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Does interference competition determine the vertical distribution of meiobenthic copepods?
J. Exp. Mar. Biol. Ecol., 1986, Vol. 95, pp. 173-181
173
Elsevier
JEM 621
DOES INTERFERENCE
COMPETITION
DISTRIBUTION
DETERMINE
OF MEIOBENTHIC
THE VERTICAL
COPEPODS?
J. W. FLEECER Department of Zoology and Physiologv, Louisiana State University, Baton Rouge, LA 70803, U.S.A.
and
J.M. N.E.R.C.
GEE
Institutefor Marine Environmental Research, Prospect Place, The Hoe, Plymouth, PLl 3DH, Devon, England
(Received 11 July 1985; revision received 10 October 1985; accepted 30 October 1985) Abstract: The meiobenthic copepod assemblage in the sand flats of the Exe estuary, Devon, England, is vertically segregated with the mean depths of individual species each offset by a few millimeters. This distribution pattern suggests resource partitioning for vertical space. An experiment was performed to determine if interference competition for space resulted in a competitive hierarchy that determined vertical position. Asellopsis intermedia (T. Scott) and Tryphoema bocqueti Bozic were added in known densities to laboratory maintained, azoic sand columns. With no other species present, both species relocated at depths very similar to their low tide field distributions. Mean depths, and the distributions as a whole of each species were also compared in single species and mixed species situations. No competitive mediated shifts in vertical position occurred. With the lack of response to ecological release and the lack of competitive displacement, we could find no evidence that vertical profile was governed by interference competition for space. Although segregated vertical patterns are common for interstitial meiofauna, and many authors have suggested that competition may regulate this pattern, other factors, perhaps related to diffusion gradients from the sediment surface downward, may be responsible. Key words: meiofauna; space competition; copepods; copepods and vertical distribution;
Tryphoema
bocqueti; Asellopsis intermedia
Meiofauna in capillary sands live in a three-dimensional environment which often extends to depths of 50 cm or more in aerobic sands (Fenchel, 1978; Hicks & Coull, 1983). Species in such environments frequently display a distinct and predictable vertical zonation. This pattern, in which the vertical location of closely related species is slightly offset, has been shown in a number of meiofauna taxa including nematodes (Warwick, 1971; Boaden, 1977; Platt, 1977; Jensen, 1983), tardigrades (Pollock, 1970), gastrotrichs (Schmidt & Teuchert, 1969; Boaden, 1977; Maguire, 1977; Hogue, 1978), harpacticoid copepods (Harris, 1972; Mielke, 1976; Moore, 1979; Joint et al., 1982) and turbellarians (Hoxhold, 1974; Boaden, 1977; Maguire, 1977). Such field distributional patterns may be the result of competition (Peterson, 1979; Branch, 1984) and 0022-0981/86/%03.50 0 1986 Elsevier Science Publishers B.V. (Biomedical Division)
174
J.W.FLEEGERANDJ.M.GEE
the offset vertical position is identical to the type of niche-shift expected by competition theory (Schoener, 1974). Several authors (Boaden, 1977; Coull& Fleeger, 1977; Hogue, 1978; Hicks & Coull, 1983) have referred to this commonly observed vertical pattern as resource partitioning. Competition may influence this vertical field distribution in at least two ways. On the one hand, vertical position may be the direct result of interference competition for space in which one species out-competes or aggressively “drives off’ another species from that space. Interference competition is common in hard substratum communities where overgrowth can occur, but rare in soft sediments (Peterson, 1979; Woodin & Jackson, 1979). Nevertheless aggressive encounters have been reported among meiobenthic copepods (Marcotte, 1984) and between small tube-building polychaetes (Bell & Coull, 1980; Levin, 1982). Interference competition for space could be especially important among interstitial and burrowing meiofauna in dynamic shallow sand flats in which sands and fauna are mixed by tidal resuspension. It is likely that fauna in such environments must resort themselves vertically after a tidal disturbance, and such a redistribution could be determined by a competitive hierarchy. Grant (1981) has experimentally shown competitive displacement between two sand flat amphipods. On the other hand, competition effects on the community may be purely historical, having acted as a selective force for habitat partitioning (Connell, 1980). The result would be species-specific tolerance limits and preferred depth ranges. Without experimentation it is not possible to discriminate between these two types of competition (if either occurs), and their roles in regulating meiofauna community structure. Joint et al. (1982) have shown that, in summer, the community of harpacticoid copepods inhabiting tidally disturbed sandflats in the Exe Estuary, Devon, England, is predictably found in a distinct, fine scale, vertical zonation sequence which does not vary even though the mean depth of individual species varies at different tidal stages. Similarly, field sampling prior to this study, in November, 1984, indicated that the vertical zonation sequence is persistent throughout the year. The purpose of this investigation was to test experimentally for spatial interference competition among these sand-dwelling harpacticoids by establishing single and mixed species populations in azoic laboratory sand columns. Differences in depth profile of one species in the absence or presence of another species would be interpreted as evidence that interference competition for space is taking place in extant communities.
MATERIALS
AND METHODS
From the seven most common harpacticoids
in the Exe sandflat community,
Asellopsis intermedia (T. Scott) and Tryphoema bocqweti Bozic were chosen as experi-
mental subjects because: (1) they live near the surface (O-3 cm) of these tidally mixed sands; (2) they are abundant with similar but distinctly offset mean depths (respectively, the second and third species from the surface in the vertical sequence); (3) they proved
COMPETITION FOR SPACE BY MEIOFAUNA
175
to be readily identifiable under low magnification while living; and (4) they could be handled and extracted without mortality. Given the tidal resuspension common on this sand flat, the maintenance of vertical position may be actively maintained, potentially as the result of a competitive hierarchy. Sand columns were prepared from washed Exe sandflat surface (O-3 cm) sediment which had been dried at 100 “C for 24 h and sieved through a graded sieve set. Sand from two sieve fractions (250 and 375 pm) was retained and mixed in equal amounts. This sand was added, to a depth of 25 mm, to columns made from 16-mm internal diameter plastic disposable syringe barrels modified for attachment to a micrometer after Joint et al. (1982). Mesh fabric (150 pm), fastened to the bottom of the column by a rubber band, was used to hold sand in place. Columns were clamped vertically just below the surface of a flow-through sea-water tank with constant temperature (16 oC), salinity (25x,), and light regime, and allowed to equilibrate for 24 h. These sand columns are similar to the “floating culture tubes” used by Hardy (1978) to successfully rear Asellopsis intermedia (hereafter referred to as Asellopsis). Hardy maintained various life history stages for months in tubes with a thin layer of sand covering a mesh fabric exposed to the water column. Asellopsis and Tryphoema bocqueti (hereafter referred to as Tryphoema) were extracted from freshly collected Exe estuary sand within 24 h by elutriation using MgCl, (McIntyre & Warwick, 1984); Asellopsis and Tryphoema were sorted and counted under a stereomicroscope immediately. Sand columns were removed from the water bath, and after draining, known numbers of either species alone or a mixture of both species were added to the sand surface by pipette. The top of the column was covered by 130~pm mesh screen; the column shaken to disperse the copepods, and replaced into the water bath for 24 h before the sand was sectioned into 25 l-mm thick sections by the micrometer method. Core fractions were fixed in 5% formalin and copepods later identified under a stereomicroscope. Known numbers (ranging from 60-260) of adult Asellopsis and Tqphoema were added to a total of 37 laboratory sand columns. Typically we added z 100 individuals in single or 200 total individuals (100 of each species) in mixed species experiments. Although densities and reproductive activities of both species fluctuate throughout the year (Gee &Warwick, 1984), densities used in the columns range from near the average field density (equivalent to z 100 of Asellopsis or Tryphoema in each column) to about twice normal (200 or more per column) for each species. Weighted mean depths for each species from the upper 15 mm of each replicate were calculated by SAS (SAS Institute Inc., 1982) programming. Frequency distributions for each species over l-mm depth intervals for each replicate were also determined. Parametric statistics comparing mean depth with densities were calculated by SAS GLM. Actual depth distributions were also compared using non-parametric statistics (Kolmogorov-Smirnov two-sample test) following the procedures of Siegel (1956).
176
J. W. FLEEGER AND J.M. GEE RESULTS
Both species were recovered from the experimental sand columns at ~87% efficiency. Discrepancies were probably due either to escape through the bottom of the column, or through loss by pipette transfer or by undercounting live animals. If the upper 15 mm are considered, the laboratory distributions of both species were quite similar to the field distributions of Joint et al. (1982); the majority of individuals were in the upper 3-8 mm with steadily declining densities through 15 mm. Although 92% of each species was recovered in the upper 15 mm, there was a tendency in both species for some aggregation at 23-25 mm especially in densely populated (single and mixed species) laboratory columns. This bimodal vertical distribution was not observed in field samples, and could have resulted from the fact that the bottom of the column was directly exposed to sea water. With diffusion through the bottom, both species may have recognized the column bottom as another “surface”. For this reason, vertical distributions are hereafter considered only through the upper 15 mm. Of the two species, Aselfopsis was consistently found at slightly shallower depths in all laboratory sand columns (Figs. 1 and 2). Furthermore, the mean depth differential between the two species in the laboratory was remarkably similar to that found from low tide field samples when all species in the taxocene were present. In single species
. .
!.: .: :. . .
l
l
.
ASELLOPSIS 6-
50
100
INTERMEDIA 150
t
.
-z =-
250 .
.
J% I
200 ,
4-
k
.
x3
;
i
.
%
2-
g
l-
. TRYPHOEMA 50
100
NO. INDIVIDUALS
BOCQUETI I 150
I 200
250
ADDED
Fig. 1. Mean depth of Asellopsis intermedia plotted against the number of A. intermedia added to experimental sand columns (upper) and mean depth of Tryphoema bocqueti plotted against the number of T. bocqueti added to experimental sand columns (lower).
COMPETITION FOR SPACE BY MEIOFAUNA
177
trials, the overall mean depth of Asellopsis was 3.1 mm, compared to 3 mm from field collections, and for ~~~~~~ overall mean depth was 4.2 compared to 5 mm from the field (field data from Joint et al., 1982). Clearly both species of copepods responded to laboratory sands by locating depth strata as they do in the field, and ecological release (sensu Ricklefs, 1973, p. 692) in resource utilization did not take place. Single species experimental densities were varied from near normal field densities (Z 100 per column) to about twice normal (200 or more per column) in an attempt to determine if depth profile was density dependent, and influenced by intraspeci~c competition (Maiorana, 1977; Grant, 1981). Linear regression was used to test for a relationship of mean depth for a species with the number of individuals of that species added to laboratory sands (Fig. 1). Mean depths did not vary with number of individuals added for Asellopsis (b = 0.0035, P = 0.52), and was not strongly indicated for ~ry~~oe~a (b = 0.010, P = 0.053). Thus at the densities used in these experiments, depth did not vary with increasing intraspeciftc density. in laboratory sand columns in which both species were present, overall mean depths were unchanged compared to single species situations (Fig. 2). Mean depth across replicates ofAsellopsis when Trypkoema was present was 3.2 mm (as opposed to 3.1 mm in single species trials); mean depth of T~phoema with Asellopsis present was 4.5 mm (as opposed to 4.2 mm in single species trials). Two methods were used to test the nuil
INTERMDIA
ASELLOPSIS
. l
.
.
a ...
a
.
..
.
l
TRYPHOEMA
NO. INCWDUALS
BOCQUETI
ADDED
Fig. 2. Mean depth of Asellopsis~te~~e~i~plotted against the number of Tryph~e~~bocquetiadded to experimental sand columns (upper) and mean depth of Tryphoem bocquetiplotted against the number of Asellopsisintermediaadded to experimental sand columns (lower).
178
J.W. FLEECER
AND J.M. GEE
hypothesis that there were no shifts in vertical profile in sands with potential competitors. Linear regression tested for a relationship of mean depth with numbers added of the potential competitor. Regressions were calculated using the mean depth for each species in each replicate against the density of the potential competitor added to that replicate. This effect should be density related as the shift in depth profile is expected to be greater when competition is stronger (i.e. when higher densities of a potential competitor are present). The slope of the line was not significantly different from zero for either species (Asellopsis, b = 0.0009, P = 0.70; Tryphoema, b = 0.0035, P = 0.29), and we can not reject the null hypothesis that shifts in mean depth did not occur with increasing “competitor” density. Mean depth is only one measure of a distribution. Changes in any aspect of the depth distribution of a copepod, caused by adding a potential competitor, must also be considered. To test for any change in vertical distribution not restricted to central tendency, a two-tailed Kolmogorov-Smirnov (KS) two-sample test was performed. The distribution (through 15 mm) of a species in single species sands was compared to its distribution in sands with both species present. Because each of these treatments (Asellopsis alone and with Tryphoema; Tvphoema alone and with Asellopsis) was replicated, a Friedman’s two-way ANOVA was first conducted to determine if the distribution among replicates was equivalent; in no case was a significant difference found. Therefore, a distribution for each treatment was prepared by summing the frequency counts at each depth across replicates, and the KS statistic computed (critical values of D were calculated at the 0.05 level). Comparing distribution in single species with that in mixed species situations, the observed value of D was 0.03 1 for Aseflopsis which is less than the critical value of 0.058, and for TVphoema the observed value of 0.057 is essentially identical to the critical value of 0.053. Thus no strong evidence for a competitor related shift or modification in any parameter of its distribution was found for either species.
DISCUSSION
The results of this study can not support the contention that interference competition for space maintains the vertical zonation pattern of Exe sandflat harpacticoids. This does not mean that the depth sequence is unaffected by all forms of competition, or that interference competition is not important for other taxa or in other habitats. Competition could have acted as a historical selective force (Connell, 1980) to derive present day tolerance and depth preferences (as argued by Hogue, 1978). These data suggest that in shallow, frequently mixed sands, a short-term competitive hierarchy does not determine vertical position. Although it has been suggested theoretically that vertical segregation may provide additional resource space (Levinton, 1977) only Peterson & Andre (1980) and Grant (198 1) utilized experimental techniques to identify vertical displacement (interference
COMPETITIONFOR
SPACEBYMEJOFAUNA
179
competition) between species. Grant’s study was most similar to ours in design, except that he used very active amphipods which could move throughout the oxygenated zone of a sand flat. However, most soft sediment benthic studies finding an effect of one species on the distribution of another (adult-adult studies) have identified either aggressive interactions between tube-builders (Levin, 1982; Wilson, 1983), or interactions between species which have contrasting effects on sediment properties (Brenchley, 1981, 1982; Wilson, 1981). Although reports of tube-dwelling or burrow construction exist for meiofauna (Riemann & Schrage, 1978; Severin et al., 1982; Bromley and Ekdale, 1984; Chandler & Fleeger, 1984), neither experimental species gives any indication of tube-building or even of the aggressive interspecific encounters observed by Marcotte (1984). In unsorted dishes, Asellopsis and Tryphoema often bumped into each other, eliciting no obvious response, and T. bocqueti was once observed grasping Asellopsis with no ill effect to either species. Both burrow through the sand but are too small to significantly alter sediment structure compared with burrowing macrofauna. Neither produces mucus to bind sediments nor are they as active as Grant’s amphipods. Thus, although competition is often mentioned as a cause of meiofauna distribution (e.g. Bell, 1983), still too little is known to be able to evaluate its importance to meiofauna communities. If short-term competitive interactions do not control depth profile, then what does? Wilson (1984) found that polychaetes on an intertidal gradient responded to habitat differences rather than competition when transplant experiments were conducted. Certainly physical factors change over vertical profile in sands (Grant, 198 1) and several authors have correlated such factors as 0, content and H, S with meiofauna abundance (Hicks & Coull, 1983). The species studied here were able to locate vertical depth as they would in the field without food signals (laboratory columns were azoic) or interference competition. It is not clear what physical factor (or factors) these animals responded to, but their precise location with depth in our sand columns suggests a relationship with surface diffusion. No RPD was observed, although 0, and dissolved organics entered from a sediment-water interface. The fact that some animals located at the bottom of the sand column (almost in a mirror-image of the pattern found near the surface) suggests that a signal is derived from this diffusion gradient. Alternatively, a species may seek a deeper depth distribution to avoid tidal resuspension. This seems particularly likely with Tryphoema which shows no tendency to swim in laboratory settings, and has excellent holdfast capabilities. Certainly more work is needed to understand the factors which control vertical profile; however, investigators must be aware that competition for space does not always regulate vertical position in meiofauna. ACKNOWLEDGMENTS
This research was conducted while the first author was a Visiting Scientist at the Institute for Marine Environmental Research. We gratefully thank C. Draper for
180
J.W. FLEEGER
AND J.M. GEE
technical assistance, R. Warwick for many helpful discussions and P. Culley and R. Clarke for statistical advice. R. Warwick, B. Coull, T. Chandler, A. Decho and T. Shirley improved earlier versions of this manuscript. This work is part of the benthic ecology programme of the Institute for Marine Environmental Research, a component body of the National Environmental Research Council.
REFERENCES BELL, S. S., 1983. An experimental study of the relationship between below-ground structure and meiofauna taxa. Mar. Biol., Vol.76, pp. 33-39. BELL, S. S. & B.C. COULL, 1980. Experimental evidence for a model of juvenile macrofauna-meiofauna interactions. In, Marine benthic dynamics, edited by K.R. Tenore & B.C. Coull, University of South Carolina Press, Columbia, SC, pp. 179-194. BOADEN, P. J. S., 1977. Thiobiotic facts and fancies (aspects of the distribution and evolution of anaerobic meiofauna). Mikrofauna Meeresboden, Vol. 61, pp. 45-63. BRANCH, G. M., 1984. Competition between marine organisms: ecological and evolutionary implications. Oceanogr. Mar. Biol. Annu. Rev., Vol. 22, pp. 429-593. BRENCHLEY, G.A., 1981. Disturbance and community structure: an experimental study of bioturbation in marine soft-bottom environments. J. Mar. Rex, Vol. 39, pp. 767-790. BRENCHLEY, G.A., 1982. Mechanisms of spatial competition in marine soft-bottom communities. J. Exp. Mar. Biol. Ecol., Vol. 60, pp. 17-33. BROMLEY, R.G. & A. A. EKDALE, 1984. Chondrites: a trace fossil indicator of anoxia in sediments. Science, Vol. 224, pp. 872-874. CHANDLER, G. T. & J. W. FLEEGER, 1984. Tube-building by a marine meiobenthic harpacticoid copepod. Mar. Bioi., Vol. 82, pp. 15-19. CONNELL, J. H., 1980. Diversity and the coevolution of competitors, or the ghost of competition past. Oikos, Vol. 35, pp. 131-138. COULL, B.C. & J. W. FLEEGER, 1977. Long-term variation and community dynamics of meiobenthic copepods. Ecology, Vol. 58, pp. 1136-l 143. FENCHEL, T., 1978. The ecology of micro- and meiobenthos. Annu. Rev. Ecol. Syst., Vol. 9, pp. 99-121. GEE, J. M. & R. M. WARWICK, 1984. Preliminary observations on the metabolic and reproductive strategies of harpacticoid copepods from an intertidal sandflat. Hydrobiologia, Vol. 118, pp. 29-37. GRANT, J., 1981. Dynamics of competition among estuarine sand-burrowing amphipods. J. Exp. Mar. Biol. Ecol.. Vol. 49, pp. 255-265. HARDY, B.L.S., 1978. A method for rearing sand-dwelling harpacticoid copepods in experimental conditions. J. Exp. Mar. Biol. Ecol., Vol. 34, pp. 143-149. HARRIS, R. P., 1972. Horizontal and vertical distribution ofthe interstitial harpacticoid copepods ofa sandy beach. .I. Mar. Biol. Assoc. U.K., Vol. 52, pp. 375-387. 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 I-222. HOXHOLD, S., 1974. Zur Populationsstruktur und Abundanzdynamik interstitieller Kalyptorhynchia (Turbellaria, Neorhabdocoela). Mikrofuuna Meeresboden, Vol. 41, pp. 1-134. JENSEN, P., 1983. Meiofauna abundance and vertical zonation in a sublittoral soR bottom, with a test of the Haps corer. Mar. Biol., Vol. 74, pp. 319-326. JOINT, I.R., J.M. GEE & R.M. WARWICK, 1982. Determination of fine-scale vertical distribution of microbes and meiofauna in an intertidal sediment. Mar. Biol., Vol. 72, pp. 157-164. LEVIN, L.A., 1982. Interference interactions among tube-dwelling polychaetes in a dense infaunal assemblage. J. Exp. Mar. Biol. Ecol., Vol. 65, pp. 107-119. LEVINTON, J.S., 1977. Ecology of shallow water deposit-feeding communities, Quisset Harbor, Massachusetts. In, Ecology of marine benfhos, edited by B.C. Coull, University South Carolina Press, Columbia, SC, pp. 191-227.
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MAGUIRE,C., 1977. Meiofaunal community structure and vertical distribution: a comparison of some Co. Down beaches. In, Biology ofbenthic organisms, edited by B.F. Keegan, P.O. Ceidigh & P.3. S. Boaden, Pergamon Press, Oxford, pp. 425-43 1. MAIORANA,V.C., 1977. Density and competition among sunfish: some alternatives. Science, Vol. 195, p. 94 only. MARCOTTE,B.M., 1984. Behaviorally defined ecological resources and speciation in Tisbe (Copepoda: Harpacticoida). J. Crust. Biol., Vol. 4, pp. 404-416. MCINTYRE,A. D. & R. M. WARWICK, 1984. Meiofauna techniques. In, Methods for the study of marine benthos, 2nd edition, edited by N.A. Holme & A. D. McIntyre, Blackwell Scientific Publications, Oxford, pp. 217-244. MIELKE. W., 1976. ijkologie der Copepoda eines Sandstrandes der Nordseeinsel Sylt. ~ikro~a~~n~7 Meeresboden, Vol. 59, pp. I-86. MOORE,C. G., 1979.The zonation ofpsammolittoral harpacticoid copepods around the Isle of Man. J. Mar. Biol. Assoc. U.K., Vol. 59, pp. 71 l-724. PETERSON,C.H., 1979. Predation, competitive exclusion and diversity in the soft-sediment benthic communites of estuaries and lagoons. In, Ecologicalprocesses in coastal and marine systems, edited by R. J. Livingston, Plenum Press, New York, pp. 233-264. PETERSON,C. Ii. & S. V. ANDRE, 1980.An experimental analysis of interspecific competition among marine filter feeders in a soft-sediment environment. Ecology, Vol. 61, pp. 129-l 39. PLATT,M.M., 1977. Vertical and horizontal distribution of free-living marine nematodes from Strangford Lough, Nnrthern Ireland. Cah. Biol. Mar., Vol. 18, pp. 261-273. POLLOCK,L. W., 1970. Distribution and dynamics of interstitial tardigrada at Woods Hole, Massachusetts, USA. Ophelia, Vol. 7, pp. 145-166. RICKLEFS,R. E., 1973. Ecology. Chiron Press, New York, 966 pp. RIEMANN,F. & M. SCHRAGE,1978. The mucus-trap h~othesis on feeding of aquatic nematodes and implications for biodegradation and sediment texture. Oecologia (Berlin), Vol. 34, pp. 75-88. SAS INSTITUTE,INC., 1982. SAS user’s guide: statistics. SAS Institute, Inc., Gary, North Carolina, 923 pp. SCHMIDT,P. & G. TEUCHERT,1969. Quantitative Untersuchungen zur ijkologie der Gastrotrichen im Gezeiten-Sandstrand der Insel Sylt. Mar. Biol., Vol. 4, pp. 4-23. SCHOENER,T.W., 1974. Resource partitioning in ecological communities. Science, Vol. 185, pp. 27-39. SEVERIN,K. P., S. J. CULVER& C. BLANPIED, 1982. Burrows and trails produced by ~ui~~uelocu~~~a impressa Reuss, a benthic foraminifer, in fine-grained sediment. ~edimento~o#, Vol. 29, pp. 897-901. SIEGEL, S., 1956. Nonparametric statisticrfar the behavioral sciences. McGraw-Hill, New York, 450 pp. WARWICK,R.M., 1971. Nematode associations in the Exe estuary. I. Mar. Biol. Assoc. U.K., Vol. 51, pp. 439-454. WILSON,W.H., JR., 1981. Sediment-mediated interactions in a densely populated infaunal community: the effects of the polychaete Abarenicola pa&a. J. Mar. Res., Vol. 39, p. 135-748. WILSON,W. H., JR., 1983.The role of density dependence in a marine infaunal community. Ecology, Vol. 64. pp. 295-306. WILSON,W. H., JR.. 1984. Non-overlapping distributions of spionid polychaetes: the relative importance of habitat and competition. J. Exp. Mar. Biol. Ecol., Vol. 75, pp. 119-127, WOODIN, S.A. & J.B.C. JACKSON, 1979. Interphyletic competition among marine benthos. Am. Zoo/., Vol. 19, pp. 1029-1043.
173
Elsevier
JEM 621
DOES INTERFERENCE
COMPETITION
DISTRIBUTION
DETERMINE
OF MEIOBENTHIC
THE VERTICAL
COPEPODS?
J. W. FLEECER Department of Zoology and Physiologv, Louisiana State University, Baton Rouge, LA 70803, U.S.A.
and
J.M. N.E.R.C.
GEE
Institutefor Marine Environmental Research, Prospect Place, The Hoe, Plymouth, PLl 3DH, Devon, England
(Received 11 July 1985; revision received 10 October 1985; accepted 30 October 1985) Abstract: The meiobenthic copepod assemblage in the sand flats of the Exe estuary, Devon, England, is vertically segregated with the mean depths of individual species each offset by a few millimeters. This distribution pattern suggests resource partitioning for vertical space. An experiment was performed to determine if interference competition for space resulted in a competitive hierarchy that determined vertical position. Asellopsis intermedia (T. Scott) and Tryphoema bocqueti Bozic were added in known densities to laboratory maintained, azoic sand columns. With no other species present, both species relocated at depths very similar to their low tide field distributions. Mean depths, and the distributions as a whole of each species were also compared in single species and mixed species situations. No competitive mediated shifts in vertical position occurred. With the lack of response to ecological release and the lack of competitive displacement, we could find no evidence that vertical profile was governed by interference competition for space. Although segregated vertical patterns are common for interstitial meiofauna, and many authors have suggested that competition may regulate this pattern, other factors, perhaps related to diffusion gradients from the sediment surface downward, may be responsible. Key words: meiofauna; space competition; copepods; copepods and vertical distribution;
Tryphoema
bocqueti; Asellopsis intermedia
Meiofauna in capillary sands live in a three-dimensional environment which often extends to depths of 50 cm or more in aerobic sands (Fenchel, 1978; Hicks & Coull, 1983). Species in such environments frequently display a distinct and predictable vertical zonation. This pattern, in which the vertical location of closely related species is slightly offset, has been shown in a number of meiofauna taxa including nematodes (Warwick, 1971; Boaden, 1977; Platt, 1977; Jensen, 1983), tardigrades (Pollock, 1970), gastrotrichs (Schmidt & Teuchert, 1969; Boaden, 1977; Maguire, 1977; Hogue, 1978), harpacticoid copepods (Harris, 1972; Mielke, 1976; Moore, 1979; Joint et al., 1982) and turbellarians (Hoxhold, 1974; Boaden, 1977; Maguire, 1977). Such field distributional patterns may be the result of competition (Peterson, 1979; Branch, 1984) and 0022-0981/86/%03.50 0 1986 Elsevier Science Publishers B.V. (Biomedical Division)
174
J.W.FLEEGERANDJ.M.GEE
the offset vertical position is identical to the type of niche-shift expected by competition theory (Schoener, 1974). Several authors (Boaden, 1977; Coull& Fleeger, 1977; Hogue, 1978; Hicks & Coull, 1983) have referred to this commonly observed vertical pattern as resource partitioning. Competition may influence this vertical field distribution in at least two ways. On the one hand, vertical position may be the direct result of interference competition for space in which one species out-competes or aggressively “drives off’ another species from that space. Interference competition is common in hard substratum communities where overgrowth can occur, but rare in soft sediments (Peterson, 1979; Woodin & Jackson, 1979). Nevertheless aggressive encounters have been reported among meiobenthic copepods (Marcotte, 1984) and between small tube-building polychaetes (Bell & Coull, 1980; Levin, 1982). Interference competition for space could be especially important among interstitial and burrowing meiofauna in dynamic shallow sand flats in which sands and fauna are mixed by tidal resuspension. It is likely that fauna in such environments must resort themselves vertically after a tidal disturbance, and such a redistribution could be determined by a competitive hierarchy. Grant (1981) has experimentally shown competitive displacement between two sand flat amphipods. On the other hand, competition effects on the community may be purely historical, having acted as a selective force for habitat partitioning (Connell, 1980). The result would be species-specific tolerance limits and preferred depth ranges. Without experimentation it is not possible to discriminate between these two types of competition (if either occurs), and their roles in regulating meiofauna community structure. Joint et al. (1982) have shown that, in summer, the community of harpacticoid copepods inhabiting tidally disturbed sandflats in the Exe Estuary, Devon, England, is predictably found in a distinct, fine scale, vertical zonation sequence which does not vary even though the mean depth of individual species varies at different tidal stages. Similarly, field sampling prior to this study, in November, 1984, indicated that the vertical zonation sequence is persistent throughout the year. The purpose of this investigation was to test experimentally for spatial interference competition among these sand-dwelling harpacticoids by establishing single and mixed species populations in azoic laboratory sand columns. Differences in depth profile of one species in the absence or presence of another species would be interpreted as evidence that interference competition for space is taking place in extant communities.
MATERIALS
AND METHODS
From the seven most common harpacticoids
in the Exe sandflat community,
Asellopsis intermedia (T. Scott) and Tryphoema bocqweti Bozic were chosen as experi-
mental subjects because: (1) they live near the surface (O-3 cm) of these tidally mixed sands; (2) they are abundant with similar but distinctly offset mean depths (respectively, the second and third species from the surface in the vertical sequence); (3) they proved
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to be readily identifiable under low magnification while living; and (4) they could be handled and extracted without mortality. Given the tidal resuspension common on this sand flat, the maintenance of vertical position may be actively maintained, potentially as the result of a competitive hierarchy. Sand columns were prepared from washed Exe sandflat surface (O-3 cm) sediment which had been dried at 100 “C for 24 h and sieved through a graded sieve set. Sand from two sieve fractions (250 and 375 pm) was retained and mixed in equal amounts. This sand was added, to a depth of 25 mm, to columns made from 16-mm internal diameter plastic disposable syringe barrels modified for attachment to a micrometer after Joint et al. (1982). Mesh fabric (150 pm), fastened to the bottom of the column by a rubber band, was used to hold sand in place. Columns were clamped vertically just below the surface of a flow-through sea-water tank with constant temperature (16 oC), salinity (25x,), and light regime, and allowed to equilibrate for 24 h. These sand columns are similar to the “floating culture tubes” used by Hardy (1978) to successfully rear Asellopsis intermedia (hereafter referred to as Asellopsis). Hardy maintained various life history stages for months in tubes with a thin layer of sand covering a mesh fabric exposed to the water column. Asellopsis and Tryphoema bocqueti (hereafter referred to as Tryphoema) were extracted from freshly collected Exe estuary sand within 24 h by elutriation using MgCl, (McIntyre & Warwick, 1984); Asellopsis and Tryphoema were sorted and counted under a stereomicroscope immediately. Sand columns were removed from the water bath, and after draining, known numbers of either species alone or a mixture of both species were added to the sand surface by pipette. The top of the column was covered by 130~pm mesh screen; the column shaken to disperse the copepods, and replaced into the water bath for 24 h before the sand was sectioned into 25 l-mm thick sections by the micrometer method. Core fractions were fixed in 5% formalin and copepods later identified under a stereomicroscope. Known numbers (ranging from 60-260) of adult Asellopsis and Tqphoema were added to a total of 37 laboratory sand columns. Typically we added z 100 individuals in single or 200 total individuals (100 of each species) in mixed species experiments. Although densities and reproductive activities of both species fluctuate throughout the year (Gee &Warwick, 1984), densities used in the columns range from near the average field density (equivalent to z 100 of Asellopsis or Tryphoema in each column) to about twice normal (200 or more per column) for each species. Weighted mean depths for each species from the upper 15 mm of each replicate were calculated by SAS (SAS Institute Inc., 1982) programming. Frequency distributions for each species over l-mm depth intervals for each replicate were also determined. Parametric statistics comparing mean depth with densities were calculated by SAS GLM. Actual depth distributions were also compared using non-parametric statistics (Kolmogorov-Smirnov two-sample test) following the procedures of Siegel (1956).
176
J. W. FLEEGER AND J.M. GEE RESULTS
Both species were recovered from the experimental sand columns at ~87% efficiency. Discrepancies were probably due either to escape through the bottom of the column, or through loss by pipette transfer or by undercounting live animals. If the upper 15 mm are considered, the laboratory distributions of both species were quite similar to the field distributions of Joint et al. (1982); the majority of individuals were in the upper 3-8 mm with steadily declining densities through 15 mm. Although 92% of each species was recovered in the upper 15 mm, there was a tendency in both species for some aggregation at 23-25 mm especially in densely populated (single and mixed species) laboratory columns. This bimodal vertical distribution was not observed in field samples, and could have resulted from the fact that the bottom of the column was directly exposed to sea water. With diffusion through the bottom, both species may have recognized the column bottom as another “surface”. For this reason, vertical distributions are hereafter considered only through the upper 15 mm. Of the two species, Aselfopsis was consistently found at slightly shallower depths in all laboratory sand columns (Figs. 1 and 2). Furthermore, the mean depth differential between the two species in the laboratory was remarkably similar to that found from low tide field samples when all species in the taxocene were present. In single species
. .
!.: .: :. . .
l
l
.
ASELLOPSIS 6-
50
100
INTERMEDIA 150
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.
-z =-
250 .
.
J% I
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.
x3
;
i
.
%
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. TRYPHOEMA 50
100
NO. INDIVIDUALS
BOCQUETI I 150
I 200
250
ADDED
Fig. 1. Mean depth of Asellopsis intermedia plotted against the number of A. intermedia added to experimental sand columns (upper) and mean depth of Tryphoema bocqueti plotted against the number of T. bocqueti added to experimental sand columns (lower).
COMPETITION FOR SPACE BY MEIOFAUNA
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trials, the overall mean depth of Asellopsis was 3.1 mm, compared to 3 mm from field collections, and for ~~~~~~ overall mean depth was 4.2 compared to 5 mm from the field (field data from Joint et al., 1982). Clearly both species of copepods responded to laboratory sands by locating depth strata as they do in the field, and ecological release (sensu Ricklefs, 1973, p. 692) in resource utilization did not take place. Single species experimental densities were varied from near normal field densities (Z 100 per column) to about twice normal (200 or more per column) in an attempt to determine if depth profile was density dependent, and influenced by intraspeci~c competition (Maiorana, 1977; Grant, 1981). Linear regression was used to test for a relationship of mean depth for a species with the number of individuals of that species added to laboratory sands (Fig. 1). Mean depths did not vary with number of individuals added for Asellopsis (b = 0.0035, P = 0.52), and was not strongly indicated for ~ry~~oe~a (b = 0.010, P = 0.053). Thus at the densities used in these experiments, depth did not vary with increasing intraspeciftc density. in laboratory sand columns in which both species were present, overall mean depths were unchanged compared to single species situations (Fig. 2). Mean depth across replicates ofAsellopsis when Trypkoema was present was 3.2 mm (as opposed to 3.1 mm in single species trials); mean depth of T~phoema with Asellopsis present was 4.5 mm (as opposed to 4.2 mm in single species trials). Two methods were used to test the nuil
INTERMDIA
ASELLOPSIS
. l
.
.
a ...
a
.
..
.
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TRYPHOEMA
NO. INCWDUALS
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Fig. 2. Mean depth of Asellopsis~te~~e~i~plotted against the number of Tryph~e~~bocquetiadded to experimental sand columns (upper) and mean depth of Tryphoem bocquetiplotted against the number of Asellopsisintermediaadded to experimental sand columns (lower).
178
J.W. FLEECER
AND J.M. GEE
hypothesis that there were no shifts in vertical profile in sands with potential competitors. Linear regression tested for a relationship of mean depth with numbers added of the potential competitor. Regressions were calculated using the mean depth for each species in each replicate against the density of the potential competitor added to that replicate. This effect should be density related as the shift in depth profile is expected to be greater when competition is stronger (i.e. when higher densities of a potential competitor are present). The slope of the line was not significantly different from zero for either species (Asellopsis, b = 0.0009, P = 0.70; Tryphoema, b = 0.0035, P = 0.29), and we can not reject the null hypothesis that shifts in mean depth did not occur with increasing “competitor” density. Mean depth is only one measure of a distribution. Changes in any aspect of the depth distribution of a copepod, caused by adding a potential competitor, must also be considered. To test for any change in vertical distribution not restricted to central tendency, a two-tailed Kolmogorov-Smirnov (KS) two-sample test was performed. The distribution (through 15 mm) of a species in single species sands was compared to its distribution in sands with both species present. Because each of these treatments (Asellopsis alone and with Tryphoema; Tvphoema alone and with Asellopsis) was replicated, a Friedman’s two-way ANOVA was first conducted to determine if the distribution among replicates was equivalent; in no case was a significant difference found. Therefore, a distribution for each treatment was prepared by summing the frequency counts at each depth across replicates, and the KS statistic computed (critical values of D were calculated at the 0.05 level). Comparing distribution in single species with that in mixed species situations, the observed value of D was 0.03 1 for Aseflopsis which is less than the critical value of 0.058, and for TVphoema the observed value of 0.057 is essentially identical to the critical value of 0.053. Thus no strong evidence for a competitor related shift or modification in any parameter of its distribution was found for either species.
DISCUSSION
The results of this study can not support the contention that interference competition for space maintains the vertical zonation pattern of Exe sandflat harpacticoids. This does not mean that the depth sequence is unaffected by all forms of competition, or that interference competition is not important for other taxa or in other habitats. Competition could have acted as a historical selective force (Connell, 1980) to derive present day tolerance and depth preferences (as argued by Hogue, 1978). These data suggest that in shallow, frequently mixed sands, a short-term competitive hierarchy does not determine vertical position. Although it has been suggested theoretically that vertical segregation may provide additional resource space (Levinton, 1977) only Peterson & Andre (1980) and Grant (198 1) utilized experimental techniques to identify vertical displacement (interference
COMPETITIONFOR
SPACEBYMEJOFAUNA
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competition) between species. Grant’s study was most similar to ours in design, except that he used very active amphipods which could move throughout the oxygenated zone of a sand flat. However, most soft sediment benthic studies finding an effect of one species on the distribution of another (adult-adult studies) have identified either aggressive interactions between tube-builders (Levin, 1982; Wilson, 1983), or interactions between species which have contrasting effects on sediment properties (Brenchley, 1981, 1982; Wilson, 1981). Although reports of tube-dwelling or burrow construction exist for meiofauna (Riemann & Schrage, 1978; Severin et al., 1982; Bromley and Ekdale, 1984; Chandler & Fleeger, 1984), neither experimental species gives any indication of tube-building or even of the aggressive interspecific encounters observed by Marcotte (1984). In unsorted dishes, Asellopsis and Tryphoema often bumped into each other, eliciting no obvious response, and T. bocqueti was once observed grasping Asellopsis with no ill effect to either species. Both burrow through the sand but are too small to significantly alter sediment structure compared with burrowing macrofauna. Neither produces mucus to bind sediments nor are they as active as Grant’s amphipods. Thus, although competition is often mentioned as a cause of meiofauna distribution (e.g. Bell, 1983), still too little is known to be able to evaluate its importance to meiofauna communities. If short-term competitive interactions do not control depth profile, then what does? Wilson (1984) found that polychaetes on an intertidal gradient responded to habitat differences rather than competition when transplant experiments were conducted. Certainly physical factors change over vertical profile in sands (Grant, 198 1) and several authors have correlated such factors as 0, content and H, S with meiofauna abundance (Hicks & Coull, 1983). The species studied here were able to locate vertical depth as they would in the field without food signals (laboratory columns were azoic) or interference competition. It is not clear what physical factor (or factors) these animals responded to, but their precise location with depth in our sand columns suggests a relationship with surface diffusion. No RPD was observed, although 0, and dissolved organics entered from a sediment-water interface. The fact that some animals located at the bottom of the sand column (almost in a mirror-image of the pattern found near the surface) suggests that a signal is derived from this diffusion gradient. Alternatively, a species may seek a deeper depth distribution to avoid tidal resuspension. This seems particularly likely with Tryphoema which shows no tendency to swim in laboratory settings, and has excellent holdfast capabilities. Certainly more work is needed to understand the factors which control vertical profile; however, investigators must be aware that competition for space does not always regulate vertical position in meiofauna. ACKNOWLEDGMENTS
This research was conducted while the first author was a Visiting Scientist at the Institute for Marine Environmental Research. We gratefully thank C. Draper for
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AND J.M. GEE
technical assistance, R. Warwick for many helpful discussions and P. Culley and R. Clarke for statistical advice. R. Warwick, B. Coull, T. Chandler, A. Decho and T. Shirley improved earlier versions of this manuscript. This work is part of the benthic ecology programme of the Institute for Marine Environmental Research, a component body of the National Environmental Research Council.
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