Lucania parva, held in combination with an omnivorous grass shrimpâPalaemonetes pugio, and a predatory diving beetleâTropisternus lateralis, were ...
Journal of Fish Biology (1996) 48, 120–130
The effects of species manipulation on growth and survival of an assemblage of juvenile estuarine fish W. A. D C. L. R* Department of Biology, Pennsylvania State University, 208 Mueller Laboratory, University Park, Pennsylvania 16802, U.S.A. (Received 30 May 1994, Accepted 19 March 1995) Growth and survival of Cyprinodon variegatus, Fundulus heteroclitus, Menidia beryllina, and Lucania parva, held in combination with an omnivorous grass shrimp—Palaemonetes pugio, and a predatory diving beetle—Tropisternus lateralis, were measured at 12–60‰ in outdoor static microcosms that simulate salt marsh ponds. We predicted that the low species richness of this abiotically harsh but highly productive habitat would lead to a high degree of interaction among species. The presence of the beetle had no effect on the fish or the shrimp. Removal of the shrimp similarly had no detectable effect on the fish. There was a trend in proportions of survival among three fish: C. variegatus>F. heteroclitus>M. beryllina. Survival of M. beryllina was greater when it was alone at low densities of its own species (333 v. 667 fish m "3), and less when it was paired with F. heteroclitus. Interactions with other species diminished the growth of M. beryllina. Survival of F. heteroclitus was greater when it was alone at low density (333 m "3), than when the same number were placed together with Menidia and Cyprinodon at a total fish density of 999 m "3. There were no effects of removal of other species on survival or growth of C. variegatus at either 12·5 or 24‰. This study showed that a complex array of interactions occurred among six common members of a salt marsh food web, but the degree of interaction was less than we predicted. ? 1996 The Fisheries Society of the British Isles Key words: community simulation; competition; predation; salinity; estuary; salt marsh.
INTRODUCTION Although mummichogs, Fundulus heteroclitus (L.), and grass shrimp, Palaemonetes sp., have been used widely in studies of developmental biology and toxicology, relatively little is known about their community ecology. Weisberg (1986) has summarized the prevailing view that competitive interactions among four species of Fundulus seem independent of abiotic variables such as salinity. Sympatric salt marsh fish may have widely divergent tolerances to abiotic factors, and Dunson et al. (1993) suggest such differences could be important in determining the outcome of biotic interactions, as occurs among salt marsh plants (Bertness & Shumway, 1993). The interactions between abiotic and biotic factors in animal communities in estuaries have not been studied adequately (Dunson & Travis, 1991, 1994). To facilitate this process we studied purely biotic interactions among members of shallow water estuarine assemblages. We examined the following four questions: (a) Are fish affected by the presence of a sympatric beetle and a grass shrimp? (b) Are carnivorous fish affected by a facultatively herbivorous fish? (c) How do the carnivorous fish affect each other? (d) What is the effect of changes in densities of the carnivorous fish? We *Author to whom correspondence should be addressed at: University of Georgia, Savannah River Ecology Laboratory, Drawer E, Aiken, South Carolina 29802, U.S.A. 120 0022–1112/96/010120+11 $12.00/0
? 1996 The Fisheries Society of the British Isles
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1° and 2° Carnivores
F
L
1° Carnivores
M
T
Zooplankton
Insects, amphipods
P Epibenthic omnivores
C Facultative herbivore
Invertebrate herbivores Algae Detritus F. 1. A conceptual food web for the assemblage of estuarine fish (C, Cyprinodon variegatus; M, Menidia beryllina; L, Lucania parva; F, Fundulus heteroclitus) and invertebrates (P, Palaemonetes pugio; T, Tropisternus lateralis) studied. The direction of an arrow indicates consumption of the resource. Experimental tests of trophic structure concerned the following six major interactions between: (a) [three species of fish (F,M,C)+a shrimp (P)] and [a beetle (T)]; (b) [three species of fish (M,C,L)] and [a shrimp (P)], (c) [two pairs of carnivorous fish (F+M;M+L)] and [a herbivorous fish (C)]; (d) [one carnivorous fish (F)] and [another carnivorous fish (M)]; (e) a two-fold change in densities of [F] and [M] alone; (f) [two pairs of a carnivorous and a herbivorous fish (C+L;M+C)] and [one carnivorous fish (M and L respectively)]. Modified from Rowe & Dunson (1995).
hypothesized that removal of any species would result in a measurable change in growth and survival of the remaining species, the magnitude of which would depend upon the trophic status of the removed species (Fig. 1). Estuarine species are commonly believed to occupy broader niches than their freshwater counterparts, due to the low species richness of the estuary. Thus we predicted that there would be broad overlap in competitive and predatory associations among the fish and invertebrates. We conducted experiments in small, static, outdoor pools that simulated temporary ponds in the high salt marsh of the mid-Atlantic region of North America. MATERIALS AND METHODS EXPERIMENT A—EFFECTS OF PRESENCE OF A BEETLE AND VARIATION IN NUMBERS OF TWO PREDATORY FISH We tested the effects of the presence or absence of a carnivorous hydrophilid beetle (Tropisternus lateralis Duges), on three fish and a shrimp, and six combinations of fish species at different densities (Table I), a total of seven treatments with four replicates each. Treatment 2 had n=24. The species chosen co-occur in salt marsh ponds and
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T I. Conditions of the estuarine microcosm tests Salinity, (‰)
Treatment no.
Assemblage species (nos/pool)
Fish density (no. m "3)
A, 1992
12·5
B, 1993
19–33
1 2 3 4 5 6 7 1 2 3 4 5 6
10F+10M+10C+5P =FMC"T 10F+10M+10C+5P+2T =FMC+T 20F+5P =FF 20M+5P =MM 10F+10M+5P =FM 10F+5P =F 10M+5P =M 4M+4C+4L+6P =ALL 4M+4C+4L =ALL"P 6C+6L+6P =ALL"M 6M+6L+6P =ALL"C 6M+6C+6P =ALL"L 12M+6P =M only
999 999 667 667 666 333 333 400 400 400 400 400 400
Experiment, year
Abbreviations: L, Lucania parva (rainwater killifish); C, Cyprinodon variegatus (sheepshead minnow); F, Fundulus heteroclitus (mummichog); M, Menidia beryllina (silversides); P, Palaemonetes pugio (grass shrimp); T, Tropisternus lateralis (hydrophilid beetle). Growth and survival were measured over the last 60 days of experiments A (30 l pools) and B (110 l pools).
have potential trophic interactions of interest (Fig. 1). Clear polyethylene tanks (0·57#0·41#0·22 m) were arranged in a randomized block design in an open outdoor area adjacent to Oyster Bay, Chincoteague Island, Virginia. The tanks were shielded from rain with 0·32 cm thick sheets of clear plexiglas. Air flow/exchange was facilitated by a 3 cm hole at either end of the tank, covered by a 2 mm mesh screen. The tanks contained c. 30 l of sea water pumped from the bay, diluted with tap water to a salinity of 12·5‰. Salinity was measured weekly with a refractometer. Evaporative loss was minimal, and tap water was added only once (at 76 days) to maintain the target salinity of 12·5‰ during the 120-day test. On 7 April, 1992 (day 0), 40 g air-dried eel grass blades (Zostera marina) and 4 g rabbit pellets (for nutrients) were added to each tank. An equal aliquot (100 g wet mass) of filamentous algae, collected from Oyster Bay and connecting canals and incubated for 10 days to insure that no fish were included, was added to each tank on day 11. On day 47, a shade cloth (which excluded c. 60% of incident sunlight) was erected over the tanks to prevent overheating. On days 49–50, five gravid female grass shrimp (Palaemonetes pugio Holthuis) and two adult T. lateralis were added to each of the designated tanks. Larval fish of three species were added to the tanks on days 59 and 63. Mummichogs (designated F) were 11·1&0·5 mm in standard length and weighed 24·5&2·5 mg (mean&..). Larval silversides, Menidia beryllina (Cope), (designated M) were 9·6&0·9 mm in length and weighed 9·1&2·2 mg. Juvenile sheepshead minnows, Cyprinodon variegatus Lacépède, (designated C) measured 11·2&0·5 mm in length and weighed 40·2&8·8 mg. The lengths of the three fish species were similar, but they were different in wet body mass. Interactions among the fish were examined in six different combinations of fish species and densities; five grass shrimp (P) were present in all treatments (Table I). Treatment 1 tested the effect of combining the facultative herbivore (C) with the two carnivores, (F and M). Treatment 2 examined the effect of adding a small carnivorous beetle (T) to treatment 1. Treatments 3 to 7 examined competitive interactions (Dunson & Travis, 1991). At 333–999 m "3, total fish densities were within the natural range measured (Rowe & Dunson, 1995). Fish survival was not monitored during the experiment, since
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T II. Survival for three species of fish under various conditions of density and assemblage composition in 30-l microcosms, 1992, means&.. (a) F. heteroclitus Treatment
n
F FF FM FMC+T FMC"T
4 3 4 24 4
Percent survival (..) 68 37 35 15 3
(13) (22) (18) (6) (3)
P-value=0·011**, F=3·83, d.f.=38.
Tukey–Kramer 95% confidence intervals for pairwise comparisons of transformed proportion survived (F. heteroclitus)
F FF FM FMC+T
FF
FM
FMC+T
FMC"T
0·713&1·788 — — —
0·856&1·656 0·139&1·788 — —
1·475&1·264** 0·762&1·434 0·623&1·264 —
1·790&1·656** 1·077&1·788 0·938&1·656 0·315&1·264
(b) M. beryllina Treatment
n
M MM FM FMC+T FMC"T
4 4 4 24 4
Percent survival (..) 33 5 5 2 0
(3) (2) (3) (1) (0)
P-value P. vulgaris>T. lateralis>F. heteroclitus>M. beryllina. C. variegatus was the overwhelming dominant, with a survival near 90%, perhaps due to its facultatively herbivorous diet. F. heteroclitus and M. beryllina are entirely carnivorous, and food for them was probably severely limiting. Survival of F. heteroclitus was significantly greater in the low density-species alone treatment (F; 333 m "3), than when the same number were combined with other species [FMC&T; Table II(a)]. This suggests that there was some competition among at least two of these species, and particularly that C. variegatus might be involved (since F+M did not differ from F). However overall fish density was a confounding variable since other combinations such as F+M were not tested at the highest density (999 m "3). Survival of M. beryllina also was greatest when it was alone at the lowest density (333 m "3) [Table II(b)]. Its survival was positively correlated with that of the grass shrimp, and was dependent on density and assemblage: M>MM, FM, FMC+T, FMC-T (Table II), probably due to food limitation. Yet growth of M. beryllina was not density dependent: M=MM, FM (Table III). There were three significant effects of assemblage type on growth of M. beryllina (Table III): (a) M>FMC+T; (b) MM>FMC+T; (c)
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. . . .
T III. Rates of instantaneous growth G (Ricker, 1979) in mean wet mass for three species of fish under various conditions of density and assemblage composition in 30-l microcosms, 1992, means&.. (a) F. heteroclitus Treatment
n
F FF FM FMC+T FMC"T
4 3 3 7 1
G (day "1) (..) 0·012 0·010 0·023 0·011 0·001
(0·003) (0·005) (0·006) (0·002) —
P-value=0·126, F=2·20, d.f.=17. Pairwise comparisons not conducted.
(b) M. beryllina Treatment
n
M MM FM FMC+T FMC"T
4 3 4 4 0
G (day "1) (..) 0·027 0·030 0·027 0·007
(0·005) (0·003) (0·005) (0·001)
P-value ALL"P 0·0052&0·0040**
MM>FM. These results suggest that addition of F. heteroclitus inhibits growth of M. beryllina more than addition of the same number of M. beryllina. Therefore F. heteroclitus would appear to be the competitive dominant under these conditions. However the lack of a difference between FM and M (Table III) does not support this conclusion. The degree to which C. variegatus may participate in competition for food with these carnivores is unclear. The lack of a difference in growth between treatments FM and FMC or FMC&T suggests that C. variegatus has little influence on growth of the other two species. In addition there were no effects of any treatment on survival or growth of C. variegatus.
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EXPERIMENT B
There were six biotic treatments, M. beryllina only, an ALL species test, and four ALL-individual species tests (ALL-M, ALL-C, ALL-L, ALL-P). A possible invertebrate predator on fish is the grass shrimp, which is well known for its impact on in-fauna (Kneib, 1986). However, the removal of shrimp had no effect on the fish; there was good survival of shrimp across all treatments (69&7%). Survival in M. beryllina was relatively low and there were no effects of the treatments (Table IV) or of the final density of any of the fish on survival. Survival of the silversides in experiment B across all treatments (32&7%, mean&..) was greater than in experiment A [Table II(b)]. Growth in M. beryllina was greater when it was grown in the absence of other fish species (rates of instantaneous growth as day "1 in mass=0·076&0·007, and total length= 0·024&0·002) than in three of the five species combinations (0·062&0·001 and 0·019&0·001 respectively for all pooled). Thus M. beryllina showed various significant effects of the treatments (Table I) at initial densities of 130–400 m "3. There was no relation between growth and final density of any of the fish species. Neither growth nor survival of C. variegatus was affected by any of the treatments (Table IV). C. variegatus was unaffected by the treatments, grew well (rates of instantaneous growth as day "1 in mass=0·064&0·001, and total length=0·019&0·0003), and had an extremely high rate of survival over 60 days (93&2%). DISCUSSION The four species of fish that we manipulated fall generally into distinct trophic categories: C—a facultative herbivore; M—a zooplanktivore; L—a small primary and secondary carnivore, restricted to areas of dense vegetation; and F—a primary and secondary carnivore of moderate adult body size that feeds in a wide variety of habitats. Our conditions were primarily designed to examine competition for food among juveniles, although we did observe M. beryllina being eaten by P. pugio and L. parva on two occasions. Thus we do not pretend to have evaluated all possible important interactions. Nevertheless we were able to clarify several of our postulated interactions (Fig. 1). C. variegatus was relatively immune from the effects of competitive interactions with the other fish. In contrast, M. beryllina was negatively affected in growth and survival both by other species and by its own density, possibly because it is a specialist feeder on zooplankton, whereas F. heteroclitus is a generalist. Growth of M. beryllina alone was greater than growth of M. beryllina+F. heteroclitus at the same overall density; thus competition was asymmetric and F. heteroclitus dominated. An uncertainty that remains is the lack of a compensatory increase in growth by M. beryllina when either C. variegatus or L. parva was removed individually. This suggests that when only one of these competitors was removed, the other occupied the vacated niche and prevented M. beryllina from profiting. C. variegatus has the unique capacity to switch back and forth between herbivory and carnivory, based on food availability. This, and the presumed greater amount of plant than animal food available, may account for its extremely high rate of survival and insulation from competitive effects of other fish in this assemblage. The decreased survival of
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F. heteroclitus when it was paired with C. variegatus and M. beryllina suggests that the increase in total fish density from 333 to 999 m "3 resulted in competition. In particular it appears that the addition of C. variegatus might be critical, although the relative effect of increased densities of the other two species needs to be tested. The present study experimentally demonstrates interactions among shallow water estuarine fish. Weisberg (1986) observed that F. heteroclitus was sympatric with only one other of three congenerics in each of three habitat types (high salt marsh, high salinity subtidal zone, low salinity subtidal zone). He suggested three possible explanations for this distribution pattern: (1) differences in physiological tolerance to abiotic factors; (2) species specific predation; or (3) competitive exclusion. From the literature he excluded differences in salinity tolerance as a factor. He favoured competitive exclusion as the most likely explanation, but noted the need for transplants and competition experiments to further distinguish among the alternatives. Kristensen (1970) manipulated algal cover, zooplankton food and some combinations of three fish species (Cyprinodon dearborni Meek, Poecilia sphenops Cuvier & Valenciennes, and Rivulus marmoratus Poey) and found striking interactions between the presence of cover and predation/cannibalism. He concluded that competitive interactions among the three species were related also to water depth, salinity, anoxia and crowding, but not to temperature. Kristensen utilized several sizes of simulated pools as well as a rich diversity of natural ponds which varied in abiotic and biotic variables. We thank J. Slusark, J. R. Stauffer and C. Bursey for taxonomic help; W. Sadinski and D. Dunson for statistical assistance; M. Donne, J. Gentile, L. Nanovic and M. Perdue for technical help; and the Chincoteague National Wildlife Refuge for permission to collect fish on Assateague Island. Work was developed in part under grants R817206-01 and R818349-01 from the Environmental Protection Agency. However, the conclusions do not necessarily represent the policy of that agency, and you should not assume endorsement by the Federal Government. Editing of the manuscript was supported by contract DE-AC09-76SROO-819 between the University of Georgia and the U.S. Department of Energy.
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