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- Materials and methods
Ruxton, Armstrong & Humphries (1999) extended existing models based on the Ideal Despotic Distribution with patches of fixed quality by exploring how animals of different social status distribute themselves among arrays of discrete patches that fluctuate in quality in time and space. Like similar models (e.g. Bernstein, Kacelnik & Krebs 1988; Abrams 2000; Gill, Sutherland & Norris 2001), this assumes that foragers seek to track profitable feeding patches, but that their ability to do this depends on social rank. Testing these assumptions requires detailed information on how animals of known rank respond to fluctuating resource distribution and we report here on a study designed to provide such information for an extensively used model system, the juvenile Atlantic salmon (Salmo salar L.).
Atlantic salmon spawn in streams and rivers during autumn and winter and their eggs hatch during the following spring. On dispersal from the nest, young fish take up residence in streams where they remain for 1 to 7 years before many of them migrate to sea (Metcalfe & Thorpe 1990). Survival and growth in fresh water are important determinants of the number of fish migrating to sea and subsequently returning as adults. In many streams, the foraging areas of juvenile salmon are separated by large boulders, so in these cases it is appropriate to model the habitat in terms of discrete feeding patches.
In simple laboratory tanks, aggressive, dominant individuals tend to monopolize food and space (Metcalfe et al. 1989; Gotceitas & Godin 1992) and to grow faster relative to subordinates, in spite of higher metabolic rates (Metcalfe, Taylor & Thorpe 1995). In a laboratory flume, Atlantic salmon parr adjusted their choice of local foraging site within a fixed resource distribution such that rank correlated with patch quality (Fausch 1984). Similarly, in natural pools where food availability tends to be consistently highest towards the upstream ends, ranks of salmonid parr matched quality of spatial position (Hughes 1992; Nakano 1995). Groups of Amago trout (Oncorhynchus masou ishikawe) offered a choice between two feeding patches of different profitability made preferential use of the better quality patch and after 4 weeks their distribution was as predicted by the Ideal Despotic Distribution (Hakoyama & Iguchi 2001). Therefore, the existing data on juvenile salmon in simple, laboratory conditions with spatially fixed food distributions are consistent with rank-related tracking of changes in resource distribution as predicted by this model.
However, observational studies in the wild have produced some problematic results. Using Passive Integrated Transponder (PIT) tags in a natural stream it has been shown that, although large juvenile salmon have a high degree of overall site attachment (Armstrong et al. 1994), on a finer scale they move between several feeding sites dispersed over c. 1–10 m lengths of stream (Armstrong, Huntingford & Herbert 1999; Martin-Smith & Armstrong 2002). Furthermore, it has been shown recently that in natural riffles the relative availability of drifting food can change over a time-scale of a few hours or less, independent of variation in water discharge (Martin-Smith & Armstrong 2002). The concept of individual fish concentrating their foraging in a single patch of fixed quality may not apply in these circumstances. Additionally, PIT tag studies have shown that the home ranges of individual fish may overlap extensively (Armstrong et al. 1999; Martin-Smith & Armstrong 2002) and several studies of juvenile salmon in natural streams have shown that dominant fish may not be at a growth advantage (Martin-Smith & Armstrong 2002; Sloman & Armstrong 2002; Harwood et al. 2003). The concept of dominant, despotic fish monopolizing favourable feeding areas, thereby enjoying better growth than subordinates, may also not apply.
To resolve these issues it is necessary to examine whether and how salmon of known rank track variable food supplies in natural conditions. This requires a test arena of suitably large scale, but also sufficient control for observed behaviours to be matched unambiguously with variations in food distributions. To achieve this objective, we used replicated sections of an artificial stream that were large enough to accommodate typical home ranges of juvenile salmon in the natural stream used in recent studies (Armstrong, Shackley & Gardiner 1994; Armstrong et al. 1999; Martin-Smith & Armstrong 2002) and a computer-based feed delivery system to generate frequent but unpredictable changes in patch quality, as in the riffle areas of natural streams. The study addressed the following questions for fish foraging in small groups:
Do juvenile Atlantic salmon make preferential use of profitable patches?
If not, what causes a fish to leave a patch in which it has been feeding?
Does social rank influence the ability or willingness of juvenile salmon to track profitable feeding sites?
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- Materials and methods
In this study we set out to determine whether the ability to track variable resources and the strong effect of social status on foraging behaviour that underpin Ideal Despotic models and that have been demonstrated clearly in juvenile Atlantic salmon under simple laboratory conditions are also evident in more complex conditions. Starting with the question of whether these fish make preferential use of profitable patches, our data show that on average the fish allocated just 5% more of their foraging activity to patches at the rich feed delivery level than those at the poor level. This was the case even though food was almost 10 times more abundant on rich patches, with concomitant differences in rates of food intake.
Far from making strongly preferential use of profitable patches, most individuals behaved randomly with respect to patch quality. Some used the feeding patches in a manner that differed statistically from random, but the nature of the non-randomness was not consistent across fish. Given the large and functionally significant difference in food availability between rich and poor levels and the number of replicates, it is unlikely that the experimental design was inadequate to permit discrimination of an effect. The complete lack of differences in behaviour between the control fish (which experienced consistently rich feeding patches) and the experimental fish (which experienced unpredictable 10-fold swings in patch quality) also suggests strongly that fish were not adjusting their behaviour to variable patch quality on the spatial and temporal scale used in this study. In addition, as all patches delivered food at the rich level approximately 50% of the time, and most fish spent less than 50% of the available time foraging (Fig. 3), even fish with low movement rates had the potential to bias their activity to the rich food levels. The fact that juvenile Atlantic salmon do not bias their foraging activity towards rich patches contradicts a core assumption of Ideal Despotic models (including that of Ruxton et al. 1999), namely that individuals switch among foraging sites on the basis of food availability.
This raises the question of what causes juvenile Atlantic salmon to leave patches on which they have been feeding, given that they did not leave in response to a change in food availability. Our focal animal observations showed that, in addition to a strong behavioural momentum (i.e. fish tended to continue doing what they were doing), in many cases (44%) when fish left a patch this was in response to an aggressive interaction, with the loser usually the one to leave. In the majority of cases, movement away from a patch was defined as spontaneous, in the sense that we could see no predictors of leaving.
In terms of the influence of social rank on the ability or willingness of juvenile salmon to track profitable feeding sites, in spite of clear and consistent behavioural polarization between dominant and subordinate individuals and in spite of the fact that losing an aggressive interaction can sometimes prompt a fish to move between feeding patches, we found surprisingly few effects of rank. The two fish that left rich patches less than predicted on a random model were both dominants, and one index of preferential use of rich patches (leave preference) was related significantly to movement rate in dominant but not subordinate fish. At the most, therefore, those dominant fish that have preferences for high-quality patches may be free to express these, whereas frequently moving subordinates are not. The fact that differences in social status that are clearly evident in juvenile salmon foraging in (almost) natural conditions have so little effect on use of feeding patches where these are so different in profitability is contrary to our strong expectations based on previous studies (e.g. Fausch 1984; Gotceitas & Godin 1992; Hughes 1992; Hakoyama & Iguchi 2001) and to the assumptions of many models based on the Ideal Despotic Distribution.
Several key features of the present study, including several that are comparable to natural conditions, may explain these unexpected results. In the first place, densities were lower than those used in most laboratory studies. In addition, the fish had several feeding patches to choose among rather than just two (as in the study of Hakoyama & Iguchi 2001, for example) and these patches were isolated visually (in contrast to the study of Gotceitas & Godin 1992, for example). Additionally, and perhaps most importantly, patch quality was variable rather than fixed, as in the study of Fausch (1984), who found that dominance rank of juvenile Atlantic salmon in an artificial stream closely matched patch quality when the spatial distribution of food was predictable over time. Given patch qualities that are stable over time, sampling among patches would allow animals to obtain necessary information on the distributions of resources and competitors before becoming attached to the best defensible site. Even if initial sampling were expensive (in terms of predation risk or attacks from conspecifics, for example), the pay-off would be substantial for most fish. When patch options can be compared visually, as in the experiment of Gotceitas & Godin (1992), sampling costs are likely to be low and hence tracking the quality of variable patches worthwhile. Decreased habitat stability and/or increased visual complexity reduce the marginal gains from a bout of sampling and make it necessary to sample more frequently to maintain foraging potential. In such conditions, the cost of sampling may well start to outweigh its benefits; an effect of predation risk, and hence the cost of sampling, on selectivity has been described in a number of taxa in the context of foraging (e.g. Mayer & Valone 1999; Leaver & Daly 2003) and mate choice (e.g. Forsgren 1992; Godin & Briggs 1996).
Little information is available on variations in patch qualities in natural streams, although on a time-scale of several hours in riffle habitats there is considerable variation (Martin-Smith & Armstrong 2002 and unpublished), probably arising from patchiness in drift from the benthic invertebrate community and aerial input and from the activities of upstream competitors, which exert shadow competition (Lubin et al. 2001) by filtering food from the water column. Thus it is likely that there is intense short-term variation in local food abundance, which means that efficient short-term tracking of patch qualities may not be possible.
It is possible that the fish in the present study were attempting to track processes fluctuating over longer time-scales than those used in our manipulations that partly determine patch quality, for example seasonal changes in discharge affecting local water velocities (Nislow, Folt & Parrish 1999). There is evidence from a simple laboratory experiment that some individual salmon track local velocity changes; however, in that case the majority of the population chose to remain locally site-attached (Kemp, Gilvear & Armstrong 2003). Some of the unexplained spontaneous movements observed could be associated with such long-term sampling.
Information accrued by sampling need not be food availability per se but could include other knowledge, for example, which other known individual con- and hetero-specific competitors remain alive within the home range. Knowledge of competitors may be as important as that concerning other environmental factors in enabling individual fish to assess risk and to improve their efficiency of habitat use (Koops & Abrahams 1999).
There are trade-offs inherent in the design of any scientific study. In our case, the principal trade-off was between studying fish in an environment that was as close as possible to that typically experienced in the wild, and using an environment where we could actually obtain the measurements needed to test our hypotheses. The detailed visual observation of feeding behaviour of juvenile salmonids necessary for this study could not be obtained from fish in a real stream without the imposition of very substantial lighting and video technologies, which would probably have affected fish behaviour significantly. Furthermore, control of food supply is essential to monitor responses of fish to changes in patch quality over time. Hence, we decided that the optimal solution was an artificial stream in a glass-sided channel with every effort made to provide as realistic a setting for the fish as possible, while retaining control of food provision. Another trade-off that we needed to tackle was between the realism of the system and the number of replicates. Because we gave the fish a very substantial area in which to range and interact, this necessarily reduced the sample sizes that we were able to achieve. While our sample sizes compare favourably with similar studies, they are not of the exhaustive nature needed to completely eliminate all reasonable concerns about the possibility of us failing to reject null hypotheses simply as a consequence of low statistical power. Hence, we accept that our arguments based on observations of no effects ought to be considered as suggestive rather than absolutely definitive.
This study provides an illustration of the potential problems in extrapolating from simple laboratory studies to make predictions of population processes within more complex environments. With respect to salmon in particular, and probably also many other animals, two areas of uncertainty emerge that need to be understood more thoroughly before further progress can be made. First, there is a need to understand in much more detail exactly how animals perceive mortality risk and integrate it into foraging decisions. It is well established that foraging is sensitive to predation risk (Lima & Dill 1990), and various mechanisms have been identified by which the presence of predators could potentially influence prey behaviour. For example, in various species individuals can identify chemical cues produced both by potential predators and by injured conspecifics (Kats & Dill 1996; Wisenden 2000) and learn to recognize areas in which they themselves (Csanyi 1985; Huntingford & Wright 1989) or their conspecific companions (Brown & Laland 2003) have received predatory attacks. However, there is little understanding of how these various cues are integrated to give an overall perception of risk by individual animals. This is in spite of the fact that there is an extensive literature on the mechanisms that underlie antipredator behaviour in animals (Kavaliers & Choleris 2001) and that the outcome of predictive models can be extremely sensitive to this factor (Lima 1998; Mitchell & Lima 2002). Secondly, the magnitude and frequency of fluctuations in relative local patch qualities need to be understood in more detail. To date, the definition of measurements of drift available to juvenile salmon has been c. 3–6 h, commensurate with obtaining an adequate sample of invertebrate drift and keeping the effects of disturbance during placement of collecting equipment small relative to the sample period. New techniques and approaches are needed to monitor the short-term variations in prey availability that may drive the behaviours of predators and explain discrepancies between studies in simple and more natural environments. Furthermore, such short-term variations need to be integrated with measurements at a range of time-scales to make predictions of how animals could sample the environment effectively.
This study points to some general principles in developing behavioural ecology. Small-scale laboratory studies in simplified environments are useful for identifying the behavioural capabilities that dictate what animals can potentially do in natural conditions. However, assumptions should be scrutinized and predictions tested in near-natural conditions, even when this requires the development of sophisticated ways of conducting manipulations in the field and controlled but complex laboratory tests.