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.
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
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
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
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
Brown WL, Eisner T, Whitaker RH (1970) Allomones and kairomones: transspecific chemical messengers. Bioscience 20:21–22
Burghardt GM (1970) Intraspecific geographic variation in chemical food cue preferences of newborn garter snakes (Thamnophis sirtalis). Behav 36:246–257
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
Carducci JP, Jakob EM (2000) Rearing environment affects behaviour of jumping spiders. Anim Behav 59:39–46
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
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
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
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
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
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
Clark RJ, Harland DP, Jackson RR (2000a) Speculative hunting by an araneophagic salticid spider. Behaviour 137:1601–1612
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
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
Davies NB, Krebs JR, West SA (2012) An introduction to behavioural ecology. John Wiley & Sons, New Jersey
Fischer A (2019) Chemical communication in spiders—a methodological review. J Arachnol 47:1–27
Foster SA, Endler JA (1999) Geographic variation in behavior: perspectives on evolutionary mechanisms. Oxford University Press, Oxford
Gaskett AC (2007) Spider sex pheromones: emission, reception, structures, and functions. Biol Rev 82:26–48
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
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
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
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
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
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
Jackson RR (1987) Comparative study of releaser pheromones associated with the silk of jumping spiders (Araneae, Salticidae). N Z J Zool 14:1–10
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
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
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
Jackson RR, Cross FR (2015) Mosquito-terminator spiders and the meaning of specialization. J Arachnol 43:123–142
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
Jackson RR, Nelson XJ (2012) Specialized exploitation of ants (Hymenoptera: Formicidae) by spiders (Araneae). Myrmecol News 17:33–49
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
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
Jackson RR, Clark RJ, Harland DP (2002) Behavioural and cognitive influences of kairomones on an araneophagic spider. Behaviour 139:749–775
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
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
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
Khalidi MA (2016) Innateness as a natural cognitive kind. Philos Psychol 29:319–333
Land MF, Nilsson D-E (2012) Animal eyes, 2nd edn. Oxford University Press, Oxford
Leander BS (2020) Predatory protists. Curr Biol 30:R451–R520
Maddison W (2015) A phylogenetic classification of jumping spiders (Araneae: Salticidae). J Arachnol 43:231–292
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
Morehouse N (2020) Spider vision. Curr Biol 30:R963–R983
Nelson XJ, Jackson RR (2009) Collective Batesian mimicry of ant groups by aggregating spiders. Anim Behav 78:123–129
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
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
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
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
Nordlund DA, Lewis WJ (1976) Terminology of chemical releasing stimuli in intraspecific and interspecific interactions. J Chem Ecol 2:211–220
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
Pekár S, Toft S (2015) Trophic specialisation in a predatory group: the case of prey-specialised spiders (Araneae). Biol Rev 90:744–761
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
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
Pigliucci M (2005) Evolution of phenotypic plasticity: where are we going now? Trends Ecol Evol 20:481–486
Platnick NI (2020) Spiders of the world: a natural history. Princeton University Press, Princeton
Prószyński J (2017) Pragmatic classification of the world’s Salticidae (Araneae). Ecol Montenegrina 12:1–133
Punzo F (2002a) Food imprinting and subsequent prey preference in the lynx spider, Oxyopes salticus (Araneae: Oxyopidae). Behav Proc 58:177–181
Punzo F (2002b) Early experience and prey preference in the lynx spider, Oxyopes salticus Hentz (Araneae: Oxyopidae). Entomol Am N Y 110:255–259
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
Riechert SE (1993) The evolution of behavioral phenotypes: lessons learned from divergent spider populations. Adv Study Behav 22:103–134
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
Ruther J, Meiners T, Steidle JLM (2002) Rich in phenomenon–lacking in terms. A classification of Kairomones. Chemoecology 12:161–167
Rutledge CE, Silk PJ, May P (2014) Use of contact chemical cues in prey discrimination by Cerceris fumipennis. Entomol Exp Appl 153:93–105
Schulz S (2013) Spider pheromones—a structural perspective. J Chem Ecol 39:1–14
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
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
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
Vet LEM, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Ann Rev Entomol 37:141–172
Via S, Lande R (1985) Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution 39:505–522
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
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
West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, New York
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
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
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.
Author information
Authors and Affiliations
Contributions
AMC carried out experiments and analysed the data. Both authors conceptualised the study and contributed to the writing of the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Ethics approval
All applicable international, national, and institutional guidelines for the care and use of animals were followed.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10164-021-00725-y