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On the vertical distribution of a benthic harpacticoid copepod: field, laboratory, and flume results
J. Exp. Mar. Biol. Ecol., 153 (1991) 153-163 © 1991 Elsevier Science Publishers B.V. All rights reserved 0022-0981/91/$03.50
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On the vertical distribution of a benthic harpacficoid copepod: field, laboratory, and flume results Michael S. Foy and David Thistle Department of Oceanography, Florida State University, Tallahassee, Florida, USA (Received 2 April 1991; Revision received 2 July 1991; accepted 17 July 1991) Abstract: To identify a target species for the investigation of factors influencing the vertical distribution of subtidal meiofauna, we conducted a year-long survey of the 2-mm-scale vertical distribution ofharpacticoid copepods at a site at 5 m depth in St George Sound, Florida (29°51'N, 84°31'W). We found that Leptastacus el. rostratus Nicholls seldom occurs in surface sediments and that its population maximum is in the 2nd cm of sediment. The results of a preference experiment suggest that factors intrinsic to the sediment column do not cause L. cf. rostratus to be rare in the 0-l-cm layer. A flume experiment demonstrated that this species burrows deeper into the sediment in response to increased flow, suggesting that Leptastacus cf. rostratus finds the surface sediments unattractive under high-flow conditions. Our results suggest that near-bottom flow influences the vertical distribution of Leptastacus at this subtidal site.
Key words: Benthos; Flow effect; Harpacticoid copepod; Meiofauna
INTRODUCTION
The identification of mechanisms controlling species' distributions remains a central concern in meiofaunal ecology (Hicks & Coull, 1983). In particular, although species can inhabit distinct mm-scale depth horizons within the sediment (Joint et al., 1982; Fleeger & Gee, 1986; Coull et al., 1989), the ecological factors responsible for this zonation are as yet little known, and no general relationships have been established. To study this issue, we have chosen to investigate factors that could influence the vertical distribution of a subtidal benthic harpacticoid copepod. From what is known of harpacticoid biology, it is possible a priori to identify factors that could affect the vertical distribution of a subtidal species. Predation has been shown to do so (Gee, 1987; Coull et al., 1989; Ellis & Coull, 1989). Because food items are not uniformly distributed in the vertical dimension (Joint et al., 1982) and species have preferences among food items (Rieper, 1982; Carman & Thistle, 1985), vertical differences in preferred foods could have an effect. Because physical properties of the sediment such as grain size have been shown to affect harpacticoids (Jansson, 1967; Correspondence address: D. Thistle, Department of Oceanography, Florida State University, TaUahassee, FL 32306, USA. Contribution 1060 from the Florida State University Marine Laboratory.
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Gray, 1968; McLachlan et al., 1977), such factors could play a role. Because erosion could expatriate suspended individuals to unsuitable habitats (Palmer & Gust, 1985) or expose them to water-column predators (D'Amours, 1988) and because the probability of an individual's being eroded is a function of the strength of the near-bottom flow and the individual's proximity to the sediment surface, harpacticoids might alter their vertical distributions in response to near-bottom flow (Palmer & Molloy, 1986). Finally, interspecific competition is a potential influence on vertical distribution (Fleeger & Gee, 1986). In this study, we first determined the fine-scale vertical distribution of a harpacticoid copepod species and then conducted a preference experiment to determine whether its vertical distribution was influenced by factors inherent in its immediate sedimentary environment, such as food items, grade of sediment, or the presence of competitors. No indication was found that such factors influenced the vertical distribution of our test species. Among possible alternative hypotheses (e.g., predation by demersal predators), we chose to study the influence of near-bottom flow with a flume experiment.
MATERIALS AND METHODS LOCALITY
The study site (29°51'N, 84°31'W) was located at a depth of 5 m in St George Sound, ~, 3 mi south of the Florida State University Marine Laboratory (see Fig. 1 of Reidenauer, 1989). The sediment was an unvegetated fine sand (mean grain size 0.254 mm) (Reidenauer, 1989). Ripples with a wavelength of 10-30 cm, observed on some visits, indicated that the site experiences near-bottom flows strong enough to move the sediment and erode harpacticoids. The site was defined by two parallel 10-m transect lines set 3 m apart and marked at 10-cm intervals. A movable 3-m cross-line, also marked at 10-cm intervals, was used to form a Cartesian coordinate system. All samples were taken at randomly chosen coordinates within the study site. MONTHLY SAMPLES
To identify a species for study and to document its fine-scale vertical distribution, scuba divers took four 15.5-cm 2 cores each month from November 1988 through October 1989. Rough seas made it necessary to transport the cores to shore before vertical sectioning. The trip took ~, 30 min during which the cores were kept in a water bath under approximately in situ temperature and light conditions. On shore, processing was begun immediately and completed in 30 min. The top 3 cm of each core was sliced into 15 2-mm layers with a precision extruder (Fuller & Butman, 1988). The layers were preserved in a sodium-borate-buffered solution of formaldehyde and tap water (1:9, v : v) with rose bengal (Fisher Scientific, Fair Lawn, New Jersey). In the laboratory, we
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155
used a modification of the Barnett (1968) troughing technique to concentrate the harpacticoids from the sediment. Specifically, each 2-mm layer from a core was placed in the through without presieving, and the fraction to be sorted was caught on a 62-/~m sieve. The median efficiency of the procedure in our laboratory on similar sediments was 100~ (n - 5). All adult harpacticoid copepods were removed under a dissecting microscope.
PREFERENCE EXPERIMENT
To investigate effects of the factors intrinsic to the sediment on the vertical distlibution of our target species, we performed a preference experiment. A few adults of the target species were collected by swirl decantation (Pfannkuche & Thiel, 1988) from the 2nd cm of sediment from a 9.6-cm 2 core. These individuals were stained with the vital dye neutral red (Kodak, Rochester, New York), so they could be distinguished from individuals of the same species that might occur naturally in the sediment used in the experiments. (After preliminary experimentation, we chose a concentration of 0.001% (w" v) neutral red in 63-#m-filtered seawater and a staining time of 40 min.) The staining procedure did not seem to affect the behavior or viability of the test animals (pers. obs.). After staining, one individual was chosen at random to be used in a given run of the preference experiment. We used single test animals to make the smallest possible perturbation to the assemblage present in the test sediment. By choosing test individuals at random, we sampled the sexes in approximately their field proportions, making the experimental results comparable to the field distribution data. To assure independence, each test animal was obtained from a different core. The sediment used for the preference experiment came from 3.8-cm 2 cores taken at random from the study site on a single day. The top 2 cm of a core was extruded intact (including the fauna) into a "collar" (a 2-cm-tall piece of the same core stock). The sediment-filled collar was sliced free from the core, and a stained test animal was placed on the surface of the sediment with a micropipet. The collar and sediment were then placed in a container, seawater was added until a few millimeters of water covered the sediment surface, and the container was placed in the dark (to eliminate the possibility that differences in illumination among the replicates could affect the results) and kept at in situ temperature. In 15 of 30 runs, the collar and the test sediment were inverted before the test individual was added so that a preference for the 1-2-cm layer based on some intrinsic factor could be distinguished from a geotactic response (e.g., Hill & Elmgren, 1987). That is, if the animal regulates its vertical position in reference to the sediment-water interface, the test individuals would move to the lower layers in both the upright and inverted sediment. The duration of the experiment was chosen to be as short as possible to minimize changes in porewater chemistry and sediment microbiology yet long enough to allow test animals sufficient time to reach the full depth of the sediment column. Preliminary
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experiments suggested that 90 min was a reasonable compromise. Therefore, after 90 min, the sediment in each collar was extruded and sliced into 10 2-mm layers.
FLUME EXPERIMENT
The flume used in our experiment was patterned after that described by Nowell et al. (1981). Entrance and exit conditions meet the criteria of Nowell & Jumars (1987). Briefly, it is a clear acrylic duct 5 m long, 0.5 m wide and 20 cm deep. A removable bottom plate is located 4.5 m from the entrance of the flume. Sediment cores can be mounted in it, coplanar with the bed of the flume. Seawater is supplied to a 416-1 constant-head tank. Flow enters the flume through a 10. l-cm (inner diameter) T-shaped diffuser and then is rectified through a "honeycomb" of hexagonal cells, each 0.5 cm in widest dimension. The discharge from the constant-head tank is regulated by a butterfly valve. A tail gate of eight vertical louvers (each 6.25 cm wide) allows uniform flow to be established across the width of the flume. At the end of the flume, the seawater falls freely into a tail tank from which it can flow to a drain or be returned to the head tank. The return system includes four pumps (each capable of moving ~, 1141. min - ~) that operate in parallel. The long axis of the flume can be tilted through angles up to 1.5 °. Our experiment was designed to determine whether a target species responded to flow differences by moving deeper into the sediment when exposed to relatively high flow. For each flume run, we took two sediment cores at random from the study site. We obtained and prepared test animals and placed them in cores following the procedures described for the preference experiment, except that the cores were collected on the day the flume run was done. The cores were mounted intact (includifig the fauna) in the flume bed, each 5 cm to one side of the center line of the flume and 4.625 m from the flume entrance. Six flume runs (three high flow and three low flow) were conducted on each of 7 days. The first run of the 1st day was randomly chosen to be a low-flow run. Thereafter, runs alternated between the two flow conditions. The seawater in the flume was filtered through a mesh of 61-/~m aperture, and the depth was maintained at 6 cm during both flow conditions. At the end of each run, the water was drained from the flume. So that the water overlying the cores could drain away without disturbing the sediment surface, a tube with a vertical row of holes 3 mm in diameter was placed over each core. After the flume had been drained, the cores were removed, and the top 2 cm of sediment was sliced into 10 2-ram layers. These fractions were preserved as above. On the day following each set of six flume runs, one of the two cores from each run was chosen at random, and the vertical position of the test animal was determined. The second core was processed only if the test animal was not found in the first core. During preliminary trials, we arrived at settings of the flume parameters (e.g., louver openings) that produced two flows of markedly different velocities. The higher flow approached, but was not equal to, the velocity required to set the sediment on the surface
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Fig. I. Electron micrograph of a gravid female Leptastacus. Scale bar, 0.1 mm.
of the cores in motion. After the completion of the flume experiment, we measured the t w o velocities by timing the movement of neutrally buoyant particles (Carey, 1983)over a 40-cm path just u p s t r e a m of the location of the cores. M e a s u r e m e n t s were m a d e on particles in the middle third of the 6-cm water column. Three velocity m e a s u r e m e n t s were m a d e during each of seven low-flow and seven TABLE I
Results of preference experiment. In half trials, sediment column was in its natural upright orientation; in half trials, sediment column was inverted. Entries indicate number of animals found in each layer after 90 min. Sediment depth (mm)
Upright
Inverted
0-2 2-4 4-6 6-8 8-10 10-12 12-14 14-16 16-18 18-20
8 1 2 0
5 3 0 0
0
0
0 0 1
0 0 1
0
1
1
1
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M.S. FOY AND D. THISTLE
high-flow runs. The runs alternated between the two flow conditions. Mean velocity was 3 c m . s - ~ (n = 7, SD = 0.5) for the low-flow condition and 20 c m . s - ~ (n = 7, SD = 0.4) for the high-flow condition. RESULTS
At the end of the 2nd month of sampling, we chose the interstitial species (Svedmark, 1964) Leptastacus cf. rostratus Nicholls (hereafter, Leptastacus) (Fig. 1) as the target species because it appeared to inhabit a distinct depth horizon. Although the vertical distribution of Leptastacus varies from month to month (Figs 2-4), few individuals are found in the top cm of sediment, and only rarely are individuals found in the top 2 mm. The peak in population abundance is found in the 2nd cm of sediment throughout the year. Further, a Kruskai-Wallis rank sum test (with the large-sample approximation; Hollander & Wolfe, 1973) reveals that, over the year, significantly more Leptastacus are present in the 2nd cm of sediment than in the 1st or 3rd (p < 0.0001). In the preference experiment, the test animal was recovered in 24 of the 30 runs. The majority of animals did not move far from where they were introduced (Table I). Nine of the 13 animals remained in the uppermost 4 mm of sediment when the sediment column was in its natural (upright) orientation, and eight of the 11 animals remained there in the inverted condition. The results of the flume experiment are illustrated in Fig. 5. After being exposed to the low-flow condition, 12 of the 21 test animals were found in the top 2 mm of sediment
MEAN NUMBER OF ADULTS 0 O-2 2-4 4-6 6-8 8-10 10-12 12-14
10
20
30
0
10 po. . . . . . . . .
"mE4
20
' . . . . . . . . .
November
30
' . . . . . . . . .
December
i
!
I
q i
16-18
E E ,,.,,,
I-i1. bJ
i l
18-20 2O-22 m m 22-24 24-26 26-28 28-30
0
t i
10
20
2-4 4-6 6-8 8-10
10-12 12-14 14-16 16-18 18-20 20-22 22-24
24-26 26-28 28-30
30
0
10
20
30
B-~ El-,
0-2
January
~-~m-~
February I I I
! I I
I
I ! I
Fig. 2. Vertical distribution of adult Leptastacus for November 1088 through February 1989. Each bar, mean of four cores. Error bars, 1 SD.
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159
MEAN NUMBER OF ADULTS o
lO
20
0
20
10
0-2 2-4
March
a-lo m 10-12 m m a m
April
------
12-14 14-16 16-18
1 I
m-2o
I
20-22 22-24
A
I
m
24-26 m 26-28 28-30
3: I"a. IJJ rt
B ~
10 ,
o
0-2 k 2-4 4-6
20
30
0
I0
May
10-12 12-14
20
30
June
,,-,6 m 16-18
18-20 20-22 m 22-24 24-26 26-28
m
2.-3o m
Fig. 3. Vertical distribution of adult Leptastacus for March 1989 through June 1989. Each bar, mean of four cores. Error bars, 1 SD.
(the layer in which they were initially placed). After exposure to the high-flow condition, only one of the 21 test animals was found in this layer. Under low-flow conditions, the 0-2-mm layer was both the median depth of the population and the layer where the MEAN NUMBER OF ADULTS 0
20
io
2-4 4.-6
H
July
8-10 10-12 ~
30
0
10
20
30
August
----
12-14 1
4
-
1
6
~
I¢:,--18 i m ~
A
E o
10 , . . . . . . . . .
20
20 ,
0 - 2 I~ ----i
2-4
4-6 m ~ 6-0 ~'~ 8-10 i 10-12
,2-,,
September
m4
m
14-16 16-18
18-2o ,,am
BB--,
22-24 24-26 ~e-2S Ih
IP
2O-22m
October !
28-30
Fig. 4. Vertical distribution of adult Leptastacus for July 1989 through October 1989. Each bar, mean of four cores. Error bars, 1 SD.
160
M.S. FOY AND D. THISTLE HIGH FLOW E E -r
pIx. i,i El I-Z i,1 =E El i,i (/)
o-a
LOW FLOW
"3
2-4
-! I
6-8
I
I
"1
4-6
e-to
. I
7
1
ta-~4 - I 14-16 16-18 IB-20
NUMBER OF ANIMALS PER LAYER
Fig. 5. Summary of flume experiment results. Illustrated are total numbers of test animals found in various layers for 21 high-flow and 21 low-flow runs, respectively.
greatest number of animals was found. In contrast, under the high-flow conditions, the median depth was 4 - 6 mm, and the layer having the most animals w a s the 6 - 8 - m m layer. The A N O V A for the flume-experiment results is shown in Table II. A randomized, mixed-model, factorial design (Kirk, 1982) was employed. The d e p e n d e n t variable was the midpoint of the depth interval at which a test individual was found. Days (a r a n d o m factor) was a blocking factor, and flow and run were fixed-factor treatments. The test animals exposed to high flow were found significantly deeper in the sediment than those exposed to low flow (Table II). The day on which the flume run was conducted affected the depth of the test animal (Table II), but the effects of the time a run was conducted on a given day and the flow-by-run interaction were not significant (Table II). This last
TABLE II
ANOVA table for results of flume experiment. "Flow" treatment had high- and low-velocitylevels and was factor of major interest in experiment. "Run" treatment refers to temporal position of a given replication of experiment on day it was done and had three levels. Day on which an experiment was done was used as a blocking factor; it had six levels. NS indicates p > 0.05. Source
ss
df
Ms
Treatments Flow Run Interaction Bloc} (days) Resicaal fotal
30.86 3.86 2.71 ! 5.62 25.24 78.29
1 2 2 6 30 41
30.86 1.93 1.36 2.60 0.84
Probability p < 0.0005 NS NS
0.01 < p < 0.025
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result suggests that any variation introduced by the longer holding time of cores run late in the day is modest and is unlikely to contribute importantly to the dramatic difference in migration depths between flow conditions. DISCUSSION
We believe that our monthly samples reflect the vertical distribution of Leptastacus in nature. Although 30-60 min elapsed between when each core was taken and when it was sliced into layers, we known from the preference experiments that in 90 min 71 of Leptastacus individuals had net displacements of < 6 mm, so the delay alone is unlikely to have altered their vertical distribution on the cm scale, which is the scale of our interest. To minimize the chance that sampling or transportation disturbance altered their distribution, we inserted cores slowly and transported them in a vibration-damping water bath. We could not, of course, eliminate all disturbance, but, in samples taken and processed in a similar manner from a 20-m site, the median depth of Leptastacus was also in the 2nd cm and several other harpacticoid species had maxima in the 0-2or 2-4-mm layers (unpubl. data), indicating, at the least, that our procedures do not result in a general movement of harpacticoids out of the near-surface layers. Our preference experiment was designed to determine whether factors intrinsic to the sediment such as differences in microflora, granulometry, or competitors were responsible for Leptastacus's vertical distribution in nature. Ifthe 0-1-cm layer were unattractive, or the l-2-cm layer attractive, because of intrinsic factors, we would expect the test animals to be found in the lower 1-cm fraction in the upright condition and in the upper l-cm fraction in the inverted condition (i.e., in sediments where they are normally abundant in nature). If Leptastacus regulated its vertical position with respect to the sediment-water interface, we would expect the test animals to be found in the lower 1-cm fraction in both the upright and inverted conditions. The results for the upright condition (Table I) show that, although the test animals were capable of migrating into the 1-2-cm layer, most (11 of 13) stayed in the 0-1-cm layer. In fact, eight of 13 did not move from the 0-2-mm layer, where they are least common in nature (Figs 2-4). We therefore conclude that the low abundance of Leptastacus in the 0-1-cm layer in nature is not caused by some intrinsic unattractiveness of that layer. That is, either such potential factors as granulometry, microbes, or competitors do not vary over the top 2 cm, or any differences between the 0-l-cm layer and the 1-2-cm layer are unimportant to the species in terms of controlling its vertical distribution. That the test animals in both the upright and the inverted cases tended to remain near the top of the sediment column suggests that Leptastacus does not prefer to live at depth in nature because of a geotactic response. In contrast, Fleeger & Gee (1986) found that two other harpacticoid species from an intertidal sand flat took up their natural depths in azoic laboratory sediment columns.
162
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Of the remaining factors that might influence Leptastacus's distribution, we chose to investigate flow. The flume experiment demonstrated that Leptastacus moves out of the surface layers when exposed to a flow that is just suberosive. The ripples in the seabed frequently observed at our site imply flows of erosive magnitude (Middleton & South~rd, 1984), i.e., stronger flows than those used in the flume experiment, so the behavior we have observed in the flume experiment is likely to occur in the field. We conclude that at least a part of Leptastacus's vertical distribution pattern arises because of the response to strong near-bottom flows. Our study did not address the question of why Leptastacus should move deeper into the sediment when exposed to strong near-bottom flows, but, given its size and specific density, the nearer an individual is to the sediment surface, the greater is its probability of being suspended during periods of strong flow. We observed that Leptastacus is a poor swimmer, and we suspect that it moves away from the sediment surface to avoid being suspended in the water column. Although a variety of reasons can be proposed to explain why being in the water column could be disadvantageous for such a species (Palmer, 1988), no data exist to justify selection among them. ACKNOWLEDGEM ENTS
The manuscript has been improved by the comments of S. C. Ertman, P. A. LaRock, M.A. Palmer, D. Nof and A.B. Thistle. A.R.M. NoweU, P.A. Jumars and S.C. Ertman provided advice on flume design. The flume was built by J. Winne, D. Oliff and K. Collins. J.E. Eckman gave us the "honeycomb" for the flow straightener. This research was supported by NSF grant OCE-8911181 and ONR contract N00014-87G-0209 to D. Thistle. We express our thanks for this kind help. REFERENCES Barnett, P. R. O., 1968. Distribution and ecology of harpacticoid copepods of an intertidal mudflat. Int. Rev. Gesamten Hydrobiol., Vol. 53, pp. 177-209. Carey, D.A., 1983. Particle resuspension in the benthic boundary layer induced by flow around polychaet~ tubes. Can. J. Fish. Aquat. Sci., Vol. 40, pp. 301-308. Carman, K.R. & D. Thistle, 1985. Microbial food partitioning by three species of benthic copepods. Mar. Biol., Vol. 88, pp. 143-148. Coull, B. C., M. A. Palmer & P. E. Myers, 1989. Controls on the vertical distribution ofmeiobenthos in mud field and flume studies with juvenile fish. Mar. Ecol. Prog. Set., Vol. 55, pp. 133-139. D'Amours, D., 1988. Vertical distribution and abundance of natant harpacticoid copepods on a vegetatec tidal flat. Neth. J. Sea Res., Vol. 22, pp. 161-170. Ellis, M.J. & B.C. Coull, 1989. Fish predation on meiobenthos: field experiments with juvenile spol Leiostornus xanthurus Lacepede. J. Exp. Mar. Biol. Ecol., Vol. 130, pp. 19-32. Fleeger, J.W. & J.M. Gee, 1986. Does interference competition determine the vertica| distribution o meiobenthic copepods? J. Exp. Mar. Biol. Ecol., Vol. 95, pp. 173-181. Fuller, C. M. & C.A. Butme.n, 19~8. g simple technique for fine-scale, vertical sectioning of fresh sedimen cores. J. Sed. Petrol., Vol. 58: pp. 763-768. Gee, J.M.~ 1987. Impact of epibenthic predation on estuarine intertidal harpacticoid copepod populations Mar. Biol., Vol. 96, pp. 497-510.
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Gray, J. S., 1968. An experimental approach to the ecology of the harpacticoid Leptastacus constrictus Lang. J. Exp. Mar. Biol. Ecol., Vol. 2, pp. 278-292. Hicks, G. R. F. & B.C. Coull, 1983. The ecology of marine meiohenthic harpacticoid copepods. Oceanogr. Mar. Biol. Annu. Rev., Vol. 21, pp. 67-175. Hill, C. & R. Elmgren, 1987. Vertical distribution in the sediment in the co-occurring benthic amph!pods Pontoporeia affinis and P. femorata. Oikos, Vol. 49, pp. 221-229. Hollander, M. & D.W. Wolfe, 1973. Nonparametric statistical methods. Wiley, New York, 503 pp. Jansson, B.O., 1967. The importance of tolerance and preference experiments for the interpretation of mesopsammon field distributions. Heigol. Wiss. Meeresunters., Vol. 15, pp. 41-58. 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. Kirk, R.E., 1982. Experimental design. Brooks/Cole, Belmont, California, 911 pp. McLachlan, A., P.E.D. Winter & L. Botha, 1977. Vertical and horizontal distribution of sub-littoral meiofauna in Algoa Bay, South Africa. Mar. Biol., Vol. 40, pp. 355-364. Middleton, G.V. & J.B. Southard, 1984. Mechanics of sediment movement. S.E.P.M. Short Course Number 3. Society of Economic Paleontologists and Mineralogists, Tulsa, Oklahoma, 401 pp. Nowell, A. R. M. & P.A. Jumars, 1987. Flumes: theoretical and experimental considerations for simulation of benthic environments. Oceanogr. Mar. Biol. Annu. Rev., Vol. 25, pp. 191-212. Nowell, A. R. M., P.A. Jumars & J.E. Eckman, 1981. Effects of biological activity on the entrainment of marine sediments. Mar. Geol., Vol. 42, pp. 133-153. Palmer, M.A., 1988. Dispersal of marine meiofauna: a review and conceptual model explaining passive transport and active emergence with implications for recruitment. Mar. Ecol. Prog. Set., Vol. 48, pp. 81-91. Palmer, M.A. & G. Gust, 1985. Dispersal of meiofauna in a turbulent tidal creek. J. Mar. Res., Vol. 43, pp. 179-210. Palmer, M.A. & R.M. Molloy, 1986. Water flow and the vertical distribution of meiofauna: a flume experiment. Estuaries, Vol. 9, pp. 225-228. Pfannkuche, O. & H. Thiel, 1988. Sample processing. In, Introduction to the study ofmeiofauna, edited by R. P. Higgins & H. Thiel, Smithsonian Institution Press, Washington, District of Columbia, pp. 134-145. Reidenauer, J.A., 1989. Sand dollar Mellita quinquiesperforata (Leske) burrow trails: sites for harpacticoid disturbance and nematode attraction. ,7. Exp. Mar. Biol. Ecol., Voi. 130, pp. 223-235. Rieper, M., 1982. Feeding preference of marine harpacticoid copepods for various species of bacteria. Mar. Ecol. Prog. Set., Vol. 7, pp. 303-307. Svedmark, B., 1964. The interstitial fauna of marine sands. Biol. Rev., Vol. 39, pp. 1-42.
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On the vertical distribution of a benthic harpacficoid copepod: field, laboratory, and flume results Michael S. Foy and David Thistle Department of Oceanography, Florida State University, Tallahassee, Florida, USA (Received 2 April 1991; Revision received 2 July 1991; accepted 17 July 1991) Abstract: To identify a target species for the investigation of factors influencing the vertical distribution of subtidal meiofauna, we conducted a year-long survey of the 2-mm-scale vertical distribution ofharpacticoid copepods at a site at 5 m depth in St George Sound, Florida (29°51'N, 84°31'W). We found that Leptastacus el. rostratus Nicholls seldom occurs in surface sediments and that its population maximum is in the 2nd cm of sediment. The results of a preference experiment suggest that factors intrinsic to the sediment column do not cause L. cf. rostratus to be rare in the 0-l-cm layer. A flume experiment demonstrated that this species burrows deeper into the sediment in response to increased flow, suggesting that Leptastacus cf. rostratus finds the surface sediments unattractive under high-flow conditions. Our results suggest that near-bottom flow influences the vertical distribution of Leptastacus at this subtidal site.
Key words: Benthos; Flow effect; Harpacticoid copepod; Meiofauna
INTRODUCTION
The identification of mechanisms controlling species' distributions remains a central concern in meiofaunal ecology (Hicks & Coull, 1983). In particular, although species can inhabit distinct mm-scale depth horizons within the sediment (Joint et al., 1982; Fleeger & Gee, 1986; Coull et al., 1989), the ecological factors responsible for this zonation are as yet little known, and no general relationships have been established. To study this issue, we have chosen to investigate factors that could influence the vertical distribution of a subtidal benthic harpacticoid copepod. From what is known of harpacticoid biology, it is possible a priori to identify factors that could affect the vertical distribution of a subtidal species. Predation has been shown to do so (Gee, 1987; Coull et al., 1989; Ellis & Coull, 1989). Because food items are not uniformly distributed in the vertical dimension (Joint et al., 1982) and species have preferences among food items (Rieper, 1982; Carman & Thistle, 1985), vertical differences in preferred foods could have an effect. Because physical properties of the sediment such as grain size have been shown to affect harpacticoids (Jansson, 1967; Correspondence address: D. Thistle, Department of Oceanography, Florida State University, TaUahassee, FL 32306, USA. Contribution 1060 from the Florida State University Marine Laboratory.
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M.S. FOY AND D. THISTLE
Gray, 1968; McLachlan et al., 1977), such factors could play a role. Because erosion could expatriate suspended individuals to unsuitable habitats (Palmer & Gust, 1985) or expose them to water-column predators (D'Amours, 1988) and because the probability of an individual's being eroded is a function of the strength of the near-bottom flow and the individual's proximity to the sediment surface, harpacticoids might alter their vertical distributions in response to near-bottom flow (Palmer & Molloy, 1986). Finally, interspecific competition is a potential influence on vertical distribution (Fleeger & Gee, 1986). In this study, we first determined the fine-scale vertical distribution of a harpacticoid copepod species and then conducted a preference experiment to determine whether its vertical distribution was influenced by factors inherent in its immediate sedimentary environment, such as food items, grade of sediment, or the presence of competitors. No indication was found that such factors influenced the vertical distribution of our test species. Among possible alternative hypotheses (e.g., predation by demersal predators), we chose to study the influence of near-bottom flow with a flume experiment.
MATERIALS AND METHODS LOCALITY
The study site (29°51'N, 84°31'W) was located at a depth of 5 m in St George Sound, ~, 3 mi south of the Florida State University Marine Laboratory (see Fig. 1 of Reidenauer, 1989). The sediment was an unvegetated fine sand (mean grain size 0.254 mm) (Reidenauer, 1989). Ripples with a wavelength of 10-30 cm, observed on some visits, indicated that the site experiences near-bottom flows strong enough to move the sediment and erode harpacticoids. The site was defined by two parallel 10-m transect lines set 3 m apart and marked at 10-cm intervals. A movable 3-m cross-line, also marked at 10-cm intervals, was used to form a Cartesian coordinate system. All samples were taken at randomly chosen coordinates within the study site. MONTHLY SAMPLES
To identify a species for study and to document its fine-scale vertical distribution, scuba divers took four 15.5-cm 2 cores each month from November 1988 through October 1989. Rough seas made it necessary to transport the cores to shore before vertical sectioning. The trip took ~, 30 min during which the cores were kept in a water bath under approximately in situ temperature and light conditions. On shore, processing was begun immediately and completed in 30 min. The top 3 cm of each core was sliced into 15 2-mm layers with a precision extruder (Fuller & Butman, 1988). The layers were preserved in a sodium-borate-buffered solution of formaldehyde and tap water (1:9, v : v) with rose bengal (Fisher Scientific, Fair Lawn, New Jersey). In the laboratory, we
VERTICAL DISTRIBUTION
155
used a modification of the Barnett (1968) troughing technique to concentrate the harpacticoids from the sediment. Specifically, each 2-mm layer from a core was placed in the through without presieving, and the fraction to be sorted was caught on a 62-/~m sieve. The median efficiency of the procedure in our laboratory on similar sediments was 100~ (n - 5). All adult harpacticoid copepods were removed under a dissecting microscope.
PREFERENCE EXPERIMENT
To investigate effects of the factors intrinsic to the sediment on the vertical distlibution of our target species, we performed a preference experiment. A few adults of the target species were collected by swirl decantation (Pfannkuche & Thiel, 1988) from the 2nd cm of sediment from a 9.6-cm 2 core. These individuals were stained with the vital dye neutral red (Kodak, Rochester, New York), so they could be distinguished from individuals of the same species that might occur naturally in the sediment used in the experiments. (After preliminary experimentation, we chose a concentration of 0.001% (w" v) neutral red in 63-#m-filtered seawater and a staining time of 40 min.) The staining procedure did not seem to affect the behavior or viability of the test animals (pers. obs.). After staining, one individual was chosen at random to be used in a given run of the preference experiment. We used single test animals to make the smallest possible perturbation to the assemblage present in the test sediment. By choosing test individuals at random, we sampled the sexes in approximately their field proportions, making the experimental results comparable to the field distribution data. To assure independence, each test animal was obtained from a different core. The sediment used for the preference experiment came from 3.8-cm 2 cores taken at random from the study site on a single day. The top 2 cm of a core was extruded intact (including the fauna) into a "collar" (a 2-cm-tall piece of the same core stock). The sediment-filled collar was sliced free from the core, and a stained test animal was placed on the surface of the sediment with a micropipet. The collar and sediment were then placed in a container, seawater was added until a few millimeters of water covered the sediment surface, and the container was placed in the dark (to eliminate the possibility that differences in illumination among the replicates could affect the results) and kept at in situ temperature. In 15 of 30 runs, the collar and the test sediment were inverted before the test individual was added so that a preference for the 1-2-cm layer based on some intrinsic factor could be distinguished from a geotactic response (e.g., Hill & Elmgren, 1987). That is, if the animal regulates its vertical position in reference to the sediment-water interface, the test individuals would move to the lower layers in both the upright and inverted sediment. The duration of the experiment was chosen to be as short as possible to minimize changes in porewater chemistry and sediment microbiology yet long enough to allow test animals sufficient time to reach the full depth of the sediment column. Preliminary
156
M.S. FOY AND D. THISTLE
experiments suggested that 90 min was a reasonable compromise. Therefore, after 90 min, the sediment in each collar was extruded and sliced into 10 2-mm layers.
FLUME EXPERIMENT
The flume used in our experiment was patterned after that described by Nowell et al. (1981). Entrance and exit conditions meet the criteria of Nowell & Jumars (1987). Briefly, it is a clear acrylic duct 5 m long, 0.5 m wide and 20 cm deep. A removable bottom plate is located 4.5 m from the entrance of the flume. Sediment cores can be mounted in it, coplanar with the bed of the flume. Seawater is supplied to a 416-1 constant-head tank. Flow enters the flume through a 10. l-cm (inner diameter) T-shaped diffuser and then is rectified through a "honeycomb" of hexagonal cells, each 0.5 cm in widest dimension. The discharge from the constant-head tank is regulated by a butterfly valve. A tail gate of eight vertical louvers (each 6.25 cm wide) allows uniform flow to be established across the width of the flume. At the end of the flume, the seawater falls freely into a tail tank from which it can flow to a drain or be returned to the head tank. The return system includes four pumps (each capable of moving ~, 1141. min - ~) that operate in parallel. The long axis of the flume can be tilted through angles up to 1.5 °. Our experiment was designed to determine whether a target species responded to flow differences by moving deeper into the sediment when exposed to relatively high flow. For each flume run, we took two sediment cores at random from the study site. We obtained and prepared test animals and placed them in cores following the procedures described for the preference experiment, except that the cores were collected on the day the flume run was done. The cores were mounted intact (includifig the fauna) in the flume bed, each 5 cm to one side of the center line of the flume and 4.625 m from the flume entrance. Six flume runs (three high flow and three low flow) were conducted on each of 7 days. The first run of the 1st day was randomly chosen to be a low-flow run. Thereafter, runs alternated between the two flow conditions. The seawater in the flume was filtered through a mesh of 61-/~m aperture, and the depth was maintained at 6 cm during both flow conditions. At the end of each run, the water was drained from the flume. So that the water overlying the cores could drain away without disturbing the sediment surface, a tube with a vertical row of holes 3 mm in diameter was placed over each core. After the flume had been drained, the cores were removed, and the top 2 cm of sediment was sliced into 10 2-ram layers. These fractions were preserved as above. On the day following each set of six flume runs, one of the two cores from each run was chosen at random, and the vertical position of the test animal was determined. The second core was processed only if the test animal was not found in the first core. During preliminary trials, we arrived at settings of the flume parameters (e.g., louver openings) that produced two flows of markedly different velocities. The higher flow approached, but was not equal to, the velocity required to set the sediment on the surface
157
VERTICAL DISTRIBUTION
Fig. I. Electron micrograph of a gravid female Leptastacus. Scale bar, 0.1 mm.
of the cores in motion. After the completion of the flume experiment, we measured the t w o velocities by timing the movement of neutrally buoyant particles (Carey, 1983)over a 40-cm path just u p s t r e a m of the location of the cores. M e a s u r e m e n t s were m a d e on particles in the middle third of the 6-cm water column. Three velocity m e a s u r e m e n t s were m a d e during each of seven low-flow and seven TABLE I
Results of preference experiment. In half trials, sediment column was in its natural upright orientation; in half trials, sediment column was inverted. Entries indicate number of animals found in each layer after 90 min. Sediment depth (mm)
Upright
Inverted
0-2 2-4 4-6 6-8 8-10 10-12 12-14 14-16 16-18 18-20
8 1 2 0
5 3 0 0
0
0
0 0 1
0 0 1
0
1
1
1
158
M.S. FOY AND D. THISTLE
high-flow runs. The runs alternated between the two flow conditions. Mean velocity was 3 c m . s - ~ (n = 7, SD = 0.5) for the low-flow condition and 20 c m . s - ~ (n = 7, SD = 0.4) for the high-flow condition. RESULTS
At the end of the 2nd month of sampling, we chose the interstitial species (Svedmark, 1964) Leptastacus cf. rostratus Nicholls (hereafter, Leptastacus) (Fig. 1) as the target species because it appeared to inhabit a distinct depth horizon. Although the vertical distribution of Leptastacus varies from month to month (Figs 2-4), few individuals are found in the top cm of sediment, and only rarely are individuals found in the top 2 mm. The peak in population abundance is found in the 2nd cm of sediment throughout the year. Further, a Kruskai-Wallis rank sum test (with the large-sample approximation; Hollander & Wolfe, 1973) reveals that, over the year, significantly more Leptastacus are present in the 2nd cm of sediment than in the 1st or 3rd (p < 0.0001). In the preference experiment, the test animal was recovered in 24 of the 30 runs. The majority of animals did not move far from where they were introduced (Table I). Nine of the 13 animals remained in the uppermost 4 mm of sediment when the sediment column was in its natural (upright) orientation, and eight of the 11 animals remained there in the inverted condition. The results of the flume experiment are illustrated in Fig. 5. After being exposed to the low-flow condition, 12 of the 21 test animals were found in the top 2 mm of sediment
MEAN NUMBER OF ADULTS 0 O-2 2-4 4-6 6-8 8-10 10-12 12-14
10
20
30
0
10 po. . . . . . . . .
"mE4
20
' . . . . . . . . .
November
30
' . . . . . . . . .
December
i
!
I
q i
16-18
E E ,,.,,,
I-i1. bJ
i l
18-20 2O-22 m m 22-24 24-26 26-28 28-30
0
t i
10
20
2-4 4-6 6-8 8-10
10-12 12-14 14-16 16-18 18-20 20-22 22-24
24-26 26-28 28-30
30
0
10
20
30
B-~ El-,
0-2
January
~-~m-~
February I I I
! I I
I
I ! I
Fig. 2. Vertical distribution of adult Leptastacus for November 1088 through February 1989. Each bar, mean of four cores. Error bars, 1 SD.
VERTICAL DISTRIBUTION
159
MEAN NUMBER OF ADULTS o
lO
20
0
20
10
0-2 2-4
March
a-lo m 10-12 m m a m
April
------
12-14 14-16 16-18
1 I
m-2o
I
20-22 22-24
A
I
m
24-26 m 26-28 28-30
3: I"a. IJJ rt
B ~
10 ,
o
0-2 k 2-4 4-6
20
30
0
I0
May
10-12 12-14
20
30
June
,,-,6 m 16-18
18-20 20-22 m 22-24 24-26 26-28
m
2.-3o m
Fig. 3. Vertical distribution of adult Leptastacus for March 1989 through June 1989. Each bar, mean of four cores. Error bars, 1 SD.
(the layer in which they were initially placed). After exposure to the high-flow condition, only one of the 21 test animals was found in this layer. Under low-flow conditions, the 0-2-mm layer was both the median depth of the population and the layer where the MEAN NUMBER OF ADULTS 0
20
io
2-4 4.-6
H
July
8-10 10-12 ~
30
0
10
20
30
August
----
12-14 1
4
-
1
6
~
I¢:,--18 i m ~
A
E o
10 , . . . . . . . . .
20
20 ,
0 - 2 I~ ----i
2-4
4-6 m ~ 6-0 ~'~ 8-10 i 10-12
,2-,,
September
m4
m
14-16 16-18
18-2o ,,am
BB--,
22-24 24-26 ~e-2S Ih
IP
2O-22m
October !
28-30
Fig. 4. Vertical distribution of adult Leptastacus for July 1989 through October 1989. Each bar, mean of four cores. Error bars, 1 SD.
160
M.S. FOY AND D. THISTLE HIGH FLOW E E -r
pIx. i,i El I-Z i,1 =E El i,i (/)
o-a
LOW FLOW
"3
2-4
-! I
6-8
I
I
"1
4-6
e-to
. I
7
1
ta-~4 - I 14-16 16-18 IB-20
NUMBER OF ANIMALS PER LAYER
Fig. 5. Summary of flume experiment results. Illustrated are total numbers of test animals found in various layers for 21 high-flow and 21 low-flow runs, respectively.
greatest number of animals was found. In contrast, under the high-flow conditions, the median depth was 4 - 6 mm, and the layer having the most animals w a s the 6 - 8 - m m layer. The A N O V A for the flume-experiment results is shown in Table II. A randomized, mixed-model, factorial design (Kirk, 1982) was employed. The d e p e n d e n t variable was the midpoint of the depth interval at which a test individual was found. Days (a r a n d o m factor) was a blocking factor, and flow and run were fixed-factor treatments. The test animals exposed to high flow were found significantly deeper in the sediment than those exposed to low flow (Table II). The day on which the flume run was conducted affected the depth of the test animal (Table II), but the effects of the time a run was conducted on a given day and the flow-by-run interaction were not significant (Table II). This last
TABLE II
ANOVA table for results of flume experiment. "Flow" treatment had high- and low-velocitylevels and was factor of major interest in experiment. "Run" treatment refers to temporal position of a given replication of experiment on day it was done and had three levels. Day on which an experiment was done was used as a blocking factor; it had six levels. NS indicates p > 0.05. Source
ss
df
Ms
Treatments Flow Run Interaction Bloc} (days) Resicaal fotal
30.86 3.86 2.71 ! 5.62 25.24 78.29
1 2 2 6 30 41
30.86 1.93 1.36 2.60 0.84
Probability p < 0.0005 NS NS
0.01 < p < 0.025
VERTICAL DISTRIBUTION
161
result suggests that any variation introduced by the longer holding time of cores run late in the day is modest and is unlikely to contribute importantly to the dramatic difference in migration depths between flow conditions. DISCUSSION
We believe that our monthly samples reflect the vertical distribution of Leptastacus in nature. Although 30-60 min elapsed between when each core was taken and when it was sliced into layers, we known from the preference experiments that in 90 min 71 of Leptastacus individuals had net displacements of < 6 mm, so the delay alone is unlikely to have altered their vertical distribution on the cm scale, which is the scale of our interest. To minimize the chance that sampling or transportation disturbance altered their distribution, we inserted cores slowly and transported them in a vibration-damping water bath. We could not, of course, eliminate all disturbance, but, in samples taken and processed in a similar manner from a 20-m site, the median depth of Leptastacus was also in the 2nd cm and several other harpacticoid species had maxima in the 0-2or 2-4-mm layers (unpubl. data), indicating, at the least, that our procedures do not result in a general movement of harpacticoids out of the near-surface layers. Our preference experiment was designed to determine whether factors intrinsic to the sediment such as differences in microflora, granulometry, or competitors were responsible for Leptastacus's vertical distribution in nature. Ifthe 0-1-cm layer were unattractive, or the l-2-cm layer attractive, because of intrinsic factors, we would expect the test animals to be found in the lower 1-cm fraction in the upright condition and in the upper l-cm fraction in the inverted condition (i.e., in sediments where they are normally abundant in nature). If Leptastacus regulated its vertical position with respect to the sediment-water interface, we would expect the test animals to be found in the lower 1-cm fraction in both the upright and inverted conditions. The results for the upright condition (Table I) show that, although the test animals were capable of migrating into the 1-2-cm layer, most (11 of 13) stayed in the 0-1-cm layer. In fact, eight of 13 did not move from the 0-2-mm layer, where they are least common in nature (Figs 2-4). We therefore conclude that the low abundance of Leptastacus in the 0-1-cm layer in nature is not caused by some intrinsic unattractiveness of that layer. That is, either such potential factors as granulometry, microbes, or competitors do not vary over the top 2 cm, or any differences between the 0-l-cm layer and the 1-2-cm layer are unimportant to the species in terms of controlling its vertical distribution. That the test animals in both the upright and the inverted cases tended to remain near the top of the sediment column suggests that Leptastacus does not prefer to live at depth in nature because of a geotactic response. In contrast, Fleeger & Gee (1986) found that two other harpacticoid species from an intertidal sand flat took up their natural depths in azoic laboratory sediment columns.
162
M.S. FOY AND D. THISTLE
Of the remaining factors that might influence Leptastacus's distribution, we chose to investigate flow. The flume experiment demonstrated that Leptastacus moves out of the surface layers when exposed to a flow that is just suberosive. The ripples in the seabed frequently observed at our site imply flows of erosive magnitude (Middleton & South~rd, 1984), i.e., stronger flows than those used in the flume experiment, so the behavior we have observed in the flume experiment is likely to occur in the field. We conclude that at least a part of Leptastacus's vertical distribution pattern arises because of the response to strong near-bottom flows. Our study did not address the question of why Leptastacus should move deeper into the sediment when exposed to strong near-bottom flows, but, given its size and specific density, the nearer an individual is to the sediment surface, the greater is its probability of being suspended during periods of strong flow. We observed that Leptastacus is a poor swimmer, and we suspect that it moves away from the sediment surface to avoid being suspended in the water column. Although a variety of reasons can be proposed to explain why being in the water column could be disadvantageous for such a species (Palmer, 1988), no data exist to justify selection among them. ACKNOWLEDGEM ENTS
The manuscript has been improved by the comments of S. C. Ertman, P. A. LaRock, M.A. Palmer, D. Nof and A.B. Thistle. A.R.M. NoweU, P.A. Jumars and S.C. Ertman provided advice on flume design. The flume was built by J. Winne, D. Oliff and K. Collins. J.E. Eckman gave us the "honeycomb" for the flow straightener. This research was supported by NSF grant OCE-8911181 and ONR contract N00014-87G-0209 to D. Thistle. We express our thanks for this kind help. REFERENCES Barnett, P. R. O., 1968. Distribution and ecology of harpacticoid copepods of an intertidal mudflat. Int. Rev. Gesamten Hydrobiol., Vol. 53, pp. 177-209. Carey, D.A., 1983. Particle resuspension in the benthic boundary layer induced by flow around polychaet~ tubes. Can. J. Fish. Aquat. Sci., Vol. 40, pp. 301-308. Carman, K.R. & D. Thistle, 1985. Microbial food partitioning by three species of benthic copepods. Mar. Biol., Vol. 88, pp. 143-148. Coull, B. C., M. A. Palmer & P. E. Myers, 1989. Controls on the vertical distribution ofmeiobenthos in mud field and flume studies with juvenile fish. Mar. Ecol. Prog. Set., Vol. 55, pp. 133-139. D'Amours, D., 1988. Vertical distribution and abundance of natant harpacticoid copepods on a vegetatec tidal flat. Neth. J. Sea Res., Vol. 22, pp. 161-170. Ellis, M.J. & B.C. Coull, 1989. Fish predation on meiobenthos: field experiments with juvenile spol Leiostornus xanthurus Lacepede. J. Exp. Mar. Biol. Ecol., Vol. 130, pp. 19-32. Fleeger, J.W. & J.M. Gee, 1986. Does interference competition determine the vertica| distribution o meiobenthic copepods? J. Exp. Mar. Biol. Ecol., Vol. 95, pp. 173-181. Fuller, C. M. & C.A. Butme.n, 19~8. g simple technique for fine-scale, vertical sectioning of fresh sedimen cores. J. Sed. Petrol., Vol. 58: pp. 763-768. Gee, J.M.~ 1987. Impact of epibenthic predation on estuarine intertidal harpacticoid copepod populations Mar. Biol., Vol. 96, pp. 497-510.
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Gray, J. S., 1968. An experimental approach to the ecology of the harpacticoid Leptastacus constrictus Lang. J. Exp. Mar. Biol. Ecol., Vol. 2, pp. 278-292. Hicks, G. R. F. & B.C. Coull, 1983. The ecology of marine meiohenthic harpacticoid copepods. Oceanogr. Mar. Biol. Annu. Rev., Vol. 21, pp. 67-175. Hill, C. & R. Elmgren, 1987. Vertical distribution in the sediment in the co-occurring benthic amph!pods Pontoporeia affinis and P. femorata. Oikos, Vol. 49, pp. 221-229. Hollander, M. & D.W. Wolfe, 1973. Nonparametric statistical methods. Wiley, New York, 503 pp. Jansson, B.O., 1967. The importance of tolerance and preference experiments for the interpretation of mesopsammon field distributions. Heigol. Wiss. Meeresunters., Vol. 15, pp. 41-58. 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. Kirk, R.E., 1982. Experimental design. Brooks/Cole, Belmont, California, 911 pp. McLachlan, A., P.E.D. Winter & L. Botha, 1977. Vertical and horizontal distribution of sub-littoral meiofauna in Algoa Bay, South Africa. Mar. Biol., Vol. 40, pp. 355-364. Middleton, G.V. & J.B. Southard, 1984. Mechanics of sediment movement. S.E.P.M. Short Course Number 3. Society of Economic Paleontologists and Mineralogists, Tulsa, Oklahoma, 401 pp. Nowell, A. R. M. & P.A. Jumars, 1987. Flumes: theoretical and experimental considerations for simulation of benthic environments. Oceanogr. Mar. Biol. Annu. Rev., Vol. 25, pp. 191-212. Nowell, A. R. M., P.A. Jumars & J.E. Eckman, 1981. Effects of biological activity on the entrainment of marine sediments. Mar. Geol., Vol. 42, pp. 133-153. Palmer, M.A., 1988. Dispersal of marine meiofauna: a review and conceptual model explaining passive transport and active emergence with implications for recruitment. Mar. Ecol. Prog. Set., Vol. 48, pp. 81-91. Palmer, M.A. & G. Gust, 1985. Dispersal of meiofauna in a turbulent tidal creek. J. Mar. Res., Vol. 43, pp. 179-210. Palmer, M.A. & R.M. Molloy, 1986. Water flow and the vertical distribution of meiofauna: a flume experiment. Estuaries, Vol. 9, pp. 225-228. Pfannkuche, O. & H. Thiel, 1988. Sample processing. In, Introduction to the study ofmeiofauna, edited by R. P. Higgins & H. Thiel, Smithsonian Institution Press, Washington, District of Columbia, pp. 134-145. Reidenauer, J.A., 1989. Sand dollar Mellita quinquiesperforata (Leske) burrow trails: sites for harpacticoid disturbance and nematode attraction. ,7. Exp. Mar. Biol. Ecol., Voi. 130, pp. 223-235. Rieper, M., 1982. Feeding preference of marine harpacticoid copepods for various species of bacteria. Mar. Ecol. Prog. Set., Vol. 7, pp. 303-307. Svedmark, B., 1964. The interstitial fauna of marine sands. Biol. Rev., Vol. 39, pp. 1-42.