Abstract
Behavioural time budgets of organisms reflect their reaction norms to environmental conditions and, as such, indicate their behavioural plasticity. In environments which limit the activity time of organisms, efficient organization of behaviours is critical to enhancing performance to achieve necessary functions and minimize time and/or energetic costs. We investigated variations in behavioural time budgets of a common deposit-feeding crab, Scopimera intermedia, to the spatio-temporal scales of environmental changes experienced on sandy shores in the monsoonal tropics, where activity times are restricted by the tides. Activity levels of the crabs varied strongly with air temperature, with crabs emerging from the sediments only when air temperature exceeded ~ 20 °C. Behavioural water uptake increased in frequency with both feeding rate and environmental temperature, and was often followed by waving displays. Water uptake and waving, therefore, appear to be multifunctional behaviours, as not only do the crabs replenish water for feeding and wave their chelipeds to court females, but these behaviours can also contribute to thermoregulation, enhancing cooling when taking up water from the sediment surface. Such plastic and multifunctional behavioural traits are likely a widespread solution for survival and reproductive success in harsh and dynamic environments, where specialized traits are energetically costly and time-inefficient to optimize performance.
Significance statement
Surviving in extreme and variable environments is challenging due to the potentially substantial energetic cost animals need to undertake in order to maximize performances under contrasting conditions. This study reveals a multitasking strategy adopted by the sand-bubbler crab to survive hot and variable temperatures within a limited activity time on tropical sandy shores. Behaviours of the crabs are strongly temperature dependent; and when active whilst the tide is out the crabs flexibly adjust their activity times to feed, stay cool and attract mates using a limited set of multifunctional behaviours. Specialized traits are therefore not necessary to achieve these critical functions and, as such, this study highlights the importance of this plastic, multitasking strategy as a common solution for animals to endure highly variable environments with minimal cost.
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All relevant data were deposited in the Open Science Framework available at https://osf.io/qy85g/.
References
Aagaard A, Warman CG, Depledge MH (1995) Tidal and seaonal changes in the temporal and spatial distribution of foraging Carcinus maenas in the weakly tidal littoral zone of Kerteminde Fjord, Denmark. Mar Ecol Prog Ser 122:165–172
Allen BJ, Rodgers B, Tuan Y, Levinton JS (2012) Size-dependent temperature and desiccation constraints on performance capacity: implications for sexual selection in a fiddler crab. J Exp Mar Biol Ecol 438:93–99
Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth
Ansell AD (1988) Migration or shelter? Behavioural options for deposit feeding crabs on tropical sandy shores. In: Chelazzi G, Vannini M (eds) Behavioral adaptation to intertidal life. Plenum Press, New York, pp 15–26
Backwell PRY, Jennions MD, Christy JH, Passmore NI (1999) Female choice in the synchronously waving fiddler crab Uca annulipes. Ethology 105:415–421
Bakken GS (1992) Measurement and application of operative and standard operative temperatures in ecology. Am Zool 32:194–216
Bartholomew GA, Lasiewski RC (1968) Patterns of panting and gular flutter in cormorants, pelicans, owls and doves. Condor 70:31–34
Bartolini F, Penha-Lopes G, Limbu S, Paula J, Cannicci S (2009) Behavioural responses of the mangrove fiddler crabs (Uca annulipes and U. inversa) to urban sewage loadings: results of a mesocosm approach. Mar Poll Bull 58:1860–1867
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models uisng lme4. J Stat Softw 67:1–48
Bauchau AG, Passelecq-Gerin (1988) Adaptive structures to filter-feeding in the sand crab Scopimera gordanae Serene and Moosa, 1981 (Crustacea Decapoda Brachyura Ocypodidae). Indo-Malay Zool 5:23–29
Burggren WW (1992) Respiration and circulation in land crabs: novel variations on the marine design. Am Zool 32:417–427
Candolin U, Heuschele J (2008) Is sexual selection beneficial during adaptation to environmental change? Trends Ecol Evol 23:446–452
Caraco T, Blanckenhorn WU, Gregory GM, Newman JA, Recer GM, Zwicker SM (1990) Risk-sensitivity: ambient temperature affects foraging choice. Anim Behav 39:338–345
Caravello HE, Cameron GN (1991) Time activity budgets of the Gulf Coast fiddler crab (Uca panacea). Am Midl Nat 126:403–407
Christy JH (1989) Rapid development of megalopae of the fiddler crab Uca pugilator reared over sediment: implications for models of larval recruitment. Mar Ecol Prog Ser 57:259–265
Crickenberger S, Hui TY, Landry Yuan F, Bonebrake TC, Williams GA (2020) Preferred temperature of intertidal ectotherms: broad patterns and methodological approaches. J Therm Biol 87:102468
Darnell MZ, Munguia P (2011) Thermoregulation as an alternate function of the sexually dimorphic fiddler crab claw. Am Nat 178:419–428
Darnell MZ, Nicholson HS, Munguia P (2015) Thermal ecology of the fiddler crab Uca panacea: thermal constraints and organismal responses. J Therm Biol 52:157–165
Davies MS, Edwards M, Williams GA (2006) Movement patterns of the limpet Cellana grata (Gould) observed over a continuous period through a changing tidal regime. Mar Biol 149:775–787
Denny MW, Miller LP (2011) Importance of behavior and morphological traits for controlling body temperature in littorinid snails. Biol Bull 220:209–223
Ducrest A-L, Keller L, Roulin A (2008) Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends Ecol Evol 23:502–510
Edney EB (1961) The water and heat relationships of fiddler crabs (Uca spp.). Trans R Soc S Afr 36:71–91
Garrity SD (1984) Some adaptations of gastropods to physical stress on a tropical rocky shore. Ecology 65:559–574
Gates DM (1980) Biophysical Ecology. Springer-Verlag, New York
Gherardi F, Russo S (2001) Burrowing activity in the sand-bubbler crab, Dotilla fenestrata (Crustacea, Ocypodidae), inhabiting a mangrove swamp in Kenya. J Zool 253:211–223
Gherardi F, Russo S, Anyona D (1999) Burrow-oriented activity in the ocypodid crab, Dotilla fenestrata, living in a mangrove swamp. J Mar Biol Asso UK 79:281–293
Gray DR, Hodgson AN (1997) Temporal variation in foraging behaviour of Patella granularis (Patellogastropoda) and Siphonaria concinna (Basommatophora) on a South African shore. J Mollus Stud 63:121–130
Hartnoll RG (1973) Factors affecting the distribution and behaviour of the crab Dotilla fenestrata on east African shores. Estuar Coast Mar Sci 1:137–152
Hazlett BA (1988) Behavioural plasticity as an adaptation to variable environment. In: Chelazzi G, Vannini M (eds) Behavioural Adaptation to Intertidal Life. Plenum, New York, pp 317–332
Heinrich B (1974) Thermoregulation in endothermic insects. Science 185:747–756
Henmi Y, Koga T, Murai M (1993) Mating behaviours of the sand bubbler crab Scopimera globosa. J Crust Biol 13:736–744
Hong Kong Observatory (2017) Climatological information services. URL: http://www.hko.gov.hk/cis/climat_e.htm. Accessed on 1/3/2017
Houston AI, McNamara JM (1999) Models of adaptive behaviour: an approach based on state. Cambridge University Press, New York
Houston AI, McNamara JM, Hutchinson JMC (1993) General results concerning the trade-off between gaining energy and avoiding predation. Philos Trans R Soc Lond B Biol Sci 341:375–397
How MJ, Zeil J, Hemmi JM (2007) Differences in context and function of two distinct waving displays in the fiddler crab, Uca perplexa (Decapoda: Ocypodidae). Behav Ecol Sociobiol 62:137–148
How MJ, Zeil J, Hemmi JM (2009) Variability of a dynamic visual signal: the fiddler crab claw-waving display. J Comp Physiol A 195:55–67
Hughes RN (1988) Optimal foraging in the intertidal environment: evidence and constraints. In: Chelazzi G, Vannini M (eds) Behavioral Adaptation to Intertidal Life. Plenum Press, New York, pp 265–282
Hui TY, Williams GA (2017) Experience matters: context-dependent decisions explain spatial foraging patterns in the deposit-feeding crab Scopimera intermedia. Proc R Soc Biol Sci 284:20171442
Hui TY, Landry Yuan F, Bonebrake TC, Williams GA (2019) Multifunctional behaviours in a sandy shore crab enhances performance in extreme intertidal environments. Oecologia 189:79–89
Jennions MD, Møller AP, Petrie M (2001) Sexually selected traits and adult survival: a meta-analysis. Q Rev Biol 76:3–36
Jennions MD, Backwell PRY, Murai M, Christy JH (2003) Hiding behaviour in fiddler crabs: how long should prey hide in response to a potential predator? Anim Behav 66:251–257
Kaehler S, Williams GA (1996) Distribution of algae on tropical rocky shores: spatial and temporal patterns of non-coralline encrusting algae in Hong Kong. Mar Biol 125:177–187
Kennish R (1998) Foraging behaviour of the tropical herbivorous crab, Grapsus albolineatus: time minimiser or nutrient maximizer? In: Morton B (ed) The Marine Biology of South China Sea III. Hong Kong University Press, Hong Kong, pp 227–237
Kim TW, Choe JC (2003) The effect of food availability on the semilunar courtship rhythm in the fiddler crab Uca lactea (de Haan) (Brachyura: Ocypodidae). Behav Ecol Sociobiol 54:210–217
Kitaura J, Wada K (2006) Evolution of waving display in brachyuran crabs of the genus Ilyoplax. J Crust Biol 26:455–462
Koch N, Lynch B, Rochette R (2007) Trade-off between mating and predation risk in the marine snail, Littorina plena. Invertebr Biol 126:257–267
Koga T (1995) Movements between microhabitats depending on reproduction and life history in the sand-bubbler crab Scopimera globosa. Mar Ecol Prog Ser 117:65–74
Kohler KE, Gill SM (2006) Coral point count with excel extensions (CPCe): a visual basic program for the determination of coral and substrate coverage using random point count methodology. Comput Geosci 32:1259–1269
Levinton JS, Lord S, Higeshide Y (2015) Are crabs stressed for water on a hot sand flat? Water loss and field water state of two species of intertidal fiddler crabs. J Exp Mar Biol Ecol 469:57–62
Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640
Lindén A, Mäntyniemi S (2011) Using the negative binomial distribution to model overdispersion in ecological count data. Ecology 92:1414–1421
Little C (1989) Factors governing patterns of foraging activity in littoral marine herbivorous molluscs. J Mollus Stud 55:273–284
Maitland DP (1990) Carapace and branchial water circulation, and water-related behaviours in the semaphore crab Heloecius cordiformis (Decapoda: Brachyura: Ocypodidae). Mar Biol 105:275–286
Mangel M (1991) Adaptive walks on behavioural landscapes and the evolution of optimal behaviour by natural selection. Evol Ecol 5:30–39
Martel A, Larrivee DH, Klein KR, Himmelman JH (1986) Reproductive cycle and seasonal feeding activity of the neogastropod Buccinum undatum. Mar Biol 92:211–221
Mat AM, Dunster GP, Sbragaglia V, Aguzzi J, de la Iglesia HO (2017) Influence of temperature on daily locomotor activity in the crab Uca pugilator. PLoS ONE 12:e0175403
McCullough EL, Emlen DJ (2013) Evaluating the costs of a sexually selected weapon: big horns at a small price. Anim Behav 86:977–985
Munguia P, Backwell PRY, Darnell MZ (2017) Thermal constraints on microhabitat selection and mating opportunities. Anim Behav 123:259–265
Murai M, Backwell PRY (2006) A conspicuous courtship signal in the fiddler crab Uca perplexa: female choice based on display structure. Behav Ecol Sociobiol 60:736–741
Nakasone Y (1982) Ecology of the fiddler crab Uca (Thalassuca) vocans (Linnaeus) (Decapoda: Ocypodidae) I. Daily activity in warm and cold seasons. Res Popul Ecol 24:97–109
Ng JSS, Williams GA (2006) Intraspecific variation in foraging behaviour: influence of shore height on temporal organization of activity in the chiton Acanthopleura japonica. Mar Ecol Prog Ser 321:183–192
Ng TPT, Lau SLY, Seuront L, Davies MS, Stafford R, Marshall DJ, Williams GA (2017) Linking behaviour and climate change in intertidal ectotherms: insights from littorinid snails. J Exp Mar Biol Ecol 492:121–131
Ohata M, Wada K, Koga T (2005) Waving display by male Scopimera globosa (Brachyura: Ocypodoidea) as courtship behaviour. J Crust Biol 25:637–639
Palmer JD (1990) The rhythmic lives of crabs. Bioscience 40:352–358
Pamatmat MM (1978) Oxygen uptake and heat production in a metabolic conformer (Littorina irrorata) and a metabolic regulator (Uca pugnax). Mar Biol 48:317–325
Powers LW, Cole JF (1976) Temperature variation in fiddler crab microhabitats. J Exp Mar Biol Ecol 21:141–157
Quinn RH (1980) Mechanisms for obtaining water for flotation feeding in the soldier crab, Mictyris longicarpus Latreille, 1806 (Decapoda, Mictyridae). J Exp Mar Biol Ecol 43:49–60
Reaney LT, Backwell PRY (2007) Temporal constraints and female preference for burrow width in the fiddler crab, Uca mjoebergi. Behav Ecol Sociobiol 61:1515–1521
Ribeiro PD, Iribarne OO (2011) Coupling between microphytobenthic biomass and fiddler crab feeding. J Exp Mar Biol Ecol 407:147–154
Salmon M, Atsaides SP (1968) Visual and acoustical signalling during courtship by fiddler crabs (Genus Uca). Int Comp Biol 8:623–639
Santos RS, Hawkins SJ, Nash RDM (1996) Reproductive phenology of the Azorean rock pool blenny a fish with alternative mating tactics. J Fish Biol 48:842–858
Sassa S, Watabe Y (2008) Threshold, optimum and critical geoenvironmental conditions for burrowing activity of sand bubbler crab, Scopimera globosa. Mar Ecol Prog Ser 354:191–199
Sibly R, McFarland D (1976) On the fitness of behavior sequences. Am Nat 110:601–617
Song B, Zhang Z-Q, Stöcklin J, Yang Y, Niu Y, Chen J-G, Sun H (2013) Multifunctional bracts enhance plant fitness during flowering and seed development in Rheum nobile (Polygonaceae), a giant herb endemic to the high Himalayas. Oecologia 172:359–370
Southwick EE, Heldmaier G (1987) Temperature control in honey bee colonies. Bioscience 37:395–399
Stephens DW, Krebs JR (1986) Foraging theory. Princeton University Press, Princeton
Suzuki H, Kikuchi T (1990) Spatial distribution and recruitment of pelagic larvae of sand bubbler crab, Scopimera globosa. La mer 28:172–179
Thompson WE, Molinaro PJ, Greco TM, Tedeschi JB, Holliday CW (1989) Regulation of hemolymph volume by uptake of sand capillary water in desiccated fiddler crabs, Uca pugilator and Uca pugnax. Comp Biochem Physiol A 94:531–538
Thurman CL (1998) Evaporative water loss, coporal temperature and the distribution of sympatric fiddler crabs (Uca) from South Texas. Comp Biochem Physiol 119:279–286
Trager GC, Coughlin D, Genin A, Achituv Y, Gangopadhyay A (1992) Foraging to the rhythm of ocean waves: porcelain crabs and barnacles synchronize feeding motions with flow oscillations. J Exp Mar Biol Ecol 164:73–86
Vogel F (1984) Comparative and functional morphology of the spoon-shaped setae on the second maxillipeds in Dotilla Stimpson, 1858 (Decapoda, Brachyura, Ocypodidae). Crustaceana 47:225–234
von Hagen H-O (1993) Waving display in females of Uca polita and of other Australian fiddler crabs. Ethology 93:3–20
Weinstein RB, Full RJ, Ahn AN (1994) Moderate dehydration decreases locomotor performance of the ghost crab, Ocypode quadrata. Physiol Zool 67:873–891
Williams GA, Chan BKK, Dong Y-w (2019) Rocky shores of mainland China, Taiwan and Hong Kong. In: Hawkins SJ, Bohn K, Firth LB, Williams GA (eds) Interactions in the Marine Benthos - Global Patterns and Processes, vol 87. Systematics Association, Cambridge University Press, Cambridge, pp 360–390
Williams GA, Little C (2007) Foraging behavior. In: Denny MW, Gaines SD (eds) Encyclopedia of tidepools and rocky shore. University of California Press, California, pp 239–242
Williams GA, Morritt D (1995) Habitat partitioning and thermal tolerance in a tropical limpet, Cellana grata. Mar Ecol Prog Ser 124:89–103
Wolcott TG (1976) Uptake of soil capillary water by ghost crabs. Nature 264:756–757
Yao H, Dao M, Imholt T, Huang J, Wheeler K, Bonilla A, Suresh S, Ortiz C (2010) Protection mechanisms of the iron-plated armor of a deep-sea hyrothermal vent gastropod. Proc Natl Acad Sci 107:987–992
Zeileis A, Kleiber C, Jackman S (2008) Regression models for count data in R. J Stat Softw 27:1–25
Acknowledgements
The authors would like to thank Mark Denny (Stanford University) for stimulating discussions over the possible functions of waving in crabs, and Stefano Cannicci (SWIMS, The University of Hong Kong) for constructive comments in improving the manuscript. T.Y.H. would also like to thank Mr. Camille Chung for demonstrating how to use Arduino and Ms. Cecily Law (SWIMS, The University of Hong Kong) for providing technical assistance. The authors would also like to thank four anonymous reviewers for their constructive comments and criticisms.
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The research was supported by a Postgraduate Studentship from the University of Hong Kong awarded to T.Y.H.
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T.Y.H. and G.A.W. conceived the study. T.Y.H. carried out fieldwork and analyses, whilst both T.Y.H. and G.A.W. contributed to writing the manuscript.
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Hui, T.Y., Williams, G.A. Behavioural plasticity in the monsoonal tropics: implications for thermoregulatory traits in sandy shore crabs. Behav Ecol Sociobiol 75, 89 (2021). https://doi.org/10.1007/s00265-021-03026-z
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DOI: https://doi.org/10.1007/s00265-021-03026-z