Differential dispersal rates in an intertidal meiofauna assemblage

Journal of Experimental Marine Biology and Ecology 268 (2002) 237 – 256 www.elsevier.com/locate/jembe

Differential dispersal rates in an intertidal meiofauna assemblage John A. Commito a,b,*, Guglielmo Tita c,1 a

Environmental Studies Department and Biology Department, Gettysburg College, Gettysburg, PA 17325, USA b Dipartimento di Scienze dell’Uomo e dell’Ambiente, Universita` di Pisa, Via Volta 6, I-56126 Pisa, Italy c Universite´ du Que´bec a` Rimouski, Institut des Sciences de la Mer, 310 alle´e des Ursulines, Rimouski, Que´bec, Canada G5L 3A1 Received 25 May 2001; received in revised form 20 November 2001; accepted 27 November 2001

Abstract Meiofaunal nematodes and copepods disperse passively with sediment bedload, and copepods also display active emergence and reentry behavior. Epigrowth-feeders may be the nematode feeding group most susceptible to passive transport because they live closest to the sediment surface. We used bottom traps at a nematode-dominated intertidal mudflat in Maine, USA, to test the hypotheses that (1) meiofauna taxa disperse in relative proportions different from those of the ambient community; (2) copepods have the highest relative dispersal rate (number of individuals trap 1 day 1 ambient individual 1) and are not as tightly linked as other taxa to sediment flux; and (3) epigrowth-feeders have the highest nematode relative dispersal rate. Results supported all three hypotheses. Nematodes accounted for 95.8% of the individuals in cores, but only 38.9% of the individuals in traps. Copepods accounted for 1.5% of the individuals in cores, but 56.7% of the individuals in traps. Less common taxa also had different relative proportions in cores and traps, as did nematode feeding groups and individual species. The relative dispersal rate was far higher for copepods than for any other taxonomic group, and the absolute (number of individuals trap 1 day 1) and bulk (number of individuals g sediment 1 trap 1 day 1) dispersal rates for copepods were equal to those of the 65-fold more abundant nematodes and higher than those for all other taxa. The non-selective deposit-feeders were the most abundant nematode feeding group in the ambient community, but the epigrowth-feeders as a group and as individual species had the highest absolute, relative, and bulk dispersal rates. Non-metric multidimensional scaling (MDS) using analysis of similarity (ANOSIM) and species similarity percentages (SIMPER) reflected these differences between ambient and dispersing nematode assemblages. Significant positive regression relationships between sediment weight and the number of individuals captured in traps for nematodes and some * Corresponding author. Environmental Studies Program and Biology Department, Gettysburg College, Gettysburg, PA 17325, USA. Tel.: +1-717-337-6030; fax: +1-717-337-6666. E-mail address: [email protected] (J.A. Commito). 1 Present address: Department of Biology, Louisiana State University, Baton Rouge, LA 70803, USA.

0022-0981/02/$ - see front matter D 2002 Elsevier Science B.V. All rights reserved. PII: S 0 0 2 2 - 0 9 8 1 ( 0 1 ) 0 0 3 8 6 - 0

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other taxa indicated that they moved passively in the bedload. Lack of a significant regression relationship for copepods suggested an active behavioral component to dispersal. Meiofauna populations in this soft-bottom community were highly dynamic, demonstrating that the role of dispersal must be included in any consideration of the ecology of soft-bottom systems at local and regional spatial scales. D 2002 Elsevier Science B.V. All rights reserved. Keywords: Bedload transport; Benthic copepods; Maine; Meiofauna dispersal; Nematode feeding groups; Sediment flux

1. Introduction Marine benthic populations are notoriously variable in space and time. Recent advances in spatial ecology have revealed the importance of local dispersal in regulating population dynamics and persistence (Levin and Pacala, 1998; Hanski, 1999; Hiebeler, 2000). Yet much of our attention in benthic ecology has been focused on dispersal at large spatial scales, often of planktonic larval stages in hard-bottom systems where adults are permanently attached to the substrate (Roughgarden et al., 1987; Underwood and Fairweather, 1989; Reed et al., 2000). For these organisms, postlarval dislodgement and transport often means death. Soft-bottom systems differ from hard-bottoms in a crucial way: organisms are not permanently attached to the substrate, so postlarval transport can provide infauna with opportunities for repeated, local dispersal events. Comparatively few soft-bottom studies have been conducted of juvenile and adult dispersal at local scales such as (in decreasing order) the individual sandflat, seagrass bed, nekton fall, foraging pit, crab burrow, fecal mound, or sediment bite (see references in Palmer, 1988a; Palmer et al., 1996; Armonies, 1994; Commito et al., 1995a,b; Fleeger et al., 1995; Turner et al., 1997; Thrush et al., 2000). Because planktonic larvae are absent in meiofauna, the active and passive transport of juveniles and adults might be crucially important to their population performance. Harpacticoid copepods tend to reside near the sediment surface, and many species are good swimmers (Palmer, 1988a; Fleeger et al., 1995). They can move passively with eroded sediments when currents are rapid. They also respond actively to flow velocity and biogenic structures like burrows that alter flow, often emerging from the sediment in great numbers when water velocity is slowest (Service and Bell, 1987; Palmer, 1988a; Fegley, 1988; DePatra and Levin, 1989; Armonies, 1994; Sun and Fleeger, 1994; Fleeger et al., 1995). On the other hand, nematodes, which often dominate the meiofauna of unvegetated mudflats and sandflats, generally show little evidence of active dispersal (Jensen, 1981; Palmer, 1988a) and probably move primarily by passive transport in the bedload and water column (Palmer, 1988a; Fegley, 1988; DePatra and Levin, 1989; Armonies, 1994; Sun and Fleeger, 1994). The nematodes closest to the sediment – water interface may be most susceptible to erosion and transport (Warwick and Gee, 1984; Eskin and Palmer, 1985), especially epigrowth-feeders (feeding group 2A, sensu Wieser, 1953) like Ptycholaimellus ponticus that live in surficial sediment because they rely primarily on a photosynthesizing food source. Data on other meiofauna taxa are rare and suggest that their dispersal mode is also largely passive (Palmer, 1988a, Fegley, 1988; Armonies, 1994). In this study of a nematode-dominated intertidal mudflat, we used bottom traps to measure sediment flux and three key rates of dispersal for each major taxonomic group of

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the meiofauna community, each nematode feeding group, and each nematode down to the level of the genus or species. We tested the following hypotheses: H1. Meiofauna taxonomic groups disperse in relative proportions different from those of the ambient community. H2. Copepods have the highest relative dispersal rate (number of individuals trap 1 day 1 ambient individual 1) and are not as tightly linked as other taxa to sediment flux. H3. Epigrowth-feeders have the highest nematode relative dispersal rate. 2. Materials and methods 2.1. Study site The study site was Bob’s Cove, an intertidal mudflat in Jonesboro, Washington County, ME, USA (44
33VN: 67
35VW). The 500-m wide  600-m long cove is sheltered from the wind on the north, east, and west sides by steeply rising, heavily forested land, and on the south by a narrow (300 m) mouth protected by islands and nearby landmasses. Consistent with this protected basin configuration, the sediment has a smooth, unrippled surface, indicative of a low-energy environment with slow wind- and tide-generated water currents. Sediment characteristics were qualitatively assessed and are similar to those at nearby Flake Point Bar, where mean F F s = 4.87 F 0.02 (Beal et al., 2001). Air temperature ranges from 35 to 35
C, and water temperature from 0 to 10
C. In the summer, shallow water moving onto or off the flat can reach 21
C. Salinity is usually about 30 PSU. See Commito (1982) and references in Commito and Rusignuolo (2000) for additional information on the ecology of this site. 2.2. Field procedures At low tide on 10 July, 1994, a grid with 75 positions was established in the mid-intertidal zone. The grid was a rectangle with sampling positions every 0.75 m along each row (seven rows with 10 positions each and one row with five positions), with rows 2 m apart. To determine the structure of the ambient community, cores were taken to a depth of 15.0 cm at 10 randomly chosen grid positions with a 15.0 cm tall 1.3 cm internal diameter, plastic, cylindrical test tube (cross-sectional area = 1.33 cm2) from which the bottom had been removed. To determine the transport of sediment and meiofauna, bottom traps were installed at 10 other randomly chosen grid positions. Traps similar to those of Fegley (1988) consisted of seawater-filled test tubes of the same dimensions as the coring device (aspect ratio, height/ diameter = 11.5:1) inserted flush with the sediment surface into holes created by carefully extracting sediment with the same coring device. Traps were left in place overnight and removed at low tide 1 day later. Core and trap contents were stained with rose bengal and preserved in 4% buffered formalin. Deployment occurred during the July spring tide with the lower amplitude. Winds in the region were light and variable when water covered the site during the trap deployment

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period, coming from the 190
– 280
sector (the protected western and southwestern side of the cove), with hourly means of 1.3 –7.3 m s 1 and peak gusts of 7.5 m s 1 (National Oceanic and Atmospheric Administration, Mount Desert Rock C-MAN station data). These wind speeds were typical for July, the month with the lowest 10-year-average and gust velocities. Thus, tidal- and wind-generated currents were moderate compared to other dates with more extreme tidal variation and wind speeds. 2.3. Laboratory procedures 2.3.1. Core samples In the laboratory, meiofauna were extracted from cores following McIntyre and Warwick (1984) and Heip et al. (1985). Each core sample was rinsed over 1 mm and 63 mm mesh sieves. The contents on the 63 mm sieve were centrifuged at 1800  g in water for 10 min. The supernatant was passed through a 63-mm sieve, and Ludoxk (specific gravity = 1.15) was added to the residue in the centrifugation tube to at least five times the volume of sediment. Three times for each sample, the sediment was brought to suspension by gentle mixing and centrifuged at 1800  g for 10 min, and the supernatant was passed through a 63-mm sieve. The final material was rinsed with tap water to prevent flocculation of Ludox and preserved in 4% formalin. The meiofauna were transferred into a gridded Petri dish, and the individuals of each taxonomic group were counted. For nematodes, a subsample of 100 randomly sorted individuals were transferred into 10% glycerol solution for species identification. When the water evaporated, the nematodes were transferred to a glycerol drop in a ring of paraffin on a glass slide, each of which was covered with a glass cover slip, warmed, and then cooled. Nematode species were identified using the keys of Platt and Warwick (1983, 1988). Their frequencies were multiplied by the total number of nematode individuals in the sample to provide an estimate of the number of individuals of each species in the sample. Individuals were assigned to feeding groups according to Wieser (1953), where 1A = selective deposit-feeders, 1B = non-selective deposit-feeders, 2A = epigrowth-feeders, and 2B = omnivores-carnivores. 2.3.2. Trap samples Trap samples contained less sediment and fewer organisms than core samples, so meiofauna extraction was simplified. The samples were rinsed with distilled water over 1 mm and 63 mm sieves, the contents on the 63 mm sieve were transferred to a gridded Petri dish, and counting and identification were carried out as for the core samples. In addition, sediment was dried at 60
C and weighed, except for the sediment lost from one trap due to an accident in the laboratory. That trap could not be included in calculations involving sediment weight. 2.3.3. Dispersal rates Dispersal rates were calculated in three ways: Absolute dispersal rate = number of individuals trap 1 day 1 = the number of individuals per trap captured during 1 day of deployment. Relative dispersal rate = number of individuals trap 1 day 1 ambient individual 1 = the number of individuals per trap captured during 1 day of deployment, divided by the mean ambient density for that meiofauna taxon, nematode feeding group, or ne-

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matode species. For some rare species at our study site, the denominator was equal to or close to zero, resulting in a relative dispersal rate tending to infinity. To avoid this problem, relative dispersal rates were calculated for the 10 species that were most abundant in traps, all of which had mean values >4 individuals trap 1 and >40 individuals core 1. Bulk dispersal rate = number of individuals g sediment 1 trap 1 day 1 = the number of individuals per trap captured during 1 day of deployment, divided by the sediment weight captured in the same trap. 2.3.4. Statistical analysis To examine differential movement into traps, the relative proportions of meiofauna taxonomic groups, nematode feeding groups, and the five top-ranked nematode species in ambient community cores were compared to those in bottom traps using the chi-square test. For the nematodes, differences in species composition between the traps and cores were examined further by means of non-metric multidimensional scaling ordination (MDS) with different degrees of data transformation. Untransformed data analysis is more sensitive to changes in abundant species, while increasingly severe square root transformations are more sensitive to changes in abundance of those that are increasingly rare (Clarke and Warwick, 1994). The differences between core and trap assemblages were investigated with a one-way analysis of similarity using the ANOSIM routine (PRIMER v4; Clarke and Warwick, 1994). The contribution of each species to the average sample dissimilarity between cores and traps was determined using the SIMPER routine (PRIMER v4; Clarke and Warwick, 1994). Densities and dispersal rates were compared across taxonomic groups, nematode feeding groups, and the five top-ranked nematode species with the non-parametric Kruskal – Wallis test followed by the Student – Newman– Keuls procedure. To determine how closely animal transport was related to sediment flux, regressions were run on the number of individuals per trap versus sediment weight per trap. The regression results were used as a crude measure of dispersal mode, based on the assumption that correlations are stronger for passive dispersers than for those with active dispersal behavior (Turner et al., 1997).

3. Results 3.1. Ambient community Nematodes dominated the ambient community, accounting for 95.8% of the individuals in cores (Fig. 1). Copepods, primarily harpacticoids, were the second most abundant taxonomic group, followed by kinorhynchs, acari, oligochaetes, polychaetes, ostracods, sipunculids, and tardigrades, in decreasing order (Fig. 1). Non-selective deposit-feeders (feeding group 1B) were the most abundant nematode feeding group, accounting for 39.4% of the nematode individuals in cores (Fig. 2). Epigrowth-feeders (2A) were the second most abundant feeding group, followed by many fewer selective deposit-feeders (1A) and omnivores/carnivores (2B) (Fig. 2). Non-selective deposit-feeders were also the most species-rich feeding group, comprising 39.1% of the nematode species in cores, followed by epigrowth-feeders (21.7%), omnivores/carnivores (21.7%), and selective deposit-feeders (17.4%).

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Of the 52 nematode species identified in this study, 46 were found in the ambient community (Appendix A), with a mean of 20.20 F 0.73 (SE) species core 1. Of these 46 species, 16 were never found in traps (Appendix A). The non-selective deposit-feeder Daptonema sp. had the highest mean density of the five top-ranked species in the ambient community (df = 4, H = 13.29, P = 0.01; Student –Newman –Keuls P < 0.05), accounting for 18.3% of the nematodes in cores (Table 1). The densities of the other four top-ranked species were not significantly different from each other. They were the epigrowth-feeder Chromadora macrolaima, followed by the omnivore/carnivore Metachromadora sp. 2, the selective deposit-feeder Terschellingia sp., and the epigrowth-feeder P. ponticus. Thus, every feeding group was represented among the five top-ranked species. 3.2. Dispersal rates 3.2.1. Absolute dispersal rates The composition of the meiofauna assemblage captured in the traps was markedly different from that of the ambient community (Fig. 1). Relative proportions of the meiofauna groups at higher taxonomic levels were significantly different between cores and traps whether all the groups were considered individually (df = 7, v2 = 118.80, P < 0.001) or the uncommon taxa were lumped into one group for comparison with nematodes and copepods (df = 2, v2 = 9832.8, P < 0.001). Copepods and nematodes had far higher absolute dispersal rates than any of the other taxa (Fig. 1). Copepods accounted for 56.7% of the individuals in traps, despite representing only 1.5% of the ambient community density. Nematodes were the second most abundant taxonomic group in traps, although not significantly different from the copepods. In decreasing order, there were small numbers of kinorhynchs, acari, ostracods, polychaetes, oligochaetes, and isopods, with no sipunculids or tardigrades. The relative proportions of the number of individuals of each nematode feeding group in traps were significantly different from those in cores (df = 3, v2 = 404.1, P < 0.001; Fig. 2). Epigrowth-feeders had the highest absolute dispersal rate of the nematode feeding groups, accounting for 53.2% of the nematode individuals in traps, compared to 30.2% in the ambient community cores (Fig. 2). The rate for epigrowth-feeders was twice that of the non-selective deposit-feeders, which was twice that of the selective deposit-feeders and omnivores/carnivores. There was no change between cores and traps in the relative proportions of the number of species in each feeding group (df = 3, v2 = 1.015, P = 0.798). Non-selective depositfeeders were still the most species-rich feeding group, comprising 38.9% of the nematode species in traps, followed by epigrowth-feeders (25.0%), selective deposit-feeders (22.2%), and omnivores/carnivores (13.9%).

Fig. 1. Ambient community densities and dispersal rates (mean F SE) for major meiofauna taxonomic groups at Bob’s Cove, ME. Note vertical axis breaks in three of the four graphs. For ease of comparison, same sequence of taxa is presented along the horizontal axis of each graph. Nem = nematodes; Cop = copepods; Kino = kinorhynchs; Acar = acari; Oligo = oligochaetes; Poly = polychaetes; Ostr = ostracods; Sipu = sipunculids; Tard = tardigrades; Isop = isopods. 0 = no animals; und = undefined because of 0 value in denominator of rate calculation. Underlined groups denote no significant difference (Student – Newman – Keuls P < 0.05 following Kruskal – Wallis tests).

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Table 1 Five top-ranking nematode species for ambient community density and three dispersal rates Rank

Species

Ambient community density (no. individuals core 1 Daptonema sp. 2 Chromadora macrolaima 3 Metachromadora sp. 2 4 Terschellingia sp. 5 Ptycholaimellus ponticus

–1

Bulk dispersal rate (no. individuals g sediment 1 Chromadora macrolaima 2 Parachromadorita sp. 3 Ptycholaimellus ponticus 4 Daptonema sp. 5 Chromadorina sp.

1

Mean F SE

1B 2A 2B 1A 2A

300.83 F 45.66 258.69 F 69.41 161.35 F 60.66 98.38 F 17.85 97.58 F 28.99

2A 2A 2A 1B 2A

28.42 F 7.11 24.90 F 8.87 24.84 F 8.87 20.37 F 4.21 12.96 F 3.40

)

Absolute dispersal rate (no. individuals trap 1 day 1 Chromadora macrolaima 2 Parachromadorita sp. 3 Ptycholaimellus ponticus 4 Daptonema sp. 5 Chromadorina sp. Relative dispersal rate (no. individuals trap 1 day 1 Parachromadorita sp. 2 Chromadorina sp. 3 Ptycholaimellus ponticus 4 Axonolaimus sp. 5 Leptolaimus elegans

Feeding group

1

1

trap

)

ambient individuals 2A 2A 2A 1B 1A 1

day

1

) 0.55 F 0.13 0.30 F 0.08 0.26 F 0.09 0.18 F 0.05 0.17 F 0.05

1

) 2A 2A 2A 1B 2A

32.42 F 9.42 27.71 F 6.52 24.90 F 6.47 21.56 F 4.15 14.68 F 5.05

Of the 52 nematode species identified in this study, 36 were found in traps (Appendix A), with a mean of 17.30 F 1.46 (SE) species trap 1. Of these 36 species, six were never found in cores (Appendix A). There were no significant differences in absolute dispersal rates among the five top-ranked species (df = 4, H = 3.77, P = 0.44). The first-ranked species was the epigrowth-feeder C. macrolaima, accounting for 16.1% of the nematodes in traps (Table 1). The others were the epigrowth-feeder Parachromadorita sp., followed by the epigrowthfeeder P. ponticus, the non-selective deposit-feeder Daptonema sp., and the epigrowthfeeder Chromadorina sp. Thus, only two feeding groups were represented among the five top-ranked species, with epigrowth-feeders accounting for 88.6% of those individuals. The relative proportions of the five most abundant nematode species in cores were significantly different from those in traps (df = 4, v2=378.2, P < 0.001). There was a clear pattern in this species composition shift between the ambient community and the dispersers. Of the Fig. 2. Ambient community densities and dispersal rates (mean F SE) for nematode feeding groups (sensu Wieser, 1953) at Bob’s Cove, ME. For ease of comparison, the same sequence of feeding groups is presented along the horizontal axis of each graph. 1B = non-selective deposit-feeders; 2A = epigrowth-feeders; 1A = selective depositfeeders; 2B = carnivores – omnivores. Underlined groups denote no significant difference (Student – Newman – Keuls P < 0.05 following Kruskal – Wallis tests).

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top five species in the ambient community, the species ranked number one (Daptonema sp.), three (Metachromadora sp.), and four (Terschellingia sp.) dropped to fourth, ninth, and twentieth, respectively, in the traps (Appendix A, Table 1). The species ranked number two (C. macrolaima) and five (P. ponticus) in the ambient community rose to first and third, respectively, in the traps. Thus, the two epigrowth-feeders rose in the rankings, and the three species from the other three feeding groups all dropped in the rankings. At the same time, the two new species to appear among the top five in traps were both epigrowth-feeders (secondranked Parachromadorita sp., up from number 11; fifth-ranked Chromadorina sp., up from number 12). The only species other than an epigrowth-feeder to be found in the top five dispersers was Daptonema sp., the most abundant nematode species in the ambient community. Multidimensional scaling ANOSIM results on untransformed data revealed significant differences between the ambient and dispersing nematode assemblages (R = 0.813, P < 0.00, stress = 0.04; Fig. 3). Clustering was similar over a range of data transformation levels (square root: R = 0.789, P < 0.00, stress = 0.07; fourth root: R = 0.703, P < 0.00, stress = 0.11), so only the untransformed data results are presented here. One trap was an outlier (Fig. 3). This trap was far different from the others, having one-tenth as many individuals and one-half as many species as the trap means. The SIMPER results demonstrated average similarities of 46.9% between cores and 43.4% between traps. The Bray –Curtis dissimilarity was 82.5% between cores and traps. The species contributing most to the dissimilarity term were Daptonema sp. (21.25%), C. macrolaima (13.34%), Metachromadora sp. 2 (8.04%), Terschellingia sp. (7.74%),

Fig. 3. Multidimensional scaling (MDS) plot of nematode species assemblages at Bob’s Cove, ME, based on numbers of individuals per sample. Cores = ambient community core samples (N = 10). Traps = bottom trap samples (N = 10).

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Sabatieria sp. 1 (5.47%), and P. ponticus (5.15%), with other species having values less than 5%. These results from the multivariate analysis are in close agreement with those from the univariate analyses. They reflect the drop of Daptonema sp. and other non-epigrowth-feeders from high ranks in the cores to lower ranks in the traps, while epigrowthfeeding species like C. macrolaima and P. ponticus rose in the trap rankings. Traps contained a mean of 0.92 F 0.11 g (SE) sediment trap 1. Regression analysis demonstrated a significant positive relationship between sediment weight trap 1 and number of individuals trap 1 for the meiofauna as a whole (Table 2). For taxonomic groups, this relationship was significant for nematodes, acari, kinorhynchs, ostracods, and the uncommon taxa lumped into one group, but not for copepods and the other taxa. For the nematode feeding groups, the relationship was significant for selective deposit-feeders, non-selective deposit-feeders, and epigrowth-feeders. At the nematode species level, it was significant for five species, including two epigrowth-feeders (Actinonema sp. and P. ponticus) and three selective deposit-feeders (Desmoscolex falcatus, Halalaimus sp., and Leptolaimus elegans). 3.2.2. Relative dispersal rates The relative dispersal rate normalized dispersal to a per capita rate by dividing absolute dispersal by the ambient density. Copepods had a relative dispersal rate of 10.09 F 2.18 Table 2 Regression parameters for number of individuals per trap ( y variable) versus sediment weight collected per trap (x variable) Y Total meiofauna Copepods Nematodes By feeding groups 1A Selective deposit-feeders 1B Non-selective deposit-feeders 2A Epigrowth feeders 2B Predators and omnivores By species Actinonema sp. Desmoscolex falcatus Halalaimus sp. Leptolaimus elegans Ptycholaimellus ponticus Other taxa combined By taxonomic group Acari Isopods Kinorhynchs Oligochaetes Ostracods Polychaetes Sipunculids Tardigrades

y-intercept

Slope

r2

P

229.76 147.20 64.83

712.75 409.03 262.72

0.54 0.26 0.63

0.02 0.16 0.01

7.60 14.36 42.34 4.73

31.59 63.47 150.48 9.81

0.59 0.57 0.61 0.23

0.02 0.02 0.01 0.19

2.99 2.80 4.05 7.43 42.84 17.44

4.10 5.30 6.16 16.68 75.43 40.81

0.46 0.66 0.46 0.54 0.76 0.86

0.04 0.01 0.04 0.03 0.00 0.00

16.59 0.49 12.40 0.76 9.95 0.82

0.74 0.24 0.57 0.13 0.83 0.31

0.00 0.18 0.02 0.34 0.00 0.12

8.53 0.34 3.45 0.36 4.62 0.43 NA NA

To save space, only significant ( P V 0.05) regressions are presented for individual nematode species. NA = none in traps.

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individuals trap 1 day 1 ambient individual 1, meaning that traps held 10 times more copepods than did ambient community cores with the same cross-sectional area (Fig. 1). This relative dispersal rate was the highest by far among the taxonomic groups. It was more than twice as high as the rate for the second highest taxonomic group, the ostracods, and nearly two orders of magnitude higher than the rate for nematodes. Epigrowth-feeders had the highest relative dispersal rate of the nematode feeding groups, more than twice the rate of any other feeding group (Fig. 2). There were no significant differences in relative dispersal rates among the five top-ranked nematode species (df = 4, H = 8.46, P = 0.08). The first three were the epigrowth-feeders Parachromadorita sp., Chromadorina sp., and P. ponticus, followed by the non-selective deposit-feeder Axonolaimus sp. and the selective deposit-feeder L. elegans (Table 1). 3.2.3. Bulk dispersal rates The bulk dispersal rate measured dispersal per unit of bedload sediment by dividing the number of animals in each trap by the weight of the sediment captured in that trap. Copepods and nematodes had much higher bulk dispersal rates than did the other taxonomic groups (Fig. 1). Although the rate for copepods was higher than that of the nematodes, the difference was not statistically significant. Epigrowth-feeders had the highest bulk dispersal rate of the nematode feeding groups, more than twice the rate of the next highest group, the non-selective deposit-feeders, which had rates twice as high as the other two groups (Fig. 2). There were no significant differences in bulk dispersal rates among the five top-ranked species (df = 4, H = 3.71, P = 0.45). Four were the epigrowth-feeders C. macrolaima, Parachromadorita sp., P. ponticus, and Chromadorina sp. (Table 1). The other was the non-selective deposit-feeder Daptonema sp., the most abundant species in the ambient community.

4. Discussion The results of this field investigation provided strong support for our hypotheses concerning meiofauna dispersal dynamics in an unvegetated intertidal mudflat community. First, comparison of traps with cores supported the hypothesis (H1) that meiofauna taxa disperse in relative proportions different from those of the ambient community. Nematodes accounted for 95.8% of the individuals in cores, but only 38.9% of the individuals in traps. Copepods accounted for only 1.5% of the individuals in cores, but 56.7% of the individuals in traps. The less common taxa also had different relative proportions in cores and traps. The same was true for nematode feeding groups and individual species, with additional evidence provided by the multivariate MDS analysis. Second, the results supported the hypothesis (H2) that copepods have the highest relative dispersal rates and are not as tightly linked to sediment flux as other taxa. The relative dispersal rate was far higher for copepods than for any other taxonomic group. Copepods also had absolute and bulk dispersal rates that were higher than those for all taxa except nematodes. These two rates were not significantly different from those for nematodes, despite the fact that nematodes were 65-fold more abundant in the ambient

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community. There was a significant regression relationship between sediment weight and the number of individuals captured in traps for nematodes and some other taxa, indicating that they moved passively in the bedload. But for copepods, there was no significant relationship, consistent with the idea that there is an active component to their dispersal. Third, the results supported the hypothesis (H3) that epigrowth-feeders have the highest nematode relative dispersal rates. The non-selective deposit-feeders were the most abundant feeding group in the ambient community. However, the epigrowth-feeders were the feeding group with the highest absolute, relative, and bulk dispersal rates. The nonselective deposit-feeder Daptonema sp. was the most common species in the ambient community. But the first, second, and third positions in the species rankings for each of the three dispersal rates were held by C. macrolaima, Chromadorina sp., Parachromadorita sp., or P. ponticus, all epigrowth-feeders. 4.1. Nematode and copepod dispersal in soft-bottom systems Our regression results linking nematodes to sediment flux indicate that passive transport is the primary means by which nematodes disperse. Although there are reports of swimming activity in some nematodes (Jensen, 1981; Palmer, 1988a), our results are consistent with those from studies that found nematodes in the water column and bottom traps after being eroded from the sediment (Fegley, 1988; Palmer, 1988a; DePatra and Levin, 1989; Armonies, 1994; Sun and Fleeger, 1994). The epigrowth-feeder genera Ptycholaimellus, Metachromadora, and Chromadora are known to live near the sediment surface and have been collected in the water column and in resuspended sediment directly above the bottom (Bell and Sherman, 1980; Eskin and Palmer, 1985). Eskin and Palmer (1985) suggested that species in these genera live close to the sediment surface and are more susceptible to erosion and transport than deeply dwelling species. Warwick and Gee (1984) made the same argument specifically for P. ponticus. Our results on these genera and species clearly support their predictions. Our results are consistent with those of other workers who found that copepods possess a suite of active emergence and reentry behaviors (see references in Palmer, 1988a; Armonies, 1994; Fleeger et al., 1995). Fleeger et al. (1995) showed quite clearly in their flume study that copepods made active sediment reentry choices under no flow conditions, but behaved like passive particles under conditions of flow. Our traps were deployed over the full tidal cycle, during which time they integrated a variety of flow conditions, possibly capturing copepods moving both actively and passively. The origins and distances traveled by the meiofauna captured in our traps are unknown. Phytal-dwelling copepods dispersed 20 m away from natural seagrass beds in 1 day (Kurdziel and Bell, 1992). Artificial substrate collectors designed to mimic filamentous microalgae and aufwuchs-bearing hard surfaces can rapidly collect meiofauna, especially copepods, from nearby sources (Atilla and Fleeger, 2000). The nearest habitats of these types (short, sparse eelgrass, Zostera marina; patches of Chaetomorpha spp. and Enteromorpha spp., and rock ledges) were at least 150 m away from our sampling grid. Recent measurements of dispersal of postlarval bivalves < 1 mm long found a median dispersal distance of 49.0 cm after 12 h (Norkko et al., 2001), consistent with the view that meiofauna in our traps after 1 day of deployment probably came from the local mudflat habitat.

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Fegley (1988) sampled meiofauna dispersal over an intertidal flat of well-sorted fine sand (graphic mean F SE = 0.141 F 0.001 mm) for 5-min periods at different tidal cycle stages with traps similar to those in our study. He found that nematodes, but not copepods, were sometimes correlated with sediment volume in traps. Moreover, he found that nematodes were dominant in the ambient sandflat community, but proportionally underrepresented in traps compared to other taxa. Our mudflat results agreed with these from his North Carolina sandflat. On the other hand, there was a major difference between Fegley’s findings and ours. Copepods were never commonly captured in his traps, ranking far behind nematodes, turbellarians, ciliates, ostracods, and tardigrades. What caused these low absolute dispersal rates? Sandy sediment has a greater amount of interstitial space than mud does, allowing meiofauna to live deeply, where they may be less susceptible to erosion. Perhaps copepods were better able to resist erosion and hydrodynamic transport than the other meiofauna taxa were. However, copepods also had low density in Fegley’s ambient community, only 3% that of the nematodes. Were they uncommon in traps because each copepod had a low probability of dispersing? Or, alternatively, were they uncommon in traps simply because they were uncommon in the ambient community? 4.2. Meiofauna dispersal rates To answer this question, we used Fegley’s data to calculate relative dispersal rates (Table 3). On a per individual basis, the copepods dispersed much more readily than the nematodes, which is also what we discovered at our study site. Thus, their rarity in the North Carolina traps was probably due to their low density in the ambient community. The nematodes had a relative dispersal rate that was 10-fold greater in fast flow (flood tide) than in no flow (high tide), consistent with the idea that they were dispersing passively. Copepods had a relative dispersal rate that was only 4-fold greater in fast flow than in no flow conditions. Using nematodes as a benchmark, copepods had relative dispersal rates that were only 2-fold higher than the rate for nematodes in fast flow but 5-fold higher during no flow, consistent with the idea that they actively avoided fast flow conditions and emerged when flow was slow or nonexistent. Our bulk dispersal calculations from Fegley’s data showed that far fewer copepods than nematodes were captured per unit of sediment at his site. This result might explain why we found so many copepods in our traps and Fegley found so few. Few studies provide the data that Fegley’s (1988) does on the full range of meiofauna taxa, ambient community densities, and sediment captured in traps necessary to calculate all three meiofauna dispersal rates. It is too simplistic to use absolute dispersal rate as the sole estimator of meiofauna dispersal. Depending upon which dispersal rate is being compared, different conclusions can be drawn when comparing taxa or sites. Another study with data that can be used to demonstrate this point is Sun and Fleeger’s (1994) analysis of meiofauna movement in a Louisiana mudflat. They found that copepods as a whole were twice as abundant as nematodes in traps, so their absolute dispersal rate was 2-fold higher (Table 3; data presented as they reported it, overall means for the three deployment periods of 24, 48, and 72 h). However, the copepod relative dispersal rate was 14-fold higher because they were so much less abundant than nematodes in the ambient community. These relative dispersal rate calculations from Fegley (1988), Sun Fleeger (1994), and our study provide evidence that a copepod is much more likely to disperse than is a

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Table 3 Comparison of mean meiofauna dispersal rates among studies Investigation

Fegley (1988) High tide Copepods Nematodes Cop/Nem Flood tide Copepods Nematodes Cop/Nem Sun and Fleeger (1994) Copepods Nematodes Cop/Nem This study Copepods Nematodes Cop/Nem

Habitat

Ambient community density

Dispersal rate Absolute

Relative

Bulk

3.35 112.30 0.03

0.22 1.44 0.15

0.066 0.013 5.14

0.76 4.94 0.15

3.35 112.30 0.03

0.86 14.12 0.06

0.256 0.126 2.03

0.38 6.17 0.06

29.3 213.4 0.14

28.5 14.8 1.97

0.97 0.07 14.06

NA NA NA

19.21 1240.61 0.016

193.82 133.89 1.45

10.09 0.11 91.73

232.07 180.71 1.28

Intertidal sandflat, North Carolina, USA

Intertidal mudflat, Louisiana, USA

Intertidal mudflat, Maine, USA

All data normalized to 1 cm2 basis to make comparisons easier, but traps were deployed for different time periods: Fegley (1988), 5 min; Sun and Fleeger (1994), overall mean for 24, 48, and 72 h; this study, 1 day. Otherwise, units as in Table 1. NA = No sediment data collected.

nematode. It would be incorrect to assume, however, that this higher dispersal rate is due only to active behavior in copepods. Sun and Fleeger (1994) assigned life-style designations to the most common copepods at their site. Despite the higher overall absolute dispersal rates for copepods than for nematodes, four of the five dominant copepod species had absolute dispersal rates that were actually far lower than the rate for nematodes, and the fifth had a rate approximately equal to that of the nematodes. We calculated relative dispersal rates for these five species and discovered that the three epibenthic copepods had rates that were 10-fold, 45-fold, and 275-fold higher than the rate for nematodes. On the other hand, the rates for the tube-building and burrowing copepods were only 1.6-fold and 3-fold higher, respectively, than the rate for the nematodes. Thus, the surface-dwelling epibenthic forms all had much higher rates of relative dispersal than the deeper-dwelling tube-builder and burrower. These species-specific results for copepods could be due to active emergence, but they also parallel our species-specific conclusions about nematodes. Despite the obvious differences in morphology, swimming ability, and behavior between copepods and nematodes, the epibenthic forms within each taxon are more susceptible to erosion and more likely to disperse than deep forms. 4.3. Dispersal rates and spatial pattern Armonies (1994) has reviewed the complex landward and seaward movements of meiofauna resulting from the interaction of wind-generated and tidal currents at his wellstudied field site. Generally speaking, however, the hydrodynamic processes leading to the

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establishment and persistence of meiofauna spatial structure remain largely unknown. As water flows over complex bottom topography (sensu Commito and Rusignuolo, 2000), it causes spatial and temporal variability in current velocities. As a result, flow-mediated passive dispersal can create and destroy spatially ordered meiofauna density differences, even during a single tidal cycle (Sherman and Coull, 1980; Grant, 1981, 1983; Grant et al., 1997; Hogue, 1982; Warwick and Gee, 1984; Kern and Taghon, 1986; Decho and Fleeger, 1988; Fegley, 1988; Savidge and Taghon, 1988; DePatra and Levin, 1989; Sun and Fleeger, 1994; Fleeger et al., 1995; Thistle, 1998; Thistle and Levin, 1998). When hydrodynamic forces are less important, i.e., where tidal- and wind-induced currents are weak, at slack high and low tides, or in no-flow laboratory experiments, then active choice may play a more dominant role in determining meiofauna spatial structure (Service and Bell, 1987; Armonies, 1994; Sun and Fleeger, 1994; Fleeger et al., 1995). Our results suggest that caution must be used when interpreting the results of static microcosm and mesocosm experiments (Austen et al., 1998; Schratzberger and Warwick 1998, 1999a,b; Tita et al., 2000). Compared to typical flow regimes in nature, no-flow laboratory conditions might cause an increase in residence times within the sediment for nematodes (especially epigrowth-feeders) and a decrease for copepods. Palmer (1988b) has demonstrated the value of incorporating realistic flow regimes into microcosm experiments designed to test for predation and bioturbation effects on meiofauna. Understanding dispersal rates can shed light on the control of distribution patterns of meiofauna in the field. The interplay between the regional pool of dispersers and local ecological processes remains poorly understood (Palmer et al., 1996; Thrush et al., 2000), but the continual movement of meiofauna caused by transport events that are highly variable in space, time, and intensity could have a dramatic impact on local population and community dynamics.

5. Conclusion This investigation demonstrated for the first time, that three measures of meiofauna dispersal varied in predictable ways on an unvegetated mudflat. Absolute, relative, and bulk dispersal rates provided different types of information on the movement of meiofauna. Absolute dispersal is the most commonly reported measure of dispersal in the literature, yet it provides little insight into the movement of animals in relation to ambient densities and bedload processes. Comparison of our results with two other studies showed that absolute dispersal rates of nematodes and copepods varied widely. However, relative dispersal rates were always higher for copepods than for nematodes, even when the reverse was true for absolute dispersal rates. The results presented here quantified the highly dynamic behavior of meiofauna populations in soft-bottom communities. At our site, meiofauna taxa dispersed in relative proportions far different from those of the ambient community. Turnover times estimated from relative dispersal rates (i.e., the inverse of relative dispersal rate) at our site ranged from much less than 1 day for the mobile copepods and ostracods to 9 days for the nematodes. These short turnover times indicate that the role of dispersal must be included in any consideration of the ecology of soft-bottom systems at local and regional spatial scales.

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Acknowledgements We thank Gettysburg College Environmental Studies Department students J. Abrahamson and D. Risso for assistance in the field. J. Fleeger, C. Lardicci, and F. Maltagliati, and two anonymous reviewers made valuable comments on an earlier version of the manuscript. This research was made possible by support for J.A.C. provided by the Gettysburg College Grants Advisory Commission and the Dipartimento di Scienze dell’Uomo e dell’Ambiente, Universita` di Pisa. [RW]

Appendix A. Nematode species ranks for ambient community cores and bottom traps. Species ranked in the top 10 for cores or traps are set in bold font Species Actinonema sp. Amphimonhysterella sp. Anoplostoma viviparum Anticomopsis sp. Antomicron sp. Aponema sp. Axonolaimus sp. Campylaimus sp. Chromadora macrolaima Chromadorina sp. Comesa sp. Cytolaimium sp. Daptonema sp. Desmoscolex falcatus Diplopeltoides sp. Doliolaimus sp. Eleutherolaimus sp. Enoploides sp. Enoplus sp. Halalaimus sp. Halichoanolaimus sp. Hopperia americana Hypodontolaimus inaequalis Leptolaimus elegans Linhystera sp. Mesacanthion sp. Metachromadora sp. 1 Metachromadora sp. 2 Metalinhomoeus sp.

Feeding group 2A 1B 1B 1A 1A 2A 1B 1B 2A 2A 1B 1B 1B 1A 1A 1B 1B 2B 2B 1A 2B 2A 2A 1A 1A 2B 2B 2B 1B

Rank Cores

Traps

42 26 30 8 – – 9 24 2 13 – 40 1 – 37 16 46 31 31 29 41 18 17 12 15 33 10 3 22

21 – – 8 34 30 6 – 1 5 28 – 4 14 – 27 32 26 – 19 – 28 24 7 31 – 12 9 23

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Monhystera sp. Monoposthia costata Nannolaimoides sp. Nemanema cylindraticaudatum Odontophora sp. Oxystomina sp. Parachromadorita sp. Paradesmodora sp. Paralinhomoeus sp. Paramonhystera sp. Parasphaerolaimus sp. Pomponema sp. Promonhystera sp. Ptycholaimellus ponticus Retrotheristus sp. Richtersia sp. Sabatieria sp. 1 Sabatieria sp. 2 Sphaerolaimus sp. Spirinia sp. Terschellingia sp. Tricoma sp. Viscosia sp.

1B 2A 2A 1A 1B 1B 2A 2A 1B 1B 2B 2B 1B 2A 1B 1B 1B 1B 2B 2A 1A 1A 2B

– 34 43 34 6 43 11 36 14 19 20 43 27 5 23 38 7 21 28 – 4 38 25

11 – – – 10 34 2 – 17 – 13 – – 3 16 15 22 34 – 33 20 24 18

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