Social deprivation early in life affects further individual development and leads to irreversible behavioural alterations later in life. Although the syndrome is well-studied in vertebrates including humans, its presence in invertebrates has been described only in eusocial insects and cockroaches. Here we show the first evidence of social deprivation in subsocial decapod crustaceans, based on analysis of video-recorded agonistic encounters of juvenile red swamp crayfish (Procambarus clarkii, Girard). In comparison with maternally incubated juveniles, isolated crayfish had altered repertoires, numbers and frequency of agonistic interactions similar to those described in vertebrates. Our results support the view on the syndrome of social deprivation as a ubiquitous trait in species with developed maternal care across diverse taxa.

Department of Animal Science and Ethology Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague Kamýcká 129 Praha Suchdol 165 00 Czech Republic

Department of Ethology Research Institute of Animal Production Přátelství 815 Praha 104 01 Czech Republic

Department of Zoology and Fisheries Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague Kamýcká 129 Praha Suchdol 165 00 Czech Republic

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Kanitz E, Tuchscherer M, Puppe B, Tuchscherer A, Stabenow B. Consequences of repeated early isolation in domestic piglets (Sus scrofa) on their behavioural, neuroendocrine, and immunological responses. Brain. Behav. Immun. 2004;18:35–45. doi: 10.1016/S0889-1591(03)00085-0. PubMed DOI

Tuchscherer M, Kanitz E, Puppe B, Tuchscherer A. Early social isolation alters behavioral and physiological responses to an endotoxin challenge in piglets. Horm. Behav. 2006;50:753–761. doi: 10.1016/j.yhbeh.2006.06.026. PubMed DOI

Gruendel AD, Arnold WJ. Effects of early social deprivation on reproductive behavior of male rats. J. Comp. Physiol. Psych. 1969;67:123–128. doi: 10.1037/h0026667. PubMed DOI

Lewis MH, Gluck JP, Petitto JM, Hensley LL, Ozer H. Early social deprivation in nonhuman primates: long-term effects on survival and cell-mediated immunity. Biol. Psychiat. 2000;47:119–126. doi: 10.1016/S0006-3223(99)00238-3. PubMed DOI

Herskin MS, Jensen KH. Effects of different degrees of social isolation on the behaviour of weaned piglets kept for experimental purposes. Anim. Welfare. 2000;9:237–249.

Panksepp J, Beatty WW. Social deprivation and play in rats. Behav. Neural Biol. 1980;30:197–206. doi: 10.1016/S0163-1047(80)91077-8. PubMed DOI

Luescher, A. U. Manual of parrot behavior. (Blackwell Publishing, 2006).

Tóth M, Halász J, Mikics É, Barsy B, Haller J. Early social deprivation induces disturbed social communication and violent aggression in adulthood. Behav. Neurosci. 2008;122:849–854. doi: 10.1037/0735-7044.122.4.849. PubMed DOI

Milde AM, Enger Ø, Murison R. The effects of postnatal maternal separation on stress responsivity and experimentally induced colitis in adult rats. Physiol. Behav. 2004;81:71–84. doi: 10.1016/j.physbeh.2004.01.002. PubMed DOI

West MJ, King AP. Enriching cowbird song by social deprivation. J. Comp. Physiol. Psych. 1980;94:263–270. doi: 10.1037/h0077657. DOI

Groothuis T. The influence of social experience on the development and fixation of the form of displays in the black-headed gull. Anim. Behav. 1992;43:1–14. doi: 10.1016/S0003-3472(05)80067-3. DOI

Harlow HF, Harlow M. Social deprivation in monkeys. Sci. Am. 1962;207:136–146. doi: 10.1038/scientificamerican1162-136. PubMed DOI

Hofer, M. A. In Symbiosis in Parent-Offspring Interactions (eds Leonard Allen Rosenblum & Howard Moltz) Ch. 4, 61–75 (Springer, 1983).

Harlow HF, Suomi SJ. Production of depressive behaviors in young monkeys. J. Autism Child. Schiz. 1971;1:246–255. doi: 10.1007/BF01557346. PubMed DOI

Carlson M, Earls F. Psychological and neuroendocrinological sequelae of early social deprivation in institutionalized children in Romania. Ann. NY. Acad. Sci. 1997;807:419–428. doi: 10.1111/j.1749-6632.1997.tb51936.x. PubMed DOI

Nelson CA, III, et al. Cognitive recovery in socially deprived young children: The Bucharest Early Intervention Project. Science. 2007;318:1937–1940. doi: 10.1126/science.1143921. PubMed DOI

O’Connell, M. E., Boat, T. & Warner, K. E. Preventing mental, emotional, and behavioral disorders among young people: Progress and possibilities. (National Academies Press, 2009). PubMed

Kravitz EA, Huber R. Aggression in invertebrates. Curr. Opin. Neurobiol. 2003;13:736–743. doi: 10.1016/j.conb.2003.10.003. PubMed DOI

Boulay R, Lenoir A. Social isolation of mature workers affects nestmate recognition in the ant Camponotus fellah. Behav. Process. 2001;55:67–73. doi: 10.1016/S0376-6357(01)00163-2. PubMed DOI

Boulay R, Quagebeur M, Godzinska E, Lenoir A. Social isolation in ants: Evidence of its impact on survivorship and behavior in Camponotus fellah (Hymenoptera: Formicidae) Sociobiology. 1999;33:111–124.

Arenas A, Ramírez GP, Balbuena MS, Farina WM. Behavioral and neural plasticity caused by early social experiences: the case of the honeybee. Front. Physiol. 2013;4:41. doi: 10.3389/fphys.2013.00041. PubMed DOI PMC

Lihoreau M, Brepson L, Rivault C. The weight of the clan: even in insects, social isolation can induce a behavioural syndrome. Behav. Process. 2009;82:81–84. doi: 10.1016/j.beproc.2009.03.008. PubMed DOI

Thiel M. Extended parental care behavior in crustaceans - A comparative overview. Crustacean Issues. 2000;12:211–226.

Reynolds, J. In Biology of Freshwater Crayfish (ed. D. M. Holdich) 152–191 (Blackwell Science, 2002).

Little EE. Ontogeny of maternal behavior and brood pheromone in crayfish. J Comp Physiol. 1976;112:133–142. doi: 10.1007/BF00606533. DOI

Aquiloni L, Gherardi F. Extended mother–offspring relationships in crayfish: the return behaviour of juvenile Procambarus clarkii. Ethology. 2008;114:946–954. doi: 10.1111/j.1439-0310.2008.01547.x. DOI

Little EE. Chemical communication in maternal behaviour of crayfish. Nature. 1975;255:400–401. doi: 10.1038/255400a0. PubMed DOI

Tóth M, Mikics É, Tulogdi A, Aliczki M, Haller J. Post-weaning social isolation induces abnormal forms of aggression in conjunction with increased glucocorticoid and autonomic stress responses. Horm. Behav. 2011;60:28–36. doi: 10.1016/j.yhbeh.2011.02.003. PubMed DOI

Patoka J, Petrtýl M, Koščo J, Rylková K. Juvenile red swamp crayfish growth affected by isolation from their mother. Biologia. 2015;70:632–635. doi: 10.1515/biolog-2015-0069. DOI

Carral J, et al. Advantages of artificial reproduction techniques for white-clawed crayfish (Austropotamobius pallipes Lereboullet) Bull. Fr. Pêche Piscic. 2003;370–371:181–184. doi: 10.1051/kmae:2003013. DOI

Leonard BV, Lennard WA, Kildea DG. A method for testing the effectiveness of artificial incubation of eggs vs. maternal brooding in the freshwater crayfish Cherax destructor (Decapoda: Parastacidae) Aquaculture. 2001;195:299–309. doi: 10.1016/S0044-8486(00)00561-5. DOI

Melendre P, Celada J, Carral J, Sáez-Royuela M, Aguilera A. Effectiveness of antifungal treatments during artificial incubation of the signal crayfish eggs (Pacifastacus leniusculus Dana. Astacidae) Aquaculture. 2006;257:257–265. doi: 10.1016/j.aquaculture.2006.02.064. DOI

Pérez JR, et al. The possibilities for artificial incubation of white-clawed crayfish (Austropotamobius pallipes Lereboullet) eggs: comparison between maternal and artificial incubation. Aquaculture. 1999;170:29–35. doi: 10.1016/S0044-8486(98)00389-5. DOI

Kozák P, Füreder L, Kouba A, Reynolds J, Souty-Grosset C. Current conservation strategies for European crayfish. Knowl. Manag. Aquat. Ec. 2011;401:01. doi: 10.1051/kmae/2011018. DOI

Gherardi F, Barbaresi S, Salvi G. Spatial and temporal patterns in the movement of Procambarus clarkii, an invasive crayfish. Aquat. Sci. 2000;62:179–193.

Tao, J., Littel, R., Patetta, M., Truxillo, C. & Wolfinger, R. Mixed models analyses using the SAS system: Course notes. (SAS Institute Inc., 2002).

Stress conditions extend maternal care and delay juvenile development in crayfish

Social deprivation in maternal mouthbrooders Tropheus sp. "Caramba" (Teleostei: Cichlidae) decreases the success rate of reproduction and survival rate of fish fry