Meiofaunal foraminiferans from the bathyal Porcupine Seabight (northeast Atlantic): size structure, standing stock, taxonomic composition, species diversity and vertical distribution in the sediment

Deep-SeaResearch,Vol. 33, No. I(L pp, 1345 1373. 1986.

0198 ,q149/86$3,00 + 0.01~ © 1986PergamonJournals Ltd.

Printed in Great Brilain.

Meiofaunal foraminiferans from the bathyal Porcupine Seabight (northeast Atlantic): size structure, standing stock, taxonomic composition, species diversity and vertical distribution in the sediment A. J. GOODAY* (Received 14 November 1985; in revised form 28 April 1986; accepted 16 May 1986) Abstract--Living benthic Foraminifera in Multiple Corer samples collectcd at 1321}--1340 m in the Porcupine Seabight have been evaluated using standard meiofaunal tcchniques. The preponderance of tiny individuals 145-106 I.tm) is believed to reflect both the small subsamplc size (3.46 cm 2) and the examination of very fine sieve fractions. Standing crops (1246-2324 livc specimens per 10 cm 2) are higher than normally reported from the deep sea. This is attributed to (a) the abundance of specimens in the rarely studied 45-62 lam sizc fraction, (b) the virtually undisturbed nature of the sediment-water interface collected by the Multiple Corer, and (c) the care taken to extract obscure, tectinous and agglutinated forms from the residues. Most of the important species have hyaline, calcareous tests (suborder Rotaliina) or multilocular or unilocular agglutinated tests (suborder Textulariina). However, forms with proteinaceous tests (suborder AIIogromiina) and various hitherto unrecognized foraminiferans which occupy empty globigerinacean shells are also abundant. Diversity is high (94-124 species per subsample) but relatively few species are common, and about half are represented by single individuals, a pattern often found in the deep sea. Within the upper 5 cm of sediment, most foraminifcrans (52.3-71.0%) occur in the top I cm, there being a steeper than linear decrease in density below this level. Unilocular agglutinated species are concentrated in the top 1 cm, hyaline, calcareous species are proportionally more abundant between 1 and 3 cm, and multilocular agglutinated species increase in relative abundance below 3 cm. Some of the abundant species are concentrated in the surface layer (01 cm), while others peak between 1 and 3 cm; a few rare species occur mainly below 3 cm. It is suspected that this tendency towards vertical segregation results from biotic interactions rather than the influence of chemical or physical factors.

INTRODUCTION FORAMINIFERAare important organisms in many benthic marine environments, and their abundance in the deep sea was established by American and British naturalists during the latter half of the 19th century (DOUGLASand WOODRUFF, 1981). Since the 1920s most work on living benthic foraminiferans, in both shelf and oceanic environments, has been carried out by geologists whose interest in these protozoans stems from their value in biostratigraphy and palaeoecology. Many recent geological studies have focused on issues such as the relationship between benthic foraminiferans and bottom water masses, and on the oxygen and carbon isotope contents of their tests, which are useful in paleooceanographic reconstructions (DOUGLAS and WOODRUFF, 1981; BERGER, 1981). Biological work on deep-sea foraminiferans and other rhizopods has proceeded at a slower rate, but their important ecological role among both the meiofauna and macro* Institute of Oceanographic Sciences, Wormley, Godalming, Surrey GU8 5UB, U.K. 1345

1346

A.J. GOODAY

fauna is becoming increasingly apparent (TENDALand HESSLER, 1977; BERNSTIENet al., 1978; THIEE, 1983; SNIDERet al., 1984). Unfortunately, the evaluation of foraminiferans is made difficult by several factors, including the fragmentation of their often delicate tests and the need to distinguish dead specimens from those that were alive when captured. Further problems for biologists arise because much of the systematic work, particularly on smaller species, has been done by geologists who have evolved an elaborate taxonomic system based on often minute aspects of shell morphology and structure (LOEBLICttand TAPPAN, 1964, 1984; HAYNES, 1981). Partly as a result of these difficulties, many deep-sea meiofauna specialists either have ignored foraminiferans entirely or have made no attempt to identify species or even, in most cases, higher taxa. This paper presents the results of a detailed study of foraminiferans occurring among the meiofauna at a single bathyal station in the northeast Atlantic. A particular attempt has been made to document the distribution and abundance of individual species as well as to describe the overall community structure. A parallel study will deal with the metazoan meiofauna extracted from the same series of samples (PFANNKUCttEand GOODAY, in preparation). METttODS The study area

The Porcupine Seabight is an amphitheatre-shaped embayment of the continental slope situated some 200 km southwest of Ireland. Brief descriptions of its physiography, geology, and hydrology are given by BILLETr and HANSEN (1982), WESTON (1985), PFANNKUCnE (1985) and LAMeITTet al. (in press). At bathyal depths, the floor of the Seabight is overlain by Mediterranean water which has a core characterized by maximum salinity and minimum oxygen concentration centred around 1000 m. The sediment in the sampling area is a foraminiferal ooze composed mainly of clay (57%) and silt-sized (35%) particles. It is oxidized (i.e. brown in colour) down to a depth of 9-10 cm (R. S. LAMPITr, personal communication). The well-defined bathymetric zonation of dead benthic foraminiferans in this region indicates little downslope sediment transport (WEsTON, 1985). Sampling

Samples were collected during Cruise 6/82 of RRS Challenger (8-21 April 1982) in the Porcupine Seabight using the Scottish Marine Biological Association's Multiple Corer (BARNETTet al., 1985). This gear is designed to lower up to 12 coring tubes gently into the sediment, and there is convincing evidence that it collects samples in which the sediment-water interface is virtually undisturbed (BILLEYret al., 1983). Cores obtained during six deployments of the Multiple Corer at IOS Sta. 51502 (around 51°36'N, 13°00'W, 1320-1340 m; see Table 1) were used in this study. From each of the six sets (nos 1, 2, 4, 5, 6, 8), four cores (a-d) were selected at random and subsampled using a 20 ml plastic medical syringe (3.46 cm 2 cross-sectional area) modified by cutting off the end and sharpening the cut edge to allow easy penetration of the sediment. The subcores were frozen sufficiently to allow handling without distortion, and then cut horizontally into 1 cm thick layers down to a depth of 5 cm below the sediment surface. Each layer was fixed separately in 4% formalin buffered with sodium borate, the sample container being shaken gently to break up sediment aggregates.

1347

M e i o f a u n a l f o r a m i n i f e r a n s f r o m the P o r c u p i n e S e a b i g h t

Table 1. Location and fate of Multiple Corer subsamples collected at Sta. Position

Depth (m)

Deployment N

Subsample

W

51502

Sorted

Sorted

for Meiofauna

for Foraminifera

Sorted for selected Foraminifera X X X

1

51°36.1 '

13°00.0 '

1320

a b c d

X X X X

X

2

51%6.2'

12°59.6 '

1340

a b c d

X X X X

X X X X

4

51036.4 '

12°59.7 '

134(I

a b c d

X X X X

X X X X

5

51°36.1 '

13°(/0.2 '

134(/

a b c d

X X X X

X X X X

6

51°35.9 '

12°59.8 '

134(/

a b c d

X X X X

a

X

8*

51°36.0 ' * Subsamples b-d

12o59.2 '

1340

X X X X X

remain unsorted at present.

Analysis In the laboratory each sediment layer was washed, using tap water, through a series of sieves (500, 150, 106, 63 and 45 lain meshes; THIVL, 1983: 178) and then stained in Rose Bengal for several hours. Sieved fractions were placed in a Petri dish and sorted for m e t a z o a n s (PFANNKUCHE and GOODAY, in preparation) and foraminiferans under a stereomicroscope. The foraminiferans were separated into putative species and preserved where possible. Hard-shelled species were mounted dry on micropalaeontological slides; forms with soft, flexible tests were preserved either in small vials of 2% formalin or in anhydrous glycerine in cavity slides. Extracting and evaluating foraminiferans is so timeconsuming that it was possible to sort completely only eight sub cores (Table 1). The Table 2.

The distribution of selected species among size fractions

Ovammina sp. Lagenammina B Leptohalysis aff. catenulata Reophax micaceus " T u r r i t e l l e l l a " laevigata* Indet. T r o c h a m m i n a c e a n t Nonionella iridea

>5(KI

>150

>106

>63

>45

-

2 15

2 4 2 5

262

132 26 85 62 144 17 109

* L i v e plus dead specimens. t A species c o m p o s e d o f coccoliths;

11 74 21 75

I

2

58

309

illustrated in Fig. 11I.

1348

A.J. GOODAY

remainder were sorted for selected species. Another difficulty concerns the quantification of fragmentary tests, a particularly acute problem in the case of large tubular species of the genus Rhizammina. To give a rough estimate of the numerical abundance of such species, all fragments from one layer and the subadjacent layer were regarded as constituting a single individual (this follows the procedure of SNIDERet al., 1984). Distinction between live and dead foraminiferans

The problems involved in using Rose Bengal to distinguish foraminiferans that were alive when captured are well known (BOLTOVSKOYand WRIGHT, 1976: 304-305; DOUGLAS, 1979: 22). Particular care was taken during this study in the enumeration of live foraminiferans. Only those having fresh-looking tests with unabraided and unbored walls and containing dense protoplasm were accepted. The more opaque specimens were broken open so that the nature of the stained material could be investigated. For some species additional criteria were adopted. These included the accumulation of finegrained sediment either around the aperture or coating the test and the presence of pellets of waste material (stercomata) within the test. Komokiaceans are to some extent a special case because the sparseness of their protoplasm usually makes routine identification of live specimens under the binocular microscope impossible. Several komoki from Sta. 51502 were therefore sectioned and found to contain protoplasm. Moreover, specimens examined in the SEM bore structures resembling pseudopodia (Fig. 5). These observations support the view of TENDALand HESSLER(1977: 76) that most komoki are alive when captured. All specimens extracted from the present samples were therefore regarded as living. RESULTS

Size structure

The assemblages of live foraminiferans are dominated by small individuals, the >63 gm residues yielding over a third (37.7%) and the >45 p.m residues more than a quarter (26.8%) of the specimens sorted (Fig. 1). At the larger end of the size spectrum, the 150 gm mesh retained more foraminiferans (18.5%) than the 106 gm mesh (11.9%), resulting in an overall bimodal size distribution. One reason for this pattern is the abundance in the >150 lam fraction of forms inhabiting globigerinacean shells (see below). The coarsest residues (>500 tam) yielded the smallest proportion (5.1%) of specimens. This general size structure is maintained at different sediment levels. However, there is some variation in the relative importance of the >150 p.m residue which contained a greater proportion of live tests in the top 1 cm than it did in deeper layers, a disparity arising partly from the larger numbers of globigerinaceans inhabitants living near the sediment surface. The size distribution of live foraminiferans was also fairly consistent in different subsamples (0-5 cm). The >63 p.m residue always yielded the largest number of specimens while the >500 p.m residue was consistently the least important. Between 11.4 and 28.6% of species were retained on the 500 gm mesh, 45.0-57.3% occurred in residues >150 gm, 55.8-72.7% in residues >106 p,m and 88.4-95.2% in residues >63 lam (Fig. 2). The finest fraction (45-63 p,m) therefore only yielded a few (4.8-11.6%) species not present in coarser residues. Most of these are minute, rare allogromiids and saccamminids. Many of the specimens retained on the finest mesh are

Meiofaunal foraminiferans from the Porcupine Seabight

1349

300

250

200' ii!iiill

Q

.E_

i i:ill i i:i

6

~

100

z 50-

i~i!iiii~i~i!iiiliiii!ii! > 500

~ 150

'> 106

> 45

Size Fractions (IJm)

Fig. l. The distribution of live foraminiferans among size fractions. The bars of the his!ogram show mean values based on 8 subsamples. The vertical lines indicate 95% confidence limits. The darker shading shows the abundance of foraminiferans inhabiting globigerinacean shells.

10o-

u')50

Size

Fig. 2.

Fractions

Cumulative distribution of species among size fractions (pooled data from subsamples la, 2a-d, 6b, 6d).

juveniles of species such as Nonionella iridea Heron-Allen and Earland and Ovammina sp. which are common as adults in the >63 lam fractions. However, the adults of some tiny species are concentrated in the finest residues (Table 2).

Standing stocks The standing stocks range from 431 to 804 per sample (1246--2324 10 cm -2) (Table 3). Foraminiferans account for 46.3-59.2% of all individual meiofaunal organisms and are usually more abundant than the nematodes (37.3-48.1%) (PFANNKUCHEand GOODAY, in preparation).

1350

A.J. GOODAY

Table 3. Standingstocks of foraminiferans, nematodes and total meiofauna (foraminiferans + metazoans) Nematode Total meiofauna % Foraminifera Subsample Foraminiferastanding stock standingstock standingstock among total (subsample l) (10 cm 2) (10 cm 2) (10 cm 2) meiofauna stocks ld 631 1823 1399 3543 51.4 2a 756 2184 1390 3690 59.2 2b 694 2006 1306 35(16 57.2 2c 521 1506 1416 3061 49.2 2d 759 2194 1613 3943 55.6 6b 431 1246 1295 2691 46.3 6d 487 1408 1182 2618 53.8 8a 804 2324 2397 4944 47./I

Taxonomic composition The suprageneric classification used throughout this paper follows that of LOEBL1CH and TAPPAN (1984). The foraminiferal assemblages at Sta. 51502 are dominated by species with hyaline, calcareous tests (suborder Rotaliina), multilocular agglutinated tests (Hormosinacea and various other superfamilies within the suborder Textulariina) and more or less sphaerical, unilocular agglutinated tests (families Saccamminidae and Hemisphaeramminidae of the superfamily Astrorhizacea, suborder Textulariina) (Tables 4 and 5). The saccamminids include species with rigid tests, such as Lagenammina spp., and species with flexible tests, for example Ovammina sp. Members of the suborder Allogromiina, which have proteinaceous tests with at least one aperture, make up 4.9-16.1% of the assemblage. The allogromiids, together with the soft-shelled saccamminids which are closely similar morphologically, are described in detail elsewhere (GOODAY, in press). Noval foraminiferans that appear to be obligate inhabitants of Globigerina and Orbulina shells account for 4.9-14.4%, and in one sample 19%, of the total (Table 4). The protoplasm of the invading foraminiferan fills one or more of the globigerinacean chambers. It is dense, granular and often associated with stercomata. In many cases, structures are developed on the exterior of the shell. These are of two main types: (a) small conical lumps, sometimes with a central depression and composed mainly of coccoliths (Figs 3 D - G ) , and (b) branching tubes consisting of organic material with a veneer of fine sediment and often scattered small globigerinacean shells (Figs 3 H J). A variety of other less common structures also has been found (Figs 3A-C, K; 4A-C). The affinities of these hitherto undocumented forms are obscure, but the presence of external structures composed of organic and agglutinated material suggests a relationship with astrorhizacean foraminiferans. Komoki (suborder Textulariina, superfamily Komokiacea) are rather uncommon. Most specimens are mudballs which are retained on the 150 and 500 lam sieves. They display occasional bead-like chambers, suggesting a placement in the genus Edgertonia (TENDALand HESSLER, 1977). When critical-point dried and examined in the SEM, delicate, anastomosing, thread-like structures are visible on the mudball surfaces (Fig. 5A). These threads may be pseudopodia. In some cases they incorporate "lumps" resembling the granules which typify the pseudopodia of foraminiferans (Fig. 5B). Tubular fragments of genera such as Rhabdammina, Saccorhiza, Dendrophyra and particularly Rhizammina (suborder Textulariina, superfamily Astrorhizacea, family Rhizamminidae) are common in coarser residues. According to the procedure outlined

11.9 3.6 25.1 1.1 13.1 9.3 17.2 0.5 2.1

4.9 3.0 25.8 1.4 9.5 15.5 30.4 1.4 3.0 631

Total numbers

756

16.1

4.9

Allogromiids Globigerina inhabitants Tubes (Rhizamminidae) Sphaerical unilocular agglutinated forms Komokiacea Multilocular agglutinated forms: (a) Hormosinidacea (b) Others Calcareous forms: (a) Rotaliina (b) Miliolina Others

2a

694

25.4 0.9 1.9

8.2 15.8

21.9 4.9

7.8 4.5

8.8

2b

521

22.6 0.6 2.9

7. I 17.7

29.4 3.4

6.7 3.1

6.5

2c

759

22.1 0.7 3.0

9.5 21.9

24.6 1.6

7.8 2.0

6.8

2d

431

19.7 0.7 4.4

3.5 16.9

21.3 2.5

19.0 2.1

10.0

6b

Gross taxonomic composition (in percentages) of the foraminiferal assemblages

ld

Table 4.

Subsample

487

31.8 0.2 4.3

16.4 19.7

8.8 1.0

7.2 4.3

6.2

6d

803

20.9 0.6 2.4

8.8 17.2

22.8 2.1

14.4 3.1

7.6

8a

ALL ALL TSS TSR TSR THS THS TR TR TR THM THM THM THM TM TM TM TM TM TM TM RT RT RT RT RT

Lagenammina sp. B Crithionina sp. A Crithionina sp. A Rhizammina sp. A *Rhizammina sp. B Rhizammina sp. C Leptohalysis aft. eatenulata (Hoglund) Reophax micaceus Earland Reophax aft. subfusiformis Earland Reophax sp. A *Haplophragmoides bradyi (Robertson) Cystammina argentea Earland *Spiroplectammina biformis (Parker and Jones) *Portatrochammina murrayi Br6nnimann and Zaninetti

Trochammina sp. Karreriella sp. "Turritellella" laevigata Earland *Epistominella levicula Resig *Cassidulina teretis Tappan *Nonionella iridea Heron-Allen and Earland

*Pseudononion aft. japonica (Asano) *Melonis barleeanus (Williamson)

Taxonomic abbreviations: ALL, Allogromiida; TSS, Textulariina, Saccamminidae (unilocular, flask-shaped, soft-shelled); TSR, Textulariina, Saccamminidae (unilocular, flask-shaped, rigid-shelled); THS, Textulariina, Hemisphaeramminidae (unilocular, spherical); TR, Textulariina, Rhizamminidae (unilocular, tubular); THM, Textulariina, Hormosinidae (multilocular, linear); TM, Textulariina, other multilocular families: RT, Rotaliina, various families. The test wall is proteinaceous in ALL, agglutinated in TSS, TSR, THS, TR, TM and calcareous in RT.

Illustrations GOODAY (in press: Fig. le). GOODAY (in press: Fig. la). GOODAY (in press: Fig. 7a). Fig. 10B. RHUMBLER(1911: pl. 2, Fig. 13; as Proteonina difflugiformis (BRADY)). Fig. 10A. Not illustrated. Not illustrated. Fig. 10C. Fig. 10D; BRADY (1884: pl. 28, Fig. 3). Fig. 10E. Fig. 10F, G. Fig. 10H, I; EARLAND(1934: pl. 2, Figs 37-40). Fig. 10J. Fig. 10K. Fig. llJ; MURRAY(1971: pl. 5, Figs 1, 2). Fig. 10Q, R; EARLAND(1934: pl. 4, Figs 17-19). Fig. 10L; HERON-ALLENand EARLAND(1932: pl. 8, Figs 29, 30). Fig. 100, P; BRONNIMANNand ZANINETTI(1984: pl. 5, Figs 7, 12-15). Fig. 10M, N. Fig. 10S. Fig. 10T, U; EARLAND(1933: pl. 3, Figs 5-8). RESlG (1958: Figs 16a-e). TAPPAN(1951: pl. 1, Fig. 30). Fig. 11A-C, H; HERON-ALLENand EARLAND(1932: pl. 16, Figs 14-16). Figs I 1E-G. Fig. 11D; MURRAY(1971: pl. 84; as M. pompilioides).

Classification

?Nodellum sp. *Nodellum membranacea (Brady) Ovammina sp. *Lagenammina sp. A

Classification and illustrations of species mentioned in text and in Table 6

Species

Table 5.

Meiofaunal foraminiferans from the Porcupine Seabight

A

1353

C

i

,,i

0.5 mm

Fig. 3. Foraminiferans inhabiting globigerinacean shells. (A) Orbulina universa D'Orbigny broken open to show protoplasmic mass and associated organic capsule. (B) O. universa with three tubular structures arising from surface. (C) O. universa with neat, circular hole through which protoplasmic mass is visible. (D-F) Globigerinacean shells bearing small conical lumps with terminal aperatures. (G) Shell with two similar lumps and protoplasm visible through wall (a tube ofAmmolagena clavata (Parker and Jones) is attached to the underside). (H-J) Shells with a variety of tubular structures. (K) Shell with two fine tubes (two agglutinated domes are also attached). Scale = 500 p.m. a b o v e (all fragments f r o m one layer and subadjacent layer = one specimen) these fragments represent only 2.0--4.5% o f the assemblage. Because of their large size, h o w e v e r , they u n d o u b t e d l y m a k e a m u c h larger contribution in terms of biomass. T h e 22 most c o m m o n species include one allogromiid, five unilocular, sphaerical agglutinated species, 11 multilocular, agglutinated species (including four belonging to Reophax and the closely related h o r m o s i n a c e a n genus Leptohalysis), and five rotaliids (Tables 5 and 6). O n e o f the globigerinacean inhabitants m e n t i o n e d a b o v e (with an external agglutinated lump) is also c o m m o n , but is o m i t t e d due to uncertainty about w h e t h e r it represents m o r e than one species. T h e two most frequently occurring species are a rotaliid (Nonionella iridea) and a saccamminid (Ovammina sp.).

1354

A . J . GOODAY

0.5 mm

l Fig. 4. Globigerinacean shells with complex branched structures arising from wall. (A) Orbulina universa. (B) Globigerina sp. (C) Globigerina sp. with single, smaller structure. Scale = 500 ~tm.

Species diversity Between 121 and 124 species were present in individual subsamples with the exception of 6d which yielded only 95 species. Values for the Shannon-Weaver diversity index (H"), Equitability (EH") and the Fisher diversity index (c~) are also high, ranging from 3.71 to 4.09, 0.81 to 0.86 and 40 to 63, respectively. The top 1 cm of sediment contains 80-105 species. Diversity values for this layer are somewhat lower (H" = 3.72-3.89; = 37-47) than those derived from the complete 0-5 cm interval, but EH" is somewhat higher (0.83-0.86). The distribution pattern of specimens among species in one of the subsamples (Fig. 6) is typical for all those studied. Relatively few species are abundant and many are rare, about half (42-55%) being represented by single specimens and 11-19% by two specimens. As explained above, fragmented species are considered to be represented by single individuals.

Vertical distribution within the sediment Between 52.3 and 71.0% of the foraminiferans within the top 5 cm of sediment live in the upper 1 cm, 73.6-84.6% in the upper 2 cm, 88.6-91.5% in the upper 3 cm, and 94.0-98.2% in the upper 4 cm. Species richness also decreases with sediment delbth: 80-97 (0-1 cm), 25-57 (1-2 cm), 10-32 (2-3 cm), 11-23 (3-4 cm), 5-20 (4-5 cm). It is the distribution of individual species which underlies the overall vertical structure of the community. The 20 or so most abundant species display several general types of distributions (Fig. 7): (a) species which are largely restricted to the top 1 cm with few, if any specimens occurring deeper (Figs 7A-G); (b) species living mainly in the upper 2 cm but to some extent penetrating below this level (Figs 7H-K); (c) species that are rather irregularly distributed but have a tendency to be more abundant in the upper 1 cm (Figs 7L-O); (d) infaunal species found throughout the interval sampled but distinctly less abundant in the top 1 cm and usually with an abundance peak between 1 and 3 cm (Figs

SEM micrographs of critical-point dried foraminiferans. (A,B) Surface of komokiacean

(C,D) Indeterminate mudball (not a komokiacean) broken open to show cavities with stercomata and protoplasm. Scales = 1 t.im (B), 5 ~m (A)~ 20 p.m (D), 50 jam (C),

(?Edgertonia sp.) showing anastomosing threads (?pseudopodia) with granule-like swellings.

Fig. 5.

1357

Meiofaunal foraminiferans from the Porcupine Seabight

Table 6. Rank

The 22 most abundant species at Sta. 51502

Species*

1 2 3 4 5 6 7

Nonionella iridea Ovammina sp. Haplophragmoides bradyi Leptohalysis aff. catentdata ?Nodellum sp. Lagenammina sp. A Pseudononion aff. japonica "Turritellella" laevigata Reophax micaceus Cystammina argentea Karreriella sp. Cassidulina teretis Crithionina sp. A Portatrochammina murrayi Melonis barleeanus Spiroplectammina biformis Trochammina sp. A Epistominella levicula Reophax aff. subfusiformis Crithionina sp. B Reophax sp. A Lagenammina sp. B

7

9 10

11 11 1`3

14 1`5 16 17 18 19 20 21 22

Number;

% Total

346 263 181.) 159 140 109 108 108 78 77 62 62 59 58 57 56 51` 47 43 41. 40 39

6.81 5.18 3.54 3.12 2.75 2.14 2.13 2.13 1.53 1.52 1.22 1.22 1.1`6 h 1`4 1.12 1.10 1.00 0.92 0.85 0.81 0.79 0.77

* Globigerinacean inhabitants are omitted because of taxonomic uncertainties (see text). t Subsamples 2a-d, 6b, 6d, 8a. Data from ld are omitted because not all species were consistently recognized in this subsample.

iI

4c

~iiiiii1111]ill

2b

26

2C

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II

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O',

0

]1111]111},,,,.,, III .......... ,io 6b

IIII1[1[11 I l t l l [ i l l l l l ] 4b

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=======!a=~J=,~LL=====~==

~l~,,~j,,,,,~,,,~,,,,:,,,,,j,,,,,,,,,,,~,,~,j,,

80

ioo

12o

Number of Species

Fig. 6. Species abundance patterns for subsample 2a. (A) Total diversity (0-5 era). (B) Diversity within 0-1 cm layer. (C) I.-2 cm layer. (D) 2-3 cm layer. (El 3-4 cm layer. (F) 4-5 cm layer.

1358

A . J . GOODAY

Number of Specimens 0

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s

5

Fig. 7. Vertical distribution patterns within the top 5 cm of sediment of the abundant species. The bars show the mean numbers of specimens occurring in each 1 cm thick layer; 95°/,, confidence limits are given by the horizontal lines. The number of subsamples (s) and the total numbers of specimens (n) on which each diagram is based are indicated below. (A) Ovarnmina sp. (s = 20, n = 652). (B) Lagenammina sp. A (s = 8, n = 119). (C) Portatrochammina murrayi (s = 8, n = 69). (D) Crithionina sp. A (s = 8, n = 69). (E) Crithionina sp. B (s = 8, n = 64). (F) Cassidulina teretis (s - 8, n = 72). (G) Reophax aft. subfusiformis (s = 7, n = 43). (H) Nonionella iridea (s = 20, n = 823). (I) Reophax micaceus (s = 8, n = 90). (J) Reophax sp. A (s = 8, n = 52). (K) Epistominella levicula (s = 8, n = 61). (L) Leptohalysis aff. catenata (s = 7, n = 159). (M) ? Nodellurn sp. (s = 7, n = 118), (N) Lagenammina sp. B (s = 8, n = 41/). (0) Cystammina argentea (s = 18, n = 133). (P) Haplophragmoides bradyi (s = 19, n = 379). (Q) Karreriella sp. (s = 14, n = 103). (R) Trochammina sp. A (s = 7, n = 51). (S) Pseudononion aff. japonica (s = 18, n = 174). (T) Melonis barleeanus (s = 9, n = 80). (U) "Turritellella" laevigata (s = 21, n = 280). (V) Nodellum membranacea (s = 20, n = 66). (W) Indeterminate saccamminid (s = 18, n = 48).

7 P - T ) . "Turritellella" laevigata E a r l a n d h a s t h i s t y p e o f p a t t e r n ( F i g . 7 U ) e x c e p t t h a t t h e d i s t r i b u t i o n is r a t h e r u n i f o r m b e l o w 1 c m , p o s s i b l y r e f l e c t i n g a g r e a t e r d e g r e e o f w i t h i n sediment mobility of this smooth cylindrical species. Other types of depth-frequency patterns are displayed by two less common species. A soft-walled saccamminid which o c c u r s i n s m a l l n u m b e r s i n m o s t s a m p l e s is u s u a l l y f o u n d b e t w e e n 3 a n d 5 c m , a n d is almost entirely absent above 2 cm (Fig. 7W). An allogromiid, Nodellum membranacea (Brady), normally a rare species but fairly common in samples 4b and 4c, actually increases progressively in abundance with sediment depth (Fig. 7V). The distribution

Meiofaunal foraminiferans from the Porcupine Seabight

1359

patterns are broadly consistent both within and between sets of cores. There may be some variation in the position of the maximum abundance peak, but this usually is not more than 1 cm. Of the three Rhizammina species found at Sta. 51502, species A and B both occur mainly in the upper 2 cm (Fig. 8), although to some extent they penetrate more deeply. In the case of Rhizammina sp. B, this pattern can be explained by careful examination of complete cores. The long branched tubes of this species lie draped across or buried just below the sediment surface, but with occasional branches extending down further into the core. Fragments of Rhizammina sp. C, on the other hand, are entirely absent from the top 1 cm and most abundant between 2 and 4 cm, a depth at which the two congeners are not usually present. The gross taxonomic composition of the assemblage changes with sediment depth in response to the vertical zonation of its constituent species (Fig. 9). In general, multilocular agglutinated foraminiferans are relatively more important at deeper levels due to the Length of Test Fragments (mm) 0

100

0

100

200

0

100 O

-g

Fig. 8. Vertical distribution within the sediment of Rhizammina spp. expressed in terms of the total lengths of fragments occurring in each layer. (A) Rhizammina sp. A , ( B ) Rhizammina sp. B , ( C ) Rhizammina sp. C. Percent of total fauna 0-1

0

10 t

20

30

40

7 /

jf

1-2.

~

\

._E

"~ 2 - 3 m .E

3-4

d//

//

%

III/

' iJ:::f Fig. 9. Relative abundance of major taxonomic groups in different sediment layers (pooled data from subsamples l d , 2 s - d , 6 b , 6 d , 8 a ) . The groups are as follows: a = rotaliids: b = multilocular, agglutinated forms other than hormosinaceans; c = h o r m o s i n a c e a n s ; d = s p h a e r i c a l , uniloc u l a r , agglutinated forms; e = a l l o g r o m i i d s ; f = globigerinacean inhabitants; g = other groups.

1360

A.J. GOODAY

increased abundance of infaunal species, particularly Haplophragmoides bradyi, Karreriella sp., Trochammina sp., "Turritellella" laevigata. The rotaliids are proportionally most important between 1 and 3 cm depth, and this reflects the distributions of the common species Nonionella iridea, Pseudononion aft. japonica (Asano) and Melonis barleeanus (Williamson). Single chambered agglutinated species are concentrated in the upper 1 cm to which layer Ovammina sp., Lagenammina sp. A and Crithionina spp. are largely restricted. Allogromiids maintain a fairly consistent proportion of the assemblage with depth in the sediment, the high percentage between 3 and 4 cm being due largely to the abundance of ? Nodillum sp. in a single sample. DISCUSSION

Size structure Counting the numbers of specimens retained on sieves of different mesh size is a crude way to determine the size structure of a population because the distribution of individuals among fractions inevitably will be influenced by their shape as well as their size. Foraminiferans pose special problems because the volume of protoplasm is less than the test volume. Generally, therefore, specimens will be retained on coarser meshes than non-testate organisms of equivalent biomass (THIEL, 1983:170). However, this method can yield useful results (PFANNKUCHE, 1985). The assemblages in the present samples are dominated by small individuals with more than 60% of specimens being retained on the >45 and >63 ~tm meshes. In part, this undoubtedly reflects the size of the subsamples. Only foraminiferans <100 pm will be collected adequately by samples as small as 3.46 cm 2 (DOUGLAS, 1979: Fig. 1). TO document properly the larger species, much bigger samples are required; for example, around 100 cm 2 in the case of foraminiferans 500 pm in diameter. Sorting large volumes of sediment means, however, that the finer residues cannot be examined if the material is to be processed on a realistic time-scale. Thus, many deep-sea studies have dealt only with the coarser residues, in some cases >150 pm (DouGLASand WOODRUVV,1981: Table 1, Fig. 4), thereby missing the very small specimens. The abundance of foraminiferans in the >45 and >63 ~tm fractions is consistent with the size structure normally found among deep-sea meiofaunal populations. THIEL (1983.:168), summarizing data of 63 samples from different depths beyond the shelf break, showed that 44-48 and 21-27% of meiofaunai organisms occurred in the 65-100 and 42-65 pm size fractions, respectively. PFANNKUCHE(1985:Fig. 4) found that nematodes were most abundant in the >42 and >65 tam residues of samples obtained at 20004850 m in the Porcupine Seabight. The overall size distributions within benthic communities have been investigated by SCHWXNGHAMER(1981). He identified three biomass peaks corresponding to organisms with equivalent spherical diameters in the ranges 0.5-1 ~tm (bacteria), 64-125 pm (interstitial meiofauna) and >2 mm (macrofauna). The abundance of small foraminiferans in the present samples is not incompatible with SCHWINGHAMER'S (1981) findings. The presence of a secondary peak in the 150-500 pm size range is anomalous but can be explained partly by the occurrence at Sta. 51502 of foraminiferans which inhabit globigerinacean shells. These forms favour the larger shells which are concentrated in the >150 ~tm residues. Minute tests such as those retained on the 45 lam mesh are known to geologists as "microforaminifera" (BoevovsKoY and WRIGHT, 1976:210). These are now considered to

1361

Meiofaunal foraminiferans from the Porcupine Seabight

include mainly the juvenile stages of normal sized species and usually are neglected. Many specimens in the 45-63 tam residues of the present samples are indeed juveniles, for example Nonionella iridea, but adults of several important species also are concentrated here (Table 2) and their abundance would have been underestimated seriously had these residues not been examined. Evidence for the existence of even smaller foraminiferans is provided by the work of BURNETr(1977, 1979, 1981) and SNIDER et al. (1984) on the deep-sea nanobiota [a term introduced by TnIEC (1983) for organisms >2 and <42-50 lam]. For example, BURNErr (1979) recorded a variety of testate protozoans in the San Diego Trough, including multichambered (10-15 lam) and singlechambered (10-30 ~tm) types which were probably Foraminifera; these accounted for some 10% of the protozoans in the nanobiota (BuRNEVr, 1981: 659). Standing stocks The densities recorded in this study were consistently > 1000 live specimens per 10 c m 2 and in four subsamples exceeded 2000 per 10 c m 2 (Table 3). These values are high for the deep sea. In general, foraminiferal standing stocks beyond the shelf break are <200 per 10 cm 2 and at abyssal depths they are often much lower (MURRAY, 1973; THIEL, 1975:582; 1983:209; DOUGLAS and WOODRUVF, 1981:1254--1257). Higher figures have been reported, for example in upwelling areas and in regions of low oxygen tension where foraminiferans thrive because macrofaunal predators are scarce (Table 7). However, neither of these conditions prevails in the Porcupine Seabight. It is notable also that Table 7.

Unusually high deep-sea foraminiferal standing crops (live specimens per 10 cm2). The figures are arranged in columns according to whether they were obtained in areas affected by upwelling, low oxygen and~or reduced macrofaunal predation, or neither of these factors

Depth (m)

Upwelling

Low O2/macrofaunal predation

100-199

1300H 10440 SLM 1074-1237U

1750 2050 2300 4750

200-299

l150H 1036-1771U 1470H 20000DCW 1232-1252U 2000DCW 1379U 1000DCW

300-399 400-499 500-599

600-699 700-799 800-899 900-999 2000-2900

1154 9300 1000 5000 2000

Other area

PS PS PS PS

1175 PS 1550 PS 2150 PS

U U DCW DCW DCW

1017 C

2355 SC

COULL et al. (1977) (western Atlantic); D C W = DOUGLAS et al. (1979) (southern California borderland, approximate values based on THIEL, 1983: Fig. 12); H = HAAKE (1980) (eastern Atlantic); PS = PHLEGER and SOUTAR (1973) (eastern Pacific). SC = SCHAFER and COLE (1982) (northwest Atlantic); SLM = SEN GUPTA et al. (1981) (western Atlantic); U = UCHIO (1960) (off southern California). C

=

1362

A.J. GOOI)AY

the present values are based on very small subsamples (3.46 cm 2 surface area). DOUGLAS et al. (1978) concluded that much larger samples (a few tens of cm 2) are required to document deep-sea foraminiferal populations adequately. The results reported here suggest, therefore, that foraminiferal standing crops have been underestimated in most, if not all previous investigations. This may be due to several factors. First, the finest sieve used :o process the samples was 45 lam, close to the lower size limit for the meiofauna (42 ~tm) recommended by Tn[EL (1983). However, the finest mesh normally used by geologists, who have provided many of the available data on deep-sea foraminiferans, is 62 ~tm and studies often have been based on much coarser meshes (DOUGLASand WOODRUFF, 1981: Table 1). A considerable proportion of the foraminiferal standing stock, as well as some of the important species (ScHNITKER, 1980), was thereby lost. A second factor may be the virtually undisturbed character of the samples collected by the Multiple Corer. Many Foraminifera live in or on the topmost flocculent sediment layer, which is blown away by the bow wave preceeding most other sampling devices (TItlEL, 1983:171 ; ELEFTttERIOUand HOLME, 1984; DOUGLASet al., 1978). The abundance of allogromiids also points to the high quality of the present samples. In shallower-water environments these foraminiferans are known to reside on the sediment surface (NYIIOLM and GERTZ, 1973: Fig. 9) where their light, delicate tests make them particularly susceptible to being pushed aside by the bow waves of descending corers. JUMARSand HESSLER(1976: 551) also invoked a decreased bow wave effect to help explain why their box core from the Aleutian Trench yielded a much higher standing crop than previous trench samples. A third probable factor is that samples were sorted wet and great care was taken to pick out obscure forms with proteinaceous or agglutinated tests. Between 16 and 40% of the populations were represented by allogromiids, soft-shelled saccamminids, and forms occupying globigerinacean shells; probably all of these would have been missed in a geologically orientated study, particularly if the samples had been dried before sorting. Structures such as mud balls and concretions of Globigerina shells were also examined carefully to determine whether they harboured or were themselves foraminiferans (TIIIEL, 1975: 583). The conclusion of THIELet al. (1975) that up to 30% of living, meiofaunal-sized foraminiferans from the San Diego Trough were counted only after samples had been treated ultrasonically emphasizes the fact that many live specimens are missed during the routine sorting of deep-sea material. Previously published values for the percentage of foraminiferans among the total meiofauna show a wide range, from <1 to >90% (Table 8). The proportion at Sta. 51502, approximately one half, is in closest agreement with the data of Stt[RAYAMA (1984a) on rhizopod biomass in the western Pacific and also that of SNIDERet al. (1984) on foraminiferal abundance in the central North Pacific. Taxonomic composition

The relative abundance of allogromiids, soft-shelled saccamminids and globigerinacean inhabitants is of particular interest because these organisms are reported rarely in the deep-sea literature. Previous records of aliogromiids and soft-shelled saccamminids are discussed elsewhere (GooDAY, in press). Foraminiferans occupying globigerinacean shells have never been described before, although RUTGERSVAN DER LOEFFand LAVALEYE (1984) noted some possible specimens in samples from the abyssal northeast

i

.j ~÷

H

M

Fig. 10. Common foraminiferans occurring at Sta. 515112. (A) Lagenammina sp. B, (B) Lagenammina sp, A, (C) Rhizammina sp. A, (D) Rhizammina sp. B, (E) Rhizammina sp. C, (F,G) Leptohalysis aff. catenulata, (H,I) Reophax micaceus, (J) Reophax aff. sut~fusi]brmis, (K) Reophax sp. A, (L) Spiroplectammina biformis, (M,N) Trochammina sp., (O,P) Portatrochammina murrayi, (Q,R) Cystammina argentea, (S) Kurreriella sp., (T, U) "Turritel/e//a" laevigata. (A,B,H-P,R,S,U) SEM micrographs: (C-G,Q,T) light micrographs. Scales = 1(I ram (A), 25 p,m (G,L,O,P,T,U); 5(I [am (B,H,I,M,N,Q-S)" 101) lain (F,J,K), 2 mm (C-E).

Fig. 11. Common foraminiferans occurring at Sta. 51502. (A-C) Nonionella iridea, (D) Melonis barleeanus, (E-G) Pseudononion aff. japonica, (H) Nonionella iridea in sediment capsule, (I) Trochamminacean composed of coccoliths, (J) Haplophragoides bradyi. (A-E,G-I) SEM micrographs; (F,J) light micrographs. Scales - 25 1am (A-C,H,I); 50 lain (E-G,J); 100 lam (D).

Meiofaunal foraminiferans from the Porcupine Seabight

Table 8.

1365

Published data for proportion of Foraminifera among total meiolauna in deep-sea samples

Area

D e p t h (m)

% Foraminifera

Number of samples

Western Atlantic

50-499 51111-999 10110-1999 2000-2500

1.9-24.1 11.11173.8 72.9-86.3 75.4-911.4

7 4 6 4

Western Atlantic

4110 8/t11 4000

7.6-81.9 7.4-72.2 22.2-85.9

13 7 8

Western Atlantic

146-567

3.4-1t).6

4

Puerto Rico Trench

8560-8580

"Little numerical significance"

Eastern Atlantic

250-1250 1250-2250 2750-4250

8-27 2-25 4-15

15 7 4

Eastern Atlantic

4000-481111

0.5-8.2

9

RUTGERS VAN DER LEOFF and LAVALEYE (1984)

Western Pacific

2000-2999 3000-3999 4000-4999 511111115999

36.11158.3 47.9-64.9 51.0 55.6-69.3

4 3 l 3

StHRAYAMA (1984a)*

Central North Pacific Arctic

5821-5874 1000-1499 1600-1999 2000-2599

49.5 24.6-80.6 75.2-85.5 14.5-84.1

2 39 33 2

227 1661 168t1

18.7 2.2 23.7

Southern Ocean

Authors T|~!TmN (1971)

CotuJ. e; al. (1977)

W|(;I£Y and MC][NTYRE (1964) GEORGE and HIGGINS (1979)

1 1 1

TllIEL (1975)

SNn)ER et al. ( 19841 PAUL and MENZmS (I974)+

PARULEKAR el al. (1983)

* Rhizopod biomass. -i- Foraminiferan biomass from displacement volumes.

Atlantic. An obvious advantage to this mode of life is the acquisition of a hard, calcareous covering at little energetic expense. It is important to distinguish between invading foraminiferans and globigerinacean shells which contain the protoplasmic remnants of their original inhabitants. The latter, which are quite common in the present samples, have been noticed by several authors (HEDLEY, 1966; SAIDOVA, 1970: 147; BOLTOVSKO¥ and LENA, 1970). These specimens contain material which stains with Rose Bengal in one or two chambers. However, this rather featureless material cannot be confused with the protoplasm of invading foraminiferans, which is denser, more granular and often is associated with stercomata as well as external structures such as agglutinated lumps and tubes (Figs 3 and 4). Several of the common species at Sta. 51502 have never been recorded before in the northeast Atlantic (Table 5). Some are almost certainly undescribed (Crithionina sp. A, Crithionina sp. B, Lagenammina sp. B, Leptohalysis aft. catenulata, ?Nodellum sp. Ovammina sp.) and one (Cystammina argentea Earland) has been known hitherto only from the Southern Ocean. There are several reasons why such species could have been overlooked in earlier studies (cf. JENSEN, 1983: 320). ?Nodellum sp. may not have been recognized previously as a foraminiferan because of its very elongate, needle-like shape. Probably, Ovammina sp. would be unrecognizable in dried samples, and its light test may

1366

A.J. GOODAY

be pushed aside easily by bow waves. Tiny species such as Lagenammina sp. B, Leptohalysis aft. catenulata, R. micaceus and "Turritellella" laevigata (the last two having been reported only once outside Antarctic waters) are retained only in the finest residues (>45 p,m and >63 ~tm; see Table 2) which are rarely examined in deep-sea studies. Finally, infaunal species like "T". laevigata and Pseudononion aft. japonica would have been missed in studies dealing just with the top 1 cm of sediment (e.g. PEARCE, 1980).

Species diversity The data on species richness and diversity presented here are provisional because, except for the more abundant species (Table 5), taxonomic studies have not extended much beyond the recognition of morphologically distinct entities. Little is known about intraspecific variability among deep-sea foraminiferans, and the possibility that variants have been counted as species certainly exists. This danger is especially acute in the case of allogromiids, which are known to display morphological plasticity in shallow-water environments, and of forms represented by single specimens. Special care has been taken in the recognition of such species. Another possible source of error is species lumping. In particular, I am hesitant about some of the forms that occupy globigerinacean shells and display few potential taxonomic characters. In most cases the main morphological types are treated as single species, but as mentioned above, I am aware that some may include more than one species. However~ the effect of these uncertainties is minor and unlikely to affect the general level and pattern of diversity reported here. The occurrence at Sta. 51502 of relatively few abundant species, and numerous rare ones, is consistent with the pattern of species abundance normally found among deep-sea foraminiferans (ScHNITKER, 1980: Fig. 1; DOUGLASand WOODRUFF, 1981: Fig. 20). However, values for the Shannon-Weaver and Fisher diversity indices derived from the present samples are higher than any previously reported for deep-sea foraminiferans (BuzAs and GIBSON, 1969; GmSON and BUZAS, 1973; MURRAY, 1973; LAGOE, 1976). This probably reflects the methods used in collecting and processing the material, as discussed above. Comparable, or even higher diversity levels have been recorded for other deepsea meiofaunal taxa, for example, nematodes (DINET and VJVIERS, 1979; TIETJEN, 1984; THISTLEand SHERMAN, 1985) and harpacticoid copepods (COULL, 1972). Vertical distribution within the sediment JUMARSand ECKMAN(1983: 437) expressed grave doubts about the reliability of most data on the vertical distribution of organisms in deep-sea sediments. They argued that it is impossible to prevent animals moving after sampling; a particular problem in the case of large, active, burrowing organisms such as polychaetes. Some shallow-water foraminiferans are able to drag themselves through sediments, either in search of food (FRANKEL, 1975a) or to escape following sedimentary burial (LEE et al., 1969: 58). According to SEVERIN and ERSK1AN(1981) and SEVERINet al. (1982), Quinquiloculina impressa Reuss takes several days to burrow vertically through 5 cm of sand. Higher rates of movement through a variety of sediments were reported by RICHTER (1961: 166) for Nonion depressulum (Walker and Jacob) (3.0-3.5 mm h-l) and by KITAZATO(1981: Table 2) for several calcareous and agglutinated species (0.84-30.0 mm h-l). It is therefore possible that some vertical movement of foraminiferans may have occurred during the recovery of core samples. However, one observation suggests that at least some important species remained static. Live specimens of Nonionella iridea, Pseudononion aft. japonica and

Meiofaunal foraminiferans from the Porcupine Seabight

1367

Haplophragmoides bradyi are usually enveloped, either partly or completely, in a delicate capsule of fine sediment which almost certainly would have been sloughed off if they had moved. The morphology of large, branched, tubular forms such as Rhizammina spp. A-C must preclude any movement within the sediment. Errors in the vertical distribution data may result also if specimens are dragged down by the syringe barrel during subsampling. The occurrence in subsurface layers (1-2 cm) of occasional specimens of Ovammina sp., a species which probably lives epifaunally, indicates that this may have happened. However, these apparently displaced specimens are uncommon and are not believed to be a serious source of bias. The general consistency of the depth-frequency patterns for individual species also argues for the basic reliability of these results. Data on the overall vertical distribution of Foraminifera in deep-sea sediments are given by THIEL (1975: 583), COULLet al. (1977), TENDAL and HESSLER (1977: 176; komokiaceans only), BASOVand KHUS~D(1983), SHIRAYAMA(1984b) and SNIDERet al. (1984). The depth frequency patterns at Sta. 51502 are most similar to those of SH1RAYAMA(1984b) for rhizopod biomass in western Pacific box cores. There is a greater concentration (52.3-71.0%) of specimens in the upper 1 cm than reported either by THIEL (1975) or COULLet al. (1977) from the eastern and western Atlantic, respectively. This disparity may reflect the virtually undisturbed character of the Multiple Corer samples. The even greater proportion of near-surface dwelling foraminiferans observed by TENDALand HESSLER(1977) and SNIDERet al. (1984) in box cores from the central North Pacific is probably due to the low food supply and low sedimentation rates that characterize this oligotrophic area (THIEL, 1983: Fig. 3). The overall decrease in foraminiferal numbers with sediment depth conforms well with the vertical patterns normally found among meiofauna and macrofauna in the deep-sea (THIEL, 1983: 182-185; JUMARSand ECKMAN, 1983: 437--438, 443; SH1RAYAMAand HORIKOSHI, 1982; SumAYAMA, 1984b; RUTGERSVAN DER LOEFF and LAVALEYE, 1984: 35-39; PFANNKUCtfE, 1985). As discussed below, such patterns probably reflect the distribution of utilizable food within the sediment. There are few published data on the vertical distribution of rhizopod taxa in deep-sea sediments. TENDALand HESSLER(1977) found komokiaceans to be most diverse in the 0-1 cm and 1-2 cm layers with few species persisting below 2 cm. There was some evidence that species were segregated vertically. Some were most abundant in the 1-2 cm layer, and five species were entirely absent from the upper 1 cm of sediment. BAsov and KH~SID (1983: 493), on the other hand, observed little change in the foraminiferal species assemblages with sediment depth. A macrofaunal xenophyophore, Occultammina profunda Tendal, Swinbanks and Shiravama, was discovered living infaunally in box-core samples from the western Pacific (8260 m depth) (TENDAL et al., 1982). Fragments were concentrated between 1 and 6 cm and were most abundant in the 1-3 cm interval. Morphologically, this branched, tubular rhizopod resembles the three Rhizammina species found at Sta. 51502, one of which is also infaunal (Fig. 8). The first detailed information on the vertical distribution of foraminiferan species within deep-sea sediments has been published recently by CORLISS(1985). In two northwest Atlantic boxcores (3000 and 4800 m depth), Hoeglundina elegans (D'Orbigny) was the dominant species in the top 2 cm of sediment while Melonis barleeanus was dominant in the 1-6 cm interval and particularly abundant between 2 and 3 cm depth. Globobulimina affinis (D'Orbigny) and Chilostomella oolina (Schwager) were the most important species

1368

A.J. GOODAY

between 6 and 15 cm and reached their maximum abundance in the 7-9 cm interval. For other meiofaunal groups in the deep sea, there appear to be no data available on sediment depth-frequency patterns at the species level (JuMARSand ECKMAN, 1983: 443). However, JUMARS(1976) published histograms showing the distribution of macrofaunal polychaete species in San Diego Trough sediments. These appear to indicate some degree of vertical segregation among subsurface dwelling species. These published observations indicate that species may be vertically stratified in deepsea sediments, a conclusion supported by the present data. Before speculating on the mechanisms which may be maintaining the patterns observed at Sta. 51502, it will be useful to consider briefly the rather extensive literature dealing with the vertical distribution of meiofauna in shallow water and intertidal environments (see BRANCtt, 1984:503--505 for a general review of stratification in soft-bottom communities). Vertical species zonation has been observed in several taxa, for example, harpacticoid copepods, tardigrades, oligochaetes, nematodes, gastrotrichs and turbellarians (FENCHELand JANSSOY, 1966; WIESNERet al., 1974; GIERE and PFANNKUCItE, 1982; WARWICKand GEE, 1984; FLEEGER and GEE, 1986 and papers quoted therein). Similar patterns are also found among marine ciliates (FENCUELand JANSSON, 1966; FENCnEL, 1969, 1971). A decisive r61e in controlling sediment penetration in these organisms is generally attributed to gradients in the redox potential (i.e. to oxygen availability) (FENCHELand JANSSON, 1966; FENCtlEL, 1969, 1971, 1978; FENCtIELand RIEDL, 1971; GIERE, 1973; McGumE, 1977; PLATT, 1977). For example, FENCHEL(1969: p. 96) found that ciliate species moved up and down with the redox discontinuity and (p. 99) that the zonation pattern broke down when the whole sediment column became oxidized. Other environmental factors which may be involved in shallow-water and intertidal environments include pH, temperature, salinity (WIEsER et al., 1974; WIESER, 1975), the availability and stratification of different food types, and diffusion gradients originating from the sediment-water interface (GIERE, 1973: 187; PLATF, 1977: 270; GIERE and PFANNKUCHE,1982: 244; JENSEN, 1983: 325; FLEEGERand GEE, 1986). Interactions between species, rather than environmental gradients, also have been implicated in the maintenance of vertical zonation among meiofauna (FLEEGER and GEE, 1986). Thus HOGUE (1978: 219) suggested that an unusually large number of gastrotrich species were able to coexist in a subtidal sand flat off South Carolina because they partitioned their habitat vertically. Similar examples among macrofaunal organisms are discussed by BRANCh (1984: 503). In deep-sea sediments the maximum depth at which organisms can live seems to be controlled mainly by oxygen availability (SHIRAYAMA, 1984b). Usually, the sediment porewaters are oxygenated to depths well below 5 cm (MURRAYand GRUNDMANIS,1980; TmEL, 1983: 181; WILSONet al., 1985). At Sta. 51502, a colour discontinuity at 9-10 cm may mark the lower limit of oxygen penetration. In the presence of oxygen, the overall vertical distribution of meiofauna is probably dictated largely by food availability (THEL, 1983: 182; StnRAYAMA,1984a). Thus, PFANNKUCttE(1985: 352) demonstrated a positive correlation in different sediment layers between the abundance of metazoan meiofauna and food, the latter being measured by chloroplastic pigment concentrations. The concentration of the total foraminiferal population in the upper 1-2 cm of sediment at Sta. 51502 is consistent with this model. Many of the common species display a similar distribution. On the other hand, some species are most abundant in the 1-2 or 2-3 cm layer and relatively uncommon in the superficial sediment. These subsurface peaks may be due to chemical or physical factors, such as sediment stratification, or to the chemical gradients known to exist within deep-sea sediments (SIHRAYAMA,1984a;

Meiofaunal foraminiferansfrom the Porcupine Seabight

1369

SNIDER et al., 1985; WILSONet al., 1985). Alternatively, they could result from biotic interactions, with some species avoiding the upper 1 cm or so of sediment because this layer contains large numbers of meiofaunal competitors, both foraminiferal and metazoan. MULLER(1975) showed how interspecific competition can affect rates of feeding and reproduction, and hence population levels, in cultures of salt marsh foraminiferans (e.g. A l l o g r o m i a laticollaris Arnold is abundant only in the absence of dominant species). The increasing scarcity of food with depth (THIEL, 1983: 184) means, however, the infaunal species can not penetrate too deeply into the sediment. Their observed concentration between 1 and 3 cm depth (Figs 7P-U) therefore may be a compromise between the need to avoid competition and at the same time retain access to food. Without experimental evidence, any explanation for these vertical distributions must be speculative. The work of FLEEGER and GEE (1986) on harpacticoids living in an estuarine sand flat demonstrates that competition cannot be assumed to account for the vertical segregation of species. They found that two species, which had distribution patterns in the field suggestive of vertical habitat partitioning, in fact maintained these patterns when isolated from each other in laboratory sediment columns. However, some indirect support for the hypothesis that biological interactions are important at Sta. 51502 is provided by studies on foraminiferans in well-oxygenated, food-rich, shallow-water sediments. Here, live foraminiferans tend to be distributed through the sediment profile in a rather irregular way (DANIELS, 1970: 61; ELLISON, 1972; BUZAS, 1974, 1977; COLLISON, 1980; VENEC-PEYREet al., 1981 ; ELLISONand PECK, 1983). Replicate cores may have rather strikingly different depth-frequency patterns which, in some cases, are attributable to the activities of burrowing macrofauna (DANIELS, 1970; ELLISON, 1972: 252, Table 2; COLLISON, 1980: Table 1; BUZAS, 1977: Table 1). These shallow-water foraminiferal communities therefore display little consistent vertical structure, and presumably this reflects the abundance of nutrients at all levels in the oxygenated part of the sediment profile. Where food is abundant, there seems to be little need for the foraminiferans to concentrate at any particular level (cf. TIIIEL, 1983: 184) or for species to partition the habitat vertically. Foraminifera, and other meiofaunal taxa living in deep-sea sediments, may be subject to a finer system of vertical zonation than can be demonstrated by the present, rather crude method of sectioning subcores. In particular, narrow vertical ranges can be expected to occur in the upper 1 cm or so of sediment, as has been demonstrated by JOINT et al. (1982) and WARWICKand GEE (1984) for intertidal harpacticoids. By analogy with shallow-water forms (NYHOLM, 1957; NYHOLMand GERTZ, 1973), many of the allogromiids found in the 0-1 cm layer, and also the saccamminid Ovamrnina sp., are likely to be sitting directly on the sediment surface or partly immersed within the uppermost flocculent layer. Other species which occupy the top 1 cm may burrow, or occupy microhabitats just below the sediment surface (cf. KITAZATO, 1981, 1984). A more complete understanding of the ecology of the very small species which dominate the present samples can be gained only through investigations which address scales as small as the "operational habitats" (MULLER, 1975: 339) of the organisms themselves (JUMARS, 1976). The work of FRANKEL(1972, 1974, 1975a,b), who was able to document life processes (feeding, reproduction etc.) among foraminiferans preserved in situ in epoxy impregnated cores, provides a good model for such an approach. Acknowledgements--The Multiple Corer samples were provided by J. Watson. Reading University Depart-

merit of Zoology made available SEM and light photomicroscopc facilitiesand the IOS Photographic Unit

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printed the photographs. Mrs C. Darter drew Figs 3 and 4. C. G. Adams and J. E. Whittaker provided taxonomic advice and access to the BMNH collections, R. W. Jones and J. F. Weston also gave valuable advice on foraminiferal taxonomy. J. Malcolm carried out the granulometric analyses of sediment samples. The manuscript was read and commented on by M. V. Angel, O. Pfannkuche, H. Thiel, D. Thistle and M. H. Thurston. I acknowledge with thanks the help of all these people. REFERENCES BARNETI" P. R. O., J. WATSON and D. CONNELLY (1985) A multiple corer for taking virtually undisturbed samples from shelf, bathyal and abyssal sediments. Oceanologica Aeta, 7,399--408 BASOV I. A. and T. A. KHUSID (1983) Biomass of benthonic foraminifers in the Sea of Okhotsk sediments. Oceanology, 23, 489-495. BERGER W. H. (1981) Paleoeeanography: the deep-sea record. In: The sea, Vol. 7, The oceanic lithosphere, C. EMIL1ANI, editor, John Wiley, New York, pp. 1437-1519. BERNSTEIN B. B., R. R. HESSLER, R. SMITH and P. A. JUMARS(1978) Spatial dispersion of benthic Foraminifera in the abyssal central North Pacific. Limnology and Oceanography, 23, 401-416. BILLETT D. S. M. and B. HANSEN (1982) Abyssal aggregations of Kolga hyalina Danielsen and Koren (Echinodermata:Holothuroidea) in the northeast Atlantic Ocean: a preliminary report. Deep-Sea Research, 29, 799-818. BnJ+ETT D. S. M., R. S. LAMPITT, A. L. RICE and R. F. C. MANTOURA (1983) Seasonal sedimentation of phytoplankton to the deep-sea benthos. Nature, 302, 52(/-522. BOLTOVSKOY E. and H. LENA (1970) On the decomposition of the protoplasm and the sinking velocity of the planktonic foraminifers, lnternationale Revue des Gesamten Hydrobiologie, 55,797-804. BOLTOVSKOY E. and R. WRIGHT (1976) Recent Foraminifera, W. JUNK, The Hague, 515 pp. BRADY H. B. (1884) Report on the Foraminifera dredged by the H.M.S. "Challenger" during the years 18731876. Report on the Scienufic Results of the Voyage of H.M.S. Challenger during the years 1873-76, Zoology, 9, 1-814, pls 1-115. BRANCtt G. M. (1984) Competition between marine organisms: ecological and evolutionary implications. Oceanography and Marine Biology Annual Review, 22,429-593. BRONN1MANN P. and L. ZANINETI'I(1984) Agglutinated Foraminifera mainly Trochamminaceae from Baia de Sepetiba, near Rio de Janeiro, Brazil. Revue de Paleobiologie, 3, 63-115. BURNETT B. R. (1977) Quantitative sampling of the mierobiota of the deep-sea benthos. 1. Sampling techniques and some data from the abyssal central North Atlantic. Deep-Sea Research, 24, 781-789. BURNET1- B. R. (1979) Quantitative sampling of microbiota of the deep-sea benthos. II. Evaluation of technique and introduction to the biota of the San Diego Trough. Transactions of the American Microscopical Society, 98,233-242. BURNETr B. R. (1981) Quantitative sampling of microbiota of the deep-sea benthos. III. The bathyal San Diego Trough. Deep-Sea Research, 28, 649-663. BUZAS M. A. (1974) Vertical distribution of Ammobaculities in the Rhode River, Maryland. Journal of Foramini]eral Research, 4, 144-147. BUZAS M. A. (1977) Vertical distribution of Foraminifera in the India River, Florida. Journal of Foraminiferal Research, 7, 234-237. BUZAS M. A. and T. G. GIBSON (1969) Species diversity: benthonic Foraminifera in Western North Atlantic. Science, 163, 72-75. COLLISON P. (1980) Vertical distribution of Foraminifera off the coast of Northumberland, England. Journal of Foraminiferal Research, 10, 75-78. CORLISS B. H. (1985) Microhabitats of benthic foraminifera within deep-sea sediments. Nature, 314, 435-438. COULL B. C. (1972) Species diversity and faunal affinities of meiobenthic Copepoda in the deep sea. Marine Biology, 14, 48-51. COULL B. C., R. L. ELLISON, J. W. FLEEGER+ R. P. HIGGINS, W. D. HOPE, W. D. HUMMON, R. M. RIEGER, W. E. STERRER, H. THIEL and J. H. TIETJEN (1977) Quantitative estimates of the meiofauna from the deep sea off North Carolina, USA. Marine Biology, 39, 233-240. DAN1ELS C. H. (1970) Quantitative 6kologische Analyse der zeitlichen und r~iumlichen Verteilung rezenter Foraminiferen im Limski kanfil bei Rovinj (n6rdliche Adria). GOttinger Arbeiten zur Geologie und Paldontologie, 8, 1-108. DINET A. and M. H. VIVIERS(1979) Le m6iobenthos abyssal du Golfe de Gascogne. II. Les peuplements de N6matodes et leur diversit6 sp6cifique. Cahiers de Biologie Marine, 20, 109-123. DOUGLAS R. G. (1979) Benthic foraminiferal ecology and paleoecology: a review of concepts and methods. In: Foraminiferal ecology and paleoecology, SEPM Short Course No. 6, Houston 1979, Society of Economic Paleontologists and Mineralogists, pp. 21-53. DOUGLAS R. G. and F. WOODRUFE (1981) Deep-sea benthic Foraminifera. In: The sea, Vol. 7. The oceanic lithosphere, C. EMIL1ANI, editor, John Wiley, New York, pp. 1233-1327.

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