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The effect of habitat complexity on predation efficiency of perch Perca fluviatilis L. and ruffe Gymnocephalus cernuus (L.)
J. E.x7~.Mar. Biol. Ecol., 157 (1992) 55-67 (.c-) 1992 Elsevier Science Publishers BV. All rights reserved 0022-0981/92/$05.00
55
JEMBE 01737
The effect of habitat complexity on predation efficiency of perch Perca fluviatilis L. and ruffe Gymnocephalus cernuus (L.) Johanna Mattila Department of Biology and Husii Biological Station. ,~bo Akademi University,/tbo, Finland (Received 9 July 1991; revision received 28 November 1991; accepted 29 November 1991)
Abstract: Aquarium experiments were conducted to test the hypothesis that a slight increase in habitat complexity significantly increases the survival of the amphipods Corophium volutator Pallas and the isopod Asellus aquaticus (L.) when preyed upon by perch Percafluviatilis L. and ruffe Gymnocephalus cernuus (L.), respectively. Artificial reed, stones, and natural plants were tested in different combinations. A slight increase in habitat complexity (e.g., small amount of stones) did not increase Corophium survival. However, artificial reeds in different forms, and natural plants, did increase the survival ofboth Asellus and Corophium. Survival increased with increasing habitat complexity. At low complexity levels the survival of the prey seemed to be higher when the elements used to provide complexity were in bigger integrated patches. Tall, shading elements like reeds or aquatic plants gave the best shelter against fish that feed visually. Key words: Crustacean prey; Gymnocephah~s cermms; Habitat complexity; Percafluviatilis; Predation efficiency
INTRODUCTION
The littoral zone is an importont feeding ground for many fish species (Pihl, 1982, 1985; Hansson, 1984; Biomqvist, 1986). It is often characterized by physical complexity and spatial patchiness (Crowde~r & Cooper, 1982; Blomqvist & Bonsdorff, 1986; Nellbring, 1988; Savino & Stein, 1i989a),which affect both the predators, their prey and the interaction between them in many ways. Physically complex habitats, e.g., with dense patchy vegetation, are usually associated with higher abundances of macroinvertebrates (Orth et al., 1984; Rabe & Gibson, 1984; Gregg & Rose, 1985) and fish predators (Summerson & Peterson, 1984; Hansson, 1985; Heck et al., 1989) than adjacent habitats lacking vegetation. Many experimental studies in the field have shown that predation efficiency is lower in vegetated habitats than in unvegetated ones (Crowder & Cooper. 1982; Summerson & Peterson, 1984; Tonn et al., 1989). Aquarium experinaents have in several cases confirmed that predation efficiency declines as habitat complexity increases, provided that a certain threshold level of complexity is reached Correspondence address: J. Mattila, Department of Biology, Abo Akademi University, 20500 /~bo, F~.mand.
56
J. MATTILA
(Heck & Thoman, 1981; Savino & Stein, 1982; Gotceitas, 1990). However, Nelson & Bonsdorff (1990) found a linear relationship without any thresholds between habitat complexity and predation efficiency. Most experiments concerning habitat complexity have studied the effect of different vegetation types on predation efficiency of fishes and crustaceans (see Gotceitas & Colgan, 1989, for review). Effects of other types of complc:dty (e.g., sediment structure, stones, decaying plant material) have been only little studied (but see Ware, 1972; Stein & Magnuson, 1976; Coull & Wells, 1983), and none of these studies has compared the effects of vegetation and other types of habitat complexity on fish predation of benthic macroinvertebrates. Many littoral soft-bottom habitats that are sparsely vegetated or totally lack vegetation may have, however, a more or less complex bottom caused by the presence of stones, gravel and/or decaying plant material. Some field experiments in the northern Baltic Sea have shown that the effects of bottom-feeding fshes remain small in these habitats, while the predators have dramatic effects on benthic invertebrates in bare-sand aquaria (Mattila & Bonsdorff, 1989). The higher level of complexity in the field compared with the simplified aquarium environment is an obvious difference between these experiments and possibly explains some of the contradictory results. The apriori hypothesis for this study was thus that a slight increase in habitat complexity will affect predation efficiency. Two percid fish predators, ruffe Gymnocephalus cernuus (L.) and perch Percaflul,iatilis L., were used in the study and tested against the limnic isopod Aseilus aquaticus L. (vs. ruffe) and the estuarine amphipod Corophium volutator Pallas (vs. perch). All species coexist abundantly in the shallow bay areas in north-western Ai,'md, south-western Finland (Blomqvist, 1986; Osterman & Bonsdorff, 1985; Mattila & Bonsdorff, 1988), and the prey species are natural food for the percids (Rask & Hiisivuori, 1985; Biomqvist, 1986: Mattik~ & Bonsdorff, 1988). Habitat complexity in the aquaria was varied with different kinds of artificial reed and stones and with living Potamogeton peJJbliatus L. plants. MATERIALS AND METHODS GENERAL EXPERIMENTAL CONDITIONS
Six different experiments were conducted to test the a priori hypothesis. In Experiments I-I11 ruffe G. cernuus was used as a predator on the isopod A. aquaticus, and in Experiments IV-VI perch P. lluviatilis was used as a predator on the amphipod C. rohaamr. All experimental animals were collected a few days prior to experiments in Gloet Bay or HusO Bay near HusO Biological Station on north-western ,~land, south-western Finland. The total length of ruffe varied between 7.4 and 11.0 cm, and the length of perch varied between 4.4 and 6.7 cm. The prey sizes were 2.5-12.5 mm for ,4sellus and 2.5-8 mm for Corophium. All prey lengths were measured from telson to rostrum. The fish were starved for 24 h prior to the experiments to ensure that they fed actively.
HABITAT COMPLEXITY AND FISH PREDATION
57
All experiments were run in small overflow aquaria (vol. 11 dm 3, area 0.061 m 2) with a l-cm layer of azoic, sieved (0.5 mm) sediment on the bottom. In the experiments with ruffe the sediment was a mixture of sand and mud and in the experiments with perch it was pure sand. The salinity of the water was 4.59-5.64%0, the pH 7.91-8.97 and the 02,0/o saturation 75-101. One predator per aquarium was used (16.4 ind. m-E), except in Experiment VI where two perch per aquarium were used (32.8 ind. m - 2). The higher predator density used in the experiment was to compensate for the lower predator activity caused by the lower water temperature (10.1-10.4 °C in Experiment VI, 14.7-21.4 °C in the other experiments; Bergman, 1988). In Experiments I - I l l 35 prey individuals (Asellus)were placed in each aquarium, which equals 574 i n d . m - 2 . In Experiments IV-VI 70 prey individuals (Corophimn)per aquarium were used (1148 i n d . m - 2). These prey densities are comparable to natural densities in shallow bay areas on north-western ,~land (Osterman & Bonsdorff, 1985; Mattila & Bonsdorff, 1989; pers. obs.). Prey animals were placed in the aquaria several hours before the predators were introduced. The duration of the experiments with ruffe was 12 h (1900-0700) and in experiments with perch 24 h, except in Experiment V where the duration was 6 days. A longer duration was chosen to test the importance of duration and to obtain results that were comparable with earlier aquarium experiments of equal duration (Mattila & Bonsdorff, 1989). The photoperiod in the aquarium followed the natural day length. Both predators are known to be most active at dawn and dusk (Alabaster & Stott, 1978) so these daily periods were included in the experimental periods. A shorter duration was chosen for ruffc because it was known fi'om earlier experiments to be a more effective predator than perch (Mattila & Bonsdorff, 1989). Habitat complexity was varied with different objects. Short round (length 4 cm, diameter 0.5 cm) plastic straws filled with sand were used to simulate growing and decaying reed ("short reeds") and tall wooden (length 30 cm, diameter 0.5 cm) dowels to simulate growing reed ("long reeds"). Cylindrical rubber corks of three different sizes (vols. 8, 16 and 63 cnl 3) w e r e used to simulate "stones". Living plants of Potamogeton peJfidiatus (length 15-20 cm) were also used to increase the complexity of the habitat in the aquaria. The densities of all the elements use;! to increase complexity were chosen on the basis of field evidence from the habitats where the experimental animals were collected. At the termination of the experiments the predators were caught and their guts examined to ensure that they had been feeding. After removal of the predators the entire contents of the aquaria were flushed on to a 0.5-mm screen and the surviving prey organisms were counted. In Experiment 1 their total length was also measured to determine possible differences in length-frequency distribution between the experimental and control treatments.
58
J. MATTILA
SPECIFIC EXPERIMENTAL DESIGN
Experiment 1 The basic sand bottom habitat (Treatment la, Table I) was varied with different combinations of short reed in three treatments (Ib-d). In one treatment stones (Ic) were also used to increase the complexity of the habitat. All treatments had a corresponding control treatment without ruffe.
Experhnent I1 The design of Experiment II was based on the results from Experiment I. In this experiment the lowest increased complexity level from Experiment I (lb = lla) was compared with a treatment with a single short reed stack (lib) in the centre of the aquarium (Table I).
Expelqment III This experiment was designed to test the conditions of spring, early summer and late summer or autumn. The spring situation, when mainly decaying reed lie on the bottom, was simulated with a stack of short reeds (Ilia), the early summer situation was simulated with a patch of short reeds standing up from the sediment (lllb), and the autumn situation was simulated with a patch of tall reeds standing up from the sediment above the water surface (lllc, Table I). The reed patches and stacks were placed in the centre o1" the aquaria.
EaT~er#nents IV and V These experiments tested the effects of different stone formations and the effect of experimental duration (Experiment IV vs. V) on the survival of Corophimn with perch (Table 1).
Exper#nent VI !n this experiment the treatment with a bare sand bottom (Via) was compared with treatments with stones (Vlb) or P. perhdiatus plants (Vlc), both with a density of 250. m - 2 (Table I). The Potamogeton plants were collected I day before the experiment and they were carefully rinsed and scraped in order to release any invertebrates attached to them. The plants were cut to a length of 15-20 cm so that they reached up to the water surface and they were pushed into the sediment. Both the stones and the plants were randomly placed in the aquaria.
I
-
-
.
.
-
.
. -
.
.
-
. .
40
0
.
0
.
0
40
-
40
40
-
40
-
40
40
-
0
Experiment l a Experiment I b Experiment I c Experiment I d Experiment l l a Experiment l i b Experiment I l i a Experiment l l l b Experiment I I l c Experiment ! V a Experiment I V b Experiment I V c Experiment V a Experiment V b Experiment V i a Experiment V I b Experiment V I c .
.
.
.
.
No. of tall reeds/aquarium
40
No. of short reeds/aquarium
Experiment treatment
.
.
.
.
.
0
0 16
-
-
-
-
-
-
-
-
-
No. of Potamogeton plants/aquarium
~
O
~
~
Random
-
-
10 cm patch
10 cm patch
10 c m s t a c k
10 cm stack
random
5 cm stacks
Vertical,
4 x ~
Random
Random
-
Arrangement
0
8
0
7
7
0
0
0
16
-
-
-
-
-
9
0
0
No. of stones/ aquarium
-
Random
-
Random
-
IEI 7 c m s t a c k
Random
-
-
-
-
-
-
-
Random
-
-
Arrangement
16.8
16.8
0
9.4
0
6.3
7.1
0
12.3
12.3
12.3
I2.3
12.5
12.3
13.5
12.5
0
Bottom cover (~o)
Description of treatments using short reeds (plastic straws), tall reeds (wooden dowels), Potamogeton plants aiid stones (rubber corks). Bottom cover (~o) in each treatment is also given ( ~ , diameter).
TABLE
~D
O Z
N
m >
N
"rl
-8 .< > Z
t" m ,...m
O
> ...]
>
60
J. MATTILA
STATISTICAL ANALYSIS
The results were analysed with a t test (Experiments II and V) or one-way ANOVA (Experiments I, III, IV and VI) depending on the experimental design (Sokal & Rohlf, 1981). Numbers of surviving prey are given as a percentage of the initial number and were arcsine-transformed before statistical analysis. The transformed data were subjected to the Fm:.,xtest before analysis in order to ensure its homogeneity. Fisher's PLSD test was applied as a test of differences between individual treatment means (StatView for Macintosh). Length-frequency distributions of the prey organisms in Experiment I were compared using the nonparametric Kolmogorov-Smirnov test (Sokal & Rohlf, 1981). RESULTS AND DISCUSSION
In Experiment I the survival of Asellus in the control and the ruffe treatments was analysed in two separate sets, one for the control treatments and one for the ruffe treatments. Survival of Asellus in the control aquaria without ruffe was good, >i 90~o of the prey survived in each treatment and there were no significant differences among the treatments (F~3.2o~= 1.201, NS). Results from these control treatments and experiences from earlier, comparable short-term experiments (Mattila & Bonsdorff, 1989) ensure a good and even survival of Corophium and Asellus in aquarium conditions, and therefore no control treatments without fish were applied in the following experiments. Survival of Aselhts in the ruffe aquaria was best in the treatment with small stacks (Id, .-i: = 63.8"/o)and lowest in the treatment with bare sand (la, :~ = 21.4%). The ANOVA showed significant differences among the treatments (F{3.zm = 6.123, p < 0.001). The clearest difference was between the bare sediment and the reed stacks treatments (p < 0.001). Significant differences were also found between the bare sediment and the t'andom reed pieces + stones (lc) treatments (p < 0.01), and the bare sediment versus the random reed (lb) treatmer~ts (p < 0.05). All increased complexity treatments thus provided improved refuges for Asellus from ruffe predation. The complexity levels could not, however, be separated from each other, because no significant differences were found among them (Fig. l a). The length frequencies of the surviving Asellus in the ruffe and the control aquaria both had a mode of 6.5 mm. The mean value in the ruffe aquaria (6.2 mm) was, however, lower than in the control aquaria (6.9 mm). The largest individuals (> 10.5 mm) were also missing in the ruffe aquaria. The nonparametric Kolmogorov-Smirnovtest revealed a significant difference ( K - S zz=0.346, P < 0.001) between the length frequencies showing that the ruffes actively chose bigger individuals fi'om the prey population. This agrees with results from other experiments showing that visual fish predation mainly affects the large size classes of benthic invertebrates, probably because they are easiest to locate (Crowder & Cooper, 1982; Flecker & Allan, 1984; Mittelbach, 1988). In Experiment 11 the single stack treatment was expected to give significantly better
80 60
a)
61
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,%%
40 )•1)
20
;%,
la sediment only
Ib short reeds, random
Id short reeds. stacks
|C
short
reeds° random +
80! J J
stones
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eeee•e
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II a short reeds, random
II b short reeds, stack ON~
I
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~ I
I00
80
'
l Wm !
c)
ON I
I
III a short reeds, stack
III b short reeds, patch
60
40 20
III c tall reeds, patch
Fig. I. Average percent survival of Asellus (+_ 1 SE). Stars on lines connecting treatment pairs indicate significant differences between these treatments (*p < 0.05, **p < 0.01, ***p < 0.001); (a) treatments in Experiment I (n = 6), (b) treatments in Experiment II (11 = 6) and (c) treatments in Experiment III (n = 5). Details of treatments are given in Table I.
62
J. M ATTI LA
shelter for Asellus from ruffe predation than the low complexity treatments in Experiment I. This hypothesis also proved acceptable as the survival of Ase2lus in the stack treatment (lib) was significantly higher (mean value 71.9%) than in the randomly placed reed treatment (lla, one-tailed t test, t = - 3.147, p < 0.01; Fig. lb). The mean survival in the randomly placed reed treatment was 43.8 + 8.1~o (7 + SE), which is comparable with the survival of Asellus in the corresponding treatment (Ib) in Experiment I (45.2 + 4.7 ~o, Fig. 1a). A single patch of high complexity in a noncomplex environment seems to be more advantageous for the prey than overall low-level complexity in the environment. The results also suggest that the patch size is critical for prey survival, at least in low complexity habitats because one larger patch gave better shelter than several smaller ones (Fig. la,b). Larger patches may be easier for the prey to find than small ones. They may also give shelter for a larger number of prey individuals without the problem of competition for space. The lowest survival of Asellus (26.9 + 11.3 °/o, ~ + SE) in Experiment III was measured in the ~'early summer" treatment (Ilia) and the highest in the "autumn" treatment (lllc, 94.9 + 1.97o, Fig. lc). The survival of Asellus in the "spring" treatment (lllb) with decaying reed was placed between these two. The ANOVA showed significant differences among these treatments (Ft2,~2~ = 22.896, p < 0.001). Fisher's PLSD test gave significant differences among all treatment pairs compared (Fig. 1c). These results show that increasing height of the vegetation significantly increases the survival of Asellus. The benthic prey gain no direct advantage from the increasing height of vegctation~ but the predators probably more often lose visual contact with the prey (Cooper & Crowder, 1979; Savino & Stein, 1982; Nelson & Bonsdorff, 1990). Tile search time thus increases and predation efficiency decreases (Stoner, 1982; Johns & Mann, 1987). Also, the structure of the complex patch is important. A patch of short reed did not offer as effective a refuge from ruffe predation as a similar sized stack of reed, possibly because the short reed does not significantly deter the predator's visual search. Similar differences in refuge effectiveness have been found for different blade and growth forms of aquatic plants (Coen et al., 1981; Stoner, 1982; Dionne & Folt, 1991). The feeding efficiency of perch in Experiment IV was considerably lower than the efficiency of ruffe in the previous experiments, and consequently the survival of Corophium was quite high (on average > 76~o) in all perch treatments (Fig. 2a). No statistical differences could be found between any pairs of treatments (F~2.~2~-- 0.395, NS). In Experiment V the duration was 6 days, which was clearly longer than in Experiment IV, and consequently the survival of Corophium in both treatments was also lower than in Experiment IV. The average survival varied between 37 and 48% (Fig. 2b), but no significant differences could be found between the treatment (t value = 0.876, NS). The survival of Corophium in the bare-sand treatment (Va) in Experiment V was comparable with the survival of Corophium in an earlier aquarium experiment (survival ,~ 20% in 14-day experiment) by Mattila & Bonsdorff (1989). In Experiment IV the survival of Corophium in the different fish treatments was clearly highest in the treatment with Potamogeton plants (Vlc, 50.2 + 5.9%, ~ + SE; Fig. 2c).
H A B I T A T C O M PL E X I T Y A N D FISH P R E D A T I O N I00
63
a)
I
80
60.
40 20
IV a sand only
E
IV b stones, random
80
IV c stones, stack
b)
,i,i t-x O t. O
60
t~
40 e.m
>. >
.m
L.
20
Vb
Va sand
stones,
only
random
8O
c)
uw i i
60
40
i I
NN I
20
VI a sand only
Vl b stones, random
Vl c plants, random
Fig. 2. Average percent survival of C~orophium( _ 1 sl~). Stars on lines connecting treatment pairs indicate significant differences between the~e treatments (*p < 0.05, **p < 0.01); (a) treatments in Experiment IV (n = 7), (b) treatments in Experiment V (n = 7) and (c) treatments in Experiment VI (n = 5). Details of treatment are given in Table I.
64
J. MATTILA
The average survival in the other treatments was 29.6 (bare sand, Via) and 34.0% (stones, VIb). The ANOVA showed a significant difference among the treatments (F~2,12~ = 7.571, p < 0.01). Fisher's PLSD test showed statistically significant differences between the bare sand and the Potamogeton treatments (p < 0.01), and between the stone and the Potamogetontreatments (p < 0.05). Although the stone densities were more than doubled and the coverage of the bottom increased from 6 to 17 ~o compared with Experiments IV and V, the stone habitat still remained insufficient to increase the survival of Corophium. Consequently, these results lead to partial rejection of the a priori hypothesis. According to Pierce (1988) and Savino & Stein (1989a), a high level of complexity does not automatically affect the predation efficiency; the prey must be able, for example, through its behaviour to utilize the complexity and the shelter it offers. In the present study the crustacean species used could not effectively utilize stones or reed pieces spread on the bottom. Coull & Wells (1983) found similar results in their experinaents, where neither stones nor gravel could affect the predation efficiency of blennies feeding on meiofauna. Ware (1972) found that wood litter covering the bottom (coverage 6 or 15 ~/o) increased the survival of amphipods against rainbow trout predation. The increments of habitat complexity resulting in lowered predation pressure in his study were comparable with the increments in this study, which, however, did not significantly affect the survival of the prey. In the present study Asellus was more favoured by small increments in habitat complexity than Corophium, probably due to the different behaviour of these species. Asellus is most often attached to the sediment surface and the vegetation and it rarely swims. Corophium, on the contrary, is more mobile and periodically swims both in nature (Holmstr0m & Morgan, 1983; Hughes, 1988) and in the aquarium environment (Hughes, 1988; Mattila & Bonsdorff, 1989). Corophium is a burrowing infaunal species, which is sheltered by increased sediment depth (Mattila & Bonsdorff, 1989). In the present experiments the sediment depth was kept at 1 cm, which may have partly provoked the swimming and crawling behaviour of Corophium. Sedentary prey are often more favoured by increased habitat complexity than motile prey (Stein & Magnuson, 1976; Savino & Stein, 1989b) or prey which may become more sedentary when complexity increases. The behaviour and mode of hunting of fish predators often changes when habitat complexity increases (Crowder & Cooper, 1982; Savino & Stein, 1982, 1989b; Wahl & Stein, 1988). The predation efficiency may decrease, because those elements providing complexity, e.g., vegetation, totally prevent or impair normal search behaviour (Savino & Stein, 1989b). Some fish predators may, however, easily adapt their search behaviour to variable complexity (Savino & Stein, 1982; Crowder & Binkowski, 1983). Winfield (1986) and Diehl (1988) have shown that the predation efficiency of perch remains relatively high even in habitats with high complexity, which might partly explain the minor effects of low level complexity on the predation efficiency of perch in the present study. Recent work, including the present study, suggests that the effects of habitat com-
HA,r'ITAT COMPLEXITY AND FISH PREDATION
65
plexity on predator-prey interactions are variable depending on the combination of a predator and a prey (Winfield, 1986; Gotceitas & Colgan, 1989; Dionne & Folt, 1991). Marinelli & Coull (1987) found that short straws standing up from the sediment (similar to those used in Experiment III) actually facilitate spot (Leiostomus) predation on meiofauna, while the results from the present study show a decreased predation effÉciency of ruffe on Asellus. Minello & Zimmerman (1983) also found that the predation efficiency of visual fish predators with different qualities was affected by Spartina stems in very variable ways. In conclusion, the present results show that the survival of brackish water invertebrate prey is positively affected by increasing habitat complexity, when exposed to predation by primarily visually feeding percids. Similar effects of habitat complexity on the survival of benthic invertebrate prey with visual predators have earlier been shown in several freshwater and marine studies (Gotceitas & Colgan, 1989). Tall plants give the best shelter for brackish water crustaceans against visual fish predators. Furthermore, patches, which are big enough and of high complexity in a noncomplex environment, affect predation efficiency more than a low overall complexity. ACKNOWLEDGEM ENTS
This study is a part of the Academy of Finland project (No. 108 1002) "Biotic interactions on shallow soft bottoms in the archipelago- experiments in the field and the laboratory". Financial support was also achieved from Jubileumsfonden for hi~gskoleviisendets 350-fo'. Hus6 Biological Station provided me with excellent laboratory facilities, which is gratefully acknowledged. I also thank E. Bonsdorff who provided advice during the experimental period and kindly commented earlier drafts of the manuscript. Two anonymous reviewers of the manuscript also offered suggestions and comments that substantially improved the paper. REFERENCES Alabaster, J.S. & B. Stott, 1978. Swimming activity of perch, Perca fluviatilis L. J. Fish Biol., Vol. 12, pp. 578-591. Bergman, E., 1988. Foraging abilities and niche breadths of two percids, Percafluviatilis and Gymnocephalus cernua, under different environme~:tal conditions. J. Anita. Ecol., Vol. 57, pp. 443-453. Blomqvist, E., 1986. A shallow water t3sh community structured by land uplift and dredging. PubL Water hist. Finl., Vol. 68, pp. 112--116. Blomqvist, E. & E. Bonsdorff 1986. Spatial and temporal variations of benthic macrofauna in a sandbottom area on Aland, northern Baltic Sea. Ophelia, Vol. 4, Suppl., pp. 27-36. Coen, L.D., K.L. Heck & L.G. Abele, 1981. Experiments on competition and predation among shrimps of seagrass meadows. Ecology, Vol. 62, pp. 1484-14q3. Cooper, W.E. & L.B. Crowder, 1979. Patterns of predation in simple and complex environments. In, Predator-prey systems in fisheries management, edited by R.H. Stroud & H. Clepper, Sport Fishing Institute, Washington, DC, pp. 257-267. -. .,~ Cou!l, B.C. & J. B.J. Wells, 1983. Refuges from fish preC:~,on: experiments with phytal meiofauna from the New Zealand rocky intertidal. Ecology VoL 6a,~pp. 1599-1609.
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Crowder, I,.B. & F.P. Binkowski, 1983. Foraging behaviors and the interaction of alewife, Alosa psemh~harengus, and bloater, Coregonus hoyi. Environ. Bh~l. Fish., Vol. 8, pp. 105-113. Crowder, L.B. & W.E. Cooper, 1982. Habitat structuro! complexity and the iateraction between bluegills and their prey. Ecology, Vol. 63, pp. 1802-1813. Diehl, S., 1988. Foraging efficiency of three freshwater fishes: effects of structural complexity and light. Oikos, Vol. 53, pp. 207-214. Dionne, M. & C.L. Folt, 1991. An experimental analysi~ of macrophyte growth forms as fish foraging habitat. Can. J. Fish. Aquat. Sci., Vol. 48, pp. 123-131. Flecker, A. S. & J. D. Allan, 1984. The importance of predation, substrate and spatial refugia in determining lotic insect distributions. Oecologia (Berlin), Vol. 64, pp. 306-313. Gotceitas, V., 1990. Variation in plant stem density and its effects on foraging success of juvenile bluegill sunfish. Environ. Biol. Fish. Vol. 27, pp. 63-70. Gotceitas, V. & P. Colgan, 1989. Predator foraging success and habitat complexity: quantitative test of the threshold hypothesis. Oecologia (Berlin), Vol. 80, pp. 158-166. Gregg, W.W. & F.L. Rose, 1985. Influences of aquatic macrophytes on invertebrate community structure, guild structure, and microdistribution in streams. Hydrobiologia, Vol, 128, pp. 45-56. Hansson, S., 1984. Competition as a factor regulating the geographical distribution offish species in a Baltic archipelago: a neutral model analysis. J. Biogeogr., Vol. 11, pp. 367-381. Hansson, S., 1985. Effects of eutrophication on fish communities with special reference to the Baltic Sea - a literature review. Rep. hist. Freshwater Res. Drottninghohn, Vol. 62, pp. 36-56. Heck, K. L., Jr., K.W. Able, M.P. Fahay & C.T. Roman, 1989. Fishes and decapod crustaceans of Cape Cod eelgrass meadows: species composition, seasonal abundance patterns and comparison with unvegetated substrates. Estuaries, Vol. 12, pp. 59-65. Heck, K. L., Jr. & T.A. Thoman, 1981. Experiments on predator-prey interactions in vegetated aquatic habitats. J. Exp. Mar. Biol. EcoL, Vol. 53, pp. 125-134. Holmstr6m, W. F. & E. Morgan, 1983. Variation in naturally occurring rhythm of the estuarine amphipod, Corophium vohaator (Pallas). J. Mar. Biol. Assoc. U.K., Vol. 63, pp. 833-850. Hughes, R.G., 1988. Dispersal by benthic invertebrates: the in situ swimming behaviour of the amphipod Corophium vohaator. J. Mar. Biol. Assoc. U.K., Vol. 68, pp. 565-579. Johns, P. M. & K. H. Mann, 1987. An experimental investigation of juvenile lobster habitat preference and mortality among habitats ofvarying structural complexity. J. Exp. Mar. Biol. Ecol., Vol. 109, pp. 275-285. Marinelli, R. L. & B.C. Coull, 1987. Structural complexity and juvenile fish predation on meiobenthos: an experimental approach. J. E.x~. Mar. Biol. Ecol., Vol. 108, pp. 67-81. Mattila, J. & E. Bonsdorff, 1988. A quantitative estimation offish predation on shallow soft bottom benthos in SW Finland. Kiei. Meeresforsch., Vol. 6, Sonderh., pp 111-125. Mattila, J. & E. Bonsdorff, 1989. The impact offish predation on shallow soft bottoms in brackish waters (SW Finland); an experimental study. Neth. J. Sea Res., Vol. 23, pp. 69-81. Minello, T.J. & R.J Zimmerman, 1983. Fish predation on juvenile brown shrimp, Penaeus aztecus Ives: the effect of simulated Spartina structure on predation rates. J. Exp. Mar. Biol. Ecol., Vol. 72, pp. 211-231. Mittelbach, G.G., 1988. Competition among refuging sunfishes and effects of fish density on littoral zone invertebrates. Ecoh~gy, Vol. 69, pp. 614-623. Nellbring, S., 1988. Quantitative and qualitative studies of fish in shallow water, northern Baltic proper, Ph.D. dissertation, University of Stockholm, Sweden, 19 pp. Nelson, W.G. & E. Bonsdorff, 1990. Fish predation and habitat complexity: Are threshold levels real? J. E.W. Mar. Biol. Ecol., Vol. 141, pp. 183-194. Orth, R.J., K. L. Heck Jr. & J. van Montfrans, 1984, Faunal commanities in seagrass beds: a review of the influence of plant structure and prey characteristics on predator-prey relationships. Estuaries, Vol. 7, pp. 339-350. Pierce, C. L., 1988. Predator avoidance, microhabitat shift, and risk-sensitive foraging in larval dragonflies. Oecologia (Berlin), Vol. 77, pp. 81-90. Pihl, L., 1982. Food intake of young cod and flounder in a shallow bay on the Swedish west coast. Neth. J. Sea Res., Vol. 16, pp. 419-432. Pihl, L., 1985. Food selection and consumption of mobile epibenthic f~::~nain shallow marine areas. Mar. Ecol. Progr. Set., Vol. 22, pp. 169-179. Rabe, F.W. & F. Gibson, 1984. The effect of macrophyte removal on the distribution of selected invertebrates in a littoral environment. J. Freshwat. Biol., Vol. 2, pp. 359-37 i.
HABITAT COMPLEXITY AND FISH PREDATION
67
Rask, M. & C. Hiisivuori, 1985. The predation on Asellus aquaticus (L.) by perch, Percafluviatilis (L.) in a small forest lake. Hydrobiologia, Vol. 121, pp. 27-33. Savino, J.F. & R.A. Stein, 1982. Predator-prey interactions between largemouth bass and bluegills as influenced by simulated submerged vegetation. Trans. Am. Fish. Soc., Vol. 111, pp. 255-266. Savino, J. F. & R.A. Stein, 1989a. Behavior of fish predators and their prey: habitat choice between open water and dense vegetation. Environ. Biol. Fish., Vol. 24, pp. 287-293. Savino, J.F. & R.A. Stein, 1989b. Behavioral interactions between fish predators and their prey: effects of plant density. Anita. Behav., Vol. 37, pp. 311-321. Sokal, R. R. & F.J. Rohif, 1981. Biometry. W. H. Freeman & Co., San Francisco, California, second edition, 859 pp. Stein, R.A. & J.J. Magnuson, 1976. Behavioral response of crayfish to a fish predator. Ecology, Vol. 57, pp. 751-761. Stoner, A.W., 1982. The influence of benthic macrophytes on the foraging behavior of pinfish Lagodon rhomboides (Linnaeus). J. Exp. Mar. Biol. Ecol., Vol. 58, pp. 271-284. Summerson, H.C. & C.H. Peterson, 1984. Role of predation in organizing benthic communities of a temperate-zone seagrass bed. Mar. Ecol. Progr. Set., Vol. 15, pp. 251-263. Tonn, W.M., G.A. Paszkowski & I.J. Holopainen, 1989. Responses of crucian carp populations to differential predation pressure in a manipulated pond. Can. J. Zool., Vol. 67, pp. 2841-2849. Wahl, D.H. & R.A. Stein, 1988. Selective predation by three esocids: the role of prey behaviour and morphology. Trans. Am. Fish. Soc., Vol. 117, pp. 142-151. Ware, D.M., 1972. Predation by rainbow trout (Salmo gairdneri): the influence of hunger, prey density and prey size. J. Fish. Res. Board Can., Vol. 29, pp. 1193-1201. Winfield, I.J., 1986. The influence of simulated aquatic macrophytes on the zooplankton consumption rate of juvenile roach, Rutilus rutilus, rudd, Scardinius erythrophtabnus, and perch, Perca fluviatilis. J. Fish Biol., Vol. 29, pp. 37-48. Osterman, C.-S. & E. Bonsdorff, 1985. ,~rstidsvariationer i djursamh~illen p~t grunda mjukbottnar. Medd. HusiJ Biol. Stn., Vol. 25, pp. 16-42.
55
JEMBE 01737
The effect of habitat complexity on predation efficiency of perch Perca fluviatilis L. and ruffe Gymnocephalus cernuus (L.) Johanna Mattila Department of Biology and Husii Biological Station. ,~bo Akademi University,/tbo, Finland (Received 9 July 1991; revision received 28 November 1991; accepted 29 November 1991)
Abstract: Aquarium experiments were conducted to test the hypothesis that a slight increase in habitat complexity significantly increases the survival of the amphipods Corophium volutator Pallas and the isopod Asellus aquaticus (L.) when preyed upon by perch Percafluviatilis L. and ruffe Gymnocephalus cernuus (L.), respectively. Artificial reed, stones, and natural plants were tested in different combinations. A slight increase in habitat complexity (e.g., small amount of stones) did not increase Corophium survival. However, artificial reeds in different forms, and natural plants, did increase the survival ofboth Asellus and Corophium. Survival increased with increasing habitat complexity. At low complexity levels the survival of the prey seemed to be higher when the elements used to provide complexity were in bigger integrated patches. Tall, shading elements like reeds or aquatic plants gave the best shelter against fish that feed visually. Key words: Crustacean prey; Gymnocephah~s cermms; Habitat complexity; Percafluviatilis; Predation efficiency
INTRODUCTION
The littoral zone is an importont feeding ground for many fish species (Pihl, 1982, 1985; Hansson, 1984; Biomqvist, 1986). It is often characterized by physical complexity and spatial patchiness (Crowde~r & Cooper, 1982; Blomqvist & Bonsdorff, 1986; Nellbring, 1988; Savino & Stein, 1i989a),which affect both the predators, their prey and the interaction between them in many ways. Physically complex habitats, e.g., with dense patchy vegetation, are usually associated with higher abundances of macroinvertebrates (Orth et al., 1984; Rabe & Gibson, 1984; Gregg & Rose, 1985) and fish predators (Summerson & Peterson, 1984; Hansson, 1985; Heck et al., 1989) than adjacent habitats lacking vegetation. Many experimental studies in the field have shown that predation efficiency is lower in vegetated habitats than in unvegetated ones (Crowder & Cooper. 1982; Summerson & Peterson, 1984; Tonn et al., 1989). Aquarium experinaents have in several cases confirmed that predation efficiency declines as habitat complexity increases, provided that a certain threshold level of complexity is reached Correspondence address: J. Mattila, Department of Biology, Abo Akademi University, 20500 /~bo, F~.mand.
56
J. MATTILA
(Heck & Thoman, 1981; Savino & Stein, 1982; Gotceitas, 1990). However, Nelson & Bonsdorff (1990) found a linear relationship without any thresholds between habitat complexity and predation efficiency. Most experiments concerning habitat complexity have studied the effect of different vegetation types on predation efficiency of fishes and crustaceans (see Gotceitas & Colgan, 1989, for review). Effects of other types of complc:dty (e.g., sediment structure, stones, decaying plant material) have been only little studied (but see Ware, 1972; Stein & Magnuson, 1976; Coull & Wells, 1983), and none of these studies has compared the effects of vegetation and other types of habitat complexity on fish predation of benthic macroinvertebrates. Many littoral soft-bottom habitats that are sparsely vegetated or totally lack vegetation may have, however, a more or less complex bottom caused by the presence of stones, gravel and/or decaying plant material. Some field experiments in the northern Baltic Sea have shown that the effects of bottom-feeding fshes remain small in these habitats, while the predators have dramatic effects on benthic invertebrates in bare-sand aquaria (Mattila & Bonsdorff, 1989). The higher level of complexity in the field compared with the simplified aquarium environment is an obvious difference between these experiments and possibly explains some of the contradictory results. The apriori hypothesis for this study was thus that a slight increase in habitat complexity will affect predation efficiency. Two percid fish predators, ruffe Gymnocephalus cernuus (L.) and perch Percaflul,iatilis L., were used in the study and tested against the limnic isopod Aseilus aquaticus L. (vs. ruffe) and the estuarine amphipod Corophium volutator Pallas (vs. perch). All species coexist abundantly in the shallow bay areas in north-western Ai,'md, south-western Finland (Blomqvist, 1986; Osterman & Bonsdorff, 1985; Mattila & Bonsdorff, 1988), and the prey species are natural food for the percids (Rask & Hiisivuori, 1985; Biomqvist, 1986: Mattik~ & Bonsdorff, 1988). Habitat complexity in the aquaria was varied with different kinds of artificial reed and stones and with living Potamogeton peJJbliatus L. plants. MATERIALS AND METHODS GENERAL EXPERIMENTAL CONDITIONS
Six different experiments were conducted to test the a priori hypothesis. In Experiments I-I11 ruffe G. cernuus was used as a predator on the isopod A. aquaticus, and in Experiments IV-VI perch P. lluviatilis was used as a predator on the amphipod C. rohaamr. All experimental animals were collected a few days prior to experiments in Gloet Bay or HusO Bay near HusO Biological Station on north-western ,~land, south-western Finland. The total length of ruffe varied between 7.4 and 11.0 cm, and the length of perch varied between 4.4 and 6.7 cm. The prey sizes were 2.5-12.5 mm for ,4sellus and 2.5-8 mm for Corophium. All prey lengths were measured from telson to rostrum. The fish were starved for 24 h prior to the experiments to ensure that they fed actively.
HABITAT COMPLEXITY AND FISH PREDATION
57
All experiments were run in small overflow aquaria (vol. 11 dm 3, area 0.061 m 2) with a l-cm layer of azoic, sieved (0.5 mm) sediment on the bottom. In the experiments with ruffe the sediment was a mixture of sand and mud and in the experiments with perch it was pure sand. The salinity of the water was 4.59-5.64%0, the pH 7.91-8.97 and the 02,0/o saturation 75-101. One predator per aquarium was used (16.4 ind. m-E), except in Experiment VI where two perch per aquarium were used (32.8 ind. m - 2). The higher predator density used in the experiment was to compensate for the lower predator activity caused by the lower water temperature (10.1-10.4 °C in Experiment VI, 14.7-21.4 °C in the other experiments; Bergman, 1988). In Experiments I - I l l 35 prey individuals (Asellus)were placed in each aquarium, which equals 574 i n d . m - 2 . In Experiments IV-VI 70 prey individuals (Corophimn)per aquarium were used (1148 i n d . m - 2). These prey densities are comparable to natural densities in shallow bay areas on north-western ,~land (Osterman & Bonsdorff, 1985; Mattila & Bonsdorff, 1989; pers. obs.). Prey animals were placed in the aquaria several hours before the predators were introduced. The duration of the experiments with ruffe was 12 h (1900-0700) and in experiments with perch 24 h, except in Experiment V where the duration was 6 days. A longer duration was chosen to test the importance of duration and to obtain results that were comparable with earlier aquarium experiments of equal duration (Mattila & Bonsdorff, 1989). The photoperiod in the aquarium followed the natural day length. Both predators are known to be most active at dawn and dusk (Alabaster & Stott, 1978) so these daily periods were included in the experimental periods. A shorter duration was chosen for ruffc because it was known fi'om earlier experiments to be a more effective predator than perch (Mattila & Bonsdorff, 1989). Habitat complexity was varied with different objects. Short round (length 4 cm, diameter 0.5 cm) plastic straws filled with sand were used to simulate growing and decaying reed ("short reeds") and tall wooden (length 30 cm, diameter 0.5 cm) dowels to simulate growing reed ("long reeds"). Cylindrical rubber corks of three different sizes (vols. 8, 16 and 63 cnl 3) w e r e used to simulate "stones". Living plants of Potamogeton peJfidiatus (length 15-20 cm) were also used to increase the complexity of the habitat in the aquaria. The densities of all the elements use;! to increase complexity were chosen on the basis of field evidence from the habitats where the experimental animals were collected. At the termination of the experiments the predators were caught and their guts examined to ensure that they had been feeding. After removal of the predators the entire contents of the aquaria were flushed on to a 0.5-mm screen and the surviving prey organisms were counted. In Experiment 1 their total length was also measured to determine possible differences in length-frequency distribution between the experimental and control treatments.
58
J. MATTILA
SPECIFIC EXPERIMENTAL DESIGN
Experiment 1 The basic sand bottom habitat (Treatment la, Table I) was varied with different combinations of short reed in three treatments (Ib-d). In one treatment stones (Ic) were also used to increase the complexity of the habitat. All treatments had a corresponding control treatment without ruffe.
Experhnent I1 The design of Experiment II was based on the results from Experiment I. In this experiment the lowest increased complexity level from Experiment I (lb = lla) was compared with a treatment with a single short reed stack (lib) in the centre of the aquarium (Table I).
Expelqment III This experiment was designed to test the conditions of spring, early summer and late summer or autumn. The spring situation, when mainly decaying reed lie on the bottom, was simulated with a stack of short reeds (Ilia), the early summer situation was simulated with a patch of short reeds standing up from the sediment (lllb), and the autumn situation was simulated with a patch of tall reeds standing up from the sediment above the water surface (lllc, Table I). The reed patches and stacks were placed in the centre o1" the aquaria.
EaT~er#nents IV and V These experiments tested the effects of different stone formations and the effect of experimental duration (Experiment IV vs. V) on the survival of Corophimn with perch (Table 1).
Exper#nent VI !n this experiment the treatment with a bare sand bottom (Via) was compared with treatments with stones (Vlb) or P. perhdiatus plants (Vlc), both with a density of 250. m - 2 (Table I). The Potamogeton plants were collected I day before the experiment and they were carefully rinsed and scraped in order to release any invertebrates attached to them. The plants were cut to a length of 15-20 cm so that they reached up to the water surface and they were pushed into the sediment. Both the stones and the plants were randomly placed in the aquaria.
I
-
-
.
.
-
.
. -
.
.
-
. .
40
0
.
0
.
0
40
-
40
40
-
40
-
40
40
-
0
Experiment l a Experiment I b Experiment I c Experiment I d Experiment l l a Experiment l i b Experiment I l i a Experiment l l l b Experiment I I l c Experiment ! V a Experiment I V b Experiment I V c Experiment V a Experiment V b Experiment V i a Experiment V I b Experiment V I c .
.
.
.
.
No. of tall reeds/aquarium
40
No. of short reeds/aquarium
Experiment treatment
.
.
.
.
.
0
0 16
-
-
-
-
-
-
-
-
-
No. of Potamogeton plants/aquarium
~
O
~
~
Random
-
-
10 cm patch
10 cm patch
10 c m s t a c k
10 cm stack
random
5 cm stacks
Vertical,
4 x ~
Random
Random
-
Arrangement
0
8
0
7
7
0
0
0
16
-
-
-
-
-
9
0
0
No. of stones/ aquarium
-
Random
-
Random
-
IEI 7 c m s t a c k
Random
-
-
-
-
-
-
-
Random
-
-
Arrangement
16.8
16.8
0
9.4
0
6.3
7.1
0
12.3
12.3
12.3
I2.3
12.5
12.3
13.5
12.5
0
Bottom cover (~o)
Description of treatments using short reeds (plastic straws), tall reeds (wooden dowels), Potamogeton plants aiid stones (rubber corks). Bottom cover (~o) in each treatment is also given ( ~ , diameter).
TABLE
~D
O Z
N
m >
N
"rl
-8 .< > Z
t" m ,...m
O
> ...]
>
60
J. MATTILA
STATISTICAL ANALYSIS
The results were analysed with a t test (Experiments II and V) or one-way ANOVA (Experiments I, III, IV and VI) depending on the experimental design (Sokal & Rohlf, 1981). Numbers of surviving prey are given as a percentage of the initial number and were arcsine-transformed before statistical analysis. The transformed data were subjected to the Fm:.,xtest before analysis in order to ensure its homogeneity. Fisher's PLSD test was applied as a test of differences between individual treatment means (StatView for Macintosh). Length-frequency distributions of the prey organisms in Experiment I were compared using the nonparametric Kolmogorov-Smirnov test (Sokal & Rohlf, 1981). RESULTS AND DISCUSSION
In Experiment I the survival of Asellus in the control and the ruffe treatments was analysed in two separate sets, one for the control treatments and one for the ruffe treatments. Survival of Asellus in the control aquaria without ruffe was good, >i 90~o of the prey survived in each treatment and there were no significant differences among the treatments (F~3.2o~= 1.201, NS). Results from these control treatments and experiences from earlier, comparable short-term experiments (Mattila & Bonsdorff, 1989) ensure a good and even survival of Corophium and Asellus in aquarium conditions, and therefore no control treatments without fish were applied in the following experiments. Survival of Aselhts in the ruffe aquaria was best in the treatment with small stacks (Id, .-i: = 63.8"/o)and lowest in the treatment with bare sand (la, :~ = 21.4%). The ANOVA showed significant differences among the treatments (F{3.zm = 6.123, p < 0.001). The clearest difference was between the bare sediment and the reed stacks treatments (p < 0.001). Significant differences were also found between the bare sediment and the t'andom reed pieces + stones (lc) treatments (p < 0.01), and the bare sediment versus the random reed (lb) treatmer~ts (p < 0.05). All increased complexity treatments thus provided improved refuges for Asellus from ruffe predation. The complexity levels could not, however, be separated from each other, because no significant differences were found among them (Fig. l a). The length frequencies of the surviving Asellus in the ruffe and the control aquaria both had a mode of 6.5 mm. The mean value in the ruffe aquaria (6.2 mm) was, however, lower than in the control aquaria (6.9 mm). The largest individuals (> 10.5 mm) were also missing in the ruffe aquaria. The nonparametric Kolmogorov-Smirnovtest revealed a significant difference ( K - S zz=0.346, P < 0.001) between the length frequencies showing that the ruffes actively chose bigger individuals fi'om the prey population. This agrees with results from other experiments showing that visual fish predation mainly affects the large size classes of benthic invertebrates, probably because they are easiest to locate (Crowder & Cooper, 1982; Flecker & Allan, 1984; Mittelbach, 1988). In Experiment 11 the single stack treatment was expected to give significantly better
80 60
a)
61
!
,%%
40 )•1)
20
;%,
la sediment only
Ib short reeds, random
Id short reeds. stacks
|C
short
reeds° random +
80! J J
stones
I
b) • •
6O
•e e•
eeee•e
4O > >
)•,eee<
'°t
" . 4 • 4 •
)•4, •~*44.•4 4 +*@+4.
0
II a short reeds, random
II b short reeds, stack ON~
I
'
~ I
I00
80
'
l Wm !
c)
ON I
I
III a short reeds, stack
III b short reeds, patch
60
40 20
III c tall reeds, patch
Fig. I. Average percent survival of Asellus (+_ 1 SE). Stars on lines connecting treatment pairs indicate significant differences between these treatments (*p < 0.05, **p < 0.01, ***p < 0.001); (a) treatments in Experiment I (n = 6), (b) treatments in Experiment II (11 = 6) and (c) treatments in Experiment III (n = 5). Details of treatments are given in Table I.
62
J. M ATTI LA
shelter for Asellus from ruffe predation than the low complexity treatments in Experiment I. This hypothesis also proved acceptable as the survival of Ase2lus in the stack treatment (lib) was significantly higher (mean value 71.9%) than in the randomly placed reed treatment (lla, one-tailed t test, t = - 3.147, p < 0.01; Fig. lb). The mean survival in the randomly placed reed treatment was 43.8 + 8.1~o (7 + SE), which is comparable with the survival of Asellus in the corresponding treatment (Ib) in Experiment I (45.2 + 4.7 ~o, Fig. 1a). A single patch of high complexity in a noncomplex environment seems to be more advantageous for the prey than overall low-level complexity in the environment. The results also suggest that the patch size is critical for prey survival, at least in low complexity habitats because one larger patch gave better shelter than several smaller ones (Fig. la,b). Larger patches may be easier for the prey to find than small ones. They may also give shelter for a larger number of prey individuals without the problem of competition for space. The lowest survival of Asellus (26.9 + 11.3 °/o, ~ + SE) in Experiment III was measured in the ~'early summer" treatment (Ilia) and the highest in the "autumn" treatment (lllc, 94.9 + 1.97o, Fig. lc). The survival of Asellus in the "spring" treatment (lllb) with decaying reed was placed between these two. The ANOVA showed significant differences among these treatments (Ft2,~2~ = 22.896, p < 0.001). Fisher's PLSD test gave significant differences among all treatment pairs compared (Fig. 1c). These results show that increasing height of the vegetation significantly increases the survival of Asellus. The benthic prey gain no direct advantage from the increasing height of vegctation~ but the predators probably more often lose visual contact with the prey (Cooper & Crowder, 1979; Savino & Stein, 1982; Nelson & Bonsdorff, 1990). Tile search time thus increases and predation efficiency decreases (Stoner, 1982; Johns & Mann, 1987). Also, the structure of the complex patch is important. A patch of short reed did not offer as effective a refuge from ruffe predation as a similar sized stack of reed, possibly because the short reed does not significantly deter the predator's visual search. Similar differences in refuge effectiveness have been found for different blade and growth forms of aquatic plants (Coen et al., 1981; Stoner, 1982; Dionne & Folt, 1991). The feeding efficiency of perch in Experiment IV was considerably lower than the efficiency of ruffe in the previous experiments, and consequently the survival of Corophium was quite high (on average > 76~o) in all perch treatments (Fig. 2a). No statistical differences could be found between any pairs of treatments (F~2.~2~-- 0.395, NS). In Experiment V the duration was 6 days, which was clearly longer than in Experiment IV, and consequently the survival of Corophium in both treatments was also lower than in Experiment IV. The average survival varied between 37 and 48% (Fig. 2b), but no significant differences could be found between the treatment (t value = 0.876, NS). The survival of Corophium in the bare-sand treatment (Va) in Experiment V was comparable with the survival of Corophium in an earlier aquarium experiment (survival ,~ 20% in 14-day experiment) by Mattila & Bonsdorff (1989). In Experiment IV the survival of Corophium in the different fish treatments was clearly highest in the treatment with Potamogeton plants (Vlc, 50.2 + 5.9%, ~ + SE; Fig. 2c).
H A B I T A T C O M PL E X I T Y A N D FISH P R E D A T I O N I00
63
a)
I
80
60.
40 20
IV a sand only
E
IV b stones, random
80
IV c stones, stack
b)
,i,i t-x O t. O
60
t~
40 e.m
>. >
.m
L.
20
Vb
Va sand
stones,
only
random
8O
c)
uw i i
60
40
i I
NN I
20
VI a sand only
Vl b stones, random
Vl c plants, random
Fig. 2. Average percent survival of C~orophium( _ 1 sl~). Stars on lines connecting treatment pairs indicate significant differences between the~e treatments (*p < 0.05, **p < 0.01); (a) treatments in Experiment IV (n = 7), (b) treatments in Experiment V (n = 7) and (c) treatments in Experiment VI (n = 5). Details of treatment are given in Table I.
64
J. MATTILA
The average survival in the other treatments was 29.6 (bare sand, Via) and 34.0% (stones, VIb). The ANOVA showed a significant difference among the treatments (F~2,12~ = 7.571, p < 0.01). Fisher's PLSD test showed statistically significant differences between the bare sand and the Potamogeton treatments (p < 0.01), and between the stone and the Potamogetontreatments (p < 0.05). Although the stone densities were more than doubled and the coverage of the bottom increased from 6 to 17 ~o compared with Experiments IV and V, the stone habitat still remained insufficient to increase the survival of Corophium. Consequently, these results lead to partial rejection of the a priori hypothesis. According to Pierce (1988) and Savino & Stein (1989a), a high level of complexity does not automatically affect the predation efficiency; the prey must be able, for example, through its behaviour to utilize the complexity and the shelter it offers. In the present study the crustacean species used could not effectively utilize stones or reed pieces spread on the bottom. Coull & Wells (1983) found similar results in their experinaents, where neither stones nor gravel could affect the predation efficiency of blennies feeding on meiofauna. Ware (1972) found that wood litter covering the bottom (coverage 6 or 15 ~/o) increased the survival of amphipods against rainbow trout predation. The increments of habitat complexity resulting in lowered predation pressure in his study were comparable with the increments in this study, which, however, did not significantly affect the survival of the prey. In the present study Asellus was more favoured by small increments in habitat complexity than Corophium, probably due to the different behaviour of these species. Asellus is most often attached to the sediment surface and the vegetation and it rarely swims. Corophium, on the contrary, is more mobile and periodically swims both in nature (Holmstr0m & Morgan, 1983; Hughes, 1988) and in the aquarium environment (Hughes, 1988; Mattila & Bonsdorff, 1989). Corophium is a burrowing infaunal species, which is sheltered by increased sediment depth (Mattila & Bonsdorff, 1989). In the present experiments the sediment depth was kept at 1 cm, which may have partly provoked the swimming and crawling behaviour of Corophium. Sedentary prey are often more favoured by increased habitat complexity than motile prey (Stein & Magnuson, 1976; Savino & Stein, 1989b) or prey which may become more sedentary when complexity increases. The behaviour and mode of hunting of fish predators often changes when habitat complexity increases (Crowder & Cooper, 1982; Savino & Stein, 1982, 1989b; Wahl & Stein, 1988). The predation efficiency may decrease, because those elements providing complexity, e.g., vegetation, totally prevent or impair normal search behaviour (Savino & Stein, 1989b). Some fish predators may, however, easily adapt their search behaviour to variable complexity (Savino & Stein, 1982; Crowder & Binkowski, 1983). Winfield (1986) and Diehl (1988) have shown that the predation efficiency of perch remains relatively high even in habitats with high complexity, which might partly explain the minor effects of low level complexity on the predation efficiency of perch in the present study. Recent work, including the present study, suggests that the effects of habitat com-
HA,r'ITAT COMPLEXITY AND FISH PREDATION
65
plexity on predator-prey interactions are variable depending on the combination of a predator and a prey (Winfield, 1986; Gotceitas & Colgan, 1989; Dionne & Folt, 1991). Marinelli & Coull (1987) found that short straws standing up from the sediment (similar to those used in Experiment III) actually facilitate spot (Leiostomus) predation on meiofauna, while the results from the present study show a decreased predation effÉciency of ruffe on Asellus. Minello & Zimmerman (1983) also found that the predation efficiency of visual fish predators with different qualities was affected by Spartina stems in very variable ways. In conclusion, the present results show that the survival of brackish water invertebrate prey is positively affected by increasing habitat complexity, when exposed to predation by primarily visually feeding percids. Similar effects of habitat complexity on the survival of benthic invertebrate prey with visual predators have earlier been shown in several freshwater and marine studies (Gotceitas & Colgan, 1989). Tall plants give the best shelter for brackish water crustaceans against visual fish predators. Furthermore, patches, which are big enough and of high complexity in a noncomplex environment, affect predation efficiency more than a low overall complexity. ACKNOWLEDGEM ENTS
This study is a part of the Academy of Finland project (No. 108 1002) "Biotic interactions on shallow soft bottoms in the archipelago- experiments in the field and the laboratory". Financial support was also achieved from Jubileumsfonden for hi~gskoleviisendets 350-fo'. Hus6 Biological Station provided me with excellent laboratory facilities, which is gratefully acknowledged. I also thank E. Bonsdorff who provided advice during the experimental period and kindly commented earlier drafts of the manuscript. Two anonymous reviewers of the manuscript also offered suggestions and comments that substantially improved the paper. REFERENCES Alabaster, J.S. & B. Stott, 1978. Swimming activity of perch, Perca fluviatilis L. J. Fish Biol., Vol. 12, pp. 578-591. Bergman, E., 1988. Foraging abilities and niche breadths of two percids, Percafluviatilis and Gymnocephalus cernua, under different environme~:tal conditions. J. Anita. Ecol., Vol. 57, pp. 443-453. Blomqvist, E., 1986. A shallow water t3sh community structured by land uplift and dredging. PubL Water hist. Finl., Vol. 68, pp. 112--116. Blomqvist, E. & E. Bonsdorff 1986. Spatial and temporal variations of benthic macrofauna in a sandbottom area on Aland, northern Baltic Sea. Ophelia, Vol. 4, Suppl., pp. 27-36. Coen, L.D., K.L. Heck & L.G. Abele, 1981. Experiments on competition and predation among shrimps of seagrass meadows. Ecology, Vol. 62, pp. 1484-14q3. Cooper, W.E. & L.B. Crowder, 1979. Patterns of predation in simple and complex environments. In, Predator-prey systems in fisheries management, edited by R.H. Stroud & H. Clepper, Sport Fishing Institute, Washington, DC, pp. 257-267. -. .,~ Cou!l, B.C. & J. B.J. Wells, 1983. Refuges from fish preC:~,on: experiments with phytal meiofauna from the New Zealand rocky intertidal. Ecology VoL 6a,~pp. 1599-1609.
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Crowder, I,.B. & F.P. Binkowski, 1983. Foraging behaviors and the interaction of alewife, Alosa psemh~harengus, and bloater, Coregonus hoyi. Environ. Bh~l. Fish., Vol. 8, pp. 105-113. Crowder, L.B. & W.E. Cooper, 1982. Habitat structuro! complexity and the iateraction between bluegills and their prey. Ecology, Vol. 63, pp. 1802-1813. Diehl, S., 1988. Foraging efficiency of three freshwater fishes: effects of structural complexity and light. Oikos, Vol. 53, pp. 207-214. Dionne, M. & C.L. Folt, 1991. An experimental analysi~ of macrophyte growth forms as fish foraging habitat. Can. J. Fish. Aquat. Sci., Vol. 48, pp. 123-131. Flecker, A. S. & J. D. Allan, 1984. The importance of predation, substrate and spatial refugia in determining lotic insect distributions. Oecologia (Berlin), Vol. 64, pp. 306-313. Gotceitas, V., 1990. Variation in plant stem density and its effects on foraging success of juvenile bluegill sunfish. Environ. Biol. Fish. Vol. 27, pp. 63-70. Gotceitas, V. & P. Colgan, 1989. Predator foraging success and habitat complexity: quantitative test of the threshold hypothesis. Oecologia (Berlin), Vol. 80, pp. 158-166. Gregg, W.W. & F.L. Rose, 1985. Influences of aquatic macrophytes on invertebrate community structure, guild structure, and microdistribution in streams. Hydrobiologia, Vol, 128, pp. 45-56. Hansson, S., 1984. Competition as a factor regulating the geographical distribution offish species in a Baltic archipelago: a neutral model analysis. J. Biogeogr., Vol. 11, pp. 367-381. Hansson, S., 1985. Effects of eutrophication on fish communities with special reference to the Baltic Sea - a literature review. Rep. hist. Freshwater Res. Drottninghohn, Vol. 62, pp. 36-56. Heck, K. L., Jr., K.W. Able, M.P. Fahay & C.T. Roman, 1989. Fishes and decapod crustaceans of Cape Cod eelgrass meadows: species composition, seasonal abundance patterns and comparison with unvegetated substrates. Estuaries, Vol. 12, pp. 59-65. Heck, K. L., Jr. & T.A. Thoman, 1981. Experiments on predator-prey interactions in vegetated aquatic habitats. J. Exp. Mar. Biol. EcoL, Vol. 53, pp. 125-134. Holmstr6m, W. F. & E. Morgan, 1983. Variation in naturally occurring rhythm of the estuarine amphipod, Corophium vohaator (Pallas). J. Mar. Biol. Assoc. U.K., Vol. 63, pp. 833-850. Hughes, R.G., 1988. Dispersal by benthic invertebrates: the in situ swimming behaviour of the amphipod Corophium vohaator. J. Mar. Biol. Assoc. U.K., Vol. 68, pp. 565-579. Johns, P. M. & K. H. Mann, 1987. An experimental investigation of juvenile lobster habitat preference and mortality among habitats ofvarying structural complexity. J. Exp. Mar. Biol. Ecol., Vol. 109, pp. 275-285. Marinelli, R. L. & B.C. Coull, 1987. Structural complexity and juvenile fish predation on meiobenthos: an experimental approach. J. E.x~. Mar. Biol. Ecol., Vol. 108, pp. 67-81. Mattila, J. & E. Bonsdorff, 1988. A quantitative estimation offish predation on shallow soft bottom benthos in SW Finland. Kiei. Meeresforsch., Vol. 6, Sonderh., pp 111-125. Mattila, J. & E. Bonsdorff, 1989. The impact offish predation on shallow soft bottoms in brackish waters (SW Finland); an experimental study. Neth. J. Sea Res., Vol. 23, pp. 69-81. Minello, T.J. & R.J Zimmerman, 1983. Fish predation on juvenile brown shrimp, Penaeus aztecus Ives: the effect of simulated Spartina structure on predation rates. J. Exp. Mar. Biol. Ecol., Vol. 72, pp. 211-231. Mittelbach, G.G., 1988. Competition among refuging sunfishes and effects of fish density on littoral zone invertebrates. Ecoh~gy, Vol. 69, pp. 614-623. Nellbring, S., 1988. Quantitative and qualitative studies of fish in shallow water, northern Baltic proper, Ph.D. dissertation, University of Stockholm, Sweden, 19 pp. Nelson, W.G. & E. Bonsdorff, 1990. Fish predation and habitat complexity: Are threshold levels real? J. E.W. Mar. Biol. Ecol., Vol. 141, pp. 183-194. Orth, R.J., K. L. Heck Jr. & J. van Montfrans, 1984, Faunal commanities in seagrass beds: a review of the influence of plant structure and prey characteristics on predator-prey relationships. Estuaries, Vol. 7, pp. 339-350. Pierce, C. L., 1988. Predator avoidance, microhabitat shift, and risk-sensitive foraging in larval dragonflies. Oecologia (Berlin), Vol. 77, pp. 81-90. Pihl, L., 1982. Food intake of young cod and flounder in a shallow bay on the Swedish west coast. Neth. J. Sea Res., Vol. 16, pp. 419-432. Pihl, L., 1985. Food selection and consumption of mobile epibenthic f~::~nain shallow marine areas. Mar. Ecol. Progr. Set., Vol. 22, pp. 169-179. Rabe, F.W. & F. Gibson, 1984. The effect of macrophyte removal on the distribution of selected invertebrates in a littoral environment. J. Freshwat. Biol., Vol. 2, pp. 359-37 i.
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Rask, M. & C. Hiisivuori, 1985. The predation on Asellus aquaticus (L.) by perch, Percafluviatilis (L.) in a small forest lake. Hydrobiologia, Vol. 121, pp. 27-33. Savino, J.F. & R.A. Stein, 1982. Predator-prey interactions between largemouth bass and bluegills as influenced by simulated submerged vegetation. Trans. Am. Fish. Soc., Vol. 111, pp. 255-266. Savino, J. F. & R.A. Stein, 1989a. Behavior of fish predators and their prey: habitat choice between open water and dense vegetation. Environ. Biol. Fish., Vol. 24, pp. 287-293. Savino, J.F. & R.A. Stein, 1989b. Behavioral interactions between fish predators and their prey: effects of plant density. Anita. Behav., Vol. 37, pp. 311-321. Sokal, R. R. & F.J. Rohif, 1981. Biometry. W. H. Freeman & Co., San Francisco, California, second edition, 859 pp. Stein, R.A. & J.J. Magnuson, 1976. Behavioral response of crayfish to a fish predator. Ecology, Vol. 57, pp. 751-761. Stoner, A.W., 1982. The influence of benthic macrophytes on the foraging behavior of pinfish Lagodon rhomboides (Linnaeus). J. Exp. Mar. Biol. Ecol., Vol. 58, pp. 271-284. Summerson, H.C. & C.H. Peterson, 1984. Role of predation in organizing benthic communities of a temperate-zone seagrass bed. Mar. Ecol. Progr. Set., Vol. 15, pp. 251-263. Tonn, W.M., G.A. Paszkowski & I.J. Holopainen, 1989. Responses of crucian carp populations to differential predation pressure in a manipulated pond. Can. J. Zool., Vol. 67, pp. 2841-2849. Wahl, D.H. & R.A. Stein, 1988. Selective predation by three esocids: the role of prey behaviour and morphology. Trans. Am. Fish. Soc., Vol. 117, pp. 142-151. Ware, D.M., 1972. Predation by rainbow trout (Salmo gairdneri): the influence of hunger, prey density and prey size. J. Fish. Res. Board Can., Vol. 29, pp. 1193-1201. Winfield, I.J., 1986. The influence of simulated aquatic macrophytes on the zooplankton consumption rate of juvenile roach, Rutilus rutilus, rudd, Scardinius erythrophtabnus, and perch, Perca fluviatilis. J. Fish Biol., Vol. 29, pp. 37-48. Osterman, C.-S. & E. Bonsdorff, 1985. ,~rstidsvariationer i djursamh~illen p~t grunda mjukbottnar. Medd. HusiJ Biol. Stn., Vol. 25, pp. 16-42.