Freshwater Biology (2003) 48, 636â€“648
Zooplankton responses to predation by larval bluegill: an enclosure experiment J. E. RETTIG W.K.Kellogg Biological Station, Michigan State University, MI, U.S.A.
SU M M A R Y 1. Larval fish are gape-limited predators that forage on prey of specific sizes, and thus may be expected to differentially affect members of a zooplankton community, possibly altering the size-structure or species composition. 2. I used an enclosure experiment to look at the effect of predation by larval bluegill on the dynamics of two zooplankton communities, one dominated by large-bodied individuals and the other by small-bodied individuals. Enclosures containing these zooplankton received a zero, low, medium, or high density of larval bluegill predators. 3. Increasing larval density had a negative effect on zooplankton abundance and abundance declined similarly in the large-bodied and small-bodied communities. 4. Zooplankton size-structure, as estimated by the length of the average zooplankton, increased and then decreased during the experiment, decreasing faster at higher larval fish densities. When zooplankton size-structure was estimated as the length of the average cladoceran, size-structure declined in the large-bodied but not in the small-bodied community and the greatest decline in size-structure was seen in the medium and high larval density treatments. 5. Ordination of each community using multidimensional scaling (MDS) indicated that the trajectory of change in species composition differed between the presence and absence of larval fish. In both communities, the degree of response by individual taxa depended on the density of bluegill larvae. This effect on zooplankton abundance, size-structure and community composition suggests that larval fish may make an important contribution to zooplankton dynamics in many lakes and ponds. Keywords: community composition, larval fish, Lepomis, multidimensional scaling, zooplankton sizestructure
Introduction Zooplankton communities are complex assemblages of species under the influence of several biotic forces, including competition and predation from invertebrates and vertebrates. Numerous studies have examined how predation can alter the species composition or size structure of zooplankton communities. As is well known, adult fish tend to consume large zooplankton in lakes and ponds, often leading to Correspondence: Jessica E. Rettig, Department of Biology, Denison University, Granville, OH 43023, U.S.A. E-mail: firstname.lastname@example.org
an increase in the density of small individuals or species (Brooks & Dodson, 1965; Hall et al., 1976; Gliwicz & Pijanowska, 1989; WahlstroÂ¨m et al., 2000). For example, experimental manipulations of fish have shown that larger zooplankton taxa (Chaoborus, Daphnia) decline, and that zooplankton shift from largebodied taxa to small-bodied taxa in the presence of adult fish (Lynch, 1979), thus altering both species composition and community size-structure. While many studies have focused on the effects of adult zooplanktivores, far fewer have addressed the effect of foraging by larval fish. As with adults, larval foraging may affect the zooplankton community by altering zooplankton abundance (e.g. Dettmers & 2003 Blackwell Publishing Ltd
Zooplankton responses to larval predation 637 Stein, 1992; Garvey & Stein, 1998), species composition (e.g. Cryer, Peirson & Townsend, 1986), or community size-structure (e.g. Qin & Culver, 1996; Romare, Bergman & Hansson, 1999). Although an individual fish larva may not consume enough prey to lead to a change in the zooplankton community, ponds and lakes can contain larvae whose combined foraging may impact the zooplankton community (e.g. van Densen & Vijverberg, 1982). For instance, Mills & Forneyâ€™s (1983) classic study on Oneida Lake showed how the abundance of Daphnia was negatively affected in years with high densities of larval perch. Such studies show that larval fish can have important effects upon a zooplankton community, but whether these effects occur in all systems is unclear. To begin to explore if larval effects on zooplankton communities apply to a diversity of aquatic systems, I used an experimental approach to compare the responses of two communities to foraging by a larval fish common to many aquatic systems in North America, the bluegill sunfish. In eastern and midwestern North America, bluegill sunfish are often dominant members of fish assemblages in ponds and lakes (Werner et al., 1977; Werner, Hall & Werner, 1978). Larval bluegill forage on zooplankton in the limnetic zone for several weeks during the summer (Werner, 1967, 1969; Rettig, 1998). Like many larval fish, bluegill are gape-limited predators able to consume only prey small enough to enter their mouths (Bremigan & Stein, 1994). This sizeselective foraging may play an important role in influencing the abundance, size, and species composition of zooplankton. For example, predation by larvae on small individuals or small-bodied taxa could shift the zooplankton community towards being dominated by larger individuals or larger taxa. However, as larval fish grow they may be able to consume larger zooplankton, possibly shifting the community towards smaller individuals or taxa. The ability of larval bluegill to change zooplankton community composition or size-structure may also depend on their abundance, with stronger effects of larvae when larvae are more abundant. Although larval fish can be patchy in their distribution (Davis, Jenkins & Young, 1990; Frank, Carscadden & Leggett, 1993; Post, Rudstam & Schael, 1995), high abundance within patches may have a substantial effect on zooplankton. To examine the effect of predation by larval fish on zooplankton community dynamics, I conducted an 2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 636â€“648
experiment that manipulated the density of larval bluegill foraging on either a large- or small-bodied zooplankton community. I chose to compare these two types of zooplankton communities because many lakes tend to show contrasting patterns in zooplankton size-structure, containing either many largebodied or many small-bodied zooplankton (e.g. Brooks & Dodson, 1965; Stein et al., 1988; McQueen et al., 1989; Tessier & Woodruff, 2002), yet bluegill are found in each lake type. I hypothesized that in both communities larval predation would lead to a decrease in zooplankton abundance and to an increase in mean size, because larvae would be limited to feeding on smaller individuals or species of zooplankton. Composition of each community was also predicted to change, as predation reduced the abundance of taxa of particular sizes in each community. Finally, I expected to observe a stronger effect of larvae on the zooplankton in treatments with higher densities of larvae.
Methods The experiment consisted of a 2 Âˇ 4 factorial design with two zooplankton communities and four levels of larval bluegill density. On July 7, 1995, I deployed 24 polyethylene bag enclosures into a 29-m diameter, 1.9-m-deep pond at the W.K. Kellogg Biological Station. Each enclosure was filled with pond water filtered through an 80-lm mesh net to remove zooplankton. Mean depth of the filled enclosures was 1.6 m and each enclosure contained about 1250 L. A mosquito netting cover on each enclosure prevented oviposition by aquatic insects such as Chaoborus, the larvae of which also prey on zooplankton. The eight experimental treatments were randomly assigned within each of the three rows of enclosures so that the rows could serve as experimental blocks. The large-bodied zooplankton community was collected from the epilimnion of Lawrence Lake, Kalamazoo County, Michigan. This zooplankton assemblage was dominated by two large-bodied Daphnia species, D. pulicaria and D. galeata mendotae (Table 1). I collected the small-bodied zooplankton community from nearby Lower Crooked Lake. This community was dominated by small-bodied species like Ceriodaphnia sp., Simocephalus sp. and Bosmina sp. (Table 1). Zooplankton were stocked into the enclosures at natural densities and left to acclimate for 36 h.
J.E. Rettig Small-bodied community
D. pulicaria D. galeata Diaphanosoma sp. Ceriodaphnia sp. Simocephalus sp. Chydorus sp. Bosmina sp. Copepod adults Copepod nauplii Keratella sp.
0.983 0.865 0.498 0.514 0.428 0.268 0.277 0.602 0.218 0.121
± ± ± ± ± ± ± ± ± ±
Density 0.159 0.169 0.033 0.016 0.320 0.011 0.007 0.029 0.011 0.002
0.033 0.351 0.218 2.515 1.728 0.291 0.669 6.156 21.17 62.34
± ± ± ± ± ± ± ± ± ±
0.021 0.070 0.113 0.332 0.503 0.690 0.102 0.612 1.577 4.834
1.410 1.240 0.487 0.503 0.486 0.224 0.234 0.602 0.210 0.119
± ± ± ± ± ± ± ± ± ±
Initial zooplankton densities in the enclosures were at the high end of the range of zooplankton densities found in local lakes (16–80 ind. L)1, Rettig, 1999). Initial density of zooplankton did not differ between the large-bodied and small-bodied communities (Mean ± 1 SE ¼ 92.8 ± 8.9 ind. L)1 versus 95.8 ± 4.3 ind. L)1, respectively; 2-factor A N O V A : F1,16 ¼ 0.513, P ¼ 0.48). Zooplankton density also did not differ among enclosures into which different densities of larval bluegill were stocked (two-factor A N O V A : F3,16 ¼ 1.73, P ¼ 0.20). The average individual in the large-bodied zooplankton community at the start of the experiment was significantly larger than the average individual in the small-bodied zooplankton community (0.236 ± 0.013 mm versus 0.195 ± 0.007 mm, respectively; 2-factor A N O V A : F1,16 ¼ 10.24; P ¼ 0.006). This difference in body size is more apparent when considering the length of the average cladoceran, which in the large-bodied community was about 2.5 times larger than in the small-bodied community (1.21 ± 0.05 mm versus 0.47 ± 0.01 mm, respectively). Prior to the addition of larval bluegill, I sampled each enclosure using a Knoechel & Campbell (1992) integrated tube sampler fitted with an 80-lm net. Although this mesh size is too coarse to adequately sample small rotifers, the proportion of rotifers passing through the net should not differ among treatments. Approximately 1% of the total water volume was collected with each sample and zooplankton were preserved 4% sucrose formalin. Larvae for the experiment were collected when they were non-swimming fry from two bluegill nests in Palmatier Lake and reared in aquaria filled with filtered pond water. At swim-up, larvae consumed a diet of rotifers and brineshrimp nauplii. On July 14, I stocked bluegill larvae (mean standard
Density 0.036 0.032 0.033 0.053 0.022 0.018 0.028 0.026 0.011 0.001
1.847 2.171 0.854 0.060 0.073 0.026 0.026 7.830 18.99 60.76
± ± ± ± ± ± ± ± ± ±
0.341 0.340 0.783 0.024 0.041 0.015 0.015 1.936 4.369 8.819
Table 1 Species present in the enclosures prior to the addition of larval bluegill. Mean (±1 SE) length given in mm and mean (±1 SE) density given in number per litre (n ¼ 12 enclosures)
length ¼ 7.53 ± 0.10 mm, mass ¼ 4.0 ± 0.22 mg) into enclosures at zero, low (six fish; 4.8 m)3), medium (12 fish; 9.6 m)3) and high (24 fish; 19.2 m)3) densities. The low-density treatment was well within the natural range of larval density observed in nearby lakes and the medium- and high-density treatments were somewhat higher than the natural range (Rettig, 1999). As lake-wide density estimates are at best underestimates of actual larval density because of limitations of sampling gear, the larval densities used in this experiment were reasonable and were in the range of larval density expected within patches in lakes. The experiment was carried out for 25 days with periodic sampling of zooplankton by collecting a single sample in each enclosure using the integrated tube sampler with an 80-lm net. Zooplankton samples were processed by identifying and counting all cladoceran, copepod and rotifer taxa to provide estimates of zooplankton density (ind. L)1). In each sample, body length (minus spines) on up to 50 individuals per taxa was recorded using a computerbased digitizer and microscope (Sigma Scan; SPSS, Chicago, IL, USA). I examined the effect of larvae on zooplankton size-structure by calculating the length of an average individual zooplankton as, n P
ðLi Di Þ
i¼1 n P
where Li is the mean length of species i in a sample and Di is the density of species i in that sample. As the zooplankton communities contained an abundance of very small taxa, like Keratella rotifers and copepod nauplii (Table 1), zooplankton size-structure was also 2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 636–648
Zooplankton responses to larval predation 639 analysed by focusing solely on cladocerans, calculating the length of the average cladoceran using the above formula (ignoring rotifer and copepod taxa). These measures provide an estimate of the length of the average zooplankton (or cladoceran), weighted by the density of each taxa in the enclosure. I used these estimates of size-structure as a dependent variable in a repeated-measures A N O V A (RMA). In these analyses, the final sampling date was not included in the RMA because zooplankton abundance in the high larval density treatment at the end of the experiment had dropped to <3% of their initial density, providing inadequate numbers of individuals for length estimates. To examine the impact of larval predation on the species composition, I used a community-level approach involving the ordination of the large-bodied and small-bodied zooplankton communities. These communities contained up to 29 different species during the course of the experiment. Many of these species were very rare, occurring with <10 individuals per enclosure on the majority of sample dates and thus were removed from the ordination data set. Of the remaining species, adult cyclopod and calanoid copepods were pooled as were Keratella quadrata and Keratella cochlearis, yielding 10 taxa for ordination (Table 1). I used a two-dimensional, non-metric multidimensional scaling (MDS) procedure to ordinate the densities of the 10 taxa on the four sampling dates (Schiffman, Reynolds & Young, 1981; Kenkel & Orloci, 1986; Clark, 1993). Multidimensional scaling was used because it makes few assumptions about the distribution of species included in the ordination, and the MSD axes coordinates (i.e. Dim 1 and Dim 2 below) are linear and orthogonal, allowing variance partitioning techniques such as A N O V A , A N C O V A and M A N O V A to be applied to them (e.g. Kenkel & Orloci, 1986; Costa & Magnusson, 2002; Legendre & Anderson, 1999). MDS analysis was performed on the standardised euclidean distance matrix of the log10(x + 1) transformed densities in order to standardise the variance and correct for density differences between small and large species. Correlations of the two MDS dimensions (Dim 1 and Dim 2) with the taxa in each community were used to assist in interpreting the two MDS dimensions produced in each analysis (e.g. Tessier & Welser, 1991). For each community, a repeated-measures A N O V A on the two dimensions was next run to see if larval treatments or time 2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 636–648
interactions contributed to patterns of zooplankton community change. When an RMA indicated a significant larval density · time interaction, I then examined patterns of change for taxa that were highly correlated with the MDS dimensions by running RMAs on these taxa. I conducted statistical analyses using Systat 7.0 (SPSS, Chicago, IL, USA) and Statview (SAS, Cary, NC, USA). For all A N O V A the model assumptions were examined for normality, tested for homogeneity of variance, and data were transformed if needed, to meet these assumptions. Initial analyses were run with blocking, but in all cases, blocking was removed from the final statistical models because it had no significant effect. For each RMA, the Greenhouse–Geisser adjustment of P-values was used as a conservative estimate of probability to compensate for a possible minor violation of the assumption of sphericity.
Results Zooplankton abundance and size-structure Average zooplankton density declined dramatically over the course of the experiment (Fig. 1, RMA: Time effect, F3,48 ¼ 38.167, P ¼ 0.001). Predation by larval bluegill had a significant effect on zooplankton
Fig. 1 Mean (±1 SE) zooplankton density (ind. L)1) in the enclosures on each of four sampling dates. Data shown on plots are not transformed; n ¼ 6 for each point on the plot.
Fig. 2 Mean (±1 SE) length (mm) of an average zooplankton on each of four sampling dates showing the larval density · time interaction from the repeated-measures A N O V A ; n ¼ 6 for each point on the plot. Data shown on plots are not transformed.
density with the greatest decline occurring in the high larval bluegill density treatment, and the least in the zero-larvae treatment (Fig. 1, RMA: time · larval density effect, F9,48 ¼ 2.618, P ¼ 0.02). Zooplankton declined in a similar manner in both communities (i.e. no time · zooplankton community effect), but over the course of the experiment the small-bodied community had a significantly more individuals (68.18 ± 4.16 ind. L)1) than the large-bodied community
(55.85 ± 4.34 ind. L)1) (RMA: Zooplankton Community effect, F1,16 ¼ 8.864, P ¼ 0.009). Zooplankton size-structure, as measured by the average zooplankton length, first increased and then decreased during the experiment (Fig. 2, RMA: time effect, F3,48 ¼ 48.548, P ¼ 0.001). The pattern of change differed significantly among larval density treatments (Fig. 2, RMA: time · larval density effect, F3,48 ¼ 6.919, P ¼ 0.0001), with zooplankton length decreasing sooner for the high and medium larval density treatments. I also found a significant difference through time among the eight larval density · zooplankton community combinations (Fig. 3, RMA: time · zooplankton community · larval density effect, F9,48 ¼ 2.593, P ¼ 0.03), indicating the independence of the size-structure trajectory followed by each treatment. For all treatments in both communities, mean zooplankton length increased and then decreased, although the timing and strength of this size change differed among treatments (Fig. 3). Finally, the change in mean length did not differ between the two zooplankton communities (RMA: time · zooplankton community effect, F3,48 ¼ 0.788, P ¼ 0.475), although the average zooplankton in the large-bodied community was bigger than that in the small-bodied community (0.293 ± 0.07 versus 0.255 ± 0.07 mm, respectively. RMA: Zooplankton Community effect, F1,16 ¼ 11.86, P ¼ 0.003).
Fig. 3 Mean (±1 SE) length (mm) of an average zooplankton on each of four sampling dates showing the zooplankton community · larval density · time interaction from the repeated-measures A N O V A . Results are split into plots of small-bodied (left) and large-bodied (right) zooplankton communities for clarity; n ¼ 3 for each point on a plot. Data shown on plots are not transformed. 2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 636–648
Zooplankton responses to larval predation 641 Zooplankton size-structure, as measured by the average cladoceran length, also changed during the course of the experiment (RMA: time effect, F3,48 ¼ 5.342, P ¼ 0.009). I found that the length of the average cladoceran declined in the large-bodied zooplankton community, but did not change in the small-bodied community (Fig. 4a, RMA: time · zooplankton community effect, F3,48 ¼ 7.577, P ¼ 0.002). The size of the average cladoceran declined through time in the medium and high larval density treatments but did not change for the zero and lowdensity treatments (Fig. 4b, RMA: time · larval density effect, F3,48 ¼ 2.428, P ¼ 0.044).
Zooplankton community composition I examined changes in zooplankton community structure using ordination with multidimensional scaling (MDS). Ordination with MDS on the large-bodied
Fig. 4 Mean (±1 SE) length (mm) of an average cladoceran on each of four sampling dates. (a) Zooplankton community · time interaction from the repeated-measures A N O V A (RMA); n ¼ 12 for each point on the plot. (B) Larval density · time interaction from the RMA; n ¼ 6 for each point on the plot. Data shown on plots are not transformed. 2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 636–648
zooplankton enclosures explained 97% of the variation in taxa density in two dimensions. Dimension 1 represented an assemblage gradient from low Keratella with high copepod nauplii and copepod adult densities to high Keratella with low copepod nauplii and adult densities (Table 2). An RMA on dimension 1 of the community showed a significant time · larval density interaction (Table 3). Specifically, later in the experiment, medium and high treatments had higher densities of Keratella with lower densities of copepod nauplii and adults compared with the zero and low treatments (Fig. 5a). Dimension 2 represented an assemblage gradient from low Daphnia species with high Diaphanosoma, Chydorus and Bosmina densities to high Daphnia with low Diaphanosoma, Chydorus and Bosmina densities (Table 2). An RMA on dimension 2 also showed a significant time · larval density interaction (Table 3), such that treatments with larval bluegill developed lower densities of Daphnia with higher densities of Diaphanosoma, Chydorus and Bosmina later in the experiment compared with the zerolarvae treatment (Fig. 5b). These analyses show that in a large-bodied zooplankton community, assemblages with bluegill larvae change through time differently than assemblages without larvae. This pattern was evident by examining taxa highly correlated with dimensions 1 or 2 from the large-bodied zooplankton community [i.e. taxa with double asterisks (**) on Table 2] Over time, increasing larval bluegill density had a negative effect on the densities of D. pulicaria (Fig. 6a, RMA: time · larval density interaction: F9,24 ¼ 2.518; P ¼ 0.03) and D. galeata (Fig. 6b, RMA: time · larval density interaction; F9,24 ¼ 3.520; P ¼ 0.007). For copepod nauplii, there was a trend towards increased density through time in the zero-larvae treatment (Fig. 6c, RMA: time · larval density interaction: F9,24 ¼ 2.116; P ¼ 0.07), such that at the end of the experiment, nauplii were twice as abundant in enclosures without larvae compared with enclosures with larvae. Keratella declined in all enclosures, but this decline in abundance occurred sooner in the enclosure with no larvae (Fig. 6d, RMA: time · larval density interaction: F9,24 ¼ 5.087; P ¼ 0.0007). Ordination with MDS on the small-bodied zooplankton communities explained 93% of the variation in taxa density in two dimensions. Dimension 1 represented an assemblage gradient from low Keratella with high Daphnia, Diaphanosoma, Bosmina, and
J.E. Rettig Large-bodied zooplankton community
Small-bodied zooplankton community
D. pulicaria D. galeata Diaphanosoma Ceriodaphnia Simocephalus Chydorus Bosmina Copepod adults Copepod nauplii Keratella
)0.171 )0.182 )0.205 0.005 )0.078 )0.282 )0.037 )0.392* )0.599** 0.899**
0.501** 0.757** )0.406* )0.030 )0.027 )0.343* )0.296* 0.030 0.043 0.108
)0.424** )0.610** )0.561** )0.391* )0.086 0.133 )0.584** )0.552** )0.556** 0.798**
0.123 )0.347* 0.186 )0.810** )0.397* )0.183 )0.006 )0.098 0.202 )0.104
Table 2 Results of the correlation of the first two dimensions from the multidimensional scaling analysis (MDS) with the density of the zooplankton taxa for four sample dates during the experiment. Correlation coefficients are given for large-bodied zooplankton communities (left) and small-bodied zooplankton communities (right)
Values significant at the a £ 0.05 level are designated by asterisk (*). Values significant at a £ 0.0025 (a ¼ 0.05 ⁄ 20) are designated by double asterisks (**).
Dimension 1 Source
Dimension 2 F
Taxa density: large-bodied zooplankton community Between subjects Density 3 3.780 7.808* Error 8 0.484 Within subject Time 3 5.070 46.037** Time · density 9 0.868 7.879** Error 24 0.110 Taxa density: small-bodied zooplankton community Between subjects Density 3 4.178 24.137** Error 8 0.173 Within subject Time 3 1.881 11.763** Time · density 9 0.728 4.554* Error 24 0.160
Table 3 Results of the repeated-measures for the first two dimensions of the MDS analysis on taxa density in the largebodied (top) and small-bodied zooplankton community (bottom) ANOVA
3 9 24
0.471 0.245 0.086
3 9 24
4.110 0.139 0.099
Values significant at the a £ 0.05 level are designated by asterisk (*). Values significant at a £ 0.001 are designated by double asterisk (**).
nauplii and adult copepod densities, to high Keratella with low Daphnia, Diaphanosoma, Bosmina, and nauplii and adult copepod densities (Table 2). An RMA on dimension 1 showed a significant time · larval density interaction (Table 3) such that the assemblage did not change through time for the high-density treatment and it changed most rapidly for the zero-larvae treatment (Fig. 7). Dimension 2 represented an assemblage gradient from high Ceriodaphnia, D. galeata and Simocephalus to low Ceriodaphnia, D. galeata, and Simocephalus (Table 2). An RMA on dimension 2 showed that the pattern of assemblage change through time did not differ among treatments, nor
did the treatments overall differ in their assemblage structure (Table 3). These analyses show that in a small-bodied zooplankton community, zooplankton assemblages respond differently through time depending on the density of larval bluegill. The pattern of assemblage change in the small-bodied zooplankton community was evident for the taxa highly correlated with dimension 1 [i.e. taxa with double asterisks (**) on Table 2]. Over time, treatments with medium and high-larval densities had a negative effect on the density of D. galeata (Fig. 8a, RMA: time · larval density interaction; F9,24 ¼ 4.082; P ¼ 0.003). 2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 636–648
Zooplankton responses to larval predation 643 Increasing larval density also had a negative effect on Bosmina density (Fig. 8b, RMA: time · larval density interaction; F9,24 ¼ 2.869; P ¼ 0.019). Copepod nauplii declined in the high larval density treatment but were relatively unchanged in the other treatments (Fig. 8c, RMA: time · larval density interaction; F9,24 ¼ 2.076; P ¼ 0.01). Among the four larval treatments, the density of the other taxa did not differ through time.
Fig. 5 Mean (±1 SE; n ¼ 3) dimension 1 (a) and dimension 2 (b) of the large-bodied zooplankton community taxa densities plotted over four sample dates. Plots show the larval density · time interaction from the repeated-measures A N O V A . Taxa that are significantly correlated with each dimension are listed to the right of each plot.
Fig. 6 Mean (±1 SE; n ¼ 3) density of taxa that are highly correlated with dimension 1 or dimension 2 of the large-bodied zooplankton communities: (a) D. pulicaria (b) D. galeata (c) copepod nauplii and (d) Keratella. Densities (ind. L)1) are plotted over four dates to show the larval density · time interaction from the repeated-measures A N O V A on the transformed densities. 2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 636–648
Predation by bluegill larvae strongly influenced both large-bodied and small-bodied zooplankton communities, affecting abundance, size-structure and species composition. In both communities, zooplankton density declined with increasing larval density. Negative effects of larval or age-0 fish on zooplankton abundance have been documented in both experimental and natural systems (Garvey & Stein, 1998; Bystro¨m & Garcia-Berthou, 1999; Romare, Bergman & Hansson, 1999), so this outcome of the experiment is not unusual. Interestingly, in both communities, average zooplankton length and average cladoceran length, both measures of size-structure, also were affected by larval predation such that increasing larval density resulted in more rapid declines in mean length. Density effects of larval fish on zooplankton sizestructure have also been seen for European perch
Fig. 7 Mean (±1 SE; n ¼ 3) dimension 1 of the small zooplankton community taxa densities plotted over four sample dates. Plots show the larval density · time interaction from a repeated-measures A N O V A . Taxa that are significantly correlated with each dimension are listed to the right of each plot.
(Romare et al., 1999), yellow perch (Mills & Forney, 1983) and gizzard shad (Kim & DeVries, 2000). In this experiment, the increase followed by a decrease in mean zooplankton length suggests that larval bluegill fed on smaller prey earlier in the experiment and later fed on larger prey. Such a feeding pattern would mean that larval bluegill were gape-limited early in the experiment and were less gape-limited later. This hypothesis is supported by data on average cladoceran length from the largebodied zooplankton community, which showed a dramatic decline in size as the experiment progressed, while no size decline occurred in the small-bodied community. This change in cladoceran body size supports the idea that larger zooplankton were consumed later in the study. In this experiment, larval fish grew in both communities throughout the study to reach a mean final length of 16.19 ± 0.68 mm and mass of 115.84 ± 17.35 mg (Rettig, 1999). Thus, large zooplankton were consumed at the end of the experiment when larval bluegill were biggest. In a recent review, Mehner & Thiel (1999) found that small and large larval fishes had a relatively minor effect on small-bodied taxa, but that larger larvae could have a negative effect on populations of large cladocerans. An alternative explanation for this change in sizestructure is that the presence of larval fish caused a series of indirect effects within the zooplankton community, in addition to their direct effect of consuming zooplankton, to yield the change in zooplankton size-structure. While this enclosure experiment was not designed to explore indirect effects, and it is possible that indirect effects occurred, the response of specific taxa to the larval density
treatments (see below) does indicate a very strong effect of larvae. My experiment suggests that the focus of larval predation changed through time as the bluegill grew, with larvae initially consuming smaller prey and later consuming larger zooplankton. Changes in size-structure seen in this experiment appear linked to larval effects on species composition. Multi-dimensional scaling showed that most of the variation in the zooplankton community was attributable to changes in the abundance of a few key taxa. Daphnia pulicaria, D. galeata, nauplii and Keratella densities underwent major changes in the largebodied zooplankton community, while D. galeata, Bosmina and nauplii densities underwent major changes in the small-bodied zooplankton community. Often MDS revealed contrasting patterns between larger and smaller taxa, such as large Daphnia abundance falling as the abundance of smaller taxa like Chydorus and Bosmina rose in the large-bodied community. Changes in community composition also often depended on larval density (Figs 4 and 6), with the high-larvae and zero-larvae treatments displaying the two extremes of difference in composition. In many cases the treatments with larvae, regardless of density, responded differently than the zero-larvae treatment to produce distinctly different zooplankton assemblages. Foraging studies of larval bluegill have produced variable results as to which prey types are preferred or avoided. Miner & Stein’s (1993) feeding trials on larval bluegill (mean size 12.5 mm TL) indicated a preference for cyclopoids and Diaphanosoma, and avoidance of Bosmina, Ceriodaphnia and Daphnia parvula. Feeding experiments by Bremigan & Stein (1994) 2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 636–648
Zooplankton responses to larval predation 645
Fig. 8 Mean (±1 SE; n ¼ 3) density of taxa that are highly correlated with dimension 1 of the small-bodied zooplankton community: (a) D. galeata, (b) Bosmina and (c) copepod nauplii. Densities (ind. L)1) are plotted over four dates to show the larval density · time interaction from the repeated-measures A N O V A on the transformed data. 2003 Blackwell Publishing Ltd, Freshwater Biology, 48, 636–648
indicated a preference for Ceriodaphnia, Daphnia magna and copepods by bluegill ranging in size from 10 to 26 mm TL. These differences in prey preference may be linked to the zooplankton used in each experiment or to the size of larvae used in the feeding trials. For instance, Bremigan & Stein (1994) used zooplankton collected by a 180-lm net, effectively excluding nauplii, rotifers and some smaller cladocerans. In this study, I attempted to mimic actual lake distributions of a wide range of zooplankton and found that some taxa in large- and small-bodied zooplankton communities can be differentially affected by larval bluegill, while other taxa respond similarly in the two communities (e.g. Daphnia declined in both). Thus, feeding trials with larval fish may not be sufficient predictors of larval effects in different types of zooplankton communities. While bluegill larvae changed zooplankton communities in this experiment, the specifics of how they will alter zooplankton communities in lakes warrants further study. In this experiment, the strongest effects of larvae on zooplankton occurred at high larval densities. However, even the low-density treatment produced negative effects on mean zooplankton density and on the density of specific taxa, such as D. pulicaria, D. galeata and copepod nauplii in the large-bodied community and Bosmina and nauplii in the small-bodied community. Such responses indicate that low or high larval bluegill abundance will likely affect communities in lakes, although responses by zooplankton will be stronger in the presence of higher larval densities. The general question of the ability of larval fish to affect zooplankton has received more attention in marine than in freshwater systems. Studies of marine systems indicate that larval fish of most species probably do not occur at high-enough densities to affect zooplankton prey (Pepin & Penney, 2000), although as larvae grow their affect upon the prey community increases (Cushing, 1983). Larval fish do occur in high-density aggregations in some marine and freshwater systems (Davis et al., 1990; Post et al., 1995) and thus have the potential to strongly influence their zooplankton prey. In shallow lakes for instance, larval fish have reached densities that led to declines in zooplankton abundance (Dettmers & Stein, 1992). It has also been suggested that synchronous spawning of one or more species could produce pulses of larval fish which would have an impact on the zooplankton community of a lake (DeVries & Stein, 1992).
Given their patchy distribution in lakes, larval bluegill have the potential to reach densities that influence zooplankton abundance, composition, or size-structure, but no field studies have directly examined this issue. Welker, Pierce & Wahl (1994) found with field surveys that zooplankton abundance remained low when bluegill larvae were present, but the initial decline in zooplankton was caused by larval gizzard shad which arrived in the limnetic zone prior to the bluegill. For other species, the potential impact of larvae on zooplankton is variable. Increases in the density of larval walleye shifted the zooplankton community from large-bodied to small-bodied taxa in ponds (Qin & Culver, 1996). An enclosure study with larval golden perch found that, late in the experiment, Daphnia and calanoid copepod densities declined in the presence of larvae (Arumugam & Geddes, 1996). In lake studies, high abundance of roach fry caused the summer zooplankton community to be dominated by copepods and rotifers, instead of cladocerans, and the size of cladocerans declined (Cryer, Peirson & Townsend, 1986). In contrast, Mehner et al. (1997) found that age-0 fish (perch, zander, ruffe, roach and bream) did not appear to control Daphnia densities, but speculated that later in the summer these young fish might depress Daphnia populations. Larval bluegill live in lakes with zooplankton communities that span a range in size structure and species composition. This study suggests that in lakes with small- or large-bodied zooplankton communities, all densities of larvae, but particularly higher densities, may dramatically reduce overall zooplankton abundance if patches of larval bluegill reach adequate densities or if pulses of adult reproduction lead to peaks in larval density during the summer. In lakes in S.W. Michigan, bluegill nesting colonies can be active several times during the summer with most nests containing larvae during each spawning period (J.E. Rettig, personal observation), thus several pulses of larvae may enter the limnetic zone during the summer. Large- or small-bodied zooplankton communities may also change as particular species are consumed by bluegill larvae. Such predation can reduce the density of selected sizes of prey, such as large Daphnia, and alter the composition and sizestructure of a zooplankton community. Pulses of larval bluegill production therefore have the potential to be an important predatory force in lakes containing
small- or large-bodied zooplankton if larvae born during a nesting period successfully migrate to the limnetic zone and feed on zooplankton. For species other than bluegill, the response of zooplankton to larvae also will likely depend on the abundance of larvae and on the foraging strategy of the larvae, with gape-limited larvae causing a different response than non-gape-limited larvae.
Acknowledgments L. Smiley and K. Maki helped build the enclosures. G. Smith, G. Mittelbach, L. Smiley and A. Tessier provided helpful comments on earlier versions of this manuscript or on the statistics. This research was supported by a NSF Dissertation Improvement grant (DEB 9520840) to the author and G. Mittelbach and by the KBS Graduate Research Training Group (RTG) funded by NSF grants DIR-09113598 and DBI9602252. This is KBS contribution number 990.
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