000) A comparative study of the defense syndromes of some New Zealand marine Crustacea. Crustaceana 73, 899–912.Google Scholar
Honma, A, Oku, S and Nishida, T (2006) Adaptive significance of death feigning posture as a specialized inducible defence against gape-limited predators. Proceedings of the Royal Society B: Biological Sciences 273, 1631–1636.Google Scholar
Hozumi, N and Miyatake, T (2005) Body-size dependent difference in death-feigning behavior of adult Callosobruchus chinensis. Journal of Insect Behavior 18, 557–566.Google Scholar
Hultgren, KM and Mittelstaedt, H (2015) Color change in a marine isopod is adaptive in reducing predation. Current Zoology 61, 739–748.Google Scholar
Humphreys, RK and Ruxton, GD (2018) A review of thanatosis (death feigning) as an anti-predator behaviour. Behavioral Ecology and Sociobiology 72, 1–16.Google Scholar
Jormalainen, V and Merilaita, S (1995) Female resistance and duration of mate-guarding in three aquatic peracarids (Crustacea). Behavioral Ecology and Sociobiology 36, 43–48.Google Scholar
Jormalainen, V and Tuomi, J (1989) Sexual differences in habitat selection and activity of the colour polymorphic isopod Idotea baltica. Animal Behaviour 38, 576–585.Google Scholar
Krams, I, Kivleniece, I, Kuusik, A, Krama, T, Freeberg, TM, Mänd, R, Vrublevska, J, Rantala, MJ and Mänd, M (2013) Predation selects for low resting metabolic rate and consistent individual differences in anti-predator behavior in a beetle. Acta Ethologica 16, 163–172.Google Scholar
Kuriwada, T, Kumano, N, Shiromoto, K and Haraguchi, D (2009) Copulation reduces the duration of death-feigning behaviour in the sweetpotato weevil, Cylas formicarius. Animal Behaviour 78, 1145–1151.Google Scholar
Leidenberger, S, Harding, K and Jonsson, PR (2012) Ecology and distribution of the isopod genus Idotea in the Baltic Sea: key species in a changing environment. Journal of Crustacean Biology 32, 359–389.Google Scholar
Lindquist, N, Barber, PH and Weisz, JB (2005) Episymbiotic microbes as food and defence for marine isopods: unique symbioses in a hostile environment. Proceedings of the Royal Society B: Biological Sciences 272, 1209–1216.Google Scholar
Mackay, DA (1929) Larval and postlarval lobsters. The American Naturalist 63, 160–170.Google Scholar
Matsumura, K, Sasaki, K and Miyatake, T (2016) Correlated responses in death-feigning behavior, activity, and brain biogenic amine expression in red flour beetle Tribolium castaneum strains selected for walking distance. Journal of Ethology 34, 97–105.Google Scholar
Merilaita, S (1998) Crypsis through disruptive coloration in an isopod. Proceedings of the Royal Society of London. Series B: Biological Sciences 265, 1059–1064.Google Scholar
Merilaita, S and Jormalainen, V (1997) Evolution of sex differences in microhabitat choice and colour polymorphism in Idotea baltica. Animal Behaviour 54, 769–778.Google Scholar
Miura, Y and Goshima, S (2016) Temporal dynamics of intersexual conflict and the effect of male quality on female fecundity in the marine isopod Cleantiella isopus. Behaviour 153, 569–589.Google Scholar
Miyatake, T (2001a) Effects of starvation on death-feigning in adults of Cylas formicarius (Coleoptera: Brentidae). Annals of the Entomological Society of America 94, 612–616.Google Scholar
Miyatake, T (2001b) Diurnal periodicity of death-feigning in Cylas formicarius (Coleoptera: Brentidae). Journal of Insect Behavior 14, 421–432.Google Scholar
Miyatake, T, Katayama, K, Takeda, Y, Nakashima, A, Sugita, A and Mizumoto, M (2004) Is death–feigning adaptive? Heritable variation in fitness difference of death–feigning behaviour. Proceedings of the Royal Society of London. Series B: Biological Sciences 271, 2293–2296.Google Scholar
Miyatake, T, Nakayama, S, Nishi, Y and Nakajima, S (2009) Tonically immobilized selfish prey can survive by sacrificing others. Proceedings of the Royal Society B: Biological Sciences 276, 2763–2767.Google Scholar
Miyatake, T, Okada, K and Harano, T (2008) Negative relationship between ambient temperature and death-feigning intensity in adult Callosobruchus maculatus and Callosobruchus chinensis. Physiological Entomology 33, 83–88.Google Scholar
Moore, KA and Williams, DD (1990) Novel strategies in the complex defense repertoire of a stonefly (Pteronarcys dorsata) nymph. Oikos 57, 49–56.Google Scholar
Mueller, T and Mueller, C (2017) Host plant effects on the behavioural phenotype of a Chrysomelid. Ecological Entomology 42, 336–344.Google Scholar
Nakayama, S, Nishi, Y and Miyatake, T (2010) Genetic correlation between behavioural traits in relation to death-feigning behaviour. Population Ecology 52, 329–335.CrossRefGoogle Scholar
Nakayama, S, Sasaki, K, Matsumura, K, Lewis, Z and Miyatake, T (2012) Dopaminergic system as the mechanism underlying personality in a beetle. Journal of Insect Physiology 58, 750–755.Google Scholar
O'Brien, TJ and Dunlap, WP (1975) Tonic immobility in the blue crab (Callinectes sapidus, Rathbun): its relation to threat of predation. Journal of Comparative and Physiological Psychology 89, 86–94.Google Scholar
Ohno, T and Miyatake, T (2007) Drop or fly? Negative genetic correlation between death-feigning intensity and flying ability as alternative anti-predator strategies. Proceedings of the Royal Society B: Biological Sciences 274, 555–560.Google Scholar
Powell, EH Jr. and Gunter, G (1968) Observations on the Stone Crab, Menippe mercenaria Say, in the vicinity of Port Aransas, Texas. Gulf Research Reports 2, 285–299.Google Scholar
Quadros, AF, Bugs, PS and Araujo, PB (2012) Tonic immobility in terrestrial isopods: intraspecific and interspecific variability. ZooKeys 176, 155–170.Google Scholar
R Core Team (2022) R: A Language and Environment for Statistical Computing. Vienna, Austria : R Foundation for Statistical Computing. Available at https://www.R-project.org/Google Scholar
Ruxton, G (2006) Grasshoppers don't play possum. Nature 440, 880–880.Google Scholar
Sakai, M (2021) Death-feigning in Insects: Mechanism and Function of Tonic Immobility. Singapore: Springer Nature.Google Scholar
Scarton, LP, Zimmermann, BL, Machado, S, Aued, AW, Manfio, D and Santos, S (2009) Thanatosis in the freshwater crab Trichodactylus panoplus (Decapoda: Brachyura: Trichodactylidae). Nauplius 17, 97–100.Google Scholar
Suzuki, S and Futami, K (2018) Predatory risk increased due to egg-brooding in Armadillidium vulgare (Isopoda: Oniscidea). Ethology 124, 256–259.Google Scholar
Takahashi, T and Goshima, S (2012) The growth, reproduction and body color pattern of Cleantiella isopus (Isopoda: Valvifera) in Hakodate Bay, Japan. Crustacean Research 41, 1–10.Google Scholar
Tuf, IH, Drábková, L and Šipoš, J (2015) Personality affects defensive behaviour of Porcellio scaber (Isopoda, Oniscidea). Zookeys 515, 159–171.Google Scholar
Vesakoski, O, Merilaita, S and Jormalainen, V (2008) Reckless males, rational females: dynamic trade-off between food and shelter in the marine isopod Idotea balthica. Behavioural Processes 79, 175–181.Google Scholar
Wahle, RA (1992) Body-size dependent anti-predator mechanisms of the American lobster. Oikos 65, 52–60.Google Scholar
Wallerstein, BR and Brusca, RC (1982) Fish predation: a preliminary study of its role in the zoogeography and evolution of shallow water idoteid isopods (Crustacea: Isopoda: Idoteidae). Journal of Biogeography 9, 135–150.Google Scholar
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