acta ethol (1999) 2:29–34
© Springer-Verlag and ISPA 1999
O R I G I N A L A RT I C L E
Jens Krause · Simon P. Loader · Emma Kirkman Graeme D. Ruxton
Refuge use by fish as a function of body weight changes
Received: 13 December 1998 / Received in revised form: 2 May 1999 / Accepted: 7 June 1999
Abstract Refuge use provides a good model for the study of trade-offs between the benefits of predator avoidance and the costs of lost feeding opportunities. We manipulated the latter costs by subjecting similar-sized three-spine sticklebacks to 2 days of food deprivation followed by a 2-day re-feeding period and recorded associated changes in body weight and refuge use. Food deprivation resulted in a decrease and re-feeding in an increase in the duration of refuge use by fish. Emergence times of fish from the refuge were extremely variable (with a ratio of 1:127 between the shortest and the longest ones) but individual ranks were highly consistent between different days of testing, suggesting that emergence times were individually characteristic. Percentage weight change of fish in response to the experimental treatments also showed a high level of inter-individual variation ranging from 0–17%. A significant positive correlation was found between the percentage weight lost and the percentage decrease in emergence time from a refuge after food deprivation and similarly between the percentage weight gained and the percentage increase in refuge use after re-feeding. The relationship between energy turnover and behavioural strategies is discussed. Key words Gasterosteus aculeatus · Foraging behaviour · Refuge use · Weight change
J. Krause (✉) · S.P. Loader · E. Kirkman Ecology & Evolution Group, Centre of Biodiversity and Conservation, School of Biology, University of Leeds, Leeds LS2 9JT, UK e-mail:
[email protected]; Tel.: +44-113-2332840; Fax: +44-114-2332835 G.D. Ruxton Division of Environmental and Evolutionary Biology, Graham Kerr Building, University of Glasgow, Glasgow G12 8QQ, UK
Introduction Two of the most important factors that determine refuge use in animals are the intensity of a predation risk and the nutritional state (Dill and Gillett 1991; Sih 1992). Staying in a refuge precludes (or severely limits) foraging activity; thus refuge use results in a trade-off between the benefits of predator avoidance and the costs of lost feeding opportunities (Sih 1997). Some recent studies have focused on the importance of the nutritional state as a predictor of emergence time in a number of different taxa (Dill and Gillett 1991: barnacles; Koivula et al. 1995: birds; Dill and Fraser 1997: polychaete worm; Krause et al. 1998: fish). Many of these studies investigated (among other factors) whether and to what degree hiding behaviour was reduced as a function of the duration of food deprivation but little attention was paid to inter-individual variation in the effects of food deprivation periods on energy reserves and corresponding behavioural strategies. Krause et al. (1998) reported that food deprivation periods of the same length caused body-length-dependent weight losses in three-spine sticklebacks (Gasterosteus aculeatus) with larger individuals losing a smaller proportion of their initial weight than small ones. This difference in relative weight loss was explained by the difference in mass-specific metabolic efficiency, which is greater in larger individuals (Weatherley and Gill 1987; Wootton 1994). As a result of higher relative metabolic costs, smaller fish generally showed shorter hiding times and decreased their hiding behaviour more strongly in response to food deprivation periods than large fish, suggesting a key role of weight loss in influencing refuging behaviour (Krause et al. 1998). Previous experiments have shown that three-spine sticklebacks respond to the introduction to a new environment by seeking shelter from which they subsequently start to investigate the surrounding area for food (Krause et al. 1998). In this study, we used this procedure to examine the effects of food deprivation and refeeding periods on refuge behaviour in fish of similar
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body length. We predicted that food deprivation would result in a decrease of hiding time whereas subsequent re-feeding would result in an increase in hiding time in fish. In particular, we investigated the degree of interindividual variation in weight loss/gain patterns to test whether inter-individual differences in weight change (losses and gains) can be related to corresponding behavioural changes in refuge use.
Methods Twenty-nine male and female three-spine sticklebacks (Gasterosteus aculeatus; standard body length: mean±SD=3.79±0.20 cm, range=3.38–4.16 cm; body weight: mean±SD=0.66±0.13, range=0.46–0.99 g, condition factor K=(body weight/body length3)×100: mean±SD=1.2±0.14) were collected from a ditch (length: 402 m, average depth: 27 cm, average width: 190 cm) near Stockton farm on the Harewood Estate about 10 km north of Leeds (UK). Large parts of the ditch were covered with reeds and contained submerged vegetation, providing cover for fish. Grey heron (Ardea cinerea) and kingfisher (Alcedo atthis) were frequently observed at the ditch. Predatory fish were not found but might be able to enter the ditch occasionally via a pipe that connects the ditch with a small lake that contains perch (Perca fluviatilis). None of the fish used for this study showed any obvious signs of external or internal parasites. Fish were kept for about 1 month at 12°C and 12L:12D before they were used in the experiments. They were fed dried chironomids to satiation once a day and occasionally given live daphnia. Both male and female sticklebacks were used. However, fish were collected in the autumn and kept at low temperatures, which means that they were not sexually active during the experiments. At the beginning of the experiments, fish were transferred into individual flower pots (diameter 12 cm, water depth 8 cm) and their refuge behaviour tested on day 1, on day 3 after a 2-day food deprivation period and on day 5 following a subsequent 2-day refeeding period. Weight measurements were carried out on a digital balance to 10–4 g (and repeated measurements were taken of each fish to check for measurement errors) on days 1, 3 and 5 after each test of refuge use was completed. Fish kept still during weighing and no anaesthetic was used. Relative weight loss (absolute weight lost between days 1 and 3 divided by initial weight on day 1) and weight gain (absolute weight gained between days 3 and 5 divided by the weight on day 3) were calculated using gross weights including the weight of the gut contents. Previous work has shown that gut contents can form an important part of the overall weight loss during the first 24 h of deprivation but that further significant weight losses occur between days 1 and 2 (Krause et al. 1998). Experiments by Pascoe and Mattey (1977) showed that sticklebacks can sustain food-deprivation periods of 2–3 weeks before any mortalities occur. Therefore food-deprivation periods of 2 days (used in this study) should not present a serious starvation risk for fish. No mortalities (or other negative effects) were observed as a result of food deprivation and most fish regained or exceeded their initial weights (day 1) after a subsequent re-feeding period (day 5). To investigate refuging behaviour we used an experimental tank (85×59×55 cm, L×W×H, 5 cm water depth) made out of opaque grey plastic. One corner of the tank provided a refuge that consisted of a small polystyrene float (size ca. 50 cm2). The fish was introduced to the refuge via a clear plastic cylinder (elliptical shape: 6×2.5 cm) that was placed through a hole in the polystyrene float so that the test fish was inside the refuge after release. This way of introducing fish was adopted after a number of pilot trials demonstrated the advantages of this method in causing less stress to the fish (see Krause et al. 1998 for details of the experimental set-up).
At the beginning of each trial, a single stickleback was transferred from its flowerpot to the plastic cylinder in the test tank and left for 3 min to settle. The cylinder was then pulled up via a remote pulley system to release the fish. The cylinder was pulled upwards by about 4.5 cm to remain in contact with the water surface to avoid potential disturbances of the water surface (Tegeder and Krause 1995). After release, we measured the time it took for the fish to appear fully from the refuge for the first time (full body out from under the float). Observations of test fish were made from a hide. Relative decreases and increases in emergence time (decrease: absolute decrease in time between days 1 and 3 divided by initial emergence time on day 1; increase: absolute increase in time between days 3 and 5 divided by the emergence time on day 3) were calculated. Given the size and structure of the refuge, searching for food inside the refuge and hiding were not mutually exclusive activities in this experiment. However, the size of the refuge was so small that sticklebacks, which forage mainly visually (FitzGerald and Wootton 1993) would be able to scan the area inside the refuge for food very quickly (Krause et al. 1998). But this would not be possible for the much larger area outside the refuge. No food was present in the test tanks.
Results Fish showed remarkable inter-individual variation in emergence time with ratios of 1:33, 1:127 and 1:45 between the shortest and the longest emergence times on day 1, 3 (after deprivation), and 5 (after re-feeding; Fig. 1). No significant correlations were found between the emergence times on days 1, 3 and 5 and body length, weight and the condition factor (values of the latter two factors were taken for that particular day of the experiment; linear regression: n=29, all r20.05). Furthermore emergence times on days 1 and 3 were not correlated with the percentage weight loss incurred during the 2-day deprivation period nor was there a relationship between emergence behaviour on day 5 and the percentage weight gain during a preceding 2-day re-feeding period (linear regression: n=29, all r20.05). The relative differences in emergence behaviour between individuals were highly consistent for days 1, 3 and 5 (Kendall coefficient of concordance: n=29, W=0.935, χ2=78.54, P
