mean crayfish abundance (estimated by trapping and expressed as catch per unit effort) ... by providing refuges for prey species and reducing ... capture, handle or digest (Sih, 1987). ...... ively related to the colonizable plant surface area and.
frbiol0133
Freshwater Biology (1996) 36, 631–646
Patterns in benthic food webs: a role for omnivorous crayfish? ¨ M, CHRISTER BRO ¨ N M A R K A N D W I L H E L M G R A N E´ L I PER NYSTRO Department of Ecology, S-223 62, Lund, Sweden
S U M M A RY 1. The biomass and species richness of macrophytes and invertebrates in artificial ponds at two sites in southern Sweden (twenty-one ponds at each site) were investigated. Alkalinity was high at one site (H ponds) and low at the other site (L ponds). The ponds chosen had different densities of signal crayfish (Pacifastacus leniusculus), with mean crayfish abundance (estimated by trapping and expressed as catch per unit effort) significantly higher in the L ponds (10.7) than in the H ponds (4.9). Macrophytes, invertebrates, the amount of periphyton on stones and the organic content of the sediment were determined in each pond. 2. Macrophyte biomass, cover and species richness declined with increasing crayfish density. Macrophyte species composition differed between ponds and was related to crayfish abundance. 3. The total biomass of invertebrates and the biomass of herbivorous/detritivorous invertebrates declined with increasing crayfish abundance, but the biomass of predatory invertebrates declined only in the L ponds. The relative biomass of Gastropoda and Odonata declined in ponds where crayfish were abundant. In ponds where crayfish were abundant the invertebrate fauna was dominated by sediment-dwelling taxa (Sialis (H and L ponds) and Chironomidae (H ponds)). 4. The number of invertebrate taxa in macrophytes declined with increasing crayfish abundance. The percentage of macrophyte-associated invertebrate taxa differed between ponds, but also between sites. The relative biomass of Gastropoda declined in H ponds where crayfish were abundant. In H ponds Trichoptera or Gammarus sp. and Heteroptera dominated where crayfish were abundant, whereas Odonata dominated in L ponds with abundant crayfish. 5. The organic content of the sediment decreased in ponds with high crayfish densities, while the amount of periphyton on stones was not related to crayfish density. 6. We conclude that the signal crayfish may play an important role as a keystone consumer in pond ecosystems, but lower trophic levels did not respond to changes in the abundance of the crayfish according to the trophic cascade model. Omnivorous crayfish may decouple the cascading effect. Introduction Predation is an important structuring force in freshwater food webs (e.g. Kerfoot & Sih, 1987; Carpenter & Kitchell, 1993). Predators can affect the prey community directly by reducing the number of species, their densities and changing their size distribution (e.g. Hall, Cooper & Werner, 1970; Peckarsky & Dodson, 1980; Gilinsky, 1984). Planktivorous fish © 1996 Blackwell Science Ltd
selectively remove larger zooplankton (Brooks & Dodson, 1965), but predation in freshwater fish– zooplankton systems can also lead to trophic cascades. If piscivorous fish are present the abundance of planktivorous fish can be affected, which in turn can influence the abundance and size distribution of zooplankton and phytoplankton (e.g. Carpenter et al.,
631
632 P. Nystro¨m, C. Bro¨nmark and W. Grane´li 1987; Vanni & Findlay, 1990; Scheffer, 1991). Predation is also an important structuring force in benthic food chains. The latter are often tightly linked, so that predators affect lower trophic levels directly and indirectly, according to the trophic cascade model (Bro¨nmark, Klosiewski & Stein, 1992; Martin et al., 1992; Bro¨nmark, 1994; Lodge et al., 1994). Omnivores (predators feeding on more than one trophic level) can affect the connectance between species in a food web, and the structure and stability of prey populations (Pimm & Lawton, 1977; Diehl, 1993a). In marine communities it has been suggested that omnivory should increase the consumer control of the community at lower trophic levels (Menge & Sutherland, 1987). Where top predators also eat herbivores, changes in the abundance of the top predator may not generate cascading effects (Polis & Holt, 1992). Habitat diversity may allow the co-existence of many species (Menge & Sutherland, 1976; Holt, 1984) by providing refuges for prey species and reducing the foraging efficiency of predators. The predation efficiency of fish (e.g. Crowder & Cooper, 1982; Gilinsky, 1984; Diehl, 1993b) and predatory invertebrates (Peckarsky & Dodson, 1980; Thompson, 1987; Williams, Barnes & Beach, 1993) is reduced in structurally complex habitats, such as macrophyte beds, and predators avoid attacking prey which are difficult to capture, handle or digest (Sih, 1987). Thus, macrophytes play an important role as refuges from predators for several invertebrate prey taxa. Macrophytes also function as substrata for periphyton, an important food source for invertebrates, for egg deposition and, after macrophyte senescence, as a detrital food source (Soszka, 1975; Carpenter & Lodge, 1986; Newman, 1991). Herbivory on freshwater macrophytes is common (see reviews by Lodge (1991) and Newman (1991)) and the mass-specific herbivory rate is higher in freshwater communities than in terrestrial ones (Cyr & Pace, 1993). A substantial loss of macrophyte biomass can be expected to increase the predation efficiency of predators and thus affect the abundance and species richness of invertebrates. Crayfish can be very abundant and constitute a large biomass in the littoral zones of lakes, ponds and streams (e.g. Abrahamsson, 1966; Abrahamsson & Goldman, 1970; Mason, 1975). Crayfish are omnivorous, although adult crayfish mostly consume vegetable food, whereas younger crayfish eat a larger proportion
of animal food (Mason, 1975; Goddard, 1988). Detritus usually forms a substantial proportion of the crayfish diet (Lund, 1944; Hessen & Skurdal, 1986; Skurdal et al., 1988), but they also graze periphytic algae (Flint & Goldman, 1975) and there are reports of cannibalism (Capelli, 1980). Freshwater crayfish, through their omnivory, relatively large size and high densities, can be expected to have a strong influence on food webs. Most of the earlier studies of effects of crayfish on lower trophic levels have been short and performed in laboratories or in cages. The direct and indirect long-term effects of omnivorous top predators in complex food webs are less well known. To examine the long-term effects of freshwater crayfish populations on littoral communities, we studied forty-two ponds in Sweden, which were devoid of predatory fish, but which had different densities of the signal crayfish (Pacifastacus leniusculus Dana). We expected that the crayfish should affect the ecosystem in a number of ways. 1 By reducing the number of species and biomass of macrophytes, especially submersed species which are easy to handle, and thereby reducing habitat complexity. In turn, these reductions should indirectly affect invertebrate biomass and species richness. 2 Selective predation on invertebrates may cause a decrease in the number of invertebrate taxa with increasing crayfish density, together with a tendency for communities to be dominated by sediment-dwelling animals, and by invertebrates with well-developed escape reactions. 3 Detritivory and herbivory could reduce the sediment organic content. 4 Since crayfish can reduce the abundance of periphyton-grazing snails (Hanson, Chambers & Prepas, 1990; Weber & Lodge, 1990; Lodge et al., 1994), increased crayfish density should have a positive, indirect effect on periphytic algae (a trophic cascade effect).
Materials and methods Study areas Effects of crayfish on macrophytes, invertebrates, periphyton and on the organic content of the sediment were studied in ponds belonging to two crayfish farms. The ponds had a v-shaped profile (6 m wide, 1.5 m deep, 70–150 m long, and separated by µ 5 m), © 1996 Blackwell Science Ltd, Freshwater Biology, 36, 631–646
A role for omnivorous crayfish 633 Table 1 Means and standard deviations of water quality data from surface samples taken at two sites (twenty-one ponds with high alkalinity and twenty-one ponds with low alkalinity) and their inflows in July 1994. *Jackson turbidity units
Site
pH
Alkalinity (mEqv l–1)
Conductivity (mS m–1)
Turbidity (JTU)*
Colour (mg Pt l–1)
Total P (µg l–1)
Total N (mg l–1)
High alkalinity (H) Inflow Low alkalinity (L) Inflow
7.61 (0.19) 8.08 6.96 (0.26) 7.01
2.56 (0.27) 2.92 0.24 (0.07) 0.01
32 (2.0) 36 10 (0.3) 10
3.3 (0.02) 18 5.8 (4.1) 90
45 (5) 55 88 (17) 200
27 (5.5) 52 61 (25) 46
0.79 (0.32) 1.65 1.09 (0.21) 0.89
and were constructed in the early 1980s in pasture. The substratum of the ponds was clay and gravel. Ponds situated in Skåne (13°E, 56°N) had a high alkalinity (hereafter named H) and the ponds in Småland (15°E, 56°509N) a low alkalinity (hereafter named L; Table 1). The ponds were stocked with juvenile signal crayfish in 1983 (H) and 1985 (L), but the success of the introduction varied between ponds. In 1990 the ponds were supplied with rocks (L) and building bricks (H) in order to increase crayfish production. Water is supplied from river Vegeån (H) and Lake Åsnen (L), and the water in the ponds is changed every fortnight (H) or month (L). The H site has thirty-nine similar ponds (µ 70 m long) and the L site 143 similar ponds (µ 150 m long). The impact of fish is negligible although, when electrofished every second year, a few brown trout and eels were caught (H). The L ponds were filled with lake water in 1985 and some ponds had dense populations of perch (Perca fluviatilis L.) in 1988. Following treatment with rotenone in 1990 these ponds have been fishless.
and outlets and at 10-m (when five samples were taken) or 20-m intervals (when three samples were taken).
Crayfish Crayfish abundance in each pond was estimated by trapping, using a method similar to that described by Abrahamsson & Goldman (1970). In lakes with low densities of predatory fish, catches of crayfish in baited traps usually give a good estimation of crayfish abundance (Collins et al., 1983). In the middle of August 1994, cylindrical traps (mesh size 15 mm) with funnel entrances at both ends were baited with dead roach (Rutilus rutilus L.) The bait was put in a net box in each trap, to prevent the crayfish from consuming the entire bait and subsequently escaping from the traps. Twenty traps were set out at 5-m intervals in each pond (L) in the late afternoon. The crayfish were harvested the following morning and the number of crayfish caught per trap (CPUE) was determined. Since the H ponds were shorter, ten traps were set on each of two days.
Experimental ponds and sampling At each site twenty-one ponds were chosen in order to obtain a range of different crayfish densities (seven ponds with low/no abundance of crayfish, seven ponds with intermediate abundance and seven with a high abundance). Ponds were selected by evaluating test fishing results from 1991 (L) and 1992 (H) (P. Nystro¨m, unpublished), and test fishing results obtained in early spring in 1994. The catches in ponds with high abundances of crayfish were not abnormally high in comparison with catches in lakes, rivers and ponds (Abrahamsson, 1966; Fu¨rst, 1989; P. Nystro¨m, unpublished). The shape of the ponds precluded a completely randomized sampling. Instead all samples of macrophytes, invertebrates, periphyton and sediment were taken 15 m (H) and 50 m (L) from the inlets © 1996 Blackwell Science Ltd, Freshwater Biology, 36, 631–646
Water chemistry Samples for water characteristics were taken on 16 July (H) and 22 July (L). A surface sample (10 cm water depth) was collected in macrophyte-free areas in the middle of each pond as well as from the inflow. Alkalinity, pH, turbidity, conductivity, and colour were analysed on the day of sampling. Samples for analysis of total phosphorus and total nitrogen were frozen and analysed within 3 months on a Technicon Auto Analyser II, according to Swedish standards (SS 028127 and SS 028131).
Macrophytes We quantified above-ground macrophyte biomass as well as percentage macrophyte cover in the ponds.
634 P. Nystro¨m, C. Bro¨nmark and W. Grane´li The biomass of macrophytes was estimated using a large PVC cylinder (diameter 50 cm, length 80 cm). One end of the cylinder was cut at an angle corresponding to the inclination of the sediment surface (µ 30°). Five samples were taken from each pond. All the macrophytes within the cylinder were collected by hand. Before each taxon was put in separate plastic bags, the macrophytes were shaken for 30 s and gently squeezed. Due to the large amount of macrophytes collected it was not possible to analyse dry weights, therefore the wet weight of the above-ground biomass was determined on the day of sampling (to the nearest 0.1 g). Macrophytes were identified to species or in a few cases to genera. In the middle of August the percentage cover of the ponds by macrophytes was determined. We used a Sony Handycam VCR, equipped with a polarizing lens which made it possible to measure not only the percentage cover of emergent and floating-leafed species, but also submersed macrophytes. Five squares (2.5 3 2.5 m) were recorded in each pond. Results were analysed by dividing a TV screen into forty-eight squares (each 5 3 5 cm). By looking at a still picture (chosen from the video), the percentage macrophyte cover for each small square was estimated, and the mean coverage from all fortyeight squares was calculated.
Periphytic algae On 8 July (H) and 17 July (L) five randomly chosen bricks (H) and stones (L) were collected at the same depth (30 cm) from different heaps in each pond. However, two of the H ponds were not sampled due to excessive macrophyte cover. On each of the stones and bricks a sharpened plastic tube (Ø 28 mm) was placed on the side exposed to light. First, periphyton outside the tube was removed, then periphyton inside the tube was thoroughly scraped off with a scalpel, transferred to vials and deep-frozen. Within 3 months the chlorophyll a content was measured using ethanol as the extraction solvent (Jespersen & Christoffersen, 1987).
Sediment Three sediment samples were taken from the deepest parts of the ponds using a sharpened Plexiglas core (internal diameter 32 mm). Each sample contained the upper 10 cm of the sediment. We placed the sediment gently in a hand net (mesh size 300 µm), removed remains of fresh macrophytes and macroinvertebrates, and then mixed the sediment. A subsample of 10 ml was taken. The dry weight (60 °C for 24 h) and the organic content of the sediment (4 h at 450 °C) were analysed.
Invertebrates Invertebrates were sampled using two methods, with a Plexiglas corer (internal diameter 105 mm), and with a hand net. The samples were taken on 4–7 July (H) and on 11–15 July (L), at the opposite side of the ponds from the macrophyte samples. In each pond five samples were taken with the corer at a water depth of 0.9 m. Each sample included the water column with vegetation and a sediment core (10 cm). The samples were sieved (0.5 mm mesh size), kept cool and deepfrozen the same day. Three hand net samples were taken in each pond by sweeping the net for 1 min through a 1-m2 stand of macrophytes. The animals were sorted alive, kept cool and deep-frozen the same day. After thawing, invertebrates were identified to species for snails and to genera or family for all other taxa. Invertebrates were counted and measured (to the nearest 0.1 mm). Dry weight (shell-free dry weight for snails) was determined by deriving length–weight relationships for the most common taxa (Smock, 1980).
Statistical analysis To avoid pseudoreplication, only the mean values from the samples taken in each pond were used in the statistical analysis. We tested the effects of crayfish density (independent variable) on several dependent variables using simple linear regression. The residuals were examined by plotting, and by the use of the Kolmogorow–Smirnov test of normality (Zar, 1984). If the assumptions of normality or homoscedasticity could not be met, the dependent variable was transformed. For percentage data we used the arcsine transformation and for data with heteroscedasticity we used a logarithmic transformation (Zar, 1984). We tested the effects of crayfish density (CPUE) at the two sites on the dependent variables in an analysis of covariance (ANCOVA), with CPUE as the covariate. The first step in the ANCOVA was to test for homogeneity of slopes (interaction effect). If there was no significant interaction effect, the analysis was repeated © 1996 Blackwell Science Ltd, Freshwater Biology, 36, 631–646
A role for omnivorous crayfish 635 without the interaction term. Then, if the ANCOVA yielded a non-significant difference between the two sites (homogeneity of the Y-intercepts) but a significant effect of CPUE on the dependent variable (slopes β Þ 0), data for the two sites were pooled in a simple regression analysis. To be able to study the species composition of invertebrate and macrophyte taxa in relation to crayfish abundance in ponds, we compared the percentage biomass of common taxa with principal components analysis (PCA). We based our analysis and interpretations mainly on the recommendations given in Dillon & Goldstein (1984). Due to differences in variance between variables we used a correlation matrix. We retained components having eigenvalues greater than 1, and at least 25% of a variable’s variance should be accounted for by a factor (an absolute loading of 0.5) to be considered as important. Interpretations were then based on those variables loading highest on a given factor, and each variable’s highest (absolute) loading is therefore shown in bold type in all tables presented. To relate differences in species composition among ponds to crayfish abundance, we derived the principal component scores for each pond. The scores were then related to the crayfish abundance by using simple linear regression.
Results Crayfish The number of crayfish caught per trap night (CPUE) was significantly greater (ANOVA, F1.40 5 13.3057, P , 0.001) in the L ponds (mean CPUE 10.7, range 2.6–19.3) than in the H ponds (mean CPUE 4.9, range 0–14.2). These results were positively correlated with the data from test trapping in 1991 and 1992 (Pearson, P 5 0.0002, r2 5 0.54 (H), P 5 0.0039, r2 5 0.36 (L)).
Macrophytes Macrophyte biomass in the H ponds was dominated by Elodea canadensis (L.C. Rich.) (32%) and Potamogeton natans (L.) (17%). In the L ponds Myriophyllum alterniflorum (DC.) (46%) and P. natans dominated (27%). With increasing crayfish abundance, both the total biomass of macrophytes and the percentage macrophyte cover decreased significantly at both sites © 1996 Blackwell Science Ltd, Freshwater Biology, 36, 631–646
Fig. 1 Linear regression of the relationship between the number of crayfish caught per trap night (CPUE) and the total biomass of macrophytes (wet weight m–2) in forty-two ponds (pooled data from twenty-one ponds with high alkalinity twenty-one ponds with low alkalinity).
Table 2 ANCOVA table of the effects of crayfish catch per trap night (CPUE; covariate) at two sites (twenty-one ponds with high alkalinity and twenty-one ponds with low alkalinity), on macrophyte biomass m–2, percentage of macrophyte cover and macrophyte species richness per unit surface area. Significant slopes (CPUE) are negative Source
df
F test
P value
Macrophyte biomass m–2 Site CPUE Error
1 1 39
0.04 33.02
0.84 ,0.0001
Percentage macrophyte cover Site 1 CPUE 1 Error 39 Macrophyte species richness Site 1 CPUE 1 Error 39
3.12 37.89
5.03 23.89
0.085 ,0.0001
0.03 ,0.0001
(Table 2, Fig. 1). In some ponds with abundant crayfish populations there were no macrophytes. The number of macrophyte taxa also decreased significantly with increasing crayfish abundance (Table 2). The mean number of macrophyte taxa per sample was 1.5 at both sites and varied between 0 and 3.8 (H) and 0 and 2.8 (L). In ponds where macrophytes were present there was a change in the species composition in relation to crayfish abundance. According to the second principal component (H), P. natans dominated in H ponds where crayfish were abundant, whereas Potamogeton alpinus (Balbis) dominated in ponds with
636 P. Nystro¨m, C. Bro¨nmark and W. Grane´li Table 3 Component loadings for percentage biomass of macrophyte taxa found in nineteen ponds with high alkalinity and twenty ponds with low alkalinity, and percentage variance explained by the retained principal component axes. Important loadings are shown in bold type. P values refer to simple regression, with the number of crayfish caught per trap night (CPUE) against the scores of the different axes Source
PC1
PC2
PC3
Ponds with high alkalinity Variance explained (%) Eigenvalues
28.70 2.01
20.80 1.46
18.35 1.28
Macrophyte taxa Sparganium emersum Elodea canadensis Alisma plantago-aquatica Potamogeton alpinus Potamogeton natans Scirpus lacustris Glyceria fluitans (L.) R. Br. Linear regression (P value)
0.73 –0.72 0.64 0.54 0.41 –0.07 0.29 0.27
0.39 0.55 0.04 0.61 –0.67 –0.41 –0.01 0.0013
–0.16 0.29 0.34 –0.24 0.38 –0.86 0.25 0.41
Fig. 2 Linear regression of the relationship between the number of crayfish caught per trap night (CPUE) and the component scores from the second principal component axis. The principal component axis reflects the percentage biomass of different macrophyte species in nineteen ponds with high alkalinity. Macrophyte species with important loadings on the axis are given.
Ponds with low alkalinity Variance explained Eigenvalues
33.35 2.00
27.07 1.62
17.99 1.08
Macrophyte taxa Myriophyllum alterniflorum Potamogeton natans Elodea canadensis Alisma plantago-aquatica Sparganium emersum Callitriche sp. Linear regression (P value)
–0.91 0.86 0.56 0.17 0.28 –0.12 0.0013
–0.01 –0.15 –0.47 0.77 0.74 0.48 0.034
–0.34 –0.35 –0.03 0.10 0.35 0.84 0.69
the biomass of herbivores/detritivores with increasing crayfish abundance at both sites (Table 4). The relationship between the total biomass of predatory invertebrates differed between sites (ANCOVA, site 3 CPUE, F1.38 5 5.8649, P 5 0.0203, Table 4). Simple linear regression revealed a significant decrease of predatory invertebrates with increasing crayfish abundance in L ponds but not in H ponds (r2 5 0.33, P 5 0.0069 (L), r2 5 0.004, P 5 0.7774 (H)). The species composition of invertebrates differed between ponds and was related to crayfish abundance. At both sites the first principal components showed that ponds with low densities of crayfish were dominated by Gastropoda and Odonata, whereas the sediment-dwelling predator Sialis sp. dominated in ponds where crayfish were abundant (Table 5, Fig. 5). Further, in H ponds the first principal component showed that the mussel Pisidium sp. and Ephemeroptera dominated in ponds with low densities of crayfish, whereas chironomids dominated in ponds with high catches of crayfish (Table 5, Fig. 5a). In L ponds the isopod Asellus aquaticus (L.) dominated in ponds with low densities of crayfish (Table 5, Fig. 5b).
low crayfish densities (Table 3, Fig. 2). For L ponds, the first principal component showed that M. alterniflorum dominated in ponds where crayfish were abundant, whereas E. canadensis and P. natans dominated in ponds with low densities of crayfish (Table 3, Fig. 3a). According to the second principal component (L), Alisma plantago-aquatica (L.) and Sparganium emersum (Rehman) were also common in ponds with low densities of crayfish (Table 3, Fig. 3b).
Invertebrates Core samples. Invertebrates in H ponds were dominated by Chironomidae (23%), Gammarus sp. (20%), Gastropoda (18%) and Sialis sp. (13%). In L ponds the invertebrates were dominated by Heteroptera (29%), Chironomidae (21%), Sialis sp. (18%) and Odonata (11%). At both sites, the total biomass of invertebrates decreased linearly with increasing crayfish abundance (Table 4, Fig. 4). There was also a significant decrease in
Hand net samples. Macrophyte-associated invertebrates in H ponds were dominated by Odonata (30%), Gastropoda (25%), Gammarus sp. (15%) and Trichoptera (11%). In L ponds the invertebrates were dominated by Odonata (53%), Heteroptera (16%) and Coleoptera (9%). The mean number of macrophyte-associated © 1996 Blackwell Science Ltd, Freshwater Biology, 36, 631–646
A role for omnivorous crayfish 637
Fig. 4 Linear regression of the relationship between the number of crayfish caught per trap night (CPUE) and the total biomass of invertebrates (dry weight m–2) from core samples in forty-two ponds (pooled data from twenty-one ponds with high alkalinity and twenty-one ponds with low alkalinity).
Table 4 ANCOVA table of the effects of crayfish catch per trap night (CPUE; covariate) at two sites (twenty-one ponds with high alkalinity and twenty-one ponds with low alkalinity), on total invertebrate biomass m–2, herbivore/ detrivore biomass m–2, predatory invertebrate biomass m–2 and macrophyte-associated invertebrate species richness m–2. Significant slopes (CPUE) are negative df
F test
P value
Total invertebrate biomass m–2 Site 1 CPUE 1 Error 39
0.89 17.88
0.35 0.0001
Herbivore/detrivore biomass m–2 Site 1 CPUE 1 Error 39
10.52 14.91
0.0024 0.0004
9.08 8.32 5.86
0.0046 0.0064 0.020
Source Fig. 3 Linear regression of the relationship between the number of crayfish caught per trap night (CPUE) and the component scores from the first (a) and the second (b) principal component axes. The principal component axes reflect the percentage biomass of different macrophyte species in twenty ponds with low alkalinity. Macrophyte species with important loadings on the axes are given.
taxa per sample declined significantly with increasing crayfish abundance at both sites (Table 4, Fig. 6). The mean numbers of taxa found were 10.5 (H) and 8.1 (L) and varied between 7.0 and 15.7 (H) and 4.0 and 13.3 (L). There was a difference in species composition of macrophyte-associated invertebrate taxa in relation to crayfish abundance (Table 6). In H ponds the percentage biomass of macrophyte-associated gastropods, leeches and coleopterans increased in ponds with low crayfish densities, whereas Trichoptera decreased (Table 6, Fig. 7a). The second principal component (H) revealed an increase in the percentage biomass of Gammarus sp. and Heteroptera in ponds where crayfish were abundant but a decrease in Odonata (Table 6, Fig. 7b). In the L ponds, as in the core © 1996 Blackwell Science Ltd, Freshwater Biology, 36, 631–646
Predatory invertebrate biomass m–2 Site 1 CPUE 1 Site 3 CPUE 1 Error 38
Macrophyte-associated invertebrate species richness Site 1 0.14 0.71 CPUE 1 59.70 ,0.0001 Error 39
samples, A. aquaticus increased in ponds with low catches of crayfish. In contrast to the results from the H ponds, the percentage biomass of macrophyteassociated Trichoptera decreased in ponds with high catches of crayfish, whereas Odonata increased (Table 6, Fig. 8).
638 P. Nystro¨m, C. Bro¨nmark and W. Grane´li Table 5 Component loadings for percentage biomass of invertebrate taxa in core samples found in twenty-one ponds with high alkalinity and twenty-one ponds with low alkalinity, and percentage of variance explained by the retained principal component axes. Important loadings are shown in bold type. P values refer to simple regression analyses of the number of crayfish caught per trap night (CPUE) in each pond against the scores of the different axes Source
PC1
PC2
PC3
Ponds with high alkalinity Variance explained Eigenvalues
33.58 2.69
22.62 1.81
14.27 1.14
Invertebrate taxa Gastropoda Odonata Sialis sp. Chironimidae Pisidium sp. Ephemeroptera Gammarus sp. Heteroptera Linear regression (P value)
0.84 0.76 –0.61 –0.55 0.52 0.50 –0.36 –0.27 ,0.0001
0.07 –0.35 0.16 0.54 0.47 0.44 –0.80 0.56 0.17
0.15 0.22 0.39 0.37 –0.14 –0.26 –0.46 –0.69 0.79
34.26 2.06
28.40 1.70
0.77 0.76 –0.61 0.56 –0.30 –0.33 0.0001
–0.17 0.12 –0.47 –0.37 0.91 0.69 0.20
Ponds with low alkalinity Variance explained (%) Eigenvalues Invertebrate taxa Asellus aquaticus Gastropoda Sialis sp. Odonata Heteroptera Chironomidae Linear regression (P value)
Detritus and periphytic algae The content of organic matter in the sediment decreased significantly in ponds where crayfish were abundant (Fig. 9). The average organic content was 6.8% (H, range 1.8–12.7) and 4.6% (L, range 1.7–12.5). The amount of periphytic algae on stones (expressed as chlorophyll a) was not related to crayfish abundance (CPUE) at either of the two sites (ANCOVA; F1.36 5 0.016, P 5 0.9).
Discussion The results of this study indicate that the signal crayfish may play an important role in freshwater benthic food webs. There was a negative relationship between crayfish abundance and macrophyte biomass, invertebrate biomass and the amount of detritus. The species composition of invertebrates and macrophytes
Fig. 5 Linear regression of the relationship between the number of crayfish caught per trap night (CPUE) and the component scores from the first principal component axes. The principal component axes reflect the percentage biomass of different invertebrate taxa from core samples in twenty-one ponds with high alkalinity (a) and low alkalinity (b). Invertebrate taxa with important loadings on the axes are given.
was different in ponds with high and low densities of crayfish. Previous studies have also shown the importance of crayfish. Momot, Gowing & Jones (1978) suggested that the crayfish Orconectes virilis (Hagen) acted as a keystone predator by switching between benthic invertebrates, detritus and periphyton as food sources, thus interacting at all trophic levels in the food web. Momot (1995) concluded that crayfish can reduce or even exclude other animals and macrophytes from the community. The crayfish Orconectes propinquus (Girard) may also act as a keystone predator in streams, by regulating the biomass of Cladophora, which in turn affects other invertebrates related to the filamentous algae, positively or negatively (Hart, 1992; © 1996 Blackwell Science Ltd, Freshwater Biology, 36, 631–646
A role for omnivorous crayfish 639 Table 6 Component loadings for percentage of total biomass of dominating macrophyte-associated invertebrate taxa in hand net samples found in twenty-one ponds with high alkalinity and twenty-one ponds with low alkalinity, and percentage of variance explained by the retained principal component axes. Important loadings are shown in bold type. P values refer to simple linear regression analyses of the number of crayfish caught per trap night (CPUE) in each pond against the scores of the different taxa Source
Fig. 6 Linear regression of the relationship between the number of crayfish caught per trap night (CPUE) and the number of macrophyte-associated invertebrate taxa in fortytwo ponds (pooled data from twenty-one ponds with high alkalinity and twenty-one ponds with low alkalinity).
Creed, 1994). Paine (1966) and Hall et al. (1970) found that top predators maintained a high species diversity at lower trophic levels by preventing competitive exclusion. In contrast, our results indicate that high crayfish abundance is associated with low numbers of macrophyte and invertebrate taxa. Herbivory and detritivory by crayfish populations may also have important long-term effects on succession in lakes and ponds.
Ponds with high alkalinity Variance explained Eigenvalues Invertebrate taxa Gastropoda Trichoptera Hirudinea Coleoptera Gammarus sp. Odonata Heteroptera Ephemeroptera Linear regression (P values)
PC1
PC2
PC3
20.42 1.63
14.22 1.14
0.91 –0.79 0.71 0.62 –0.54 –0.45 –0.12 0.05 0.0097
–0.14 0.03 0.03 –0.05 –0.72 0.71 –0.60 0.47 0.0018
0.13 0.18 0.13 0.18 0.16 0.26 –0.55 –0.80 0.88
36.71 2.20
20.43 1.23
0.87 –0.77 0.76 –0.11 0.19 0.46 ,0.0001
0.02 0.31 0.04 –0.84 –0.50 0.41 0.065
35.82 2.87
Macrophytes
Ponds with low alkalinity Variance explained Eigenvalues Invertebrate taxa Asellus aquaticus Odonata Trichoptera Heteroptera Coleoptera Gastropoda Linear regression (P values)
The negative relationship between crayfish abundance and both macrophyte coverage and total macrophyte abundance is likely to be an effect of crayfish grazing. Several investigations of other crayfish species have shown similar results in lakes (Magnuson et al., 1975; Lodge & Lorman, 1987) and in ponds (Abrahamsson, 1966; Ricket, 1974). The abundance of macrophytes increases in lakes and ponds that have lost their native crayfish species due to the crayfish plague (Abrahamsson, 1966; Matthews & Reynolds, 1992). Like Lodge & Lorman (1987), we found a decrease in macrophyte species richness with increasing crayfish abundance. Lodge et al. (1994) found twelve species of macrophytes in crayfish exclosures, whereas there were only three species left in cages with crayfish. Several experimental (e.g. Olsen et al., 1991; Lodge, 1991; Nystro¨m & Strand, 1996) and field studies (Dean, 1969; Lodge & Lorman, 1987; Hazlett et al., 1992) have shown that crayfish graze macrophytes selectively. In
general, submerged vegetation is more affected than robust emergents. Consequently, we expected the biomass of submerged macrophyte species to decline with increasing crayfish density. Although the results from the principal components analyses indicated differences in macrophyte species composition, and a decreased number of species in relation to crayfish density, there is no strong support for this hypothesis. In L ponds with dense populations of crayfish the dominant macrophyte was M. alterniflorum, whereas ponds with low crayfish densities were dominated by the floating- leafed Potamogeton natans, and the submerged E. canadensis or emergent species (Alisma plantago-aquatica and Sparganium emersum). Several studies have shown that crayfish consume Myriophyllum species (Flint & Goldman, 1975; Chambers et al., 1990). Since Myriophyllum species can survive and
© 1996 Blackwell Science Ltd, Freshwater Biology, 36, 631–646
640 P. Nystro¨m, C. Bro¨nmark and W. Grane´li
Fig. 8 Linear regression of the relationship between the number of crayfish caught per trap night (CPUE) and the component scores from the first principal component axes. The principal component axes reflects the percentage biomass of different invertebrate taxa from hand net samples in twentyone ponds with low alkalinity. Invertebrate taxa with important loadings on the axes are given.
Fig. 7 Linear regression of the relationship between the number of crayfish caught per trap night (CPUE) and the component scores from the first (a) and the second (b) principal component axes. The principal component axes reflect the percentage biomass of different invertebrate taxa from hand net samples in twenty-one ponds with high alkalinity. Invertebrate taxa with important loadings on the axes are given.
regenerate after grazing (Sculthorpe, 1971), they may be less sensitive to crayfish. We do not know which macrophyte species were present before the crayfish populations developed. Dense crayfish populations may inhibit establishment and growth even of sexually reproducing emergent species. Submerged juvenile plants of the emergent Scirpus lacustris and the floating-leafed species P. natans are readily eaten by the signal crayfish and by the noble crayfish (Astacus astacus L.) (Nystro¨m & Strand, 1996).
Fig. 9 Linear regression of the relationship between the number of crayfish caught per trap night (CPUE) and the percentage of organic content of the sediment (upper 10 cm) in forty-two ponds (pooled data from twenty-one ponds with high alkalinity and twenty-one ponds with low alkalinity). The regression line is calculated from arcsine-transformed data.
Invertebrates We expected that crayfish would have negative effects on macrophyte-associated invertebrates and invertebrates with weak escape reactions, both directly, by predation, and indirectly, by reducing habitat complexity. Both the total biomass and the number of invertebrate taxa in macrophytes decreased with increasing crayfish abundance. There was also a change in the species composition of the invertebrate © 1996 Blackwell Science Ltd, Freshwater Biology, 36, 631–646
A role for omnivorous crayfish 641 community. Gastropods were negatively related to crayfish abundance at both sites. Gastropod abundance and species richness have been shown to be related to the usable area of substratum and plant species (Lodge, 1985; Kershner & Lodge, 1990). However, several field and experimental studies (e.g. Lodge & Lorman, 1987; Hanson et al., 1990; Lodge et al., 1994) have suggested that crayfish are efficient predators on snails. In the H ponds we found that the percentage biomass of snails, leeches and the mussel Pisidium decreased with crayfish abundance. After the outbreak of crayfish plague, Abrahamsson (1966) observed an increase in the numbers of molluscs and leeches, and Matthews & Reynolds (1992) an increase in the total number of macrophyte-associated invertebrates, including A. aquaticus, Gammarus sp., Trichoptera and Pisidium. As we predicted, sediment-dwelling taxa, such as Sialis sp. and Chironomidae, dominated in ponds where crayfish were abundant. Macrophyte-associated invertebrate taxa were dominated by either mobile invertebrates (Gammarus sp. and Heteroptera) (H) or by Odonata (L). Although earlier studies have shown that Gammarus is readily eaten by crayfish (Skurdal et al., 1988; Hanson et al., 1990; P. Nystro¨m, unpublished), Gammarus might be more successful in escaping crayfish predation than less mobile prey. Abrahamsson (1966) observed that the invertebrate fauna in a pond with a dense population of the noble crayfish was characterized by a large number of active species. Lodge et al. (1994) suggested that although there was a decrease in the biomass of macrophytes, non-snail invertebrates may move quickly enough to escape crayfish predation. In laboratory experiments Reynolds (1978) found that Austropotamobius pallipes (Lereboullet) consumed most invertebrate taxa, except Corixidae, which dominated the biomass of Heteroptera in our ponds. The relationship with macrophyteassociated Trichoptera and Odonata in this study differed between the two sites. In H ponds with dense crayfish populations, the percentage of Trichoptera increased with crayfish density, whereas Odonata (mainly consisting of Anisoptera) decreased. In L ponds, Odonata (consisting mainly of Zygoptera) increased but there was a decline in Trichoptera with increasing crayfish abundance. In H ponds, the large sand-grain cases of larvae of Anabolia, the dominant trichopteran, may be difficult for crayfish to handle. However, in the L ponds Trichoptera consisted almost © 1996 Blackwell Science Ltd, Freshwater Biology, 36, 631–646
exclusively of the small genus Triaenodes, which use small pieces of fresh macrophytes as case-building material. There are probably several indirect effects on invertebrate biomass and species richness related to the loss of macrophytes. It has been shown that in lakes (Miller, Becket & Bacon, 1989; Blindow et al., 1993) and streams (Gregg & Rose, 1985) areas without vegetation have lower biomasses of invertebrates than those with macrophytes, and the permanence of the macrophyte stand can affect the invertebrate species composition (Hargeby, 1990). When crayfish were abundant, there was a reduction in the number of macrophyte taxa, and several invertebrate taxa are found more often on certain macrophytes (Rooke, 1984; Schramm, Jirka & Hoyer, 1987; Chilton, 1990). Mixed stands of macrophytes contain more invertebrate taxa and have greater densities than stands with few macrophyte taxa (Brown et al., 1988). The distribution and abundance of macrophyte-associated invertebrates are often positively related to the colonizable plant surface area and weed density (Dvorak & Best, 1982; Cyr & Downing, 1988; Becket, Aartila & Miller, 1992; Brown & Lodge, 1993). Crayfish predation efficiency might increase in less complex habitats. Although there are no other studies supporting the hypothesis that crayfish predation is a function of habitat complexity, Leber (1985) found that, with increasing microhabitat structural complexity, the effect of the predatory shrimp Penaeus duorarum (Burkenroad) on invertebrate prey decreased for several prey species. Since the distribution and abundance of invertebrates is influenced by the amount of leaf damage and the onset of decomposition (Smock & Stoneburner, 1980; Becket et al., 1992), and the organic content of the sediment (Cyr & Downing, 1988), the reduced amount of detritus in ponds with high crayfish densities might have influenced the invertebrate fauna. However, Huryn & Wallace (1987) suggested that in temperate woodland streams, collector-gatherers (such as Chironomidae) can indirectly benefit from the fact that crayfish convert slowly processed leaf litter to fine particles. In general, the results indicate that sedimentdwelling invertebrates (Chironomidae and Sialis sp.) dominate in ponds with dense crayfish populations. The macrophyte-associated invertebrate fauna in ponds with dense crayfish populations is dominated either by larger invertebrates (Odonata or Trichoptera with robust cases), or by mobile taxa (Gammarus and
642 P. Nystro¨m, C. Bro¨nmark and W. Grane´li Heteroptera). However, since this is a correlative study we have not determined the mechanisms behind observed patterns.
Detritus and periphytic algae Macrophytes are the primary source of littoral detritus in fresh waters (Wetzel, 1983). Macro-invertebrates are important in regulating detritus processing in streams and lakes, and a decrease in macro-invertebrate abundance can lead to an accumulation of organic matter (Wallace, Webster & Cuffney, 1982; Appelberg et al., 1993). However, in this study there was a decrease in the number of herbivorous/detritivorous invertebrates, and a decrease in the amount of organic matter in the sediments in ponds where crayfish were abundant. The decrease in the amount of organic matter in the sediment was probably due to crayfish detritivory, and indirectly to crayfish consumption of macrophytes. The signal crayfish (Mason, 1975) and other crayfish have a large proportion of detritus in their diet (Lund, 1944; Hessen & Skurdal, 1986; Skurdal et al., 1988); the annual litter processing by the crayfish Cambarus bartonii (Fabr.) in one stream ranged from 4 to 6% of the annual litter input (Huryn & Wallace, 1987). We could not find any effects of crayfish on periphytic algae. The numbers of periphyton grazers (mostly snails) decrease with increasing crayfish density, and periphytic algae are positively affected (Weber & Lodge, 1990; Lodge et al., 1994). Although both the proportion of snails and the total biomass of herbivores decreased with increasing crayfish abundance, periphytic algae appeared unaffected. Crayfish grazing on periphytic algae might counterbalance a food chainmediated indirect effect (Carpenter & Lodge, 1986). In Lake Tahoe periphytic algae were overgrazed at crayfish densities exceeding 203 g m–2 (approximately six adult crayfish m–2; Flint & Goldman, 1975).
Omnivorous crayfish and the trophic cascade model Cascading effects have often been demonstrated in freshwater benthic food chains (Power, 1990; Bro¨nmark et al., 1992; Martin et al., 1992; Bro¨nmark, 1994), but few studies have incorporated the influence of omnivorous crayfish (Lodge et al., 1994; Hill & Lodge, 1995). Predators that utilize resources from several lower trophic levels decouple the cascading effect (Polis & Holt, 1992). Trophic cascades are restricted to low-density
communities, influenced by one or few herbivore keystone species and with a low proportion of omnivores (Strong, 1992). Assuming that the food chain in the crayfish ponds has four trophic levels, crayfish (top consumer), predatory invertebrates (intermediate consumers), invertebrate prey (consumers), and primary producers (macrophytes and periphytic algae) and detritus at the lowest level (resources), the trophic cascade model predicts that the effect of the top predator (crayfish) should alternate down through lower trophic levels. In L ponds, crayfish abundance was inversely related to the biomass of predatory invertebrates, herbivorous/detritivorous invertebrates, macrophytes and detritus, but the amount of periphyton was not affected. In H ponds the results were similar, except that there was no relationship with the intermediate consumers. Thus, our results do not support the traditional trophic cascade model at either of the two sites. Our results support the Menge & Sutherland (1987) model, which predicts that omnivory increases connectance and predator control of the community at lower trophic levels. Hill & Lodge (1995) found, in an experiment, that crayfish directly affected more than one trophic level (detritivorous/herbivorous macro-invertebrates and macrophytes). Bowlby & Roff (1986) argued that omnivory (fish feeding on both predatory and non-predatory invertebrates) could explain why their studied stream food web did not respond by being alternately food and predator limited down the food chain. In his review, Diehl (1993b) found that when size differences between omnivorous top consumers and intermediate consumers were large, top consumers usually had a strong, direct impact on the abundance of intermediate consumers, and an intermediate to strong, direct negative effect on the lowest level (resources). In conclusion, our results indicate that the signal crayfish plays an important role as a keystone consumer in pond ecosystems, by directly and indirectly affecting the biomass and species composition of macrophytes and invertebrates, but also by affecting the amount of organic matter in the sediment. The presence of omnivorous crayfish in these ponds for several years may have caused direct and indirect ‘top-down’ effects, but the lower trophic levels did not respond to changes in the abundance of crayfish according to the trophic cascade model. Our results are probably also relevant for abundant crayfish populations in the © 1996 Blackwell Science Ltd, Freshwater Biology, 36, 631–646
A role for omnivorous crayfish 643 littoral zones of lakes. However, in the presence of predatory fish, crayfish activity might decrease (Blake & Hart, 1993; Garvey, Stein & Thomas, 1994) resulting in decreased food consumption (e.g. Stein & Magnuson, 1976; Hill & Lodge, 1995). Since the results obtained in this study are based on correlative observations, experimental studies are needed to determine the mechanisms behind observed patterns.
Acknowledgments This investigation was financed by the Swedish Environmental Protection Agency (grant no. 13414 to Wilhelm Grane´li). We are grateful to Simontorp Aquaculture AB for letting us use the ponds and for the use of earlier data on crayfish catches. We are also very grateful to Måns Denward, Anna Axelsson and Kajsa Åbjo¨rnsson for assistance in the field.
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