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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.
Similarly, animals placed in plastic trays Boyle, 1972 or aquaria Hagen and Mann, 1994 are assumed to show natural responses to stimuli. There have been few tests of the
effects of collecting, handling or maintaining the animals under artificial conditions on their subsequent behaviour. Some studies used animals soon after collection, in an
attempt to minimise potential effects of disturbance Boyle, 1972. Others have maintained animals under laboratory conditions, with or without natural food, for a
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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.
The second type of quasi-field experiment was to take the laboratory into the field in order to maintain controlled conditions. Therefore, Evans 1961 examined movement of
Littorina punctata Gmelin on damp, sloping boards placed on the seashore, varying the slope and direction of light. Similarly, Colombini et al. 1994 examined orientation of
the beach-dwelling beetle, Eurynebria complanata Linnaeus by placing them in covered arenas in the field. Again, it is not clear how responses of disturbed animals in
such artificial surroundings, even if these are then placed outside rather than inside a building, can explain natural patterns of distribution or movement in the field
Underwood, 1979. Some experiments that have tested hypotheses about structural complexity of the habitat on movement used attempted to use artificial structures
constructed to resemble natural substratum Chapman and Underwood, 1994; Jones and
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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.
Natural patterns of activity or behaviour have been recorded for many animals, often with minimal amounts of disturbance. If one is examining such variables as the
proportion of a population that is active or feeding or found in particular habitats or patterns of dispersion e.g. Moran, 1985; Chapman and Underwood, 1996, it is not
necessary to identify individual animals. In studies for which it is important to collect data from individuals, e.g. distances or directions dispersed by different animals
Underwood, 1977 or individual variability in behaviour West, 1988; Chelazzi et al.,
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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?
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