Variation in megafaunal assemblages on the continental margin south of New England

Deep-$~ R*mMeck,VoL 3'7,No. I. pp. 37-57, 1990. Pr~-,d m Gnat Bntmn.

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Variation in megafaunal assemblages on the continental margin south of New England BARBARA HECKER*

(Received 26 August 1988; in revisedform 26 June 1989; accepted 24 July 1989) AbstrKt--Megafaunal assemblages at four locations on the slope south of New England were surveyed using a towed camera sled, with photographs taken at automatic 15 s intervals. A total of 284,692 organisms were seen in 94,380 m" of sea floor viewed. Classification and ordination analysis defined four megafaunal zones that corresponded to different regions of the slope: an upper slope zone, an upper-middle slope zone, a transitional zone on the lower-middle slope, and a lower slope zone. Each of these zones could be further subdivided into shallow and deep portions of higher species similarity. Faunal densities were high in the upper and lower slope zones and low in the two middle slope zones. The boundaries between zones were frequently marked by abrupt shifts in faunal density and trophic structure. High species overlap between adjacent zones suggested a pattern of continual species turnover along the depth gradient, with zones representing regions of lesser faunal changes separated by regions of greater faunal change. Species replacement with depth was very abrupt in steep areas and gradual in flat areas. The pattern of species turnover and the depths of faunal boundaries varied among geographic locations, reflecting differences in local topography and geology. Patterns of density, and species composition, with depth were very similar at three of the locations but differed significantly at the eastern edge of Georges Bank, a site characterized by very steep topography and numerous glacial erratics and outcrops. Faunal a~semblages in zones were frequently dominated by one or two very abundant species, and the boundaries between zones usually reflected the depth limits of these species. At each location, depths of major faunal boundaries coincided with relative changes in slope declivity rather than absolute angles of inclination. Environmental heterogeneity provided by different substrata may further enhance species turnover along the depth gradient. Variable relief also may allow extension of depth ranges by providing refuge from predation and/or altering food resources. Factors controlling the distribution of megafaunal assemblages on sediment-covered slopes may be related to the effect of local topography on current intensities and related differences in food availability.

INTRODUCTION

CU^NOE in species composition with depth on continental slopes has been well established (VINoOaADOVA,1962; ROWEand MENZlES, 1969; MENZlESet al., 1973; HAEDRICUet al., 1972, 1980; CAGEY et al., 1983). Data from many studies suggest that zones of faunal assemblages extend along continental margins in bands parallel to isobaths. Zonation is probably related to a multiplicity of both physical and biological factors. But neither the horizontal extent of "zones" nor their variability within a geographic area has been well documented. Most studies have been concerned with the degree to which different taxa are zoned with depth. Faunal turnover patterns vary considerably among groups of taxa and different size categories (R~x, 1981). Megafaunal invertebrates are thought to be more pronouncedly zoned than the smaller size categories. Explanations for vertical • Lamont-Dohcrty Geological Observatory of Columbia University, Palisades, NY 10964, U.S.A. 37

38

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distributions have centered either on physical factors that vary with depth (HAEDRICHet al., 1975, 1980) or on biological parameters, such as life-history tactics (GgASSLE et al., 1979) and the relative importance of competition and predation at different trophic levels (REx, 1977). Megafaunal assemblages on the continental slope off the northeastern U.S. coast have been investigated extensively (GgAsst~ et al., 1975; HAEDPdCHet al., 1975, 1980). The slope in this region frequently is viewed as being relatively homogeneous in topography and associated physical characteristics. Depths of maximum faunal change from samples collected over relatively large areas frequently have been related to changes in topography and associated environmental parameters, based on a stylized view of the slope. Recent advances in sea-floor imaging techniques show that the topography of the continental slope in this region is variable and complex. Using long-range sidescan sonar, SCANLON(1984) has shown that approximately 80% of the continental slope in this region consists of a complex gully and ridge morphology. Relating faunal changes in samples collected over varying habitats to an idealized gradient may resolve the environment at a much larger scale than is relevant to the organisms being studied. In the process, important clues to parameters controlling faunal distributions may be obscured. In this paper I present data on megafaunal populations based on an analysis of 35 mm color slides taken with a towed camera sled. The tows were conducted over a 5 year period, as part of two projects that investigated various physical and biological parameters of the northern U.S. continental margin. A photographic method was chosen because it allowed continuous fine-scale sampling along transects that spanned the slope. A depth transducer on the camera sled provided a detailed topographic profile, and the photographs provided ancillary information on surficial geology. The data presented in this paper show that patterns of megafaunal abundance and species turnover rate vary among locations, and that these variations may in part be related to the effect of local topography on current intensities and food availability. MATERIALS AND METHODS Field sampling Epifaunal populations were surveyed with cross-isobath, camera-sled tows at four different locations on the continental slope south of New England (Fig. l). The four locations were chosen to (a) obtain wide geographic coverage, (b) examine the effect of differing slope topographies, and (c) coincide with other concurrent biological and physical studies. Tows at two of the locations were conducted as part of the multidisciplinary North Atlantic Slope and Rise Study (MACIOLEKet al., 1987). The westernmost location (WT) at longitude 70°55'W also coincided with the DOE Shelf Edge Exchange Processes (SEEP) transect (WALS[t et al., 1988). Two camera tows, one year apart (May 1985 and May 1986), were conducted at this location. The other location (USB), at the eastern edge of Georges Bank, was near the U.S.-Canadian Boundary. Three tows (November 1984, May 1985 and May 1986) were conducted in this vicinity. Tows at the other two locations were conducted in 1981 as part of the Canyon and Slope Processes Study (HECKERet al., 1983). Both of these locations (WS and ES) were on the slope near the western edge of Georges Bank. Two tows, one on a ridge and one in a valley, were conducted at each of these locations. The camera sleds used for these tows, BERNEI and BABS, were designed to ride on the sea floor, with the forward-pointing camera mounted at an angle of 13.5° down from

Variation in mcgafaunalassemblages

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Fig. t, Map of studyareashowingpositionof the four locationssurveycdwith camera-sled tows, WT (coincided with the SEEP line) and USB were surveyedfor the North Atlantic Slope and Rise Study, and WS and WT were surv¢ycdfor the Canyon and Slope ProcessesStudy. horizontal 0.43 m above the skids. When photographing a level surface this configuration resulted in a clear picture of approximately 5 m 2 of the sea floor, illumination was provided by a 200 W strobe mounted to the side and slightly above the camera, The combination of low viewing angle and side illumination provided exceptionally clear close-up photographs of the organisms. The resulting side views, by showing such features as fine configuration of fish and polyp configuration of corals, greatly aided in identifying many of the organisms. Proximity to the sea floor allowed enumeration of smaller taxa, and side illumination provided shadows for discerning substrate-colored or translucent taxa. The major disadvantage of the low viewing angle was the large variation of area photographed (m 2) when the camera sled traversed steep slopes, in these cases (approximately 25% of the pictures) area viewed was estimated based on the position of the horizon on the photograph and on the size of organisms. The camera sled was towed by attaching a 100 m polypropylene tether to a 600 kg weight at the end of the trawl cable. A low towing angle for maximum horizontal bottom contact was facilitated by the use of two transponders, one mounted on the trawl cable 5 m above the weight and one mounted on the sled. An optimum towing angle was obtained with the weight approximately 5 m above the sea floor. The camera was towed at an average speed of 1 kn, with exposures taken at automatic 15 s intervals throughout each tow. The film consisted of 400 ft reels, allowing a maximum bottom time of 13.3 h. However, the tows were occassionally terminated early due to the high density of lobster traps along the 300 m isobath. At a 1 kn towing speed, with 15 s exposures, a maximum quantifiable coverage of 25% of a 2.5 m wide swath could be attained. Coverage was usually less, however, because the camera sled did not maintain continuous bottom contact in steep rocky areas and tended to photograph less area on steep slopes. Run number, time and depth were recorded automatically on each frame.

40

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The continuous sampling provided by this type of photographic survey was particularly desirable because multivariate pattern recognition techniques used in studying zonation are very sensitive to the allocation of samples along a gradient and to gaps in the sampling regime (GAUCH, 1982; CARNEYet al., 1983). Additionally, photographs provide a more accurate assessment of benthic megafaunal densities than the more traditional trawling technique (GRASSt~ et al., 1975; I-L~DPaCHet al., 1975), survey firmly attached organisms, can be used in regions of high relief, and provide information about physical characteristics of the environment (RowE, 1971). Uz~,rN et al. (1977) found that photographic techniques underestimated densities of benthopelagic species, probably due to a photonegative response of these taxa. However, my experience with submersibles and camera sleds indicates that although some taxa avoid the vehicle, others are attracted to it. Additionally, the characteristic puffs of sediment, indicating a recently departed organism, were rarely encountered in the photographs: when they were, the organism responsible for the disturbance usually was also photographed.

Laboratory analysis Each slide was systematically analysed for area viewed (me), surficial geology, topography, and species occurrences and abundance. The number of square meters viewed was calculated by photographing a grid in air and correcting for the refractive index of seawater. Species identification from photographs is tenative, and it was virtually impossible to identify every organism observed on the slides. Each organism was identified as specifically as possible. More than 95% of the organisms observed could be assigned to a species category. Species designations for most of the categories of dominant taxa were determined by collecting "voucher" specimens with trawls, dredges and submersibles. However, some lumping was unavoidable because species differences between congeners frequently could not be discerned in photographs. The only common species where this was a problem were the rattails Nezumia aequalis and N. bairdi, which were lumped as Nezumia spp.; the eels Synaphobranchua" affinis and S. kaupi, which were lumped as Synaphobranchus spp.; and cerianthid anemones. Differences between the congeneric fish are slight, and they also have been pooled by previous investigators using trawl samples. The problem in distinguishing between species of cerianthids is not unique to the photographic method used in this study (Rowe and MENZIES, 1969; GRASSt.E et al. 1975; SHEPARDet al., 1986). Identification of cerianthids is exceptionally difficult even with specimens in hand (K. SEBEr~S, personal communication), and the deep-water cerianthids occurring in this region have not been described (SEBENS, 1985; SHEPARD et al., 1986). Where this inability to differentiate between congeners affected the results, alternative interpretations are discussed. All recognizable taxa were counted, but some were omitted from subsequent data analyses. All strictly planktonic organisms, such as medusae and salps, and the protozoan xenophyophores were omitted. Worm tubes, with the exception of Hyalinoecia artifex, also were not included because it was impossible to determine if they were inhabited. The only H. artifex counted were individuals that showed recent movement, by leaving trails, or actually had part of the organism exposed. General taxanomic categories (i.e. anemone, sponge, fish) were retained only for abundance estimates. Statistical analyses To facilitate inter-area comparisons, each tow was divided into 100 m depth intervals. Summary statistics of mean depth, dominant substrate types and the abundance of each

Variation in megafaunalassemblages

41

species were generated for each depth interval. The depth intervals from each of the tows were then treated as separate samples. To reduce discrepancies between samples with unequal areal coverage, abundances were .standardized to number per 100 m 2. Additional analyses, not presented here, conducted on 30 picture intervals showed that the observed faunal patterns were not biased by the artificial division into 100 m intervals or by uneven areal coverage. Two multivariate pattern recognition techniques, classification and ordination, were used to assess faunal changes with depth and geographic location. For both of these analyses, the original data matrix of 161 species in 159 samples was reduced to 68 species by retaining only those taxa that were present in abundances of 50 or more individuals in the entire data set. Classification analysis consisted of a pairwise comparison of the species composition of all samples, using the percent similarity coefficient (Wm'rrAr,ER and FAIRBANKS,1958) PS = 100(1.0-0.52 [P~a-Pibl)= 100 min 2 (p,~, pit,), where p/~ is the fraction of species i in sample a and P~b is the same for sample b. This coefficient is equivalent to the sum of the lesser proportion of each species common to both samples and provides a direct measure of the similarity in their species composition. Unweighted pair-group clustering was used to group samples with similar species composition (SOgAL and SNEArrl, 1963). This strategy has the advantage of being reasonably conservative in clustering intensity, while avoiding the chaining effect (successive samples fusing to a group one at a time, rather than forming a new group) of less intense strategies. A problem with use of classification analysis to examine species change along a gradient is that it tends to impose discontinuities even if a continuum of change exists. In addition, the one-dimensionality of a dendrogram focuses on inter-group resemblances, without adequately retaining the finer inter-sample relationships. This can be understood best if one visualizes a dendrogram as a three-dimensional "mobile" that becomes distorted when flattened into a two-dimensional space. To overcome these disadvantages, the data also were examined with reciprocal averaging ordination (HILL, 1973, 1974). This eigenvector technique has been shown to be particularly useful where species turnover along a gradient is high, such as along a long transect (WARWlCg and GAGE, 1975) or over a large depth range (WENNERand BOESOi, 1979). It is also less susceptible to effects of sampling error and sample clusters than the related principal components technique (FAsHAM, 1977). One final advantage of reciprocal averaging is that it simultaneously ordinates samples and species in the same space, and thus facilitates interpretation of the placement of samples along the gradient in terms of their species composition. RESULTS

A total of 284,692 organisms were seen on the 94,380 m 2 of sea floor analysed for this study. The depths surveyed were from 340 to 2100 m on the westernmost transect (WT), 291 to 2035 m on the slope at the western edge of Georges Bank (WS), 569 to 2045 m on the slope slightly to the east (ES) of WS, and 242 to 2394 m on the transect near the U.S.-Canadian Boundary (USB). As mentioned earlier, obtaining coverage above the 300 m isobath was usually impossible because of the danger of tangling lobster traps.

42

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Geological setting The four locations differed considerably in slope topography and surficial geology (Fig. 2). Overall declivity was gentle at two locations (WT and ES) and steep at the other two (WS and USB). The slope at all locations consisted of relatively gradual declining upper and lower sections (above 500-700 m and below 1600 m), separated by a substantially steeper middle section. For clarity in the remainder of this paper, the gradually declining sections are considered the upper and lower slopes, respectively, and the steep section the middle slope. Topographic differences between the locations were most pronounced on the steep middle slope. At WT declivity gradually increased from 1.7° on the upper slope (between 340 and 700 m), to 3.7 ° and 6.70 (between 700 and 1100 m and between 1100 and 1600 m, respectively) on the middle slope, and abruptly decreased to 2.8 ° (below 1600 m) on the lower slope. At ES the middle slope consisted of two relatively steep sections (4.3 ° between 600 and 800 m, and 7.5 ° between 900 and 1300 m), separated by two flatter sections (2.2 ° between 800 and 900 m, and 3.4 ° between 1300 and 1600 m) that ended in a broad terrace at 1600 m and gave way to an exceptionally flat lower slope (1.8°). WS was characterized by a moderately deep upper slope (5° between 291 and 500 m), and a declivitous middle slope (9.6 ° between 500 and 1575 m) that terminated in a small terrace. Below 1600 m the lower slope progressively flattened to less than 1°. The USB transect exhibited a relatively declivitous topography across the entire slope, with angles of 5.5 ° between 242 and 500 m, 11.8° between 500 and 1600 m and 3.5 ° below 1600 m. The middle slope in this region was interrupted by a small, flat terrace between 1050 and 1100 m. The surficial geology was quite variable on the upper and middle slope along the USB transect. The sea floor above 1300 m in this region was frequently covered by glacial erratics, ranging in size from gravel to boulders, and was occasionally interrupted by lowO--

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43

Variation in megafaunal auemblagcs

refef outcrops. In contrast, the upper and middle slopes at the other three locations were sediment covered. Low-refief outcrops and occasional glacial erratics were found on the lower slope at WT and WS, and a small outcrop was encountered on the middle slope at ES.

Conununity analysis Classification analysis showed groupings of samples to be primarily a function of depth (Fig. 3). Six distinct clusters were formed, with each of the clusters further divided into more coherent groups on the basis of depth and/or location. Within-cluster coherence generally increased with increasing depth, indicating that faunal homogeneity was greater in the deeper regions. The depth limits of the clusters were 200-700 m (1), 5001300 m (2), 700-1200 m (3), 1100-2100 m (4), 1200-1700 m (5), and 1200-2400 m (6). DEPTH (m) WT

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The considerable overlap in the depth li~nits of the clusters frequently reflected differences between geographic locations, and clusters usually did not overlap within a location. One of the clusters (3) and several of the groups (la, lc and 2a) consisted entirely of depth intervals from USB, and reflected differences in some of the dominant taxa found at that location. The three outlier areas from WT (represented by the bottom two legs of the dendrogram) resulted from very few organisms being seen in the shallower interval and several dense aggregations of a small holothurian, Peniagonesp., being seen in the two deeper intervals. The other taxa seen in these intervals were typical of their respective depths. The large depth range encompassed by cluster 4 may have resulted from lumping two species of cerianthid anemones. Cerianthids totally dominated the fauna in each of the depth intervals within this cluster. The depth distribution of cerianthids was bimodal, with a sparse population peaking between 1100 and 1300 m and an abundant population peaking between 1800 and 2000 m, suggesting that two separate species may be present. Because the ranges of the populations overlapped, and they did not exhibit any pronounced anatomical or habitat differences, it was impossible to separate them. However, they were retained in the analyses because they represented such a dominant component of the fauna (23% of all the individuals seen). If the cerianthids observed in this study do represent two species, the clustering by depth would be augmented, and the deeper intervals in cluster 4 would form a separate group with a high affinity to cluster 6. The faunal boundaries defined by these clusters differed slightly among locations: 700, 1200-1300, 1400-1500 and 1600-1700 m at WT; 500, 1200, 1300 and 1600 m at WS; 600, 1100, 1300, 1500-1600 and 1900 m at ES; and 500-700, 1200 and 1300 m at USB. Differences in the depths of faunal boundaries among locations frequently reflected topographic differences. At the three western locations the faunal boundaries between 500 and 700 m and around 1600 m coincided with major changes in slope declivity. Considerable species overlap between adjacent clusters, and the tighter groupings by depth within clusters, indicate that species change was continuous across the depth gradient. With this in mind, the clusters should be viewed as representing regions of lesser species turnover, separated by regions of slightly greater turnover (boundaries). Ordination permits examination of relative rates of faunal change along a gradient. Arrangement of the samples by ordination resulted in a curvilinear array of points aligned primarily by depth and, to a lesser degree, by location (Fig. 4). To facilitate comparisons with the classification analysis, symbols for the clusters also are shown in this diagram. The first axis accounted for 33% of the total variance. This axis clearly represented species turnover along much of the depth gradient, with sample scores on this axis being highly correlated with depth (r = --0.945). Upper- and lower-slope samples occupied the extremes of the first axis, and middle slope samples were stretched out between them. A Iocational difference also was reflected on this axis: values on axis 1 for most of the samples from the shoaler portion of the middle slope at USB (cluster 3) were lower than those from comparable depths at the other three locations (cluster 2). The second axis represented depth and locality differences on the upper slope: shallow and USB intervals had high values and deeper intervals at the three western locations had low values. The third axis separated the flat upper and lower slope (high values) from the steep middle slope (low values). The fourth axis further represented geographic variation at mid-slope depths by separating the USB middle-slope samples from the other middleslope samples (Fig. 5). The coenocline represented by the ordination model depicts a

Variation in megafaunal assemblages

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pattern of continuous species turned along the depth gradient, with a pronounced shift at the upper/middle slope boundary and very rapid change across the lower portion of the middle slope. If species turnover occurred at a constant rate across the slope, the relationship of depth with score on the first axis would be linear. Conversely, if the fauna were arranged along the depth gradient as homogeneous, discretely bordered zones, this relationship would approximate a step function. Separate plots of score on the first axis vs mean depth show that the pattern of species turnover along the depth gradient varied among geographic locations (Fig. 6). A general pattern of abrupt species turnover in steep regions and gradual turnover in flat regions was found. One extreme of this pattern was seen at the very steep USB location, which showed exceptionally abrupt turnover above 1000 m. In addition to steep topography, this high turnover also reflected the environmental heterogeneity, provided by the variety of substrate types, found in this area. Species turnover across the middle slope at the other three locations was gradual and continuous at WT, slightly greater and followed by a faunal shift between 1100 and 1300 m at WS, and lesser, followed by a more pronounced shift at 1100 m at ES. Relative to the overall gradient represented by the first axis, the fauna on the upper and lower slope was homogeneous at all four locations. The varying scores of the upper slope samples on the second axis indicate that this apparent homogeneity is partially an artifact

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of the analysis, which tends to compress the ends of the gradient and Om.oa, 1986).

(GAUCH,1982;

Faunal zones

A schematic diagram of cluster designations for depth intervals presents a clearer picture of faunal zonation among the four locations (Fig. 7). In several instances (mainly the outliers) minor changes in cluster designation based on the ordination results were made. Four faunal zones (an upper slope zone, an upper-middle slope zone, a lower slope zone, and a less defined transitional zone) were identified. At each geographic location, these four zones were further subdivided into shallow and deep regions, each representing areas of high species similarity. Additional subdivisions within zones represented faunal differences between locations. The zonation pattern was similar at the three western locations, and quite different at USB. This difference was most noticeable on the middle slope where a separate cluster (3) replaced most of the upper-middle slope zone, the transitional zone was compressed to a 100 m depth interval, and the lower slope zone emerged onto the middle slope. This difference between the three western locations and USB also was reflected in the pattern of density with depth (Fig. 8). The three western locations had moderate to high densities on the upper slope, uniformly low densities on the middle slope, and high densities on the lower slope. Abrupt changes in faunal density occurred at the boundaries between the upper and upper-middle slope zones, and the lower-middle and lower slope zones. In contrast, faunal densities were moderate to high on the middle slope at USB, and the boundaries between zones were not marked by sharp changes in density. Several less pronounced differences among the locations also were noted: densities on the upper slope were highest at WT and densities on the lower slope were highest at the two steep locations (WS and USB). Depth (m)

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Fig. 8. Density with depth of total megafauna (top line) and the nine most abundant taxa (filled arcas). Density per 1 0 0 m interval is plotted at the 5 0 m mark. Vertical lines represent faunal boundaries defined by classification ( - - - boundaries between the upper-middle and middle-lower slope ...... boundary between the upper- and Iower-middlc slope and at the ES location, an additional faunal boundary found on the Iowcr slope).

Dominance in the megafauna was very marked, with the moderate to high densities on the upper and lower slope, and on the middle USB slope, largely reflecting the depth distributions of nine very abundant taxa (Fig. 8). Two solitary scleractinians, Dasmosmilia lymani and Flabellum alabastrum, and the quill worm Hyalinoecia artifex, dominated the fauna on the upper slope. The two scleractinians were not found at all locations, D. lymani was absent from USB and F. alabastrum was absent from WS. Three taxa, the ophiurid Ophiom~ium lymani, a cerianthid and the sea pen Distichoptilum gracile, dominated the fauna on the lower slope at all four locations. An additional moderately abundant species, the urchin Echinus affinis, was found only on the lower slope at WT and WS. Two alcyonarians, Acanella arbuscula and Eunephthya florida, which dominated the fauna on the shoaler portion of the middle slope, were found only at USB. Among-location differences in the depth limits of zones largely reflected differences in the depth distributions of several of these taxa. To examine the faunal zones in more detail, physical characteristics and density of dominant taxa in each of the faunal zones, and their subdivisions, are summarized in Table 1. The degree of species overlap indicates that the zones represented regions of lesser faunal change separated by regions of greater faunal change, rather than discrete faunal assemblages. The lower boundary of the upper slope zone (cluster 1) largely reflected the lower limit of D. lymani at WT (700 m), WS (500 m), and ES (600 m), and

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F. alabastrum and H. artifex at USB (500-700 m). A less-pronounced faunal boundary was observed at 400 m at the three locations that had coverage above 500 m (Fig. 7). This intermediate boundary coincided with a shift in dominance from F. a/abastrum to D. lyman/at WT (lb--ld), from Cerianthus borealis and Bolocera tudiae to D. lyrnani at WS (1-1d), and from Actinauge longicornis to F. alabastrum and H. artifex at USB (la or b-lc). None of these taxa extended onto the middle slope in appreciable abundance. In contrast, several of the taxa inhabiting the upper--middle slope zone did extend onto the upper slope, but their densities were low in comparison to the more abundant upper slope taxa. The upper-middle slope zone was inhabited primarily by sparse populations of the red crab Geryon quinqueidens and several fish, Synaphobranchus spp., Nezumia spp., Phycis chesteri and Glyptocephalus cynoglossus (duster 2). Species differences between the shallow and deep regions of this zone largely reflected higher abundances of G. quinqueidens in the shallow portion (2b). Comparable abundances of this crab were seen at the WT location, but the seaward extension of the more abundant D. lymani masked this transition (from ld to 2c). While supporting the same fauna found at the three other locations, the USB upper-middle slope zone also supported a sparse population of Amphilimna olivacea (2a), and dense populations of A. arbuscula, E. florida, Anthomastus agassizii, and a stalked crinoid (cluster 3). This difference in the faunal constituents of the upper-middle slope zone could be attributed partly to the numerous glacial erratics and outcrops found in the USB area, because two of these species, E. florida and A. agassizii, require hard-substrate attachment sites. The fauna inhabiting the transitional zone consisted of sparse overlapping populations of middle and lower slope taxa. Although several of the fish characteristic of the middle slope zone extended down into this region, the fauna was dominated by sparse populations of a cerianthid in the shallower portion (cluster 4) and D. gracile in the deeper portion (cluster 5). The compression of this transitional zone at USB reflected the emergence of the lower slope zone (cluster 6). At all four locations the upper boundary of the lower slope zone was largely determined by the upper limit of O. lymani. This ophiuroid dominated the fauna throughout the lower slope zone, but shifts in the relative abundance of two other taxa also were observed. The shallower portion at all locations was dominated totally by O. lymani (6a), which was joined by high abundances of a cerianthid in the deeper portion (6b). An additional faunal shift was observed at the two western locations, where moderate abundances of E. affinis were observed below 1800 m (6c). Moderate abundances of O. lymani extended to the limits of the coverage at three of the locations (2100 m at W'F and WS, and 2400 m at USB), but only to 1900 m at ES. Its absence below 1900 m at this location resulted in a shift back to cluster 4 in the deeper intervals. As mentioned earlier, the apparent affinity between the shallower and deeper areas in this cluster possibly reflects the difficulty in differentiating congeneric cerianthid species. The faunal heterogeneity of the upper and middle slope at the USB location, as evidenced by differences between comparable depth intervals within this region, appeared to reflect patchiness in both geological characteristics and in faunal distributions. Substrate differences between camera tows in this region could account for only some of the observed patchiness. DISCUSSION

The photographic survey reported here indicates that megafaunal assemblages on the continental slope south of New England vary with both depth and geographic location.

Variation in megafatmalmemblages

51

Faunal patterns were very similar among the three western locations (WT, WS and ES) and quite different at the eastern location (USB). Four faunal zones were identified at each of the locations studied: an upper slope zone, an upper-middle slope zone, a transitional zone, and a lower slope zone. The transitional zone, which was located on the lower portion of the middle slope, represents a region of overlapping middle and lower slope faunas. Species turnover was continuous along the depth gradient, with zones representing regions of lesser change, rather than discrete species assemblages, separated by regions of greater change (boundaries). The boundaries between the upper and upper-middle slope zones and between the transitional and lower slope zones were usually marked by abrupt shifts in faunal density and slope declivity. Rate of species turnover varied with topography; turnover was lesser in gradually declining regions and greater in steep regions. Depths of boundaries between zones, several of the dominate faunal constituents of zones, and the pattern of species turnover varied between geographic locations. These faunal differences mirrored topographic and geologic differences among the locations, which ranged from a gently inclined sediment-covered slope at the westernmost location (WT) to a very steep, rocky slope at the eastern edge of Georges Bank (USB). Boundaries between zones occurred at 700, 1200-1300 and 1600-1700 m at WT; 500, 1200 and 1600 m at WS; 600, 1100, 1500-1600 and 1900 m at ES; and 500-700, 1200 and 1300 m at USB. Additional, less pronounced faunal boundaries also occurred at each of the locations. The upper two boundaries are similar to those found by HAEDRICHef tI[. (1980) in a previous study of megafaunal populations on the continental slope of this area. Using data collected from trawls within the depth range covered by the present study, they found boundaries at 650, 1300 and 20(}0-2100 m. Comparable boundaries have also been found by SHEPARDet al. (1986) for cerianthids off Georges Bank (500, 1000 and 1600 m), by WEN~ER and BOESCtt (1979) for decapod crustaceans off the midAtlantic states (200 and 1200 m), by DAY and PEARCY(1968) for fish off Oregon (400 and 1200 m), by P~RC'Y et al. (1982) for fish off Oregon and Washington (400-700 m and 1900-2200 m), and by OtrrA (1983) for megafauna off Japan (400, 700, 1200 and 17002000 m). The near universality of boundaries between 400 and 700 m and around 1200 m suggests that changes in important controlling parameters are associated with these depths. The results of HAEDRtCHet al. (1980), who collected samples between Hudson Canyon and the w ' r location, are the most comparable to the present study. They identified four faunal zones within the depth range covered by the present study: an upper slope zone (283-650 m), a middle slope zone (650-1290 m), a lower slope zone (1380-1947 m), and a transitional slope to rise zone (2116-2481 m). Although the upper two boundaries found in both studies correspond, Haedrich et al. did not find the additional boundary around 1600 m. This disparity partially reflects differences in the taxa emphasized by the two survey techniques. Of the four common taxa found on the lower slope at WT, two, the cerianthid anemone and Distichopfilum gracile, were not reported by Haedrich et al. These two species would not be sampled reliably by a trawl because they are firmly attached to the sea floor and extend only a few centimeters above the sediment. Ophiomusium lymani, which was only found in appreciable abundances below 1600 m at w'r, was the dominant species in both the lower slope and transitional slope to rise zones reported by Haedrich et al. This disparity in the upper limit of O. lymani between the photographic and trawl surveys may be explained by the results of SOtOENER(1968), who reported that mainly juveniles of this species were found in epibenthic sled samples from

52

B.

t-~cr~a

middle slope depths in this area. Because of their small size (<5 mm disk diameter), juveniles would not readily be discerned on photographs, but could be collected by trawl. This difference would explain the absence of a faunal boundary at 1600 m in the data reported by Haedrich et al.; unfortunately, they did not report the size of O. lymani collected in their samples. GRASSLEet aL (1975) also reported that appreciable abundances of O. lymani were seen in photographs only below 1550 m. I believe that the faunal boundary found around 1600 m in the present study is valid, because the juveniles further up the slope do not appear to be a viable reproducing population (GAGE, 1982). Despite differences in the top ranking taxa of the upper slope zone, there was good correspondence in the depth of the lower limit of this zone. In the present study, the dominant taxa found on the upper slope at the WT location were Dasmosmilia lymani, Hyalinoecia artifex and Flabellum alabastrum. Of these three species, only H. artifex was reported by HAEORZCHet al. (1980), who ranked it as the third most abundant member of their upper slope assemblage. In both studies, the same three taxa, Synaphobranchus spp., Geryon quinquedens and Nezumia spp., ranked as top dominants in the middle slope zone. The good correspondence of the depths of these boundaries, despite differences in some of the dominant taxa, suggests that the boundaries are real and apply to the megafauna as a whole. The WT location was approximately 40 km west of a site where megafaunal populations at 500, 1000, 1300, 1500 and 1800 m had previously been photographed during 10 Alvin dives (GgAsSLE et al., 1975). Faunal densities and dominant taxa found in the two studies are very similar (Table 2). Grassle et al. found a similar pattern of low densities at middle slope depths (1000, 1350 and 1500 m) and high densities at lower slope depths (1800 m). The photographs in that study were taken with Alvin's external bow camera, which was mounted approximately 2 m above the sea floor and illuminated an area of approximately 9 m 2. The greater resolution afforded by the lower camera elevation used in the present study may account for the higher densities found at the 500 m location. The scleractinian D. lymani, which dominated the fauna at 500 m at WT, was very small and probably would not have shown up in their photographs. The observed megafaunal zonation patterns are undoubtedly related to a variety of Table 2. Comparison of megafaunal densities observed at WT with those from GRASSL~ et al. (1975) for comparable depth intervals. Densities from both studies have been rounded and standardized to number of individuals per 100 m z. Data from the present study are in bold type Depth interval (m)

495-499 395--499

Hyalinoecia artifex

146 104-149 2 2--4 5 0

Geryon quinquidens Synaphobranchus spp. Ccrianthid

992-1000 900-999

1298-1399 1300-1399

1465-1550 1400-1599

1778-1830 1700-1899

0.2 0.1 1.5 5-7 0 0.1

O.1 2-4 0 6-10

1 0-1 0 2,-.-6 63.6 2 0.5 0

0--0.3 0-0.8 47--81 93-136 172-245 32,--291 26 0-22

3 9--12

17 16-20

71 14-41

246--355 168-550

Ophiomusium lymani Echinua affinis Total fauna

155 385-478

Variation in megafaunalassemblages

53

factors. Some of the zonation may reflect changes in food resources that are at least partially mediated by topography. This would be particularly relevant to the uppermiddle slope (500-700 m) and transition-lower slope (around 1600 m) boundaries that were marked by abrupt shifts in faunal density and trophic composition, since they also coincided with changes in slope declivity. The higher faunal densities on the upper and lower slope argue for increased food availability in these regions, while the uniformly low densities on the middle slope argue for decreased food availability in this region. The moderate to high densities on the upper slope primarily reflected filter feeders (D. lymani and F. alabastrum), the low densities on the middle slope mainly reflected carnivore scavengers in the shallower section and suspension feeders in the deeper section, and the high densities on the lower slope reflected both suspension (D. gracile and the cerianthid anemone) and deposit feeders (O. lymani and E. affini$). This pattern would argue for higher particle fluxes on the upper and lower slope, than on the middle slope, and greater nutrient value of the sediments on the lower slope. Evidence from the SEEP study suggests that current regimes and particle fluxes are influenced by topography. CSANADYet al. (1988) found higher current intensities, and more frequent resuspension events, on the upper and lower slope than on the middle slope. The authors suggest that the steepness of the middle slope "insulates" it from impingement by topographic waves, which are thought to produce the strongest nearbottom currents on the slope. The strong currents on the upper and lower slope would provide a greater flux Of particulate food to the fauna inhabiting those regions. The authors also suggest that the lack of strong currents on the middle slope results in a broad depositional band. Sediment grain-size data collected during the present study support these findings: the finest-textured sediments were found on the middle slope (1250 m), and coarser sediments were found on the upper (250 and 550 m) and lower (2100 m) slope (MA¢IOLEKet al., 1987). The USB location was somewhat anomalous in that it had very fine sediment on the lower slope as well as on the middle slope. Evidence for the accumulation of nutrient-rich fine particles on the lower slope is provided by sediment trap results from the SEEP study. Based on the 2'°Pb inventories and Corg/N ratios of material collected in sediment traps, BISCAYEel al., (1988) concluded that in addition to vertical flux of particles from near-surface waters, the lower slope and upper rise received both fresh biogenic particles and resuspended sediment from upslope. Additionally, the freshest particles (based on the lowest Corg/N ratio) were consistently found at the base of the slope. The authors suggest that a likely mechanism for this downslope transport is the weak net downslope flow in the bottom boundary layer (>7 m and <50 m) reported by BLrrMAN(1988). BISeAYEet al. argue that the freshest particles also would be the lightest and thus would be preferentially transported downslope by the weak cross-slope current, while the heavier resuspended particles would be deposited on the middle slope. The depth distributions of several of the dominant taxa also support the premise that a topographically mediated food gradient may be responsible for some of the observed zonation. The lower limit of the dominant upper slope species, D. lymani (700 m at WT, 500 m at WS, and 600 m at ES), corresponds to the transition between the flatter upper slope and the steeper middle slope. Relative declivity, rather than absolute slope angle, appears to be the major factor determining this organism's distribution, because the inclination of the upper slope at WS (5°) is greater than that of the shallower middle slope at WT and ES (3.7° and 4.3 °, respectively). Depth per se also does not appear to be

54

B . ~

the main determinant of the distribution of O. lyman/on the lower slope. At the three western locations, the upper limit and highest densities of this brittle star were found just seaward of the base of the middle slope, with densities decreasing across the lower slope. This distribution was most noticeable at the gently sloping ES location, where the lower limit of O. lymani was encountered at 1900 m. In contrast, this brittle star was found in appreciable abundances to at least 2100 m at WT and WS and 2400 m at USB. These distributions could be explained by the preferential accumulation of fine particulates at the base of steep slopes and the decrease of accumulation with distance from the slope. Greater accumulations of fine particulates at the base of very steep slopes also would explain the higher densities of O. lymani at WS and USB. In contrast, densities of the cerianthid anemone were highest on the flatter portions of the lower slope, where the currents would also be higher. Faunal differences between the three western locations and USB were only partly attributable to the availability of hard substrate at the USB location. With the exception of D. lymani, the dominant taxa on the upper slope were the same. The absence of this coral from the USB location is not surprising, because its reported northern limit is Georges Bank (CAIRNS, 1981). The high faunal densities found on the middle slope at the USB location predominantly reflected four sessile suspension feeders in the shoaler portion and the emergence of O. lymani onto the deeper portion. Only two of the four dominant sessile taxa, Eunephthya florida and Anthomastus agassizii, were restricted to the glacial erratics found at this location. The other two taxa, Acanella arbuscula and a stalked crinoid, were not limited to hard substrates. Additionally, the eastern edge of Georges Bank is not the southern limit of any of these taxa, because all four were abundant in Lydonia Canyon and at other locations farther south (HECKERel al., 1983). The exposure of ice-rafted, glacial debris at the USB location indicates that currents in this region are strong enough to prevent sediment accumulation. Similar' exposures of glacial debris in the canyons off Georges Bank have been ascribed to strong currents ( V ^ ~ " n ~ E et al., 1980; BUTMAN, 1986). Additional evidence for the presence of stronger currents at the USB location is that mid-slope samples from this region had a coarser sediment texture than mid-slope samples from the WT location (MACIOLEKet al., 1987). Enhanced current intensities would favor sessile suspension feeders by providing them with a greater flux of particulate food. The emergence of adult O. lymani onto the middle slope at USB is not as readily explained. At the other three locations the upper limit of adults coincided with the base of the middle slope (1500-1700 m). GA~s (1982), in a re-examination of SCHO~ER'S (1968) data, concluded that the upper limit of adult O. lyrnaniin the western North Atlantic reflected high mortality on the middle slope. He suggested that the high adult mortality on the middle slope results from either an insufficient food supply or increased predation. The upward extension of adult O. lymani in the USB region does not appear to be related to a decrease in the number of predators, since fish abundances and species composition were similar at all four geographic locations. However, alternative explanations can be entertained. If predation controls the upper limit of O. lymani, then the environmental heterogeneity provided by the many glacial erratics found in the shallower region of the USB area may afford refuges for this species. However, refuges from predation would not explain the high densities on the deeper portion of the middle slope, where few glacial erratics were found. On the other hand, if the upper limit of adults is controlled by food availability, then more nutrients must be reaching the sea floor in this

vm.tioe in eL-g~.enalme,-Uages

55

region, as a result of either increased resnspension events or greater downslope transport. The sediment on the lower slope at the USB location was much freer than at several locations to the west (MAaotzx et al., 1987), indicating that downslope transport may be greater, or current intensifies may be less, at this location. Unfortunately, not enough ancillary data are available to assess the relative merits of these hypotheses. Although the distributions of sessile or relatively sedentary taxa appear to be largely controlled by a topographically mediated food gradient, a mechanism responsible for the rapid species turnover on the middle slope is not as apparent. REx (1977) presented the hypothesis that zonation may be partly a function of trophic level, with taxa in higher trophic levels being more stenobathic than taxa in lower trophic levels. HAEDtUCttet al. (1980) argued that this hypothesis must be modified to accommodate differences in selectivity and motility, with mobile generalists being the most eurybathic. The data available concerning the food habits of bathyal and abyssal taxa suggest that they are not particularly selective in their choice of food items or prey (ScXO~R and Rowe, 1970; C A t ~ , 1972; PEARCYand AMm.ER, 1974; McLeU.EN, 1977; SEDeERRYand MUSlCK,1978; MAUCm.nCEand GORDON, 1983a,b; PEARSONand G^OE, 1984). Following the argument advanced by Haedrich et al. would predict that fish would show the widest depth ranges. The data from the present study do not support this premise. The depth ranges of the 24 species that were abundant enough to give reliable estimates and were not restricted to hard substrate appeared to be independent of trophic level and motility. Sessile filter feeders (corals), limitedly mobile deposit feeders (echinoderms), and very mobile carnivores (fish) all had roughly comparable depth ranges. Depth ranges were narrow on the upper slope and broader on the lower slope. Additionally, the depth ranges of most lower slope taxa were considerably broader at USB than at the three western locations, reflecting an extension of their upper limit. Possible explanations for broader depth ranges deeper on the slope are greater environmental stability of deeper habitats; increased generalism in a nutrient-poor environment; and less enzymatic sensitivity at depths below 700 m, as has been suggested by SOMEROet al. (1983). The extension of the upper limit of lower slope taxa at USB suggests that depth ranges of bathyal taxa are variable and may reflect physical differences in the environment, rather than physiological constraints. MENZtES et al. (1973) present evidence for a recurrent set of zones found world-wide, with the specifics of zones varying among geographic locations. However, few studies have addressed the horizontal variability of these zones within a geographic area. MARg~e and MUSlCK(1974) found gradual changes in fish populations along the 900 m isobath in the Mid-Atlantic Bight. The data presented here suggest that the concept of megafaunal zones extending as continuous narrow bands along continental margins needs to be modified. Horizontal changes in both the faunal constituents and depths of boundaries of zones can be quite pronounced. These differences may be related to horizontal variability in physical parameters within a geographic area. The data suggest that interpreting species composition of samples from different localities in light o f a generalized gradient examines environmental parameters at a scale that may have little relevance to the biology of the populations. Finer-scale resolution of the environment can provide important clues to some of the mechanisms responsible for zonation. Acknowled~l

thank all the people, particularly I. Bitte and P. R. Gibson, who have worked on various aspects of these projects over the years. The following people generously provided aid in identifying some of the dominant t a n : S. Cairns (sderactinians), M. Downey (starfish), D. Pawson (echinoids and

56

B. HEC~R

holothuroids), F. Bayer and D. Opreska (alcyonarians), K. Sulak (fish), K. Sebens (anemones) and A. Williams (crustaceans). My thanks also go to J. Gage, M. Rex, and two anonymous reviewers for many helpful comments on the manuscript. This work was supported by the U.S. Department of the Interior, Minerals Management Service Contract nos 14-12-0001-29178 to Lamont and 14-12-30064 to Battelle Memorial Institute. REFERENCES BtSCAYE P. E., R. F. ANDERSONand B. L. DECK (1988) Fluxes of particles and constituents to the eastern United States continental slope and rise: SEEPml. Continental Shelf Research, 8, 855-904. BUTMA~B. (1986) North Atlantic Slope and Canyon Study. Final Report to U.S. Department of the Interior, Minerals Management Service, Interagency Agreement IA14-12-0001-30180,563 pp. BU'rMAN B. (1988) Downslope Eulerian mean flow associated with high-frequency current fluctuations observed on the outer continental shelf and slope" along the northeastern United States continental margin: implications for sediment transport. Continental Shelf Research, g, 811-840. CAIRNSS. D. (1981) Marine flora and fauna of the northeastern United States, Cnidaria: Seleractinia. U.S. Dept. Commer. NOAA Tech. Rep. National Marine Fisheries Service. CAREY A.G. (1972) Food sources of sublittoral bathyl and abyssal asteroids in the northeast Pacific Ocean. Ophelia, 10. 35-47. CARNEy R. S., R. L. HAEDRIC'Hand G. T. ROWE (1983) Zonation of fauna in the deep sea. In: Deep-sea biology, Thesea, Vol. 8, G. T. RoWE, editor, Wiley-Interscience, New York, pp. 371-398. CsAN/~oYG. T., J. H. CURCmLLand B. BUTMAN(1988) Near bottom currents over the continentalslope in the Mid-Atlantic Bight. Continental Shelf Research, 8, 653-672. D^Y D. S. and W. G. PEARC'r(1968) Species associations of benthic fishes on the continental shelf and slope off Oregon. Journal of the Fisheries Research Board of Canada, 25, 2665-2675. FASHAMM. J. R. (1977) A comparison of nonmetric multidimensional scaling, principal components and reciprocal averaging for the ordination of simulated coenoclines and cocnoplanes. Ecology, 58.55 i-561. GAGEJ. D. (1982) Age structure in populations of the deep-sea brittle star Ophiomusiura lymani: a regional comparison. Deep.Sea Research. 29, 1565-1586. G^uct! H. G. (1982) Multivariate analysis in community ecology. Cambridge University Press, Cambridge, U.K., 298 pp. GRASSLEJ. F., H. L. SANDERS.R. R. HF~SSLER,G. T. RoWEand T. MCLELLAN(1975) Pattern and zonation: a study of the bathyl megafauna using the research submersible, Alvin. Deep.Sea Research, 22, 457-481. GRASSLEJ. F., H. L. SANDERSand W. K. SMITtl (1979) Faunal changes with depth in the deep-sea benthos (9). Ambio Special Report, 6, 47--50. HAEDRICl! R. L., G. T. ROWEand P. T. POLLONI(1975) Zonation and faunal composition of epibenthic populations on the continental slope south of New England. Journal of Marine Research, 33, 191-212. HAEDRICllR. L., G. T. RoWEand P. T. POLLONI(1980) The megabenthic fauna in the deep sea south of New England, USA. Marine Biology, 57, 165--179. HECKERB., D. T. LOGAN,F. E. G^NDARILLASand P. R. GIBSON(1983) Megafaunal assemblages in Lydonia Canyon, Baltimore Canyon, and selected slope areas. In: Canyon and slope processes study, Vol. 3, Final Report for U.S. Department of the Interior, Minerals Management Service Contract 14-12-001-29178, pp. 1-140. HILL M. O. (1973) Reciprocal averaging: an eigenvector method of ordination. Journal of Ecology, 61, 237-249. HILL M. O. (1974) Correspondence analysis: a neglected multivariate method. Journal of the Royal Statistical Society, Series C, 23, 340--354. K,~KEL N. C. and L. Onx~cl (1986) Applying metric and nonmetric multidimensional scaling to ecological studies: some new results. Ecology, 67, 919-928. MAClOt.EKN., J. F. GRASSLE,B. HECTOR,B. BROWN,J. A. BLARE,P. D. BOEHM,R. PErmECCA,S. Du~'v, E. BAI'TlSTEand R. E. RUFF(1987) Study of biological processes on the U.S. North Atlantic slope and rise. Final Report for U.S. Department of the Interior, Minerals Management Service, Contract 14-1230064, 362 pp. plus appendices. MARK~ D. F. and J. A. MusiCK (1974) Benthic-slope fishes found at 900 m depth along a transect in the Western N. Atlantic Ocean. Marine Biology, 26, 225-233. MAUCHLINEJ. and J. D. M. GORDON(19&3a) Diets of the sharks and chimaeroids of the RockaU Trough, northeastern Atlantic Ocean. Marine Biology, 75, 269-278. MAUCHLn~J. and J. D. M. GORDON(1983b) Diets of clupeoid, stomiatuid and salmonoid fish of the Rockall Trough, northeastern Atlantic Ocean. Marine Biology, 77, 67-78. McLELLAN T. (1977) Feeding strategies of the macrourids. Deep-Sea Research, 24, 1019-1036. M~rZIES R. J., R. Y. GEORGEand G. T. RoWE (1973) Abyssal environment and ecology of the world oceans. John Wiley, New York, 488 pp.

Variation in megafaunal assemblages

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