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Meiofaunal colonization of azoic estuarine sediment in Louisiana: Mechanisms of dispersal1
J. Exp. Mar. Biol. Ecol., 1983, Vol. 69, pp. 175-188
175
Elsevier
MEIOFAUNAL
COLONIZATION
OF AZOIC ESTUARINE
LOUISIANA: MECHANISMS
G. THOMAS
CHANDLER
SEDIMENT
IN
OF DISPERSAL’
and JOHN W. FLEEGER
Department of Zoology and Physiology, Louisiana State University, Baton Rouge, LA 70803. U.S.A.
Abstract: Two mechanisms of muddy-bottom meiofaunal dispersal, waterborne suspended transport and holobenthic infaunal immigration, were compared as to their rate and effectiveness in mediating community reestablishment after small-scale defaunation. Colonizing meiofauna were quantitatively sampled in winter and summer from 16 replicates of two azoic sediment chamber designs on 2 and 29 days postplacement. The chambers were u 3750 cm3; one design allowed colonization via suspended movement through an open top, while the other design permitted entry only by infaunal crawling through subsurface open sides. After 48 h, mean harpacticoid copepod and naupliar densities in sediment chambers open to colonization exclusively by meiofauna in suspended transport were not significantly different from background sediment densities. Sediment chambers allowing colonization exclusively via infaunal immigration through the sediment, however, contained copepod and naupliar densities that were significantly less than densities in background sediments and suspension-colonized chambers. In contrast, nematode densities in both suspension- and infaunally colonized chambers were significantly less than in background sediments, but densities were not significantly different between the chamber treatments. Thus for a small-scale defaunation, copepods most rapidly and completely recolonize sediments via suspended transport. Nematode dispersal occurs equally well via suspended or infaunal movement; however nematodes never seemed to utilize the chambers fully because densities did not reach background levels even after 29 days.
INTRODUCTION
Natural and man induced perturbations of marine and estuarine soft-bottom environments frequently defaunate communities. Large-scale disturbances such as hypoxia (Coull, 1969), red tides (Simon & Dauer, 1972) and dredging (Rhoads et al., 1978) can cause massive mortality of both macrofauna and meiofauna in soft sediments. Meiofauna may also be susceptible to small-scale, defaunating disturbances caused by macrofaunal burrowing and feeding activities (Thistle, 1980; Reidenauer & Thistle, 1981). Although dispersal and colonizing mechanisms (e.g. rates, modes of immigrant transport, etc.) of marine macrofauna have been extensively studied in hard bottoms (Connell, 1961,197s; Paine, 1966,1974; Dayton, 1971; Menge, 1974; Sousa, 1979)and soft bottoms (Dauer & Simon, 1976; Brunswig et al., 1976; McCall, 1977; Desbruyeres et al., 1980; Santos & Simon, 1980; Grant, 1981), less is known about these mechanisms in the meiofauna. Several studies have reported suspension of meiofauna ’ LUMCON Contribution No. 83-01, Louisiana Universities Marine Consortium, Star Route Box 541, Chauvin, LA 70344, U.S.A. 0022-0981/83/$03.00 0 1983 Elsevier Science Publishers B.V.
176
G.THOMASCHANDLERANDJOHNW.FLEEGER
from sands and muds and implicate its importance to rapid dispersal and recolonization (Alldredge & Ring, 1980; Sherman & Coull, 1980; Bell & Sherman. 1980; Hagerman & Rieger, 1981; Sibert, 1981) and to tidally induced changes in sediment densities (Palmer & Brand& 198 1). Suspension of mud-dwelling meiofauna is likely because they lack adhesive organs, and predominate in the easily resuspended, sediment surface layers (Rhoads et al., 1975, 1978). On the other hand, mud-dwelling meiofauna are well adapted for an infaunal existence with morphologies and appendages adapted for burrowing (e.g. harpacticoids have attenuated bodies, shovel-like rostra, and setose antennae and pereiopods). No studies have provided empirical evidence of the relative importance ofwater-borne, suspended movement versus infaunal, lateral crawling to the recolonization of large- or small-scale, defaunated muddy habitats. The purpose of this investigation was to determine which method of colonization is most rapid and effective in reestablishing an estuarine meiofaunal community after a simulated, small-scale defaunation. MATERIALS
AND
METHODS
The study area is located in the Terrebonne Bay estuary, Cocodrie, Louisiana, U.S.A. (29” 15’N : 91”21’W); a poorly mixed (mean tidal range = 0.3 m), highly productive estuary with wide salinity variation (l&26%,) and broad expanses of Spartina alterniflora Loisel marsh. Tides are diurnal, but tidal effect on water movement is almost negligible compared with wind effects. The study site is a shallow (0.5 m), unimpacted pond (25 m x 15 m) fed by a slow creek and surrounded by Spartina on all sides. In October 1980 and June 1981, 150 kg of sediment were collected from the pond in an area 10 m from the experimental area, and made azoic by repeated freezing (to - 20 ‘C) and thawing three or more times. Sediments were predominantly composed of silts (41%) and clays (17%) with a median grain diameter of 38 pm. Two principal azoic sediment chamber designs were used with two accessory designs to determine the rate and method of meiofaunal colonization - either by holobenthic immigration of infaunal adults, juveniles and/or larvae, or by swimming or passive suspension in the water column. Design I consisted of opened-top, plastic chambers (Fig. 1) filled with azoic sediment and carefully pushed into the pond sediment. A 2-cm lip extended above the sediment-water interface. Meiofaunal colonization by infaunal immigration was thereby prevented, but active or passive settlement via the water column could occur. Design II consisted of plastic trays covered with 63-pm Nitex mesh but with open sides (4 mm Vexar mesh covered) exclusively accessible to crawling or burrowing infauna. The Nitex covering prevented water-borne colonization by adult and juvenile copepods and adult nematodes, but allowed water and gas exchange. The chambers were pushed into the sediment leaving a 2-cm lip exposed, but to prevent epibenthic immigration of meiofauna, the side openings were 0.5 cm below the sediment-water interface. The two accessory designs consisted of (1) opened-top chambers (as in Design I) elevated 12 cm above the sediment-water interface by four small,
MEIOFAUNAL
COLONIZATION
AND DISPERSAL
177
Plexiglas, pedestals {Fig. l), and (2) open-sided chamber (as in Design II) pushed into the sediment but fitted with tightly seded, plastic lids. The elevated chambers were used to determine the short-term colonizing ability of meiofauna above the flocculent sediment surface. The lid-covered chambers were used to test the short-term effectiveness of the Nitex mesh in excluding meiofauna. DESIGN OF AZOIC
SEDIMENT
AIR-WATER
CMAMBERS
INTERFACE
ElEVATED
p
OPEN TOP
OPEN TOP
OPEN &ES
Fig. 1. Schematic of azoic sediment chamber designs, benthic placement, and ambient RPD depths. date-‘.
On 7 November, 1980, eight opened-top and eight open-sided chambers were equally dis~buted among four randomized sites in the pond sediment. At each site, ~disturbed sediments serving as the source pools of colonizers were cored 0.3 and 0.5 m from the chambers and used as controls. A total of nine control cores were collected on each sampling date. Two and 29 days after placement, meiofauna samples were taken among the four replicates of each treatment. A total of nine cores * treatment- ’ - date- ’ were taken with at least two per tray. The same experimental design was initiated on 6 July, 1981, with two exceptions: (a) four replicates of each accessory chamber design were distributed among the four pond sites, and (b) initial samples were taken at 1 day postplacement to determine ifcomplete colonization occurs before 2 days. Water depth in the pond ranged from 10 to 50 cm during the study. The mean RPD depth was determined for all treatments and control sites with an Eh meter and platinum electrode. Samples were taken from a boat with plastic piston corers (inner diameter = 2.7 cm). Coring was randomized by use of a numbered, plastic grid fitted to each chamber surface. Core positions were recorded so that tests for edge effects on the meiofaunal distribution within the chambers could be performed. Meiofaunal vertical positions in the sediment were preserved by freezing (within 12 s) intact cores in liquid nitrogen.
17s
G.THOMAS
CHANDLERANDJOHN
W.FLEEGER
Cores were stored on dry ice until sectioned with a coping saw at 0- 1, i-2,2-3 cm depth intervals. Samples were stained with rose bengal and preserved in 100,; buffered formalin. After sonification (35 s) in 10% Na(PO,), to dissociate clay aggregates, samples were passed through 500 and 63 ,um sieves and all individuals retained were enumerated to major taxon. Copepods were identified to species, staged and sexed. Nauplii were counted but not identified to species. Nematodes, if present at densities greater than 500 per sample, were subsampled (Sherman et al., in press). Tests for differences across treatments and controls, and among chambers nested within treatments, were calculated for mean densities of major meiofauna groups and individual copepod species by nested analysis of variance (ANOVA). If a significant difference was indicated, Duncan’s multiple range test was applied to obtain all pairwise comparisons among the sample means. Principal components ordination (Hotelling, 1933; Bloom et al., 1977) was applied to copepod species densities to determine the similarity of community structures across all treatments and dates. An alpha level of 0.05 was used for all tests of significance.
RESULTS
Nematodes were the most abundant meiofaunal taxon, accounting for 823, of the total meiofauna in control sediments, and 867, and 657~ in the open-sided and opened-top chambers respectively. Seven harpacticoid and one cyclopoid copepod species were found in the pond benthos: Pseudostenhelia wellsi Coull and Fleeger, Microarthridion littorale (Poppe), Paronychocamptus huntsmani (Willey), Scottolana canadensis (Willey), and Enhydrosoma woodiniThistle were the five major species, while Haliqclops fosteri M.S. Wilson, Cletocamptus deitersi (Richard) and an unidentified harpacticoid (fam. Ectinosomatidae) occurred sporadically. Generally meiofauna were most abundant in the uppermost centimeter of sediment; however, nematodes were found to 3 cm in depth. For nematodes over all sampling dates, 53 y0 of control, 78 T; in open-sided chambers, and 68% in opened-top chambers were found at the O-l cm depth. Seasonal differences in nematode vertical densities occurred in control sediments and opened-top chambers with a slightly shallower depth distribution in winter collections. Copepods and nauplii were highly restricted to the uppermost cm of sediment even when RPD depth was considerably deeper than 1 cm. Overall. 939; in controls and 970/b in open-sided and opened-top chambers occurred at the O-l cm depth. No seasonal changes in copepod or naupliar vertical distributions occurred. RPD depths in opened-top chambers on Days 2 and 29 in winter averaged 1.2 and 2.3 cm respectively. Open-sided chambers had more shallow RPD depths of 0.7 and 1.3 cm on Days 2 and 29. In summer on Days 1 and 29, RPD depths were 0.7 and and 0.6 and 0.9 cm in open-sided 0.9 cm respectively in opened-top chambers; chambers on these days. Control RPD depths were generally deeper, averaging 2.1 and
MEIOFAUNAL
COLONIZATION
AND DISPERSAL
179
3.9 cm on Days 2 and 29 in winter and 0.9 and 1.0 cm on Days 1 and 29 in summer. One-way ANOVA of RPD depths on each sampling date (d.f. = 2, 7 for Days 2 and found no 29 in winter and Day 29 in summer; d.f. = 4, 10 for Day 1 in surer) signiticant differences (a = 0.05) among treatments and controls within any date. Nested ANOVA of the major meiofauna groups and individual copepod species found no significant differences among replicate colonization chambers nested within treatments on Day 2 in winter or on Day 1 in summer (d.f. = 6, 18). On Day 29 in winter, ~aro~yc~ocarn~~s ~~~~rnani and En~ydr~soma ~oodinj exhibited mean densities that were significantly different among several chambers nested within treatments. Thus for all taxa, replicability among chambers was excellent for l-2 days, but after 29 days replicability decreased. One-way ANOVA was used to test for si~~c~t differences in mean densities of the major meiofauna groups and individual copepod species among the four control sites in the pond. No significant differences were found (d.f. = 3, 5), and the null hypothesis that the meiofaunal densities were equivalent among all control sites could not be rejected. Therefore, the meiofauna within the study site appear to be homogeneously distributed, although the sample sizes may have been too small to detect significant differences. The paired t-statistic was calculated for each treatment on cores taken from the chamber edge versus cores taken from the chamber center. No significant differences in mean meiofaun~ densities were found, thus no chamber edge effect was indicated. NESTED
ANOVA
OF MAJOR GROUPS
AND
COPEPOD
SPECIES
Mean densities of the major meiofauna groups (expressed - 10 cm-‘) encountered in the treatment and control sediments are presented in Fig. 2. Duncan’s multiple range test results (d.f. = 2, 18) are depicted by letters on top of the blocks such that means with the same letter(s) are not signiticantly different among treatments and/or controls within each date. In winter by 2 days or two tidal cycles after chamber placement, nematode densities in infaunally colonized chambers (i.e. “sides open” treatment) and suspension colonized chambers (i.e. “top open” treatment) were not significantly different, but both were significantly less than density in control sediments. After 29 days these trends remained unchanged. Copepod densities on Days 2 and 29 were not si~i~c~tly different in control sediments and opened-top chambers; however, density in open-sided chambers was significantly less for both collections. Naupliar density on Day 2 was significantly lower in open-sided chambers than in control sediments, but density in opened-top chambers was intermediate and not signilicantly different from the former two. By Day 29, naupliar density in opened-top chambers was significantly higher than in open-sided chambers, and was not significantly different from the control sediment density. In summer, 1 and 29 days after chamber placement, nematode densities in open-sided and opened-top chambers were not significantly different, but both were significantly less than the control density. Copepod and naupliar densities in opened-top chambers
G. THOMAS CHANDLER AND JOHN W. FLEEGER
I80
on day one were s~gn~c~tly higher than in open-sided chambers; but unlike Day 2 in winter, densities in opened-top chambers were significantly less than control densities. Therefore complete colonization by copepods probably occurs between one and two days. By Day 29, copepod densities in opened-top chambers and control sediments were not significantly different, but both were signifmtntly higher than in open-sided chambers. Simiiarly, nauphar density in open-sided chambers on Day 29 was sign& cantly less than in opened-top chambers, but control density was intermediate and not significantly different from either treatment. In the accessory treatments, nematode density in elevated chambers (x = 87.89, S, = 28.39) was not si~i~c~tly different from opened-top chambers (Fig. 2) but was
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Fig. 2. Mean densities of major meiofauna groups (expressed. 10 cm-“) for each treatment and sampling date: means sharing the same letter(s) across treatments are not si~i~cantly different; nested ANOVA and Duncan’s multiple range test; r = 0.05; d.f. = 2. 18.
significantly higher than in open-sided chambers. Nematode (x = 12.67, ST = 3.57) and naupliar (x = 8.85, S, = 3.56) densities in lid-covered chambers and open-sided chambers were not significantly different, therefore the short-term Nitex exclusion was effective. Copepod and naupliar densities (xcope = 37.81, S, = 8.59; ~__, = 50.08, S, = 4.74) in elevated chambers and opened-top chambers were not significantly different, indicating that colonization via suspension is equally as effective 12 cm above the interface as at 2 cm. Among individual copepod species, densities in the opened-top chambers were very similar to control levels, while densities in open-sided chambers tended to be depressed
MEIOFAUNAL
COLONIZATION
AND DISPERSAL
181
(Fig. 3). For winter samples, 2 days after chamber placement Parun~h~amptus colonizing opened-top chambers (Fig. 3). Higher densities were recorded in opened-top chambers on Days 2 and 29 than in control sediments or open-sided chambers for P. huntsmani. However, densities did not differ significantly. Pse~~stenheZiff wellsi was the most abundant harpacticoid in controls, and was the dominant species colonizing open-sided chambers on Day 2. Micruarthridion litturale was the dominant copepod in controls and open-top chambers on Day 29, however densities were significantly lower in open-sided chambers.
huntsmani was the dominant harpacticoid
ExPLAllrllTill
TREDTrnENIS
rxPmI#EWIRL
TRCRllEWTI
Fig. 3. Mean densities of major copepod species (expressed * 10 cmw2) for each treatment and sampling date: means sharing the same letter(s) across treatments are not significantly different; nested ANOVA and Duncan’s multiple range test; t( = 0.05; d.f. = 2, 18.
In summer, 1 day after chamber placement all copepod densities in the four chamber designs were significantly less than the control densities, except for the cyclopoid, Halicyclupsfosteri, which showed no difference among controls and experimental treatments. Copepod densities were significantly higher in opened-top chambers than in open-sided chambers for all species except H. fosteri. In elevated chambers, Paronychocamptus huntsmani@ = 1.89,5& = 0.5 1) was the only species with a density significantly different from (less than) that in opened-top chambers. Hulicyclups fisteti was the dominant colonizer on Day 1: control x = 9.25, S, = 1.58; open-sided x = 3.22, S, = 1.83; opened-top x = 14.08, S, = 6.01; elevated x = 15.69, S, = 6.87. After 29 days, Scottulana canadensis control density declined from the Day 1 level,
181
G. THOMAS CHANDLER
AND JOHN W. FLEEGER
but density in opened-top ch~bers increased and became si~i~c~t~y higher than in open-sided chambers (Fig. 3). Fse~dostenheIiu wellsi reached a density in opened-top chambers that was 15 times the Day 1 density and Feplaced Scottolana canadensis as the predominant species. Enhydrosoma wood&i was the only harpacticoid to reach equivalent densities in both the infauna@ colonized, open-sided chambers and the suspension colonized, opened-top chambers. PRINCIPAL
COMPONENTS
ORDINATION
OF COPEPOD
COMMUNITY
STRUCTURE
Principal components or~nation of the copepod collections (Fig. 4) shows the proximity (i.e. similarity) of suspension-colonized, infaunahy-colonized and natural communities in 3-vector, ordination space. The three axes account for 83.10, of the total variance: Axis 1 = 39.8%, Axis 2 = 26.8”,b, and Axis 3 = 16.5”,;. Generally, on every sampling date (except Summer: Day 29 open-sided chambers), ordination scores for treatments and controls on Axis 3 are equivalent (between - 0.3 and 0.4). Axis 1 scores separate the control and chamber communities into similardate groups, while Axis 2 scores separate the three communities within each date. For samples taken 2 days after chamber placement in winter, the copepod ordination scores for open-sided chambers and controls are almost identical on all three axes. The opened-top chamber community is clearly different, however, as the score on Axis 2 is 3 units from controls and open-sided chambers. After 29 days, the Axis 2 scores for open-sided chambers and controls are almost equal, but opened-top chamber scores are 2.2 units away. The overall ordination pattern for Day 29, however, shows general similarity among all three copepod communities. One day after placement in summer, total copepod densities in all chambers were depressed, and the community ordination scores for both chamber treatments are almost identical, but over 4 units from the control score on this date. After 29 days, ordination scores on Axis 1 are variable, ranging from 0.9 to 9.0. Axis 2 scores produce a pattern more consistant with Day 29 in winter: Scores for controls and open-sided chambers are similar (1.4 units apart), but opened-top chambers are over 4 units from the control. Significantly poor replicability among chambers may have caused the aberrant pattern on Axes I and 3. DISCUSSION
Our experiments have shown that copepod and nauphar colonization via suspended movement into azoic sediment chambers was extremely rapid, because densities reached ambient control levels after only 2 days (i.e. two tidal cycles). After only 1 day, densities in the suspension-colonized chambers were significantly higher than in chambers colonized exclusively by infaun~ ~mmi~at~on. Therefore copepods and nauplii more rapidly colonize defaunated sediments via suspended transport than by holobenthic, infaunal immigration. In contrast, nematode densities in suspension colonized (opened-
MEIOFAUNAL
COLONIZATION
AND DISPERSAL
183
top) and infaunally colonized (open-sided) chambers were not significantly different on any sample date. Densities in both chamber designs were, however, signiticantly less than control densities on all sampling dates, even after 29 days. Thus for nematodes, either dispersal mode, suspended or infaunal, is effective for dispersal and colonization over short distances, but complete colonization requires >29 days in this system. Several studies have investigated rates and extent of meiofaunal colonization of defaunated or azoic habitats. Sherman & Coull(l980) found almost complete colonization (i.e. predisturbance densities were reestablished) of a partially defaunated, intertidal mud-flat by copepods and nematodes after one tidal cycle (12 h), and suggested that suspended transport may have been the mechanism for colonization. Thistle (1980) also found rapid (< 24 h) colonization of defaunated enteropneust fecal mounds by subtidal harpacticoids. However, Alongi (1981) showed that in subtidally placed, azoic sediment trays, nematodes required 7 days to reach background densities while copepods took 5 days. Bell & Coen (1982) found that copepods and nauplii took from 1 to 5 days to colonize azoic Diopatra tube caps reimplanted in a sand flat, but they could not conclude which pathway was more efficient - infaunal or suspended. Contrasts in colonizing modes used by copepods and nematodes are probably caused by their different abilities to become suspended, and by differences in their vertical distribution in the sediment. Harpacticoid and epibenthic cyclopoid copepods have been captured while suspended in waters overlying a subtidal sand flat (e.g. Cyclopina sp. and Tisbe sp.; Alldredge & King, 1980) and an intertidal mud flat (e.g. Halicyclops coulli, Microarthridion littorale, and Enhydrosoma propinquum; Bell & Sherman, 1980) but few or no nematodes were found suspended at either site. Hagerman & Rieger (1981) found that not only harpacticoids but nematodes, polychaetes, kinorhynchs, turbellarians, gastrotichs, gnathostomulids, rotifers and halicarid mites occur regularly in the water column from 1 to 1.5 m above the sediment-water interface. Although meiofauna have been found in suspension a meter or more above the bottom, Sibert’s work (1981) suggests that meiofauna in the water column tend to behave demersally (sensu Alldredge & King, 1980), being most numerous just above the sediment-water interface: 5 cm above an unscoured, tidal channel bottom, nematodes were 2 to 5 times more abundant than at 30 cm, and harpacticoids averaged 7 to 12 times more abundant. Microarthridion littorale, the only copepod common to Sibert’s and our study, was 3 to 24 times more abundant at 5 cm. Palmer & Brandt (198 1) proposed that tidal currents suspended the meiofauna from intertidal sediments and caused copepod sediment densities to increase at slack high and low tide, when settlement occurs, but decrease during flooding and ebbing - periods of high resuspension. Little work has been conducted on meiofauna to determine if the mechanism of suspension is active, e.g. by swimming behavior, or passive, i.e. mediated by current flow. Many mud-dwelling harpacticoids and cyclopoids can swim, and suspension by active means is possible and likely. Nematodes, however, are usually thought of as non-swimming, but our results show that they were significantly more abundant in chambers elevated 12 cm into the water column than in infaunally colonized chambers
184
G. THOMAS
CHANDLER
AND JOHN
W. FLEEGER
after one day indicating considerable ability to become suspended. Literature reports of nematode dispersal by passive, suspended movement and the existence of an active swimming mode do exist. For example, the viviparous nematode, Anoplostoma viviparum, has a life history that minimizes the deleterious effects and maximizes the beneficial effects of water-borne dispersal. Gravid females buffer themselves from suspension by “gestating” in the deep anoxic layer; hatching juveniles then migrate to the flocculent, surface layer and are dispersed in suspension by water currents (Surey-Gent, 1981). Jensen (1981) showed that the phytal, epistrate-feeding nematode, Chromadorita tenuis, can rapidly swim (5 cm. s- ‘) from the benthos to submerged vegetation. A writhing or serpentine swimming behavior may insure that they remain in suspension long enough to be passively dispersed with currents, and for longer distances than swimming alone could achieve. In our study, > 95 y0 of the copepods and nauplii in control sediments were restricted to the oxidized, uppermost cm of sediment; whereas nematodes, although most abundant in the upper cm, occurred abundantly to 3 cm in depth. Copepods were thus more nearly complete colonizers of the opened-top chambers than were the nematodes, and probably because of (a) a surticial distribution that enhances the probability of passive suspension from current action, etc., and limits the possible pathways for infaunal movement, (b) better swimming ability, and (c) easier suspension due to a larger body volume with many setose appendages. The combination of high densities (436 to 3696 . 10 cme2) in the flocculent, easily suspended, surface sediments with considerable numbers in deeper sediments (461 to 2159. 10 cm-‘) enabled the nematodes to colonize the azoic sediment equally well via suspended transport or infaunal immigration. Surficial meiofauna may have been suspended by current scouring, macrofaunal activities (e.g. feeding, burrowing, swimming, etc.), and/or active swimming and then swept into the opened-top chambers by water movement, but deeper occurring individuals would escape suspension. With deeper sediment distribution, the nematodes are exposed to more avenues of infaunal movement than the shallow-occurring copepods and thus were better colonizers of the open-sided chambers. However, the open-sided chambers with side openings 0.5 cm below the sediment surface (Fig. 1) may have biased our copepod results by precluding colonization of species with biologies restricting them to the hyper- or epibenthos (e.g. Scottolana canadensis). Nonetheless copepods colonize so effectively by suspended movement that by comparison infaunal crawling is undoubtedly much less important to dispersal in muddy habitats. Among the individual copepod species in our study, those species that were predominant in control sediments generally predominated in opened-top sediment chambers by 2 days. Passive suspension of the copepod community from control sediments may have resulted in an in toto transport of all species from the control areas into the opened-top chambers. However, only if passive suspension afFected every species uniformly would the community formed from subsequent random settlement have a structure similar to control sediments. Active movement by some meiofauna into the water column or chambers would tend to alter, i.e. weight, the relative densities of the immigrating species
MEIOFAUNAL
COLONIZATION
185
AND DISPERSAL
expected from passive suspension and random resettlement. Non-uniform suspension of individuals with morphologies or behaviors capable of enhancing (e.g. setose forms) or avoiding (e.g. burrowers) suspending influences would have the same effect. Although relative densities of most species in opened-top chambers approximate the control heirarchy found on Days 2 and 29 in winter and Day 29 in summer, principal components ordination shows that the chamber community structure is different. Species associations upon initial settlement are probably not a result of entirely random, passive processes. Based on differences in swimming abilities alone, some species would be expected to colonize the opened-top chambers more effkiently. Active immigrants may have caused a change in the control-like community structure expected from uniform suspension and random resettlement because of their weighting influence on relative densities. Our evidence suggests that opened-top chamber community structure was influenced by protracted immigration and emigration of individuals throughout the study period. Open-sided chamber communities on Days 2 and 29 in winter and Day 29 in summer were nearest to the control community in ordination space (Fig. 4). Open-sided chambers provided direct, lateral access to copepods burrowing infaunally from PRINCIPAL
AXIS
Ill
-S-
Fig. 4. Principal components ordination of copepod communities across dates Day 2 control; 2, winter: Day 2 open-top; 3, winter: Day 2 open-sides; 4, winter: Day 29 open-top; 6, winter: Day 29 open-sides; 7, summer: Day 1 control; 8, 9, summer: Day 1 open-sides; 10, summer: Day 29 control; 11, summer: Day Day 29 open-sides.
-9
and treatments: 1, winter: Day 29 control; 5, winter: summer: Day 1 open-top; 29 open-top; 12, summer:
186
G. THOMAS
CHANDLER
AND JOHN W. FLEEGER
adjacent control sediments. Therefore the resulting community structure was more similar to controls even though densities were uniformly depressed (Fig. 3) among species. Colonization seemed to be characterized subsurface open sides by all of the mud-dwelling Individual copepod species showed differential
by random, species. colonization
Day 2 of colonization, the predominant harpacticoid stenheliu wellsi, did not colonize opened-top chambers
active encounter responses.
of the
In winter on
in control sediments, Pseudoas densely as the less abundant
Paronychocamptus huntsmani (see Fig. 3), indicating either active immigration by the latter or active chamber avoidance by the former. P. weffsimay be an efficient burrower as it showed a significantly higher density than any other species in the infaunally colonized chambers on this date. After 29 days, densities of Microarthridion littorale increased dramatically, while densities of Pseudostenheliu wellsiwere depressed in both chamber treatments. In summer, control densities of Microarthridion littorule were low (2 = 2.00. 10 cm-‘), and Pseudostenhelia wellsi and Puronychocamptus huntsmuni reached equivalent densities in both chambers after 1 day. After 29 days in the opened-top chambers, Pseudostenhelia wellsiincreased to a significantly higher density than Paronychocamptus huntsmani and control levels; possibly indicating a faster colonization rate, higher reproductive output, better ability to avoid passive emigration, better competitive abilities and/or better ability to avoid predators - none of which could be tested by our design. The second most abundant species, Scott&mu cunadensis. is an epibenthic, albeit photonegative, species (Harris, 1977) with abundant planktonic nauplii (Heinle, 1969). Therefore, not surprisingly, S. cunadensis was predominantly a suspension colonizer reaching a density of 48 . 10 cm ’ in opened-top chambers by Day 29, but found at ~3. 10 cm ’ in infaunally colonized chambers on all sampling dates. In contrast, Halicyclopsfosteri, an epibenthic but also planktonic (Lindsay, 1974; Aurand & Daiber. 1979) copepod was the only species to reach densities in all chamber treatments equivalent to control levels after 1 day, indicating considerable capability for burrowing as well as swimming. Enh_vdrosomawondinialso immigrated equally well via infaunal or suspended movement, as densities in opened-top and opensided chambers were equal and not significantly different from controls by Day 29 in summer. This species was often found from O-3 cm depth and thus would be expected to utilize either and ecologically colonizing pathway. Enhydrosoma propinquum, ;1 morphologicallysimilar species had been considered a strictly burrowing species until Bell & Sherman (I 980) found it suspended in overlying waters. E. woodini seems to behave in a similar Way.
Large-scale defaunations of meiobenthic communities (eg. Coull, 1969) recover more slowly than small-scale disturbances. The greater distance between potential colonizers and the epicenter of a large scale disturbance is more diEcult to traverse because meiofauna generally lack pelagic larvae. However active or passive suspension of meiofauna would probably increase recolonization rates and be faster than infaunal immigration over the large scale. Small-scale defaunations are less likely to undergo the
MEIOFAUNALCOLONIZATIONANDDISPERSAL
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successional changes in predominant species or species guilds suggested by Grassle & Sanders (1973), as immigration distance is short and suspended transport effects rapid community restoration (2 days for copepods in our system). Successional changes in the meiofaunal communities colonizing large-scale defaunations need to be studied, and the structuring influences of species interactions on developing communities need to be determined. In muddy-bottoms, suspending influences (e.g. current scouring, macrofaunal feeding and locomotory movements, active emergence into overlying waters, etc.) generate a mobile meiofaunal community, and may be equally or more important than biotic interactions in structuring the community in space.
ACKNOWLEDGEMENTS
Special thanks to the Louisiana Universities Marine Consortium (LUMCON) and its director, D. F. Boesch, for the abundant facilities and equipment support. Thanks also to Y. Ledoux for assistance in graphics, G. R. Fitzhugh for field work, T. C. Shirley and D. W. Garton for computer programming, and D. F. Boesch, W. B. Stickle and W. J. Harman for reviewing an earlier manuscript. This research was part of an MS. thesis by G.T. Chandler at Louisiana State University.
REFERENCES ALLDREDGE,A. L. & J. M. KING, 1980. Effects of moonlight on the vertical migration patterns of demersal zooplankton. J. Exp. Mar. Biol. Ecol., Vol. 44, pp. 133-156. ALONGI,D.M., 1981. Recolonization ofmeiobenthos in oiled azoic subtidal muddy sands ofthe York River estuary, Virginia. M.A. thesis, College of William and Mary, Virginia, 96 pp. AURAND,D. & F. C. DAIBER, 1979. Further observations on the occurrence of Halicyclops fosferi Wilson (Copepoda, Cyclopoida) in the Delaware Bay region, U.S.A. Crustaceana, Vol. 36, pp. 155-165. BELL, S. S. & K. M. SHERMAN,1980. A field investigation of meiofaunal dispersal: tidal resuspension and implications. Mar. Ecol. Prog. Ser., Vol.3, pp. 245-249. BELL, S. S. & L. D. COEN, 1982. Investigations on epibenthic meiofauna. I. Repopulation of the tube caps of Diopatra cuprea (Polychaeta : Onuphidae) in a subtropical system. Mar. Biol., Vol. 67, pp. 303-309. BLOOM,S.A., S. L. SANTOS& J. G. FIELD, 1977. A package of computer programs for benthic community analyses. Bull. Mar. Sci., Vol.27, pp. 577-580. BRUNSWIG,D., W. E. ARNTZ & H. RUMOHR, 1976. A tentative field experiment on population dynamics of macrobenthos in the western Baltic. Kiel. Meeresforsch., Vol. 3, pp. 49-59. CONNELL,J. H., 1961. The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus. Ecology, Vol. 42, pp. 710-723. CONNELL,J. H., 1978. Diversity in tropical rain forests and coral reefs. Science, Vol. 198, pp. 1302-1310. COULL,B.C., 1969. Hydrographic control of meiobenthos in Bermuda. Limnol. Oceanogr., Vol. 14, No. 6, pp. 953-957. DAUER, D.M. & J.L. SIMON, 1976. Habitat expansion among polychaetous annelids repopulating a defaunated marine habitat. Mar. Biol., Vol. 37, pp. 169-177. DAYTON,P. K., 1971.Competition, disturbance, and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecol. Monogr., Vol. 41, pp. 351-389. DESBRUYERES,D., J.Y. BERVAS& A. KHRIPOUNOFF,1980. Un cas de colonization rapide dun sediment profond. Oceanol. Acta, Vol. 3, No. 3, pp. 285-291. GRANT, J., 1981. Sediment transport and disturbance on an intertidal sandflat: infaunal distribution and recolonization. Mar. Ecol. Prog. Ser., Vol. 6, pp. 249-255.
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W. FLEEGER
GRASSLE,J. F. & H.F. SANDERS, 1973. Life histories and the role of disturbance. Deep-Sea Res., Vol. 20, pp. 643-659. HAGERMAN,G.M. & R.M. RIEGER, 1981. Dispersal of benthic meiofauna by wave and current action in Bogue Sound, North Carolina, U.S.A. Mar. Ecol., Vol. 2, No. 3, pp. 245-270. HEINLE, D.R., 1969. Temperature and zooplankton. Chesapeake Sci., Vol. 10, pp. 186-209. HOTELLING,H., 1933. Analysis of a complex of statistical variables into principal components. J. E&c. Psychol., Vol. 24, pp. 417-441. JENSEN, P., 1981. Phyto-chemical sensitivity and swimming behavior of the free-living marine nematode Chromadorita tent&. Mar. Ecol. Prog. Ser., Vol. 4, pp. 203-206. HARRIS, R.P., 1977. Some aspects of the biology of the harpacticoid copepod, Scottolana canadensis (Willey), maintained in laboratory culture. Chesapeake Sci., Vol. 18, pp. 245-252. LINDSAY,J. A.,1974. The occurrence of a Gulf of Mexico cyclopoid copepod Halicyclopsfosteri Wilson, in the Delaware River estuary with comments on morphological variation. Crustaceana, Vol. 27, pp. 184-188. MCCALL, P. L., 1977. Community patterns and adaptive strategies of the infaunal benthos of L.ong Island Sound. J. Mar. Res., Vol. 35, pp. 221-226. MENGE. B.A., 1974. Effect of wave action and competition on brooding and reproductive effort in the seastar, Leptasterias hexactis. Ecology, Vol. 55, pp. 54-93. PAINE, R.T., 1966. Food web complexity and species diversity. Am. Nat., Vol. 100, pp. 65-75. PAINE, R.T., 1974. Intertidal community structure: experimental studies on the relationship between a dominant competitor and its principal predator. Oecologia (Berlin), Vol. 15, pp. 93-120. PALMER,M. A. & R. R. BRANDT,1981. Tidal variation in sediment densities of marine benthic copepods. Mar. Ecol. Prog. Ser., Vol. 4, pp. 207-212. REIDENAUER,J. A. & D. THISTLE, 1981. Response of a soft-bottom harpacticoid community to stringray (Dasyatis sabina) disturbance. Mar. Biol., Vol. 65, pp. 261-267. RHOADS,D. C., K. R. TENORE& M. BROWNE,1975. The role of suspended bottom mud in nutrient cycles of shallow embayments. In, Estuatine research. Vol. I. Chemistry, biology and the estuarine system, edited by L. E. Cronin, Academic Press, New York, pp. 563-579. RHOADS,D.C., P. L. MCCALL& J.Y. YINGST, 1978. Disturbance and production on the estuarine seafloor. Am. Sci., Vol. 66, pp. 577-586. RHOADS,D. C., J.Y. YINGST& W. J. ULLMAN,1978. Seafloor stability in central Long island Sound: part 1. Temporal changes in erodability offind-grained sediment. In, Estuarlne interactions, edited by M. L. Wiley, Academic Press, New York, pp. 221-244. SANTOS, S. L. & J. L. SIMON, 1980. Marine soft-bottom community establishment following annual defaunation: larval or adult recruitment? Mar. Ecol. Prog. Ser., Vol. 2, pp. 235-241. SHERMAN,K.M. & B.C. COULL, 1980. The response of meiofauna to sediment disturbance. J. Exp. Mar. Biol. Ecol.. Vol. 45, pp. 59-71. SHERMAN,K. M., J. A. REIDENAUER& D. THISTLE,in press. A technique for subsampling an abundant taxon while completely sorting other taxa. Mar. Ecol. Prog. Ser. SIBERT, J.R., 1981. Intertidal hyperbenthic populations in the Nanaimo estuary. Mar. Biol., Vol. 46, pp. 259-265. SIMON,J. L. & D. M. DAUER, 1972. A quantitative evaluation of red tide induced mass mortalities of benthic invertebrates. Environ. Lett., Vol. 3, pp. 229-234. SOUSA,W. P., 1979. Disturbance in marine intertidal boulder fields: the nonequilibrium of species diversity. Ecology, Vol. 60, pp. 1225-1239. SUREY-GENT,S.C., 1981. Distribution of Anoplostoma viviparum (Nematoda) in Southampton water sediments. Mar. Biol., Vol. 62, pp. 157-160. THISTLE,D., 1980.The response of a harpacticoid copepod community to a small-scale natural disturbance. J. Mar. Res., Vol. 38, pp. 281-295.
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Elsevier
MEIOFAUNAL
COLONIZATION
OF AZOIC ESTUARINE
LOUISIANA: MECHANISMS
G. THOMAS
CHANDLER
SEDIMENT
IN
OF DISPERSAL’
and JOHN W. FLEEGER
Department of Zoology and Physiology, Louisiana State University, Baton Rouge, LA 70803. U.S.A.
Abstract: Two mechanisms of muddy-bottom meiofaunal dispersal, waterborne suspended transport and holobenthic infaunal immigration, were compared as to their rate and effectiveness in mediating community reestablishment after small-scale defaunation. Colonizing meiofauna were quantitatively sampled in winter and summer from 16 replicates of two azoic sediment chamber designs on 2 and 29 days postplacement. The chambers were u 3750 cm3; one design allowed colonization via suspended movement through an open top, while the other design permitted entry only by infaunal crawling through subsurface open sides. After 48 h, mean harpacticoid copepod and naupliar densities in sediment chambers open to colonization exclusively by meiofauna in suspended transport were not significantly different from background sediment densities. Sediment chambers allowing colonization exclusively via infaunal immigration through the sediment, however, contained copepod and naupliar densities that were significantly less than densities in background sediments and suspension-colonized chambers. In contrast, nematode densities in both suspension- and infaunally colonized chambers were significantly less than in background sediments, but densities were not significantly different between the chamber treatments. Thus for a small-scale defaunation, copepods most rapidly and completely recolonize sediments via suspended transport. Nematode dispersal occurs equally well via suspended or infaunal movement; however nematodes never seemed to utilize the chambers fully because densities did not reach background levels even after 29 days.
INTRODUCTION
Natural and man induced perturbations of marine and estuarine soft-bottom environments frequently defaunate communities. Large-scale disturbances such as hypoxia (Coull, 1969), red tides (Simon & Dauer, 1972) and dredging (Rhoads et al., 1978) can cause massive mortality of both macrofauna and meiofauna in soft sediments. Meiofauna may also be susceptible to small-scale, defaunating disturbances caused by macrofaunal burrowing and feeding activities (Thistle, 1980; Reidenauer & Thistle, 1981). Although dispersal and colonizing mechanisms (e.g. rates, modes of immigrant transport, etc.) of marine macrofauna have been extensively studied in hard bottoms (Connell, 1961,197s; Paine, 1966,1974; Dayton, 1971; Menge, 1974; Sousa, 1979)and soft bottoms (Dauer & Simon, 1976; Brunswig et al., 1976; McCall, 1977; Desbruyeres et al., 1980; Santos & Simon, 1980; Grant, 1981), less is known about these mechanisms in the meiofauna. Several studies have reported suspension of meiofauna ’ LUMCON Contribution No. 83-01, Louisiana Universities Marine Consortium, Star Route Box 541, Chauvin, LA 70344, U.S.A. 0022-0981/83/$03.00 0 1983 Elsevier Science Publishers B.V.
176
G.THOMASCHANDLERANDJOHNW.FLEEGER
from sands and muds and implicate its importance to rapid dispersal and recolonization (Alldredge & Ring, 1980; Sherman & Coull, 1980; Bell & Sherman. 1980; Hagerman & Rieger, 1981; Sibert, 1981) and to tidally induced changes in sediment densities (Palmer & Brand& 198 1). Suspension of mud-dwelling meiofauna is likely because they lack adhesive organs, and predominate in the easily resuspended, sediment surface layers (Rhoads et al., 1975, 1978). On the other hand, mud-dwelling meiofauna are well adapted for an infaunal existence with morphologies and appendages adapted for burrowing (e.g. harpacticoids have attenuated bodies, shovel-like rostra, and setose antennae and pereiopods). No studies have provided empirical evidence of the relative importance ofwater-borne, suspended movement versus infaunal, lateral crawling to the recolonization of large- or small-scale, defaunated muddy habitats. The purpose of this investigation was to determine which method of colonization is most rapid and effective in reestablishing an estuarine meiofaunal community after a simulated, small-scale defaunation. MATERIALS
AND
METHODS
The study area is located in the Terrebonne Bay estuary, Cocodrie, Louisiana, U.S.A. (29” 15’N : 91”21’W); a poorly mixed (mean tidal range = 0.3 m), highly productive estuary with wide salinity variation (l&26%,) and broad expanses of Spartina alterniflora Loisel marsh. Tides are diurnal, but tidal effect on water movement is almost negligible compared with wind effects. The study site is a shallow (0.5 m), unimpacted pond (25 m x 15 m) fed by a slow creek and surrounded by Spartina on all sides. In October 1980 and June 1981, 150 kg of sediment were collected from the pond in an area 10 m from the experimental area, and made azoic by repeated freezing (to - 20 ‘C) and thawing three or more times. Sediments were predominantly composed of silts (41%) and clays (17%) with a median grain diameter of 38 pm. Two principal azoic sediment chamber designs were used with two accessory designs to determine the rate and method of meiofaunal colonization - either by holobenthic immigration of infaunal adults, juveniles and/or larvae, or by swimming or passive suspension in the water column. Design I consisted of opened-top, plastic chambers (Fig. 1) filled with azoic sediment and carefully pushed into the pond sediment. A 2-cm lip extended above the sediment-water interface. Meiofaunal colonization by infaunal immigration was thereby prevented, but active or passive settlement via the water column could occur. Design II consisted of plastic trays covered with 63-pm Nitex mesh but with open sides (4 mm Vexar mesh covered) exclusively accessible to crawling or burrowing infauna. The Nitex covering prevented water-borne colonization by adult and juvenile copepods and adult nematodes, but allowed water and gas exchange. The chambers were pushed into the sediment leaving a 2-cm lip exposed, but to prevent epibenthic immigration of meiofauna, the side openings were 0.5 cm below the sediment-water interface. The two accessory designs consisted of (1) opened-top chambers (as in Design I) elevated 12 cm above the sediment-water interface by four small,
MEIOFAUNAL
COLONIZATION
AND DISPERSAL
177
Plexiglas, pedestals {Fig. l), and (2) open-sided chamber (as in Design II) pushed into the sediment but fitted with tightly seded, plastic lids. The elevated chambers were used to determine the short-term colonizing ability of meiofauna above the flocculent sediment surface. The lid-covered chambers were used to test the short-term effectiveness of the Nitex mesh in excluding meiofauna. DESIGN OF AZOIC
SEDIMENT
AIR-WATER
CMAMBERS
INTERFACE
ElEVATED
p
OPEN TOP
OPEN TOP
OPEN &ES
Fig. 1. Schematic of azoic sediment chamber designs, benthic placement, and ambient RPD depths. date-‘.
On 7 November, 1980, eight opened-top and eight open-sided chambers were equally dis~buted among four randomized sites in the pond sediment. At each site, ~disturbed sediments serving as the source pools of colonizers were cored 0.3 and 0.5 m from the chambers and used as controls. A total of nine control cores were collected on each sampling date. Two and 29 days after placement, meiofauna samples were taken among the four replicates of each treatment. A total of nine cores * treatment- ’ - date- ’ were taken with at least two per tray. The same experimental design was initiated on 6 July, 1981, with two exceptions: (a) four replicates of each accessory chamber design were distributed among the four pond sites, and (b) initial samples were taken at 1 day postplacement to determine ifcomplete colonization occurs before 2 days. Water depth in the pond ranged from 10 to 50 cm during the study. The mean RPD depth was determined for all treatments and control sites with an Eh meter and platinum electrode. Samples were taken from a boat with plastic piston corers (inner diameter = 2.7 cm). Coring was randomized by use of a numbered, plastic grid fitted to each chamber surface. Core positions were recorded so that tests for edge effects on the meiofaunal distribution within the chambers could be performed. Meiofaunal vertical positions in the sediment were preserved by freezing (within 12 s) intact cores in liquid nitrogen.
17s
G.THOMAS
CHANDLERANDJOHN
W.FLEEGER
Cores were stored on dry ice until sectioned with a coping saw at 0- 1, i-2,2-3 cm depth intervals. Samples were stained with rose bengal and preserved in 100,; buffered formalin. After sonification (35 s) in 10% Na(PO,), to dissociate clay aggregates, samples were passed through 500 and 63 ,um sieves and all individuals retained were enumerated to major taxon. Copepods were identified to species, staged and sexed. Nauplii were counted but not identified to species. Nematodes, if present at densities greater than 500 per sample, were subsampled (Sherman et al., in press). Tests for differences across treatments and controls, and among chambers nested within treatments, were calculated for mean densities of major meiofauna groups and individual copepod species by nested analysis of variance (ANOVA). If a significant difference was indicated, Duncan’s multiple range test was applied to obtain all pairwise comparisons among the sample means. Principal components ordination (Hotelling, 1933; Bloom et al., 1977) was applied to copepod species densities to determine the similarity of community structures across all treatments and dates. An alpha level of 0.05 was used for all tests of significance.
RESULTS
Nematodes were the most abundant meiofaunal taxon, accounting for 823, of the total meiofauna in control sediments, and 867, and 657~ in the open-sided and opened-top chambers respectively. Seven harpacticoid and one cyclopoid copepod species were found in the pond benthos: Pseudostenhelia wellsi Coull and Fleeger, Microarthridion littorale (Poppe), Paronychocamptus huntsmani (Willey), Scottolana canadensis (Willey), and Enhydrosoma woodiniThistle were the five major species, while Haliqclops fosteri M.S. Wilson, Cletocamptus deitersi (Richard) and an unidentified harpacticoid (fam. Ectinosomatidae) occurred sporadically. Generally meiofauna were most abundant in the uppermost centimeter of sediment; however, nematodes were found to 3 cm in depth. For nematodes over all sampling dates, 53 y0 of control, 78 T; in open-sided chambers, and 68% in opened-top chambers were found at the O-l cm depth. Seasonal differences in nematode vertical densities occurred in control sediments and opened-top chambers with a slightly shallower depth distribution in winter collections. Copepods and nauplii were highly restricted to the uppermost cm of sediment even when RPD depth was considerably deeper than 1 cm. Overall. 939; in controls and 970/b in open-sided and opened-top chambers occurred at the O-l cm depth. No seasonal changes in copepod or naupliar vertical distributions occurred. RPD depths in opened-top chambers on Days 2 and 29 in winter averaged 1.2 and 2.3 cm respectively. Open-sided chambers had more shallow RPD depths of 0.7 and 1.3 cm on Days 2 and 29. In summer on Days 1 and 29, RPD depths were 0.7 and and 0.6 and 0.9 cm in open-sided 0.9 cm respectively in opened-top chambers; chambers on these days. Control RPD depths were generally deeper, averaging 2.1 and
MEIOFAUNAL
COLONIZATION
AND DISPERSAL
179
3.9 cm on Days 2 and 29 in winter and 0.9 and 1.0 cm on Days 1 and 29 in summer. One-way ANOVA of RPD depths on each sampling date (d.f. = 2, 7 for Days 2 and found no 29 in winter and Day 29 in summer; d.f. = 4, 10 for Day 1 in surer) signiticant differences (a = 0.05) among treatments and controls within any date. Nested ANOVA of the major meiofauna groups and individual copepod species found no significant differences among replicate colonization chambers nested within treatments on Day 2 in winter or on Day 1 in summer (d.f. = 6, 18). On Day 29 in winter, ~aro~yc~ocarn~~s ~~~~rnani and En~ydr~soma ~oodinj exhibited mean densities that were significantly different among several chambers nested within treatments. Thus for all taxa, replicability among chambers was excellent for l-2 days, but after 29 days replicability decreased. One-way ANOVA was used to test for si~~c~t differences in mean densities of the major meiofauna groups and individual copepod species among the four control sites in the pond. No significant differences were found (d.f. = 3, 5), and the null hypothesis that the meiofaunal densities were equivalent among all control sites could not be rejected. Therefore, the meiofauna within the study site appear to be homogeneously distributed, although the sample sizes may have been too small to detect significant differences. The paired t-statistic was calculated for each treatment on cores taken from the chamber edge versus cores taken from the chamber center. No significant differences in mean meiofaun~ densities were found, thus no chamber edge effect was indicated. NESTED
ANOVA
OF MAJOR GROUPS
AND
COPEPOD
SPECIES
Mean densities of the major meiofauna groups (expressed - 10 cm-‘) encountered in the treatment and control sediments are presented in Fig. 2. Duncan’s multiple range test results (d.f. = 2, 18) are depicted by letters on top of the blocks such that means with the same letter(s) are not signiticantly different among treatments and/or controls within each date. In winter by 2 days or two tidal cycles after chamber placement, nematode densities in infaunally colonized chambers (i.e. “sides open” treatment) and suspension colonized chambers (i.e. “top open” treatment) were not significantly different, but both were significantly less than density in control sediments. After 29 days these trends remained unchanged. Copepod densities on Days 2 and 29 were not si~i~c~tly different in control sediments and opened-top chambers; however, density in open-sided chambers was significantly less for both collections. Naupliar density on Day 2 was significantly lower in open-sided chambers than in control sediments, but density in opened-top chambers was intermediate and not signilicantly different from the former two. By Day 29, naupliar density in opened-top chambers was significantly higher than in open-sided chambers, and was not significantly different from the control sediment density. In summer, 1 and 29 days after chamber placement, nematode densities in open-sided and opened-top chambers were not significantly different, but both were significantly less than the control density. Copepod and naupliar densities in opened-top chambers
G. THOMAS CHANDLER AND JOHN W. FLEEGER
I80
on day one were s~gn~c~tly higher than in open-sided chambers; but unlike Day 2 in winter, densities in opened-top chambers were significantly less than control densities. Therefore complete colonization by copepods probably occurs between one and two days. By Day 29, copepod densities in opened-top chambers and control sediments were not significantly different, but both were signifmtntly higher than in open-sided chambers. Simiiarly, nauphar density in open-sided chambers on Day 29 was sign& cantly less than in opened-top chambers, but control density was intermediate and not significantly different from either treatment. In the accessory treatments, nematode density in elevated chambers (x = 87.89, S, = 28.39) was not si~i~c~tly different from opened-top chambers (Fig. 2) but was
lO”,.lE
L
COiiiRbL
/
IS”,
/
-‘m-*
:“piq,v:l.l,l
I”,
ALTIIPTIPTN.Yrll”L”li
II
,,./
’ ‘~
,9.u CmmI.
.’
,,a
2C10FIilPrl rrv,~i,ni*,*.
,
‘-Tm.
IIJ’“” wPF*
iRill,*t*l:
Fig. 2. Mean densities of major meiofauna groups (expressed. 10 cm-“) for each treatment and sampling date: means sharing the same letter(s) across treatments are not si~i~cantly different; nested ANOVA and Duncan’s multiple range test; r = 0.05; d.f. = 2. 18.
significantly higher than in open-sided chambers. Nematode (x = 12.67, ST = 3.57) and naupliar (x = 8.85, S, = 3.56) densities in lid-covered chambers and open-sided chambers were not significantly different, therefore the short-term Nitex exclusion was effective. Copepod and naupliar densities (xcope = 37.81, S, = 8.59; ~__, = 50.08, S, = 4.74) in elevated chambers and opened-top chambers were not significantly different, indicating that colonization via suspension is equally as effective 12 cm above the interface as at 2 cm. Among individual copepod species, densities in the opened-top chambers were very similar to control levels, while densities in open-sided chambers tended to be depressed
MEIOFAUNAL
COLONIZATION
AND DISPERSAL
181
(Fig. 3). For winter samples, 2 days after chamber placement Parun~h~amptus colonizing opened-top chambers (Fig. 3). Higher densities were recorded in opened-top chambers on Days 2 and 29 than in control sediments or open-sided chambers for P. huntsmani. However, densities did not differ significantly. Pse~~stenheZiff wellsi was the most abundant harpacticoid in controls, and was the dominant species colonizing open-sided chambers on Day 2. Micruarthridion litturale was the dominant copepod in controls and open-top chambers on Day 29, however densities were significantly lower in open-sided chambers.
huntsmani was the dominant harpacticoid
ExPLAllrllTill
TREDTrnENIS
rxPmI#EWIRL
TRCRllEWTI
Fig. 3. Mean densities of major copepod species (expressed * 10 cmw2) for each treatment and sampling date: means sharing the same letter(s) across treatments are not significantly different; nested ANOVA and Duncan’s multiple range test; t( = 0.05; d.f. = 2, 18.
In summer, 1 day after chamber placement all copepod densities in the four chamber designs were significantly less than the control densities, except for the cyclopoid, Halicyclupsfosteri, which showed no difference among controls and experimental treatments. Copepod densities were significantly higher in opened-top chambers than in open-sided chambers for all species except H. fosteri. In elevated chambers, Paronychocamptus huntsmani@ = 1.89,5& = 0.5 1) was the only species with a density significantly different from (less than) that in opened-top chambers. Hulicyclups fisteti was the dominant colonizer on Day 1: control x = 9.25, S, = 1.58; open-sided x = 3.22, S, = 1.83; opened-top x = 14.08, S, = 6.01; elevated x = 15.69, S, = 6.87. After 29 days, Scottulana canadensis control density declined from the Day 1 level,
181
G. THOMAS CHANDLER
AND JOHN W. FLEEGER
but density in opened-top ch~bers increased and became si~i~c~t~y higher than in open-sided chambers (Fig. 3). Fse~dostenheIiu wellsi reached a density in opened-top chambers that was 15 times the Day 1 density and Feplaced Scottolana canadensis as the predominant species. Enhydrosoma wood&i was the only harpacticoid to reach equivalent densities in both the infauna@ colonized, open-sided chambers and the suspension colonized, opened-top chambers. PRINCIPAL
COMPONENTS
ORDINATION
OF COPEPOD
COMMUNITY
STRUCTURE
Principal components or~nation of the copepod collections (Fig. 4) shows the proximity (i.e. similarity) of suspension-colonized, infaunahy-colonized and natural communities in 3-vector, ordination space. The three axes account for 83.10, of the total variance: Axis 1 = 39.8%, Axis 2 = 26.8”,b, and Axis 3 = 16.5”,;. Generally, on every sampling date (except Summer: Day 29 open-sided chambers), ordination scores for treatments and controls on Axis 3 are equivalent (between - 0.3 and 0.4). Axis 1 scores separate the control and chamber communities into similardate groups, while Axis 2 scores separate the three communities within each date. For samples taken 2 days after chamber placement in winter, the copepod ordination scores for open-sided chambers and controls are almost identical on all three axes. The opened-top chamber community is clearly different, however, as the score on Axis 2 is 3 units from controls and open-sided chambers. After 29 days, the Axis 2 scores for open-sided chambers and controls are almost equal, but opened-top chamber scores are 2.2 units away. The overall ordination pattern for Day 29, however, shows general similarity among all three copepod communities. One day after placement in summer, total copepod densities in all chambers were depressed, and the community ordination scores for both chamber treatments are almost identical, but over 4 units from the control score on this date. After 29 days, ordination scores on Axis 1 are variable, ranging from 0.9 to 9.0. Axis 2 scores produce a pattern more consistant with Day 29 in winter: Scores for controls and open-sided chambers are similar (1.4 units apart), but opened-top chambers are over 4 units from the control. Significantly poor replicability among chambers may have caused the aberrant pattern on Axes I and 3. DISCUSSION
Our experiments have shown that copepod and nauphar colonization via suspended movement into azoic sediment chambers was extremely rapid, because densities reached ambient control levels after only 2 days (i.e. two tidal cycles). After only 1 day, densities in the suspension-colonized chambers were significantly higher than in chambers colonized exclusively by infaun~ ~mmi~at~on. Therefore copepods and nauplii more rapidly colonize defaunated sediments via suspended transport than by holobenthic, infaunal immigration. In contrast, nematode densities in suspension colonized (opened-
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top) and infaunally colonized (open-sided) chambers were not significantly different on any sample date. Densities in both chamber designs were, however, signiticantly less than control densities on all sampling dates, even after 29 days. Thus for nematodes, either dispersal mode, suspended or infaunal, is effective for dispersal and colonization over short distances, but complete colonization requires >29 days in this system. Several studies have investigated rates and extent of meiofaunal colonization of defaunated or azoic habitats. Sherman & Coull(l980) found almost complete colonization (i.e. predisturbance densities were reestablished) of a partially defaunated, intertidal mud-flat by copepods and nematodes after one tidal cycle (12 h), and suggested that suspended transport may have been the mechanism for colonization. Thistle (1980) also found rapid (< 24 h) colonization of defaunated enteropneust fecal mounds by subtidal harpacticoids. However, Alongi (1981) showed that in subtidally placed, azoic sediment trays, nematodes required 7 days to reach background densities while copepods took 5 days. Bell & Coen (1982) found that copepods and nauplii took from 1 to 5 days to colonize azoic Diopatra tube caps reimplanted in a sand flat, but they could not conclude which pathway was more efficient - infaunal or suspended. Contrasts in colonizing modes used by copepods and nematodes are probably caused by their different abilities to become suspended, and by differences in their vertical distribution in the sediment. Harpacticoid and epibenthic cyclopoid copepods have been captured while suspended in waters overlying a subtidal sand flat (e.g. Cyclopina sp. and Tisbe sp.; Alldredge & King, 1980) and an intertidal mud flat (e.g. Halicyclops coulli, Microarthridion littorale, and Enhydrosoma propinquum; Bell & Sherman, 1980) but few or no nematodes were found suspended at either site. Hagerman & Rieger (1981) found that not only harpacticoids but nematodes, polychaetes, kinorhynchs, turbellarians, gastrotichs, gnathostomulids, rotifers and halicarid mites occur regularly in the water column from 1 to 1.5 m above the sediment-water interface. Although meiofauna have been found in suspension a meter or more above the bottom, Sibert’s work (1981) suggests that meiofauna in the water column tend to behave demersally (sensu Alldredge & King, 1980), being most numerous just above the sediment-water interface: 5 cm above an unscoured, tidal channel bottom, nematodes were 2 to 5 times more abundant than at 30 cm, and harpacticoids averaged 7 to 12 times more abundant. Microarthridion littorale, the only copepod common to Sibert’s and our study, was 3 to 24 times more abundant at 5 cm. Palmer & Brandt (198 1) proposed that tidal currents suspended the meiofauna from intertidal sediments and caused copepod sediment densities to increase at slack high and low tide, when settlement occurs, but decrease during flooding and ebbing - periods of high resuspension. Little work has been conducted on meiofauna to determine if the mechanism of suspension is active, e.g. by swimming behavior, or passive, i.e. mediated by current flow. Many mud-dwelling harpacticoids and cyclopoids can swim, and suspension by active means is possible and likely. Nematodes, however, are usually thought of as non-swimming, but our results show that they were significantly more abundant in chambers elevated 12 cm into the water column than in infaunally colonized chambers
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after one day indicating considerable ability to become suspended. Literature reports of nematode dispersal by passive, suspended movement and the existence of an active swimming mode do exist. For example, the viviparous nematode, Anoplostoma viviparum, has a life history that minimizes the deleterious effects and maximizes the beneficial effects of water-borne dispersal. Gravid females buffer themselves from suspension by “gestating” in the deep anoxic layer; hatching juveniles then migrate to the flocculent, surface layer and are dispersed in suspension by water currents (Surey-Gent, 1981). Jensen (1981) showed that the phytal, epistrate-feeding nematode, Chromadorita tenuis, can rapidly swim (5 cm. s- ‘) from the benthos to submerged vegetation. A writhing or serpentine swimming behavior may insure that they remain in suspension long enough to be passively dispersed with currents, and for longer distances than swimming alone could achieve. In our study, > 95 y0 of the copepods and nauplii in control sediments were restricted to the oxidized, uppermost cm of sediment; whereas nematodes, although most abundant in the upper cm, occurred abundantly to 3 cm in depth. Copepods were thus more nearly complete colonizers of the opened-top chambers than were the nematodes, and probably because of (a) a surticial distribution that enhances the probability of passive suspension from current action, etc., and limits the possible pathways for infaunal movement, (b) better swimming ability, and (c) easier suspension due to a larger body volume with many setose appendages. The combination of high densities (436 to 3696 . 10 cme2) in the flocculent, easily suspended, surface sediments with considerable numbers in deeper sediments (461 to 2159. 10 cm-‘) enabled the nematodes to colonize the azoic sediment equally well via suspended transport or infaunal immigration. Surficial meiofauna may have been suspended by current scouring, macrofaunal activities (e.g. feeding, burrowing, swimming, etc.), and/or active swimming and then swept into the opened-top chambers by water movement, but deeper occurring individuals would escape suspension. With deeper sediment distribution, the nematodes are exposed to more avenues of infaunal movement than the shallow-occurring copepods and thus were better colonizers of the open-sided chambers. However, the open-sided chambers with side openings 0.5 cm below the sediment surface (Fig. 1) may have biased our copepod results by precluding colonization of species with biologies restricting them to the hyper- or epibenthos (e.g. Scottolana canadensis). Nonetheless copepods colonize so effectively by suspended movement that by comparison infaunal crawling is undoubtedly much less important to dispersal in muddy habitats. Among the individual copepod species in our study, those species that were predominant in control sediments generally predominated in opened-top sediment chambers by 2 days. Passive suspension of the copepod community from control sediments may have resulted in an in toto transport of all species from the control areas into the opened-top chambers. However, only if passive suspension afFected every species uniformly would the community formed from subsequent random settlement have a structure similar to control sediments. Active movement by some meiofauna into the water column or chambers would tend to alter, i.e. weight, the relative densities of the immigrating species
MEIOFAUNAL
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AND DISPERSAL
expected from passive suspension and random resettlement. Non-uniform suspension of individuals with morphologies or behaviors capable of enhancing (e.g. setose forms) or avoiding (e.g. burrowers) suspending influences would have the same effect. Although relative densities of most species in opened-top chambers approximate the control heirarchy found on Days 2 and 29 in winter and Day 29 in summer, principal components ordination shows that the chamber community structure is different. Species associations upon initial settlement are probably not a result of entirely random, passive processes. Based on differences in swimming abilities alone, some species would be expected to colonize the opened-top chambers more effkiently. Active immigrants may have caused a change in the control-like community structure expected from uniform suspension and random resettlement because of their weighting influence on relative densities. Our evidence suggests that opened-top chamber community structure was influenced by protracted immigration and emigration of individuals throughout the study period. Open-sided chamber communities on Days 2 and 29 in winter and Day 29 in summer were nearest to the control community in ordination space (Fig. 4). Open-sided chambers provided direct, lateral access to copepods burrowing infaunally from PRINCIPAL
AXIS
Ill
-S-
Fig. 4. Principal components ordination of copepod communities across dates Day 2 control; 2, winter: Day 2 open-top; 3, winter: Day 2 open-sides; 4, winter: Day 29 open-top; 6, winter: Day 29 open-sides; 7, summer: Day 1 control; 8, 9, summer: Day 1 open-sides; 10, summer: Day 29 control; 11, summer: Day Day 29 open-sides.
-9
and treatments: 1, winter: Day 29 control; 5, winter: summer: Day 1 open-top; 29 open-top; 12, summer:
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adjacent control sediments. Therefore the resulting community structure was more similar to controls even though densities were uniformly depressed (Fig. 3) among species. Colonization seemed to be characterized subsurface open sides by all of the mud-dwelling Individual copepod species showed differential
by random, species. colonization
Day 2 of colonization, the predominant harpacticoid stenheliu wellsi, did not colonize opened-top chambers
active encounter responses.
of the
In winter on
in control sediments, Pseudoas densely as the less abundant
Paronychocamptus huntsmani (see Fig. 3), indicating either active immigration by the latter or active chamber avoidance by the former. P. weffsimay be an efficient burrower as it showed a significantly higher density than any other species in the infaunally colonized chambers on this date. After 29 days, densities of Microarthridion littorale increased dramatically, while densities of Pseudostenheliu wellsiwere depressed in both chamber treatments. In summer, control densities of Microarthridion littorule were low (2 = 2.00. 10 cm-‘), and Pseudostenhelia wellsi and Puronychocamptus huntsmuni reached equivalent densities in both chambers after 1 day. After 29 days in the opened-top chambers, Pseudostenhelia wellsiincreased to a significantly higher density than Paronychocamptus huntsmani and control levels; possibly indicating a faster colonization rate, higher reproductive output, better ability to avoid passive emigration, better competitive abilities and/or better ability to avoid predators - none of which could be tested by our design. The second most abundant species, Scott&mu cunadensis. is an epibenthic, albeit photonegative, species (Harris, 1977) with abundant planktonic nauplii (Heinle, 1969). Therefore, not surprisingly, S. cunadensis was predominantly a suspension colonizer reaching a density of 48 . 10 cm ’ in opened-top chambers by Day 29, but found at ~3. 10 cm ’ in infaunally colonized chambers on all sampling dates. In contrast, Halicyclopsfosteri, an epibenthic but also planktonic (Lindsay, 1974; Aurand & Daiber. 1979) copepod was the only species to reach densities in all chamber treatments equivalent to control levels after 1 day, indicating considerable capability for burrowing as well as swimming. Enh_vdrosomawondinialso immigrated equally well via infaunal or suspended movement, as densities in opened-top and opensided chambers were equal and not significantly different from controls by Day 29 in summer. This species was often found from O-3 cm depth and thus would be expected to utilize either and ecologically colonizing pathway. Enhydrosoma propinquum, ;1 morphologicallysimilar species had been considered a strictly burrowing species until Bell & Sherman (I 980) found it suspended in overlying waters. E. woodini seems to behave in a similar Way.
Large-scale defaunations of meiobenthic communities (eg. Coull, 1969) recover more slowly than small-scale disturbances. The greater distance between potential colonizers and the epicenter of a large scale disturbance is more diEcult to traverse because meiofauna generally lack pelagic larvae. However active or passive suspension of meiofauna would probably increase recolonization rates and be faster than infaunal immigration over the large scale. Small-scale defaunations are less likely to undergo the
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successional changes in predominant species or species guilds suggested by Grassle & Sanders (1973), as immigration distance is short and suspended transport effects rapid community restoration (2 days for copepods in our system). Successional changes in the meiofaunal communities colonizing large-scale defaunations need to be studied, and the structuring influences of species interactions on developing communities need to be determined. In muddy-bottoms, suspending influences (e.g. current scouring, macrofaunal feeding and locomotory movements, active emergence into overlying waters, etc.) generate a mobile meiofaunal community, and may be equally or more important than biotic interactions in structuring the community in space.
ACKNOWLEDGEMENTS
Special thanks to the Louisiana Universities Marine Consortium (LUMCON) and its director, D. F. Boesch, for the abundant facilities and equipment support. Thanks also to Y. Ledoux for assistance in graphics, G. R. Fitzhugh for field work, T. C. Shirley and D. W. Garton for computer programming, and D. F. Boesch, W. B. Stickle and W. J. Harman for reviewing an earlier manuscript. This research was part of an MS. thesis by G.T. Chandler at Louisiana State University.
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