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The role of biologically produced habitat heterogeneity in deep-sea diversity maintenance
Deep-Sea Research, Vol. 30, No. 12A, pp. 1235 to 1245, 1983. Printed in Great Britain.
The
0198-0149/83 $3.00 + 0.00 © 1983 Pergamon Press Ltd.
role of biologically produced habitat heterogeneity in deep-sea diversity maintenance DAVID THISTLE*
(Received lO January 1983; accepted 11 February 1983;final revision received 10 May 1983) Abstraet--A model in which biologically generated habitat heterogeneity plays a leading role has been proposed to explain the relatively high diversity of the deep sea: as the rates of physical and biological disturbance decrease with depth the habitat heterogeneity created by organisms becomes increasingly available to other organisms for habitat partitioning or as prey refuges, allowing larger numbers of species to be accommodated locally. The theory was tested by comparing the level of association between organism-generated habitat heterogeneity and harpacticoid copepod species' distributions from two deep-sea sites. The expectation under the model that the site with the greater degree of association would have the greater diversity was not met.
INTRODUCTION
SEVERAL taxa are more diverse in deep-sea soft bottoms than in similar shallow-water locations, e.g., polychaetes and bivalves (SANDERS, 1968), foraminiferans (BUZAS and GIBSON, 1969), cumaceans (JONES and SANDERS, 1972), harpacticoid copepods (COULL, 1972; THISTLE, 1978), polychaetes (HESSLER and JUMARS, 1974), and gastropods (REx, 1981). The cause of the pattern is not yet clear, but a body of theory has arisen to explain it (SANDERS, 1968, 1969; St~3SODKIN and SANDERS, 1969; DAYTON and Hr~SLER, 1972; GRASSLE and SANDERS, 1973; GRAY, 1974; MENOE and SUTHERLAND,1976; REX, 1976; AeELE and WALTERS,1979; HUSTON, 1979). Prominent among the theories is the idea that species of the diverse taxa have highly specialized niches such that competition is minimized, allowing large numbers of similar species to co-occur. A major alternative thesis suggests that species populations are kept so low by predation or disturbance that competition never results in the exclusion of a species, and high diversity can be achieved locally. Several authors have proposed intermediate views, but no theory has achieved wide acceptance. In a different approach, JUMARS(1975a, 1976; JUMARSand GALLAGHER, 1982; JUMARS and ECKMAN, 1983) argued that biologically produced habitat heterogeneity may be an important factor in the maintenance of high diversity in the deep sea. He reasoned that, in shallow water, where physical conditions are relatively energetic and rates of biological disturbance are high, the effects of an organism on its local environment are rapidly obliterated, in general, and cannot be exploited by another organism as a habitat patch. As water depth increases, both physical energy levels and biological activity rates decrease, so the effects on * Department of Oceanography, Florida State University, Tallahassee, FL 32306, U.S.A. 1235
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DAVIDTHISTU~
their immediate environment of increasing numbers of organisms persist long enough to serve as distinct habitat patches. Such biologically produced patches could serve to isolate potentially competing species by providing a large number of distinguishable microhabitats within a community. Alternatively, such a patch structure could decrease the probability of prey extinctions by providing refuges for prey and reducing predator efficiency (M~NGE and StJTHERLAND, 1976). Given the increased longevity of such biologically produced patches as rates of physical and biological activity decrease with depth, this factor could explain, at least in part, the observed correlation of diversity with depth as one moves from shallow water into the deep sea. JUMARS (1976) pointed out that any test of the role of this type of habitat heterogeneity in diversity maintenance faces the difficulty that one must sample habitat patches whose scale is that of a macrofaunal individual. The problem can be circumvented, at least in part, if one studies the effects of organisms that create recoverable markers, e.g., tubes, tests, and mud balls (JU~tARS, 1975C, Fig. 1; "IMISTLE, 1979, Fig. 3). The relative abundances of classes of biogenous structures could then be tested for association with species of a diverse taxon. Clearly, not all biologically produced habitat heterogeneity can be so assessed; in particular, burrows will not be considered. Harpacticoid copepods are an appropriate taxon for such a test. These benthic crustaceans are highly diverse in the deep sea (THISTLE, 1978). They are small (total body length < 1.0 mm), so habitat patches created by macrofauna individuals are relatively large and more likely to act as distinct habitats for them than for larger organisms. In an attempt to test the theory, harpacticoid data and biogenous structure measurements from the deep North Atlantic obtained as part of the High Energy Benthic Boundary Layer Experiment (HEBBLE) preliminary work (NowELL et al., 1982) were used. This region has strong near-bottom currents relative to typical abyssal conditions (RICHARDSONet aL, 1981), but it is unclear whether the near-bottom current regime affects the importance of environmental heterogeneity to harpacticoids. If the theory is correct and if the physical violence is sufficient to make it less likely that biologically produced habitat heterogeneity can be used as habitat patches by harpaeticoids, one would predict lower diversity of the harpacticoid fauna than in a region where such habitat heterogeneity can be used. If biologically produced habitat heterogeneity is important despite the physical conditions, diversity should be high. A test of the theory requires that the degree of association of harpacticoid species with biogenous structures (as markers of biologically produced habitat patches) at the HEBBLE site be contrasted with that at another site. The site with the greater degree of association should have the highest diversity. LOCALITIES
The HEBBLE samples were taken on the upper part of the Scotian Rise, where the Western Boundary Undercurrent is thought to alter sea-bottom topography (FIoLLISTeR and ~ E ~ , 1972) (Fig. I). The region has higher mean current velocities (12.2 cm s-1) than other abyssal regions (RICHARDSON et al., 1981). An 8-month current meter record obtained 33 km away at 4500-m depth revealed that the background conditions were punctuated by frequent, several-day interludes when daily average velocities were 20 to 25 cm s-~ (WEA~ERLY and KELLEY, 1983). The measured velocities are among the highest recorded in the deep ocean and are capable of eroding surficial sediment (RicHARDSON et aL, 1981; WEATHERLY and K~LLEY, 1983). As a consequence, near-bottom suspended
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Biogenous structures and diversity maintenance
izoo~'
/~'"
":i
40 e
N
t o 35 ° N
)BERMUDA I
*
70 e W
Fig. I .
I 65 ° W
I 60 ° W
Chart of the northwestern Atlantic showing the site of the HEBBLE preliminary samples (circle); modified from UCHtWl(1971).
particulate matter concentrations in the HEBBLE area are higher than those of strong nepheloid layers known elsewhere in the world ocean (BIscA~ et aL, 1980). Two locations 3 km apart but at the same depth (4626 m) were sampled (40°24.0'N, 63°07.4'W and 40°24.YN, 63°09.6'W). The sediment consisted of 6.0% sand, 50.6% silt, and 39.3% clay (median of eight determinations on the 0- to l-cm layer, B. TUCHOLKE, personal communication) and was oxidized to at least 10-cm depth. The nearbottom temperature varies between 2.23 and 2.27°C, and the salinity varies between 34.89 and 34.90 x 10-3 (G. L. WeATHESJ~Y,personal communication). San Diego Trough is 16 km wide and extends for 80 km along the southern California coast. It is the innermost basin in the continental borderland. Tms-n~E (1978) described the physical characteristics of the site and concluded that it has high physical stability. The samples were taken at 32°35.75'N, 117°29.00'W at 1218 to 1223 m. MATERIALS AND METHODS
The samples were obtained using a 0.25-m 2 "Sandia" box corer (I-Iesst~R and Ju~a~Rs, 1974) modified according to designs developed to reduce the adverse effects of the bow wave by R.R. Hessler, P.A. Jumars, and J. Finger. The modification had doors in the corer head that were held open during descent and sampling and were closed during pull out and ascent. The core box contained 22 10 x 10-cm subcores (JUM~RS, 1975b). The inner nine subcores contained 5 x 5-cm subsubcores (used for microbial studies) whose edges were beveled such that each subcore sampled 77 cm 2 (Fig. 2). On deck, the water overlying each subcore was passed through a 0.044-mm aperture sieve. The residue was
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l I
l i
l I
I
{
I I
I0 ¢m
Fig. 2.
A schematic representation of a core box showing the in situ subsamplers.
combined with the 0- to 1-cm layer and fixed in 20% formaldehyde-f'fltered seawater solution. In the laboratory, the samples were sieved on nested 1.00-, 0.500-, 0.420-, 0.300-, and 0.062-ram aperture sieves and preserved in 80% ethanol. The harpacticoids in the 0.062-ram fraction were concentrated using a sorting-trough technique (B^aNETT, 1968) that was 100% efficient (n = 3). The concentrated 0.062-mm fraction and each of the larger fractions were stained with rose bengal. The harpacticoids were removed under a dissecthlg microscope and identified to 'working' (not formally named) species. Taxonomic treatment of this largely new fauna has begun (REIDENAUER and TmSTU~, 1983). In the course of the study, the working species determinations became more accurate, so there are small differences between the data used here and those used by Tms'r~ (1983). To quantify markers of biologio~y produced habitat heterogeneity, eight classes of biogenous structure were recognized: (1) Foraminifera that were unbranched but that had a proloculus, e.g., Hyperamm~; (2) unbranched Foraminifera, e.g., Bathystphon; (3) branched Foraminifera, e.g., R/~amm/na; (4) bush-like Foraminifera, e.g., Dendrophrya; (5) u n i s ~ Foraminifera, e.g., R ~ ; (6) radiating Forlur-'zmifera, e.g., AstrorMza; (7) planisplral Foraminifera, e.g., Crtbrostomotdea;and (8) metazoan tubes, plus the abiotic class pebbles. Because the branched foraminiferans had test-wall characteristics that differed from those of the unbranched foraminiferans, the two groups could be quantified accurately despite the breakage of individual foraminiferans during proccumg. Mctazoan tubes probably included tubes made by tanald crustaceans and polychaetea; the two types could not be distingui~mi reliably. Specimens of these uzuctural cla|um were sorted from the 1.0-mm fraction. Specimens with one dimension >0.5 mm were measured if the circumference of the piece was somewhere intact. C ~ I, 4, and 5 were rare and are not considered further. The remaining classes were assigned geometric approximations: cylinder--2, 3, and 8; prelate spheroid---6, some pebbles; oblate spheroid--7; rectangular parallelepiped--some pebbles. For each specimen of each class, appropriate orthogonal axes were measured and volumes were calculated (Table I).
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Biogenous structures and diversity maintenance
Table 1. Relative volume by structural class for the subcores o f the two HEBBLE box cores. The subcores are numbered as O"they were from a 5 x 5 array Structural class Box core Subcore
Unbranched Foraminifera
Branched Foraminifera
Radiating Foraminifera
Planispiral Foraminifera
Metazoan tubes
Pebbles
I
7 8 9 12 13 14 17 18 19
391.61 49.40 354.08 669.92 138.61 610.34 1275.61 498.19 238.84
172.92 173.6 i 131.29 527.11 276.89 374.58 472.80 409.60 438.73
0 0 22.47 82.21 0 0 0 20.65 14.14
0 0 14.42 16.42 2.95 0 0 3.63 12.89
0.31 77.82 1409.70 235.49 84.54 1008.53 10.02 249.17 119.30
541.81 27.61 5953.47 14810.23 412.83 2960.34 1416.00 3759.64 231.36
II
7 8 9 12 13 14 17 18 19
1326.60 ! 405.15 554.53 77.65 225.70 318.43 384.30 87.56 254.64
34.85 77.99 202.26 115.81 59.24 31.35 76.82 53.35 42.76
17.21 5.54 0 0 0 0 0 0 0
12.73 61.96 0 0 0 0 0 0 37.64
627.56 215.24 132.37 398.43 70.19 261.15 235.83 42.75 2.96
80.27 773.28 94.39 39.78 317.98 432.59 55.28 532.34 932.73
The San Diego Trough samples were taken by a remote underwater manipulator using a modified Ekman grab. The grab was 20 x 20 cm and contained four 10 x 10-cm subcores (TresTLE, 1978). Fourteen subeores were analyzed for harpacticoid copepods. The subcores were processed as the HEBBLE samples were except that the 0.062-mm fraction was not concentrated with a sorting trough before sorting and the structural classes were appropriate to the San Diego Trough. The statistical measure of association used was not a conventional correlation coefficient. For most harpacticoid species, the subcore counts were low; as a result, the number of ties was excessive and probabilities derived from conventional correlation coefficients were unlikely to be accurate. I modified the rank test (T^TE and CLELLAND, 1957) to provide a measure of association for the data. Briefly, the subcores from a box core can be ranked based on the amount of a particular structural class present. The subcores can also be divided into those that have more than the median abundance of a particular variable (i.e., a harpacticoid species) and those that do not. For the subcores that have higher than median abundance of the variable, the sum of their ranks based on the structural ranking is calculated. Tables of the rank-test statistic are then consulted to determine whether the observed value is larger (positive correlation) or smaller (negative correlation) than expected by chance. In Jumars' theory, harpacticoid species should be associated with the habitat patches marked by biogenous structures, so only positive correlations were of interest; all tests were one-tailed. The tests for association between structural classes and harpacticoid species assume that the values measured in each subeore of a box core are independent. Given the systematic nature of the samples and their contiguity, the assumption requires justification. If the subcore values of a variable are independent, then the large departures from mean abundance should not be unusually close together or far apart compared to a random
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DAVIDTHlSrt.L-
distribution of the values. The null hypothesis of random spatial distribution of values tbr each variable was tested using spatial autocorrelation (Moran's I, CLIFF and ORD, 1973). Adjacent subcores were joined; weights were inverse distance between core centers. Significance was determined by comparison of the observed index value to the distribution of index values obtained from 200 random permutations of the subcore values. The 95% significance level was used unless otherwise stated. RESULTS
Each structural class and each harpacticoid species was tested for the independence of its subcore abundances within each box core. Structural class 7, planispiral Foraminifera, was significantly spatially autocorrelated in box core I and was eliminated from the analysis. Two harpacticoid species were significantly spatially autocorrelated. The number of significant correlations is less than expected by chance given the number of tests performed. Therefore, there is no reason to reject the null hypothesis of independence for any harpacticoid species. The test proposed in the introduction required the comparison of the degree of association between harpacticoid species and classes of biogenous structure from the HEBBLE site and from the San Diego Trough. The association of each species with each structural class was tested using the modified rank test described above (treating each subcore as an independent sample). Sixty-six species occurred in more than one subcore in the HEBBLE data; there were four structural classes. Of the 264 tests, 3.03% were significant and positive (one-tailed test, n = 18). The San Diego Trough data reported by TreSTLE (1979) were re-analyzed using the same methods. Of the 868 tests (124 spp., seven structural classes), 6.57% were significant (one-tailed test, n = 14). To determine whether the percentages differed significantly, the null hypothesis that the probability of a significant species-structure association was independent of location was tested. The hypothesis was rejected (P < 0.05); the San Diego Trough data contained significantly more significant associations than the HEBBLE data. To complete the test of the theory, the diversities of the two sites must be compared. The statistical approach and its justification are presented in THISTLE (1983) together with the result. The two sites cannot be shown to differ in diversity. Although the above results suffice for a test of the theory, the data allow a further exploration of the role of habitat heterogeneity at the HEBBLE site. Because no species can be identified in advance as likely to be associated with a structural class, no a priori test can be specified. To identify specific species-structural class associations, a procedure that corrects for the inflation of Type-I-error probability caused by multiple testing by establishing an experiment-wise error rate was adopted (SoKAL and R o n ~ , 1969). Specifically, five species occurred in at least three subcores in both box cores. Each was tested against the four structural classes at a single-test significance level of 0.05. To be judged significant, a species-structure combination had to be significant in both data sets (experimentwise error rate = 0.0625). No species-structural class association met even this slightly relaxed criterion. The analysis was extended by treating species as replicates (JtrMARS, 1975a; THtSa'LE, 1979) to detect average effects rather than to identify specific species-structural class associations. In box core I, the signed-rank statistic can be calculated for each species on each structural class. The resulting value can be scored as indicating positive or negative
Biogenous structures and diversity maintenance
124 1
association. The result can be compared to the result from the same species-structural class calculation in box core II. There are four possible outcomes: both values positive, both negative, the first positive and the second negative, and the first negative and the second positive. If species are unaffected by the presence of biogenous structure, then the number of occurrences of the four outcomes should be equal on the average. The expectation was tested against the one-tailed alternative of an excess of positive-positive matches, which would indicate positive association of harpacticoid species with a given structural class. None of the structural classes had significantly more positive-positive matches than would be expected by chance (single-test alpha = 0.05). Given the theory described in the introduction, interest was focused on classes of biogenous structure. However, at the HEBBLE site, pebbles occurred in all subcores (1 to 32 per subcore), and their subcore volumes were comparable to those of the other structural classes. They were of a size to serve as potential sources of habitat heterogeneity for harpacticoids. However, none of the five species that occurred in three or more subcores in each box core was significantly associated with this structural class in both box cores, so individual species could not be shown to be positively associated with pebbles. When species were treated as replicates and the frequency of positive-positive matches was considered, significantly more species had positive-positive matches than expected by chance (one-tailed P < 0.025), suggesting that some harpacticoid species were positively associated with pebbles at the HEBBLE site. DISCUSSION
Although other, as yet unmeasured, sources of biologically produced habitat heterogeneity may be important, associations between biogenous structures and deep-sea faunal components are known (BEKNSTEIN et al., 1978; BERNSTEIN and MEADOR, 1979; THISTLE, 1979, 1982). In the present case, there are no detectable associations between harpacticoid copepods and biogenous structures at the HEBBLE site, a lack of association that could be artifactual. In particular, the subcores are large compared to the size of the biogenous structures studied, so other sources of variance could obscure real associations. Also, the HEBBLE samples were taken with a box corer designed to minimize bow wave, whereas the San Diego Trough samples were taken using an underwater manipulator. It has been suggested elsewhere (THISTLE, 1983) that the HEBBLE samples showed no evidence of a bow-wave-induced bias, but any tendency for structures or harpacticoids living on the surface or in the upper few millimeters to be redistributed as the samples were taken (disrupting real associations) would be greater in the HEBBLE samples. Although such effects cannot be dismissed, the fact that it was possible to detect significant associations between harpacticoid species and pebbles suggests that harpacticoid-biogenous-structur¢ associations could have been detected in the HEBBLE samples. If, as in the theory, biologically produced habitat heterogeneity contributes to the maintenance of diversity (JUMARS, 1975a, 1976; JUMARS and GALLAOHER,1982), then a location that has more biologically produced habitat heterogeneity should have the higher diversity. In the comparison, the San Diego Trough has significantly more associations between harpacticoid species and biogenous structures than does the HEBBLE site, but the anticipated difference in diversities cannot be demonstrated. To this extent the theory is falsified. Given that the experiment was uncontrolled, alternative interpretations should
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DAvtD THISTLE
be considered. For example, if a decrease in diversity resulting from the reduction of biologically produced habitat heterogeneity is counterbalanced by an increase in the diversifying effect of predators (REx, 1976) or of physical disturbance (Hus'roN, 1979; MILLER, 1982) at the HEBBLE site, then the present results could be obtained. Similar compensations could be proposed for the other factors thought to influence deep-sea diversity. The theory cannot be rejected. If the HEBBLE results are taken at face value, high diversity is maintained in the absence of biologically created habitat heterogeneity. DAv'rON and I-IessL~R (1972) provided a model under which such a circumstance could arise. They suggested that, if non-selective predation is predictable enough and intense enough, then competing species will seldom reach population sizes at which competitive exclusion occurs, so high diversities can be maintained [see SLOBOI>KIN (1962) for some unstated assumptions]. Although Dayton and Hessler presented their model in terms of biological sources of mortality, non-selective mortality is the crucial aspect, and it can be imposed by physical factors. At the HEBBLE site, intense benthic storms occur more than once a year (RICHARDSON et al., 1981; WEATI~ERLYand K~LLE~', 1983); they are periods of intense erosion; just after a storm there is massive deposition (by ordinary deep-sea standards) (C. D. HOLLIST~, personal communication; YINOSTand ALLER, 1982). If harpacticoids are
|
,,r
~ L E
SOT
Frequency of Reduction Fig. 3. A schematic representation of HUSTON'S(1979) dynamic equilibrium model Diversity is plotted as contours; the hil~ut values are in the inner elipsoid. The diverl/ty of the San Diego Trough fauna is indistinliu/shable from that of the HEBBLE fauna, so they lie on the same contour. The rate of physically imposed population reduction is greater at the HEBBLE site than in the San Diego Trough. Although the exact value of the difference is not known, the direction is, so the two sites can be ordered on the frequency of reduction axis. One project/on of the two sites onto the rate of displacement axis is shown.
Biogenous structures and diversitymaintenance
1243
i "6 £ D rr
t.~lllt.I r
Frequency of Reduction Fig. 4.
The figure is identical to Fig. 3 except that an alternative projection of the two sites onto the frequencyof displacementaxis is shown.
killed when eroded, transported or buried, storms could serve as the non-selective mortality source of Dayton and Hessler's model and maintain high diversity in the absence of a high degree of habitat partitioning among species. The physical regime of the HEBBLE site could account for lack of association between harpacticoid species and hiogenous structures in a second way. The central tenet of Jumars' theory is that small patches that persist long enough can serve as habitat heterogeneity. However, the frequent wholesale movement of surficial sediments by storms may cause organism-created patches to be too short-lived to be exploitable. Therefore, a mechanism other than Jumars' must allow the high diversity observed. HUSTDN (1979) presented a model as a general explanation of geographic variation in diversity. The model has been well received by some workers (GRAY, 1981; Rex, 1981), but, when the data in this paper were used to test it, the model made ambiguous predictions. Specifically, I wished to use the rank order of the two sites on the frequency of reduction axis and the two diversities to predict the relative position of the two sites on the rate of displacement axis, then to evaluate the reasonableness of the predicted ra~king. Based on the available data (THISTLe, 1983 and above), the order of the San Diego Trough and the HEBBLE site can be established on the frequency of reduction axis (Fig. 3) in that physically imposed mortality events occur with greater (probably much greater) frequency at the HEBBLE site. The diversifies are indistinguishable and, therefore, must lie on the same diversity contour. But the facts do not allow an unambiguous prediction of the ranking of the two stations on the frequency of displacement axis (compare Figs 3 and 4). The ambiguity extends beyond the twosite case. If one ranks three sites on the frequency of reduction axis, given the geometry, five
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DAVID ~HISTLE
to six p e r m u t a t i o n s o f the r a n k s are possible o u t c o m e s on the frequency of displacement axis. F o r the four-site case, 15 o f 24 r a n k orders are possible. The only way to falsify H u s t o n ' s model with this a p p r o a c h a p p e a r s to be to find in n a t u r e a n example of a case forbidden under the model.
Acknowledgements--The HEBBLE samples were taken with the assistance of R. ALLER, R. CHANDLER, P. JUMARS, and J. YINGST.The San Diego Trough samples were taken by R. HESSLERand his colleagues during Expedition Quagmire. C. HOLLISTERand B. TUCHOLKEprovided unpublished data. S. CULVER suggested the structural classes for the Foraminifera. Computer time was donated by Florida State University. J. MERR1Tr guided my programming. J. GAGE, P. JUMAI*,S,A. NOWELL, J. REIDENAUER, K. SHERMAN, A. THISTLE, G. WEATHERLY, and J. YINGSTread and commented on the manuscript. The research was sponsored by the Office of Naval Research under Contract N00014-75-C-0201. I wish to acknowledge this kind help.
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MENOE B.A. and J. P. SUTHERLAND(1976) Species diversity gradients: synthesis of the roles of predation, competition, and temporal heterogeneity. American Naturalist, 110, 351-369. MILLER T.E. (1982) Community diversity and interactions between the size and frequency of disturbance. American Naturalist, 120, 533-536. NOWELL A. R. M., C.D. HOLLISTERand P. A. JUMARS(1982) High Energy Benthic Boundary Layer Experiment: HEBBLE. EOS, 65, 594-595. REIDENAUER J.A. and D. THISTLE (1983) Sarsameira (Copepoda, Harpacticoida): an update and a new species from the deep sea. Transactions of the American Microscopical Society, 102, 105-112. REX M.A. (1976) Biological accommodation in the deep-sea benthos: comparative evidence on the importance of predation and productivity. Deep-Sea Research, 23, 975-987. REX M. A. (1981) Community structure in the dcep-sea benthos. Annual Review of Ecology and Systematics, 12, 331-353. RICHARDSON M..I., M. WIMBUSH and L. MAYER (1981) Exceptionally strong near-bottom flows on the continental rise of Nova Scotia. Science, Wash., 213, 887-888. SANDERS H. L. (1968) Marine benthic diversity: a comparative study. American Naturalist, 102, 243-282. SANDERS H. L. (1969) Benthic marine diversity and the stability-time hypothesis. Brookhaven Symposium in Biology, 22, 71-80. SLOBOKDIN L.B. (1962) Growth and regulation of animal populations, Holt, Rinehart & Winston, New York, 184 pp. SLOSODKIN L.B. and H.L. SANDERS (1969) On the contribution of environmental predictability to species diversity. Brookhaven Symposium in Biology, 22, 82-93. SOKAL R. R. and F.J. ROHLF (1969) Biometry, W. H. Freeman, San Francisco, 766 pp. TATE M.W. and R.C. CLELLAND (1957) Nonparametric and shortcut statistics, Interstate, Danville, Illinois, 171 pp. THISTLE D. (1978) Harpacticoid dispersion patterns: implications for deep-sea diversity maintenance. Journal of Marine Research, 36, 377-397. THISTLE D. (1979) Harpacticoid copepods and biogenic structures: implications for deep-sea diversity maintenance. In: Ecological processes in coastal and marine systems, R.J. LIVINGSTON,editor, Plenum Press, New York, pp. 217-231. THISTLE D. (1982) Aspects of the natural history of the harpacticoid copepods of San Diego Trough. Biological Oceanography, 1, 225-238. THISTLE D. (1983) The stability-time hypothesis as a predictor of diversity in deep-sea soft-bottom communities: a test. Deep-Sea Research, 30, 267-277. UCHUPI E. (1971) The bathymetric atlas of the Atlantic, Caribbean and Gulf of Mexico. Woods Hole Oceanographic Institution Technical Report WHOI-71-72, 10 pp. WEATHERLY G. L. and E.A. KELLEY, JP.. (1983) 'Too cold' bottom layers at the base of the Scotian Rise. Journal of Marine Research, 40, 985-1012. YINGST J.Y. and R.C. ALLER (1982) Biological activity and associated sedimentary structures in HEBBLEarea deposits, western North Atlantic. Marine Geology, 48, MT-MI5.
The
0198-0149/83 $3.00 + 0.00 © 1983 Pergamon Press Ltd.
role of biologically produced habitat heterogeneity in deep-sea diversity maintenance DAVID THISTLE*
(Received lO January 1983; accepted 11 February 1983;final revision received 10 May 1983) Abstraet--A model in which biologically generated habitat heterogeneity plays a leading role has been proposed to explain the relatively high diversity of the deep sea: as the rates of physical and biological disturbance decrease with depth the habitat heterogeneity created by organisms becomes increasingly available to other organisms for habitat partitioning or as prey refuges, allowing larger numbers of species to be accommodated locally. The theory was tested by comparing the level of association between organism-generated habitat heterogeneity and harpacticoid copepod species' distributions from two deep-sea sites. The expectation under the model that the site with the greater degree of association would have the greater diversity was not met.
INTRODUCTION
SEVERAL taxa are more diverse in deep-sea soft bottoms than in similar shallow-water locations, e.g., polychaetes and bivalves (SANDERS, 1968), foraminiferans (BUZAS and GIBSON, 1969), cumaceans (JONES and SANDERS, 1972), harpacticoid copepods (COULL, 1972; THISTLE, 1978), polychaetes (HESSLER and JUMARS, 1974), and gastropods (REx, 1981). The cause of the pattern is not yet clear, but a body of theory has arisen to explain it (SANDERS, 1968, 1969; St~3SODKIN and SANDERS, 1969; DAYTON and Hr~SLER, 1972; GRASSLE and SANDERS, 1973; GRAY, 1974; MENOE and SUTHERLAND,1976; REX, 1976; AeELE and WALTERS,1979; HUSTON, 1979). Prominent among the theories is the idea that species of the diverse taxa have highly specialized niches such that competition is minimized, allowing large numbers of similar species to co-occur. A major alternative thesis suggests that species populations are kept so low by predation or disturbance that competition never results in the exclusion of a species, and high diversity can be achieved locally. Several authors have proposed intermediate views, but no theory has achieved wide acceptance. In a different approach, JUMARS(1975a, 1976; JUMARSand GALLAGHER, 1982; JUMARS and ECKMAN, 1983) argued that biologically produced habitat heterogeneity may be an important factor in the maintenance of high diversity in the deep sea. He reasoned that, in shallow water, where physical conditions are relatively energetic and rates of biological disturbance are high, the effects of an organism on its local environment are rapidly obliterated, in general, and cannot be exploited by another organism as a habitat patch. As water depth increases, both physical energy levels and biological activity rates decrease, so the effects on * Department of Oceanography, Florida State University, Tallahassee, FL 32306, U.S.A. 1235
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DAVIDTHISTU~
their immediate environment of increasing numbers of organisms persist long enough to serve as distinct habitat patches. Such biologically produced patches could serve to isolate potentially competing species by providing a large number of distinguishable microhabitats within a community. Alternatively, such a patch structure could decrease the probability of prey extinctions by providing refuges for prey and reducing predator efficiency (M~NGE and StJTHERLAND, 1976). Given the increased longevity of such biologically produced patches as rates of physical and biological activity decrease with depth, this factor could explain, at least in part, the observed correlation of diversity with depth as one moves from shallow water into the deep sea. JUMARS (1976) pointed out that any test of the role of this type of habitat heterogeneity in diversity maintenance faces the difficulty that one must sample habitat patches whose scale is that of a macrofaunal individual. The problem can be circumvented, at least in part, if one studies the effects of organisms that create recoverable markers, e.g., tubes, tests, and mud balls (JU~tARS, 1975C, Fig. 1; "IMISTLE, 1979, Fig. 3). The relative abundances of classes of biogenous structures could then be tested for association with species of a diverse taxon. Clearly, not all biologically produced habitat heterogeneity can be so assessed; in particular, burrows will not be considered. Harpacticoid copepods are an appropriate taxon for such a test. These benthic crustaceans are highly diverse in the deep sea (THISTLE, 1978). They are small (total body length < 1.0 mm), so habitat patches created by macrofauna individuals are relatively large and more likely to act as distinct habitats for them than for larger organisms. In an attempt to test the theory, harpacticoid data and biogenous structure measurements from the deep North Atlantic obtained as part of the High Energy Benthic Boundary Layer Experiment (HEBBLE) preliminary work (NowELL et al., 1982) were used. This region has strong near-bottom currents relative to typical abyssal conditions (RICHARDSONet aL, 1981), but it is unclear whether the near-bottom current regime affects the importance of environmental heterogeneity to harpacticoids. If the theory is correct and if the physical violence is sufficient to make it less likely that biologically produced habitat heterogeneity can be used as habitat patches by harpaeticoids, one would predict lower diversity of the harpacticoid fauna than in a region where such habitat heterogeneity can be used. If biologically produced habitat heterogeneity is important despite the physical conditions, diversity should be high. A test of the theory requires that the degree of association of harpacticoid species with biogenous structures (as markers of biologically produced habitat patches) at the HEBBLE site be contrasted with that at another site. The site with the greater degree of association should have the highest diversity. LOCALITIES
The HEBBLE samples were taken on the upper part of the Scotian Rise, where the Western Boundary Undercurrent is thought to alter sea-bottom topography (FIoLLISTeR and ~ E ~ , 1972) (Fig. I). The region has higher mean current velocities (12.2 cm s-1) than other abyssal regions (RICHARDSON et al., 1981). An 8-month current meter record obtained 33 km away at 4500-m depth revealed that the background conditions were punctuated by frequent, several-day interludes when daily average velocities were 20 to 25 cm s-~ (WEA~ERLY and KELLEY, 1983). The measured velocities are among the highest recorded in the deep ocean and are capable of eroding surficial sediment (RicHARDSON et aL, 1981; WEATHERLY and K~LLEY, 1983). As a consequence, near-bottom suspended
1237
Biogenous structures and diversity maintenance
izoo~'
/~'"
":i
40 e
N
t o 35 ° N
)BERMUDA I
*
70 e W
Fig. I .
I 65 ° W
I 60 ° W
Chart of the northwestern Atlantic showing the site of the HEBBLE preliminary samples (circle); modified from UCHtWl(1971).
particulate matter concentrations in the HEBBLE area are higher than those of strong nepheloid layers known elsewhere in the world ocean (BIscA~ et aL, 1980). Two locations 3 km apart but at the same depth (4626 m) were sampled (40°24.0'N, 63°07.4'W and 40°24.YN, 63°09.6'W). The sediment consisted of 6.0% sand, 50.6% silt, and 39.3% clay (median of eight determinations on the 0- to l-cm layer, B. TUCHOLKE, personal communication) and was oxidized to at least 10-cm depth. The nearbottom temperature varies between 2.23 and 2.27°C, and the salinity varies between 34.89 and 34.90 x 10-3 (G. L. WeATHESJ~Y,personal communication). San Diego Trough is 16 km wide and extends for 80 km along the southern California coast. It is the innermost basin in the continental borderland. Tms-n~E (1978) described the physical characteristics of the site and concluded that it has high physical stability. The samples were taken at 32°35.75'N, 117°29.00'W at 1218 to 1223 m. MATERIALS AND METHODS
The samples were obtained using a 0.25-m 2 "Sandia" box corer (I-Iesst~R and Ju~a~Rs, 1974) modified according to designs developed to reduce the adverse effects of the bow wave by R.R. Hessler, P.A. Jumars, and J. Finger. The modification had doors in the corer head that were held open during descent and sampling and were closed during pull out and ascent. The core box contained 22 10 x 10-cm subcores (JUM~RS, 1975b). The inner nine subcores contained 5 x 5-cm subsubcores (used for microbial studies) whose edges were beveled such that each subcore sampled 77 cm 2 (Fig. 2). On deck, the water overlying each subcore was passed through a 0.044-mm aperture sieve. The residue was
1238
DAWDTHISTLE
l I
l i
l I
I
{
I I
I0 ¢m
Fig. 2.
A schematic representation of a core box showing the in situ subsamplers.
combined with the 0- to 1-cm layer and fixed in 20% formaldehyde-f'fltered seawater solution. In the laboratory, the samples were sieved on nested 1.00-, 0.500-, 0.420-, 0.300-, and 0.062-ram aperture sieves and preserved in 80% ethanol. The harpacticoids in the 0.062-ram fraction were concentrated using a sorting-trough technique (B^aNETT, 1968) that was 100% efficient (n = 3). The concentrated 0.062-mm fraction and each of the larger fractions were stained with rose bengal. The harpacticoids were removed under a dissecthlg microscope and identified to 'working' (not formally named) species. Taxonomic treatment of this largely new fauna has begun (REIDENAUER and TmSTU~, 1983). In the course of the study, the working species determinations became more accurate, so there are small differences between the data used here and those used by Tms'r~ (1983). To quantify markers of biologio~y produced habitat heterogeneity, eight classes of biogenous structure were recognized: (1) Foraminifera that were unbranched but that had a proloculus, e.g., Hyperamm~; (2) unbranched Foraminifera, e.g., Bathystphon; (3) branched Foraminifera, e.g., R/~amm/na; (4) bush-like Foraminifera, e.g., Dendrophrya; (5) u n i s ~ Foraminifera, e.g., R ~ ; (6) radiating Forlur-'zmifera, e.g., AstrorMza; (7) planisplral Foraminifera, e.g., Crtbrostomotdea;and (8) metazoan tubes, plus the abiotic class pebbles. Because the branched foraminiferans had test-wall characteristics that differed from those of the unbranched foraminiferans, the two groups could be quantified accurately despite the breakage of individual foraminiferans during proccumg. Mctazoan tubes probably included tubes made by tanald crustaceans and polychaetea; the two types could not be distingui~mi reliably. Specimens of these uzuctural cla|um were sorted from the 1.0-mm fraction. Specimens with one dimension >0.5 mm were measured if the circumference of the piece was somewhere intact. C ~ I, 4, and 5 were rare and are not considered further. The remaining classes were assigned geometric approximations: cylinder--2, 3, and 8; prelate spheroid---6, some pebbles; oblate spheroid--7; rectangular parallelepiped--some pebbles. For each specimen of each class, appropriate orthogonal axes were measured and volumes were calculated (Table I).
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Biogenous structures and diversity maintenance
Table 1. Relative volume by structural class for the subcores o f the two HEBBLE box cores. The subcores are numbered as O"they were from a 5 x 5 array Structural class Box core Subcore
Unbranched Foraminifera
Branched Foraminifera
Radiating Foraminifera
Planispiral Foraminifera
Metazoan tubes
Pebbles
I
7 8 9 12 13 14 17 18 19
391.61 49.40 354.08 669.92 138.61 610.34 1275.61 498.19 238.84
172.92 173.6 i 131.29 527.11 276.89 374.58 472.80 409.60 438.73
0 0 22.47 82.21 0 0 0 20.65 14.14
0 0 14.42 16.42 2.95 0 0 3.63 12.89
0.31 77.82 1409.70 235.49 84.54 1008.53 10.02 249.17 119.30
541.81 27.61 5953.47 14810.23 412.83 2960.34 1416.00 3759.64 231.36
II
7 8 9 12 13 14 17 18 19
1326.60 ! 405.15 554.53 77.65 225.70 318.43 384.30 87.56 254.64
34.85 77.99 202.26 115.81 59.24 31.35 76.82 53.35 42.76
17.21 5.54 0 0 0 0 0 0 0
12.73 61.96 0 0 0 0 0 0 37.64
627.56 215.24 132.37 398.43 70.19 261.15 235.83 42.75 2.96
80.27 773.28 94.39 39.78 317.98 432.59 55.28 532.34 932.73
The San Diego Trough samples were taken by a remote underwater manipulator using a modified Ekman grab. The grab was 20 x 20 cm and contained four 10 x 10-cm subcores (TresTLE, 1978). Fourteen subeores were analyzed for harpacticoid copepods. The subcores were processed as the HEBBLE samples were except that the 0.062-mm fraction was not concentrated with a sorting trough before sorting and the structural classes were appropriate to the San Diego Trough. The statistical measure of association used was not a conventional correlation coefficient. For most harpacticoid species, the subcore counts were low; as a result, the number of ties was excessive and probabilities derived from conventional correlation coefficients were unlikely to be accurate. I modified the rank test (T^TE and CLELLAND, 1957) to provide a measure of association for the data. Briefly, the subcores from a box core can be ranked based on the amount of a particular structural class present. The subcores can also be divided into those that have more than the median abundance of a particular variable (i.e., a harpacticoid species) and those that do not. For the subcores that have higher than median abundance of the variable, the sum of their ranks based on the structural ranking is calculated. Tables of the rank-test statistic are then consulted to determine whether the observed value is larger (positive correlation) or smaller (negative correlation) than expected by chance. In Jumars' theory, harpacticoid species should be associated with the habitat patches marked by biogenous structures, so only positive correlations were of interest; all tests were one-tailed. The tests for association between structural classes and harpacticoid species assume that the values measured in each subeore of a box core are independent. Given the systematic nature of the samples and their contiguity, the assumption requires justification. If the subcore values of a variable are independent, then the large departures from mean abundance should not be unusually close together or far apart compared to a random
1240
DAVIDTHlSrt.L-
distribution of the values. The null hypothesis of random spatial distribution of values tbr each variable was tested using spatial autocorrelation (Moran's I, CLIFF and ORD, 1973). Adjacent subcores were joined; weights were inverse distance between core centers. Significance was determined by comparison of the observed index value to the distribution of index values obtained from 200 random permutations of the subcore values. The 95% significance level was used unless otherwise stated. RESULTS
Each structural class and each harpacticoid species was tested for the independence of its subcore abundances within each box core. Structural class 7, planispiral Foraminifera, was significantly spatially autocorrelated in box core I and was eliminated from the analysis. Two harpacticoid species were significantly spatially autocorrelated. The number of significant correlations is less than expected by chance given the number of tests performed. Therefore, there is no reason to reject the null hypothesis of independence for any harpacticoid species. The test proposed in the introduction required the comparison of the degree of association between harpacticoid species and classes of biogenous structure from the HEBBLE site and from the San Diego Trough. The association of each species with each structural class was tested using the modified rank test described above (treating each subcore as an independent sample). Sixty-six species occurred in more than one subcore in the HEBBLE data; there were four structural classes. Of the 264 tests, 3.03% were significant and positive (one-tailed test, n = 18). The San Diego Trough data reported by TreSTLE (1979) were re-analyzed using the same methods. Of the 868 tests (124 spp., seven structural classes), 6.57% were significant (one-tailed test, n = 14). To determine whether the percentages differed significantly, the null hypothesis that the probability of a significant species-structure association was independent of location was tested. The hypothesis was rejected (P < 0.05); the San Diego Trough data contained significantly more significant associations than the HEBBLE data. To complete the test of the theory, the diversities of the two sites must be compared. The statistical approach and its justification are presented in THISTLE (1983) together with the result. The two sites cannot be shown to differ in diversity. Although the above results suffice for a test of the theory, the data allow a further exploration of the role of habitat heterogeneity at the HEBBLE site. Because no species can be identified in advance as likely to be associated with a structural class, no a priori test can be specified. To identify specific species-structural class associations, a procedure that corrects for the inflation of Type-I-error probability caused by multiple testing by establishing an experiment-wise error rate was adopted (SoKAL and R o n ~ , 1969). Specifically, five species occurred in at least three subcores in both box cores. Each was tested against the four structural classes at a single-test significance level of 0.05. To be judged significant, a species-structure combination had to be significant in both data sets (experimentwise error rate = 0.0625). No species-structural class association met even this slightly relaxed criterion. The analysis was extended by treating species as replicates (JtrMARS, 1975a; THtSa'LE, 1979) to detect average effects rather than to identify specific species-structural class associations. In box core I, the signed-rank statistic can be calculated for each species on each structural class. The resulting value can be scored as indicating positive or negative
Biogenous structures and diversity maintenance
124 1
association. The result can be compared to the result from the same species-structural class calculation in box core II. There are four possible outcomes: both values positive, both negative, the first positive and the second negative, and the first negative and the second positive. If species are unaffected by the presence of biogenous structure, then the number of occurrences of the four outcomes should be equal on the average. The expectation was tested against the one-tailed alternative of an excess of positive-positive matches, which would indicate positive association of harpacticoid species with a given structural class. None of the structural classes had significantly more positive-positive matches than would be expected by chance (single-test alpha = 0.05). Given the theory described in the introduction, interest was focused on classes of biogenous structure. However, at the HEBBLE site, pebbles occurred in all subcores (1 to 32 per subcore), and their subcore volumes were comparable to those of the other structural classes. They were of a size to serve as potential sources of habitat heterogeneity for harpacticoids. However, none of the five species that occurred in three or more subcores in each box core was significantly associated with this structural class in both box cores, so individual species could not be shown to be positively associated with pebbles. When species were treated as replicates and the frequency of positive-positive matches was considered, significantly more species had positive-positive matches than expected by chance (one-tailed P < 0.025), suggesting that some harpacticoid species were positively associated with pebbles at the HEBBLE site. DISCUSSION
Although other, as yet unmeasured, sources of biologically produced habitat heterogeneity may be important, associations between biogenous structures and deep-sea faunal components are known (BEKNSTEIN et al., 1978; BERNSTEIN and MEADOR, 1979; THISTLE, 1979, 1982). In the present case, there are no detectable associations between harpacticoid copepods and biogenous structures at the HEBBLE site, a lack of association that could be artifactual. In particular, the subcores are large compared to the size of the biogenous structures studied, so other sources of variance could obscure real associations. Also, the HEBBLE samples were taken with a box corer designed to minimize bow wave, whereas the San Diego Trough samples were taken using an underwater manipulator. It has been suggested elsewhere (THISTLE, 1983) that the HEBBLE samples showed no evidence of a bow-wave-induced bias, but any tendency for structures or harpacticoids living on the surface or in the upper few millimeters to be redistributed as the samples were taken (disrupting real associations) would be greater in the HEBBLE samples. Although such effects cannot be dismissed, the fact that it was possible to detect significant associations between harpacticoid species and pebbles suggests that harpacticoid-biogenous-structur¢ associations could have been detected in the HEBBLE samples. If, as in the theory, biologically produced habitat heterogeneity contributes to the maintenance of diversity (JUMARS, 1975a, 1976; JUMARS and GALLAOHER,1982), then a location that has more biologically produced habitat heterogeneity should have the higher diversity. In the comparison, the San Diego Trough has significantly more associations between harpacticoid species and biogenous structures than does the HEBBLE site, but the anticipated difference in diversities cannot be demonstrated. To this extent the theory is falsified. Given that the experiment was uncontrolled, alternative interpretations should
1242
DAvtD THISTLE
be considered. For example, if a decrease in diversity resulting from the reduction of biologically produced habitat heterogeneity is counterbalanced by an increase in the diversifying effect of predators (REx, 1976) or of physical disturbance (Hus'roN, 1979; MILLER, 1982) at the HEBBLE site, then the present results could be obtained. Similar compensations could be proposed for the other factors thought to influence deep-sea diversity. The theory cannot be rejected. If the HEBBLE results are taken at face value, high diversity is maintained in the absence of biologically created habitat heterogeneity. DAv'rON and I-IessL~R (1972) provided a model under which such a circumstance could arise. They suggested that, if non-selective predation is predictable enough and intense enough, then competing species will seldom reach population sizes at which competitive exclusion occurs, so high diversities can be maintained [see SLOBOI>KIN (1962) for some unstated assumptions]. Although Dayton and Hessler presented their model in terms of biological sources of mortality, non-selective mortality is the crucial aspect, and it can be imposed by physical factors. At the HEBBLE site, intense benthic storms occur more than once a year (RICHARDSON et al., 1981; WEATI~ERLYand K~LLE~', 1983); they are periods of intense erosion; just after a storm there is massive deposition (by ordinary deep-sea standards) (C. D. HOLLIST~, personal communication; YINOSTand ALLER, 1982). If harpacticoids are
|
,,r
~ L E
SOT
Frequency of Reduction Fig. 3. A schematic representation of HUSTON'S(1979) dynamic equilibrium model Diversity is plotted as contours; the hil~ut values are in the inner elipsoid. The diverl/ty of the San Diego Trough fauna is indistinliu/shable from that of the HEBBLE fauna, so they lie on the same contour. The rate of physically imposed population reduction is greater at the HEBBLE site than in the San Diego Trough. Although the exact value of the difference is not known, the direction is, so the two sites can be ordered on the frequency of reduction axis. One project/on of the two sites onto the rate of displacement axis is shown.
Biogenous structures and diversitymaintenance
1243
i "6 £ D rr
t.~lllt.I r
Frequency of Reduction Fig. 4.
The figure is identical to Fig. 3 except that an alternative projection of the two sites onto the frequencyof displacementaxis is shown.
killed when eroded, transported or buried, storms could serve as the non-selective mortality source of Dayton and Hessler's model and maintain high diversity in the absence of a high degree of habitat partitioning among species. The physical regime of the HEBBLE site could account for lack of association between harpacticoid species and hiogenous structures in a second way. The central tenet of Jumars' theory is that small patches that persist long enough can serve as habitat heterogeneity. However, the frequent wholesale movement of surficial sediments by storms may cause organism-created patches to be too short-lived to be exploitable. Therefore, a mechanism other than Jumars' must allow the high diversity observed. HUSTDN (1979) presented a model as a general explanation of geographic variation in diversity. The model has been well received by some workers (GRAY, 1981; Rex, 1981), but, when the data in this paper were used to test it, the model made ambiguous predictions. Specifically, I wished to use the rank order of the two sites on the frequency of reduction axis and the two diversities to predict the relative position of the two sites on the rate of displacement axis, then to evaluate the reasonableness of the predicted ra~king. Based on the available data (THISTLe, 1983 and above), the order of the San Diego Trough and the HEBBLE site can be established on the frequency of reduction axis (Fig. 3) in that physically imposed mortality events occur with greater (probably much greater) frequency at the HEBBLE site. The diversifies are indistinguishable and, therefore, must lie on the same diversity contour. But the facts do not allow an unambiguous prediction of the ranking of the two stations on the frequency of displacement axis (compare Figs 3 and 4). The ambiguity extends beyond the twosite case. If one ranks three sites on the frequency of reduction axis, given the geometry, five
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DAVID ~HISTLE
to six p e r m u t a t i o n s o f the r a n k s are possible o u t c o m e s on the frequency of displacement axis. F o r the four-site case, 15 o f 24 r a n k orders are possible. The only way to falsify H u s t o n ' s model with this a p p r o a c h a p p e a r s to be to find in n a t u r e a n example of a case forbidden under the model.
Acknowledgements--The HEBBLE samples were taken with the assistance of R. ALLER, R. CHANDLER, P. JUMARS, and J. YINGST.The San Diego Trough samples were taken by R. HESSLERand his colleagues during Expedition Quagmire. C. HOLLISTERand B. TUCHOLKEprovided unpublished data. S. CULVER suggested the structural classes for the Foraminifera. Computer time was donated by Florida State University. J. MERR1Tr guided my programming. J. GAGE, P. JUMAI*,S,A. NOWELL, J. REIDENAUER, K. SHERMAN, A. THISTLE, G. WEATHERLY, and J. YINGSTread and commented on the manuscript. The research was sponsored by the Office of Naval Research under Contract N00014-75-C-0201. I wish to acknowledge this kind help.
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