Skip to main content

Development, Ontogeny and Parasite-Mediated Changes in Social Behaviour

  • Chapter
  • First Online:
Sociality: The Behaviour of Group-Living Animals

Abstract

Tinbergen (1963) identified the development of a behavioural trait during an animal’s lifetime as one of the four key questions that should be asked about a given trait in order to understand it. The study of the development, or ontogeny, of sociality throughout animals’ lives provides an insight to both the mechanisms of sociality and its functions. In this chapter, we examine first the development of sociality. Many animal species spend the initial stages of life in a social environment, for example, if eggs are clustered or young are born into a litter of sibs. This means that an aggregation of a cohort of kin is formed. These may subsequently go on to form a true social group, based on social attraction, or they may simply remain together through philopatry, and it can be difficult to distinguish between these. Nonetheless, the development of social attraction to conspecifics in early life has been examined in a few species in conjunction with the development of sensory and locomotive capabilities, and we describe these here. Once the ability to identify and locate conspecifics is developed, then the likelihood of an animal seeking out others of its kind in order to associate with them and to form groups is governed by a range of factors. These include the early-life social environment of offspring, the neural development of individuals, the action of hormones and the genetic predisposition of animals to sociality. We consider each of these in relation to the development and expression of sociality and further how this relates to the ecological context in which the animal operates. Following on from this, we consider how parasitism, a near ubiquitous reality for free-ranging animals, affects patterns of association among animals.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adar E, Nottebohm F, Barnea A (2008) The relationship between nature of social change, age, and position of new neurons and their survival in adult zebra finch brain. J Neurosci 28:5394–5400

    Article  CAS  PubMed  Google Scholar 

  • Anacker AMJ, Beery AK (2013) Life in groups: the roles of oxytocin in mammalian sociality. Front Behav Neurosci 7:185

    Article  PubMed  PubMed Central  Google Scholar 

  • Anderson JR, Nilssen AC (1996a) Trapping oestrid parasites of reindeer: the relative age, fat body content and gonotrophic conditions of Cephenemyia trompe and Hypoderma tarandi females caught in baited traps. Med Vet Entomol 10:347–353

    Article  CAS  PubMed  Google Scholar 

  • Anderson JR, Nilssen AC (1996b) Trapping oestrid parasites of reindeer: the response of Cephenemyia trompe and Hypoderma tarandi to baited traps. Med Vet Entomol 10:337–346

    Article  CAS  PubMed  Google Scholar 

  • Arnold C, Taborsky B (2010) Social experience in early ontogeny has lasting effects on social skills in cooperatively breeding cichlids. Anim Behav 79:621–630

    Article  Google Scholar 

  • Arnold SJ, Wassersug RJ (1978) Differential predation on metamorphic anurans by garter snakes (thamnophis) – social-behavior as a possible defense. Ecology 59:1014–1022

    Article  Google Scholar 

  • Baarendse PJJ, Counotte DS, O’Donnell P, Vanderschuren L (2013) Early social experience is critical for the development of cognitive control and dopamine modulation of prefrontal cortex function. Neuropsychopharmacology 38:1485–1494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beani L, Dallai R, Mercati D, Cappa F, Giusti F, Manfredini F (2011) When a parasite breaks all the rules of a colony: morphology and fate of wasps infected by a strepsipteran endoparasite. Anim Behav 82:1305–1312

    Article  Google Scholar 

  • Beckers R, Deneubourg JL, Goss S (1993) Modulation of trail laying in the ant lasius-niger (Hymenoptera, Formicidae) and its role in the collective selection of a food source. J Insect Behav 6:751–759

    Article  Google Scholar 

  • Behringer DC, Butler MJ (2010) Disease avoidance influences shelter use and predation in Caribbean spiny lobster. Behav Ecol Sociobiol 64:747–755

    Article  Google Scholar 

  • Bertram BCR (1992) The ostrich communal nesting system. Princeton University Press, Princeton

    Book  Google Scholar 

  • Boogert NJ, Farine DR, Spencer KA (2014) Developmental stress predicts social network position. Biol Lett 10:20140561

    Article  PubMed  PubMed Central  Google Scholar 

  • Boyd LE (1988) Ontogeny of behavior in Przewalski horses. Appl Anim Behav Sci 21:41–69

    Article  Google Scholar 

  • Buhl J, Sumpter DJT, Couzin ID, Hale JJ, Despland E, Miller ER, Simpson SJ (2006) From disorder to order in marching locusts. Science 312(5778):1402–1406. doi:10.1126/science.1125142

    Article  CAS  PubMed  Google Scholar 

  • Buske C, Gerlai R (2011) Shoaling develops with age in Zebrafish (Danio rerio). Prog Neuropsychopharmacol Biol Psychiatry 35:1409–1415

    Article  PubMed  PubMed Central  Google Scholar 

  • Butler MJ, MacDiarmid AB, Booth JD (1999) The cause and consequence of ontogenetic changes in social aggregation in New Zealand spiny lobsters. Mar Ecol Prog Ser 188:179–191

    Article  Google Scholar 

  • Byrne RW, Whiten A (1988) Machiavellian Intelligence: social expertise and the evolution of intellect in monkeys apes and humans. Oxford University Press, Oxford

    Google Scholar 

  • Carson K, Woodgush DGM (1983) Equine behavior.1. A review of the literature on social and dam foal behavior. App Anim Ethol 10:165–178

    Article  Google Scholar 

  • Carter CS, Grippo AJ, Pournajafi-Nazarloo H, Ruscio MG, Porges SW (2008) Oxytocin, vasopressin and sociality. Prog Brain Res 170:331–336

    Article  CAS  PubMed  Google Scholar 

  • Catterall CP, Kikkawa J, Gray C (1989) Interrelated age-dependent patterns of ecology and behavior in a population of silvereyes (Aves, Zzosteropidae). J Anim Ecol 58:557–570

    Article  Google Scholar 

  • Chapman CA (1990) Association patterns of spider monkeys – the influence of ecology and sex on social-organization. Behav Ecol Sociobiol 26:409–414

    Article  Google Scholar 

  • Childress MC, Herrnkind WF (1996) The ontogeny of social behavior among juvenile Caribbean spiny lobsters. Anim Behav 51:675–687

    Article  Google Scholar 

  • Childress MJ, Herrnkind WF (2001) The guide effect influence on the gregariousness of juvenile Caribbean spiny lobsters. Anim Behav 62:465–472

    Article  Google Scholar 

  • Conradt L, Roper TJ (2000) Activity synchrony and social cohesion: a fission-fusion model. Proc Royal Soc Lon Series B Bio Sci 267:2213–2218

    Article  CAS  Google Scholar 

  • Costa JT, Gotzek DA, Janzen DH (2003) Late-instar shift in foraging strategy and trail-pheromone use by caterpillars of the neotropical moth Arsenura armida (Cramer) (Saturniidae: Arsenurinae). J Lepidopera Soc 57:220–229

    Google Scholar 

  • Cote IM, Poulin R (1995) Parasitism and group-size in social animals – a metaanalysis. Behav Ecol 6:159–165

    Article  Google Scholar 

  • Courtney SP (1984) The evolution of egg clustering by butterflies and other insects. Am Nat 123:276–281

    Article  Google Scholar 

  • Cozzie LR, Irby WS (2010) Anti-insect defensive behaviors in equines post-West Nile virus infection. J Veterinary Beha Clini Appl Res 5:13–21

    Article  Google Scholar 

  • Delestrade A (1994) Factors affecting flock size in the alpine chough pyrrhocorax-graculus. Ibis 136:91–96

    Article  Google Scholar 

  • Delville Y, David JT, Taravosh-Lahn K, Wommack JC (2003) Stress and the development of agonistic behavior in golden hamsters. Horm Behav 44:263–270

    Article  PubMed  Google Scholar 

  • Despland E, Hamzeh S (2004) Ontogenetic changes in social behaviour in the forest tent caterpillar, Malacosoma disstria. Behav Ecol Sociobiol 56:177–184

    Article  Google Scholar 

  • Devito J, Chivers DP, Kiesecker JM, Marco A, Wildy EL, Blaustein AR (1998) The effects of snake predation on metamorphosis of western toads, Bufo boreas (Amphibia, Bufonidae). Etholo 104(3):185–193

    Article  Google Scholar 

  • Dugatkin LA, Fitzgerald GJ, Lavoie J (1994) Juvenile 3-spined sticklebacks avoid parasitized conspecifics. Environ Biol Fishes 39:215–218

    Article  Google Scholar 

  • Dunbar RIM (1998) The social brain hypothesis. Evol Anthropol 6:178–190

    Article  Google Scholar 

  • Dunbar RIM, Shultz S (2007) Evolution in the social brain. Science 317:1344–1347

    Article  CAS  PubMed  Google Scholar 

  • Edwards DH, Kravitz EA (1997) Serotonin, social status and aggression. Curr Opin Neurobiol 7:812–819

    Article  CAS  PubMed  Google Scholar 

  • Einon DF, Morgan MJ (1977) Critical period for social-isolation in rat. Dev Psychobiol 10:123–132

    Article  CAS  PubMed  Google Scholar 

  • Elekonich MM, Wingfield JC (2000) Seasonality and hormonal control of territorial aggression in female song sparrows (Passeriformes: Emberizidae: Melospiza melodia). Etholo 106:493–510

    Article  Google Scholar 

  • Engeszer RE, Ryan MJ, Parichy DM (2004) Learned social preference in zebrafish. Curr Biol 14:881–884

    Article  CAS  PubMed  Google Scholar 

  • Fairbanks LA (1993) Risk-taking by juvenile vervet monkeys. Behaviour 124:57–72

    Article  Google Scholar 

  • Fauchald P, Rodven R, Bardsen BJ, Langeland K, Tveraa T, Yoccoz NG, Ims RA (2007) Escaping parasitism in the selfish herd: age, size and density-dependent warble fly infestation in reindeer. Oikos 116:491–499

    Article  Google Scholar 

  • Fischer S, Bessert-Nettelbeck M, Kotrschal A, Taborsky B (2015) Rearing-group size determines social competence and brain structure in a cooperatively breeding cichlid. Am Natu 186:123–140

    Article  Google Scholar 

  • Fitzgerald TD (1993) Sociality in caterpillars. In: Stamp N, Casey T (eds) Caterpillars: ecological and evolutionary constraints on foraging. Chapman and Hall, New York, pp 372–403

    Google Scholar 

  • Fone KCF, Porkess MV (2008) Behavioural and neurochemical effects of post-weaning social isolation in rodents – relevance to developmental neuropsychiatric disorders. Neurosci Biobehav Rev 32:1087–1102

    Article  CAS  PubMed  Google Scholar 

  • Fowler CD, Liu Y, Ouimet C, Wang Z (2002) The effects of social environment on adult neurogenesis in the female prairie vole. J Neurobiol 51:115–128

    Article  PubMed  Google Scholar 

  • Fuiman LA, Magurran AE (1994) Development of predator defenses in fishes. Rev Fish Biol Fisher 4:145–183

    Article  Google Scholar 

  • Giesing ER, Suski CD, Warner RE, Bell AM (2011) Female sticklebacks transfer information via eggs: effects of maternal experience with predators on offspring. Proc Royal Soc B Biol Sci 278:1753–1759

    Article  Google Scholar 

  • Gonda A, Herczeg G, Merila J (2009) Habitat-dependent and -independent plastic responses to social environment in the nine-spined stickleback (Pungitius pungitius) brain. Proce Royal Soc London Series B Biol Sci 276:2085–2092

    Article  Google Scholar 

  • Goodson JL (1998a) Territorial aggression and dawn song are modulated by septal vasotocin and vasoactive intestinal polypeptide in male field sparrows (Spizella pusilla). Horm Behav 34:67–77

    Article  CAS  PubMed  Google Scholar 

  • Goodson JL (1998b) Vasotocin and vasoactive intestinal polypeptide modulate aggression in a territorial songbird, the violet-eared waxbill (Estrildidae: Uraeginthus granatina). Gen Comp Endocrinol 111:233–244

    Article  CAS  PubMed  Google Scholar 

  • Goodson JL, Adkins-Regan E (1999) Effect of intraseptal vasotocin and vasoactive intestinal polypeptide infusions on courtship song and aggression in the male zebra finch (Taeniopygia guttata). J Neuroendocrinol 11:19–25

    Article  CAS  PubMed  Google Scholar 

  • Goodson JL, Schrock SE, Klatt JD, Kabelik D, Kingsbury MA (2009) Mesotocin and nonapeptide receptors promote estrildid flocking behavior. Science 325:862–866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hamner WM, Hamner PP (2000) Behavior of Antarctic krill (Euphausia superba): schooling, foraging, and antipredatory behavior. Can J Fish Aquat Sci 57:192–202

    Article  Google Scholar 

  • Hamner WM, Hamner PP, Obst BS, Carleton JH (1989) Field observations on the ontogeny of schooling of Euphausia superba furciliae and its relationship to ice in antarctic waters. Limnol Oceanogr 34:451–456

    Article  Google Scholar 

  • Helle T (1980) Abundance of warble fly (Oedemagena tarandi) larvae in semi-domestic reindeer (Rangifer tarandus) in Finland. Reports Kevo Subarctic Res Station 16:1–6

    Google Scholar 

  • Helle T, Aspi J, Lempa K, Taskinen E (1992) Strategies to avoid biting flies by reindeer – field experiments with silhouette traps. Ann Zoo Fennici 29(2):69–74

    Google Scholar 

  • Hillman JC (1974) Ecology and behavior of the wild eland. Wildlife News 9:6–9

    Google Scholar 

  • Hillman JC (1979) The biology of the eland (Taurotragus oryx Pallas) in the wild. Nairobi University

    Google Scholar 

  • Hogstad O (1987) It is expensive to be dominant. Auk 104(2):333–336

    Google Scholar 

  • Holbrook GL, Armstrong E, Bachmann JAS, Deasy BM, Schal C (2000) Role of feeding in the reproductive ‘group effect’ in females of the German cockroach Blattella germanica (L.). J Insect Physiol 46:941–949

    Article  CAS  PubMed  Google Scholar 

  • Hughes DP, Kathirithamby J, Turillazzi S, Beani L (2004) Social wasps desert the colony and aggregate outside if parasitized: parasite manipulation? Beha Ecolo 15:1037–1043

    Article  Google Scholar 

  • Ims RA (1990) On the adaptive value of reproductive synchrony as a predator-swamping strategy. Am Natu 136:485–498

    Article  Google Scholar 

  • Karvonen A, Seppala O, Valtonen ET (2004) Parasite resistance and avoidance behaviour in preventing eye fluke infections in fish. Parasitology 129:159–164

    Article  CAS  PubMed  Google Scholar 

  • Kavaliers M, Choleris E, Agmo A, Pfaff DW (2004) Olfactory-mediated parasite recognition and avoidance: linking genes to behavior. Horm Behav 46:272–283

    Article  PubMed  Google Scholar 

  • Kavaliers M, Choleris E, Pfaff DW (2005) Genes, odours and the recognition of parasitized individuals by rodents. Trends Parasitol 21:423–429

    Article  CAS  PubMed  Google Scholar 

  • Kleiman DG (2011) Canid mating systems, social behavior, parental care and ontogeny: are they flexible? Behav Genet 41:803–809

    Article  PubMed  Google Scholar 

  • Kozak GM, Boughman JW (2008) Experience influences shoal member preference in a species pair of sticklebacks. Behav Ecolo 19:667–676

    Article  Google Scholar 

  • Krause J, Godin JGJ (1994) Influence of parasitism on the shoaling behavior of banded killifish, Fundulus diaphanus. Can J Zool Revue Can De Zool 72:1775–1779

    Article  Google Scholar 

  • Krause J, Godin JGJ (1996a) Influence of prey foraging posture on flight behavior and predation risk: predators take advantage of unwary prey. Behav Ecolo 7(3):264–271

    Article  Google Scholar 

  • Krause J, Godin JGJ (1996b) Influence of parasitism on shoal choice in the banded killifish (Fundulus diaphanus, Teleostei, Cyprinodontidae). Ethology 102:40–49

    Article  Google Scholar 

  • Kruijt JP (1964) Ontogeny of social behaviour in Burmese red junglefowl (Gallus gallus spadiceus). Behav Suppl 12:1–201

    Google Scholar 

  • Lafferty KD, Shaw JC (2013) Comparing mechanisms of host manipulation across host and parasite taxa. J Exp Biol 216:56–66

    Article  PubMed  Google Scholar 

  • Lewis SE, Hodel A, Sturdy T, Todd R, Weigl C (2012) Impact of acanthocephalan parasites on aggregation behavior of amphipods (Gammarus pseudolimnaeus). Behav Processes 91:159–163

    Article  PubMed  Google Scholar 

  • Lickliter RE (1987) Activity patterns and companion preferences of domestic goat kids. Appl Anim Behav Sci 19:137–145

    Article  Google Scholar 

  • Lihoreau M, Rivault C (2008) Tactile stimuli trigger group effects in cockroach aggregations. Anim Behav 75:1965–1972

    Article  Google Scholar 

  • Lipkind D, Nottebohm F, Rado R, Barnea A (2002) Social change affects the survival of new neurons in the forebrain of adult songbirds. Behav Brain Res 133:31–43

    Article  CAS  PubMed  Google Scholar 

  • Lukkes JL, Mokin MV, Scholl JL, Forster GL (2009) Adult rats exposed to early-life social isolation exhibit increased anxiety and conditioned fear behavior, and altered hormonal stress responses. Horm Behav 55:248–256

    Article  CAS  PubMed  Google Scholar 

  • Lurling M, Scheffer M (2007) Info-disruption: pollution and the transfer of chemical information between organisms. Trends Ecol Evol 22:374–379

    Article  PubMed  Google Scholar 

  • Maeno K, Tanaka S (2010) Epigenetic transmission of phase in the desert locust, Schistocerca gregaria determining the stage sensitive to crowding for the maternal determination of progeny characteristics. J Insect Physiol 56:1883–1888

    Article  CAS  PubMed  Google Scholar 

  • Masuda R, Tsukamoto K (1999) School formation and concurrent developmental changes in carangid fish with reference to dietary conditions. Environ Biol Fishes 56:243–252

    Article  Google Scholar 

  • McCaffery AR, Simpson SJ, Islam MS, Roessingh P (1998) A gregarizing factor present in the egg pod foam of the desert locust Schistocerca gregaria. J Exper Biol 201:347–363

    Google Scholar 

  • Mooring MS, Hart BL (1992) Animal grouping for protection from parasites – selfish herd and encounter-dilution effects. Behaviour 123:173–193

    Article  Google Scholar 

  • Mougenot F, Combe M, Jeanson R (2012) Ontogenesis and dynamics of aggregation in a solitary spider. Anim Behav 84:391–398

    Article  Google Scholar 

  • Nelson RJ (2000) An introduction to behavioral endocrinology. Sinauer Associates, Sunderland

    Google Scholar 

  • Nicieza AG (1999) Context-dependent aggregation in Common Frog Rana temporaria tadpoles: influence of developmental stage, predation risk and social environment. Func Ecolo 13:852–858

    Article  Google Scholar 

  • O’Brien DP (1987) Direct observations of the behavior of Euphausia superba and Euphausia crystallorophias (Crustacea, Euphausiacea) under pack ice during the antarctic spring of 1985. J Crustacean Biol 7:437–448

    Article  Google Scholar 

  • Ott SR, Rogers SM (2010) Gregarious desert locusts have substantially larger brains with altered proportions compared with the solitarious phase. Proc Royal Soc B Biol Sci 277:3087–3096

    Article  Google Scholar 

  • Pellis SM, Pellis VC (1988) Play-fighting in the Syrian golden hamster Mesocricetus auratus Waterhouse, and its relationship to serious fighting during postweaning development. Dev Psychobiol 21:323–337

    Article  CAS  PubMed  Google Scholar 

  • Pellis SM, Pellis VC (1998) Play fighting of rats in comparative perspective: a schema for neurobehavioral analyses. Neurosci Biobehav Rev 23:87–101

    Article  CAS  PubMed  Google Scholar 

  • Perez-Barberia FJ, Shultz S, Dunbar RIM (2007) Evidence for coevolution of sociality and relative brain size in three orders of mammals. Evolution 61:2811–2821

    Article  PubMed  Google Scholar 

  • Poulin R (2010) Parasite manipulation of host behavior: an update and frequently asked questions. Adv Study Behav 41(41):151–186

    Article  Google Scholar 

  • Pusey AE (1983) Mother offspring relationships in chimpanzees after weaning. Anim Behav 31:363–377

    Article  Google Scholar 

  • Ratchford SG, Eggleston DB (1998) Size- and scale-dependent chemical attraction contribute to an ontogenetic shift in sociality. Anim Behav 56:1027–1034

    Article  PubMed  Google Scholar 

  • Ratti O, Ojanen U, Helle P (2006) Increasing group size dilutes black fly attack rate in Black Grouse. Ornis Fennica 83:86–90

    Google Scholar 

  • Rifkin JL, Nunn CL, Garamszegi LZ (2012) Do animals living in larger groups experience greater parasitism? A meta-analysis. Am Nat 180:70–82

    Article  PubMed  Google Scholar 

  • Ritz DA (2000) Is social aggregation in aquatic crustaceans a strategy to conserve energy? Can J Fish Aquat Sci 57:59–67

    Article  Google Scholar 

  • Ritz DA, Hobday AJ, Montgomery JC, Ward AJW (2011) Social aggregation in the pelagic zone with special reference to fish and invertebrates. In: Lesser M (ed) Advances in marine biology, vol 60, Vol., pp 161–227

    Google Scholar 

  • Rode NO, Lievens EJP, Flaven E, Segard A, Jabbour-Zahab R, Sanchez MI, Lenormand T (2013) Why join groups? Lessons from parasite-manipulated Artemia. Ecol Lett 16:493–501

    Article  PubMed  Google Scholar 

  • Rohwer S, Ewald PW (1981) The cost of dominance and advantage of subordination in a badge signaling system. Evolution 35(3):441–454. doi:10.2307/2408193

    Article  Google Scholar 

  • Roskaft E, Jarvi T, Bakken M, Bech C, Reinertsen RE (1986) The relationship between social-status and resting metabolic-rate in great tits (Parus major) and pied flycatchers (Ficedula hypoleuca). Anim Behav 34:838–842. doi:10.1016/s0003-3472(86)80069-0

    Article  Google Scholar 

  • Roth LM, Willis ER (1960) The biotic associations of cockroaches. Smithsonian Misc Coll 141:1–470

    Google Scholar 

  • Sachser N, Kaiser S (2010) The social modulation of behavioural development. In: Kappeler P (ed) Animal behaviour: evolution and mechanisms. Springer, Berlin/London/New York, pp 505–536

    Chapter  Google Scholar 

  • Seeley TD, Towne WF (1992) Tactics of dance choice in honey-bees – do foragers compare dances. Behav Ecol Sociobiol 30:59–69

    Article  Google Scholar 

  • Seppala O, Karvonen A, Valtonen ET (2008) Shoaling behaviour of fish under parasitism and predation risk. Anim Behav 75:145–150

    Article  Google Scholar 

  • Simpson SJ, McCaffery AR, Hagele BF (1999) A behavioural analysis of phase change in the desert locust. Biol Rev Camb Philos Soc 74:461–480

    Article  Google Scholar 

  • Sinervo B, Miles DB, Frankino WA, Klukowski M, DeNardo DF (2000) Testosterone, endurance, and Darwinian fitness: natural and sexual selection on the physiological bases of alternative male behaviors in side-blotched lizards. Horm Behav 38:222–233

    Article  CAS  PubMed  Google Scholar 

  • Skogland T (1989) Natural-selection of wild reindeer life-history traits by food limitation and predation. Oikos 55:101–110

    Article  Google Scholar 

  • Soma KK, Wingfield JC (2001) Dehydroepiandrosterone in songbird plasma: seasonal regulation and relationship to territorial aggression. Gen Comp Endocrinol 123:144–155

    Article  CAS  PubMed  Google Scholar 

  • Sperry TS, Wingfield JC (2003) Serotonergic regulation of glucocorticoid release in male white-crowned sparrows. Integr Comp Biol 43:925

    Google Scholar 

  • Sword GA, Simpson SJ, El Hadi OTM, Wilps H (2000) Density-dependent aposematism in the desert locust. Proc Royal Soc B-Biol Sci 267:63–68

    Article  CAS  Google Scholar 

  • Taborsky B, Oliveira RF (2012) Social competence: an evolutionary approach. Trends Ecol Evol 27:679–688

    Article  PubMed  Google Scholar 

  • Tanabe Y, Nakamura T, Fujioka K, Doi O (1979) Production and secretion of sex steroid-hormones by the testes, the ovary, and the adrenal-glands of embryonic and young chickens (Gallus domesticus). Gen Comp Endocrinol 39:26–33

    Article  CAS  PubMed  Google Scholar 

  • Tanaka S, Maeno K (2010) A review of maternal and embryonic control of phase-dependent progeny characteristics in the desert locust. J Insect Physiol 56:911–918

    Article  CAS  PubMed  Google Scholar 

  • Ten Eyck GR (2008) Serotonin modulates vocalizations and territorial behavior in an amphibian. Behav Brain Res 193:144–147

    Article  PubMed  CAS  Google Scholar 

  • Tinbergen N (1963) On aims and methods of ethology. Z Tierpsychol 20:410–433

    Article  Google Scholar 

  • Trainor BC, Sisk CL, Nelson RJ (2009) Hormones and the development and expression of aggressive behavior. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT (eds) Hormones brain and behavior. Academic Press, Amsterdam, pp 167–203

    Chapter  Google Scholar 

  • Treisman M (1975a) Predation and evolution of gregariousness.1. Models for concealment and evasion. Anim Behav 23:779–800

    Article  Google Scholar 

  • Treisman M (1975b) Predation and evolution of gregariousness.2. Economic model for predator–prey interaction. Anim Behav 23:801–825

    Article  Google Scholar 

  • Trokovic N, Gonda A, Herczeg G, Laurila A, Merila J (2011) Brain plasticity over the metamorphic boundary: carry-over effect of larval environment on froglet brain development. J Evol Biol 24:1380–1385

    Article  CAS  PubMed  Google Scholar 

  • van Leeuwen EJC, Mulenga IC, Chidester DL (2014) Early social deprivation negatively affects social skill acquisition in chimpanzees (Pan troglodytes). Anim Cogn 17:407–414

    Article  PubMed  Google Scholar 

  • Veissier I, Leneindre P, Garel JP (1990) Decrease in cow-calf attachment after weaning. Behav Processes 21:95–105

    Article  CAS  PubMed  Google Scholar 

  • Vicsek T, Czirok A, Benjacob E, Cohen I, Shochet O (1995) Novel type of phase-transition in a system of self-driven particles. Phys Rev Lett 75(6):1226–1229. doi:10.1103/PhysRevLett.75.1226

    Article  CAS  PubMed  Google Scholar 

  • Walser ES, Hague P, Yeomans M (1983) Preferences for sibling or mother in dalesbred and jacob twin lambs. Appl Anim Etholo 9:289–297

    Article  Google Scholar 

  • Warburton K, Lees N (1996) Species discrimination in guppies: learned responses to visual cues. Anim Behav 52:371–378

    Article  Google Scholar 

  • Ward AJW, Axford S, Krause J (2002a) Mixed-species shoaling in fish: the sensory mechanisms and costs of shoal choice. Behav Ecolo Sociobiolo 52(3):182–187. doi:10.1007/s00265-002-0505-z

    Article  Google Scholar 

  • Ward AJW, Hoare DJ, Couzin ID, Broom M, Krause J (2002b) The effects of parasitism and body length on positioning within wild fish shoals. J An Ecolo 71:10–14

    Article  Google Scholar 

  • Ward AJW, Duff AJ, Horsfall JS, Currie S (2008a) Scents and scents-ability: pollution disrupts chemical social recognition and shoaling in fish. Proc Royal Soc B Biolo Sci 275:101–105

    Article  Google Scholar 

  • Ward AJW, Sumpter DJT, Couzin LD, Hart PJB, Krause J (2008b) Quorum decision-making facilitates information transfer in fish shoals. Proc Natl Acad Sci U S A 105:6948–6953

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size structured populations. Ann Rev Ecolo Syst 15:393–425

    Article  Google Scholar 

  • Wingfield JC, Ball GF, Dufty AM, Hegner RE, Ramenofsky M (1987) Testosterone and aggression in birds. Am Sci 75:602–608

    Google Scholar 

  • Wingfield JC, Hegner RE, Dufty AM, Ball GF (1990) The challenge hypothesis – theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Natu 136:829–846

    Article  Google Scholar 

  • Wingfield JC, Lynn SE, Soma KK (2001) Avoiding the ‘costs’ of testosterone: ecological bases of hormone-behavior interactions. Brain Behav Evol 57:239–251

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Ward, A., Webster, M. (2016). Development, Ontogeny and Parasite-Mediated Changes in Social Behaviour. In: Sociality: The Behaviour of Group-Living Animals. Springer, Cham. https://doi.org/10.1007/978-3-319-28585-6_9

Download citation

Publish with us

Policies and ethics