Leaf me alone: visual constraints on the ecology of social group formation

  • Elliott P. SteeleEmail author
  • Mark E. LaidreEmail author
Original Article


Complex environments may place constraints on animal sensory perception. However, little is known about how ecological constraints impact the formation of animal social groups, which ultimately necessitate that conspecifics detect one another. Here we studied the fission–fusion social groups of highly social terrestrial hermit crabs (Coenobita compressus), which frequently split and recombine, requiring individuals to actively sense the location of conspecifics. We manipulated the environment by relocating abundant natural fallen leaves on the beach, testing how and why this debris may constrain social group formation. Our experiments revealed that fallen leaves impose a fundamental limit on social grouping, with experimentally simulated groups attracting significantly fewer conspecifics (75% less) if they were surrounded by leaves. This constraint on social grouping was not the result of leaves acting as a physical barrier to movement. Furthermore, leaves only hindered visual perception of conspecifics and did not hinder other modalities besides vision. By experimentally moving leaves above the horizon, such that they no longer blocked animals’ field of view, we found that the impact of these visual constraints on grouping could be effectively abolished. Broadly, these experiments elucidate how complex environments impose sensory constraints on social animals’ ability to navigate toward groups.

Significance statement

Social animals must be able to detect and orient toward conspecifics if they are to form social groups. Features of the environment, however, may impose constraints on sensory perception that interfere with the detection of conspecifics. Here we studied social hermit crabs, which form social groupings within a complex habitat that contains abundant fallen leaves along the beach–forest interface. By experimentally manipulating leaves, we show that these seemingly insignificant ecological materials create visual constraints that block the cues free-wandering individuals normally use to orient toward social groups. Our study thus reveals how common aspects of the environment can exert major constraints on sensory perception, thereby severely limiting social group formation and ultimately sociality.


Social grouping Fission–fusion Sensory ecology Visual constraints Environmental noise 



We thank Osa Conservation staff and the Laidre lab for assistance in the field. This study was supported by a EEES/GAANN fellowship to ES and Dartmouth College startup funds to ML. For helpful feedback, we thank Mike Webster and an anonymous reviewer as well as the audience of a conference talk on these experiments at the summer 2018 International Society for Behavioral Ecology in Minneapolis.

Author contributions

ML conceived the study and designed the experiments; both authors then worked jointly to collect the data in the field, analyze the data, and write the manuscript together.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Supplementary material

265_2019_2662_MOESM1_ESM.docx (4.2 mb)
ESM 1 (DOCX 4318 kb)


  1. Alcaraz G, Jofre GI (2017) Aggressiveness compensates for low muscle strength and metabolic disadvantages in shell fighting: an outcome of the individual’s past. Behav Ecol Sociobiol 71:87CrossRefGoogle Scholar
  2. Bates KM, Laidre ME (2018) When to socialize: perception of time-sensitive social structures among social hermit crabs. Anim Behav 138:19–27CrossRefGoogle Scholar
  3. Bear A, Hasson O (1997) The predatory response of a stalking spider, Plexippus paykulli, to camouflage and prey type. Anim Behav 54:993–998CrossRefGoogle Scholar
  4. Bermudez-Cuamatzin E, Rios-Chelen AA, Gil D, Garcia CM (2010) Experimental evidence for real-time song frequency shift in response to urban noise in a passerine bird. Biol Lett 8:320–320CrossRefGoogle Scholar
  5. Bonnie KE, Earley RL (2007) Expanding the scope for social information use. Anim Behav 74:171–181CrossRefGoogle Scholar
  6. Bradbury JW, Vehrencamp SL (2011) Principles of animal communication, 2nd edn. Sinauer Associates, Sunderland, MAGoogle Scholar
  7. Couzin ID, Laidre ME (2009) Fission-fusion populations. Curr Biol 19:R633–R635CrossRefGoogle Scholar
  8. Cronin TW, Johnsen S, Marshall NJ, Warrant EJ (2014) Visual ecology. Princeton University Press, Princeton, NJCrossRefGoogle Scholar
  9. Dall SRX, Giraldeau L-A, Olsson O, McNamara JM, Stephens DW (2005) Information and its use by animals in evolutionary ecology. Trends Ecol Evol 20:187–193CrossRefGoogle Scholar
  10. Danchin E (2004) Public information: from nosy neighbors to cultural evolution. Science 305:487–491CrossRefGoogle Scholar
  11. Fleishman LJ (1992) The influence of the sensory system and the environment on motion patterns in the visual displays of Anoline lizards and other vertebrates. Am Nat 139:S36–S61CrossRefGoogle Scholar
  12. Girard MB, Elias DO, Kasumovic MM (2015) Female preference for multi-modal courtship: multiple signals are important for male mating success in peacock spiders. Proc R Soc B 282:20152222CrossRefGoogle Scholar
  13. Janzen DH (1983) Costa Rican natural history. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  14. Johnsen S (2012) The optics of life: a biologist’s guide to light in nature. Princeton University Press, Princeton, NJCrossRefGoogle Scholar
  15. Laidre ME (2010) How rugged individualists enable one another to find food and shelter: field experiments with tropical hermit crabs. Proc R Soc B 277:1361–1369CrossRefGoogle Scholar
  16. Laidre ME (2012a) Niche construction drives social dependence in hermit crabs. Curr Biol 22:R861–R863CrossRefGoogle Scholar
  17. Laidre ME (2012b) Homes for hermits: temporal, spatial and structural dynamics as transportable homes are incorporated into a population. J Zool 288:33–40CrossRefGoogle Scholar
  18. Laidre ME (2013a) Eavesdropping foragers use level of collective commotion as public information to target high quality patches. Oikos 122:1505–1511Google Scholar
  19. Laidre ME (2013b) Foraging across ecosystems: diet diversity and social foraging spanning aquatic and terrestrial ecosystems by an invertebrate. Mar Ecol 34:80–89CrossRefGoogle Scholar
  20. Laidre ME (2014) The social lives of hermits. Nat Hist 122:24–29Google Scholar
  21. Laidre ME (2018a) Evolutionary ecology of burrow construction and social life. In: Wellborn GA, Thiel M (eds) Life histories. Oxford University Press, New York, NY, pp 279–301Google Scholar
  22. Laidre ME (2018b) Social cognition in the wild: from lab to field in hermit crabs. In: Bueno-Guerra N, Amici F (eds) Field and laboratory methods in animal cognition: a comparative guide. Cambridge University Press, New York, NY, pp 237–239Google Scholar
  23. Laidre ME, Johnstone RA (2013) Animal signals: a primer. Curr Biol 23:R829–R833CrossRefGoogle Scholar
  24. Laidre ME, Vermeij GJ (2012) A biodiverse housing market in hermit crabs: proposal for a new biodiversity index. Cuadernos de Investigación UNED 4:175–179Google Scholar
  25. Laidre ME, Patten E, Pruitt L (2012) Costs of a more spacious home after remodelling by hermit crabs. J Roy Soc Interface 9:3574–3577CrossRefGoogle Scholar
  26. Land MF, Nilsson D (2012) Animal eyes. Oxford University Press, New York, NYCrossRefGoogle Scholar
  27. Mcnett GD, Luan LH, Cocroft RB (2010) Wind-induced noise alters signaler and receiver behavior in vibrational communication. Behav Ecol Sociobiol 64:2043–2051CrossRefGoogle Scholar
  28. Ord TJ, Peters RA, Clucas B, Stamps JA (2007) Lizards speed up visual displays in noisy motion habitats. Proc R Soc B 274:1057–1062CrossRefGoogle Scholar
  29. Peters RA, Evans CS (2003) Design of the Jacky dragon visual display: signal and noise characteristics in a complex moving environment. J Comp Physiol A 189:447–459CrossRefGoogle Scholar
  30. Peters RA, Hemmi JM, Zeil J (2007) Signaling against the wind: modifying motion-signal structure in response to increased noise. Curr Biol 17:1231–1234CrossRefGoogle Scholar
  31. Rieucau G, Giraldeau L-A (2011) Exploring the costs and benefits of social information use: an appraisal of current experimental evidence. Phil Trans Roy Soc B 366:949–957CrossRefGoogle Scholar
  32. Smolka J, Hemmi JM (2009) Topography of vision and behaviour. J Exp Biol 212:3522–3532CrossRefGoogle Scholar
  33. Stevens M (2013) Sensory ecology, behaviour, and evolution. Oxford University Press, New York, NYCrossRefGoogle Scholar
  34. Strassmann JE, Queller DC (2014) Privatization and property in biology. Anim Behav 92:305–311CrossRefGoogle Scholar
  35. Uy JAC, Endler JA (2004) Modification of the visual background increases the conspicuousness of golden-collared manakin displays. Behav Ecol 15:1003–1010CrossRefGoogle Scholar
  36. Valdes L, Laidre ME (2019) Scent of death: evolution from sea to land of an extreme collective attraction to conspecific death. Ecol Evol 9:2171–2179. CrossRefPubMedPubMedCentralGoogle Scholar
  37. Ward A, Webster M (2016) Sociality: the behaviour of group-living animals. Springer, New York, NYCrossRefGoogle Scholar
  38. Whitchurch EA, Takahashi TT (2006) Combined auditory and visual stimuli facilitate head saccades in the barn owl (Tyto alba). J Neurophysiol 96:730–745CrossRefGoogle Scholar
  39. Wignall AE, Jackson RR, Wilcox RS, Taylor PW (2011) Exploitation of environmental noise by an araneophagic assassin bug. Anim Behav 82:1037–1042CrossRefGoogle Scholar
  40. Yoshizawa M, Gori S, Soares D, Jeffery WR (2010) Evolution of a behavioral shift mediated by superficial neuromasts helps cavefish find food in darkness. Curr Biol 20:1631–1636CrossRefGoogle Scholar
  41. Zeil J, Hemmi JM (2005) The visual ecology of fiddler crabs. J Comp Physiol A 192:1–25CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Biological SciencesDartmouth CollegeHanoverUSA
  2. 2.Graduate Program in Ecology, Evolution, Ecosystems, and SocietyDartmouth CollegeHanoverUSA

Personalised recommendations