Vol. 16: 177–188, 2012 AQUATIC BIOLOGY Published online August 16 doi: 10.3354/ab00441 Aquat Biol Small-scale temporal and spatial variability in foraging behaviour of the mid-shore gastropod Nerita yoldii on seasonal, tropical, rocky shores Ariel Chung Yan Yeung, Gray A. Williams* The Swire Institute of Marine Science and Division of Ecology & Biodiversity, School of Biological Sciences, The University of Hong Kong, Pokfulam Road, Hong Kong SAR ABSTRACT: Describing temporal variation in the foraging behaviour of intertidal gastropods is important to gain an understanding of the environmental conditions that constrain their activity patterns. Foraging behaviour in the tropical gastropod Nerita yoldi was mainly deter- mined by the tidal cycle: individuals foraged when they were awash, or emersed when the rock was wet, migrating downshore to forage and upshore when they returned to refuges. Apart from tidal influences, foraging in N. yoldii also varied with season and tidal state. Indi- viduals were generally more active in summer than in winter and on neap than spring tides; although small-scale daily variation existed. Such temporal variation may be caused by several interacting environmental variables, especially air temperature, pressure and irradi- ance, which influence physical conditions as well as individuals’ metabolism. Individual for- aging patterns were also highly labile between seasons: most individuals would stop and remain stationary on the open rock surface in winter, but returned to refuges after foraging in summer, a pattern probably driven by physical stress. The foraging behaviour of N. yoldii, therefore, is predictable on a coarse scale, in terms of when they are active, but highly labile in duration and foraging range, which indicates the importance of local, daily variation in environmental factors controlling foraging on shores that have strong temporal changes in abiotic conditions. KEY WORDS: Nerita · Foraging behaviour · Tropical shore Resale or republication not permitted without written consent of the publisher INTRODUCTION haviour can, however, be labile within the same spe- cies, varying temporally, for example, with different Variation in the temporal and spatial distribution of seasons (Ng & Williams 2006) and diurnal and tidal foraging behaviour in intertidal organisms is impor- cycles (Chelazzi 1982, Santini et al. 2004, 2011). Such tant in mediating the interactions between different behaviour can also vary spatially with different site species, which in turn can influence community locations (Hartnoll & Wright 1977), habitats (Hawkins structure (Hawkins & Hartnoll 1983, Chapman & & Hartnoll 1982, Williams et al. 1999) and tidal levels Underwood 1992a, Williams et al. 1999, Williams & (Williams & Morritt 1991). These differences are Little 2007). The timing of foraging of nearly all inter- prob ably due to local variation in environmental fac- tidal grazers shows some tidal correlation, presum- tors, which can be causal in driving foraging behav- ably driven by physical stress or predation risk (Little iour or inhibiting activity when conditions are un- 1989, Chapman & Underwood 1992a). Foraging be - favourable (Little et al. 1988, Williams & Little 2007). *Corresponding author. Email: [email protected] © Inter-Research 2012 · www.int-res.com 178 Aquat Biol 16: 177–188, 2012 Such lability in foraging behaviour represents impor- MATERIALS AND METHODS tant adaptive traits in organisms (Mery & Burns 2010). Climatic seasonality, for example, is a large Study sites time-scale temporal pattern that affects foraging behaviour owing to changes in physical stress, Two gently sloping sites (Site 1, ~9 and Site 2,~5 m predation pressure and food availability as well as wide, ~17° slope), ~20 m apart, were selected at Lung associated changes in tidal and diurnal conditions. Kwu Tan, Hong Kong (22° 15’ N, 114° 10’ E) between As a result, such variation in foraging behaviour can 1.25 and 1.75 m above chart datum (CD; i.e. the make it difficult to define precise behavioural pat- height of the lowest astronomical tide), which is the terns of a species (Chapman & Underwood 1992a, most abundant zone of Nerita yoldii (Yeung 2006). Ng & Williams 2006, Santini et al. 2011). The high shore (>1.75 m above CD) at both sites The gastropod genus Nerita Linnaeus 1758 (Neri- appeared barren, whilst the mid and low shores were tacea) has a high abundance and diversity in tropical covered by a layer of biofilm from June to December regions (Vermeij 1973). Most species, such as N. tex- and a low turf of macroalgae (Ulva spp., Enteromor- tilis (Chelazzi et al. 1983) and N. polita (Chelazzi pha spp.) from January to May (Yeung 2006). At both 1982) are zonal shuttlers (Chelazzi et al. 1988), which study sites, a 50 × 50 cm grid of small holes was forage from a refuge either up- or downshore during drilled in the rock, into which a 50 × 50 cm aluminum each tidal cycle before returning to their resting level quadrat (evenly divided using nylon lines to form 100 (Chelazzi et al. 1988). Previous observations on the 5 × 5 cm squares) could be fitted via adjustable, behaviour of Nerita have not, however, investigated 15 cm long, screw legs at each corner of the quadrat, longer-term variations in foraging patterns, such as which held the quadrat over the rock surface. monthly or seasonal variation, al though a longer- term study of N. plicata, N. textilis and N. undata in Kenya showed these species to be more active on Observations of foraging behaviour spring than neap tides (Ruwa & Jaccarini 1988). Nerita are important herbivores in the Hong Kong To investigate temporal variation in the foraging rocky intertidal zone (Hill 1980). In contrast to other behaviour of Nerita yoldii, observations were con- tropical localities where the foraging behaviour of ducted for 24.5 h on 6 occasions in summer 2003 and Nerita has been studied (e.g. Panama, Levings & winter 2003/2004: 3 times during spring tides (daily Garrity 1983), Hong Kong has a strongly seasonal cli- tidal range, >2 m) and 3 times during neap tides mate, with hot, wet summers and cool, dry winters (daily tidal range, <1.25 m). On each randomly (Kaehler & Williams 1996). In addition, Hong Kong’s chosen sampling date, 18 different individuals (size, tidal cycle also shows temporal variation, from semi- 14.4 ± 2.1 mm [mean ± SD]) were tagged 24 h before diurnal (two unequal tides a day during spring tides, observation (Σn = 2 sites × 2 seasons × 2 tidal condi- with ~2.5 m tidal range) to almost diurnal tides (one tions × 3 d × 18 individuals per observation = 432). tide a day, with ~1.0 m tidal range, during neap tides, At 30 min intervals, the location of tagged indi - Morton et al. 1996). As a result, rocky shores ex - viduals was determined to the nearest 2.5 × 2.5 cm perience great temporal variation in environmental square, by recording the corner of the respective 5 × factors, which are likely to influence foraging behav- 5 cm square of the quadrat that the individual was iour patterns of intertidal gastropods (Santini et al. closest to (e.g. upper left) when viewed in the per- 2011). pendicular plane. To do this at night, a red filtered The present study investigated large and small light was used, which did not appear to disturb the scale patterns of temporal variation (with season and nerites (see Little et al. 1988). Preliminary observa- monthly cycles) in the foraging behaviour of an tions showed that Nerita yoldii are inactive and do abundant nerite, Nerita yoldii. The aim of this study not move when they are submerged during high tide. was to identify the general patterns of foraging of N. Observations were, therefore, not made when tagged yoldii to determine the overall rhythms that constrain individuals were immersed by the tide, as they were the behavioural repertoire of this species. Observa- assumed to be inactive. tions of smaller-scale (e.g. daily) variation in foraging The environmental conditions experienced by indi- behaviour, and associated causal factors, were under - viduals were defined as: taken to examine how labile the behaviour of this (1) immersed by the tide (an individual that was com- species can be, and to describe how N. yoldii may re - pletely submerged by the tide); (2) immersed in a spond to local, environmental changes. pool (an individual that was completely submerged Yeung & Williams: Foraging behaviour of Nerita yoldii 179 in a pool); (3) awash (an individual that was washed mine if the direction of the resultant vector differed by waves on the ebbing or rising tide); (4) wet, significantly from random during different seasons emersed (an individual located in any wet microhab- and tidal conditions. itat, but not washed by waves or submerged by the Percentage activity (%) was calculated as the tide or in a pool; an individual partially submerged percentage of individuals exhibiting movement at in a pool was also considered as wet, emersed); and a particular time. Other parameters used to inves- (5) dry, emersed (an individual located in any dry tigate the foraging behaviour of the traced indi - habitat). viduals were: (1) total distance traveled (cm, the To investigate the influence of temperature vari- sum of the distance traveled by an individual dur- ables on individuals’ foraging behaviour, air (~5 cm ing a foraging excursion); (2) foraging range (cm, above the rock surface), seawater, dry and wet rock the maximum displacement of an individual from surfaces and crevice temperatures were measured its initial refuge during a foraging excursion); (3) hourly during each observation period (±0.1°C, n = 5) maximum speed (cm min−1, the maximum speed at both study sites with an Omega K-type (Teflon achieved by an individual during a foraging excur- insulated) thermocouple (dia meter, 0.25 mm) con- sion) and (4) activity duration (h, the total duration nected to a portable thermo meter (Omega).