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Sand-dollar mellita quinquiesperforata (Leske) burrow trails: sites of harpacticoid disturbance and nematode attraction
J. Exp. Mar. EM &A.,
1989, Vol. 130, pp. 223-235
223
Elsevier
JEMBE 01300
Sand-dollar Mel&z quinquiesperforuta(Leske) burrow trails: sites of harpacticoid disturbance and nematode attraction Jeffrey A. R~~d~na~er ~e~~rt~z~nt of Oce~n~~phy,
Florida S#ate ~niver~ty, ~aliah~~ee, ~~~r~d~,U.S.A.
(Received 1 March 1989; revision received 5 May 1989; accepted 14 &me 1989) Abstract: The effect of sand-dollar MeZEtaq~jnqu~e~pe~rut~ (Leske) burrowing on a soft-bottom meiofauna community was examined at a subtidal site located off the northwest Florida coast. M. quinquiesperjbruta were common at the site with an average of 3 ind .0.25m __2 and their burrow trails were a distinctive feature of the sediment surface. At the site, sand dollars disrupted z 14% of the sediment surface. h _ ‘, Sand-dollar burrowing did not decrease total meiofauna abundances significantly (P > 0.05); however, the abundances of one harpacticoid species, Halectinosoma sp., foraminifera and mites were significantly lower (P < 0.05) in sampies collected from a burrow trail than in samples collected in front of the sand dollar. The lower abundances o~~alectinoso~a sp. and mites in the burrow trail were probably due to sediment disturbance. The lower abundances of foraminifera in the burrow trails were probably due to sand-dollar predation. In contrast to studies in intertidal areas, total nematode abundances were si~ific~tly higher (P -C 0.05) in the samples collected behind a moving sand dollar than in samples collected in front of the sand dollar. Possible reasons for the enhanced abundances are: (1) increased food availability in the form of mucus and/or excreted cells &at line the sand-dollar gut; and (2)increased pore space within the sediment.
Key words: Disturbance; Harpacticoid; Meiofauna; Nematode; Sand dollar; Sediment disturbance
In soft-bottom marine habitats, disturbances are often recognizable as visibfe disrupon the sediment surface. For example, ray feeding pits (Reidenauer & Thistle, 1981; VanBl~com, 1982; Grant, 1983), horseshoe crab trails (Woodin, 1981; Botton, 1984) and gastropod trails (Rhoads, 1967; W&se, 1980) are documented sites of disturbance to soft-bottom benthic communities. As disturbances are dissimilar in size and appearance, they are also different in their initial postdisturb~~~ conditions. The effects of natural disturbances may vary from complete removal of the resident fauna and creation of an azoic patch (i.e., disaster and catastrophe) to reductions in species numbers and densities within the disturbed patch. Many biologically produced disturbances are important in determining macrofaunal community structure (Woodin, 1978; Zajac & Whitlatch, 1982; Oliver et a!., 1985) and tions
Correspondence 36633. U.S.A.
address: J.A. Reidenauer, BCM Converse inc., IO8 St. Anthony Street, Mobile, AL
0022-098i/89/$O3.50 0 1989 Elsevier Science Publishers B.V. (Biom~dic~ Division)
224
J.A. REIDENAUER
are critical in the life history of individual macrofaunal species (e.g., ~phipods VanRlaricom, 1982; bivalves - W&se, 1980; and, polychaetes - Levin, 1984). In contrast, the effects of disturbance on the meiofauna are not well established. Only a limited number of field experiments have investigated the effect of biologically produced natural disturbances on meiofauna (Coull & Palmer, 1984). The results of these studies document a variety of effects. In some cases, catastrophic removal of the community occurs such as when rays excavate meiofauna along with the sediment in their search for deep-living prey (Reidenauer & Thistle, 1981; Sherman et al., 1983) and when entropneusts ingest sediment and defecate material upon the sediment surface (Thistle, 1980). In contrast, sand-dollar burrow trails represent a category of s~dimcnt disturbances that are ~o~catastrophjc to the overah meiofauna community but nonetheless have species-specific effects. Two previous investigations have examined the effects of sand-do&r Mel&z q~j~q~je~~e~~u~u (Leske) bu~owing on intertidal meiofaunal communities : (I) at Alligator Point, Florida (Findlay & White, 19831, and (2) at North Inlet, South Carolina (Creed & Coull, 1984). Each study concluded that the dist~b~ce generated by the sand dollars were generally noncatastrophic to the resident meiofaun~ comm~ity. Nonetheless, both investigations documented reductions in specific meiofauna taxa while other taxa were unaffected. Given iM. ~~~~~~e~~~r~~~‘s abundance and potentid importance in subtidaf regions, it is appropriate to test the conclusions reached by the intertidal investigators in a subtidal cnv~onment. To that end, a field experiment was conducted at a subtidal site in St George Sound, Florida, where M. qu~~q~~espe~rur~ were common. To facilitate comparisons, the sampling strategy was similar to the one utilized in the intertidal studies. MATERIALS AND METHODS LOCALITY The study site was located at adepth of 5 m on an unvegetated sand-flat x 7 km south of Turkey Point, Florida, in St George Sound (29”5I’N, 84”3I’W) (Fig. I). Bottom salinity was 307& and median grain size of the sediment was 0.254 mm. The site was protected from strong storm swells by Dog Island Reef, a submerged barrier island located % 0.7 km to the south of the site. The area was characterized by a persistent and tempor~Iy dense iM. q~~~q~ie~per~~ff~ff population. Mean sand-dollar density during January 1984 was 3 .0.25 m - 2 {range l-5 * 0.25 m - 2, pf = 5). The expe~ment was conducted on 15 January 1984; the water temperature was 11.5 “C!, Winter was chosen for two reasons. (1) Good underwater visibility was required for the successful execution of the experiment and it was optimal (2-3 m) during this season. (2) Meiofaunal abundances at the study site were at a peak (unpubl. data).
SAND-DOLLAR
225
BURROW TRAILS
Weather conditions during the experiment were calm with no storm surge or sediment movement. In addition, ripple marks were absent, indicating calm conditions for the preceding few days. These factors are noted because sand-dollar burrowing behavior, especially depth in the sediment, at this site (pers. obs.) and others (Salsman & Tolbert, 1965; Bell & Frey, 1969) appears weather dependent. On calm days at the study site,
20
km
Fig. 1. Study area location.
h4. quinquiesperforuta burrowed a few millimeters below the sediment surface creating
distinctive trails. On stormy days, when the surface sediment was in motion, the majority of sand dollars were found 2-3 cm below the sediment surface. FIELD
EXPERIMENT
The primary objective of this investigation was to determine the immediate effect of sand-dollar bu~o~ng/feed~g on a subtidal meiofauna assemblage. The sampling strategy was similar to the previous intertidal investigations (e.g., Findiay & White, 1983 ; Creed & Could, 1984) in that an undisturbed (control) sample was taken 5 cm in front of an actively burrowing sand dollar and a disturbed (treatment) sample was taken
226
J. A. REIDENA~~ER
I cm behind the sand dollar within the newly created trail. It differed from the other investigations in that it attempted to establish the time that elapsed from initial disturbance to sample collection. Samples were taken with 36cm diameter cores. The fieldwork was done with scuba. The experiment consisted of two parts: (1) manipulated sand dollars and (2) unmanipulated sand dollars. Because Mel&a individuals travel at different rates, the time that elapsed since a sand dollar traveled over a particular point within a burrow trail could not be accurately determined without selecting and monitoring specific individuals. Therefore, sand dollars were collected and released from a marked point and sampled after 1 h to assure the sediment was recently disturbed. Sand dollars treated in this manner were called m~ipulated sand dollars. Unmanipulated sand dollars were comprised of actively burrowing individuals selected at random from the native population. The manipulated and unmanipulated samples were compared to determine if there was any artificial effect as a result of the manipulation. 10 M. quinquiesperfrata, x&cm diameter, were selected from an area near the experimental site and placed in a straight line on the sediment surface with x20 cm between individuals. Numbered cylindrical stakes (13 cm long x 0.3 cm diameter) were placed 0.2 cm behind the posterior margin of each sand dollar. After 1 h, the distance traveled from the stake was measured and disturbed and undisturbed cores were collected as described above. Only six of the original 10 sand dollars could be sampled. One individu~ rotated around its marker stake, two crossed visible preexisting sanddollar trails and one could not be located. The remaining six were sampled in random order. After the manipulated sand dollars were sampled, 12 actively burrowing M. quinquiesperfhata were located from the native population. Six were randomly selected and sampled as described above. Once the cores were taken and returned to the boat, the overlying water was aspirated off and preserved along with the O-l-cm sediment layer in 47; filtered (0.044 mm) seawater-formaldehyde. In the laboratory, the samples were stained with Rose Bengal. The meiofauna were separated from the bulk sediment and concentrated onto a 0.0%mm sieve using the troughing technique described by Bamett (1968). Although it was an efficient method for concentrating h~a~ticoid copepods, nematodes, kinorynchs, mites and ostracods (L 95 % of the total for these taxa, n = 3), troughing was not as efficient for the foraminifera (a: 70% of the total, n = 3). As a consequence, the entire portion of the sediment that remained on the trough was also examined. This procedure proved a more rapid method of sample processing, especially for enumerating nematodes, than merely sorting the complete sample without troughing. The meiofauna were enumerated and identified to major taxon with a dissecting microscope. Harpacticoids were identified to “functional group” based on body form (after Coull, 1977) with the burrowing and epibenthic forms identified to species with a compound microscope. The paired comp~sons (i.e., disturbed and undisturbed samples) were anaiysed as
227
SAND-DOLLAR BURROWTRAILS
a randomized complete-blocks design (Sokal & Rohlf, 1981). Comparisons of total meiofauna and indi~du~ taxa abundances between m~ipulat~ and unm~ipuIated sand dollars were made using a Model I ANOVA test (Sokal & Rohlf, 198 1). The 95 y; significance level was used throughout. Area1 coverage of M. quinquiesperforata burrowing was calculated by multiplying sand-dollar diameter by distance traveled per unit time and abundance per unit area. RESULTS SAND-DOLLARLOCOMOTIONRATE AND LIME SINCE DISTURBANCE The six manipulated M. quinquiesperforata moved at an average rate of 19.2 cm - h - ’ (range 12-2.5 cm * h-- ‘). The values fall within the range, 5-32 cm * h- ‘, for unmanipulated individuals measured at this site (unpubl. data). Given a mean sand-dollar locomotion rate of 19.2 cm * h - ‘, the 3.6cm diameter core taken 1 cm behind a manipulated sand doll-cont~ned sediment that had been disturbed by a sand dollar z 3-14 min before sampling. In other words, it took a sand dollar x 11 min to travel the 3.6 cm horizontal distance sampled by the core. DISTURBANCEFREQUENCY Given a mean sand-dollar diameter of 6 cm, mean locomotion rate of 19.2 cm ’ h - ’ and mean density of 3 sand dollars * 0.25 m _-* for the study area, % 14% of the sediment surface was disturbed in < 1 h (assuming no overIapping trails). MEIOFAUNAABUNDANCES Table I presents the results of the core samples taken in the two parts of the experiment. Total meiofauna abundances include nematodes, harpacticoid copepods,
TABLE I Mean abundances and SD values of meiofauna taxa in undisturbed (U) and disturbed (D) cores (3.6 cm diameter) collected from manipulated and unmanipulated sand dollars (n = 6). Unmanipulated -.-
Manipulated __... U Total meiofauna Nematodes Harpacticoids Ostracods Foraminifera Mites Kinorynchs
580 f 306 f 202 + 33+ 20* 19+ l*
140 145 55 13 9 7 1
D -.. 756 _+209 437 * 190 264 + 86 312 18 II& 9 12* 7 I& 1
U
D
._ 732 & 195 397 5 134 255 I: 61 29& 12 271 10 24& 7 1 21
1033 + 234 680 + 166 293 & 70 26& 7 14* 3 17* 8 2& 2
Manipulated sand dollars Unmanipulated sand dollars 0.002
0.012
0.014
0.020
NS
0.006
NS
NS
Foraminifera
Harpacticoid copepods
Total meiofauna
Nematodes
NS
NS
Ostracods
0.029
NS
Mites
NS
NS
Kinorynchs
Results of statistical analyses on meiofauna taxa sampled in front (undisturbed) and behind (disturbed) M. quinquiesperforafa. P values are given for results that are signi~cantiy different (P < 0.05); NS denotes results that are not significantly different (P > 0.05).
TABLE II
SAND-DOLLAR BURROW TRAILS
229
ostracods, kinorynchs, mites and foraminifera. Table II presents the results of the statistical comparisons between the disturbed and undisturbed samples. In the unmanipulated sand-dollar case, total meiofauna abundances were significantly (P = 0.012) higher in the disturbed samples than in the undisturbed samples due to the high nematode abundances. Mean meiofauna values were 29% higher in the disturbed cores. In the manipulated sand-dollar case, the disturbed and undisturbed samples were not significantly different (P = 0.08) although mean total meiofauna abundances were 23% higher in the disturbed samples. Nematodes were the most abundant meiofauna taxon, comprising a mean of FZ59% of the total meiofauna abundance (n = 12). In both the manipulated and unmanipulated experiments, nematode abundances were significantly higher (P = 0.007 and 0.002, respectively) in cores taken behind the sand dollars. In all 12 pairs of samples collected, nematode abundances were higher in the disturbed cores than in the undisturbed cores. Harpacticoid copepods were the second most abundant meiofauna taxon, comprising a mean of cz 33 % of the total meiofauna abundance (n = 12). Disturbed- and undisturbed-s~ple abundances were not si~~c~tly different (P > 0.05) in both the manipulated and unm~ipulated cases. In addition, analysis of h~pacticoid “functions groups” did not reveal any significant differences between disturbed and undisturbed cores. However, one burrowing species, ~aIectinoso~a sp., was si~i~c~tly more
TABLE III
Halectinosoma sp. abundances
.3.6-cm- ’ diameter core in undisturbed samples taken in front of a sand dollar and disturbed samples taken in sand-dollar burrow trail. Manipulated Replicate
Undisturbed
Disturbed
1
3 2 2 2 4 3 ;i:= 2.1
1 0 2 1 1 1 1.0
2 3 4 5 6
Unmanipulated Replicate
Undisturbed
I
3 2
2 3 4 5 6
1
3 2 3 X = 2.33
Disturbed 0 1 I
1 1 0 0.67
230
J. A. REIDENAUER
abundant in the undisturbed cores than in the disturbed cores (manipulated, P = 0.013; unmanipulated, P = 0.04) (Table III). This species was the largest (x 1 mm total body length) encountered at the study site. For~inifera were si~~c~tly less abundant in the disturbed cores than in the undisturbed cores for both m~ipulat~ and unm~ipulated cases (P = 0.020 and 0.014, respectively). Of the rem~ning three taxa examined, ostracods, mites and kino~chs, the only significant difference between disturbed and undisturbed cores was for mites in the unmanipulated case. The abundance of mites was significantly lower in the disturbed cores than in the undisturbed samples (P = 0.03). Mean mite abundances were 26% lower in the unmanipulated disturbed cores than in the undisturbed cores (n = 6). Although not significant (P = 0.07) mean mite abundances were 37% lower in the manipulated disturbed samples than in the undisturbed cores (n = 6). To determine if there were any artificial effects as a result of collecting and releasing the sand dollars, the total meiofauna and individual taxa results of the manipulated sand dollars were compared to the results of the unmanipulated sand dollars. All the comparisons were not significantly different (P > 0.05) except one; nematode abundances were significantly higher (P = 0.044) in the disturbed cores of the unmanipulated sand dollars than in the disturbed cores of the manipulated sand dollars. As noted previously, nematode abundances were significantly higher in the disturbed cores than the undisturbed cores for both the manipulated and unmanipulated sand dollars. Consequently, the difference in the nematode abundances between the manipulated and unmanipulated sand do&us may have been the result of slightly altered sand-dollar behavior, as a result of the manipulation, which affected the magnitude of nematode enhancement within the burrow trails. The result, however, does not affect the conclusion that nematode abundances were higher within the burrows.
DISCUSSIQN
Because the majority of meiofauna at the study site lived within the O-l cm sediment layer, the sediment disturbance caused by M. quinquiesperforata burrowing/feeding was expected to be associated with a reduction in meiofauna abundance. This expectation was enhanced further during the experiment because the calm weather conditions at the study site aliowed the sand dollars to concentrate their burrowing in the near-surface sediment. Nevertheless, M. quinquiespe&rata burrowing/feeding resulted in significant reductions in only foraminifera, mites, and the harpacticoid Halectinosoma sp. (Table IV). It cannot be classified as a disaster or catastrophic disturbance such as the ray feeding pits documented at a nearshore site in St George Sound (Reidenauer & Thistle, 19XI). The sediment disturb~ce caused by M. quinquie~pe~ruta occurred at a high frequency. The sand dollars at the site disturbed z 14% of the sediment surface in 1 h.
231
SAND-DOLLAR BURROW TRAILS
In addition,
it occurred
centimeters)
(Thistle,
quiesperfbrata movement,
on a spatial scale similar to enteropneust 1980). Nevertheless, the intensity
because
of the disturbance
fecal mounds
of the mechanics
(i.e.,
of M. quin-
may not have been very severe.
The sand dollar does not plow through but “tends to glide between . . . the layers of sediment” (Bell & Frey, 1969). As sediment passes over the test, it is deposited back onto the surface and a distinctive but the geographic or horizontal test does not change noticeably.
trail is formed. location
Sand grains are displaced
vertically
of the sand layer that covers the sand-dollar
TABLE IV Summary of M. quinquiesperfbrata burrowing/feeding effects on subtidal meiofauna and proposed mechanisms. Taxon
Immediate effect
Proposed mechanism
Nematodes (total) Harpacticoids (total) Functional groups Halectinosoma sp. Foraminifera Mites Ostracods Kinorynchs
57% increase None None 67 % decrease 47% decrease 31% decrease None None
Food resource
Disturbance Predation Disturbance
A few of the results obtained in this study were in contrast to those reported in two previous M. quinquiespefiruta-meiofauna investigations (Findlay & White, 1983 ; Creed & Coull, 1984). The most apparent inconsistency was the increased nematode abundances found in the sediment recently disturbed by a sand dollar at the present study site. In both of the other studies, nematode abundances were lower in the burrow trail than in the undisturbed sediment. The difference in the sampling seasons between this study (winter) and the studies conducted by Findlay & White (1983) and Creed & Coull (1984) (late spring and summer) may explain the disparity in the results. The feeding rate and absorption efficiency of M. quinquiesperfrata varies seasonally. M. quinquiesperforata feeds primarily on nonphotosynthetic microeukaryotes in the sediment and not bacteria (White et al., 1980; Findlay & White, 1983). During the winter months, December and January, Lane & Lawrence (1982) reported that the sediments near Mullet Key, off the mid-west coast of Florida, contained the lowest caloric content of food measured throughout the year for the sand dollars. These months also corresponded to negative absorption efficiencies in Mellita. To account for these anomalous negative values, they postulated that M. quinquiesperjxata may release mucus or the cells that line the gut and indicated that a temporary enrichment of the calorically poor sediments may result (Lane & Lawrence, 1981). Nematodes in the sediment adjacent to the trail may be attracted to
NA, not available.
Present study
*, 1980 field data presented.
IntertidalAlligator Pt, Florida IntertidalNorth Inlet, South Carolina SubtidalSt George Sound, Florida
Findlay & White (1983)*
Creed & Coull (1984)
Locations
Study
o-1
5
presented
O-10
0.1-0.25
**, abundances
NA
Sample depth (cm)
0
Water depth during sampling (m)
are
-
10 cm - 2.
9.8
1.77
4.52
Core area (cm’)
397
6 unmanipulated
680
473
306
6 manipulated
217
960** 800**
475
255 --
293
264
22*’
25**
202
101
52 --
D
U
u
D
Harpacticoids
Nematodes
Mean abundances. core-
16
6
Number of sample pairs
21
20
NA
91
U
14
11
NA
41
D
Foraminifera
’
Results of field samples taken in front (undisturbed = U) and behind (disturbed = D) moving M. quinquiesperforufu. Underlined results indicate no significant difference (P > 0.05) between undisturbed (U) and disturbed (D) samples. Results not underlined indicate a significant difference (P < 0.05) between undisturbed (U) and disturbed (D) samples. Data from Creed & Coull (1984) were interpreted from their graph.
TABLE V
SAND-DOLLAR
BURROW TRAILS
233
the mucus-enriched sediments given that mucus is an important food resource to a variety of marine invertebrates (Hobbie & Lee, 1980; Baird, 1984). Food availability has been noted as a primary cause of small-scale patchiness in nematode populations (Gerlach, 1977; Hogue, 1982). Given that the passage of a sand dollar did not appear to cause the nematode fauna to vacate the disrupted sediment, the release of mucus or gut cells may have attracted nematodes. Another possible explanation may be increased pore space available in the sediments disrupted by the sand dollar. ~eIl~t~ pumps some water down through its lunules, thus increasing the pore water content of the disrupted sediment (Ghiold, 1979). Nematodes are interstitial org~isms and an increase in habitat space could result in higher abundances. At first, the rapidity of the response, in I 15 min, is astonishing given that nematodes usually take longer to recolonize disturbed patches than harpacticoids and some other meiofauna taxa (e-g., Sherman et al., 1983). However, given the spatial scale (r+:&cm wide trail) and low intensity of the sand-dollar disruption, the quick response may be understandable. Nematodes can move 0.5 cm in < 1 min (pers. obs). Therefore, individuals along the edge of a newly formed bu~ow trail would have had sufficient time to move into the trait within the time that a sand dollar disturbed the sediment and a sample was collected. In contrast to the nematode results, the results for the other meiofauna taxa were in general agreement with the previous studies. Harpacticoids were unaffected by the passage of a sand dollar both in total abundance and at the functional-group level. These results agree with those of Findlay & White (1983) and Creed & Coull (1984). creed & Coull f 1984) reported signi~~~tly lower abundances of one h~acticoid species, ~po~o~s.~~l~s~~~~~~j~ Coull et Hogue, in sand-dolls burrow trails. This investigation can add an additional species, Halect~no~~ma sp,, which demonstrated reduced abundances within sand-dollar trails. The reduction in foraminifera abundance after the passage of a sand dollar was probably due to predation. Foraminifera are prey for many deposit feeders (Buzas, 1978). Lane (1977) analyzed the gut contents of M. quz’raquiesperjbrataand reported that it ingests diatoms, foraminifera, dinoflagellates and organic detritus. Findlay & White (1983) reported that M. q~j~q~~e~~e~~ata selectively feeds on microeukaryotes and bacteria attached to the silt and clay fractions of the sediments. In addition, 80% of the gut contents of M. q#~~q~je~~e~~~ta were sediment particles SO.062 mm in diameter (Findlay & White, 1983). Of the r~m~ning fauna, only the mites responded in any way to sod-dolls burrowing. Their reduced abundances (26 and 37 % lower behind unm~ipulated and manipulated sand dollars, respectively) in the burrow trail indicated that M. q~j~q~~e~~e~~~t~ may act as a disturbance. Predation appears unlikely given the mobility of mites and that mite hardparts have not been reported in the sand dollar gut. In conclusion, although M. q~jnquie~~~rata burrowing/feeding visibly disturbed the sediment surface, it only si~i~~~tly reduced the abundances of one harpa~ticoid
234
J.A. REIDENAUER
species, foraminifera and mites and in the case of nematodes appeared to have enhanced densities. The sand dollar’s effect on the subtidal meiofauna appears taxon-specitic (Tabie V) with different mechanisms operating simultaneously.
ACKNOWLEDGEMENTS
The research is part of a dissertation conducted in partial ful~Ilment of a Ph.D. from the Department of Oceanography, Fforida State University. I am indebted to my major professor, D. Thistle, who provided guidance during all phases of the study. I thank W. Herrnkind, C. Reidenauer, D. Strong, K. Sherman, K. Carmen, the personnel at the FSU Marine Laboratory at Turkey Point and K. Nettles.
REFERENCES Baird, B., 1984. Utilization of extracellular polymer by a deposit-feeding holothurian. M.S. thesis, Florida State University, Tallahassee, Florida, 41 pp. Barnett, P.R. O., 1968. Distribution and ecology of harpacticoid copepods of an intertidal mudflat. fnt. Rev. Gesamten ~ydrobioi., Vol. 53, pp. 177-209. Bell, B. M. & R. W. Frey, 1969. Observations on ecology and the feeding and burrowing mechanisms of Mellita quinquiesperforata (Leske). J. Paleont., Vol. 43, pp. 553-560. Botton, M.L., 1984. The importance of predation by horseshoe crabs, Limuluspolyphemus, to an intertidal sand flat community. J. Mar. Res., Vol. 42, pp. 139-161. Buzas, M.A., 1978. Foraminifera as prey for benthic deposit feeders: results of predator exclusion experiments. J. Mar, Res., Vol. 36, pp. 617-625. Coull, B.C., 1977. Marine flora and fauna of the northeastern United States. Copepoda : Harpacticoida. NOAA Tech. Rep. NMFS C&c., No. 399, pp. l-49. Coull, B.C. & M.A. Palmer, 1984. Field experimentation in meiofaunal ecology. Hydrobioiogia, Vol. 118, pp. l-19. Creed, E. L. & B.C. Coull, 1984. Sand dollar, Mellita quinquiespetirata (Leske), and sea pansy, Renilla reniformis (Cuvier), effects on meiofaunal abundance. J. Exp. Mar. Biof. Ecol., Vol. 84, pp. 225-234. Findlay, R.H. & D.C. White, 1983. The effects of feeding by the sand dollar Me&a quinqujespe~rara (Leske) on the benthic microbic community. .I. Exp. Mar. Biol. Ecol., Vol. 72, pp. 25-41. Gerlach, S.A., 1977. Attraction to decaying organisms as a possible cause for patchy distribution of nematodes in a Bermuda beach. Ophefia, Vol. 16, pp. 1.51-165. Ghiold, J., 1979. Spine morphology and its significance in feeding and burrowing in the sand dollar, Mellita quinquiesperjkata (Echinodermata: Echinoidea). l&U. Mar. Sci., Vol. 19, pp. 481-490. Grant, J., 1983. The relative magnitude of biological and physical sediment reworking in an intertidal community. J. Mar. Res., Vol. 41, pp. 673-689. Hobbie. J. E. & C. Lee, 1980. Microbial production ofextracelhdar material: importance in benthic ecology. In, Marine benfhic dynamics, edited by K. R. Tenore & B.C. Coull, University of South Carolina Press, Columbia, South Carolina, pp. 341-346. Hague, E.W., 1982. Sediment disturbance and the spatial distributions of shallow water meiobenthic nematodes on the open Oregon coast. J. Mar. Res., Vol. 40, pp. 551-573. Lane, J. E. M., 1977. Bioenergetics of the sand dollar, Me/&u quinquiespefiratu (Leske, 1778). Ph.D. Diss., University of South Florida, Tampa, Florida, 363 pp. Lane, J. E. M. & J. M. Lawrence, 198I. Effect of body size and temperature on the release of ammonia and dissolved organic carbon. Comp. Biochem. Physiol., Vol. 70, pp. 603-606. Lane, J. E. M. & J. M. Lawrence, 1982. Food, feeding and absorption efficiencies of the sand dollar, Mel&a quinquiespefirata (Leske). Es&urine Coastal Shef Sci., Vol. 14, pp. 421-43 1.
SAND-DOLLAR
BURROW
TRAILS
235
Levin, L. A., 1984. Life history and dispersal patterns in a dense infaunal polychaete assemblage: community structure and response to disturbance. Ecology, Vol. 65, pp. 1185-1200. Oliver, J.S., R.G. Kvitek & P.N. Slattery, 1985. Walrus feeding disturbance: scavenging habits and recolonization of the Bering Sea benthos. J. Exp. Mar. Biol. Ecol., Vol. 91, pp. 233-246. Reidenauer, J.A. & D. Thistle, 1981. Response of a soft-bottom harpacticoid community to stingray (Dasyafis sabina) disturbance. Mar. Biol., Vol. 65, pp. 261-267. Rhoads, D.C., 1967. Biogenic reworking of intertidal and subtidal sediments in Barnstable Harbor and Buzzards Bay, Massachusetts. J. Geol., Vol. 75, pp. 461-476. Salsman, G. G. & W. H. Tolbert, 1965. Observations on the sand dollar, Mellita quinquiesperjkata. Limnol. Oceanogr., Vol. 10, pp. 152-155. Sherman, K.M., J.A. Reidenauer, D. Thistle & D. Meeter, 1983. Role of a natural disturbance in an assemblage of marine free-living nematodes. Mar. Ecol. Prog. Ser., Vol. 11, pp. 23-30. Sokal, R. R. & F. J. Rohlf, 1981. Biomeo. W. H. Freeman & Co., San Francisco, California, second edition, 859 pp. Thistle, D., 1980. The response of a harpacticoid copepod community to a small-scale natural disturbance. J. Mar. Res., Vol. 38, pp. 381-395. VanBlaricom, G.R., 1982. Experimental analyses of structural regulation in a marine sand community exposed to oceanic swell. Ecol. Monogr., Vol. 52, pp. 283-305. White, D. C., R. H. Findlay, S. D. Fazio, R. J. Bobbie, J. S. Nickels, W.M. Davis, G. A. Smith & R. F. Martz, 1980. Effects of bioturbation and predation by Mel&a quinquiesperjkata on sedimentary microbial community structure. In, Estuarineperspectives, edited by V.S. Kennedy, Academic Press, New York, New York, pp. 163-171. Wiltse, W. I., 1980. Effects of Polinices duplicatus (Gastropoda:Naticidae) on infaunal community structure at Barnstable Harbor, MA, USA. Mar. Biol., Vol. 56, pp. 301-310. Woodin, S. A., 1978. Refuge, disturbance, and community structure: a marine soft-bottom example. Ecology. Vol. 59, pp. 274-284. Woodin, S. A., 1981. Disturbance and community structure in a shallow water sand flat. Ecology, Vol. 62, pp. 1052-1066. Zajac, R.N. & R. W. Whitlatch, 1982. Responses ofestuarine infauna to disturbance. I. Spatial and temporal variations in initial recolonization. Mar. Ecol. Prog. Ser., Vol. 10, pp. l-14.
1989, Vol. 130, pp. 223-235
223
Elsevier
JEMBE 01300
Sand-dollar Mel&z quinquiesperforuta(Leske) burrow trails: sites of harpacticoid disturbance and nematode attraction Jeffrey A. R~~d~na~er ~e~~rt~z~nt of Oce~n~~phy,
Florida S#ate ~niver~ty, ~aliah~~ee, ~~~r~d~,U.S.A.
(Received 1 March 1989; revision received 5 May 1989; accepted 14 &me 1989) Abstract: The effect of sand-dollar MeZEtaq~jnqu~e~pe~rut~ (Leske) burrowing on a soft-bottom meiofauna community was examined at a subtidal site located off the northwest Florida coast. M. quinquiesperjbruta were common at the site with an average of 3 ind .0.25m __2 and their burrow trails were a distinctive feature of the sediment surface. At the site, sand dollars disrupted z 14% of the sediment surface. h _ ‘, Sand-dollar burrowing did not decrease total meiofauna abundances significantly (P > 0.05); however, the abundances of one harpacticoid species, Halectinosoma sp., foraminifera and mites were significantly lower (P < 0.05) in sampies collected from a burrow trail than in samples collected in front of the sand dollar. The lower abundances o~~alectinoso~a sp. and mites in the burrow trail were probably due to sediment disturbance. The lower abundances of foraminifera in the burrow trails were probably due to sand-dollar predation. In contrast to studies in intertidal areas, total nematode abundances were si~ific~tly higher (P -C 0.05) in the samples collected behind a moving sand dollar than in samples collected in front of the sand dollar. Possible reasons for the enhanced abundances are: (1) increased food availability in the form of mucus and/or excreted cells &at line the sand-dollar gut; and (2)increased pore space within the sediment.
Key words: Disturbance; Harpacticoid; Meiofauna; Nematode; Sand dollar; Sediment disturbance
In soft-bottom marine habitats, disturbances are often recognizable as visibfe disrupon the sediment surface. For example, ray feeding pits (Reidenauer & Thistle, 1981; VanBl~com, 1982; Grant, 1983), horseshoe crab trails (Woodin, 1981; Botton, 1984) and gastropod trails (Rhoads, 1967; W&se, 1980) are documented sites of disturbance to soft-bottom benthic communities. As disturbances are dissimilar in size and appearance, they are also different in their initial postdisturb~~~ conditions. The effects of natural disturbances may vary from complete removal of the resident fauna and creation of an azoic patch (i.e., disaster and catastrophe) to reductions in species numbers and densities within the disturbed patch. Many biologically produced disturbances are important in determining macrofaunal community structure (Woodin, 1978; Zajac & Whitlatch, 1982; Oliver et a!., 1985) and tions
Correspondence 36633. U.S.A.
address: J.A. Reidenauer, BCM Converse inc., IO8 St. Anthony Street, Mobile, AL
0022-098i/89/$O3.50 0 1989 Elsevier Science Publishers B.V. (Biom~dic~ Division)
224
J.A. REIDENAUER
are critical in the life history of individual macrofaunal species (e.g., ~phipods VanRlaricom, 1982; bivalves - W&se, 1980; and, polychaetes - Levin, 1984). In contrast, the effects of disturbance on the meiofauna are not well established. Only a limited number of field experiments have investigated the effect of biologically produced natural disturbances on meiofauna (Coull & Palmer, 1984). The results of these studies document a variety of effects. In some cases, catastrophic removal of the community occurs such as when rays excavate meiofauna along with the sediment in their search for deep-living prey (Reidenauer & Thistle, 1981; Sherman et al., 1983) and when entropneusts ingest sediment and defecate material upon the sediment surface (Thistle, 1980). In contrast, sand-dollar burrow trails represent a category of s~dimcnt disturbances that are ~o~catastrophjc to the overah meiofauna community but nonetheless have species-specific effects. Two previous investigations have examined the effects of sand-do&r Mel&z q~j~q~je~~e~~u~u (Leske) bu~owing on intertidal meiofaunal communities : (I) at Alligator Point, Florida (Findlay & White, 19831, and (2) at North Inlet, South Carolina (Creed & Coull, 1984). Each study concluded that the dist~b~ce generated by the sand dollars were generally noncatastrophic to the resident meiofaun~ comm~ity. Nonetheless, both investigations documented reductions in specific meiofauna taxa while other taxa were unaffected. Given iM. ~~~~~~e~~~r~~~‘s abundance and potentid importance in subtidaf regions, it is appropriate to test the conclusions reached by the intertidal investigators in a subtidal cnv~onment. To that end, a field experiment was conducted at a subtidal site in St George Sound, Florida, where M. qu~~q~~espe~rur~ were common. To facilitate comparisons, the sampling strategy was similar to the one utilized in the intertidal studies. MATERIALS AND METHODS LOCALITY The study site was located at adepth of 5 m on an unvegetated sand-flat x 7 km south of Turkey Point, Florida, in St George Sound (29”5I’N, 84”3I’W) (Fig. I). Bottom salinity was 307& and median grain size of the sediment was 0.254 mm. The site was protected from strong storm swells by Dog Island Reef, a submerged barrier island located % 0.7 km to the south of the site. The area was characterized by a persistent and tempor~Iy dense iM. q~~~q~ie~per~~ff~ff population. Mean sand-dollar density during January 1984 was 3 .0.25 m - 2 {range l-5 * 0.25 m - 2, pf = 5). The expe~ment was conducted on 15 January 1984; the water temperature was 11.5 “C!, Winter was chosen for two reasons. (1) Good underwater visibility was required for the successful execution of the experiment and it was optimal (2-3 m) during this season. (2) Meiofaunal abundances at the study site were at a peak (unpubl. data).
SAND-DOLLAR
225
BURROW TRAILS
Weather conditions during the experiment were calm with no storm surge or sediment movement. In addition, ripple marks were absent, indicating calm conditions for the preceding few days. These factors are noted because sand-dollar burrowing behavior, especially depth in the sediment, at this site (pers. obs.) and others (Salsman & Tolbert, 1965; Bell & Frey, 1969) appears weather dependent. On calm days at the study site,
20
km
Fig. 1. Study area location.
h4. quinquiesperforuta burrowed a few millimeters below the sediment surface creating
distinctive trails. On stormy days, when the surface sediment was in motion, the majority of sand dollars were found 2-3 cm below the sediment surface. FIELD
EXPERIMENT
The primary objective of this investigation was to determine the immediate effect of sand-dollar bu~o~ng/feed~g on a subtidal meiofauna assemblage. The sampling strategy was similar to the previous intertidal investigations (e.g., Findiay & White, 1983 ; Creed & Could, 1984) in that an undisturbed (control) sample was taken 5 cm in front of an actively burrowing sand dollar and a disturbed (treatment) sample was taken
226
J. A. REIDENA~~ER
I cm behind the sand dollar within the newly created trail. It differed from the other investigations in that it attempted to establish the time that elapsed from initial disturbance to sample collection. Samples were taken with 36cm diameter cores. The fieldwork was done with scuba. The experiment consisted of two parts: (1) manipulated sand dollars and (2) unmanipulated sand dollars. Because Mel&a individuals travel at different rates, the time that elapsed since a sand dollar traveled over a particular point within a burrow trail could not be accurately determined without selecting and monitoring specific individuals. Therefore, sand dollars were collected and released from a marked point and sampled after 1 h to assure the sediment was recently disturbed. Sand dollars treated in this manner were called m~ipulated sand dollars. Unmanipulated sand dollars were comprised of actively burrowing individuals selected at random from the native population. The manipulated and unmanipulated samples were compared to determine if there was any artificial effect as a result of the manipulation. 10 M. quinquiesperfrata, x&cm diameter, were selected from an area near the experimental site and placed in a straight line on the sediment surface with x20 cm between individuals. Numbered cylindrical stakes (13 cm long x 0.3 cm diameter) were placed 0.2 cm behind the posterior margin of each sand dollar. After 1 h, the distance traveled from the stake was measured and disturbed and undisturbed cores were collected as described above. Only six of the original 10 sand dollars could be sampled. One individu~ rotated around its marker stake, two crossed visible preexisting sanddollar trails and one could not be located. The remaining six were sampled in random order. After the manipulated sand dollars were sampled, 12 actively burrowing M. quinquiesperfhata were located from the native population. Six were randomly selected and sampled as described above. Once the cores were taken and returned to the boat, the overlying water was aspirated off and preserved along with the O-l-cm sediment layer in 47; filtered (0.044 mm) seawater-formaldehyde. In the laboratory, the samples were stained with Rose Bengal. The meiofauna were separated from the bulk sediment and concentrated onto a 0.0%mm sieve using the troughing technique described by Bamett (1968). Although it was an efficient method for concentrating h~a~ticoid copepods, nematodes, kinorynchs, mites and ostracods (L 95 % of the total for these taxa, n = 3), troughing was not as efficient for the foraminifera (a: 70% of the total, n = 3). As a consequence, the entire portion of the sediment that remained on the trough was also examined. This procedure proved a more rapid method of sample processing, especially for enumerating nematodes, than merely sorting the complete sample without troughing. The meiofauna were enumerated and identified to major taxon with a dissecting microscope. Harpacticoids were identified to “functional group” based on body form (after Coull, 1977) with the burrowing and epibenthic forms identified to species with a compound microscope. The paired comp~sons (i.e., disturbed and undisturbed samples) were anaiysed as
227
SAND-DOLLAR BURROWTRAILS
a randomized complete-blocks design (Sokal & Rohlf, 1981). Comparisons of total meiofauna and indi~du~ taxa abundances between m~ipulat~ and unm~ipuIated sand dollars were made using a Model I ANOVA test (Sokal & Rohlf, 198 1). The 95 y; significance level was used throughout. Area1 coverage of M. quinquiesperforata burrowing was calculated by multiplying sand-dollar diameter by distance traveled per unit time and abundance per unit area. RESULTS SAND-DOLLARLOCOMOTIONRATE AND LIME SINCE DISTURBANCE The six manipulated M. quinquiesperforata moved at an average rate of 19.2 cm - h - ’ (range 12-2.5 cm * h-- ‘). The values fall within the range, 5-32 cm * h- ‘, for unmanipulated individuals measured at this site (unpubl. data). Given a mean sand-dollar locomotion rate of 19.2 cm * h - ‘, the 3.6cm diameter core taken 1 cm behind a manipulated sand doll-cont~ned sediment that had been disturbed by a sand dollar z 3-14 min before sampling. In other words, it took a sand dollar x 11 min to travel the 3.6 cm horizontal distance sampled by the core. DISTURBANCEFREQUENCY Given a mean sand-dollar diameter of 6 cm, mean locomotion rate of 19.2 cm ’ h - ’ and mean density of 3 sand dollars * 0.25 m _-* for the study area, % 14% of the sediment surface was disturbed in < 1 h (assuming no overIapping trails). MEIOFAUNAABUNDANCES Table I presents the results of the core samples taken in the two parts of the experiment. Total meiofauna abundances include nematodes, harpacticoid copepods,
TABLE I Mean abundances and SD values of meiofauna taxa in undisturbed (U) and disturbed (D) cores (3.6 cm diameter) collected from manipulated and unmanipulated sand dollars (n = 6). Unmanipulated -.-
Manipulated __... U Total meiofauna Nematodes Harpacticoids Ostracods Foraminifera Mites Kinorynchs
580 f 306 f 202 + 33+ 20* 19+ l*
140 145 55 13 9 7 1
D -.. 756 _+209 437 * 190 264 + 86 312 18 II& 9 12* 7 I& 1
U
D
._ 732 & 195 397 5 134 255 I: 61 29& 12 271 10 24& 7 1 21
1033 + 234 680 + 166 293 & 70 26& 7 14* 3 17* 8 2& 2
Manipulated sand dollars Unmanipulated sand dollars 0.002
0.012
0.014
0.020
NS
0.006
NS
NS
Foraminifera
Harpacticoid copepods
Total meiofauna
Nematodes
NS
NS
Ostracods
0.029
NS
Mites
NS
NS
Kinorynchs
Results of statistical analyses on meiofauna taxa sampled in front (undisturbed) and behind (disturbed) M. quinquiesperforafa. P values are given for results that are signi~cantiy different (P < 0.05); NS denotes results that are not significantly different (P > 0.05).
TABLE II
SAND-DOLLAR BURROW TRAILS
229
ostracods, kinorynchs, mites and foraminifera. Table II presents the results of the statistical comparisons between the disturbed and undisturbed samples. In the unmanipulated sand-dollar case, total meiofauna abundances were significantly (P = 0.012) higher in the disturbed samples than in the undisturbed samples due to the high nematode abundances. Mean meiofauna values were 29% higher in the disturbed cores. In the manipulated sand-dollar case, the disturbed and undisturbed samples were not significantly different (P = 0.08) although mean total meiofauna abundances were 23% higher in the disturbed samples. Nematodes were the most abundant meiofauna taxon, comprising a mean of FZ59% of the total meiofauna abundance (n = 12). In both the manipulated and unmanipulated experiments, nematode abundances were significantly higher (P = 0.007 and 0.002, respectively) in cores taken behind the sand dollars. In all 12 pairs of samples collected, nematode abundances were higher in the disturbed cores than in the undisturbed cores. Harpacticoid copepods were the second most abundant meiofauna taxon, comprising a mean of cz 33 % of the total meiofauna abundance (n = 12). Disturbed- and undisturbed-s~ple abundances were not si~~c~tly different (P > 0.05) in both the manipulated and unm~ipulated cases. In addition, analysis of h~pacticoid “functions groups” did not reveal any significant differences between disturbed and undisturbed cores. However, one burrowing species, ~aIectinoso~a sp., was si~i~c~tly more
TABLE III
Halectinosoma sp. abundances
.3.6-cm- ’ diameter core in undisturbed samples taken in front of a sand dollar and disturbed samples taken in sand-dollar burrow trail. Manipulated Replicate
Undisturbed
Disturbed
1
3 2 2 2 4 3 ;i:= 2.1
1 0 2 1 1 1 1.0
2 3 4 5 6
Unmanipulated Replicate
Undisturbed
I
3 2
2 3 4 5 6
1
3 2 3 X = 2.33
Disturbed 0 1 I
1 1 0 0.67
230
J. A. REIDENAUER
abundant in the undisturbed cores than in the disturbed cores (manipulated, P = 0.013; unmanipulated, P = 0.04) (Table III). This species was the largest (x 1 mm total body length) encountered at the study site. For~inifera were si~~c~tly less abundant in the disturbed cores than in the undisturbed cores for both m~ipulat~ and unm~ipulated cases (P = 0.020 and 0.014, respectively). Of the rem~ning three taxa examined, ostracods, mites and kino~chs, the only significant difference between disturbed and undisturbed cores was for mites in the unmanipulated case. The abundance of mites was significantly lower in the disturbed cores than in the undisturbed samples (P = 0.03). Mean mite abundances were 26% lower in the unmanipulated disturbed cores than in the undisturbed cores (n = 6). Although not significant (P = 0.07) mean mite abundances were 37% lower in the manipulated disturbed samples than in the undisturbed cores (n = 6). To determine if there were any artificial effects as a result of collecting and releasing the sand dollars, the total meiofauna and individual taxa results of the manipulated sand dollars were compared to the results of the unmanipulated sand dollars. All the comparisons were not significantly different (P > 0.05) except one; nematode abundances were significantly higher (P = 0.044) in the disturbed cores of the unmanipulated sand dollars than in the disturbed cores of the manipulated sand dollars. As noted previously, nematode abundances were significantly higher in the disturbed cores than the undisturbed cores for both the manipulated and unmanipulated sand dollars. Consequently, the difference in the nematode abundances between the manipulated and unmanipulated sand do&us may have been the result of slightly altered sand-dollar behavior, as a result of the manipulation, which affected the magnitude of nematode enhancement within the burrow trails. The result, however, does not affect the conclusion that nematode abundances were higher within the burrows.
DISCUSSIQN
Because the majority of meiofauna at the study site lived within the O-l cm sediment layer, the sediment disturbance caused by M. quinquiesperforata burrowing/feeding was expected to be associated with a reduction in meiofauna abundance. This expectation was enhanced further during the experiment because the calm weather conditions at the study site aliowed the sand dollars to concentrate their burrowing in the near-surface sediment. Nevertheless, M. quinquiespe&rata burrowing/feeding resulted in significant reductions in only foraminifera, mites, and the harpacticoid Halectinosoma sp. (Table IV). It cannot be classified as a disaster or catastrophic disturbance such as the ray feeding pits documented at a nearshore site in St George Sound (Reidenauer & Thistle, 19XI). The sediment disturb~ce caused by M. quinquie~pe~ruta occurred at a high frequency. The sand dollars at the site disturbed z 14% of the sediment surface in 1 h.
231
SAND-DOLLAR BURROW TRAILS
In addition,
it occurred
centimeters)
(Thistle,
quiesperfbrata movement,
on a spatial scale similar to enteropneust 1980). Nevertheless, the intensity
because
of the disturbance
fecal mounds
of the mechanics
(i.e.,
of M. quin-
may not have been very severe.
The sand dollar does not plow through but “tends to glide between . . . the layers of sediment” (Bell & Frey, 1969). As sediment passes over the test, it is deposited back onto the surface and a distinctive but the geographic or horizontal test does not change noticeably.
trail is formed. location
Sand grains are displaced
vertically
of the sand layer that covers the sand-dollar
TABLE IV Summary of M. quinquiesperfbrata burrowing/feeding effects on subtidal meiofauna and proposed mechanisms. Taxon
Immediate effect
Proposed mechanism
Nematodes (total) Harpacticoids (total) Functional groups Halectinosoma sp. Foraminifera Mites Ostracods Kinorynchs
57% increase None None 67 % decrease 47% decrease 31% decrease None None
Food resource
Disturbance Predation Disturbance
A few of the results obtained in this study were in contrast to those reported in two previous M. quinquiespefiruta-meiofauna investigations (Findlay & White, 1983 ; Creed & Coull, 1984). The most apparent inconsistency was the increased nematode abundances found in the sediment recently disturbed by a sand dollar at the present study site. In both of the other studies, nematode abundances were lower in the burrow trail than in the undisturbed sediment. The difference in the sampling seasons between this study (winter) and the studies conducted by Findlay & White (1983) and Creed & Coull (1984) (late spring and summer) may explain the disparity in the results. The feeding rate and absorption efficiency of M. quinquiesperfrata varies seasonally. M. quinquiesperforata feeds primarily on nonphotosynthetic microeukaryotes in the sediment and not bacteria (White et al., 1980; Findlay & White, 1983). During the winter months, December and January, Lane & Lawrence (1982) reported that the sediments near Mullet Key, off the mid-west coast of Florida, contained the lowest caloric content of food measured throughout the year for the sand dollars. These months also corresponded to negative absorption efficiencies in Mellita. To account for these anomalous negative values, they postulated that M. quinquiesperjxata may release mucus or the cells that line the gut and indicated that a temporary enrichment of the calorically poor sediments may result (Lane & Lawrence, 1981). Nematodes in the sediment adjacent to the trail may be attracted to
NA, not available.
Present study
*, 1980 field data presented.
IntertidalAlligator Pt, Florida IntertidalNorth Inlet, South Carolina SubtidalSt George Sound, Florida
Findlay & White (1983)*
Creed & Coull (1984)
Locations
Study
o-1
5
presented
O-10
0.1-0.25
**, abundances
NA
Sample depth (cm)
0
Water depth during sampling (m)
are
-
10 cm - 2.
9.8
1.77
4.52
Core area (cm’)
397
6 unmanipulated
680
473
306
6 manipulated
217
960** 800**
475
255 --
293
264
22*’
25**
202
101
52 --
D
U
u
D
Harpacticoids
Nematodes
Mean abundances. core-
16
6
Number of sample pairs
21
20
NA
91
U
14
11
NA
41
D
Foraminifera
’
Results of field samples taken in front (undisturbed = U) and behind (disturbed = D) moving M. quinquiesperforufu. Underlined results indicate no significant difference (P > 0.05) between undisturbed (U) and disturbed (D) samples. Results not underlined indicate a significant difference (P < 0.05) between undisturbed (U) and disturbed (D) samples. Data from Creed & Coull (1984) were interpreted from their graph.
TABLE V
SAND-DOLLAR
BURROW TRAILS
233
the mucus-enriched sediments given that mucus is an important food resource to a variety of marine invertebrates (Hobbie & Lee, 1980; Baird, 1984). Food availability has been noted as a primary cause of small-scale patchiness in nematode populations (Gerlach, 1977; Hogue, 1982). Given that the passage of a sand dollar did not appear to cause the nematode fauna to vacate the disrupted sediment, the release of mucus or gut cells may have attracted nematodes. Another possible explanation may be increased pore space available in the sediments disrupted by the sand dollar. ~eIl~t~ pumps some water down through its lunules, thus increasing the pore water content of the disrupted sediment (Ghiold, 1979). Nematodes are interstitial org~isms and an increase in habitat space could result in higher abundances. At first, the rapidity of the response, in I 15 min, is astonishing given that nematodes usually take longer to recolonize disturbed patches than harpacticoids and some other meiofauna taxa (e-g., Sherman et al., 1983). However, given the spatial scale (r+:&cm wide trail) and low intensity of the sand-dollar disruption, the quick response may be understandable. Nematodes can move 0.5 cm in < 1 min (pers. obs). Therefore, individuals along the edge of a newly formed bu~ow trail would have had sufficient time to move into the trait within the time that a sand dollar disturbed the sediment and a sample was collected. In contrast to the nematode results, the results for the other meiofauna taxa were in general agreement with the previous studies. Harpacticoids were unaffected by the passage of a sand dollar both in total abundance and at the functional-group level. These results agree with those of Findlay & White (1983) and Creed & Coull (1984). creed & Coull f 1984) reported signi~~~tly lower abundances of one h~acticoid species, ~po~o~s.~~l~s~~~~~~j~ Coull et Hogue, in sand-dolls burrow trails. This investigation can add an additional species, Halect~no~~ma sp,, which demonstrated reduced abundances within sand-dollar trails. The reduction in foraminifera abundance after the passage of a sand dollar was probably due to predation. Foraminifera are prey for many deposit feeders (Buzas, 1978). Lane (1977) analyzed the gut contents of M. quz’raquiesperjbrataand reported that it ingests diatoms, foraminifera, dinoflagellates and organic detritus. Findlay & White (1983) reported that M. q~j~q~~e~~e~~ata selectively feeds on microeukaryotes and bacteria attached to the silt and clay fractions of the sediments. In addition, 80% of the gut contents of M. q#~~q~je~~e~~~ta were sediment particles SO.062 mm in diameter (Findlay & White, 1983). Of the r~m~ning fauna, only the mites responded in any way to sod-dolls burrowing. Their reduced abundances (26 and 37 % lower behind unm~ipulated and manipulated sand dollars, respectively) in the burrow trail indicated that M. q~j~q~~e~~e~~~t~ may act as a disturbance. Predation appears unlikely given the mobility of mites and that mite hardparts have not been reported in the sand dollar gut. In conclusion, although M. q~jnquie~~~rata burrowing/feeding visibly disturbed the sediment surface, it only si~i~~~tly reduced the abundances of one harpa~ticoid
234
J.A. REIDENAUER
species, foraminifera and mites and in the case of nematodes appeared to have enhanced densities. The sand dollar’s effect on the subtidal meiofauna appears taxon-specitic (Tabie V) with different mechanisms operating simultaneously.
ACKNOWLEDGEMENTS
The research is part of a dissertation conducted in partial ful~Ilment of a Ph.D. from the Department of Oceanography, Fforida State University. I am indebted to my major professor, D. Thistle, who provided guidance during all phases of the study. I thank W. Herrnkind, C. Reidenauer, D. Strong, K. Sherman, K. Carmen, the personnel at the FSU Marine Laboratory at Turkey Point and K. Nettles.
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