the sublittoral macrofaunal benthos of the antarctic shelf

Environment International, Vol. 13, pp. 71-81, 1987 0160-4120/87 $3.00 + .00 Printed in the USA. All rights reserved. Copyright © 1987 Pergamon Journals Ltd.

THE SUBLITTORAL MACROFAUNAL BENTHOS OF THE ANTARCTIC SHELF

V. A. Gallardo Departamento de Oceanologfa, Universidad de Concepci6n, Concepci6n, Chile

(Received 5 March 1986; Accepted 29 March 1986)

A general review of the salient features of the sublittoral macrofaunal benthos of the Antarctic shelf is presented. The need of recognizing a mixed epi-infauna biota, which includes an unusual epi-faunal soft- bottom component, is suggested. This would help the study of the structure of the Antarctic macroben- thos and lend some validity to future quantitative (density and biomass) distribution data. While in large time and space scales the Antarctic environment appears to be rather stable, contributing to a high species diversity, there are sources of disturbances which change the general benthic pattern to a complex mosaic of different successional stages, intergrading with undisturbed communities. Among these sources of disturbance which may be important in structuring benthic communities in Antarctica are anchor ice, ice plucking, ice calving, mud slides, rafted clastic rain, and most important perhaps, iceberg ploughing. The Antarctic benthic realm is unique because of its high taxonomic diversity, widespread endemism, and mostly K-adapted species; biomass is generally high and diverse suspension-feeding communities dominate. There are at present no effective means of establishing extensive protected marine areas or setting aside benthic reserves. SCAR has recognised three marine Sites of Special Scientific Interest, but these have slim chances of being recognized by the Antarctic Treaty itself. While the agreed Measures for the Conservation of Antarctic Fauna and Flora and CCAMLR are not seen as means to develop such extensive marine conservation areas in Antarctica, hope is placed in the Antarctic Minerals Regime which is being negotiated at present. In order to establish a scientifically based scheme for benthic realm conservation, however, both descriptive and experimental research on benthos will have to be greatly expanded around Antarctica.

I n t roduc t ion

By the tu rn o f the cen tury in the n o r t h e r n hemisphe re the s tudy o f sub l i t t o ra l m a c r o b e n t h o s had a l r e a dy en- te red its quan t i t a t i ve synecologica l ( communi ty ) phase , whereas the s tudy o f the m o r e complex A n t a r c t i c benthic c o m m u n i t i e s is j u s t beginning . Several fea tures have been recognised for this system, i .e. h igh species r ichness, w idesp read endemism, the p r e d o m i n a n c e o f K-se lec ted r ep roduc t i ve s t ra tegies , the high s t and ing c rop , and d ivers i ty o f the c o m m u n i t i e s d o m i n a t e d by suspens ion feeders . The de ta i l ed p ic ture is, however , much less c lear and shou ld be the ob jec t ive for fu ture A n t a r c t i c ben th ic research . The es t ab l i shment o f year- r o u n d scient if ic bases and the ava i l ab i l i ty o f research vessels capab le o f work ing in winter and under ice-con- d i t ions will sure ly lead to i m p o r t a n t deve lopmen t s . Con- s ider ing the extent o f the A n t a r c t i c con t inen ta l shelf (35 × 106 k m 2) and the po ten t i a l r isks tha t can ar ise in the A n t a r c t i c e n v i r o n m e n t f r o m poss ib le fu ture exp lo ra - t ion and exp lo i t a t i on o f o f f sho re oil , new knowledge

a b o u t A n t a r c t i c ben thos will be mos t we lcome for An t - arct ic conse rva t ion . In this connec t ion , benth ic research shou ld be pa r t i cu l a r ly o r i en ted t ow a rds the u n d e r s t a n d - ing o f ben th ic c o m m u n i t y s t ruc ture and o rgan i s a t i on , its degree o f res is tance to d i s tu rbances , and the deve lopmen t o f cr i ter ia to es tabl i sh p ro t ec t ed areas large enough to be cons is ten t wi th the fu ture scale o f h u m a n d e m a n d s on the An ta r c t i c m a r i n e env i ronment .

71

The An ta rc t i c Sub l i t to ra l Env i ronment and Its Biota

H e d g p e t h (1957) n a m e d the ben th ic zone ex tending f rom low water m a r k to the shelf edge, the sub l i t to ra l zone, which in mos t par t s o f the wor ld reaches a dep th o f a b o u t 200 m. A r o u n d A n t a r c t i c a , however , because o f the isostat ic pressure o f the ice-cap, it occurs general ly to dep ths o f a b o u t 400-600 m. In the Ross Sea the shelf edge is nea r ly 800 m deep. In genera l the An ta r c t i c sub- l i t tora l zone is qui te na r row except for the two large em- b a y m e n t s o f the Ross and We dde l l Seas, and m o r e o v e r

72 V.A. Gallardo

it is mostly ice-covered. It is with some licence then that the term sublittoral is used in this paper for this environment.

Benthic biota consists of the epifauna, or animals that live on hard substrates, and the infauna, or animals that live in, or intimately associated with, level soft substrates (Thorson 1957). In the Antarctic both types are present, but because of the peculiar nature of the sublittoral deposits, i.e. presence of clastics on soft bottoms and the occurrence of peculiar adaptations for life on soft substrates in certain benthic taxa that otherwise live on hard bottoms, their distinction is very difficult. Thus a third type can be recognised, the epi-infauna, which consists of epifaunal sessile suspension feeders occurring in the midst of a soft substratum. The nature of the Antarc- tic shelf topography and its sediments determines the broad distribution of these types. In the Greater Ant- arctic sector the inner shelf, down to 250-300 m, has a bottom characterised by a tectonical topography of ridges and submarine hills. The rapid subsidence of the continent and rise of sea-level prevented levellihg of the sublittoral and provided abundant hard surfaces on the sea floor, the ideal substrate for the epifauna.

In the Antarctic seas sedimentation of unsorted glacial debris occurs which, with the probable exception of Greenland, is peculiar to the region. Between 75%- 98% of the sediments falling on the Antarctic shelf are of terrigenous origin, the rest being biogenous. The terrigenous material consists of unsorted arenaceous-silty deposits mixed with abundant pebbles, gravel, stones, rocks (Znachko-Yavorsky et al., 1966). Glacial-marine deposits around Antarctica contain clastics (grains larger than 1 mm varying from 10 to 100 kg/m ~ of surficial sediment (Lisitsin, 1960, fide Arnaud, 1974). This sedimentation is affected by the complex interaction of two depositional agents: glaciers and currents (Domack, 1981). The effect of glacial sediments carried by ice is believed to extend to the northern limit of the pack ice, although it is probably more intense closer to the continent (Dell, 1972). This feature favours the development of epifauna in areas of the sublittoral zone that elsewhere in the world contain only infauna. Deposit-feeding infauna requires soft organic-rich sediments, whereas epifauna develops wherever there are solid objects on the surface of the sea floor and sufficient concentrations of suspended particulate organic matter (Rhoads and Young, 1970). It has been suggested that Paleozoic benthos was dominated by soft-bottom suspension feeders and that deposit-feeding infauna evolved later (Thayer, 1979). At present, because of the depositional environment prevailing in the sublittoral around Antarctica, a well-developed suspension-feeding "soft-bottom" epifauna attains its most extreme expression to such an extent that infaunal assemblages appear smothered by it (Mills and Hessler, 1974). A gradual succession occurs across the open shelf from epifaunal communities in-shore to infaunal communities far off-shore. Below 50 m deep

there is a prevailing northward-flowing current which can reach speeds of 0.5-1 knot (Arnaud, 1974). These currents, rich in the organic detritus (diatoms, proto- zoans, plankton debris, etc.), which is the food for the suspension-feeders, keep the sedimentation rate low, e.g. 2-5 cm/1000 years for Adelie Land (Lisitzin, 1960, fide Arnaud, 1974). The sediment that is deposited has a low organic carbon (0.3%-0.5%) content in the nearshore regions (Bordovsky, 1968, fide Arnaud, 1974; Mills and Hessler, 1974; Mills, 1975).

A special type of bottom deposit is composed of sponge spicule mats or felts which can be as much as 65 cm thick off the Banzare Coast, in the Davis Sea and also occur off the coasts of Lars Christensen Land, Mac Robertson Land, Prince Olav Land, etc. It is not known if these sponge spicule mats have accumulated gradually as a result of natural sponge mortality or are the effect of catastrophic disturbance. The hydrographic characteristics of the waters covering the sublittoral zone are highly predictable and stable through a year cycle. For example, Littlepage (1965) found that at 75 m deep in McMurdo Sound there was negligible variation in the mean annual temperature of - 1.87°C, the mean salinity 34.7°o and the mean dissolved oxygen 6.79 ml/l. Only the deep sea shows comparable stability in the physical environment, with the only major seasonal perturbation being the peak in food supply resulting from the spring bloom (Dayton and Oliver, 1977).

Finally, of overriding importance to the biology and evolution of the Antarctic sublittoral benthos is that it has been isolated for approximately 40 × 106 years from adjacent shelf environments by cold deep waters and by the circumantarctic current systems (Dayton and Oliver, 1977). From the isotopic compositions of micro- fossils in oceanic sediments it is suggested that the per- manent ice cap began to form in the Antarctic about 14 × 106 years BP (Shackleton 1982).

This pattern of long time and large space scale stability of the Antarctic benthic environment is overlain by a pattern derived from small time and space scale perturbation by anchor ice formation, iceberg ploughing, ice- calving, and mud slides which may have important influences on the evolution, ecology, and adaptation of the Antarctic benthos.

General Characteristics of the Antarctic Sublittoral Macrobenthic Biota

Knox and Lowry (1977) concluded that the Antarctic is richer than the Arctic in total species numbers in various taxonomic groups by about 50%-100°70 (Fig. 1). Ekman (1953) had already observed that the Antarctic seas were richer in amphipod and echinoderm species than the austral region of South America. Ekman's conclusions foreshadowed important ecological principles when he stated that "It is clear that the Antarctic shelf has been a centre of development for marine

Sublittoral macrofaunal benthos of Antarctic shelf 73

,.o,,o

m m ,.,,.°,,o

eRYOZOANS ~ ISOPOOS

Fig. 1. Comparison of the numbr of species of benthic invertebrates in the Arctic and the Antarctic (from Know and Lowry, 1977),

animals during long geological periods. A cold climate has continued without disturbance from the transition between the Cretaceous and the Tertiary Periods into recent times." He also implied a concept which in benthic community ecology has become known as the "stability- time hypothesis" (Sanders, 1968) when he stated that "Just as the Indo-Malayan fauna is the richest tropical marine fauna in the world and lives in a region which has been exempt from any great climatic changes for longer than for instance the tropical Atlantic, so the richest antarctic marine fauna lives in a polar region which for a very long time seems to have had a constant antarctic climate."

The degree of endemism is a very important feature because it establishes the degree of faunal isolation and provides insights into evolutionary history (Ekman, 1953). Dell (1972) suggested that the high degree of endemism in the Antarctic is one of the few objective measures we have of the degree to which the Antarctic fauna and flora has been isolated, and thus the age of the biota (see Table 1). Knox and Lowry (1977) provided more recent information for selected groups (Table 2). While species endemism ranges from 57°70 to 95070, generic endemism is much lower at 507o-70070 and there is no cor- relation between the two types of endemism. This is taken to show that the extinction and evolutionary rates have varied among different groups of organisms since the Miocene and the increasing cooling, up to the max- imum in the Pleistocene (Menzies et al., 1973). Prior to Jurassic times, shelf faunas of Gondwanaland were strikingly similar, according to these authors. Thus the increasing cooling and extinction of tropical components, which had inhabited Antarctica since the Jurassic, affected each group differently. Certain groups show a decreasing diversity of genera and species such as Mol-

Table 1. Number of species and percent of endemic species for Antarctic shelf groups (from Dell, 1972).

Group No. Spp % Endemic

Littoral fish 49 96 Ascidians 54 90 Holothurians (littoral) 39 85 Echinoidea, Ophiuroidea,

Asteroidea (littoral) 106 77 Crinoidea 16 75 Pycnogonida 77 91 Isopoda 49 78 Mollusca 30 64 Bryozoa 36 89 Nemertea 19 84 Polychaeta 36 31 Actiniaria and Zoantharia 18 87 Scleractinian corals 10 60 Octocorals 16 56 Hydroids 37 55 Hexactinellid sponges 26 77 Sponges (Calcarea) 52 73

lusca, Echinodermata, Cirripedia, and corals. Stoma- topods, well represented in tropical environments, have vanished, and crab-like decapods are represented by only one or a few species. In contrast other groups such as Ascidiacea, Porifera and Sipunculida show an increased species diversity (Menzies et al., 1973). Condi- tions developing in Antarctica seem to have been particularly suitable for peracarid crustaceans as they have undergone speciation (see Isopoda, Tanaidacea, and Amphipoda in Table 2). In cumaceans, another peracarid group, Dell (1972) finds that although 93% of 41 species are endemic to Antarctic and Subantarctic regions no genera are endemic. The important common character which these groups share is the retention of the young in a brood pouch where they develop directly without going through a free swimming larval stage. Brood protection is one of the commonest characteristics of Antarc- tic invertebrates (Arnaud, 1974, 1977), and it has been calculated that at least 1000 species have this character- istic.

The present composition of the Antarctic sublittoral fauna is, however, not only the result of extinctions and

Table 2. Degree of endemism in selected Antarctic groups (from Knox and Lowry, 1977).

Genera Species (%) (%)

lsopoda and Tanaidacea 10 66 Fishes 70 95 Pycnogonida 14 90 Echinodermata 27 73 Echinoidea 25 77 Holothuroidea 5 58 Bryozoa -- 58 Polychaeta 5 57 Amphipoda 39 90

74 V.A. Gallardo

speciation, but also of immigration. In the Magellanic region a number of species have been able to pass along the bridge formed by the Scotia Arc in both directions (Dell, 1969). Comparison of the Magellanic and Antarc- tic regions would clarify the extent to which these ecosystems are mutually dependent.

The Antarctic sublittoral benthos has also been sup- plemented by immigration of deep-living taxa from the abyssal plains. Abyssal species adapted to the cold environment of the deep ocean were preadapted to the climatic conditions of the Antarctic shelf.

Fischer (1961), when presenting data to support the existence of a higher species diversity in the tropics than elsewhere, accepted Thorson's view that among the benthic faunas, only the littoral epifaunistic groups followed this pattern, while the sublittoral infaunas showed no significant species diversity variation with latitude. This cannot be completely upheld in the light of recent knowledge of the tropical and the Antarctic sublittoral faunas. It now appears that both tropical and Antarctic sublittoral benthos have high species richness, together with the deep sea, while the temperate and the Arctic sublittoral have low species richness (Day, 1963; Sanders, 1968; Gallardo, 1968; Gallardo and Castillo, 1969; Gallardo et al., 1977). What is now clear is that the Antarctic sublittoral environment is not a harsh environment for life to adapt to; on the contrary, life there seems to have evolved to high levels of biological diversity in both the population and the community levels of organisation. The Antarctic sublittoral environment is not devoid of environmental instability at the short temporal and small spatial scales, but these do not pose a threat to the benthic ecosystem as a whole but rather perhaps contribute to its diversity and to maintaining reserve capacity for adjustment within the benthic community.

The recognition that the benthic system of Antarctica is evolutionarily mature has gradually led to the aban- donment of attempts to compare the young Arctic and the old Antarctic ecosystems as a single group of polar

u

~o z

I -

N ~° $

L A T I T U D E

Fig. 2. Suggested curve for sublittoral taxonomic diversity. Whether the tropical sublittoral is more, equally, or less diverse than the Ant- arctic sublittoral, it remains to be seen.

or high latitude ecosystems (Dunbar, 1968). It is more fruitful to compare the latter with either tropical ecosystems (Hedgpeth, 1971; Margalef, 1977) or abyssal faunas (Lowry, 1969; Dayton and Oliver, 1977; Lipps and Hickman, 1982).

Figure 2 depicts the distribution of taxonomic diversity, valid perhaps for most of the invertebrate benthic faunas of the world's sublittoral zone.

Beliaev and Ushakov (1957) used quantitative grabs for the first time in the Antarctic. Table 3 summarizes some of their pioneer quantitative Antarctic benthic data. There was an early recognition that the Antarctic benthos had little or no potential as a source of human food but some recent work is examining this subject (Murano et aL, 1982).

Hedgpeth (1969) compared Antarctic and Arctic benthos on the basis of Soviet biomass data and concluded that at comparable depths average biomass ranges from one to several orders of magnitude greater in the Ant- arctic than in the Arctic and that the composition dif- fered markedly in both regions. While in the Barents Sea there is a bot tom assemblage consisting mostly of sponges, the Arctic does not have the dense sponge- Bryozoa associations of the Antarctic. Conversely, the Antarctic lacks the well-developed bivalve ophiuroid assemblages of shallow Arctic waters, although excep- tions to this have been reported recently (Fratt and Dearborn, 1984). Knox and Lowry (1977) noted that at

Table 3. Biomass (g/m s) of major benthic taxa (Greater Antarctica). (from Beliaev and Ushakov, 1957).

Depth Total (m) Sponges Worms Mol luscs Crustaceans P o l y z o a Echinoderms Ascidiams Others biomass

105 2400 50 0.6 -- 0.4 42.6 0.4 - 2494 190 162 4.6 0.4 0.4 - 14 0.2 1.4 183 197 439 75 58 -- 374 132 282 3 1363 210 9 20 0.6 0.5 3.2 0.8 82 -- 116.1 228 ll7 13 11 0.2 30 1.8 11 -- 184 330 138 220 0.2 0.1 -- 120 0.1 4.4 482.8 397 -- 8.8 1.2 8.4 2.4 0.8 16.4 3.2 41.2 420 238 61 39 -- 20 4 10 -- 372 525 0.4 0.8 0.8 0.8 0.8 -- -- -- 3.6 550 10.8 6.2 0.6 0.3 -- 42.5 -- 1.6 62 760 -- 22.5 -- -- -- 22.5 -- 26 71 840 0.8 5.6 0.8 -- 0.6 0.4 -- -- 8.2 910 26 38 0.4 0.8 1.6 0.8 -- -- 67.6

1070 0.6 0.6 . . . . . . 1.2


about 500 m in the Davis Sea the biomass is comparable with that of the Bering Sea, while at depths of 1000 m and less the average values are greater in the Bering Sea. Mills and Hessler (1974), on the basis of samples taken in the South Shetland Islands, concluded that communities inhabiting hard bottoms maintained a high biomass, whereas those of soft bottoms had low biomass values comparable to those found by other researchers (Gal- lardo and Castillo, 1969) in Chile Bay (Greenwich Is- land). Moreover, Mills and Hessler suggested that the low soft bottom biomasses were due to the reduced abundance of epifaunal animals, although epifaunal organisms such as sponges and tunicates were not totally absent from the soft bottoms in the region. In the enclosed waters of the South Shetland Islands and the archipelagos of the Antarctic Peninsula there is a more distinct segregation of epifauna and infauna, similar to that of other latitudes, than occurs on the shelf of Greater Antarc- tica, for example. Recent further observations by the author around the South Shetland Islands lend support to the view of Mills and Hessler (1974) and Mills (1975) that the relatively small biomasses of infaunal organisms on soft bottoms are probably limited by the filter feeders reducing the food material reaching the sediments. The total organic matter content in the surficial sediments of the area averages only 2°7o-3°7o (unpub- lished results). There is also a lack of reduced, anaerobic, or dysaerobic deposits in the Antarctic region sublittoral, except in localised situations of disturbance. While sed- entary epifaunal organisms accumulate skeletal supportive materials (sponge spicules, tunicate tests, bryo- zoan, and coral calcareous skeletons) and associated tissue, the infaunal organisms are usually small forms adapted to burrowing in the sediment and thus have little need for skeletal supportive material. Antarctic infaunal organisms can occasionally attain relatively large sizes as a result of growth with age of a soft body. Mills (1975) suggested that in Antarctic conditions where most of the benthic biomass is in the form of relatively in- digestible filter feeder epifauna with a high ratio of non- nutritive supporting material to digestible parts, preda- tor biomasses, such as those of demersal fish, will be much lower than where the benthic biomass is in the form of relatively more digestible organisms such as polychaetes and bivalves. Thus benthic biomass estimates, if they are to have ecological meaning, must distinguish between the two major benthic biota forms, This poses a problem with the epi-infaunal benthos typical of the Antarctic sublittoral for which adequate quantitative sampling methods are yet to be devised, Bottom photography, coupled with large quadrat sampling of the benthos, may be the best approach. At present benthos biomass estimates are of a very limited value in getting a quantitative picture of the Antarctic sublittoral communities.

In general, however, epifauna appears to have a biomass which may be one or two orders of magnitude larger than the infauna. The biomass of the epi-infauna

consists of a varying combination of both components. The same could be said of the numbers of organisms whose determination is also problematic. In a recent review by White (1984) it was suggested that the observed variations in numbers of organisms per unit area, which range over three orders of magnitude, may be as much the results of natural variability as sampling artefact, e.g. the differences detected by Dayton and Oliver (1977) in McMurdo Sound. In some cases the variation may be due to screen size to process the samples and/or the method of screening, i.e. bulk or float. At present it is not possible to make meaningful comparisons of density between habitats. Furthermore, the observed local density of organisms in a community will depend on the successional stage it had attained after a disturbance. During many postcatastrophic recoveries, a temporary peak occurs either in the value of biomass or the number of individuals (Orensanz and Gallucci, 1982). The abundance of small time and space scale disturbances in the Antarctic sublittoral has been already mentioned, and iceberg ploughing seems to play a major role in shaping the sublittoral benthic community (Kauffman, 1974; Richardson and Hedgpeth, 1977; Moreno et al., 1982; Zamorano, personal communication), with anchor ice formation (Dayton, et al., 1969) and ice-calving (Rich- ardson and Hedgpeth, 1977) being also important.

Although the Antarctic sublittoral is very extensive, the scanty available literature implies that some zonation patterns occur. Three zones have been proposed within the nearshore predominantly rock bottoms down to 50-60 m: (1) a winter anchor ice affected zone to a depth of 10-15 m, (2) a coelenterate-dominated zone (30-35 m), and, (3) a sponge dominated zone, below 30-35 m. This zonation is typical for McMurdo Sound but appears to hold in other areas like the Davis Sea and around the Haswell Islands. It may be generally applicable although subject to localized differences as a result of variations in slope, substrate type, and ice action (Knox and Lowry, 1977). Below 50 m zonation becomes more difficult to interpret. The much-cited data for the Ross Sea (Bullivant and Dearborn, 1967) cannot be considered representative of the whole of the Antarctic deep sublittoral. Epifaunal assemblages, mixed in varying degrees with infauna, differ with depth, and in the deeper parts there may be a predominance of level soft bottoms occupied mainly by infauna. Amensalism, the interaction between two populations in which one is in- hibited while the other is not, has been used to describe the interactions between two trophic groups composed of several taxa (Rhoads and Young, 1970). Usually, where this interaction has been studied, the amensals (suspension-feeders and sessile organisms) are either discouraged from settling or are killed during early ben- thonic stages through the reworking of sediments by the inhibitors (the infaunal deposit-feeders). In the many photographic records of Antarctic benthos some of the dense populations of suspension-feeding fauna appear to be living directly on the muddy substrate, presumably

76 V.A. Gallardo

having originally settled on a clastic particle, which became buried, thus constituting the epi-infauna (or soft bottom epifauna of the Antarctic) biota described above; is this a case of amensalism? Contrary to other authors, Mills (1975) considered the amensal trophic group in this Antarctic situation to be the detritus-feeding infauna. The ecology of the Antarctic benthos has characteristics which may be radically different to those encountered elsewhere and which are still little understood. Antarctic soft bottom sediments with their dense populations of immobile suspension feeders (sharing the environment with a generally abundant and diverse mostly motile infauna) are reminiscent of the descrip- tion of Paleozoic benthic habitats given by Thayer (1979). Elsewhere, present day comparable bottom types are dominated by deposit feeders, which appear to have evolved relatively recently. Are these taxa really less common in the Antarctic sublittoral than elsewhere? If so, why? Perhaps they cannot cope being swamped by a continuous invasion of "soft bottom" epifauna favoured by the clastic rain over the shelf?.

The Sublittoral Soft-Bottom Communities

The application of more or less standardized sampling and sample processing methods is difficult even in the enclosed inshore areas of Lesser Antarctica, where there is a clearer segregation of infauna and epifauna, than in other Antarctic areas.

Pioneer quantitative work in the Indian Ocean sector by Beliaev and Ushakov (1957) showed that benthic biomass below about 500 m is predominantly infaunal (Ta- ble 3). Bullivant and Dearborn (1967) suggested that only in the deep soft substrates of the Ross Sea, where polychactes and echinoderms are common, are there af- finities with the deep living benthos of other oceans.

The first intensive quantitative surveys of soft-substrate areas in Antarctica were carried out at Port Foster (Deception Island) and Chile Bay (Greenwich Island), both in the South Shetland (Gallardo and Castillo, 1968, 1969; Gallardo et aL, 1977). Port Foster was in- vestigated in order to observe the effects of the volcanic eruption that had occurred only seventeen days before the sampling, and as expected, revealed a mass mortality of the benthic fauna. The survey of the undisturbed bottom fauna of Chile Bay disclosed a predominantly infaunal community where polychaetes dominated in abundance (61.3% of the total) and biomass (46.6% of the total). Chile Bay was studied by means of 43 samples collected between 35 and 355 m depth using a 0.1-m ~ Petersen grab, and sieved through a 1-mm 2 mesh sieve. Twenty-eight major benthic groups were extracted from the samples, of which 12 groups showed 50% occurrence. The macroinfauna of Chile Bay exhibited a most striking feature which was detected while sorting:

Although samples from deeper than ca. 100 m were con- sistently dominated in numbers and biomass by the polychaete worm Maldane sarsi antarctica, this species was almost completely absent in samples from shallower depths. Two assemblages were thus distinguished, the Maldane-dominated and the non-Malclane assemblage, which showed significant differences in the relative abundance of the major taxa. Crustaceans appeared most important in the shallow non-Maldane assemblage, whereas polychaetes and bivalves were more important in the deeper one. On average the relative abundance of main taxa in the benthic infauna of Chile Bay were Polychaeta 61.4°70, Crustacea 13.8°70, Mollusca 12.7°70, and other taxa 12.1%. The mean density and biomass (wet weight) for the infauna were 4,707 indiv./m 2 and 172 g/m 2, respectively.

In general terms, a comparatively large number of species and a low representation of each of them (lack of dominance) characterizes a diversified assemblage, while a comparatively low number of species and a high numerical representation by one or few of them ("domi- nants") characterize a low diversity community. A different possibility can be found in situations where a dominant (or well-represented) species exists in the con- text of a large number of species. Several indices have been developed to measure diversity, but because for these Chile Bay samples specific determinations had not been (and are not yet) completed, the calculation of diversity is not possible. However, comments can be made on the dominance factor.

The "non-Maldane" assemblage has high diversity with large numbers of species with no clearly dominant species, whereas the Maldane-dominated assemblage, although dominated by a single species is unusual in containing a rich variety of other species. The samples were also analysed for spatial distribution patterns, and regularities were observed which correlated with the occurrence of two distinct benthic environments created by a ridge extending across the Bay. From a preliminary comparison with a tropical infaunal study Gallardo et al. (1977) concluded that Chile Bay's infaunal community showed a high species richness, comparable or even greater than the tropical community.

Mills and Hessler (1974) studied communities inhabiting mud (silt-clay) bottoms off the South Shetland Islands at depths between 46 and 282 m. Animal densities ranged from 6720 to 17,960 indiv./m 2 (mean 168 g/m 2) (Mills, 1975). Probably the best year-round infaunal study in the Antarctic is that of Lowry (1975). He studied the soft-bottom community of Arthur Harbor (Anvers Is- land, Antarctic Peninsula) emphasising species composition, community structure, and species diversity. The density of organisms ranged from 3265 to 14,756 m 2 (mean 7629 m 2) at his Station I, and from 2244 to 11,747 (mean 6285 m s) at Station II. The major components of the community were numerically Annelida


(Oligochaeta and Polychaeta) 51o70, Arthropoda (Crus- tacea and others) 38o70, Mollusca 4°70, and other groups 7°7o. Biomass was not determined. In terms of diversity Arthur Harbor's infauna has many species with individuals distributed so that their number decreases gradually from most abundant to least abundant; thus the community may be said to contain much information. Lowry, using the Shannon-Wiener index, found that his mea- surements indicated high diversities. The index varied slightly during the year, with reductions in the middle of summer and late winter-early spring caused by seasonal increases in abundance of some of the species. The most conspicuous drop in diversity occurred in late winter and late spring. Lowry concluded that the benthic community of Arthur Harbor shared many of the characteristics of communities living under environmental stability, i.e. high species-richness, high diversity, and low genetic variability. Numerical fluctuations were caused by biotic rather than abiotic factors, and the prevalent adoption of brooding of offspring results in the production of fewer offspring generally reducing the size of the seasonal effect of recruitment on diversity. The physical parameters of Arthur Harbor with yearly bottom temperature fluctuations of 2°C and bottom salinities of 0.6%o indicate a constant environment with little physical stress.

Richardson and Hedgpeth (1977) also worked on the soft-bottom macroinfaunal community of Arthur Har- bor. They found densities of organisms 5 times greater than those reported for Chile Bay and considered these as a result of the high primary productivity of Arthur Harbor. They regarded the benthic community of Ar- thur Harbor as efficient with a stable structure and low turnover rate due to the slow growth of Antarctic species and the physical stability of the environment. Fur- thermore, the low organic content of the sediments and the lack of hydrogen sulphide at all but one glacially disturbed station was thought to indicate a rapid and efficient utilization of organic matter by the benthos. The glacially disturbed station, located at a depth of 50 m very near a glacial face, was exposed to glacial calving. There sediment was a very poorly sorted clayey silt, and the community was dominated by the polychaete Tharyx cincinnatus (2846 indiv./m 2) which comprised about 72°7o of the individuals found. Community diversity, species richness, evenness values, and density were lower here than elsewhere in the area.

Large variations in density were reported for the infauna of McMurdo Sound (Dayton and Oliver, 1977). There are differences of an order of magnitude between the West and the East Sound sites which were attributed to differences in primary productivity. Thus at the eutrophic East Sound at depths of 20-30 m densities were 118,712 to 155,572 m -2, while the West Sound site densities varied from 2184 to 45,294 m-L In contrast, densities obtained from the Ross Sea are strikingly

low with an average of 1960 m-L Dayton and Oliver also identified and counted macrofauna from cores taken from each side of the Sound. A core collected at a depth of 20 m at Cape Armitage (East Sound) contained 2828 individuals of 37 species, whereas in another core taken at 40 m at New Harbor (West Sound) there were 176 individuals of 50 species. Species richness was higher in the oligotrophic west sound and comparable to deep slope and shallow tropical environments (Sanders, 1969), but nearby in the East Sound infaunal densities were very high in relation to the number of species with many species occurring in great abundance.

Benthic Stability

If our concern is conservation, the question of stability acquires an overriding importance. Environmental stability has been analysed by Thiery (1982) and according to his definitions the Antarctic sublittoral environment could be classified in somewhat large space and time scales as stable, both because of its constancy in terms of the small variations in physical parameters close to the bottom and of its predictability or contingency due to periodic changes such as food supply. As far as the sublittoral benthos is concerned, even this contingency of food supply may have different implications to the suspension feeders and to the deposit-feeders. Several mechanisms have been reported whereby suspension feeders can buffer the effects of seasonal variation in food supply, such as low metabolism, flexibility of feeding rates and habits, and "hibernation" (Arnaud, 1974, 1977; Grusov, 1977; Fratt and Dearborn, 1984). The food supply to the infauna is seasonally more stable (Thayer, 1979), although admittedly less is known about the life histories of the Antarctic infauna.

Smaller spatial and shorter time-scales instabilities occur in the Antarctic sublittoral environment that modify the general benthic stability, although not much is known about them. They are caused by the scouring effect of sea ice, anchor ice formation, mainly at depths shallower than about 30 m (Dayton et al., 1969; Gruzov, 1977), the rain of ice-rafted clastics, glacial ice calving (Richard- son and Hedgpeth 1977), iceberg ploughing (Kauffman, 1974; Richardson and Hedgpeth, 1977; Moreno et al., 1982; Zamorano, 1983), underwater land-slides (Dayton, 1975), and volcanic eruptions (Gallardo and Castillo, 1968; Gallardo et al., 1977). The list can be extended to include man-made disturbances, such as organic pollution (Dayton and Robilliard, 1971). However, the natural sources of environmental instability, far from en- dangering the sublittoral ecosystem, contribute to creating and maintaining reserve capacity for adaptation within the system. Conservationists need to know how effective this reserve capacity would be in buffering the Antarctic sublittoral community from the effects of anthropogenic influences.

78 V.A. Gallardo

On large time and spatial scales the Antarctic sublittoral habitat appears to be both very stable and ancient, features which have been related to community diversity, in the benthos by Sanders (1968, 1969) and in more general terms by Thiery (1982). Environmental stability and community diversity are related through two different sets of mechanisms (brought together by Sanders in his stability-time hypothesis), i.e. the evolutionary mechanisms, operating over very long time, and the ecological mechanisms, operating over relatively short time. Evo- lutionary mechanisms increase community diversity through speciation, and ecological mechanisms control the numbers of species and their relative abundance. Several hypotheses have been proposed to explain how the evolutionary mechanisms operate. The most applicable to the Antarctic benthos is the evolutionary-time hypothesis which states that the older the environment (regardless of its stability) the more diverse it is; and the combined environmental-constancy hypothesis, which stated that the more constant and predictable the environment the more diverse it will be. These fit very well the observed facts about the Antarctic taxonomic diversity and endemism. Other ecological mechanisms that have been suggested to affect diversity include spatial heterogeneity, competition, predation, and productivity, all of which could find some support from what is known about the Antarctic benthos, in particular the spatial heterogeneity theory (Simpson, 1964; fide San- ders, 1968). This states that the more heterogeneous and complex the physical (topographic) environment, the more complex and diverse its flora and fauna become. Except perhaps for the tropical coral reef, there probably is no other benthic system that exhibits the high spatial heterogeneity that has been described from Ant- arctica's benthos, particularly in the nearshore areas of hard and mixed bottoms in the McMurdo Sound (Bulli- vant and Dearborn, 1967).

The question of stability can be approached either from the environment side or from the community as- pect. Connell and Sousa (1983) believe that community stability can be understood as the degree of constancy in the number of organisms. Thorson (1957) had already suggested that the most stable level-bottom community is one in which the whole set of animals is long-lived and without larval stages. The life spans of individuals overlap, smoothing the fluctuations in population size caused by recruitment and mortality. Direct, nonpelagic development results in the population of a species being exposed to the same environment from birth to death. This type of community might only occur in Arctic coastal waters and in the very deep sea. However, it is doubtful if a community exists in which the whole population shows these characteristics. Nevertheless, many authors have dealt with the special adaptations of Antarctic organisms to polar conditions, especially the broadly distributed feature of brood protection (Dell, 1972;

Arnaud, 1974, 1977; White, 1977; Picken, 1980). Sur- prisingly long-lived and slow-growing forms have been recorded within the benthic community (Dayton and Robilliard, 1971; Pearse, 1969) and documented in de- tail by Clarke (1979, 1980, 1982, 1983). There are excep- tions; the sponge Mycale acerata, for example, may increase its mass by as much as 67°7o in one year (Dayton et al., 1974). Future research needs to determine whether the occurrence of these features actually render these Antarctic benthic sublittoral communities stable; also whether differences between the deposit-feeding infauna and the suspension-feeding epifauna (both of hard and soft bottoms) communities can be expected. Gruzov, (1977) reported that in the Davis Sea the biomass of detritus-feeding and omnivorous animals such as Sterechinus neumayeri and Odontaster validus, respectively, is more or less stable seasonally, while the biomass of planktonophagous animals declines drasti- cally in winter. Cucumaria spatha enters a diapause and ceases to feed, and in the hydrozoan Oswaldella antarctica mortality of feeding polyps has been observed.

At smaller time- and/or spatial-scales, however, other factors may contribute to community stability. The phe- nomena generating sublittoral disturbance in the Ant- arctic, some of which have been mentioned above, dis- rupt equilibria states. At the same time they provide natural experiments demonstrating the community's capability for resistance (i.e., remaining in equilibrium when faced with disturbing forces) and adjustment (i.e. of returning to an equilibrium state). Two elements are distinguished in the adjustment: One relates to the speed of the recovery process (elasticity or resiliency) and the degree to which the system can be disturbed and still return to the same equilibrium state. Additionally, there is the question of existence or extinction, i.e. persistence, in the face of natural or man-made disturbances. The criterion proposed by Connell and Sousa (1983) to judge persistence is based on whether a population or species becomes extinct in a given area, and if so can recoloni- zation occur within the time span of a single generation.

Zaret (1982) has shown that the concept that higher diversity leads directly to increased community stability is based more on intuition than scientific proof. Zaret tested two hypothesis that relate diversity and stability: (1) that stable environments have a higher diversity and (2) that stable environments have a fauna with higher stability (resilience) than less stable ones. His findings supported hypothesis (1) but not (2), and on the contrary, supported that stable environments have lower faunal resilience. The suggestion is made that several alternative methods should be used to study these problems, including field, laboratory, and simulation tech- niques whenever possible.

From the viewpoint of conservation the resolution of these questions is very important. Data available at present are insufficient to decide whether the benthic com-


munities of the Antarctic sublittoral will be easily dis- rupted by man-made impacts and whether they would then be able to return to equilibrium and what the speed of such recovery would be. Zaret's findings, however tentative, suggest that the capability for resistance of the Antarctic benthic sublittoral community may be quite low, and if affected by the low speed of all biological processes there, quite slow. Gruzov (1977) observed small seasonal changes in the biomass of detritivores and omnivores in the benthic community of the Davis Sea but substantial changes in the biomass of plankton- feeders. On the other extreme, the local extinction of sponge populations by anchor ice formation and plucking has been described (Dayton et ak, 1969) at depths shallower than 23 m in McMurdo Sound. Kauffman (1974) observed the successional process triggered in the benthos following iceberg ploughing at Arthur Harbor, Anvers Island, over the subsequent 8 months. Icebergs ramming into the bottom release organic and inorganic matter from the sediment which is made available to the ecosystem. Successional studies following gouging showed that flocculent bottom material was shifted by current and wave action and formed a continuous homogeneous covering over the gouged area. This initial recovery pe- riod lasted about a week and affected the top-most centi- metre. Concurrently, long-term filling and levelling of the disturbed site with sediment and detrital material occurred. One sample site of 13 m 2 returned to its former appearance in less than a year; only the top-most layer of 2-3 cm containing the microfauna and microflora, however, were identical to undisturbed areas. The meio- fauna were comparable but varied in composition and quantity. Macrofauna, such as the bivalves Laternula elliptica and Yoldia eightsii, were absent completely.

The patchiness of biota can be attributed in many cases to iceberg activity, and areas of the bottom down to 200 m may be subject to abrasion on rocky substrates or to gouging on soft ones. Photographic records in the literature seem to reveal that iceberg action is quite fre- quent and may be more important in determining soft- bottom benthos structure than it is at present realised. The chaotic pictures of the bottom in plates 3, 4, and 15b of Bullivant and Dearborn (1967) seem to represent iceberg-disturbed bottoms where the community may differ substantially from that in adjacent undisturbed areas in terms of general species composition, density of organisms, biomass, and diversity. The degree of differ- ence probably depends on the age of the disturbance, as suggested by colonization and succession experiments (Arntz and Rumohr, 1982) and field observations (Oren- zans and Gallucci, 1982), assuming these processes are similar under Antarctic conditions. Evidence that iceberg ploughing may be strong enough a disturbance to shift the soft-bottom community equilibrium state is emerging from observations and experiments. Moreno et al. (1982) and Zamorano (1983 and personal corn-

munication) have observed that iceberg ploughing increase spatial heterogeneity by making refuges available to fish; the deep-burrowing bivalve Laternula elliptica once exposed by iceberg action is unable to rebury itself, and so it dies and becomes available to predators.

Casual observations support the idea of the importance of small-scale disturbances on Antarctic soft-bottom community structure (Richardson and Hedgpeth, 1977; Lowry, 1975). If iceberg ploughing is as common, as suggested here, the Antarctic benthos, particularly of the upper sublittoral soft-bottoms, may be a complex mosaic of undisturbed and disturbed communities in varying stages of succession (Dayton, 1984). Species adapted to exploit the ephemeral opportunities created by such catastrophic events and perhaps some of the generalist species otherwise not complying with the K-strategist character of most of the other species may prove to be indicators of disturbance. Studies on the disturbed benthos of Port Foster indicated that great variations in the structure and composition of the benthic community occurred in the years following the 1967 eruption (Gallardo et al., 1977). Disturbance, as a se- quel of the eruptive events, is considered to be on-going (Fratt and Dearborn, 1984). Our most recent observations (January 1985) indicate that Ophionotus victoriae and Sterechinus neumayeri are still the dominant organisms at Port Foster, just as they were two weeks after the 1967 eruption, and even when the Deuxi6me Expedi- tion Frangaise visited Port Foster in 1907 and 1909. Whatever is happening with the benthic community of Port Foster, it continues to be a natural experiment for the study of the ecology of catastrophic perturbation in the Antarctic.

The Benthic Realm and Antarctic Conservation

More knowledge on Antarctic benthic ecology is needed for the development and application of appro- priate conservation measures in Antarctica, such as the establishment of protected areas or reserves, although the urgency of this need may now be less than was thought a few years ago, since Antarctic mineral exploitation is considered to be at the bottom of the list of ventures that entrepreneurs would choose to carry out within a forseeable future there. Nevertheless, conservation action should go ahead while it is relatively easy and before economical investment begins to increase the dif- ficulties to a level where such actions, if not fully pre- cluded, will be at least hampered. It is encouraging that new capabilities and experimental approaches to benthic ecological research are becoming available and are being applied at present (Dayton, 1972, 1975).

Within the Antarctic ecosystem, the benthic realm with its unique, species- and biomass-rich communities, could be the next large natural system that could be directly modified by man. Although this may not seem

80 V.A, Gallardo

likely in the foreseeable future, natural resource scarcity, changing demands, and prices could shift the prospect closer, and conservation ma3~ be caught with an unfin- ished task. At present, opportunities for conservation measures within the benthic realm of Antarctica are few. The Antarctic Treaty System has found it not accept- able even to approve Marine Sites of Special Scientific Interest under the Agreed Measures for the Conser- vation of Antarctic Fauna and Flora, despite their accep- tance by SCAR (see Bonner and Smith 1985). The next possible source of conservation measures applicable to marine areas to Antarctica is the Convention for the Conservation of Antarctic Living Resources (CCAMLR), which aims at the conservation (including rational use) of marine living resources (meaning "the populations of fin fish, molluscs, crustaceans, and all other species of living organisms, including birds"), and the ecosystem (meaning "the complex of relationships of Antarctic marine living resources with each other and with the physical environment"). While CCAMLR's stated objectives may raise hopes in connection with conservation of marine areas (for protection of benthos against bottom trawling, if for nothing else), its record so far, ap- parently preoccupied with economically important resources, does not warrant any optimism. The only other legal source under negotiation is the Antarctic Mineral Regime which is considering the inclusion of rigorous ecological principles in order to protect the marine ecosystem, particularly over the shelf, where the environmental risks will be greater. It would be desirable to include a mechanism in this regime that will allow setting aside Antarctic benthic reserves of sufficient size to ful- fil conservation objectives. In order to select these areas widely, both benthic descriptive and experimental research will have to improve methodologically and be substantially extended around the Antarctic continent.

Acknowledgements-I am most grateful to Nigel Bonner of the British Antarctic Survey and Wolf Arntz of the Alfred Wegener In- stitut fur Polar-und Meeresforschung, Bremerhaven, for their sus- tained support and encouragement; and to my sponsoring institutions, the Chilean Antarctic Institute, the Chilean National Committee for Antarctic Research, and the University of Concepci6n.

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the sublittoral macrofaunal benthos of the antarctic shelf

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