J .S. Hindell et al. J. Exp. Mar. Biol. Ecol. 255 2000 153 –174
167 Table 4
The percent abundance N , percent mass M , and percent frequency of occurrence F of dietary categories from stomach contents of Arripis truttacea n 5 15 enclosed in cages within unvegetated sand and seagrass
habitats
Prey items Bare sand
Seagrass N
M F
N M
F Fish
Atherinidae 5
12 13
3 2
7 Syngnathidae
– –
– 5
4 7
a
Unknown fish 3
– 13
– –
– Other
Crustaceans 92
87 60
89 93
40 Polychaetes
3 2
7 –
– –
a
Value , 0.5.
significant difference in the abundance of small fish between exclusion cages and predator cages existed, despite trends which suggest otherwise Fig. 4b.
The syngnathids in the enclosure experiment displayed similar patterns to those seen for syngnathids in the exclosure experiment Figs. 3 and 4c. Despite the trends Fig.
4c, the abundance of syngnathids did not vary statistically across cages, blocks or habitats Table 3 and Fig. 4c.
3.3. Dietary analysis of enclosed Arripis truttacea In seagrass habitats, 40 of Arripis truttacea contained no food compared with 53
of A . truttacea enclosed over unvegetated sand. Of the A. truttacea with stomachs
containing prey, crustaceans were the most common dietary item, and represented 92 and 87 abundance N and percent mass M , respectively. Teleost prey, which
included atherinids, syngnathids and unknown fish remains Table 4, appeared to be a more important component in the diets of A
. truttacea enclosed over unvegetated sand than seagrass Table 4. While atherinids were consumed in both unvegetated sand and
seagrass, syngnathids were consumed only in seagrass, the habitat within which they occur most commonly.
4. Discussion
Fish assemblages vary over a range of spatial and temporal scales Kingsford, 1998. While the importance of choosing an appropriate spatial scale to study fish is well
documented Chesson, 1998; Sale, 1998, very little attention is paid to the role of small-scale temporal variability in experimental studies. Specifically, fish assemblages
vary over relatively short time scales, i.e., tidal and diel cycles Robertson, 1980; Sogard and Able, 1994; Gibson et al., 1996, and therefore, the associated biological interac-
tions, such as predation, are also likely to vary over shorter time scales Laprise and Blaber, 1992. But many studies make only a single recording of fish assemblage
168 J
.S. Hindell et al. J. Exp. Mar. Biol. Ecol. 255 2000 153 –174
structure at the end of an experiment, even though selecting the appropriate duration of an experiment is crucial to the nature of impacts observed Minello, 1993, and
therefore, may ‘lose’ information about how effects may change through time. In our study, the time at which our experiment was sampled had a pronounced effect on not
only whether differences between cage treatments consistent with predation effects were observed, but whether these differences were confounded by cage effects. For example,
during the first two sampling times in the exclusion experiment, the mean numbers of atherinids were similar between cage treatments, and therefore fish were responding
neither to the structure of the cage treatments nor predation. At the third sampling time, uncaged areas contained significantly fewer fish than exclusion cages or cage controls,
and this suggested that atherinids were responding to the cage structure rather than predation. At the final sampling time, exclusion cages contained more fish than either
cage controls or uncaged areas, which contained similar numbers of fish, and this clearly demonstrated that predation by fish, not some artefact associated with the structure of the
cage, was important in determining the abundances of atherinids. Clearly, sampling the same experimental units at short time intervals several days strongly influences the
relative variability in the numbers of fish between caging treatments. However, it is unclear whether these results represent temporal variability in predation and cage effects,
or whether they simply reflect an initial prey response to structure, with a later-emerging predation effect. Replicated experiments that evaluate the consistency of results from
caging studies over variable lengths of time, and over the same temporal scales at different times, are needed to separate these alternatives. Irrespective of how the
numbers of fish varied between cage treatments in our study, this work clearly demonstrates that a strong effect of piscivorous fishes can be measured after 4 weeks,
and this effect depends on the habitat within which it was measured.
Investigations into the impacts of predatory fish on their teleost prey have traditionally used exclusion cages to manipulate predator abundance Doherty and Sale, 1985;
Kennelly, 1991; Steele, 1998. But interpreting the importance of predation relative to cage effects can be problematic because of the difficulty in creating a suitable control,
i.e., a structure that has all the physical effects of a cage but does not keep out predators Virnstein, 1978. Preliminary analysis of our caging experiment suggested that
predation was decreasing abundances of fish outside of areas enclosed by a cage, i.e., small fish abundances were greater inside exclusion cages than uncaged areas. However,
the intermediate numbers of fish associated with cage controls implied a cage effect, i.e., differential attraction of fish to structure provided by exclusion and partial cages and or
intermediate physical effects of the cage controls — partial interference with predatory fishes. The use of enclosure cages, in association with exclusion and partial cages,
enabled us to further evaluate predator effects without confounding results with variable levels of cage structure, i.e., the controls and treatments have the same amounts of
artificial structure — although experiments in which predatory fish are enclosed have been criticised because, even though relatively large enclosures allow more normal
behaviour by predators Virnstein, 1978, the contrived conditions under which predatory fish are enclosed may alter their behaviour and generate ‘unreal’ impacts. In
our enclosure exclusion experiment, significantly more fish were sampled from within
J .S. Hindell et al. J. Exp. Mar. Biol. Ecol. 255 2000 153 –174
169
partial and enclosure cages, both of which contained similar numbers of small fish, than uncaged areas. And there was a trend for more fish to be associated with exclusion cages
than either enclosure cages or cage controls. These data suggest that either predation pressure is similar inside enclosure and partial cages, or the various effects of these two
treatments balance.
Recent experiments using video recorders to quantify local abundances of predatory fish have shown that the design of the cage controls used in this study neither influences
the ambient densities or movement of Arripis truttacea, nor attracts juvenile fishes J. Hindell, unpublished data. Therefore, the predation pressure inside partial cages is
likely to be similar to that exerted in areas without any form of cage structure, and the structure per se of cage treatments does not appear to be important in attracting juvenile
fishes. Furthermore, enclosed A
. truttacea were observed to swim and feed uninhibited — they consumed similar categories of prey to those published elsewhere Robertson,
1982; Hoedt and Dimmlich, 1994. Given that predation impact is similar in enclosures and partial cages, we contend that partial cages may be a form of intermediate protection
for small fish, and differences between partial and exclusion cages are more likely to reflect predation and not simply a linear increase in fish attracted to additional artificial
structure per se.
Because partial cages may not provide an unambiguous test for cage effects, the results from caging studies which exclude predators should be augmented with
additional data which elucidates the effects of cage structure Connell, 1997. Tradition- al measures of cage effects, such as organic content, particle size distribution and
meiofaunal abundances in sediments were unaffected by the design of the cages and controls used in this study J. Hindell, unpublished data; however, a more ecologically
meaningful alternative to assessing cage artefacts, especially in relation to the attraction of juvenile fishes, may be through measuring the variability in abundances of fish
between cage treatments that have a strong affinity with habitat structure. Sygnathids are strongly associated with structurally complex habitats Gomon et al., 1994, but can be
found in unstructured habitats, such as unvegetated sand, where drift algae occurs. Additionally, the general length of syngnathids measured in our study are rarely
consumed by Arripis truttacea, therefore, differences between cage structures are more likely to reflect habitat selection rather than predation, and these fish may be useful in
evaluating the role of cage effects related to the facilitation of structure. In our experiment, unvegetated sand habitats contained larger numbers of syngnathids where
cages and cage controls provided structure, but there was no difference in the numbers of syngnathids between cage treatments. This implies that there may be some threshold
level of structure see Gotceitas and Colgan, 1989, as reflected in our cage controls, above which, additional structure is less important in facilitating increases in
syngnathids. Our results suggest that the additional structure presented in exclusion cages, as compared to partial cages, does not further attract syngnathids. Therefore, the
provision of structure per se, not necessarily the amount, may be more important in determining fish abundances, and the differences in numbers of fish between our cage
controls and exclusion cages are more likely to reflect predation than simply attraction of fish.
170 J
.S. Hindell et al. J. Exp. Mar. Biol. Ecol. 255 2000 153 –174
Further data are required which a evaluate how the predation pressure imposed by confined fish differs from that imposed by uncaged fish, and b establish the importance
of varying levels of structure in determining fish abundances. As Virnstein 1980 commented, a single line of evidence by itself is weak and, therefore, a pluralistic
approach to caging experiments, i.e., exclusion and enclosure cages in concert with other measures of cage effects, potentially provides researchers with a rigorous evaluation of
the importance of predation versus cage effects. On the basis of the syngnathid data and the results from the enclosure exclusion experiments, the patterns in fish abundances
between cage treatments can be interpreted as representing discernible contributions by both cage and predation effects.
Biomass of vegetation is positively associated with the abundance and diversity of animals Pollard, 1984; Bell and Westoby, 1986a,b; Edgar, 1990; Edgar and Robertson,
1992; Connolly, 1994. In marine environments, fish faunas associated with seagrass are often more diverse and abundant than those in nearby unvegetated soft sediments
Pollard, 1984. While food resources, level of physical structure, number of mi- crohabitats, reduction of environmental disturbance and stabilisation of sediments may
help to explain these patterns Lewis, 1984, the mediation of predation by aspects of the seagrass may also be important in determining fish abundance Orth et al., 1984. If
predation by fish is important in structuring assemblages of small fish, and structural complexity mediates this predation, then we can expect predation pressure to be greatest
in areas where structural complexity is low, such as unvegetated sand. When predators are excluded from habitats which differ in structural complexity, the effect of excluding
predatory fish should be less in seagrass, whose structural complexity interferes with foraging by fish. And if predation produced the pattern of greater fish density in seagrass
than unvegetated sand habitats, then one would predict a greater effect of predators and a larger relative change in prey abundances in unvegetated sand than seagrass as shown
by Summerson and Peterson, 1984. Our results suggest that patterns are at least partially explained by predation. Small fish under pressure from fish predation no cage
are more abundant in seagrass than unvegetated sand. When predators are excluded, the relative increase in small fish is greater over unvegetated sand than seagrass, suggesting
that the structural complexity generated by aspects of the seagrass may be mediating predation. However, regardless of habitat, the numbers of fish varied between cage
treatments in qualitatively similar ways. These results suggest therefore, that while predation influences abundances of fish in both seagrass and unvegetated sand habitats, it
is relatively more important in habitats without any form of refuge. Therefore, we consider that a substantial portion of the variability in fish abundance between seagrass
and unvegetated sand may be related to differential predation pressure between these two habitats.
If the only role of habitat complexity is to mediate predation, then we would expect the numbers of fish associated with habitats of variable structural complexity to be
similar when released from predation. But our results showed that more fish occurred in areas of unvegetated sand than seagrass from which predators were excluded. Therefore,
fish may prefer alternative, unvegetated sand habitats, but their distributions are restricted to structurally complex seagrass habitats which, in addition to the processes
J .S. Hindell et al. J. Exp. Mar. Biol. Ecol. 255 2000 153 –174
171
suggested by Lewis 1984, provide a refuge from predation. Bologna and Heck 1999 found that scallops experience highest predation pressure in the areas favourable to
growth, and fish may alter their foraging patterns amongst structurally variable habitats in the presence of predators Gotceitas and Brown, 1993. Whether our results were due
to the selection of habitats which either offer refuge or have low numbers of predators, or whether they were the result of direct mortality, i.e., being eaten, is not known.
Theoretically, either alternative is possible — Levin et al. 1997 showed that predatory fish can directly alter the population structure of fish by consuming small individuals,
while Jordan et al. 1996 demonstrated that behaviourally mediated predator avoidance modifies the habitat use in pinfish. Dietary analysis of caged Arripis truttacea and
extensive dietary data on predatory fish at Grand Scenic Hindell et al., 2000 demonstrate the potential for predation, but further research is required to separate the
importance of direct predation versus anti-predator behaviour.
5. Conclusion
