Is the predation risk of mate-searching different between the sexes?

Abstract

In animals that communicate for pair formation, generally one sex invests more effort in mate searching. Differential predation risk of mate searching between the sexes is hypothesised to determine which sex invests more effort in mate searching. Although searching by males is prevalent in most animals, in orthopteran insects and some other taxa females physically move to localise signalling males who are predominantly sedentary. Although the two sexes thus share mate searching effort in orthopterans, their behavioural strategies are different and sexual selection theory predicts that signalling males may be following the riskier strategy and incurring higher costs. However, relative levels of risk posed by the two mate searching strategies remain largely unexplored. Hence, we estimated the relative predation risk experienced in natural populations by signalling males and responding females. We did this by quantifying predation risk as a probability of mortality in the context of acoustic communication in a tree cricket, Oecanthus henryi from its ecologically relevant predator, a lynx spider, Peucetia viridans. Spiders may perceive calling in males and movement in females by their ability to detect both airborne acoustic cues and substrate-borne vibratory cues. Probability of mortality was quantified by partitioning it into three spatial components at which crickets and spiders interact, using a combination of extensive field observations and manipulative experiments in a semi-natural setup. We found no differences in predation risk faced by calling males and responding females, supporting the prediction that similar sex-specific costs can explain shared mate searching responsibilities. Our findings therefore suggest that direct benefits offered by males to females upon pair formation may better explain shared mate searching effort between the sexes in orthopterans.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Data availability

The datasets generated and analysed during the current study can be accessed at https://doi.org/10.6084/m9.figshare.7794131.v1.

References

  1. Alem S, Koselj K, Siemers BM, Greenfield MD (2011) Bat predation and the evolution of leks in acoustic moths. Behav Ecol Sociobiol 65:2105–2116

    Article  Google Scholar 

  2. Andersson MB (1994) Sexual selection. Princeton University Press, Princeton

    Google Scholar 

  3. Arnqvist G, Nilsson T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav 60:145–164

    Article  CAS  Google Scholar 

  4. Balakrishnan R (2016) Behavioral ecology of insect acoustic communication. In: Pollack GS, Mason AC, Popper AN, Fay RR (eds) Insect hearing. Springer International Publishing, Bern, pp 49–80

    Google Scholar 

  5. Barth FG (2002) A spider’s world: senses and behavior. Springer, New York

    Google Scholar 

  6. Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368

    Article  CAS  Google Scholar 

  7. Bell PD (1979) Acoustic attraction of herons by crickets. J N Y Entomol Soc 87:126–127

    Google Scholar 

  8. Belwood JJ, Morris GK (1987) Bat predation and its influence on calling behavior in neotropical katydids. Science 238:64–67

    Article  CAS  Google Scholar 

  9. Bhattacharya M (2016) Investigating pattern recognition and bi-coordinate sound localization in the tree cricket species. Ph.D. dissertation, Centre for Ecological Sciences, Indian Institute of Science, Bangalore, India

  10. Brechbühl R, Casas J, Bacher S (2011) Diet choice of a predator in the wild: overabundance of prey and missed opportunities along the prey capture sequence. Ecosphere 2:1–15

    Article  Google Scholar 

  11. Byers J, Dunn S (2012) Bateman in nature: predation on offspring reduces the potential for sexual selection. Science 338:802–804

    Article  CAS  PubMed  Google Scholar 

  12. Cumming G, Finch S (2005) Inference by eye: confidence intervals and how to read pictures of data. Am Psychol 60:170–180

    Article  PubMed  Google Scholar 

  13. Dangles O, Ory N, Steinmann T, Christides JP, Casas J (2006) Spider’s attack versus cricket’s escape: velocity modes determine success. Anim Behav 72:603–610

    Article  Google Scholar 

  14. Darwin C (1871) The descent of man and selection in relation to sex. John Murray, London

    Google Scholar 

  15. Deb R (2015) Mate choice, mate sampling and baffling behaviour in the tree cricket. Ph.D. dissertation, Centre for Ecological Sciences, Indian Institute of Science, Bangalore, India

  16. Ercit K (2013) Size and sex of cricket prey predict capture by a sphecid wasp. Ecol Entomol 39:195–202

    Article  Google Scholar 

  17. Fromhage L, Jennions MD, Kokko H (2016) The evolution of sex roles in mate searching. Evolution 70:617–624

    Article  Google Scholar 

  18. Fulton BB (1915) The tree crickets of New York: life history and bionomics. N Y Agric Exp Station Tech Bull 42:1–47

    Google Scholar 

  19. Gwynne DT (1987) Sex-biased predation and the risky mate-locating behaviour of male tick-tock cicadas (Homoptera: Cicadidae). Anim Behav 35:571–576

    Article  Google Scholar 

  20. Gwynne DT (1995) Phylogeny of the Ensifera (Orthoptera): a hypothesis supporting multiple origins of acoustical signalling, complex spermatophores and maternal care in crickets, katydids, and weta. J Orthop Res 4:203–218

    Article  Google Scholar 

  21. Gwynne DT (1997) The evolution of edible ‘sperm sacs’ and other forms of courtship feeding in crickets, katydids and their kin (Orthoptera: Ensifera). In: Choe JC, Crespi BJ (eds) The evolution of mating systems in insects and arachnids. Cambridge University Press, Cambridge, pp 110–129

    Google Scholar 

  22. Hammerstein P, Parker GA (1987) Sexual selection: games between the sexes. In: Bradbury JW, Andersson MB (eds) Sexual selection: testing the alternatives. Wiley, Chichester, pp 119–142

    Google Scholar 

  23. Hebblewhite M, Merrill EH, McDonald TL (2005) Spatial decomposition of predation risk using resource selection functions: an example in a wolf–elk predator–prey system. Oikos 111:101–111

    Article  Google Scholar 

  24. Hedrick AV, Kortet R (2006) Hiding behaviour in two cricket populations that differ in predation pressure. Anim Behav 72:1111–1118

    Article  Google Scholar 

  25. Heller KG (1992) Risk shift between males and females in the pair-forming behavior of bushcrickets. Naturwissenschaften 79:89–91

    Article  Google Scholar 

  26. Heller KG, Arlettaz R (1994) Is there a sex ratio bias in the bushcricket prey of the scops owl due to predation on calling males? J Orthop Res 2:41–42

    Article  Google Scholar 

  27. Holling CS (1959) The components of predation as revealed by a study of small-mammal predation of the European Pine Sawfly. Can Entomol 91:293–320

    Article  Google Scholar 

  28. Houghton CO (1909) Observations on the mating habits of Oecanthus. Entomol News 274–279

  29. Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640

    Article  Google Scholar 

  30. Lohrey AK, Clark DL, Gordon SD, Uetz GW (2009) Antipredator responses of wolf spiders (Araneae: Lycosidae) to sensory cues representing an avian predator. Anim Behav 77:813–821

    Article  Google Scholar 

  31. Magnhagen C (1991) Predation risk as a cost of reproduction. TREE 6:183–186

    CAS  PubMed  Google Scholar 

  32. Manly BFJ (2006) Randomization, bootstrap and Monte Carlo methods in biology, 3rd edn. Chapman and Hall/CRC, New York

    Google Scholar 

  33. McCartney J, Kokko H, Heller KG, Gwynne DT (2012) The evolution of sex differences in mate searching when females benefit: new theory and a comparative test. Proc R Soc Lond B Biol Sci 279:1225–1232

    Article  CAS  Google Scholar 

  34. Metrani S, Balakrishnan R (2005) The utility of song and morphological characters in delineating species boundaries among sympatric tree crickets of the genus Oecanthus (Orthoptera: Gryllidae: Oecanthinae): a numerical taxonomic approach. J Orthop Res 14:1–16

    Article  Google Scholar 

  35. Nakagawa S, Cuthill IC (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev Camb Philos Soc 82:591–605

    Article  PubMed  Google Scholar 

  36. O’Neill KM, O’Neill RP (2003) Sex allocation, nests, and prey in the grass-carrying wasp Isodontia mexicana (Saussure) (Hymenoptera: Sphecidae). J Kans Entomol Soc 76:447–454

    Google Scholar 

  37. Ponce-Wainer JX, Del Castillo RC (2008) Female mate choice and no detected predation risk in relation to the calling song of Oecanthus niveus (Gryllidae: Oecanthinae). Ann Entomol Soc Am 101:260–265

    Article  Google Scholar 

  38. R Core Team (2017) A language and environment for statistical computing. R Foundation for Statistical Computing. http://www.R-project.org

  39. Raghuram H, Deb R, Nandi D, Balakrishnan R (2015) Silent katydid females are at higher risk of bat predation than acoustically signalling katydid males. Proc R Soc Lond B Biol Sci 282:20142319

    Article  Google Scholar 

  40. Rodríguez-Muñoz R, Bretman A, Slate J, Walling CA, Tregenza T (2010) Natural and sexual selection in a wild insect population. Science 328:1269–1272

    Article  CAS  PubMed  Google Scholar 

  41. Ryan MJ, Tuttle MD, Rand SA (1982) Bat predation and sexual advertisement in a neotropical anuran. Am Nat 119:136–139

    Article  Google Scholar 

  42. Shamble PS, Menda G, Golden JR, Nitzany EI, WaldenK Beatus T, Elias DO, Cohen I, Miles RN, Hoy RR (2016) Airborne acoustic perception by a jumping spider. Curr Biol 26:2913–2920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Sih A (2005) Predator–prey space use as an emergent outcome of a behavioral response race. In: Barbosa P, Castellanos I (eds) Ecology of predator–prey interactions. Oxford University Press, New York, pp 240–255

    Google Scholar 

  44. Storm JJ, Lima SL (2010) Mothers forewarn offspring about predators: a transgenerational maternal effect on behavior. Am Nat 175:382–390

    Article  PubMed  Google Scholar 

  45. Thornhill R (1979) Male and female sexual selection and the evolution of mating strategies in insects. In: Blum M, Blum N (eds) Sexual selection and reproductive competition in insects. Academic Press, New York, pp 81–121

    Google Scholar 

  46. Trivers RL (1972) Sexual selection and parental investment. In: Campbell BG (ed) Sexual selection and the descent of man. Aldine Press, Chicago, pp 136–179

    Google Scholar 

  47. Tuttle MD, Ryan MJ (1981) Bat predation and the evolution of frog vocalizations in the neotropics. Science 214:677–678

    Article  CAS  PubMed  Google Scholar 

  48. Walker TJJ (1957) Specificity in the response of female tree crickets (Orthoptera, Gryllidae, Oecanthinae) to calling songs of the males. Ann Entomol Soc Am 50:626–636

    Article  Google Scholar 

  49. Walker TJJ (1964) Experimental demonstration of a cat locating orthopteran prey by the prey’s calling song. The Florida Entomol 47:163–165

    Article  Google Scholar 

  50. Wickham W (2009) ggplot2: Elegant graphics for data analysis. Springer, New York

    Google Scholar 

  51. Zuk M, Kolluru GR (1998) Exploitation of sexual signals by predators and parasitoids. Q Rev Biol 73:415–438

    Article  Google Scholar 

  52. Zuk M, Rotenberry JT, Tinghitella RM (2006) Silent night: adaptive disappearance of a sexual signal in a parasitized population of field crickets. Biol Lett 2:521–524

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank the DBT-IISc partnership programme (2012–2017) of the Department of Biotechnology, Government of India for funding the fieldwork and Ministry of Human Resource Development, Government of India for funding the research fellowship of VRT. We thank the DST-FIST program of the Govt. of India for some of the equipment used in the study. We thank Diptarup Nandi, Rittik Deb and Monisha Bhattacharya for helpful discussions and Diptarup Nandi for comments on the manuscript. We thank Mr. B. Sridhar (Garden and Nursery Technical Officer) and Nursery staff for their support. We would like to thank Ayan, Babu, Chaithra, Chirag, Dakshin, Girish, Himamshu, Harsha, Ismail, Lakshmipriya, Manoj, Meenakshi, Meghana, Murthy, Shivaraju, Sidanth, Sonu, Sriniketh, Srinivasan, Sunaina and Vinayaka for their help in making behavioural observations and Manjunatha Reddy for his assistance in fieldwork.

Author information

Affiliations

Authors

Contributions

VRT participated in conceptualising and designing the study, carried out data collection and analysis and wrote the manuscript. KI contributed to data analysis, interpretation and writing the manuscript. RB contributed to conceptualising and designing the study, interpretation of data and writing the manuscript.

Corresponding author

Correspondence to Viraj R. Torsekar.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All behavioural data sampling and experiments were performed in accordance with the national guidelines for the ethical treatment of animals laid out by the National Biodiversity Authority (Government of India).

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 66 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Torsekar, V.R., Isvaran, K. & Balakrishnan, R. Is the predation risk of mate-searching different between the sexes?. Evol Ecol 33, 329–343 (2019). https://doi.org/10.1007/s10682-019-09982-3

Download citation

Keywords

  • Communication
  • Sex-specific costs
  • Sex roles
  • Predation risk
  • Mate searching
  • Crickets