Plasticity in the Temporal Organization of Behaviour in the Limpet Cellana Grata

View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Florence Research Mar Biol (2011) 158:1377–1386 DOI 10.1007/s00227-011-1656-0 ORIGINAL PAPER Plasticity in the temporal organization of behaviour in the limpet Cellana grata Giacomo Santini • Avis Ngan • Gray A. Williams Received: 2 August 2010 / Accepted: 22 February 2011 / Published online: 13 March 2011 Ó Springer-Verlag 2011 Abstract The behaviour of intertidal consumers is often Introduction tightly constrained to tidal movements, although activity patterns can vary within these constraints. Spatio-temporal Rocky intertidal organisms are strongly influenced by fluc- variability in behaviour of a limpet, Cellana grata, was tuations in stress levels due to natural variations in their analysed over different tidal conditions (spring and neap environment (Branch 1981; Garrity 1984; McMahon 1990; tides) and during different times of the year (one summer Denny and Wethey 2001; Helmuth 2002). These fluctua- and one winter) at sites in Hong Kong. Activity was gen- tions are usually cyclical and mobile organisms often exhibit erally dictated by tidal movements, being concentrated behavioural patterns which are consistent with stress mini- when animals were awash. Plasticity in behaviour was mizing strategies, by matching activity bouts with periods of observed, with some limpets anticipating activity during more favourable conditions (Little 1989; Chapman and the summer period and delaying activity during winter Underwood 1992). Such favourable periods may be tem- time. Limpets were active for a time equal, or slightly less, porally consistent, resulting in rhythmicity in the animals’ than time awash. As the time awash exceeded *14–16 h, activities (Della Santina and Chelazzi 1991; Della Santina however, activity duration decreased. Within this general et al. 1994; Williams and Little 2007). Such rhythmic pattern, tidal variation as well as variation among times of behaviour of many intertidal gastropod grazers is thought to the year was noted, with the lowest dependence on time be cued by zeitgebers such as daylight and/or tidal cycles awash being recorded during winter neap tides. Limpets (Hawkins and Hartnoll 1983; Little and Stirling 1985; Della showed a slight preference for being active during night- Santina and Naylor 1993; Gray and Hodgson 1999). time, which was particularly evident when animals were The temporal consistency of activity patterns has been emersed during the summer period. Although the basic used to identify a species’ Potential Activity Phase (i.e. the activity in C. grata is constrained to a specific temporal combination of diel and tidal phases where recorded window, this limpet is able to modulate its foraging strat- activity of one species is maximal), which is usually con- egies and resting height, according to local, daily changes sidered to be rigid and species specific (Burrows et al. in environmental conditions. 2000). Even strongly predictable patterns may, however, exhibit temporal and/or spatial variation from the norm, due to variable external conditions (Chapman and Under- Communicated by F. Bulleri. wood 1992; Raffaelli and Hawkins 1996; Williams and Little 2007). On a short temporal scale, for example, daily & G. Santini ( ) changes in weather conditions, such as rainfall, wave Department of Evolutionary Biology, University of Florence, Via Romana 17, 50125 Florence, Italy action, wind or atmospheric pressure, are known to influ- e-mail: giacomo.santini@unifi.it ence activity in some species (Little et al. 1991; Della Santina and Chelazzi 1991). On a longer temporal scale, A. Ngan Á G. A. Williams seasonal influences are known to affect behaviour in lim- The Swire Institute of Marine Science and Division of Ecology & Biodiversity, School of Biological Sciences, The University of pets (Gray and Hodgson 1997; Santini et al. 2004) and Hong Kong, Hong Kong SAR, People’s Republic of China chitons (Ng and Williams 2006), due to changes in abiotic 123 1378 Mar Biol (2011) 158:1377–1386 (e.g. temperature, wave action) factors. Furthermore, Davies et al. 2006). Three moderately exposed sites intrinsic changes in energy metabolism such as gonad (Sites 1–3, *15–25 m in length) with different features development (e.g. Blackmore 1969; Morais et al. 2003)or (orientation, slope) were chosen over an area of *90 m changes in food composition and availability (Hill and along the Cape d’Aguilar peninsula, to represent the Hawkins 1991; Nagarkar and Williams 1999) have the variable conditions which C. grata would naturally potential to affect consumer behaviour. experience (for further details see Ngan 2006). Spatial variations in species’ behavioural patterns have All limpets [20 mm at the sites were marked been documented among separate populations facing dif- (Rn = 102) using Mollusc Tags (Hallprint, Australia) and ferent sets of biotic and abiotic conditions (Hartnoll and a code written on the shell with permanent marker pens Wright 1977; Branch 1985; Della Santina et al. 1994) and (Pilot, Japan). Tagging took place 2 months before the also among individuals of the same population experienc- start of the observations, to allow for any possible dis- ing different substratum slopes (Williams et al. 1999; turbance effects. The average size of limpets (maximum Santini et al. 2004) or shore heights (Little and Stirling length, ±0.1 mm) differed among sites (F2,99 = 23.8, 1985; Little et al. 1988; Takada 2001; Ng and Williams P \ 0.0001), limpets being smaller at Site 3 (34.4 ± SE 2006). Given this variability, intertidal animals represent 0.5 mm, n = 58) than at Sites 1 and 2 (38.9 ± 1.0 mm, ideal subjects for the study of behavioural plasticity, which n = 25 and 40.7 ± 0.7 mm, n = 19, respectively; Tukey is a specific component of phenotypic plasticity, involving test: 3 \ [2 = 1]). The activity patterns of Cellana grata rapid and reversible adaptive responses to environmental at the three sites were recorded during summer (July– cues (Komers 1997; Brockmann 2001; Dingemanse et al. September 2003) and winter (December 2003–March 2010; Mery and Burns 2010). 2004, see Kaehler and Williams (1996) for a description Cellana grata is a dominant grazer found on moderately of Hong Kong climate). During each season, observations exposed to exposed rocky shores throughout south-east Asia were replicated on three randomly chosen dates during (Williams and Morritt 1995; Huang 2001). This non-homing neap and spring tides (Rn = 3 sites 9 2 seasons 9 2 limpet is active only when awash (Williams and Morritt 1995; tidal conditions 9 3 dates = 36). Predicted tidal ampli- Erlandsson et al. 1999; Davies et al. 2006) and its activity tudes during neap and spring tides were 100–200 cm and appears not to be synchronized to the light–dark cycle (Gray 50–250 cm above Chart Datum (CD), respectively. Dur- and Williams 2010). Individuals move up the shore with the ing each observation period, the activity (active or rising tide, slow their movement during the peak of the tide inactive) and physical state (emersed, awash or sub- and return to their resting height in the mid-high shore with merged) of the limpets were recorded at 60-min intervals the ebbing tide (Williams and Morritt 1995; Davies et al. for up to 25 h. In practice, each limpet was observed for 2006). Although the basic behavioural patterns of this species 15 consecutive seconds every hour. The order of sites have been previously documented (Williams and Morritt and limpets observation was randomized each day. 1995; Davies et al. 2006), comparatively little is known about Activity was defined as any observable movement within how such patterns may change over temporal scales in a 15-s time frame. Active limpets lift their shell from the response to long-term (seasonal) changes in favourable substratum, which is clearly recognizable even during conditions. Furthermore, how daily environmental variations submergence or splashing by waves. ‘‘Emersed active’’ (related to weather conditions) or local habitat features (wave described limpets found active above the wave splash splash, etc.) may influence the behaviour of this species is also zone, where wave splash did not reach the individual largely unexplored (but see Davies et al. 2006). To address within the 15-s observation period. As such, this defini- these knowledge gaps, this paper elucidates temporal and tion refers to a dry limpet, but can also include indi- spatial variabilities in the behaviour of C. grata over a com- viduals that were infrequently splashed by waves. bination of different times of the year (winter, summer) and ‘‘Awash’’ refers to limpets continuously splashed by tidal conditions (neap, spring). Investigating the behavioural waves or successively covered by seawater and exposed patterns of C. grata over these temporal and spatial scales to air within 15 s. ‘‘Submerged’’ refers to limpets con- allows an evaluation of the repertoire of behavioural strate- tinuously and completely covered by seawater during the gies available to this limpet to accommodate variation in 15-s time frame. Red light was used during nighttime environmental conditions. observations to minimize possible disturbance (see Little and Stirling 1985; Williams and Morritt 1995). Finally, it was assumed that the activity and physical state observed Materials and methods for each limpet within the 15-s observation windows was maintained for the remaining hour (i.e., a limpet observed This study was carried out at Cape d’Aguilar (22°130N, active for 15 s was scored as being active for the entire 114°120E), Hong Kong (see Williams and Morritt 1995; hour). 123 Mar Biol (2011) 158:1377–1386 1379 To assess variability in global activity patterns during then assessed using Markov Chains Monte Carlo simula- tide, time of the year, day and sites, the following variables tions (n = 50,000 runs), as described by Baayen et al. were measured: (2008). Model assumptions for the within-group errors (independent and identical, normally distributed within- 1.

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