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Sand dollar, Mellita quinquiesperforata (Leske), and sea pansy, Renilla reniformis (Cuvier) effects on meiofaunal abundance
J. Exp. Mar. Biol. Ecol., 1984, Vol. 84, pp. 225-234
225
Elsevier
JEM 392
SAND DOLLAR, MELLITA PANSY, RENILLA
QUINQUIESPERFORATA
RENIFORMIS
(Leske), AND SEA
(Cuvier) EFFECTS ON MEIOFAUNAL
ABUNDANCE’
ELIZABETH
L. CREED’
and BRUCE C. COULL
Belle W. Baruch Institute for Marine Biology and Coastal Research, Marine Science Program and Department of Biology, University of South Carolina, Columbia, SC 29208, U.S.A.
Abstract: The effect of disturbance by two macroinvertebrates, the sand dollar Me&a quinquiespe&rata (Leske) and the sea pansy RenilZareniformb (Cuvier) on meiofauna was studied on a sandbar in North Inlet, Georgetown, South Carolina. Abundances of nematodes and the harpacticoid copepod Apodopsyllus unguiformir Could 8c Hogue decreased significantly in the presence of sand dollars; other taxa were not affected. In two ReniUa experiments, one natural and another where artificial and real Renilla were implanted, we could determine no consistent effect on any meiobenthic taxon. However, sediments disturbed by implanting living and artificial Renilla returned to ambient levels within 1 h. Key words: meiofauna; sand dollars; sea pansies; interactions; South Carolina
Natural disturbances (sensu Zajac & Whitlatch, 1982) are important structuring forces in marine communities (Woodin, 1978; Thistle, 1980, 1981; Reidenauer & Thistle, 1981; Smith, 1981; Zajac & Whitlatch, 1982) which can alter both the habitat and the associated organisms. In marine soft bottom habitats a variety of biological disturbers are known to affect meiofauna abundance, e.g. stingrays (Reidenauer & Thistle, 1981), acorn worms (Thistle, 1980), grass shrimp (Bell & Coull, 1978), lugworms (Reise, 1983) and fish (see Hicks & Coull, 1983 for review). See Coull & Palmer (1984) for a review of disturbance and meiofauna. Herewith we report on the effect of two potential meiofauna disturbers, the sand dollar Mellita quinquiesperforata (Leske) (Echinoidea : Clypeasteroida) and the sea pansy Renilla renijbmis (Cuvier) (Anthozoa : Pennatulacea). Specifically, we attempted to determine (1) if any meiofauna taxon was selectively affected by sand dollars or sea pansies and (2) if the disturbance effect with sea pansies was caused by physical (shading, squashing or displacing) or biological phenomena (e.g. chemical secretions) of the disturber. Additionally, the time course of colonization was monitored.
1 Contribution No. 554 from the Belle W. Baruch Institute for Marine Biology and Coastal Research. Z Present address: Department of Marine, Earth and Atmospheric Sciences, Box 8208, North Carolina State University, Raleigh, NC 27695, U.S.A. 0022-0981/84/$03.00 0 1984 Elsevier Science Publishers B.V
226
ELIZABETHL. CREEDAND BRUCEC. COULL MATERIALS AND METHODS
STUDY SITE The study area was located in North Inlet, South Carolina at O-O.5 m depth (MLW) on a broad sandbar formed at the confluence of Debidue and Town Creeks (33”20,05’N : 79” 10.08/W). The site is hydrodynamically active with megaripples, a median grain size between 173-197 pm, sorting coefficients of 1.20-1.40 and a redox potential discontin~ty (RPD) between 4 and 7 cm (during the time sampled). This site is noteworthy not only because it is one of the sites of Coull’s long-term study on meiofauna population/community dynamics (B.C. Coull, unpubl. data), but also a large published data base exists for these meiofauna (Vernberg & Coull, 1974, 1975; Coull & Vernberg, 1975; Sellner, 1976; Vemberg et al., 1977; Coull & Fleeger, 1977; Hogue, 1978; Levy & Coull, 1978; Ivester, 1980; Findlay, 1981, 1982). See Cot111& Vernberg (1975) and Coull & Fleeger (1977) for physical characteristics of this site. This sandbar also has large populations of sand dollars and sea pansies and thus was an ideal location to study potential sand dollar and sea pansy/meiofaunal interactions. SAND DOLLAREXPERIMENT Two replicate meiofauna cores (1.5 cm inner diameter) were taken 10 cm in front of (i.e. an area not disturbed) and two cores were taken directly behind the same sand dollar as it passed along a track. In May 1982 meiofauna from 16 sand dollar tracks were sampled in this manner. The area in front of each sand dollar was divided into four quadrants and a random numbers table was used to determine the sample quadrants. All cores were taken at low tide to 10 cm depth, preserved in 10% formalin and stained with rose bengal. In the laboratory, samples were washed through a 63-pm mesh sieve, sorted and enumerated to major taxon. All copepods were identified to species. Meiofauna taxa and copepod species abundances were enumerated on an area basis (number/ 10 cm’). SEA PANSYEXPERIMENTS There were two Renillu field experiments. In July 1982, 10 cores (3.5 cm inner diameter) were taken to include in situ undisturbed ~3.5 cm diameter (range 2.9-3.4. cm) intertidal sea pansies. The Renilla were removed from the core, rinsed over the respective sample container with filtered (63 pm) sea water and discarded. A control core (no Renillu) was taken 0.5 m away from each sampled Reniila at that site. Samples were taken to the RPD (redox potential discontinuity layer) at low tide. The fixed cores were processed as in the sand dollar experiment. Meiofauna taxon abundances were enumerated on an area basis (number/IO cm2) and copepod numbers were calculated on this and on a volume basis (number/l0 cm’). Copepod abundance was significantly lower (see p. 229) in cores with, versus cores without, Renilla in the fast sea pansy experiment, but we could not determine if the
MACROFAUNAL
EFFECTS ON MEIOFAUNAL
ABUNDANCE
221
response was a structural response (i.e. the copepods reacted to the sea pansies because the sea pansies were a structure in the sediment) or a biological response (the copepods reacted to sea pansy secretions, predation, etc.). Thus we established Sea Pansy Experiment II (November 1982), where we implanted five sets (eight replicates/ set) of real (n = 40) and artificial (100% black silicone caulk) (n = 40) sea pansies in the field 3 h before low tide. Each artificial or real Renilla was 0.5 m away from its nearest neighbor. A set (i.e. eight real; eight artificial) was sampled as in the first Renilla experiment, at 0,0.25, 1,3 and 6 h after the Renilla were implanted. A control core was taken 0.5 m away from each real and fake Renilla pair. Total number of samples was 120. Samples were washed through 500~pm and retained on 63-pm mesh sieves, and copepod species enumerated on a per area and per volume basis. Originally, we planned to analyze abundance on a per area basis, the standard in meiofauna studies (e.g. McIntyre, 1969; Coull & Bell, 1979); however, since the redox depth varied (4-8 cm deep) from core to core and there was a possibility of sediment displacement by Renilla’s primary polyp, we analyzed the data both as abundance/ 10 cm’ and 10 cm3 of core sediment. The volume measurements take into account the area occupied by Renilla’s primary polyp. DATA ANALYSIS
All statistical analyses were performed on untransformed data using SAS software (Helwig & Council, 1979); sample measurements followed the basic assumptions of an analysis of variance (ANOVA) (random sampling, normal distribution of the error terms and homoscedasticity; Sokal & Rohlf, 1981). The sand dollar experiment was set up as a randomized block design and the taxon and copepod species data were analyzed by two-way ANOVA i.e. position and taxon (Ott, 1977). When significant differences were evident from the ANOVA, a Studentized maximum modulus (GT2) test (alpha = 0.05; Sokal & Rohlf, 1981), rather than a standard t-method test, was used because one sample was missing from a front replicate. Ranking of the mean abundances in all GT2 tests was from highest to lowest. Both sea pansy experiments were established as randomized block designs and the data were analyzed by two-way ANOVA. Copepods were defined as either being interstitial or epibenthic, and a one-way ANOVA was calculated for the effect of treatment (i.e. Renilla, no Renilla) on each such guild. In the second experiment, the Studentized maximum modulus (GT2) test was calculated where significant differences in treatment and time occurred (alpha = 0.05). In addition, a three-way ANOVA was calculated for the effect of treatment and time on each copepod species’ abundance; the results of which can be obtained from the authors.
ELIZABETHL. CREEDAND BRUCEC. COULL
228
RESULTS SAND DOLLAREXPERIMENT There were no significant differences between front and rear abundances for copepods (d.f. = 1, F = 0.33, P = 0.51), gastrotrichs (d.f. = 1, F = 2.19, P = 0.14) or other taxa (d.f. = 1, F = 0.18, P = 0.78) (Fig. 1). However, nematode abundances were significantly lower (P = 0.0014) behind, versus in front of, the sand dollars, and were also different between sand dollars (d.f. = 15, F = 12.28, P = 0.0359) (Fig. 1).
E ” 0 ; z
800-
2 f 2 220-
I IO-
COPEPOOS
NEMATODES
GASTROTRICHS
CTHERS
Fig. 1. Mean no./10 cm2 of major meiofaunal taxa, comparing abundances in the front and rear of sixteen in situ sand dollars: error bars are 2 SD about the mean; * significant (P = 0.0014) difference between front and rear abundances. Although total copepod abundance was not significantly different between the front and rear of Mellita, a two-way ANOVA on treatment and species abundance indicated that Apodopsylus unguiformis Coull & Hogue was more abundant (d.f. = 4, F = 12.16, P-c 0.0001) in front of, versus behind, the sand dollars (GT2 test, critical value = 2.819).
MACROFAUNAL
EFFECTS ON MEIOFAUNAL
ABUNDANCE
229
SEA PANSY EXPERIMENTS
Experiment I: eflect of live in situ sea pansies on meiofauna
There were no differences in the abundances of total meiofauna (d.f. = 1, F = 1.02, (F = 0.14, P = 0.715), gastrotrichs (F = 2.01, P = 0.173) or other taxa (d.f. = 1, F = 1.67, P = 0.223) in cores with and cores without Renilla when analyzed per unit area or volume. Total copepod density was significantly lower
P = 0.325), nematodes
SEA PANSY
IN T E R S TIT IA L
EXPERIMENT
1
@
ABSENT
0
PRESENT
EPIBENTHIC
Fig. 2. Interstitial and epibenthic copepod mean abundance/lo cm2 (in the presence and absence of sea pansies) from the first sea pansy experiment: error bars are 2 SD about the mean; * significant (P = 0.0003) differences between abundances underneath and away from Renih.
(F = 10.62, P = 0.0004) in cores with versus cores without Renilla. However, when the copepods were divided into guilds only the epibenthic copepod abundance decreased significantly (P = 0.0003 for area analysis; P = 0.0007 for volume analysis) in the presence of Renilla, interstitial copepods were unaffected (P = 0.9446 for area analysis; P = 0.6489 for volume analysis) (Fig. 2). Experiment II: eflect of implanted real and artificial sea pansies on copepods Since copepods were the only taxon affected in the first experiment, we dealt solely with changes in copepod abundances in the second Renilla experiment. In the area analysis there was no effect of treatment (control, real vs. artiticial Renilla) on the abundance of interstitial copepods (d.f. = 2, F = 0.22, P = 0.7999), but time of sample collection was significant (d.f. = 4, F = 12.74, P < 0.0001). However, epibenthic copepods (as in Renilla experiment I) were affected by both treatment i.e. no, artiticial or real sea pansies (d.f. = 2, F = 4.75, P = 0.0106) and time (0, 0.25, 1, 3, or 6 h, d.f. = 4, F = 18.96, P < 0.0001; Fig. 3). When analyzed on a volume basis the volume and area results were the same for interstitial copepod abundance, i.e. no effect of treatment, but a significant difference
230
ELIZABETH
L. CREED
AND
BRUCE
C. COULL
in time of collection. Where the epibenthic guild showed both treatment and time effects in the area analysis, only time was a significant (d.f. = 4, F = 17.01, P < 0.0001) variable in the sediment volume analysis. SEA
PANSY
EXPERIMENT
2
140-
120-
loo-
ri’ i
Fig. 3. Epibenthic copepod mean abundance/l0 and time of collection after implantation
cm* sediment, of sea pansies:
by treatment (no, fake or real sea pansies) error bars are 2 SD about the mean.
While our test of the original question, i.e. is the Renilla effect structural or biological, was inconclusive, more importantly the analyses on time of collection proved most informative. In every case, the 15-min (0.25 h) copepod abundances were significantly higher than the abundances at all other times (Table I). Fig. 3 illustrates one example, i.e. abundance of epibenthic copepod species per 10 cm2.
MACROFAUNAL
EFFECTS ON MEIOFAUNAL
231
ABUNDANCE
TABLEI Results of Studentized maximum modulus (GT2) test on time of collection (all treatments) in Sea Pansy Experiment II: samples were collected at 0,0.25,1,3, and 6 h after implanting real and artificial sea pansies; those hours underlined are not significantly different from each other at P % 0.05; values are given for area (10 cm2) and volumetric (10 cm3) abundances of copepods ; note that 0.25 h (15 mm) is significantly different in all cases; time of collection rankings are given in order of abundances. Time of collection (h) Interstitial copepods per 10 cm2 per 10 cm3
0.25 0.25
0 0
6 6
1 1
3 3
Epibenthic copepods per 10 cm2 per 10 cm3
0.25 0.25
1 1
0 3
3 0
6 6
Total copepods per 10 cm2 per 10 cm3
0.25 0.25
1 1
0 3
3 0
6 6
DISCUSSION SAND DOLLAR EXPERIMENT
Mellifa quinquiespeforata move 1-15 cm/h (Findlay & White, 1983) and are thought to be ciliary mucoid feeders selecting particles < 62 pm in size (Lane & Lawrence, 1982), probably non-photosynthetic microeucaryotes (Findlay & White, 1983). Thus it is unlikely that the significantly lower nematode and Apodopsyllus unguiformis (Copepoda) abundances behind, versus in front of, the sand dollars was caused by predation. We did not measure sand dollar movement directly. We assumed that by collecting samples directly behind (< 1 cm) the sand dollar and within 6 min of its passing (Y of 10 cm/h’ ; Findlay & White, 1983) we would have observed an effect on other taxa had there been one. Findlay 8z White (1983), using a similar sampling technique, found no effect of sand dollars on any meiofaunal taxon except foraminiferans. Possibly, this difference in sand dollar effect is because we took 16 replicates; they took three to six replicates (Findlay & White, 1983, their Table III), and their sediments contained an abundance of foraminiferans which were uncommon at our site (included in “other” taxa; Fig. 1). The dominant taxa other than nematodes (i.e. gastrotrichs, copepods in toto) are relatively rapid movers. Gastrotrichs are ciliary gliders (Swedmark, 1964), and many copepods can swim from spot to spot. Nematodes, however, are relatively slow movers that wriggle through the sediment (Pitcher, 1975). We suspect that the nematodes either went deeper into the sediment, since Findlay & White (1983) have shown that Mellita passage increases the depth of the redox layer, or they were pushed out of the way by the sand dollars and were unable to move back into the area before our “rear” samples
232
ELIZABETH
L. CREED
AND BRUCE
C. COULL
were taken. Apodopsyllus similarly is very poor at locomotion and wriggles like a nematode (Coull, unpubl.). Representatives of this genus are also the most tolerant of all harpacticoids to anoxia (Weiser et al., 1974) and whether it was pushed away, or down into the sediment, is immaterial. It did not come back to pre-test levels because, we believe, of its inability to move quickly. SEA PANSY
EXPERIMENTS
Because Renilla are sand-dwelling, suspension feeders anchored in the sand by a fleshy peduncle extending from a primary polyp displacing the upper millimeters of sediment, they should primarily affect epibenthos. Indeed, our first Renilla experiment, where we sampled to include and exclude Renilla, was consistent with such an hypothesis in that of all the meiofauna taxa only the epibenthic copepods were reduced in the presence of Renilla (Fig. 2). Our second Renillu experiment, where real and artificial Renilla were implanted, was designed to test whether the Renilla exclusion effect on epibenthic copepods was primarily structural (physical) or biological. Our results are inconclusive (Fig. 3). While we found that epibenthic copepod density was different in the area (10 cm’) analysis it was not different in the volume analysis (10 cm3). However, and more importantly, when sampling time after implantation is considered, time was always a significant variable affecting copepod abundance. While there is not a consistent pattern of time e.g. hour 1 always has more (or less) copepods than hour 3 etc., 0.25 his always different from any other time (Table I, Fig. 3). While the experiment was a priori established to distinguish structural versus biological effects, a posteriori the experiment tested for disturbance and subsequent recolonization. Previously, Sherman & Coull (1980) reported return to pre-test abundances took place within 12 h on a mudflat disturbed by overturning the sediment. The data presented here suggest that in sand the return to control levels took place between 15 min and 1 h. There are no significant differences in the copepod abundances between time 0 (start of experiment), 1 h, 3 h, and 6 h (Table 1); only 0.25 h is different, and it is always different regardless of method of abundance calculation (area, volume) or copepod guild (interstitial, epibenthic). Our implanting of the Renilla and walking on the flat, resulted in increased copepod abundances at 15 minutes (Fig. 3). By 1 h the assemblage had decreased to time zero abundance (ambient?); an abundance subsequently maintained for at least 6 h. When individual copepod species were compared, we could not distinguish preferential time species differences. Apodopsyllus unguformis (the “slow” species from the sand dollar experiment) abundance was not different over time; even at 0.25 h. Although enumeration of all meiofaunal taxa in Renilla Experiment II would be useful to determine if there were taxon differences with time, the fact that the other taxon data are missing does not refute the conclusion that control abundances of copepods were reached within 1 h.
MACROFAUNAL
EFFECTS ON MEIOFAUNAL
ABUNDANCE
233
ACKNOWLEDGEMENTS
Many people helped during the course of this study. We thank L. A. J. Clements, B. W. Dudley, R. A. E&in, P.A. Montagna and M.A. Palmer; R. J. Feller and S. E. Stancyk for helpful field assistance, criticisms and advice; D. Edwards of the Statistical Laboratory, University of South Carolina for assistance in data analysis; and two anonymous reviewers who made us rewrite the paper for the better. Financial support was provided by the Marine Science Program and the Belle W. Baruch Institute for Marine Biology and Coastal Research, University of South Carolina; and by the Biological Oceanography Program, National Science Foundation, Grant No. OCE8007968 (B. C. Coull, principal investigator).
REFERENCES
BELL, S. S. & B.C. COULL, 1978. Field evidence that shrimp predation regulates meiofauna, Oecologiu (Berlin), Vol. 35, pp. 141-148. COULL, B.C. & S. S. BELL, 1979. Perspectives of marine meiofaunal ecology. In, EcoZogical processes in coastal marine ecosystems, edited by R.J. Livingston,Plenum Press, New York, pp. 189-216. COULL,B.C. & J. W. FLEEGER,1977. Long-term temporal variation and community dynamics of meiobenthic copepods. Ecology, Vol. 50, pp. 1136-l 143. COULL,B.C. & M.A. PALMER,1984. Field experimentation in meiofaunal ecology. Hydrobiologia, in press. COULL, B.C. & W. B. VERNBERG,1975. Reproductive periodicity of meiobenthic copepods: seasonal or continuous? Mar. Biol., Vol. 32, pp. 289-293. FINDLAY,S.E. G., 1981. Small scale spatial distribution of meiofauna on a mud- and sandflat. Estuarine Coastal Sherf Sci., Vol. 12, pp. 471-484. FINDLAY,S. E. G., 1982. Influence of sampling scale on apparent distribution of meiofauna on a sandflat. Estuaries, Vol. 5, pp. 322-324. FINDLAY,R.H. & D. C. WHITE, 1983. The effects of feeding by the sand dollar Mellita quinquiesperforata (Leske) on the benthic microbial community. J. Exp. Mar. Biol. Ecol., Vol. 72, pp. 25-41. HELWIG,J.T. & K.A. COUNCIL(eds.), 1979. SAS user’s guide, 1979 edition. SAS Institute, Cary, North Carolina, 494 pp. HICKS, G. R. F. & B.C. COULL,1983. The ecology of marine meiobenthic harpacticoid copepods. Oceanogr. Mar. Biol. Annu. Rev., Vol. 21, pp. 67-175. HOGUE, E. W., 1978. Spatial and temporal dynamics of a subtidal estuarine gastrotrich assemblage. Mar. Biol., Vol. 49, pp. 21 l-222. IVESTER,M. S., 1980. The distribution of meiobenthic copepods along a sediment gradient: factor and niche analysis. Bull. Mar. Sci., Vol. 30, pp. 634-645. LANE, J. M. & J. M. LAWRENCE,1982. Food, feeding and absorption efficiencies of the sand dollar, Mellita quinquiesperforata (Leske). Estuarine Coastal ShelfSci., Vol. 14, pp. 421-431. LEVY,R. V. & B.C. COULL, 1978. Feeding groups and size analysis of marine meiobenthic nematodes from South Carolina, U.S.A. Vie Milieu, Vol. 27, pp. 586-645. MCINTYRE,A.D., 1969. Ecology of marine meiobenthos. Biol. Rev., Vol. 44, pp. 245-290. On, L. 1977. An introduction to statisticalmetho& and data analysis. North Scituate, Mass., Duxbury Press, 730 pp. PITCHER,R. S., 1975. Factors influencing the movement of nematodes in soil. In, Nematodes vectors ofplunt viruses, edited by F. Lambert, C. E. Taylor 8~ J. W. Seinhorst, NATO Advanced Study Institute Series, A: Life Sciences, Volume 2, New York, pp. 460. REIDENAUER,J.A. & D. THISTLE, 1981. Response of a soft-bottom harpacticoid community to stingray (Dasyatis sabina) disturbance. Mar. Biol., Vol. 65, pp. 261-267.
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AND BRUCE
C. COULL
removal of lugworms from marine sand affect small zoobenthos. Mar. Biol., Vol. 14, pp. 327-333. SELLNER, B.W., 1976. Survival and metabolism of the harpacticoid copepod Thompsonula hyaenae (Thompson) fed on different diatoms. Hydrobiologiu, Vol. 50, pp. 233-238. SHERMAN, K. M. & B.C. COULL, 1980. The response of meiofauna to sediment disturbance; J. Exp. Mar. Biol. Ecol., Vol. 46, pp. 59-71. SMITH, A.L., 1981. Comparison of macrofauna invertebrates in sand dollar (Dendruster excentricus) beds and in adjacent areas free of sand dollars. Mar. Biol., Vol. 65, pp. 191-198. SOKAL, R.R. & F. J. ROHLF, 1981. Biometry. W.H. Freeman and Company, San Francisco, 2nd edition, 859 pp. SWEDMARK,B., 1964. The interstitial fauna of marine sand. Biol. Rev., Vol. 39, pp. l-42.
REISE, K., 1983. Experimental
THISTLE,D., 1980. The response ofa harpacticoid copepod community to a small-scale natural disturbance. J. Mar. Res., Vol. 38, pp. 381-395. THISTLE,D., 1981. Natural disturbances and communities of marine soft bottoms. Mar. Ecol. Prog. Ser., Vol. 6, pp. 223-228.
VERNBERG,W. B. & B.C. COULL,1974. Respiration of an interstitial ciliate and benthic energy relationships. Oecologia (Berlin), Vol. 16, pp. 259-264. VERNBERG,W.B. & B.C. COULL, 1975. Multiple factor effects of environmental parameters on the physiology, ecology and distribution of some marine meiofauna. Cub. Biol. Mar., Vol. 16, pp. 721-732. VERNBERG,W. B., B.C. COULL& D. D. JORGENSON,1977. The reliability of laboratory metabolic measurements of meiofauna. J. Fish. Rex. Board Can., Vol. 34, pp. 164-167. WIESER, W., J. OTT, F. SCH~EMER& E. GNAIGNER, 1974. An ecophysiological study of some meiofauna inhabiting a sandy beach at Bermuda. Mar. Biol., Vol. 26, pp. 235-249. WOODIN, S.A., 1978. Refuges, disturbance, and community structure: a marine soft-bottom example. Ecology, Vol. 59, pp. 274-284.
ZAJAC, R.N. & R.B. WHITLATCH,1982. Responses of estuarine infauna to disturbance. I. Spatial and temporal variation of initial recolonization. Mar. Ecol. Prog. Ser., Vol. 10, pp. l-14.
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Elsevier
JEM 392
SAND DOLLAR, MELLITA PANSY, RENILLA
QUINQUIESPERFORATA
RENIFORMIS
(Leske), AND SEA
(Cuvier) EFFECTS ON MEIOFAUNAL
ABUNDANCE’
ELIZABETH
L. CREED’
and BRUCE C. COULL
Belle W. Baruch Institute for Marine Biology and Coastal Research, Marine Science Program and Department of Biology, University of South Carolina, Columbia, SC 29208, U.S.A.
Abstract: The effect of disturbance by two macroinvertebrates, the sand dollar Me&a quinquiespe&rata (Leske) and the sea pansy RenilZareniformb (Cuvier) on meiofauna was studied on a sandbar in North Inlet, Georgetown, South Carolina. Abundances of nematodes and the harpacticoid copepod Apodopsyllus unguiformir Could 8c Hogue decreased significantly in the presence of sand dollars; other taxa were not affected. In two ReniUa experiments, one natural and another where artificial and real Renilla were implanted, we could determine no consistent effect on any meiobenthic taxon. However, sediments disturbed by implanting living and artificial Renilla returned to ambient levels within 1 h. Key words: meiofauna; sand dollars; sea pansies; interactions; South Carolina
Natural disturbances (sensu Zajac & Whitlatch, 1982) are important structuring forces in marine communities (Woodin, 1978; Thistle, 1980, 1981; Reidenauer & Thistle, 1981; Smith, 1981; Zajac & Whitlatch, 1982) which can alter both the habitat and the associated organisms. In marine soft bottom habitats a variety of biological disturbers are known to affect meiofauna abundance, e.g. stingrays (Reidenauer & Thistle, 1981), acorn worms (Thistle, 1980), grass shrimp (Bell & Coull, 1978), lugworms (Reise, 1983) and fish (see Hicks & Coull, 1983 for review). See Coull & Palmer (1984) for a review of disturbance and meiofauna. Herewith we report on the effect of two potential meiofauna disturbers, the sand dollar Mellita quinquiesperforata (Leske) (Echinoidea : Clypeasteroida) and the sea pansy Renilla renijbmis (Cuvier) (Anthozoa : Pennatulacea). Specifically, we attempted to determine (1) if any meiofauna taxon was selectively affected by sand dollars or sea pansies and (2) if the disturbance effect with sea pansies was caused by physical (shading, squashing or displacing) or biological phenomena (e.g. chemical secretions) of the disturber. Additionally, the time course of colonization was monitored.
1 Contribution No. 554 from the Belle W. Baruch Institute for Marine Biology and Coastal Research. Z Present address: Department of Marine, Earth and Atmospheric Sciences, Box 8208, North Carolina State University, Raleigh, NC 27695, U.S.A. 0022-0981/84/$03.00 0 1984 Elsevier Science Publishers B.V
226
ELIZABETHL. CREEDAND BRUCEC. COULL MATERIALS AND METHODS
STUDY SITE The study area was located in North Inlet, South Carolina at O-O.5 m depth (MLW) on a broad sandbar formed at the confluence of Debidue and Town Creeks (33”20,05’N : 79” 10.08/W). The site is hydrodynamically active with megaripples, a median grain size between 173-197 pm, sorting coefficients of 1.20-1.40 and a redox potential discontin~ty (RPD) between 4 and 7 cm (during the time sampled). This site is noteworthy not only because it is one of the sites of Coull’s long-term study on meiofauna population/community dynamics (B.C. Coull, unpubl. data), but also a large published data base exists for these meiofauna (Vernberg & Coull, 1974, 1975; Coull & Vernberg, 1975; Sellner, 1976; Vemberg et al., 1977; Coull & Fleeger, 1977; Hogue, 1978; Levy & Coull, 1978; Ivester, 1980; Findlay, 1981, 1982). See Cot111& Vernberg (1975) and Coull & Fleeger (1977) for physical characteristics of this site. This sandbar also has large populations of sand dollars and sea pansies and thus was an ideal location to study potential sand dollar and sea pansy/meiofaunal interactions. SAND DOLLAREXPERIMENT Two replicate meiofauna cores (1.5 cm inner diameter) were taken 10 cm in front of (i.e. an area not disturbed) and two cores were taken directly behind the same sand dollar as it passed along a track. In May 1982 meiofauna from 16 sand dollar tracks were sampled in this manner. The area in front of each sand dollar was divided into four quadrants and a random numbers table was used to determine the sample quadrants. All cores were taken at low tide to 10 cm depth, preserved in 10% formalin and stained with rose bengal. In the laboratory, samples were washed through a 63-pm mesh sieve, sorted and enumerated to major taxon. All copepods were identified to species. Meiofauna taxa and copepod species abundances were enumerated on an area basis (number/ 10 cm’). SEA PANSYEXPERIMENTS There were two Renillu field experiments. In July 1982, 10 cores (3.5 cm inner diameter) were taken to include in situ undisturbed ~3.5 cm diameter (range 2.9-3.4. cm) intertidal sea pansies. The Renilla were removed from the core, rinsed over the respective sample container with filtered (63 pm) sea water and discarded. A control core (no Renillu) was taken 0.5 m away from each sampled Reniila at that site. Samples were taken to the RPD (redox potential discontinuity layer) at low tide. The fixed cores were processed as in the sand dollar experiment. Meiofauna taxon abundances were enumerated on an area basis (number/IO cm2) and copepod numbers were calculated on this and on a volume basis (number/l0 cm’). Copepod abundance was significantly lower (see p. 229) in cores with, versus cores without, Renilla in the fast sea pansy experiment, but we could not determine if the
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response was a structural response (i.e. the copepods reacted to the sea pansies because the sea pansies were a structure in the sediment) or a biological response (the copepods reacted to sea pansy secretions, predation, etc.). Thus we established Sea Pansy Experiment II (November 1982), where we implanted five sets (eight replicates/ set) of real (n = 40) and artificial (100% black silicone caulk) (n = 40) sea pansies in the field 3 h before low tide. Each artificial or real Renilla was 0.5 m away from its nearest neighbor. A set (i.e. eight real; eight artificial) was sampled as in the first Renilla experiment, at 0,0.25, 1,3 and 6 h after the Renilla were implanted. A control core was taken 0.5 m away from each real and fake Renilla pair. Total number of samples was 120. Samples were washed through 500~pm and retained on 63-pm mesh sieves, and copepod species enumerated on a per area and per volume basis. Originally, we planned to analyze abundance on a per area basis, the standard in meiofauna studies (e.g. McIntyre, 1969; Coull & Bell, 1979); however, since the redox depth varied (4-8 cm deep) from core to core and there was a possibility of sediment displacement by Renilla’s primary polyp, we analyzed the data both as abundance/ 10 cm’ and 10 cm3 of core sediment. The volume measurements take into account the area occupied by Renilla’s primary polyp. DATA ANALYSIS
All statistical analyses were performed on untransformed data using SAS software (Helwig & Council, 1979); sample measurements followed the basic assumptions of an analysis of variance (ANOVA) (random sampling, normal distribution of the error terms and homoscedasticity; Sokal & Rohlf, 1981). The sand dollar experiment was set up as a randomized block design and the taxon and copepod species data were analyzed by two-way ANOVA i.e. position and taxon (Ott, 1977). When significant differences were evident from the ANOVA, a Studentized maximum modulus (GT2) test (alpha = 0.05; Sokal & Rohlf, 1981), rather than a standard t-method test, was used because one sample was missing from a front replicate. Ranking of the mean abundances in all GT2 tests was from highest to lowest. Both sea pansy experiments were established as randomized block designs and the data were analyzed by two-way ANOVA. Copepods were defined as either being interstitial or epibenthic, and a one-way ANOVA was calculated for the effect of treatment (i.e. Renilla, no Renilla) on each such guild. In the second experiment, the Studentized maximum modulus (GT2) test was calculated where significant differences in treatment and time occurred (alpha = 0.05). In addition, a three-way ANOVA was calculated for the effect of treatment and time on each copepod species’ abundance; the results of which can be obtained from the authors.
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RESULTS SAND DOLLAREXPERIMENT There were no significant differences between front and rear abundances for copepods (d.f. = 1, F = 0.33, P = 0.51), gastrotrichs (d.f. = 1, F = 2.19, P = 0.14) or other taxa (d.f. = 1, F = 0.18, P = 0.78) (Fig. 1). However, nematode abundances were significantly lower (P = 0.0014) behind, versus in front of, the sand dollars, and were also different between sand dollars (d.f. = 15, F = 12.28, P = 0.0359) (Fig. 1).
E ” 0 ; z
800-
2 f 2 220-
I IO-
COPEPOOS
NEMATODES
GASTROTRICHS
CTHERS
Fig. 1. Mean no./10 cm2 of major meiofaunal taxa, comparing abundances in the front and rear of sixteen in situ sand dollars: error bars are 2 SD about the mean; * significant (P = 0.0014) difference between front and rear abundances. Although total copepod abundance was not significantly different between the front and rear of Mellita, a two-way ANOVA on treatment and species abundance indicated that Apodopsylus unguiformis Coull & Hogue was more abundant (d.f. = 4, F = 12.16, P-c 0.0001) in front of, versus behind, the sand dollars (GT2 test, critical value = 2.819).
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SEA PANSY EXPERIMENTS
Experiment I: eflect of live in situ sea pansies on meiofauna
There were no differences in the abundances of total meiofauna (d.f. = 1, F = 1.02, (F = 0.14, P = 0.715), gastrotrichs (F = 2.01, P = 0.173) or other taxa (d.f. = 1, F = 1.67, P = 0.223) in cores with and cores without Renilla when analyzed per unit area or volume. Total copepod density was significantly lower
P = 0.325), nematodes
SEA PANSY
IN T E R S TIT IA L
EXPERIMENT
1
@
ABSENT
0
PRESENT
EPIBENTHIC
Fig. 2. Interstitial and epibenthic copepod mean abundance/lo cm2 (in the presence and absence of sea pansies) from the first sea pansy experiment: error bars are 2 SD about the mean; * significant (P = 0.0003) differences between abundances underneath and away from Renih.
(F = 10.62, P = 0.0004) in cores with versus cores without Renilla. However, when the copepods were divided into guilds only the epibenthic copepod abundance decreased significantly (P = 0.0003 for area analysis; P = 0.0007 for volume analysis) in the presence of Renilla, interstitial copepods were unaffected (P = 0.9446 for area analysis; P = 0.6489 for volume analysis) (Fig. 2). Experiment II: eflect of implanted real and artificial sea pansies on copepods Since copepods were the only taxon affected in the first experiment, we dealt solely with changes in copepod abundances in the second Renilla experiment. In the area analysis there was no effect of treatment (control, real vs. artiticial Renilla) on the abundance of interstitial copepods (d.f. = 2, F = 0.22, P = 0.7999), but time of sample collection was significant (d.f. = 4, F = 12.74, P < 0.0001). However, epibenthic copepods (as in Renilla experiment I) were affected by both treatment i.e. no, artiticial or real sea pansies (d.f. = 2, F = 4.75, P = 0.0106) and time (0, 0.25, 1, 3, or 6 h, d.f. = 4, F = 18.96, P < 0.0001; Fig. 3). When analyzed on a volume basis the volume and area results were the same for interstitial copepod abundance, i.e. no effect of treatment, but a significant difference
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in time of collection. Where the epibenthic guild showed both treatment and time effects in the area analysis, only time was a significant (d.f. = 4, F = 17.01, P < 0.0001) variable in the sediment volume analysis. SEA
PANSY
EXPERIMENT
2
140-
120-
loo-
ri’ i
Fig. 3. Epibenthic copepod mean abundance/l0 and time of collection after implantation
cm* sediment, of sea pansies:
by treatment (no, fake or real sea pansies) error bars are 2 SD about the mean.
While our test of the original question, i.e. is the Renilla effect structural or biological, was inconclusive, more importantly the analyses on time of collection proved most informative. In every case, the 15-min (0.25 h) copepod abundances were significantly higher than the abundances at all other times (Table I). Fig. 3 illustrates one example, i.e. abundance of epibenthic copepod species per 10 cm2.
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ABUNDANCE
TABLEI Results of Studentized maximum modulus (GT2) test on time of collection (all treatments) in Sea Pansy Experiment II: samples were collected at 0,0.25,1,3, and 6 h after implanting real and artificial sea pansies; those hours underlined are not significantly different from each other at P % 0.05; values are given for area (10 cm2) and volumetric (10 cm3) abundances of copepods ; note that 0.25 h (15 mm) is significantly different in all cases; time of collection rankings are given in order of abundances. Time of collection (h) Interstitial copepods per 10 cm2 per 10 cm3
0.25 0.25
0 0
6 6
1 1
3 3
Epibenthic copepods per 10 cm2 per 10 cm3
0.25 0.25
1 1
0 3
3 0
6 6
Total copepods per 10 cm2 per 10 cm3
0.25 0.25
1 1
0 3
3 0
6 6
DISCUSSION SAND DOLLAR EXPERIMENT
Mellifa quinquiespeforata move 1-15 cm/h (Findlay & White, 1983) and are thought to be ciliary mucoid feeders selecting particles < 62 pm in size (Lane & Lawrence, 1982), probably non-photosynthetic microeucaryotes (Findlay & White, 1983). Thus it is unlikely that the significantly lower nematode and Apodopsyllus unguiformis (Copepoda) abundances behind, versus in front of, the sand dollars was caused by predation. We did not measure sand dollar movement directly. We assumed that by collecting samples directly behind (< 1 cm) the sand dollar and within 6 min of its passing (Y of 10 cm/h’ ; Findlay & White, 1983) we would have observed an effect on other taxa had there been one. Findlay 8z White (1983), using a similar sampling technique, found no effect of sand dollars on any meiofaunal taxon except foraminiferans. Possibly, this difference in sand dollar effect is because we took 16 replicates; they took three to six replicates (Findlay & White, 1983, their Table III), and their sediments contained an abundance of foraminiferans which were uncommon at our site (included in “other” taxa; Fig. 1). The dominant taxa other than nematodes (i.e. gastrotrichs, copepods in toto) are relatively rapid movers. Gastrotrichs are ciliary gliders (Swedmark, 1964), and many copepods can swim from spot to spot. Nematodes, however, are relatively slow movers that wriggle through the sediment (Pitcher, 1975). We suspect that the nematodes either went deeper into the sediment, since Findlay & White (1983) have shown that Mellita passage increases the depth of the redox layer, or they were pushed out of the way by the sand dollars and were unable to move back into the area before our “rear” samples
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were taken. Apodopsyllus similarly is very poor at locomotion and wriggles like a nematode (Coull, unpubl.). Representatives of this genus are also the most tolerant of all harpacticoids to anoxia (Weiser et al., 1974) and whether it was pushed away, or down into the sediment, is immaterial. It did not come back to pre-test levels because, we believe, of its inability to move quickly. SEA PANSY
EXPERIMENTS
Because Renilla are sand-dwelling, suspension feeders anchored in the sand by a fleshy peduncle extending from a primary polyp displacing the upper millimeters of sediment, they should primarily affect epibenthos. Indeed, our first Renilla experiment, where we sampled to include and exclude Renilla, was consistent with such an hypothesis in that of all the meiofauna taxa only the epibenthic copepods were reduced in the presence of Renilla (Fig. 2). Our second Renillu experiment, where real and artificial Renilla were implanted, was designed to test whether the Renilla exclusion effect on epibenthic copepods was primarily structural (physical) or biological. Our results are inconclusive (Fig. 3). While we found that epibenthic copepod density was different in the area (10 cm’) analysis it was not different in the volume analysis (10 cm3). However, and more importantly, when sampling time after implantation is considered, time was always a significant variable affecting copepod abundance. While there is not a consistent pattern of time e.g. hour 1 always has more (or less) copepods than hour 3 etc., 0.25 his always different from any other time (Table I, Fig. 3). While the experiment was a priori established to distinguish structural versus biological effects, a posteriori the experiment tested for disturbance and subsequent recolonization. Previously, Sherman & Coull (1980) reported return to pre-test abundances took place within 12 h on a mudflat disturbed by overturning the sediment. The data presented here suggest that in sand the return to control levels took place between 15 min and 1 h. There are no significant differences in the copepod abundances between time 0 (start of experiment), 1 h, 3 h, and 6 h (Table 1); only 0.25 h is different, and it is always different regardless of method of abundance calculation (area, volume) or copepod guild (interstitial, epibenthic). Our implanting of the Renilla and walking on the flat, resulted in increased copepod abundances at 15 minutes (Fig. 3). By 1 h the assemblage had decreased to time zero abundance (ambient?); an abundance subsequently maintained for at least 6 h. When individual copepod species were compared, we could not distinguish preferential time species differences. Apodopsyllus unguformis (the “slow” species from the sand dollar experiment) abundance was not different over time; even at 0.25 h. Although enumeration of all meiofaunal taxa in Renilla Experiment II would be useful to determine if there were taxon differences with time, the fact that the other taxon data are missing does not refute the conclusion that control abundances of copepods were reached within 1 h.
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ACKNOWLEDGEMENTS
Many people helped during the course of this study. We thank L. A. J. Clements, B. W. Dudley, R. A. E&in, P.A. Montagna and M.A. Palmer; R. J. Feller and S. E. Stancyk for helpful field assistance, criticisms and advice; D. Edwards of the Statistical Laboratory, University of South Carolina for assistance in data analysis; and two anonymous reviewers who made us rewrite the paper for the better. Financial support was provided by the Marine Science Program and the Belle W. Baruch Institute for Marine Biology and Coastal Research, University of South Carolina; and by the Biological Oceanography Program, National Science Foundation, Grant No. OCE8007968 (B. C. Coull, principal investigator).
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