Meiofauna meso-scale variability in two estuarine habitats

Estuarine,

Coastal

and Shelf

Science

(1985) 21,745-756

Meiofauna Estuarine

Meso-scale Habitats

F. E. Phillips

and J. W. Fleeger

Department Rouge, LA Received

of Zoology and Physiology, 70803, U.S.A.

25 July

Keywords:

Variability

1984 and in revised

spatial variations;

Louisiana

form

State

19 December

meiobenthos;

in Two

University,

Baton

1984

estuaries; mudflats

Spatial and temporal variations in meiofauna abundances were measured for 13 months within two estuarine habitats, an intertidal mudflat and a small, usually subtidal pond. Three locales within each habitat were sampled monthly (nine replicate cores per habitat) to quantify nematode and copepod species withinhabitat, meso-scale (m-km) variation. Significant levels of variation were found between habitats (all taxa tested), among locales within habitats (all taxa except the harpacticoid species Microarthridion littorale) and among months. The magnitude of variation differed greatly within the two habitats. Species with marsh affinities predominated in two of the three mudflat locales, while the third locale was predominated by subtidal species. This within-habitat heterogeneity was related to the proximity to the marsh and/or to the position on an exposure gradient. Although significant meso-scale variability was also found in the pond, species responses were more individualistic suggesting that physical

gradientswere not as influential. These data indicate that meso-scalevariability should be considered when planning long-term investigations to assure that the study is representative subsequentecological inferences are valid.

or baseline meiofauna of the habitat and that

Introduction

The traditional approach to the study of communities in estuaries is to examine differences in fauna1 compositions or population dynamics along physical gradients. Daiber (1982) lists numerous estuarine zonation patterns for a variety of animals acrosssalinity and exposure gradients or habitat types. Several examples of meiofauna zonation exist. For harpacticoid copepods, Barnett (1968) found zonation within a mudflat, Coull et al. (1979) identified species-specific habitat patterns on an intertidal-subtidal transect, and Harris (1972) found horizontal patchiness in an intertidal beach. Feller (1980) and Palmer (1980) have discovered differences in life history characteristics of given species between nearby but similar habitats. Findlay (1981) has suggestedthat such meso-scale (m-km) variations are due to differences in physical factors. Given the small size of meiofauna, they are especially susceptible to frequent and extensive within-habitat physical variability. Therefore, meso-scale variability in physically disturbed habitats should occur frequently. 745 1)272-771~~85~110745+12$03.00,'0

0 1985 Academic Press Inc. (London! Limited

746

F. E. Phillips &J. W. Fleeger

Recent trends show that the majority of meiofauna studies in estuaries concentrate sampling over many weeks or months at single, arbitrarily chosen locations within a habitat (Cot111 & Fleeger, 1977; Bell, 1979,198O; Houge, 1978; Fleeger, 1979,198O). The rationale for this approach is to permit one to take a large number of subsamples from a defined location to reduce to an acceptable level the sampling error caused by small-scale variability (see Findlay, 1982; Green, 1979). Invalid inferences may be made unless this single station is representative of the habitat. Repeated collections may not always resample the exact same location or the arbitrary location may change compared to its surroundings if micro-environmental or -physical factors vary. In fact, what is assumed to be temporal variation at one site may actually be a manifestation of even a moderate degree of meso-scale, within-habitat variation. Only sampling designs which replicate locations within habitats can separate temporal from spatial and between-habitat from within-habitat variability (see Hurlbert, 1984). Relatively little is known of meiofauna within-habitat, meso-scale variability in estuarines. Until more is known, possibly significant variations within habitat types should be considered when planning long-term studies and pollution baselines. If a single arbitrary site cannot serve as an adequate representative of a habitat, a more complex design must be chosen. The purpose of this study was to determine the levels of meso-scale variation in two estuarine habitats in Louisiana using a design with replicate locations as well as samples within each habitat. Methods The study area is located in Terrebonne Parish, near Cocodrie, Louisiana (29” 15’N; 91” 21’W) and is characterized by extensive stands of Spartina alterniflora Loisel. Water movement is largely wind-dominated with small diurnal tidal amplitudes (0.3 m) and wide salinity fluctuations (2-26 ppt). Two nearby sampling sites, representing two habitats, a shallow pond and a frequently exposed mudflat, were located along Bayou Sale. Within each site, three locales, approximately 05 m2 in area, were randomly chosen to determine the extent of spatial variability. Each locale was monitored monthly for trends in meiofauna density, species composition and community dynamics. The pond site (25 x 15 m) is a protected, shallow enclosure (0.5 m in depth) surrounded by S. alterni’ora (see Chandler & Fleeger, 1983). A small, slow creek, visible along one side of the pond at low tide, feeds and drains the pond. Sediments are largely silt-clay with an RPD at l-3 cm. Of the three locales, two are situated approximately 5 m from the edge towards the centre of the pond. The third locale is situated along the side of the small creek near the outlet (or inlet) of the pond. The pond is rarely air exposed except during the winter when north winds lower the water level in the estuary. Sediment disturbances from boats do not occur because no small boats enter this restricted area. The mudflat site (20 x 4 m) is an intertidal area between the S. aZtern$ora marsh and a frequently travelled bayou, and is commonly exposed to disturbances such as boat wakes. Sediments are sandier than the pond with an RPD of l-3 cm. During the winter months the mudflat is regularly air exposed and becomes covered by a lush algal mat (Cladophora sp.). In the spring fiddler crabs actively rework the sediment as the algal mat disappears. Locale 1 is situated at the end of the mudflat close to the edge but near ( < 1 m) the marsh. Locale 2 abutted directly on the marsh, and locale 3 was situated 4 m

Meiofauna

rneso-scale

variation

747

from S. alterni’ora plants. Locale 3 was the least protected from boat wakes, and the most subtidal. Three replicate cores were taken at each locale monthly for 13 consecutive months, using modified Xl-cm3 syringes (inner diameter 2.7 cm). Cores were taken to a depth of 6 cm, and were immediately frozen in liquid nitrogen to preserve the substrate surface. The upper 4 cm were retained in 2-cm intervals, preserved in lo”,, formalin, and stained with rose bengal. Two methods were used to extract the meiofauna from the sediment. A density gradient centrifugation technique using Ludox (following Fleeger & Chandler, 1983) extracted both copepods and nematodes with high efficiencies (greater than 90”,, ). However, Ludox supplies were limited and were exhausted quickly. The majority of the sediment samples were separated on two sieves, a 500 and a 63 pm. Macrofauna were retained on the 500~urn sieve and examined. The sediment portion of the 63-pm sieve solution which served to was soaked for 10 min in 10” (, sodium hexametaphosphate dissociate clay aggregates. Sediment was then placed in a sonicator which further broke apart sediment particles using sound waves (Thiel et al., 1975). All meiofauna were enumerated to major taxon; copepods were identified to species. Males, females, gravid females, and copepodites were tallied for each species. The number of nematodes were either determined by direct count or by a subsampling technique similar to that of Sherman et al. (1984). A three-way multiple analysis of variance (MANOVA) was chosen to analyse copepod abundance patterns. MANOVA tested for variation in densities (using the eight most abundant copepod species as dependent variables) among all dates, sites and locales. If this test is significant then one can be assured that at least one of the eight mean densities of dependent taxa is significantly different. With this assurance, univariate three-way ANOVAs were conducted to test spatial (between sites and among locales) and temporal variation for individual species if MANOVA was significant. These same ANOVAs were conducted on nematodes, total copepods and total meiofauna. Scheffe’s multiple comparison test was used with all ANOVAs to compare individual differences in mean densities across sites, dates or locales. All analyses were conducted by SAS GLM (SAS Institute, Inc., 1982). Detrended correspondence analysis (as recommended by Gauch, 1983) was used as a method of ordination to investigate patterns in community variation by the DECORANA computer program (Hill, 1979). This ordination describes spatial or temporal patterns in communities by using shared species compositions. A multidimensional coordinate system is created which locates various entities (in this case locale or date collections) and describes their relationship to one another. Ordination was conducted to describe seasonal and spatial variability at the locale level (each locale-date combination was analysed at each site, 39 entities). Spatial variability among sites was also examined using ordination by disregarding locales and grouping dates and sites together (26 entities). Results Nematodes (comprising 899, of the total meiofauna), and copepods (lo”,,) were the most abundant groups. A total of 11 harpaticoid and one cyclopoid copepod species were identified. While predominant species differed at each site, all 12 species were found at some time at both sites. Total numbers of copepods, adults and copepodites combined

748

F. E. Phillips& J. W. Fleeger

5500 (a) 5000

-

1 1 1 1 01 OMAMJJASONDJFMZ

1

1

1

I

I

I

I

I

I

OMAMJJASONDJFM2 Months

Figure 1. Density (per 10 cm’) of (a) nematodes at the pond and mudllat sites (averaged across three locales at each site) and (b) copepods (adults and copepodites combined) sampled each month from March 1982-March 1983 (M2). Solid line=pond; dashed line = mudflat.

per month, ranged from 87435 per 10 cm2 on the mudflat to 53-307 per 10 cm2 in the pond (Figure 1). Generally, total copepod densities were lower in the summer months of June-August while peak densities occurred in the first spring on the mudflat and the second spring in the pond. Certain copepods dominated the seasonal density patterns at each site. Nannopus palustris Brady, with a spring reproductive burst, reached its highest density of 407 per 10 cm’ in the first March on the mudllat. Low densities, with no noticeable reproductive activity, followed through the fall and winter, but by the second March, higher numbers returned. Some speciesdisplayed sporadic, unpredictable densities while being present and reproducing year round. Scottolana canadensis (Wiley), with density peaks in January, February, and the second March, and Pseudostenheliawellsi Coull and Fleeger, with highs from May to July and September to November, were the most abundant speciesin the pond. S. canadensisand Cletocamptus deitersi (Richard) exhibited their

Meiofauna

mesa-scale variation

Species

Figure Means

2. Density of most abundant copepod species at the mudflat and pond are per 10 cm2 across three locales at each site. I, mudflat; , pond

sites.

1. Mean values and a summary of Schetfe’s multiple comparison test over all and locales for the most abundant copepod species, total copepods, nematodes, and total meiofauna. Means are densities per 10 cm’. Means with the same letter in each row are not significantly different from each other TABLE

dates

‘I‘axon I’. S. ‘M. H. C. E. P. N.

milsi L~anadensu littorale mulli detterst woodini huntsmani pulustris

Nematodes Copepods Meiofauna

Pond 25.5 ‘2.6

5.1 4.7 2.8 3.4

16.6 0.02

661.8 83.8 743-O

A A A A B B A B B B B

Mudflat 3.8 B 15.1 B 3.5 B 0.9 B 14.8 A

9.8 A 55B 52.9 A 950.1 A 107-2 A 1057.0 A

highest mudflat densities in July (Figure 2). C. deitersi remained very abundant from July to November and was present in fairly constant densities at other times. S. iunadensis was somewhat more variable as it dropped to very low numbers in March, August and November. Statistical analysis of the three core replicates from each locale was conducted on the most abundant copepods species, Pseudostenhelia wellsi, Scottolana canadensis, Microarthridion littorale, Halicyclops coulli, Cletocamptus deitersi, Enhydrosoma woodini, Paronychocamptus huntsmani (Wiley), and Nannopus palustris. A three-way MANOVA grouped all major copepod species and indicated significant variation (P = 0.0001 I in densities among dates, sites, locales and each of the interactions. Univariate three-way ANOVAs were conducted to test for differences in densities of each of the major copepod species, nematodes, copepods and meiofauna among dates, sites, locales and the various interactions between these three. All copepod species showed significant date, site and locale variation except M. littorale among locales and H. coulli for date-by-locale, site-by-locale and date-by-site-by-locale interactions. Scheffe’s multiple comparison test compared densities between the two sites (Table 1 j and indicated significantly higher numbers in the pond for P. wellsi, S. canadensis, M. iittorale, P. huntsmani and H. coulti. On the mudflat significantly higher densities of (1. deitersi, E. woodini and N. palustris were found. Nematodes, total copepods and total meiofauna were significantly more abundant at the mudflat.

750

F. E. Phillips & J. W. Fleeger

TABLE 2. Mean values and a summary of Scheffe’s test for differences among locales over all dates. Means are densities per 10 cm’. Meansin eachrow with thesame lener are not significantly different from each other Taxon

Pond

P. wellsi

19.8 B 20.1 AB 6.1 A 4.0 AB 1.4 B 2.0 B 0.03 B 15.1 AB 71.1 BC 674.1 B 743.2 B

S. canadensis M. littorale H. coulli C. deitersi E. woodini N. palustris P. huntsmani Copepods Nematodes Meiofauna

1

Pond 2

Pond 3

24.9 AB 11.9 B 2.6 A 6.2 A 2.9 B 1.7 B 0 B 10.3 B 62.9 C 716.2 B 776.9 B

31.7 A 35.7 A 6.5 A 3.9 AB 4.2 B 7.0 B 0.03 B 24.4 A 116.8 B 595.1 B 708.9 B

Mudflat 2.3 C 8.5 B 2.2 A 0.6 B 9.0 B 5.7 B 43.6 B 5.0 B 77.4 BC 885.8 AB 963.0 AB

1 Mudflat 1.5 C 12.9 B 6.8 A 1.6 B 32.5 A 16.6 A 98.2 A 5.5 B 176.6 A 1224.7 A 1401.0 A

2 Mudflat

3

7.7 C 23.8 Al.3 1.6 A 0.6 B 2.8 B 7.0 B 16.7 B 5.9 B 67.6 BC 739.8 B 807.0 B

Scheffe’s test also compared variation in density of the major copepod speciesamong locales(Table 2). Only M. littorale exhibited no significant differences in densities across all six locales of the pond and mudflat. E. woodini, C. deitersi and N. palustris were highest at the second locale on the mudflat. Nematodes and total meiofauna were significantly higher at the first two locales on the mudflat. Total copepod numbers were significantly higher at the second locale on the mudflat. No clear patterns were indicated for speciespreference of a locale in the pond. Detrended correspondence analysis was conducted to investigate patterns in community dynamics. Two formats were used: one analysis grouped dates and sites (26 entities) by species(Figure 3), while the second analysis grouped the locales and dates of a site (39 entities) by species(Figures 4 and 5). In each caseonly axes 1 and 2 were used due to the low eigenvalues of additional axes. Axes 1 and 2 combined always accounted for greater than 70% of the variation. The units on each axis represent standard deviations of speciesturnover. A standard deviation of 1 represents a 50% change in species composition. In addition a specieswill rise to its mode and disappear in about 4,standard deviations (Gauch, 1982). The ordination of sites and months by species shows some distinctive groupings between mudflat and pond sites (Figure 3). Axis 1 represents 0.26 standard deviations. This small value indicates that little variability can be placed on groupings along this axis, asall entities are quite similar. Axis 2 extends to 2.8 standard deviations indicating a large community change. Entities along this axis are clearly separated into pond and mudflat community assemblages. The ordination of locales and months showed different spatial and seasonalcommunity patterns for the two sites. For the mudflat (Figure 4), locale 3 collections, at the outer edge of the mudflat, were tightly grouped indicating a relative lack of seasonality

Meiofauna

meso-scale

variation

751

,o-

3

MRI *

Mudflat

i1P 2 .5 - * MY *

AG +

N ‘z ;I

MR2 *

JL *

2 ODC s FB

NV

*

* J* *

I .5 -

SP *

oi *

JN *

Pond 1,oAP *

DC *

MR2 x

MRI *

FB “,” *

NV *

05 JL * * 0.

bz &X

I

I O-05

Figure 3. Ordination site. MRl and MR2

I o-10

MY * JN *, 0.15

OT *

0.20

I 0.25

SP +

1: 32

of dates and sites by species. Each point designates refer to the fist and second March, consecutively.

a month

and a

'r

0.0

O-5

I.0

I.5

2.0

25

Axis I

Figure 4. Ordination of dates and locales at the mudflat sampling site. Months are listed with each of the three locales. When two numbers are present, the first designates the locale and the second refers to the first or second year.

752

F. E. Phillips &J.

W. Fleeget

--------I

Axis

I

Figure 5. Ordination of dates and locales at the pond sampling with each of the three locales. When two numbers are present, locale and the second refers to the first or second year.

site. Months are listed the first designates the

and high similarity of all collections from this locale. Locales 1 and 2 were mixed in their placement at the opposite end of axis 1 showing greater heterogeneity over time. Axis 1 ranged from 0 to 2.6 standard deviations indicating that locale 3 was substantially different from locales 1 and 2. Seasonalgroupings were not as clear as spatial clusters. All three locales for the first March were very close to locales 1 and 2 of April, May and the second March. A fall grouping also appeared which contained locales 1 and 2 of August, September, October, November and December. In contrast to the mudflat ordinations, locale collections within the pond showed little similarity to each other through space and time with no clear seasonalor spatial groupings (Figure 5). Here, axis 1 represented 1.3 standard deviations which was half that of the mudflat ordination. Discussion Meiofauna spatial and temporal variability occurred at all levels examined in these estuarine habitats. In no instance, however, was within-habitat variability so great that between-habitat differences or temporal variation could not be detected. All major taxa and all copepod speciesdiffered in density between the mudflat and pond sites(Table l), and ordination clearly distinguished mudflat and pond assemblages(Figure 3). Such between-habitat variability is not uncommon to meiofauna (see Barnett, 1968; Bell, 1979; Fleeger, 1980), and our results for harpacticoid copepods parallel the zonation pattern of Coull et al. (1979). Especially in agreement with the Atlantic coast zonation were Nannopus palustris, always found in highest densities in close proximity to Spartina, and Scottolana canadensis which preferred the more subtidal habitats. Differences existed in species composition (Cletocamptus deitersi is not reported from the Atlantic coast; Paronychocamptus wilsoni is not reported from the Gulf of Mexico) and in the speciesutilization of the gradient. In South Carolina, Pseudostenhelia wellsi is found only in the intertidal, low marsh environment, but in Louisiana its highest abundances are at the more subtidal stations. Chandler and Fleeger (1984) report that P. wellsi dwells in delicate, mucus tubes, and sediment type or hydrodynamic energy, which both differ between coastlines, may determine its optimal environment. Nevertheless, within-habitat variation (among locales) was significant for all taxa tested except Microarthridion littorale. This added variation associatedwith locales was

Meiofauna

meso-scale

variation

753

qualitatively different at the mudflat and the pond. At the mudflat a distinct pattern emerged. Locale 2, close to the marsh, was consistently higher in nematode numbers and in copepod densities for those species with marsh affinities (i.e. N. palustris, C. deitersi and Enhydrosoma woodiniseeFleeger & Chandler, 1983). Ordination, however, shows a recognizable copepod assemblageat the most subtidal site, locale 3 (Figure 4), and a mixture of seasonalgroupings from the faunistically similar locales 1 and 2 (both close to the marsh). This separation was due to the distribution of the four most abundant species. Species with subtidal affinities, S. canadensis and P. wellsi, experienced the majority of their highest densities at locale 3; C. deitersi and N. palustris had seasonal peaks at locales 1 and 2 but consistently low densities at locale 3. These patterns appear to be consistent and are probably related to physical gradients such as proximity ( < 0.5 m for locales 1 and 2) to Spar&a (root matter has been found to affect copepod and nematode densities Bell et al., 1978; Osenga & Coull, 1983) or position on the exposure gradient. Although significant levels of heterogeneity were also found for pond taxa, differences among the locales were not as striking nor were spatial patterns consistent as at the mudflat. P. huntsmani and S. canadensis both exhibited significantly more individuals at locale 3, nearest to the inlet/outlet channel, but nematode numbers did not vary among the locales. Also, ordination does not readily identify spatial patterns (Figure 5) and when the mudflat and pond ordinations are compared, the overall variation among pond collections was about half that of the mudflat. Seasonalgroupings of localeswere inconsistent. Therefore, while variability was great within the pond, no clear patterns related to physical gradients emerged. In the absence of physical gradients, the sources or controls over among-locale variation in the pond are unknown. Several factors, e.g. competition or predation, are thought to bring about small-scalepatchiness (Findlay, 1981) but should not be effective over metre scaledistances. Biogenic structures (Thistle, 1980; Bell & Coen, 1982) affect distributions, but no large macrofauna structures or emergent vegetation are present in the pond. The distribution of food supplies may causevariability (Lee et al., 1977; Gray, 1968), however, the pond displayed no isolated patches of algae or bacteria. Tidalinduced variation should be considered in the flocculent pond sediments, however. Tidal movement has been related to suspensionof meiofauna into the water column (Palmer & Brandt, Fleeger et al., 1984). Movement into the water column may be active or passive and not all taxa are affected equally (seePalmer, 1984). Either entrainment or settlement could cause large-scale differential aggregations as seenin the pond (see Eckman, 1983; Jumars & Nowell, 1984). Entrainment may vary spatially depending on current velocity or direction. Settlement patterns may vary with wind speedor duration. In a relatively homogeneous physical environment such as the pond, meiofauna presumably survive equally well at any locale. Conversely, tidal currents may diminish heterogeneity and control the level of meso-scale variability by dispersing fauna aggregated from such intrinsic processes as reproduction (Heip, 1975). Before meso-scale variability in a homogeneous environment like the pond can be predicted, further work is needed to determine the causesof small-scale patterns and the effects of tidal movement on the meiofauna. Temporal variation was identifiable for all taxa at both sites. Nannopus palustris was the only speciesto display a predictable pattern based on literature reports. Densities bloomed in the spring, and no ovigerous females were found after May. Spring reproductive bursts of this species have been well documented as a consistent temporal

754

F. E. Phillips

&

3.

W. Fleeger

pattern in estuaries (Bodin, 1972; Brickman, 1972; Fleeger, 1980; Fleeger & Chandler, 1983). All other species lacked distinct reproductive cycles, as several reproduced sporadically and had more than one seasonal abundance peak. Similar observations of variable, year-to-year reproductive success have been noted by Palmer (1980) and Bell (1979). Two conclusions are clear from this study. Meiofauna vary in time and at a variety of spatial scales, and these variabilities are not equivalent in the two habitats studied. Replication of locales in this experimental design made it possible to separate adequately temporal from spatial variations. The significant additional variance associated with locales at both sites of this study indicates that data from any single locale over a long period of time must be limited in scope and interpretation (see also Hurlbert, 1984). Apparent temporal variation may be due to unpredictably changing meso-scale variability or to error associated with repeated sampling at slightly different locations. Longterm data sets may have unexplained variance components, and baseline studies for pollution may be more variable than needed, making it more difficult to identify a pollution effect. If meso-scale variation can be quantified, conclusions concerning long-term cycles and pollution studies will be less open to question. The fact that different scales of variation were identified at the pond and mudflat sites suggests that preliminary sampling programmes, as recommended by Green (1979), should be followed when establishing a meiofauna sampling programme in an unknown environment. It also suggests that sampling designs be tailored to the question being asked. If species composition and long-term population cycles are of interest (e.g. Coull & Fleeger, 1977), at least two sites may be needed in a habitat with distinct physical gradients (e.g. the mudflat of this study). A choice of only one of the three locales would have reduced the observed number of species and changed the conclusions about seasonality and community dynamics on the mudflat. In pond studies, the best approach may be to spread a given number of cores over a large area because no clear pattern of heterogeneity was related to the physical environment. For studies involving field experiments, knowledge of meso-scale variability is equally important (Hurlbert, 1984). The levels found here at both sites suggest that controls for each experimental treatment replicate should be used and that controls and treatments be interspersed within a small area. If controls are grouped in one area and experimentals in another, these areas may not be faunistically equivalent. Replication in more than one locale may also benefit studies of small-scale patterns (Findlay, 1982; Heip, 1975) since unique patterns and spurious conclusions may result largely from meso-scale variation. Acknowledgements We extend our thanks to the Louisiana Universities Marine Consortium (LUMCON) for the unlimited use of their facilities, boats and equipment. Thanks also to G. T. Chandler and A. W. Decho for discussion, critical review of the manuscript, and fieldwork. This research was part of an M.S. thesis by F. E. Phillips at Louisiana State University. References Bamett, P. R. 0. 1968 Distribution and ecology of harpacticoid nationale Revue der Gesamten Hydrobiologie, 53,177-209. Bell, S. S. 1979 Short- and long-term variation in a high marsh Marine Science, 9,331-350.

copepods meiofauna

of an intertidal community.

mudlk.

Znter-

Estuarine

Coastal

Meiojauna

Bell,

meso-scale

variation

555

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