Habituation to a predatory stimulus in a harvester (Arachnida, Opiliones).

Defensive behavior Experience Non-associative learning Retention

Journal

Animal cognition
ISSN: 1435-9456
Titre abrégé: Anim Cogn
Pays: Germany
ID NLM: 9814573

Informations de publication

Date de publication:
05 Mar 2024
Historique:
received: 10 08 2023
accepted: 11 10 2023
revised: 11 10 2023
medline: 5 3 2024
pubmed: 5 3 2024
entrez: 5 3 2024
Statut: epublish

Résumé

Several studies have investigated habituation in a defensive context, but few have addressed responses to dangerous stimuli. In such cases, animals should not habituate since this could cost their lives. Here we have stimulated individuals of the harvester Mischonyx squalidus with a predatory stimulus (squeezing with tweezers) in repeated trials within and between days, and measured the occurrence and magnitude of nipping, a defensive behavior. Contrary to our expectations, they did habituate to this stimulus. The probability and magnitude of response declined over trials during each of three days of testing in a typical habituation pattern. During the trials we also observed other defensive behaviors. We discuss our results mainly considering alternative defensive responses. Our data show that we lack information on (1) the role played by the ambiguity of stimuli, (2) the role played by subsequent stimuli and (3) the importance of the array of defensive behaviors of a species in understanding habituation. Although ubiquitous across animals and therefore expected, habituation is described for the first time in the order Opiliones.

Identifiants

pubmed: 38441671
doi: 10.1007/s10071-024-01857-7
pii: 10.1007/s10071-024-01857-7
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

21

Subventions

Organisme : Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq 001)
ID : (CNPq 001)
Organisme : Fundacão de Amparo à Pesquisa do Estado de São Paulo (FAPESP)
ID : (2020/05158-5)
Organisme : Conselho Nacional de Desenvolvimento Científico e Tecnológico
ID : (302879/2016-1)

Informations de copyright

© 2024. The Author(s).

Références

Ardiel EL, Giles AC, Yu AJ, Lindsay TH, Lockery SR, Rankin CH (2016) Dopamine receptor DOP-4 modulates habituation to repetitive photoactivation of a C. elegans polymodal nociceptor. Learn Mem 23:495–503. https://doi.org/10.1101/lm.041830.116
doi: 10.1101/lm.041830.116 pubmed: 27634141 pmcid: 5026203
Ardiel EL, Yu AJ, Giles AC, Rankin CH (2017) Habituation as an adaptive shift in response strategy mediated by neuropeptides. NPJ Sci Learn 2:9–10. https://doi.org/10.1038/s41539-017-0011-8
doi: 10.1038/s41539-017-0011-8 pubmed: 30631455 pmcid: 6161508
Bell AM, Peeke HVS (2012) Individual variation in habituation: behaviour over time toward different stimuli in threespine sticklebacks (Gasterosteus aculeatus). Behaviour 149:1339–1365. https://doi.org/10.1163/1568539X-00003019
doi: 10.1163/1568539X-00003019 pubmed: 25678715 pmcid: 4323190
Cokendolpher JC, Mitov PG. (2007) Natural enemies (Chapter 9). In: Pinto da Rocha R, Machado G, Giribet G (eds) Harvestmen: the biology of opiliones. Harvard University Press, Cambridge, Boston
Dias BC, Willemart RH (2013) The effectiveness of post-contact defenses in a prey with no pre-contact detection. Zoology 116:168–174
doi: 10.1016/j.zool.2012.12.001 pubmed: 23669196
Eisenstein EM, Eisenstein D, Smith JC (2001) The evolutionary significance of habituation and sensitization across phylogeny: a behavioral homeostasis model. Integr Psychol Behav Sci 36:251–265. https://doi.org/10.1007/BF02688794
doi: 10.1007/BF02688794
Evans SM (1969) Habituation of the withdrawal response in nereid polychaetes. 2. Rates of habituation in intact and decerebrate worms. Biol Bull 137:105–117. https://doi.org/10.2307/1539934
doi: 10.2307/1539934
Gueratto CBA,  Benedetti A, Pinto-da-Rocha R (2021) Phylogenetic relationships of the genus Mischonyx Bertkau, 1880, with taxonomic changes and three new species description (Opiliones: Gonyleptidae). PeerJ 9:e11682. https://doi.org/10.7717/peerj.11682
doi: 10.7717/peerj.11682 pubmed: 34692238 pmcid: 8485841
Gnaspini P, Hara MR (2007) Defense mechanisms. In: Pinto-da-Rocha R, Machado G, Giribet G (eds) Harvestmen: the biology of opiliones. Harvard University Press, Cambridge, Boston, pp 374–399
Groves PM, Thompson RF (1970) Habituation: a dual-process theory. Psychol Rev 77:419–450. https://doi.org/10.1037/h0029810
doi: 10.1037/h0029810 pubmed: 4319167
Hara MR, Cavalheiro AJ, Gnaspini P, Santos DYAC (2005) A comparative analysis of the chemical nature of defensive secretions of Gonyleptidae (Arachnida: Opiliones: Laniatores). Biochem Syst Ecol 33:1210–1225. https://doi.org/10.1016/j.bse.2005.07.012
doi: 10.1016/j.bse.2005.07.012
Helfman GS (1989) Threat-sensitive predator avoidance in damselfish–trumpetfish interactions. Behav Ecol 24:47–58. https://doi.org/10.1007/BF00300117
doi: 10.1007/BF00300117
Hemmi JM, Zeil J (2003) Burrow surveillance in fiddler crabs I. Description of behaviour. J Exp Biol 206:3935–3950. https://doi.org/10.1242/jeb.00632
doi: 10.1242/jeb.00632 pubmed: 14555735
Herrel A, Podos J, Huber SK, Hendry AP (2005) Evolution of bite force in Darwin’s finches: a key role for head width. J Evol Biol 18:669–675. https://doi.org/10.1111/j.1420-9101.2004.00857.x
doi: 10.1111/j.1420-9101.2004.00857.x pubmed: 15842496
Liang JJH, Cole BE, Rankin CH (2019) Habituation. In: Encyclopedia of animal behavior, 2nd edn. pp 411–422. https://doi.org/10.1016/B978-0-12-809633-8.90786-6
Long TM, Hanlon RT, Maat AT, Pinsker HM (1989) Non-associative learning in the squid Lolliguncula brevis (Mollusca, Cephalopoda). Mar Behav Physiol 16:1–9. https://doi.org/10.1080/10236248909378736
doi: 10.1080/10236248909378736
Machado G, Carrera PC, Pomini AM, Marsaioli AJ (2005) Chemical defense in harvestmen (Arachnida, Opiliones): do benzoquinone secretions deter invertebrate and vertebrate predators? J Chem Ecol 31:2519–2539. https://doi.org/10.1007/s10886-005-7611-0
doi: 10.1007/s10886-005-7611-0 pubmed: 16273426
Masini CV, Sauer S, White J, Day HEW, Campeau S (2006) Non-associative defensive responses of rats to ferret odor. Physiol Behav 87:72–81. https://doi.org/10.1016/j.physbeh.2005.08.044
doi: 10.1016/j.physbeh.2005.08.044 pubmed: 16183085
May ML, Hoy RR (1991) Habituation of the ultrasound-induced acoustic startle response in flying crickets. J Exp Biol 159:489
doi: 10.1242/jeb.159.1.489 pubmed: 1940771
McDiarmid TA, Yu AJ, Rankin CH (2019) Habituation is more than learning to ignore: multiple mechanisms serve to facilitate shifts in behavioral strategy. BioEssays 41:e1900077. https://doi.org/10.1002/bies.201900077
doi: 10.1002/bies.201900077 pubmed: 31429094
Nazareth TM, Machado G (2015) Egg production constrains chemical defenses in a Neotropical arachnid. PLoS ONE 10(9):e0134908. https://doi.org/10.1371/journal.pone.0134908
doi: 10.1371/journal.pone.0134908 pubmed: 26331946 pmcid: 4557954
Nazareth TM, Sudatti DB, Machado G (2016) Chemical defense as a condition-dependent trait in harvestmen. J Chem Ecol 42:1047–1051
doi: 10.1007/s10886-016-0749-0 pubmed: 27539587
Prestrude AM, Crawford FT (1970) Tonic immobility in the lizard, Iguana iguana. Anim Behav 18:391–395. https://doi.org/10.1016/S0003-3472(70)80052-5
doi: 10.1016/S0003-3472(70)80052-5
Pueta M, Ardanaz D, Tallone JC (2021) Habituation in anuran tadpoles and the role of risk uncertainty. Anim Cogn. https://doi.org/10.1007/s10071-021-01534-z
doi: 10.1007/s10071-021-01534-z pubmed: 34302566
Raderschall CA, Magrath RD, Hemmi JM (2011) Habituation under natural conditions: model predators are distinguished by approach direction. J Exp Biol 214:4209–4216. https://doi.org/10.1242/jeb.061614
doi: 10.1242/jeb.061614 pubmed: 22116764
Randlett O, Haesemeyer M, Forkin G, Shoenhard H, Schier AF, Engert F, Granato M (2019) Distributed plasticity drives visual habituation learning in larval zebrafish. Curr Biol 29:1337-1345.e4. https://doi.org/10.1016/j.cub.2019.02.039
doi: 10.1016/j.cub.2019.02.039 pubmed: 30955936 pmcid: 6545104
Rankin CH, Abrams T, Barry RJ, Bhatnagar S, Clayton DF, Colombo J, Coppola G, Geyer MA, Glanzman DL, Marsland S, McSweeney FK, Wilson DA, Wu C, Thompson RF (2009) Habituation revisited: An updated and revised description of the behavioral characteristics of habituation. Neurobiol Learn Mem 92:135–138. https://doi.org/10.1016/j.nlm.2008.09.012
doi: 10.1016/j.nlm.2008.09.012 pubmed: 18854219
Rodríguez-Prieto I, Fernández-Juricic E, Martín J (2006) Anti-predator behavioral responses of mosquito pupae to aerial predation risk. J Insect Behav 19:373–381. https://doi.org/10.1007/s10905-006-9033-4
doi: 10.1007/s10905-006-9033-4
Rodríguez-Prieto I, Martín J, Fernández-Juricic E (2010) Habituation to low-risk predators improves body condition in lizards. Behav Ecol Sociobiol 64:1937–1945. https://doi.org/10.1007/s00265-010-1004-
doi: 10.1007/s00265-010-1004-
Rushford NB, Burnett AL, Maynard R (1963) Behavior in hydra: contraction responses of Hydra pirardi to mechanical and light stimuli. Science 139:760–761. https://doi.org/10.1126/science.139.3556.760
doi: 10.1126/science.139.3556.760
Segovia JMG, Del-Claro K, Willemart RH (2015) Defences of a Neotropical harvestman against different levels of threat by the recluse spider. Behaviour 152:757–773. https://doi.org/10.1163/1568539X-00003252
doi: 10.1163/1568539X-00003252
Shettleworth SJ. (2010) Cognition, evolution, and behavior, 2nd edn. Oxford University Press, New York
Silva MS, Willemart RH, Carbayo F (2018) Sticky flatworms (Platyhelminthes) kill armored harvestmen (Arachnida, Opiliones) but are not immune to the prey′s weapons. J Zool 306:88–94. https://doi.org/10.1111/jzo.12570
doi: 10.1111/jzo.12570
Tomsic D, Massoni V, Maldonado H (1993) Habituation to a danger stimulus in two semiterrestrial crabs: ontogenic, ecological and opioid modulation correlates. J Comp Physiol A 173:621–633. https://doi.org/10.1007/BF00197770
doi: 10.1007/BF00197770
Wolfe KD, Wainwright ML, Smee DL, Mozzachiodi R (2016) Eat or be eaten? Modifications of Aplysia californica feeding behaviour in response to natural aversive stimuli. Anim Behav 120:123–133. https://doi.org/10.1016/j.anbehav.2016.07.030
doi: 10.1016/j.anbehav.2016.07.030
Zangrossi H, File SE (1992) Behavioral consequences in animal tests of anxiety and exploration of exposure to cat odor. Brain Res Bull 29:381–388. https://doi.org/10.1016/0361-9230(92)90072-6
doi: 10.1016/0361-9230(92)90072-6 pubmed: 1393611

Auteurs

Guilherme Ferreira Pagoti (GF)

Laboratório de Ecologia Sensorial e Comportamento de Artrópodes, Escola de Artes, Ciências e Humanidades, Universidade de São Paulo, Rua Arlindo Béttio, 1000, Ermelino Matarazzo, São Paulo, SP, 03828-000, Brazil. guilherme.pagoti@hotmail.com.
Programa de Pós-Graduação em Zoologia, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, 321, Travessa 14, Cidade Universitária, São Paulo, SP, 05508-090, Brazil. guilherme.pagoti@hotmail.com.

Jerry A Hogan (JA)

Department of Psychology, University of Toronto, 100 St. George Street, 4th Floor Sidney Smith Hall, Toronto, Ontario, M5S 3G3, Canada.

Rodrigo Hirata Willemart (RH)

Laboratório de Ecologia Sensorial e Comportamento de Artrópodes, Escola de Artes, Ciências e Humanidades, Universidade de São Paulo, Rua Arlindo Béttio, 1000, Ermelino Matarazzo, São Paulo, SP, 03828-000, Brazil.
Programa de Pós-Graduação em Zoologia, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, 321, Travessa 14, Cidade Universitária, São Paulo, SP, 05508-090, Brazil.

Classifications MeSH