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Inter-population variation and phenotypic plasticity in kairomone use by a poly-specialist spider-eating predator

Abstract

Previous research on Cyrba algerina (Araneae, Salticidae) has shown this jumping spider expresses predatory specialisation with respect to spiders as prey as well as inter-population variation in responsiveness to prey-spider odour. However, this earlier research pertained to a single prey species (Oecobius machadoi) and only field-collected C. algerina individuals were tested. Here we extend the previous research by using laboratory-reared, as well as field-collected, individuals of C. algerina and also by using another prey-spider species, Zelotes thorelli, as well as O. machadoi. Two localities in Portugal are considered, Sintra where C. algerina and both prey species are abundant and Tavira where C. algerina is present but neither prey species has been found. In olfactometer experiments, field-collected C. algerina individuals from Sintra, but not Tavira, were attracted to the odour of both prey species. Next, we tested the response of laboratory-reared Sintra C. algerina individuals that had been maintained with no prior experience with the odour of either prey species. We found no evidence of laboratory-reared individuals being attracted to the odour of either prey species in the olfactometer. These findings suggest that prior experience mediates responsiveness of C. algerina to the odour of local prey.

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Availability of data and materials

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  • Aguilar-Arguello S, Nelson XJ (2021) Jumping spiders: an exceptional group for comparative cognition studies. Learn Behav. https://doi.org/10.3758/s13420-020-00445-2

    Article  PubMed  Google Scholar 

  • Auld JR, Agrawal AA, Relyea RA (2010) Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proc Roy Soc Lond B 277:503–511

    Google Scholar 

  • Ayelo PM, Pirk CWW, Yusuf AA, Chailleux A, Mohamed SA, Deletre E (2021) Exploring the kairomone-based foraging behaviour of natural enemies to enhance biological control: a review. Front Ecol Evol 9:641974

    Google Scholar 

  • Blest AD, O’Carroll DC, Carter M (1990) Comparative ultrastructure of layer I mosaics in principal eyes of jumping spiders: the evolution of regular arrays of light guides. Cell Tiss Res 26:445–460

    Google Scholar 

  • Brown WL, Eisner T, Whitaker RH (1970) Allomones and kairomones: transspecific chemical messengers. Bioscience 20:21–22

    CAS  Google Scholar 

  • Burghardt GM (1970) Intraspecific geographic variation in chemical food cue preferences of newborn garter snakes (Thamnophis sirtalis). Behav 36:246–257

    Google Scholar 

  • Cade DE, Carey N, Domenici P, Potvin J, Goldbogen JA (2020) Predator-informed looming stimulus experiments reveal how large filter feeding whales capture highly maneuverable forage fish. Proc Natl Acad Sci 117:472–478

    CAS  PubMed  Google Scholar 

  • Carducci JP, Jakob EM (2000) Rearing environment affects behaviour of jumping spiders. Anim Behav 59:39–46

    CAS  PubMed  Google Scholar 

  • Carvalho LM, Bueno VHP, Castane C (2011) Olfactory response towards its prey Frankliniella occidentalis of wild and laboratory-reared Orius insidiosus and Orius laevigatus. J Appl Entomol 135:177–183

    Google Scholar 

  • Cerveira AM, Jackson RR (2011) Interpopulation variation in oecobiid-specific prey-capture behaviour and kairomone use by Cyrba algerina, an araneophagic jumping spider from Portugal. J Ethol 29:121–129

    Google Scholar 

  • Cerveira AM, Jackson RR (2013a) Love is in the air: olfaction-based mate-odour identification by jumping spiders from the genus Cyrba. J Ethol 31:29–34

    Google Scholar 

  • Cerveira AM, Jackson RR (2013b) Love is in the air and on the ground: olfactory and tactile cues elicit visual courtship behavior by Cyrba males (Araneae: Salticidae). J Arachnol 41:374–380

    Google Scholar 

  • Cerveira AM, Jackson RR, Guseinov EF (2003) Stalking decisions of web-invading araneophagic jumping spiders from Australia, Azerbaijan, Israel, Kenya, Portugal, and Sri Lanka: the opportunistic smokescreen tactics of Brettus, Cocalus, Cyrba, and Portia N Z. J Zool 30:21–30

    Google Scholar 

  • Cerveira AM, Jackson RR, Nelson XJ (2019) Dim-light vision in jumping spiders (Araneae, Salticidae): identification of prey and rivals. J Exp Biol 222:jeb198069. https://doi.org/10.1242/jeb.198069

  • Cerveira AM, Nelson XJ, Jackson RR (2021) Spatial acuity-sensitivity trade-off in the principal eyes of a jumping spider: possible adaptations to a ‘blended’ lifestyle. J Comp Physiol A 207:437–448

    Google Scholar 

  • Clark RJ, Harland DP, Jackson RR (2000a) Speculative hunting by an araneophagic salticid spider. Behaviour 137:1601–1612

    Google Scholar 

  • Clark RJ, Jackson RR, Cutler B (2000b) Chemical cues from ants influence predatory behavior in Habrocestum pulex (Hentz), an ant-eating jumping spider (Araneae, Salticidae). J Arachnol 28:299–341

    Google Scholar 

  • Cross FR, Carvell GE, Jackson RR, Grace RC (2020) Arthropod Intelligence? The case for Portia. Front Psychol. https://doi.org/10.3389/fpsyg.2020.568049

  • Curio E (1976) The ethology of predation. Springer-Verlag, Berlin

    Google Scholar 

  • Davies NB, Krebs JR, West SA (2012) An introduction to behavioural ecology. John Wiley & Sons, New Jersey

    Google Scholar 

  • Fischer A (2019) Chemical communication in spiders—a methodological review. J Arachnol 47:1–27

    Google Scholar 

  • Foster SA, Endler JA (1999) Geographic variation in behavior: perspectives on evolutionary mechanisms. Oxford University Press, Oxford

    Google Scholar 

  • Gaskett AC (2007) Spider sex pheromones: emission, reception, structures, and functions. Biol Rev 82:26–48

    Google Scholar 

  • Gemeno C, Yeargan KV, Haynes KF (2000) Aggressive chemical mimicry by the bolas spider Mastophora hutchinsoni: identification and quantification of a major prey’s sex pheromone components in the spider’s volatile emissions. J Chem Ecol 26:1235–1243

    CAS  Google Scholar 

  • Guseinov EF, Cerveira AM, Jackson RR (2004) The predatory strategy, natural diet, and life cycle of Cyrba algerina, an araneophagic jumping spider (Salticidae: Spartaeinae) from Azerbaijan. N Z J Zool 31:291–303

    Google Scholar 

  • Harland DP, Jackson RR (2000) Cues by which Portia fimbriata, an araneophagic jumping spider, distinguishes jumping-spider prey from other prey. J Exp Biol 203:3485–3494

    CAS  PubMed  Google Scholar 

  • Harland DP, Jackson RR (2001) Prey classification by Portia fimbriata, a salticid spider that specializes at preying on other salticids: species that elicit cryptic stalking. J Zool Lond 255:445–460

    Google Scholar 

  • Harland DP, Li D, Jackson RR (2012) How jumping spiders see the world. In: Lazareva O, Shimizu T, Wasserman EA (eds) How animals see the world: comparative behavior, biology, and evolution of vision. Oxford University Press, Oxford, pp 133–164

    Google Scholar 

  • IBM Corp (2017) IBM SPSS statistics for windows. IBM Corp., Armonk, NY. Retrieved from https://hadoop.apache.org

  • Jackson RR (1980) The mating strategy of Phidippus johnsoni (Araneae, Salticidae): IV. Interpopulational variation in courtship persistence. Behav Ecol Sociobiol 6:257–263

    Google Scholar 

  • Jackson RR (1987) Comparative study of releaser pheromones associated with the silk of jumping spiders (Araneae, Salticidae). N Z J Zool 14:1–10

    CAS  Google Scholar 

  • Jackson RR (1990) Predatory versatility and intraspecific interactions of Cyrba algerina and C. ocellata, web-invading spartaeine jumping spiders (Araneae, Salticidae). N Z J Zool 17:157–168

    Google Scholar 

  • Jackson RR (2000) Prey preferences and visual discrimination ability of Brettus, Cocalus and Cyrba, araneophagic jumping spiders (Araneae: Salticidae) from Australia, Kenya and Sri Lanka. N Z J Zool 27:29–39

    Google Scholar 

  • Jackson RR, Carter CM (2001) Geographic variation in reliance on trial-and-error signal derivation by Portia labiata, an araneophagic jumping spider from the Philippines. J Insect Behav 14:799–827

    Google Scholar 

  • Jackson RR, Cross FR (2015) Mosquito-terminator spiders and the meaning of specialization. J Arachnol 43:123–142

    Google Scholar 

  • Jackson RR, Li D (1998) Prey preferences and visual discrimination ability of Cyrba algerina, an araneophagic jumping spider (Araneae: Salticidae) with primitive retinae. Israel J Zool 44:227–242

    Google Scholar 

  • Jackson RR, Nelson XJ (2012) Specialized exploitation of ants (Hymenoptera: Formicidae) by spiders (Araneae). Myrmecol News 17:33–49

    Google Scholar 

  • Jackson RR, Wilcox RS (1990) Aggressive mimicry, prey-specific predatory behaviour and predator recognition in the predator-prey interactions of Portia fimbriata and Euryattus sp., jumping spiders from Queensland. Behav Ecol Sociobiol 26:111–119

    Google Scholar 

  • Jackson RR, Wilcox RS (1993) Predator-prey co-evolution of Portia fimbriata and Euryattus sp., jumping spiders from Queensland. Mem Queensland Mus 33:557–560

    Google Scholar 

  • Jackson RR, Clark RJ, Harland DP (2002) Behavioural and cognitive influences of kairomones on an araneophagic spider. Behaviour 139:749–775

    Google Scholar 

  • Jackson RR, Nelson XJ, Sune GO (2005) A spider that feeds indirectly on vertebrate blood by choosing female mosquitoes as prey. Proc Natl Acad Sci USA 102:15155–15160

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jackson RR, Cross FR, Carter CM (2006) Geographic variation in a spider’s ability to solve a confinement problem by trial and error. Int J Comp Psychol 19:282–296

    Google Scholar 

  • Jackson RR, Li D, Woon JRW, Hashim R, Cross FR (2014) Intricate predatory decisions by a mosquito-specialist spider from Malaysia. Roy Soc Open Sci 1:140131

    Google Scholar 

  • Khalidi MA (2016) Innateness as a natural cognitive kind. Philos Psychol 29:319–333

    Google Scholar 

  • Land MF, Nilsson D-E (2012) Animal eyes, 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  • Leander BS (2020) Predatory protists. Curr Biol 30:R451–R520

    Google Scholar 

  • Maddison W (2015) A phylogenetic classification of jumping spiders (Araneae: Salticidae). J Arachnol 43:231–292

    Google Scholar 

  • Mendel Z, Assael F, Dunkelblum E (2004) Kairomonal attraction of predatory bugs (Heteroptera: Anthocoridae) and brown lacewings (Neuroptera: Hemerobiidae) to sex pheromones of Matsucoccus species (Hemiptera: Matsucoccidae). Biol Control 30:134–440

    CAS  Google Scholar 

  • Morehouse N (2020) Spider vision. Curr Biol 30:R963–R983

    Google Scholar 

  • Nelson XJ, Jackson RR (2009) Collective Batesian mimicry of ant groups by aggregating spiders. Anim Behav 78:123–129

    Google Scholar 

  • Nelson XJ, Jackson RR (2011) Flexibility in the foraging strategies of spiders. In: Herberstein ME (ed) Spider behaviour: flexibility and versatility. Cambridge University Press, Cambridge, pp 31–56

    Google Scholar 

  • Nelson XJ, Garnett DT, Evans CS (2010) Receiver psychology and the design of the deceptive caudal luring signal of the death adder. Anim Behav 79:555–561

    Google Scholar 

  • Nelson XJ, Warui CM, Jackson RR (2012) Widespread reliance on olfactory sex and species identification by lyssomanine and spartaeine jumping spiders. Biol J Linn Soc 107:664–677

    Google Scholar 

  • Nilsson D-E (2021) The diversity of eyes and vision. Annu Rev Vis Sci 7:19–41. https://doi.org/10.1146/annurev-vision-121820-074736

    Article  PubMed  Google Scholar 

  • Nordlund DA, Lewis WJ (1976) Terminology of chemical releasing stimuli in intraspecific and interspecific interactions. J Chem Ecol 2:211–220

    Google Scholar 

  • O’Neill E (2015) Relativizing innateness: innateness as the insensitivity of the appearance of a trait with respect to specified environmental variation. Biol Philos 30:211–225

    Google Scholar 

  • Pekár S, Toft S (2015) Trophic specialisation in a predatory group: the case of prey-specialised spiders (Araneae). Biol Rev 90:744–761

    PubMed  Google Scholar 

  • Pekár S, Petrakova L, Sedo O, Korenko S, Zdrahal Z (2018) Trophic niche, capture efficiency and venom profiles of six sympatric ant-eating spider species (Araneae: Zodariidae). Mol Ecol 27:1053–1064

    PubMed  Google Scholar 

  • Persons MH, Rypstra AL (2000) Preference for chemical cues associated with recent prey in the wolf spider Hogna helluo (Araneae: Lycosidae). Ethology 106:27–35

    Google Scholar 

  • Pigliucci M (2005) Evolution of phenotypic plasticity: where are we going now? Trends Ecol Evol 20:481–486

    PubMed  Google Scholar 

  • Platnick NI (2020) Spiders of the world: a natural history. Princeton University Press, Princeton

    Google Scholar 

  • Prószyński J (2017) Pragmatic classification of the world’s Salticidae (Araneae). Ecol Montenegrina 12:1–133

    Google Scholar 

  • Punzo F (2002a) Food imprinting and subsequent prey preference in the lynx spider, Oxyopes salticus (Araneae: Oxyopidae). Behav Proc 58:177–181

    Google Scholar 

  • Punzo F (2002b) Early experience and prey preference in the lynx spider, Oxyopes salticus Hentz (Araneae: Oxyopidae). Entomol Am N Y 110:255–259

    Google Scholar 

  • Rahmani H, Hoffmann D, Walzer A, Schausberger P (2009) Adaptive learning in the foraging behavior of the predatory mite Phytoseiulus persimilis. Behav Ecol 20:946–950

    Google Scholar 

  • Riechert SE (1993) The evolution of behavioral phenotypes: lessons learned from divergent spider populations. Adv Study Behav 22:103–134

    Google Scholar 

  • Riechert SE (1999) The use of behavioral ecotypes in the study of evolutionary processes. In: Endler JA, Foster SA (eds) Geographic variation in behavior: perspectives on evolutionary mechanisms. Oxford University Press, Oxford, pp 3–32

    Google Scholar 

  • Ruther J, Meiners T, Steidle JLM (2002) Rich in phenomenon–lacking in terms. A classification of Kairomones. Chemoecology 12:161–167

    Google Scholar 

  • Rutledge CE, Silk PJ, May P (2014) Use of contact chemical cues in prey discrimination by Cerceris fumipennis. Entomol Exp Appl 153:93–105

    CAS  Google Scholar 

  • Schulz S (2013) Spider pheromones—a structural perspective. J Chem Ecol 39:1–14

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Su KFY, Meier R, Jackson RR, Harland DP, Li D (2007) Convergent evolution of eye ultrastructure and divergent evolution of vision-mediated predatory behaviour in jumping spiders. J Evol Biol 20:1478–1489

    CAS  PubMed  Google Scholar 

  • Torres JP, Lin Z, Watkins, Salcedo MPF, Baskin RP, Elhabian S, Safavi-Hemami H, Taylor D, Tun J, Concepcion GP, Saguil N, Yanagihara AA, Fang Y, McArthur JR, Tae H-S, Finol-Urdaneta RK, Özpolat BD, Olivera BM, Schmidt EW (2021) Small-molecule mimicry hunting strategy in the imperial cone snail, Conus imperialis. Sci Adv 7:eabf2704. https://doi.org/10.1126/sciadv.abf2704

  • Uetz GW, Cangialosi KR (1986) Genetic differences in social behavior and spacing in populations of Metepeira spinipes, a communal-territorial orb weaver (Araneae, Araneidae). J Arachnol 14:159–173

    Google Scholar 

  • Vet LEM, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Ann Rev Entomol 37:141–172

    Google Scholar 

  • Via S, Lande R (1985) Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution 39:505–522

    PubMed  Google Scholar 

  • Via S, Gomulkiewicz R, De Jong G, Scheiner SM, Schlichting CD, Van Tienderen PH (1995) Adaptive phenotypic plasticity: consensus and controversy. Trends Ecol Evol 10:212–217

    CAS  PubMed  Google Scholar 

  • Wanless FR (1984) A review of the spider subfamily Spartaeinae nom. n. (Araneae: Salticidae) with descriptions of six new genera. B Brit Mus, Nat Hist Zool 46:135–205

    Google Scholar 

  • West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, New York

    Google Scholar 

  • World Spider Catalog (2021) Version 22.0. Natural History Museum Bern, online at http://wsc.nmbe.ch. Accessed 18 May 2021

  • Wyatt TD (2003) Pheromones and animal behaviour. Cambridge University Press, Cambridge

    Google Scholar 

  • Ylönen H, Sundell J, Tiilikainen R, Eccard JA, Horne T (2003) Weasels’ (Mustela nivalis nivalis) preference for olfactory cues of the vole (Clethrionomys glareolus). Ecology 84:1447–1452

    Google Scholar 

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Acknowledgements

AMC thanks Fundação para a Ciência e a Tecnologia for the financial support it provided through national funds. We would also like to thank the National Geographic Society (grant (WW-146R-17) and the Royal Society of New Zealand Marsden Fund for financial assistance to RRJ.

Funding

Our research was assisted by grants to RRJ from the Royal Society of New Zealand Marsden Fund (M1096) and the National Geographic Society (WW-146R-17), and AMC from FCT/MCTES (UIDP/50017/2020 + UIDB/50017/2020) through national funds. AMC is currently funded by national funds (OE), through FCT—Fundação para a Ciência e a Tecnologia, I.P., in the scope of the framework contract foreseen in the numbers 4, 5 and 6 of the article 23, of the Decree-Law 57/2016, of August 29, changed by Law 57/2017, of July 19.

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AMC carried out experiments and analysed the data. Both authors conceptualised the study and contributed to the writing of the final manuscript.

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Correspondence to Ana M. Cerveira.

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Cerveira, A.M., Jackson, R.R. Inter-population variation and phenotypic plasticity in kairomone use by a poly-specialist spider-eating predator. J Ethol 40, 37–48 (2022). https://doi.org/10.1007/s10164-021-00725-y

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Keywords

  • Foraging kairomone
  • Araneophagy
  • Predatory specialisation
  • Jumping spider
  • Salticidae