250 (2000) 77–95
www.elsevier.nl / locate / jembe
Poor design of behavioural experiments gets poor results:
examples from intertidal habitats
* M.G. Chapman
Centre for Research on Ecological Impacts of Coastal Cities, Marine Ecology Laboratories A11,
University of Sydney, Sydney, NSW 2006, Australia
Abstract
Many patterns of distribution and abundance of intertidal animals are explained by processes of movements of animals, selecting particular habitats or levels on the shore, or interacting with other species. Movements of intertidal animals have therefore been studied over many years. During this long history, much intertidal ecology has changed in focus from broad-scale to small-scale patterns and processes, although there has been recent refocus on a combination of many scales. Simultaneously, there has been an increase in the incidence of field experiments and growing recognition that behaviour is more flexible than originally thought. This review examines changes in the ways that experiments on movements on intertidal animals have been and are being done, taking into account these changes in emphasis. Although some progress has been made, there is still a long way to go. The idea is still prevalent that behaviour is simple, rather invariant and that the animals respond to broad-scale cues that have traditionally been of interest to many investigators. This means that many experiments are still designed to minimise (or ignore) natural variation in behaviour rather than to measure it and that any associated disturbances are considered irrelevant and therefore not evaluated. Understanding the role that behaviour has in establishing and maintaining many of the patterns observed on intertidal shores is crucial to our understanding of the ecology of these habitats. Better experiments, designed logically with appropriate controls to evaluate realistic processes and to measure how behaviour varies among places and from time to time can only improve this understanding. 2000 Elsevier Science B.V. All rights reserved.
Keywords: Behaviour; Experimental design; Intertidal; Movements; Variability
1. Introduction
Patterns of distribution and abundance of intertidal animals are frequently explained
*Tel.: 161-2-9351-4778; fax: 161-2-9351-6713.
E-mail address: gee@bio.usyd.edu.au (M.G. Chapman).
by the behaviour of the species under consideration, or of those with which they interact. Although patterns of sessile species may be determined initially by larval behaviour (e.g. Crisp, 1974; Bourget, 1987), these patterns can be altered by mortality caused by mobile animals. Consumers remove species in a patchy manner (Fairweather, 1988a), which can subsequently affect the distribution and abundance of animals which feed on or shelter amongst these prey (Underwood et al., 1983). In addition, small animals can be killed during foraging by larger animals (Dayton, 1971; Denley and Underwood, 1979; Hill and Hawkins, 1991). Behaviour of large mobile animals, therefore, has a major influence on patterns of distribution, abundance and dispersion of many species on intertidal shores.
These effects are patchy because the animals are not distributed evenly across intertidal shores. Animals are generally limited to certain heights on a shore (Lewis, 1964), are more abundant in particular habitats (Underwood, 1976; Emsen and Faller-Fritsch, 1976; Raffaelli and Hughes, 1978; Byers and Mitton, 1981; Chapman, 1994) or may aggregate without any obvious correlation with habitat (Chapman, 1995). They can select among different patches of habitat and change behaviour and patterns of movement from time to time or place to place, in response to physical conditions (Mackay and Underwood, 1977; Moran, 1985; Jones and Boulding, 1999), growth (Moreno et al., 1993) or the presence of other animals (Fairweather, 1988b). For most species, the precise cues that cause variation in behaviour have not yet been identified. The behaviour of intertidal animals has been studied for a long time, partly because patterns of distribution, abundance and dispersion are easily quantified and because many species and their habitats are suitable for experimental investigation (reviewed by Underwood, 1979, 1985). Many species are easy to see and capture, can be handled, marked or manipulated to alter densities (Menge, 1972; Underwood, 1988), or can be moved among habitats (Chapman and Underwood, 1994) or to different heights on the shore (Gendron, 1977; McQuaid, 1981). Their surroundings may also be manipulated to identify cues to which the animals respond (Cook, 1969; Menge et al., 1983; Worthington and Fairweather, 1989; Underwood and Chapman, 1992; Chapman and Underwood, 1994; Crowe, 1996). Thus, the behaviour of intertidal animals on rocky shores has a long history of direct experimental study, often under natural conditions.
Because the behaviour of mobile intertidal animals is a broad topic, this review will focus on experimental studies of movement, orientation and selection of habitat by intertidal animals, particularly molluscs. Some species have been studied on different rocky shores using different methodologies, e.g. Patella vulgata L. (Lewis and Bowman, 1975; Hartnoll and Wright, 1977; Little et al., 1988; Evans and Williams, 1991; Chelazzi et al., 1994). In other studies, different species have been compared on the same shores (Underwood, 1976; Levings and Garrity, 1983; Fairweather, 1988b; Chapman, 2000). These may allow evaluation of general trends in behaviour, in addition to documenting how variable they may be.
patterns of patchiness (Underwood and Denley, 1984; Thompson et al., 1996) and from studies of behaviour done in the laboratory (e.g. Fraenkel, 1927) to experimental field studies (Underwood, 1993). These changes have influenced the way in which experi-ments on the behaviour of intertidal animals were done, are still being done and the way that results are interpreted. Although these trends will be examined separately, it is important to remember that they occurred simultaneously.
This review will evaluate changes in the ways that movements and habitat-selection of intertidal animals has been studied while these broad changes in focus have evolved. It is attempted in the spirit of learning from mistakes of the past in order to progress into the future with a more rigorous and logical approach to understanding behavioural ecology of intertidal animals. Unfortunately, it has therefore been necessary to criticise what has been wrong with the ways in which many studies have been done, rather than spending too much time on what had been found out in such studies. The references cited are a few chosen from a very large set of papers on these topics, simply to illustrate the points being made. Most are not particularly better or worse than many others that could have been discussed. Most of the errors illustrated are not limited to these papers, but are widespread in the literature, including many of my own published studies. We can all learn from critical evaluation of past practices. Better behavioural experiments will give better ecological understanding. It is hoped that this review will help in the design and interpretation of such experiments.
2. Change in focus from fixed to variable behaviour
For many years during the early studies of animal behaviour, it was believed that behaviour of animals, invertebrates in particular, was rather invariable — any variation shown was simply ‘noise’ and of little interest (reviewed by Foster and Endler, 1999). This was followed by increasing recognition of variability in behaviour, particularly at a geographic scale, which was thought to represent adaptational changes of populations to local conditions. Most of the focus of this work has been terrestrial vertebrates (Foster and Endler, 1999). The reproductive strategy of many marine invertebrates, i.e. broadcast fertilization and long-lived planktonic larvae suggests considerable genetic interchange among populations (Scheltema, 1971) and little genetic connection between adults and recruiting larvae on local shores (Berger, 1973; Snyder and Gooch, 1973). These traits would tend to counteract many local adaptations.
There are many examples of differences in behaviour among populations of intertidal invertebrates, for some of which there is a genetic basis. For example, Scapini et al. (1999) showed in laboratory experiments that the amphipod Talitrus saltator (Montagu) orientated seawards, towards the sun or randomly, depending on their shore of origin. Breeding experiments suggested that orientation was partly genetic, but was also influenced by experiences of juveniles. McKillup (1983) showed that populations of Nassarius pauperatus (Lamarck) varied in their behavioural responses to conspecifics differently among shores. There were two distinct forms of behaviour — twisting and non-twisting. Twisters showed specific rotations of their shells when in contact with conspecifics. Non-twisters did not. The prevalence of each within a population depended on whether the population had been feeding on a point or diffuse source of food. The behaviour was fixed within individuals and the relative abundance of different morphs from population to population determined the predominant behaviour in the population. Interchange among populations via planktonic larvae maintained each morph in each population.
Some forms of polymorphic behaviour can show differences at very small spatial scales, despite considerable genetic interchange among populations. Thus, populations of the small limpet, Patelloida mufria (Hedley) living on intertidal rock-platforms, are epizoic on the shells of other gastropods (Mapstone et al., 1984). The shells of the limpets grow to fit the curvature of their host shells and they cannot attach firmly to the rocky substratum. The same species is found under intertidal and shallow subtidal boulders (unpublished data) and on subtidal rocky reefs (Fletcher, 1988), where they co-exist with a suite of other limpets on the rock surface. Intertidal and subtidal populations may only be separated by a few metres and are not geographically isolated. Many species show very marked differences in behaviour among different shores, or among different patches of habitat on the same shore, e.g. in response to tidal amplitude or exposure (Cook and Cook, 1978), to different amounts of food (Mackay and Underwood, 1977), or to availability of microhabitat (Chapman and Underwood, 1994). Some species show marked ontogenetic changes in behaviour. The limpet Acmaea incessa (Hinds) change from feeding on micro-algae on the feeding scars of adults to developing their own feeding scars on the kelp Egregia laevigata (Setchell) as they get older (Black, 1976). Similarly, young Patella longicosta Lamarck settle and feed on the shells of adults until large enough to defend their own feeding territories on the rock surface (Branch, 1971). These changes in behaviour are well documented, but for many species, it is not known whether behaviour changes markedly as the animals get older and, for many species, it is not easy to equate size with age (or maturity). Therefore, how much of the variability in behaviour among populations may be governed by the age-structure of the populations is seldom known.
Bourget, 1989) and littorinds (Chapman and Underwood, 1996) was influenced by local environmental heterogeneity, time of emersion and the weather. The decision to forage by the whelk Thais lapillus (L.) was influenced by local environmental conditions and the state of hunger of the animals (Burrows and Hughes, 1989, 1991).
Much evidence now suggests that behaviour of intertidal invertebrates is very flexible. It changes in response to broad-scale and localized environmental and physiological cues and, therefore, would be expected to vary spatially and temporally. Nevertheless, many studies of behaviour are done once in one area and the results presented as if they demonstrate fixed patterns of behaviour.
3. The change in focus from broad to small scales of spatial patterns
Along with the change of emphasis from fixed to variable patterns of behaviour, there has been a change in focus from broad-scale patterns of distribution and abundance to patterns of abundance which vary at an hierarchy of different spatial scales, which themselves can vary from place to place (Underwood and Chapman, 1996). Many factors cause patchiness, but this change in focus has been strongly influenced by the recognition of the importance that natural disturbances play in ecological interactions (Pickett and White, 1985) and that, on intertidal shores, many disturbances are relatively localized and patchy (e.g. Dayton, 1971; Sousa, 1979, 1984; Archambault and Bourget, 1996; Benedetti-Cecchi and Cinelli, 1996; Underwood, 1999).
Distribution and abundance of animals on intertidal shores were originally thought to be governed primarily by large-scale physical factors, particularly the height above sea level, or the degree of exposure to waves (Lewis, 1964; Stephenson and Stephenson, 1972). These theories were often supported by laboratory tests on physiological tolerances of different species to desiccation or heat, which often showed a greater tolerance in those species which lived higher on the shore (Brown, 1960). In many cases, tolerances were, however, far in excess of what might normally be encountered and their ecological importance has been debated (McMahon, 1990). In other studies, there has been little relationship between vertical zonation and physiological tolerances (McMahon and Britton, 1985), or animals have behaviours that cause them to avoid potential lethal conditions (Wolcott, 1973). Subsequent experimental work on responses of organisms to physical stress in the field (Connell, 1972; Menge, 1978a,b; Underwood, 1991a, among many others) and detailed quantification of patterns of abundance at a hierarchy of scales (Archambault and Bourget, 1996; Benedetti-Cecchi and Cinelli, 1996; Thompson et al., 1996; Underwood and Chapman, 1996) have suggested that physical stresses associated with these two broad-scale gradients are not adequate to describe patterns of abundance for many intertidal organisms.
the same level of a single shore. Behaviour was compared among shores which differed in wave-exposure or tidal inundation, as if there was little variability within a shore, using a single site per shore and thereby replicating the wrong units of focus (pseudoreplication sensu Hurlbert, 1984). For example, Cook and Cook (1978) examined patterns of activity in two species of siphonarian limpets in three sites in the Marshall Islands and two sites in Bermuda. The sites were selected to vary according to wave-exposure, slope, drainage and exposure to sun, but, within each site, the activity of the limpets was measured in as small an area as possible, to minimise local environmen-tal variability. Nevertheless, the activity in these small patches of habitat was assumed to represent activity in the site as a whole. Comparisons among different environmental conditions were thus made without comparable data from replicate sites within each set of environmental conditions.
Similarly, many early experiments that examined changes in behaviour when animals were transplanted from one height on the shore to another, did not examine replicate sites at each height (McQuaid, 1981; McCormack, 1982), assuming that the only factor that might influence movement was height on the shore. Without measures of variability from site to site within each height, it is not possible to interpret any difference between one site at one height and one site at a different height to be due to the heights of the two sites. Studies that have examined similar transplant experiments in multiple sites and in multiple experiments, incorporating all necessary controls for disturbing and transplant-ing the animals (Underwood, 1988; Chapman and Underwood, 1992) have shown considerable small-scale spatial variability in the responses of intertidal animals to experimental treatments (Chapman and Underwood, 1994; Crowe, 1996; Chapman, 1999a).
Measuring variation among sites does not mean that general patterns of behaviour cannot be identified because similar trends can be shown in different sites, even if detailed differences among treatments vary from place to place (Chapman, 1999a). In this case, what is important is the general pattern of behaviour and the spatial and temporal scales at which it varies, thereby focussing attention of causation at the relevant scales. Of course, if patterns of behaviour do vary significantly in different ways among replicate sites in what was expected to be a homogeneous habitat, then the results indicate that we are focussing on the wrong variables to measure the habitat. The animals must be responding to some environmental condition or feature of habitat which was not considered in the general model, i.e. there may be no generality of behaviour at the scales we are investigating. Many behaviours appear to be very plastic traits, changing rapidly and differently to varying environmental conditions.
4. The change in focus from laboratory to field experiments
4.1. Laboratory-based studies
Much of the work on behaviour on intertidal animals has been done using gastropods, which are large, have distinct patterns of distribution and abundance and are relatively easy to collect and maintain in aquaria. Early focus on invariant behaviour and large-scale patterns of distribution and abundance inevitably led to the early studies of behaviour focussed on simple variables to which animals responded in fixed ways. These responses were primarily studied in the laboratory, e.g. the classic work by Fraenkel (1927) on the role of positive and negative phototaxes and negative geotaxis on the highshore distribution of Littorina neritoides (L.). It was believed that orientation and movement of invertebrates largely consisted of fixed responses to environmental cues, e.g. taxes or kineses in response to light or gravity. The importance of such cues was investigated in the laboratory so that the environment could be rigorously controlled, except for the particular cues being applied. The results of such studies were then used to describe behaviour and explain patterns of distribution and abundance in the field.
For many years, simple and invariant patterns of behaviour measured in very artificial conditions in the laboratory were considered adequate to describe patterns of distribution and abundance of L. neritoides and other similar species, despite documented patterns of distribution which could not be explained by such models of movement (reviewed by Underwood, 1979). Many of these experiments would not have been done, nor the particular cues investigated, had more attention been paid to quantifying the patterns of distribution and abundance in adequate detail, or examining the different conditions in field under which the particular behaviours were shown.
Trail-following by snails has also received a lot of attention in laboratory studies. Many snails follow their own or conspecific trails (Wells and Buckley, 1972; Tanker-sley, 1990; Chapman, 1998) or those of their prey (Paine, 1963). Certain species of limpets (Branch, 1981) or chitons (Chelazzi et al., 1990) consistently home to fixed sites on the shore, frequently by returning along outgoing trails. Much of the research on the incidence of trail-following (Wells and Buckley, 1972; Erlandsson and Kostylev, 1995) or the cues that snails or limpets use to identify trails (Cook, 1971; Cook and Cook, 1975) is laboratory-based, whereas homing has generally been studied in the field. In the laboratory, trails were usually laid on glass or other artificial surfaces and the responses of animals recorded after they were picked up and placed on these trails. The animals are generally assumed to behave in the laboratory as they would in the field and little consideration has been given to the possibility that trails laid on artificial surfaces cause abnormal behaviour.
number of days prior to experimentation (Hagen and Mann, 1994; Davies and Beckwith, 1999). Chapman (1998) showed that the incidence of trail-following increased in animals maintained in the laboratory compared to freshly collected animals.
One reason that trail-following is frequently examined in the laboratory is that trails are difficult to see in the field, or the animals move at times when it is difficult to measure accurately their path, e.g. when the rocks are awash (Chapman, 1998). Homing by limpets has been examined in the field using photography (Cook et al., 1969) or triangulation (Cook, 1969). Recent advances by Chelazzi et al. (1987, 1990) involve attaching light-emitting diodes (LEDs) to the shell of gastropods and chitons, so that individual animals can be tracked during the day and night for relatively long periods of time. This technology does, however, mean that animals are generally only tracked in relatively small patches of habitat, thereby not recording spatial variability in behaviour, or more importantly, interactions between spatial and temporal patterns.
4.2. Quasi-field experiments
Growing awareness that behaviour measured under artificial laboratory conditions is unlikely to reflect accurately what animals do in the field has led to two new approaches. The first was to try to make laboratory conditions more realistic. One of the earlier attempts to do this was to measure behaviour in tidal tanks, which are essentially aquaria with regular changes in water level to mimic tidal change (Underwood, 1972). These subjected animals to what was considered to be the most important aspect of intertidal habitats — the rise and fall of the tide. Using a tidal tank, Evans (1965) found that four species of littorinid snails distributed themselves in the tank in a manner that mimicked their distribution on the shore and that L. neritoides reversed the ‘fixed’ taxes shown earlier by Fraenkel (1927). This pattern of zonation broke down, however, in the dark, although there is no evidence that natural patterns of distribution on the shore vary between day and night.
Another method of attempting to make laboratory conditions more natural is to transfer the animals into the laboratory along with patches of natural habitat, assuming that this causes no or minimal disturbance (Della Santina and Naylor, 1994). Field experiments have, however, shown that many intertidal gastropods respond rapidly to various experimental disturbances (Petraitis, 1982; Underwood, 1988; Chapman, 1998), suggesting that this assumption should always be tested first.
Boulding, 1999) and incorporated controls to test for artefacts associated with the artificial structures (Chapman and Underwood, 1994).
4.3. Field experiments
Over the past 30 or so years, there has been an increasing tendency to do experiments in the field to investigate processes that influence the behaviour of animals in habitats where such processes are likely to be operating (Underwood, 1993). This came about partly from better documentation of the considerable and hierarchical spatial (Dayton, 1971; Underwood, 1975, 1976, 1981; Menge et al., 1985; Chapman, 1994; Archambault and Bourget, 1996; Underwood and Chapman, 1996). and temporal (Connell, 1985; Moran, 1985; Chapman and Underwood, 1996) variability of patterns of distribution and abundance at various scales. Such complex patterns cannot be explained by fixed responses to simple variables. In addition, there has been growing recognition that field experiments are not only possible, but essential to an understanding of natural processes (Connell, 1974; Underwood, 1985, 1986, 1988). For example, although it can be demonstrated that many snails show fixed responses to light, gravity or other physical variables in aquaria in the laboratory, they live in a world with crevices, holes, ridges and lumps and an array of other species that provide complex habitat at a variety of scales, in places where environmental conditions change rapidly and unpredictably.
With the recognition that it is more relevant to examine behaviour of animals in the field in order to explain natural patterns of distribution, abundance and dispersion, field experiments now predominate in the literature. These may be supplemented by laboratory experiments which can examine responses of animals to particular stimuli (Barnes, 1981; McQuaid and Scherman, 1988; Chapman, 1998), but there has been a change of emphasis so that the results obtained in the laboratory supplement those obtained in the field, rather than the other way around.
Field studies on movement, orientation and habitat-selection fall into two general categories. Many studies monitor the behaviour of undisturbed animals in order to record natural patterns of activity (Underwood, 1977; Cook and Cook, 1978; Chelazzi et al., 1987; West, 1988; Chapman, 1999b, 2000). Others use experimental manipulations of the animals themselves (Gendron, 1977; McQuaid, 1981; Chapman, 1998, 1999a) or of their habitat (Menge et al., 1983; Fairweather, 1987; Chapman and Underwood, 1994; Crowe, 1996) to attempt to identify particular cues to which the animals respond. Many studies are a combination of the two approaches. Models that might explain particular patterns of behaviour may be proposed from patterns of undisturbed activity and hypotheses from these tested using manipulative experiments (e.g. Mackay and Underwood, 1977; Underwood, 1988; Chapman and Underwood, 1994).
1990), it is necessary that the animals are individually marked, even if they are not moved or otherwise disturbed. Gastropods are often marked using paint (Chapman, 1986) or small markers glued onto the shell (Cook and Cook, 1978; Chelazzi et al., 1987, 1990). These methods of marking individuals in situ are usually assumed not to alter behaviour, although there have been few investigations of whether this is the case (Chapman, 1986). If marking individuals involves removing them from the substratum, there may be excessive disturbances, that may lead to artificial patterns of behaviour (Underwood, 1988; Chapman and Underwood, 1992).
Some of the more informative field experiments have involved manipulations of animals or their habitats to test very specific hypotheses about mechanisms causing spatial patterns of abundance. For example, there have been numerous field in-vestigations of the role that differential patterns of movement may play in vertical patterns of distribution or vertical size-gradients of intertidal species (Gendron, 1977; McQuaid, 1981; Doering and Phillips, 1983; Williams, 1995; Chapman, 1999a). Such experiments generally involve transplantation of snails to different levels on the shore. The direction and extent of movement of these transplanted animals are compared to animals remaining within their normal zone of distribution. Such studies have frequently identified movement back towards natural levels on the shore and have been considered adequate to explain the maintenance of zonation of certain species. There are many flaws in the design and analyses in many of these experiments because moving animals from one height on the shore to another has many associated experimental artefacts that need to be tested before any patterns of movement can unambiguously be attributed to height (reviewed by Chapman and Underwood, 1992). Nevertheless, with appropriate controls, these and similar experiments can be very informative about the role of movement in the observed patterns of distribution and abundance and the specific features of habitat to which the animals respond (Underwood, 1988; Chapman and Underwood, 1992; Crowe, 1996).
5. Where have these changes in emphasis got us?
Having summarised the three broad changes that have gone on over the past 50 years in the study of the behaviour of intertidal animals, it is appropriate to examine what progress has been made and, more importantly, what still needs to change if we are to advance our understanding of these topics.
5.1. Laboratory versus field studies
given to the value of the results of such work in explaining natural patterns of distribution and abundance (e.g. Hagen and Mann, 1994; Johnsen and Kier, 1999).
Models that are proposed to explain natural patterns of distribution, abundance, etc., must be relevant to the conditions and scales at which the patterns are described. Tests of hypotheses derived from such models will generally be more informative if done under the natural conditions similar to those under which the patterns were originally described. It is very important that future studies of behaviour of intertidal animals use field experiments wherever possible. Then, behaviour will be expressed under the same sorts of environmental conditions as the documented patterns that the behaviour is proposed to explain. When addressing questions that cannot be addressed easily in the field, e.g. trail-following in species where the trails cannot be followed in the field (e.g. Chapman, 1998), it is essential that such studies be accompanied by field tests of related hypotheses, so that differences between field-based behaviour and laboratory-based behaviour can be measured and the relevance of the laboratory studies sensibly evaluated.
5.2. Spatial and temporal variability
Recent field-based experimentation in different sites and on different shores has clearly illustrated that animals do not behave the same way in different places. They respond to their immediate surroundings and these surroundings are patchy. For many organisms, this occurs at a scale of centimetres, not metres or hundreds of metres (Chapman, 1995; Underwood and Chapman, 1996). Animals may respond to cues that are not visible to us and therefore are seldom measured (e.g. patchy micro-algae, Mackay and Underwood, 1977), or to cues which we do not even recognise as being present or important.
within each time frame of interest (as discussed by Underwood, 1991b) with respect to assessments of environmental impacts.
Experiments are sometimes repeated in the same or different places, but then analysed as separate experiments. Thus, any advantage that might have been obtained by quantifying variability in behaviour at different times or places is lost. Repeating experiments may not only provide such data (e.g. Crowe, 1999; Chapman, 1999a,b, 2000), but can also provide more powerful analyses of behaviour by specifically looking for generality against measured background variability (e.g. Underwood and Chapman, 1992). The use of cross-study analyses requires a lot of careful thought in design and interpretation (e.g. Underwood and Petraitis, 1993; Osenberg et al., 1999), but these are potentially useful tools that deserve more consideration in studies of behaviour on intertidal shores. Unfortunately, general conclusions about factors influencing move-ment, orientation and habitat-selection are still drawn from studies of very few animals, examined for very short periods of time, in one small site on one shore. To some extent, this is because researchers act as though they retain the background idea that behaviour is relatively invariant. Therefore, under this paradigm, searching for variation would appear to be pointless and no attempt is made to replicate the study.
The argument that ecologists and statisticians need to change from emphasising mean values to more consideration of variances (Underwood, 1994), applies equally to studies of behaviour. The factors that cause variation in behaviour at a small scale have to be identified and measured if the role of behaviour in determining patterns of distribution and abundance at a large scale is to be understood. This is increasingly important as anthropogenic activities fragment and alter natural habitats.
5.3. Experimental artefacts
Recently, there has been increased emphasis on appropriate experimental design in ecology, including experiments to test behavioural responses of animals (Chapman, 1986; Underwood, 1988, 1997; Chapman and Underwood, 1992; Quinn and Keough, 1993; Peterson and Black, 1994; Huston, 1997; Crowe and Underwood, 1998; Fernandes et al., 1999, amongst others). Despite this literature, many behavioural experimentalists have not given enough thought to appropriate controls for various experimental artefacts, nor for potential effects of handling and other disturbances on the behaviour of the animals.
of the different controls needed to distinguish between increasing density per se and moving animals into unfamiliar surroundings in experiments designed to test for effects of increasing density on dispersal. Some marine gastropods therefore respond very quickly and in major ways to what have been considered relatively minor disturbances. This is also likely to be equally true for other intertidal animals, although it has not been measured for many species.
In addition, experimental disturbances can interact with habitat (e.g. Peterson and Black, 1994) and what might appear to be no measurable disturbance of experimental manipulations in some experiments (e.g. translocation: Chapman, 1986) may cause disturbance in others, even when tests are done using the same species (Chapman, 1999a). Therefore, considerably more attention needs to be paid to designing experi-ments that measure associated disturbances. Ignoring them does not make them go away. Many analyses used in behavioural ecology are inadequate for the models being investigated. The sorts of experiments needed to unravel what are complex behavioural responses in complex habitats are, necessarily, complex. The data cannot be correctly interpreted unless use is made of the full range of appropriate analytical tools available. Therefore, multifactorial hypotheses about variation in behaviour, need multifactorial experimental designs and multifactorial analyses (e.g. Underwood and Chapman, 1985; Underwood, 1997). Simple analyses and subjective comparisons of results among treatments are not really adequate. Nevertheless, they are still used in published accounts of behaviour of intertidal animals.
5.4. Scale of investigation
Some species have been examined over long enough periods of time to illustrate the change in approach of the researchers to particular ecological questions. For example, the alternate patterns of dispersal and aggregation of whelks have been studied for many years by many different researchers. Early work emphasized the role of large-scale environmental variables on these behaviours, e.g. the effects of season or inclement weather (e.g. Feare, 1971) on the tendency to shelter or feed. Recent work has tended to concentrate on such factors as local abundances of different prey or habitat (e.g. Fairweather, 1988b), interactions between shore-level, weather and tides (e.g. Moran, 1985) and the interaction between environmental conditions and the physiological state of the animals (e.g. Burrows and Hughes, 1989, 1991). This illustrates the shift in emphasis from large-scale factors to a more realistic assessment of what might be the structuring processes at the scales at which the animals operate.
move, when to stop feeding, which microhabitat to occupy, etc. are going to be made at the scale at which these animals experience their surroundings. They must, therefore, vary from place to place interactively with time to time. Experiments that ignore this variability cannot provide a great deal of useful information. There is growing awareness that in order to understand how animals respond to habitat, it is necessary to envisage the world from the perspective of the animal in question (Wiens and Milne, 1989; Wiens et al., 1995; With and Crist, 1995). This approach has yet to be incorporated broadly into studies of animals moving in intertidal habitats.
Acknowledgements
This review was supported by funds from the Centre for Research on Ecological Impacts of Coastal Cities. I have benefited over many years from critical reviews from many anonymous referees on my manuscripts and helpful and pertinent discussions with many colleagues and students. Particular thanks to T. Crowe, J. Grayson, B. Kelaher, A.J. Underwood and R.V. Vadas. P. Archambault, A.J. Underwood and two anonymous referees offered helpful comments on an earlier draft of this manuscript. [AU]
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