FOUNDATIONS FOR ECOLOGICAL RESEARCH WEST OF THE ANTARCTIC PENINSULA ANTARCTIC RESEARCH SERIES , VOLUME 70, PAGES 373-388
MARINE BENTHIC POPULATIONS IN ANTARCTICA: PATTERNS AND PROCESSES
Andrew Clarke
British Antarctic Survey. High Cross, Madingley Road, Cambridge eB3 OET. U.K.
Sampling difficulties have meant that there have been more studies of population patterns than of proc esses in Antarctic benthos, but a number of generalizations can be made. Benthic marine invenebrates in Antarctica have species/abundance relationships similar to those found in temperate or tropical regions but, several striking examples of gigantism notwithstanding. most species are small. Diversity is generally high, particularly in comparison with the Arctic, although some taxa (for example molluscs) are low in diversity when compared with temperate or tropicaJ faunas. Most species produce larger eggs than related non-polar species, and embryonic development is typically slow. Although the Southern Ocean contains fewer taxa reproducing by feeding pelagic larvae than elsewhere, such larvae are by no means absent. Somewhat paradoxically, these larvae are often released in winter. Post-juvenile growth rates are typically slow, and recruitment rates are slow and episodic. The low temperature slows many biological processes, but other fac tors are also involved. Ice is an irnponant factor in many biological processes, and the recently described sub-decadal variability in the e"tent of winter sea-ice is likely to e"ert a profound influence on benthic ceo- 10gica1 processes in Antarctica.
I, INTRODUCTION 2_ ECOLOGICAL PATfERNS
It has long been traditional in ecology to draw a distinc 2_1. Ecological PaJtems in Antarctic Benthos: Species Size tion between the study of pattern and process. These two and Abundance complementary approaches provide different infonnation, and require different techniques. In particular studies of eco The large-scale and small-scale distributional patterns of logical processes require time, and in Antarctica, where Antan:tic benthos have been described elsewhere in this vol many ecological processes take place slowly, such studies ume [Clarke, this volume]. Overall, the distribution of Ant are necessarily long-tenn. The particular difficulties of eco arctic benthos appears to be governed by substratum, depth, logical research in Antarctica mean that most studies have food supply and ice impact. been directed at understanding ecological patterns; studies of In general, distributional studies of Antarctic benthos have ecological processes have been less common, although a few relied on remote sampling techniques which are essentially generalizations can be made. destructive (for example, grabs, dredges and bottom trawls). Aspects of the biology of Antarctic benthic organisms Trawls and dredges in particular suffer from the intense dis have been reviewed regularly during the past twenty years advantages of damaging many specimens, destroying any [Hedgpeth, 1971; Dell, 1972; Clarke, 1983; White, 1984; structure in the community (such as tiering or ecological Dayton, 1990; Arntz et 01., 1994, in press]_ In this review associations) and mixing samples from many different I shall therefore concentrate on selected features of panicu habitats, thereby masking any heterogeneity in the distribu lar interest to the Antarctic Peninsula area. Di stributional tion of different assemblages. In shallow waters these diffi patterns are discussed elsewhere [Clarke, this volume]; in culties can be overcome by the use of SCUBA techniques, this chapter I shall concentrate on species/abundance patterns but safety considerations restrict both the depth and the and diversity. For ecological processes I shall discuss repro amount of time available underwater and thereby limit the ductive ecology, settlement, growth rate and the influences types of study that can be undertaken. Remote photographic of temperature and sea-ice. techniques were used in deeper waters for some of the
Published in 1996 by the American Geophysical Union. 373 374 ECOLOGICAL RESEARCH WEST OF THE PENINSULA l'oo 1966, 1978; Arnaud, 1974]. True size spectra can only be • derived where communities have been sampled exhaustively and quantitatively. Unfortunately few such studies have been l• " '0 undertaken in Antarctica; two are summarized in Figure I. 60 The cumulative size/frequency spectra show that for at least il'c •, some taxa. most Antarctic species are small. In the case of I " gastropods, for example, many Antarctic species are so small l.• as 10 be missed by some conventional types of sampling or .., 20 sorting gear. The curve for the Canadian Arctic proso ,E 0 branchs is distinctly different; in direct contrast to the data for Signy Island, most species included in the data set were so 60 70 80 90 large. This may reflect a real difference in the assemblages Maximum size (mm) between these two polar regions, possibly related to evolu tionary and biogeographic history [Dunlon, 1992]; alterna Fig. I. Cumulative size/frequency spectra for prosobranch gas· tively it may be that the collections on which the curve is tropods from a variety of polar sites and one tropical beach. The based suffered from a sampling bias against the sm:iller spe data are plotted as cumulative percentage frequency against maxi cies. Given the extensive ecological differences between the mum size of each species. 1: Shallow water prosobranchs from northern and southern polar marine benthos [Daylon, 1990], Signy Island (n = 31 species). 2: All prosobranchs collected at this intriguing difference needs further investigation. Signy Island (n = 51). 3: Prosobranch gastropods from Terre A second feature of importance in describing patterns in Ad~lie (n = 61, Arnaud, 1974). 4: Prosobranch gastropods from a tropical beach in Costa Rica (n = 72, from data in Spight, 1976). animal communities is the distribution of individuals 5: Prosobranch gastropods from the Canadian An:tic (data compiled amongst species. Typically species/abundance plots will ex by Arnaud from Macpherson, 1971). hibit a log-normal distribution, and the conventional graphi cal representation is that proposed by PreSIon [1962]. Con struction of Preston plots requires careful attention to sam earliest studies of Antarctic benthos [Bullivant & Dearborn, pling teclmiques: the sampling must be quantitative to ensure 1967] but were then largely ignored. Recently, however, all individuals are taken, cover the entire size range, and be German bioiogist<; have made extensive use of modem sufficiently thorough to ensure that most of the rare species photographic teclmiques in the Weddell Sea, and these new are sampled. Two samples where these criteria have been studies have demonstrated clearly the value of such tech fulfilled at least approximately are shown in Figure 2. niques to marine ecology [Barthel el aI., 1991; GUll el al., These two plots derive from very different types of sample, 1991; GUll and Pipenburg, 1991; Ekau and Gull, 1991; GUll but both approximale to the expected conventional log el al., 1994]. nonmal species/abundance distribution. The gastropod data One of the primary considerations for any ecologist faced were obtained by pooling a series of repeated monthly sam with making the choice of sampling gear is that of size ples of obtained by suction sampling of standard sized quad selectivity. Photographic teclmiques are by their very nature rants (0.25 m') in an area of shallow water (2-12 m depth) limited to epifaunal macroinvertebrates above a certain size. with a mixed substratum. These data therefore represent a Sampling teclmiques based on nets will also miss all or fully quantitative sample for all animals above about 2 mm ganisms below a size set by the mesh of net being used, and in size. The Preston plot (Figure 2a) nevertheless indicates the mesh size of sieves used for sorting will also influence that these data are subject to sampling error (no data in the size distribution of organisms finally collected. These octaves 3 to 5), and three species were represented by two considerations are of particular relevance to Antarctic ben or fewer individuals. thic communities, for although the small number of Ant The amphipod data are from a semi-quantitative study arctic taxa which are unusually large have long attracted which coveted a range of different habitats using a variety attention [Arnaud, 1974] it is now recognized that many of sampling teclmiques. The full collection was then ana Southern Ocean benthic organisms are very small. lyzed by Thurslon [1972]. The Preston plot (Figure 2b) indi Brey and Clarke [1993] collated all the data on the pop cates that some rare species were probably missed, and eight ulation dynamics of Antarctic marine benthos available up species were represented by three or fewer individuals. to 1992. Comparison of the polar species with species from Ecologists have long debated the significance of the shape temperate and tropical waters indicated no significant dif of Preston species/abundance plots. A typical plot of loga ference in mean adult size. This result, however, reflects the rithmically Iransfonmed data where a large number of indi tendency of ecologists to choose larger organisms for study viduals have been sampled often looks as though it would be rather than the actual size distribution of polar marine in well described by a nonmal distribution truncated to the left vertebrates. Antarctic bivalves and gastropods, for example, This truncation (the so-called veil line) is inevitable because have long been known to typically be small [Nicol, 1964, those species which are so rare that the expected number of CLARKE: BENTHIC POPULATIONS 375
15 The underlying process (or processes) leading to the fre, quently (but by no means universally) observed log-normal distribution of species' abundances has remained elusive. Although some theoretical models have proved successful under some circumstances, no single model has been found o 2 4 >.<' to provide a general description of species/abundance data. "> - ~", In fnet the log-nonna) distribution would be expected as a I ' " result of a large number of interacting influences, and hence 2 its general applicability as a descriptor may simply be telling 5 5 Z us that the abundance of species in the wild is dictated by - many factors and not a single process. Figure 2 shows the only species/abundance data for Ant arctic marine benthos known to the author where a quanti
3 5 7 9 11 13 15 17 tati ve collection has been accompanied by a thorough taxo Individuals per species (octaves) nomic study. These data indicate that although many species are small, species/abundance distributions are nol discemibly r r different from those found in marine habitats elsewhere [Gray, 1987; Magurran, 1988; Gaston, 1994).
3 2.2. Diversity
o , For many people, reference to the polar regions conjures pictures of a vast bleak wasteland populated by those few handy species able to maintain a precarious existence in the I face of extremely harsh physical conditions. Although to - some extent this is \rue of the high polar deserts on land, it is certainly not true for the marine environment. Under water, life is both rich in abundance and taxonomically J 7 9 11 13 15 17 diverse and although a fully developed hand substrntum epi Inl1ividuals per species (octayes) faunal assemblage in Antarctica may not quite rival a IrOpi cal reef in diversity it is nevertheless rich in species. Fig. 2. Species/abundance (Preston) plots for two groups of Ant Although the study of Antarctic ~nthic communities has arctic benthic marine invertebrates at Signy Island, Antarctica. a long and distinguished history [Dayton, 1990) detailed Units for the abscissa are )og2(n), where n is the number of indi studies of the An:tic fauna have lead to the impression that vidua1s for each species (octaves: Preston , 1%2). Inset histograms polar marine communities in general are typically lacking in show the same data. but with the abscissa expressed as )ogI O(n). diversity. The An:tic is indeed impoverished in its marine Note the differing ordinate scaJe for the two plots. A. Prosobranch benthic fauna [Curtis, 1975). This may be relaled in pan to gastropods; data from a collection of 138650 individuals of 3 J spe the high riverine sediment input and extreme disturbance, cies taken by suction sampler in Borge Bay by Picken [1980a] . B. Amphipods; d... from a collection of 34718 individuals of 62 spec' both physically by ice and biologically by marine mammal ies analysed by Thurston [1972] . foraging activity [DaytOil, 1990), but it is also a consequence of the relative youth of the An:tic marine system [DUn/on, 1992). Recently, Venneij [1 991] has shown convincingly individuals in the sample being planed is less than one, from molluscan data that colonization of the An:tic basin is would be unlikely to be recorded [Pieloll, 1969). The posi, currently underway from the north Pacifi c. tion of the veHline would be expected to move to the left as The combination of a depauperate An:tic fauna, and the sample size increases [Magurrall, 1988] . intensely rich shallow-water faunas of the Indo-West Pacific Transforming the data to 10glO (n) smooths the distri lead inevitably to a cline in species richness from tropics to bution by reducing sampling error (Figure 2a, 2b, insets). poles in the northern hemisphere. This cline is not simply This suggests that the gaslrOpod data are well described by a function of the two end-points, however, for careful exam a log/normal distribution, although a veil line is clearly ination of several taxa have shown the existence of lati apparent. indicating that some very rare species were not tudinal clines in species richness in more temperate areas sampled. The amphipod data are less well described by a (for a particularly detailed example see the recent analysis of log/normal distribution, exhibiting a di stinci tail to the left molluscan distribution along the Pacific seaboand of North (Figure 2b); this may reflect the semi-quantitative nature of America by Roy et al., 1994). the sampling [Thurston, 1972]. It has long been known that the Southern Ocean supports 376 ECOLOGICAL RESEARCH WEST OF THE PENINSULA arich and dive"" benthic fauna [Dell, 1972]. Recent work evidence from anywhere of a latitudinal cline in the within in the deep sea has suggested that broadscale patterns of di habitat (alpha) dive"ity of shallow-water soft-bottom com ve"ity may differ between the northern and southern hemi munities [Clarke and Crame, in press]. Interestingly, there spheres [Rex et 01., 1993] and Clarke [1992] raised the is evidence of such a cline in the deep sea [Rex et 01., 1993] question of whether there was any compelling evidence at but the reasons for this difference remain obscure. all for a latitudinal dive"ity cline in non-calcareous marine It is not clear to what extent there may be a latitudinal taX"- Continuing taxonomic work has confirmed the rich cline in dive"ity within the Southern Ocean. Although sam ness of the Southern Ocean benthic marine fauna [Poore and pling has been undertaken widely around Antan:tica, this has Wilson, 1993; Brey et 01., 1994; Arntz et aI., in press] and at mainly clarified the circumpolar nature of the distribution of present there is no convincing evidence for a latitudinal di many taxa and suggested a division into major biogeo ve"ity cline in marine shallow-water benthos in the southern graphic provinces [Hedgpeth, 1969; Dell, 1972; Clarke, this hemisphere to match that in the northern hemisphere [Clarke volume]. The only study which is sufficiently detailed to re and Crame, in press]. Such a cline may well exist, but at veal a latitudinal cline within Antarctica is that of Moe and present there is no finn evidence either way. DeLaca [1976] on macroalgal distribution. This study re The primary reasons for the striking differences between vealed a statistically significant decline in species richness the dive"ity of shallow-water marine benthos in the Arctic from Elephant Island (61°S) to Marguerite Bay (68°S). A and the Southern Ocean appear to be the very different tec broader-scale analysis of southern hemisphere marine algal tonic and evolutionary histories of the two regions [Clarke distribution has confirmed this general pattern [John et aI., and Crarne, in press]. Whereas the Arctic basin is relatively 1994], although recent work has increased the number of young, the Southern Ocean has a long history of evolution macroalgal species recorded at a number of sites (Signy in situ [Lipps and Hicknum, 1982; Clarke and Crame, 1989, Island: Brouwer et aI., 1995; King George Island: Chung et 1992]. There is no evidence that speCiation proceeds any 01., 1994; KlOser et aI., 1994, Anve" Island: Amsler et aI., more slowly in the polar regions [Crame and Clarke, in 1990). press] and the frequent climatic cycles which have char Part of the cline in dive"ity along the Antan:tic Penin acterized the Cenozoic history of the high southern latitudes sula will reflect the increasingly severe physical constraints may actually have promoted speciation [Crarne, 1993, 1995, limiting macroalgal growth at high latitudes (particularly ice in press]. scour), but it may also reflect the evolutionary and biogeo Although the overall dive"ity of the Southern Ocean graphic history of Southern Ocean macroalgae in relation to benthic marine fauna appears to be quite high [Arntz et 01., elimination of the previous flora by extension of the ice in press], the fauna comprises a mixture of species-poor (for sheet and subsequent recolonization along the Antan:tic Pen example, gastropod and bivalve molluscs) and species-rich insula [Clayton, 1994]. Unfortunately we have no compa (for example, ascidians, polychaetes, sponges, bryozoans, . rable data for any animal taXa, so it remains unclear whether amphipods and isopods) taXa [Clarke and Crame, in press]. this is a general result, or limited to macroalgae (or perhaps Unfortunately, a critical appraisal of Southern Ocean (in the shallow sub-tidal ecosystem). deed, southern hemisphere) marine benthic dive"ity is hin dered by the poor state of taxonomic knowledge of many 3. ECOLOGICAL PROCESSES IN SOUTHERN groups [Winston , 1992] (fable I). OCEAN BENTHOS An alternative approach to the problem of broad patterns in dive"ity is to look for geographical patterns in within 3.1. Egg Size and Reproductive Effort habitat dive"ity. Thorson [1957] could find no evidence of a latitudinal cline in the species-richness of shallow-water The life history of organisms is essentially cyclical (adult soft-bottom communities in the northern hemisphere, and to egg to adult) and hence the choice of a starting point for this result has been confirmed by more recent analyses [Ken description of reproductive ecology is somewhat arbitrary. dall and Aschan, 1993]. In polar regions, however, the embryonic stages (eggs and The only measurement of infaunal community dive"ity at larvae) show striking differences from warmer latitudes, and an Antarctic site is that at Arthur Harbour, Anve" Island thus reproductive biology forms a logical point to initiate [Richardson, 1976; Richardson and Hedgpeth, 1977]. The discussion. dive"ity at this site, expressed both as Shannon-Wiener and It has been recognized since the pioneering work on Arc Margalef indices, was fully comparable with a range of oth tic and cold-temperate benthos by Thorson [1936, 1950] that er, lower latitude, soft-bottom communities (mostly from the there is a distinct tendency for polar marine invertebrates to northern hemisphere). This comparison is confounded by produce a smaUer number of larger eggs than related species the traditional difficulties for dive"ity studies of compara from lower latitudes. Thorson's studies in Greenland concen bility of sampling and analytical protocols, and also the im trated on molluscs (gastropods and bivalves) and echino pact of the seasonality of recruitment on the evenness com derms, though he also examined polychaetes and crusta ponent of diversity statistics. Nevertheless there is as yet no ceans. In all cases he observed a wide range of egg sizes, CLARKE: BENTHIC POPULA nONS 377
TABLE I. A summary of marine benthic diversity in the Southern Ocean . Species richness data for the Southern Ocean are an amalgamation of data collated by Arntz el 01. (in press] and Clarke and e Crame (in press); estimates of the percentage of Antarclic species known arc from Winston (1992) and estimates of IOta] taxon diversity are from MindJi (1993).
Estimated number Estimated percentage Estimated number of Southern Ocean of Southern Ocean of species in s Taxon species known spec ies known the world f PORIFERA >300 50 6000 CNIDARIA Octocorallia 33 50 Scleractinia 37 90 Actiniaria 31 95
BRACHIOPODA 16 335
BRYOZOA >350 40-50 5000
PRIAPULIDA 3 9
MOLLUSCA -870 130000' Gastropoda 604' Bivalvia 166'
SIPUNCULIDA -IS 320
POLYCHAETA 562 12000
PYCNOGONIDA >150 1000 CRUSTACEA Decapoda 4 10000 Amphipoda 520 8600 Cirrepedia 37 1220 lsopoda 346 10000
ECHfNODERMATA 6700 Asteroidea 104 Crinoidea 27 Echinoidea 25 80 Ophiuroidea 87 70 Holothuroidca 103 80
TUNICATA 3000 Ascidia >130 95
• Data for number of species be low 50°5, so includes some Subantarctic w.xn. II Other estimates arc 50000 and 75000 (Minelli. 1993).
indicating in tum a range of reproductive strategies in the Although it was lllOcson's work in east Greenland which species present in Greenland. Based on a relationship be· first established the tendency for polar marine invertebrates tween egg size and development mode proposed by Mortell to avoid a pelagic larval phase, earlier work in th~ Southern sen [1921. 19361. Thorson concluded that most east Green Ocean had already demonstrated that Antarctic echinodenns land echinodenns and prosobranch gastropods reproduced contained a high proportion of species which brooded their without a pelagic larval phase. Thorson also established. eggs (for a succinct summary of the histo!), of these ideas however, that some bivalves did reproduce via a pelagic lar· see Pearse alld Bosci •• 1994). Mileilwvsky [19711 undertook va. and that the appearance of these larvae in the plankton a reMevaluation of the available data and, basing his argu was distinctly seasonal. ment around prosobranch gastropods. established a clear Iati- 378 ECOLOGICAL RESEARCH WEST OF THE PENINSULA
100 to direct development, polar echinoderms switch from feed ing to non-feeding larvae (Table 2). Pearse and Bosch [19- • 94] propose that this switch has evolved not in response to • patterns of food availability (as argued by Thorson , 1936 80 and Clarke, 1983), but in response to 1he oceanographic • regime which developed followed the opening of Drake Passage. The Antarctic cilCumpolar current would tend to ~. • sweep long-lived pelagic larvae into areas with few suitable • • sites for settlement (deep water), and comparison wi1h o1her ." • areas dominated by similar current regimes (for example, sou1hern Australia and New Zealand) reveals a similar high • incidence of non-pelagic development [Pearse and Bosch, 1994]. In this context it is intriguing 1hat many demersal fish • in 1he Sou1hern Ocean have retained a pelagic larval stage • [North and White, 1987] . • The resurrection, and refinement, by Pearse and Bosch 20 [1994] of 1he original hypo1hesis relating 1he high incidence • of non-pelagic development to 1he impact of the oceano graphic current regime on dispersal is provocative. It is also • important in highlighting two factors often ignored in eco O~-,--~--.--,~-,--.---.--,--~.- logical discussion: 1he physical environment and phylo 90 60 30 a genetic history. Ecologists are now recognizing the extent to Latitude (N) which 1he oceanographic environment controls the spatial distribution of larvae, and hence the distribution and abun Fig. 3. 'Thorson's rule' exemplified by a clear latitudinal cline in dance of adults (for a recent short review see Grasberg and the proportion of prosobranch gasbUpod species reproducing via a Levitan, 1992). There is also a growing recognition of the pelagic larval stage. Redmwn from Mileikov,ky [19711 . influence of phylogeny on ecology, and in 1he case of reproductive strategies it is imponant to distinguish between 1he evolution of non-pelagic development from ancestors tudinal cline in 1he proportion of species reproducing via a wi1h pelagic development, and selection for species showing pelagic larva from, almost all species in 1he tropics, to vir non-pelagic development in a clade which already possessed tually none in 1he polar regions. Mileiiwv,1cy lermed 1his this trait (as may well be 1he case for isopods, amphipods cline 'Thorron's Rule' and a11hough 1he original term was and ctenocidarid echinoids in Antarctica: Fell, 1976; Brandt, concerned primarily wi1h larval development, it has now 1992). broadened 1hrough use to include a suite of (not necessarily A11hough 1he predominance in 1he Sou1hem Ocean of spe related) reproductive features including a large egg size, the cies wi1hout a pelagic feeding larva is now well established, avoidance of a pelagic larva, and brooding. 1here are none1heless many species which do produce such A cline in 1he proportion of species reproducing via a pe larvae and, ra1her intriguingly, 1hey are often very common lagic larva is shown most clearly by prosobranch gastropods [Clarke, 1992]. A recent two-year systematic study of the (Figure 3). 1lwrson [1950] explained this pattern on the ba presence of marine invertebrate larvae in the plankton at sis 1hat 1he very slow rates of development resulting from Signy Island has revealed a wide range of larvae, including 1he low seawater temperatures and 1he associated very brief echinoderms, molluscs, crustaceans, polychaetes and nemer summer period of food availability would not allow 1he lar leanS (D.P. Stanwell-Smi1h, perronal communication, 1995). vae to reach metamorphosis before starvation. Work on In some cases 1he appearance of larvae was distinctly sea echinoderms by Pearse and colleagues at McMurdo Sound sonal (for example, most echinoderm larvae appeared in and subsequently at Palmer Station has, however, shown winter), whereas in o1hers larvae appeared to be present all clearly iliat explanations for patterns of larval development year round at low densities (for example, nemertean pilidia). in polar regions based simply on 1he seasonality of food Some of 1hese larvae are clearly planktotrophic and it is availability are unlikely to be correct [Bosch and Pearse, 19- therefore of interest 1hat simultaneous measurements of wa 90; Pearse and Bosch, 1994]. ter column chlorophyll showed 1hat whereas the larger dia This comprehensive study of development in Antarctic toms and colonial forms exhibited 1he classical short summer echinoderms has shown clearly 1hat many species reproduce bloom, nanoflagellates showed an extended bloom wi1h by pelagic larvae but 1hat most of 1hese larvae are leci1ho significant concentrations remaining in the water column trophic (and hence do not feed in 1he plankton). Whereas during winter [Clarke and Leakey, in press]. polar gastropods exhibit a switch from pelagic-feeding larvae In crustacean groups which brood 1heir eggs (amphipods, CLARKE: BENTHIC POPULATIONS 379
TABLE 2. Mode of larval development in echinodenns from two polar and one temperate location. Table compiled from data in Pearse [1994), incorporating original data from Th orson (1936]. Data are number of species at that location utilizing a given mode of larval development, with percentage of total species in parentheses.
Number of species reproducing by
Site Pelagic feeding Pelagic non-feeding larva Protected larva development
TEMPERATE Monterey Bay. CA 18 (50%) 8 (22%) 10 (28%) POLAR N.E. Greenland 4 (17%) 16 (70%) 3 (13%) McMurdo Sound 5 (23%) II (50%) 6 (27%) caridean decapods and isopods) egg size has shown to be lations at higher latitudes represent an increased investment larger in Southern Ocean species compared with related per embryo [Clarke. 1993a]. and comparison between indi species from lower latitudes [Bone. 1972; Bregau.i. 1972; vidual females within a population has revealed subtle but Clarke. 1979 ]. In caridean shrimps the larger egg size is significant trade-offs between egg size and fecundity accompanied by a reduced overall brood mass [fahle 3; [Clarke. 1993b]. Clarke. 1979]. This might suggest an overall reduction in The presence in the nearshore Southern Ocean fauna of a reproductive investment, but model calculations indicate that number of common species with pelagic feeding larvae and this is not the case [Clarke. 1987]. Indeed data for the Alc the clines in egg size within Antarctica shown by some spe tic deep-water caridean Palldalus barealis suggest that the cies suggest that there are more factors influencing repro balance between a reduced annual investment in eggs and ductive biology than just dispersal. Reproductive ecology. the lower bas ..1 (maintenance) metabolism characteristic of particularly in relation to population structure as shown by high latitude marine invertebrates result in an overall lifetime modem molecular techniques (an almost untouched field in reproductive effort similar to shorter-lived wanner water Antarctic marine biology to date) is clearly a research area species [Clarke. 1987]. Unfortunately there are too few data in need of urgent work. to test whether this might be a general result. Recent data have shown thai there are also clines in egg 3.2. Recruilmenl size within Southern Ocean crustaceans [Wagele . 1987; Clarke and G~rt. 1992: Gorny et 01 .• 1992]. Chemical anal There have been relativoly few studies of recruitment in yses have shown that the larger eggs produced by popu- the nearshore Antarctic marine environment. Rauschert [19-
TABLE 3. Egg size (dry mass, mg) and reproductive output (RO: mass newly spawned eggs/mass female) in polar and temperate earidean decapods (shrimps). Data from Clarke [1979, 1987. 1993a] , presented as mean and standard deviation with number of individuals analyzed in parentheses. ND: no data . All (mta are for newly spawned eggs.
Specie ~ Egg dry mass (mg)' RO Climatic Zone
PANDALIDAE Panda/us borealis 0.88 ± 0.08 (10) 0.177 ± 0.024 (95) Polar Pandalus mOlltagui 0.021" 0.242 ± 0.056 (39) Temperate HIPPOL YTIDAE Chorismus antarclicus 1.01 ± 0.07 (119) 0.171 ± 0.QI8 (28) Polar LLbbeus pawris 2.88 ± 0.23 (5) 0.131 ± 0.034 (12) Polar Eua/us gamardi; 0. 15 ± 0.04 (99) ND Polar CRANGONIDAE Crangon crangon 0.0059" 0.165 ± 0.033 (68) Temperate NOlocrangon anlarCliCl1S 0.80 ± 0.05 (34) 0.118 ± 0.014 (23) Polar Sabin~a septtmcarillata 0.63 ± 0.07 (16) 0.136 ± 0.060 (29) Polar
-Note that egg mass varies froiil siL! La site; representative data are provided fo r a single site. "Mean egg mass deri ved from a single sample of eggs pooled from 20 individuals. 380 ECOLOGICAL RESEARCH WEST OF THE PENINSULA
TABLE 4. Colonization of settlement plates over a 20 month period at Signy [siand, South Orkney Islands, maritime Antarctic. Plates were deployed at three depths, and the tot31 coverage by all taxa combined assessed by image anruysis. Coverage of the lOp surface, bottom surface and sides was assessed separately. Data are presented as mean coverage (% total area), with maximum value in parentheses; from Barnes [in press}.
Depth (m) n' Coverage (% total area)
Upper surface Lower surface Sides
6 5 0.72 (1.77) 1.25 (2.69) 0.71 (1.34)
12 4 0.19 (0.23) 2.41 (4.60) 1.09 (1.30)
25 4 6.54 (11.62) 4.71 (8.63) 7.49 (12.30)
-Five plates were deployed at each depth, but some plates were destroyed by ice impact before recovery.
30 Celleporella bougalnvll/el 91] deployed settlement plates at King George Island and 25 noted that those plates which survived ice damage were heavily colonized after three years. In contras~ artificial substrata deployed at McMurdo Sound showed virtually no • 20 a colonization after five years, but then inspection after a '0 '.0 further four years revealed a dense recruitment of a typical '0 15 ;; hard substratum fouling community [Dayton, 1989]. With D E, only two such long-term studies having been undertaken it z 10 is difficult to know whether the results represent a true dif ference between recruitment dynamics in the high Antarctic 5 (McMurdo Sound) and maritime Antarctic (King George Island), or simply fortuitous timing in relation to infrequent 0 recntittnenteven~. 0 so 100 lSO 200 250 300 A recent study of recruitment to perspex settlement panels deployed at Signy Island (in the maritime Antarctic) for 20 30 months revealed very low levels of recmitment (Table 4). Inversluta nutrix At 6 m the plates were colonized only by calcareous algae 25 and spiroroid polychaetes and two plates were destroyed by ice impact. No algae were present on plates deployed at 12 where the colonizing fauna comprised spiroroids, one • 20 m. • cyclostome and two cheilostome bryozoans. At 25 m the ~ '.0 dominant colonizers were again spiroroid polychaetes and '0 15 ;; bryozoans (two cyclostome and 15 cheilostome species). D E, Three species, Celleporelw bougainvil/ei, Celleporella ant Z 10 arctica and lnversiula nutrix together comprised between 55% and 80% of all bryozoan colonies, and size-frequency 5 histograms suggested that there had been two settlement events during the 20 month deployment (Figure 4). Mor 0 tality following settlement (for example, caused by preda 0 so 100 lSO 200 2SO 300 tion) can he detected from the presence of empty ancestrulae Number 01 zooids or zooids. In this case no significant mortality could be detected and so it would appear that the eartier settlement Fig. 4. Frequency histograms. with fitted models. of colony size event was smaller than the later one. (number of zooids) of the two most abundant bryowan species colo The most striking feature of these results is the very low nizing perspex settlement panels deployed at 25 m in Borge Bay, Signy Island. The models were fined using the software package rate of colonization (by over an order of magnitude) com MIX, and suggest two settlement events of dissimilar magnitude; the pared with settlement plates immersed in tropical or tem absence of significant number.» of empty ancestrulae of zooids indi perate latitudes [Bames, in press]. This has important eco cated that post-settlement mortality was not the explanation for the logical consequences both in terms of the dynamics of difference in recruinnent between years (reproduced, with permis recovery from ice impact in the shallow water marine eco sion, from Barnes, in press). system, and also for recovery from human impact. The CLARKE: BENTHIC POPULATIONS 381
30 polar species was significantly lower than that of temperate or tropical species. These data were subsequently expanded and analysed further, expressing overall growth performance as the generalized measure 4> :
4> = [log(K) + (0.667 x 10g(M..))]
" where K and M.. are the two parameter.; of the von Ber talanffy growth function [see Arntz et aI., 1994, for further details]. Comparison of data for 28 Antan:tic benthic popu· with 20 ., lations 141 data sets for non-Antan:tic sites showed " Sholl length (mm) clearly that the growth index was significantly lower (p < 0.002) in the Antan:tic populations (Figure 7). Tabulated Fig, S. SizelfI'Ut.!.!cr •..:) ' histogram for sample of 592 individuals of biomass, production and PIB data are given in Brey and the infaunal nuculanid bivalve Yoldia eightsi collected by suction Clarke [1993] and Arntz et al. [1994]. sampler (cut-off size 2 mm) 111 Borge Bay, Signy IslllIld, December Most studies of growth in Antan:tic benthic marine in 1989. illustrating the relathe lack. of younger animms. vertebrates have, for obvious practical reasons, tended to concentrate on the Jarger and more common species; since most polar marine invertebrates are small (Figure I), there intriguing question, to which we have ali yet no answer, is is a possible bias to these results. Important studies of small whether this background level of very low recruitment {a species have included those of the prosobranch Laevilacu hard substrata is intel~per>ed with intermittent year.; of very naria antarctica [Picken, 1979], and the two philobryid bi heavy recruitment [Dayton, 1989]. valves Lissarca miliaris [Richardson, 1979] and Lissarca notorcadensis [Brey and Hain , 1992]. 3.3. luvenile Survival We do not yet fully under.;tand why the growth rates of most polar benthic marine invertebrates are so slow. Where We know very little about either recruitment to soft-bot detailt:d studies have been undertaken these have usually tom communities in Antarctica, or about the su!JseqUCnl sur indicated a strongly seasonal pattern of growth; examples "vival of juveniles. Several published size-frequency histo include the caridean shrimp Chorismus antarc/icus [Clarke grams lack the expected large size class(es) of juvenile and Laklwni, 1979], the philobryid bivalve Lissarca miliaris forms. This could be the result either of episodic recruit [Richardson, 1979], the prosohranch Laevilacunaria antarc ment events, or of the sampling techniques being used tica [Picken, 1979] and seroM iS0podS [Luxmoore, 1982]. having missed the smaller juvenile stages (Figure 5). This seasonality of growth is cleariy related to the overall
3.4. Growth Rate B
It was quickly established by the early autoecological studies of Antan:tic benthos that most species grew slowly, 6 \" . .. . •• I or very slowly, and tended to have long life-spans [reviewed E by Arnaud, 1974; Everson, 1977; Clarke, 1980, 1983]. .s There are, however, a number of interesting exceptions to c 4 this general rule. These include the sponges Mycale ace rata "E .. i!! and Homaxinella balfourensis in McMurdo Sound [Dayton o · et al., 1974; Dayton, 1989] and the ascidians Ascidia chal oS 2 lengeri, Cnemidocarpa verrucosa and Mo/gula pedllflcuJata at King George Island [Rauschen, 1991] all of which have been shown to grow rapidly in comparison with other Ant arctic marine invertebrates. A relatively fast growth rate o 10 20 30 40 50 was also determined for the Antarctic limpet. Nacella CO/l' cinna by a marklrecapture study at Palmer Station (Figure 6) Inilial length (mm) and a similarly fast growth rate has recently ·been noted in Fig. 6. Growth rate in the Antarctic Limpet, Nocella concinna, as the same species at Signy Island [Clarke and Pro/ltero· detennined by a mark/recapture experiment. The data have been Thamas, unpublished data] . taken from Shabico [1976} and ploned to show the annual incre Breyand Clarke [1993] collated all available data on the ment in shell length as a function of length at initial measurement production and biomass of Antan:tic benthic marine inverte (lx>th in mm). Note thallhis measure of growth declines with adult brates and showed that the productionibiomass (PIB) ratio of size, but that growth can be quite fast in smaller limpets. 382 ECOLOGICAL RESEARCH WEST OF THE PENINSULA
16 take larger particles (such as large diatoms or colonial forms) exhibited a much longer period of starvation than those taxa believed to take smaller cells such as nanonagel lates. In this context it is intriguing that almost all of the 12 Antarctic benthic marine invertebrates which have been shown to grow relatively fast are suspension feeders. The relationship between feeding and energetics in polar marine benthos clearly needs further clarification, particu larly in relation to temperature adaptation in growth.
4, ENVIRONMENTAL FACTORS INFLUENCING ECOLOGICAL PROCESSES IN TIlE SOUTHERN OCEAN MARINE BENTHOS
The etymology of the term 'ecology' highlights the recog nition that biological processes can only be understood in terms of the physical environment in which they operate. Of particular importance is the relationship between biological -2 -1 o 2 processes and the scales of temporal and spatial variability Growth Index in the environment This is a growing area in marine ecol ogy, and I will touch on three subjects here: temperature, Fig. 7. A comparison of an index of overall growth perfonnnnce sea-ice and habitat heterogeneity. (derived from the generalized von BenaJanffy growth equation) in 28 Antarctic (black bars) and 141 non-Antan:tic (open bars) of 4.1. Temperature benthic marine invertebrates. 1he index is significantly lower in the Antarctic populations (Mann-Whitney test. P
4,2, Long-tenn TemperaJure Change , Cl Cl == = Cl - , Although the high Southern latitudes are currently very i: cold, and thereby contribute to a strong latitudinal tempera ture gradient from tropics to poles, this has not always been I0 the case. The Southern Ocean fauna that we see today has " ., evolved in situ over a long period, during which time it has been subject to variations in glacial extent, the fragmentation ., of Gondwana, massive changes in oceanographic circulation ,... ,.. , ,... and an overall decline in temperature of perhaps 15-20 K "" "., during the past 55 million years [IJpps and Hickman, 1982; Clarke and Crame, 1989, 1992]. Fig. 8. Seasonal and interannual variability in seawater temperature. The marine invertebrates and fish living today are thus the Data an: from 10m depth at a nearshore oceanographic station in descendants of ancestor.; who lived in much warmer water.;. Berge Bay, Signy Island. The line shown at -i.SoC marks an arbi Current evidence, however, indicates that the present fauna trary threshold for integrating summer thermal environment. Note is highly stenotherroal [Somero and DeVries, 1967; Somera, thaI the summer maximum temperature varies significantly from 1991]. It is not clear whether this stenothermal physiology year to year, and is related to the duration of fast-ice, (shown ~Y . the is an inevitable consequence of adaptation to a low tempera open bars) in the previous winter. Reproduced, with pcmusslon, ture or may have been selected for on energetic grounds from Clark< and Leakey [in press]. [Clarke, 1991, 1993] .. Neither is it clear the extent to which it may represent an evolutionary blind alley, limiting the rather it is likely to be seasonal resource limitation. ability of polar marine organisms and fish to respond to con One physiological process which does, however, show ex tinued temperature change [Somera, 1986]. treme temperature sensitivity, particularly at the lowest tem peratures, is embryonic development For many polar marine 4,3, Sea-ice organisms the rate of egg andlor larval development be comes very slow indeed at temperatures below about -1.5'C The impact of sea-ice on polar marine ecosystems is all [Ross el al., 1988; Clarke, 1992]. pervasive, but there are five key areas where the ecological The second feature of interest is the overall low tempera effects of sea-ice are of particular importance to benthic pop ture. Since, all else being equal, a low temperature slows ulations: down the rate of physiological reactions, polar organisms o Ice-scour in the intertidal and shallow sub-littoral will need to have evolved some mechanism(s) of compen o The impact of iceberg grounding in deeper water.; sating for the effect of this low temperature. This is an anea o The effect of winter sea-ice in influencing water of active investigation. though most studies are concerned column productivity, and hence food availability with fish (Clarke [1983, 1991] provides reviews of this sub for benthos ject). o The rafting of debris into deeper water where One of the most striking physiological correlations with drop-stones may provide isolated patches of hard temperature is that of basal (or maintenance) metabolic rate: substratum habitat polar marine invertebrates exhibit a much lower resting o Sub-decadal variability in ice dynamics metabolism than temperate or tropical species [Clarke, 1991, Ice-scour and the effect of anchor-ice in structuring shal where original citations are provided]. The reduced meta low-water benthic communities has been dealt with else bolic rate in polar species has important consequences for where in this volume [Clarke, this volume]. overwintering energy requirements [Clarke and Peck, 1991], The rafting of land-derived material by ice is a complex but also has subtle implications for overall energy budgeting, process which can have a variety of impacts on benthic pop including reproductive invesunent [Clarke, 1987]. Of current ulations. Where glacial outflow is substantial, then a high interest is the extent to which the energetic benefits to be rate of deposition of unsorted rock flour and moraine debris gained from a low resting metabolism are offset by a con can limit benthic communities to those species tolerant of comitant reduction in overall maximum metabolic rate. high rates of disturbance [Dayton, 1990]. In deeper water, The third feature of interest which emerges from the five ice-rafting can introduce isolated islands of hard substratum year temperature record in Figure 8 is interannual variability. (drop-stones) into areas otherwise dominated by soft sedi There arc significant differences between years in the maxi ments. Colonization of such habitats thus represents a chal mum summer temperature reached, and the overall inte lenge somewhat akin to that of the more ephemeral vent grated thermal environment (degree-days above -1.5' C). communities. nus is an area which has received relatively This variability is linked to variability in ice dynamics and little attention from polar biologists, primarily because of is part of a wider-scale process (see next section). sampling difficulties. 384 ECOLOGICAL RESEARCH WEST OF THE PENINSULA
circumpolar ice extent around the Antarctic continent. This precession has a period of approximately 7-9 years and sug • gests Ihat a sub-decadal variability is likely to affect many ecological processes in the Southern Ocean [Mllrphy et aI., 1995]. At present there are almost no long-tenn data sets to ex amine for such sub-decadal variability. although the tem perature record at Signy Island (Figure 8) reveals a signifi cant correlation between summer seawater temperature and ice duration in the previous winter [Murphy et 01 .• 1995]. The only benthic ecological data available which suggests 0L-______~ ______~ the impact of this variability are those of Dayton [1989]. .t11 If11 It,. tHO 1"' lHO .", .910 1990 which indicate a possible sub-decadal variability in recruit You ment to settlement panels in McMurdo Sound, itself possibly related 10 oceanographic variability. In the pelagic realm Fig. 9. The duration of winter fast-ice at Signy Island (solid line) there are preliminary indications that variability in ice dy and at Laurie Island, 40 Ian due east (brolren line). The shaft of the namics may influence year-class (recruitment) strength in arrow shows the period for which satellite sea-icc data are available. Antarctic krill, EuphallSia sllperba [Ross and Qlletin, 1991] The lrey features of these long-t.eml data sets and the overall decline and variability al higher trophic levels [Testa et 01., 1991; in the average duration of winter fast-ice i:l the Sacth Orkney Fraser et 01., 1992]. Nevertheless the ecological impact of Islands in the 19405 and 19505. and the strong 7-9 year cyclicity the seasonal ice-cover in polar regions is sufficiently impor apparent from the mid-l960s to 1990. From Murphy", {. f. [1995J. Ian! and all-pervasive Ihat it is safe to assume that the re cenUy described long-Ienn variability will carry through 10 ecological processes. Sea-ice is of intense significance 10 Ihe patterns of energy The dynamics of sea-ice and its impact on marine ecol flow in polar marine ecosystems. II stabilizes the water col ogy is an impot1an1 area of polar marine biology, which umn, thereby allowing much of the suspended particulale needs increased attention in bolh benthic and pelagic realms. material 10 sink to the seabed where it is utilized by both macrofauna and the microbial flora The resultant high 4.5. Habitat Heterageneily water clarity can lead to very high rates of primary produc tion in the early spring, in both the water column and, in Whereas the discussion of temperature and sea-ice con shallow waters, in benthic algae [Gilbert, 1991]. In more cems primarily variability in time, habitat heterogeneity con oceanic waters the stabilization of the waler column may cerns variability in space. It has loog been recognized that lead to ice-edge blooms [Smith and Sakshallg, 1990] though an increased diversity of habitats is related in some way to it is now clear that such blooms are by no means a universaJ an increased diversity of the associated flora and fauna, and feature of a retreating ice-edge. Where such blooms do oc for example it is likely that Ihe overall low diversity of the cur, however, they can result in a significant flux of phyto Southern Ocean fish fauna is related to the low habitat plankton material to the seabed [Honjo, 1990]. Sel-ice also diversity. The almost complele absence in the Southern influences !he biology of the pelagic zone by providing feed Ocean of habitats traditionally rich in fish species, such as ing and habitat for zooplanklon [Ross et 01., this volume]. estuaries or tidal flats, has resulted in a low overall fish diversity although individual habitats may be as species-rich 4.4. Sea-ice Dynamics in the Southern Ocean as comparable habitats elsewhere [Eastman, 1993]. There are few data for marine invertebrales, although Analysis of a long-tenn fast-ice record from Ihe South Pickell [1979] has suggested that the contagious (overdis Orkney Islands has revealed a number of features of eco persed) distribution of prosobranch gastropods in shallow logical interest [Mllrphy et 01., 1995]. Although there has water habilats is related to the contagious distribution of been an overall decrease in the duration of winter fast-ice at !heir macroalgal habitat Further woIic in this area is needed, the South Orkney Islands, this has nol been a simple linear particularly to elucidate the extent to which differences in decline but is the result of a reduction in fast-ice duration in habitat heterogeneity may help explain the marked differ !he 19405 and 1950s. There was also a period of clear sub ences in diversity between the Iwo polar regions. decadal cyclicity from Ihe mid-1960s to 1990 (Figure 9). On a larger spatial scale, patterns of habitat helerogeneity Comparison with satellite microwave data showed that vari are important in influencing population dynamics through ability in fast-ice duration at the South Orkney Islands the creation of fragmented population structure (melapopula reflects the larger-scale ice dynamics in the Weddell Sea, tions) and the resultant impact on dispersal and recruitmenl and that this in tum reflects the precession of anomalies in dynamics in populations dominated by species with low- CLARKE: BENllUC POPULATIONS 385
dispersal larval or juvenile stages. At present we know very gions antarctiques et subantarctiques, Tithys, 6, 465-656, 1974. g little of the population structure of most benthic marine Arntz, W.E. . J. Gun, and M. Klages, Antarctic marine biodiversity, Iy invertebrates, although the very different dispersal dynamics in AnlQrctic Communities: Species. StrucllU'e And Swviva/, edited I., in water means that direct comparison with metapopulation by B. Battaglia, I. Valencia and D.W.H. WailOn, Cambridge Uni dynamics in terrestrial habitats may be misleading. versity Press, in press. ,- AmIZ, W.E., T. Brey, and V.A. Gallardo, Antarctic zoobenthos. Oceanogr. Mar. Bioi. Ann. Rev. . 32. 241-304. . I 5. CONCLUSIONS Bames, D.K.A., Seasonal and annual growth in erect species of i Antarctic bryozoans, J. Exp. Mar. BioI. &01., 188, 181-198, d Although there is a long history of both descriptive and 1995. ecological work on Southern Ocean benthos [Hedgpeth, Bames, D.K.A., Low levels of colonisation in Antarctica: the role s 1971; Dell, 1972; White, 1984; Dayton, 1990; Arntz et al., of bryozoans in early community development, in Bryozoans in I, 1994, in press], there remain many gaps in our knowledge Space and Time, edited by D.P. Gordon, A.M. Smith, and I.A. and under.;tanding. Taxa are generally well described but Grant-Mackie, National Institute of Water and Atmospheric Re we have few thorough analyses of communities or assem search, Wellington, New Zealand, in press. Barnes, D.K.A., and A. Clarke, Seasonal variation in the feeding blages. Many taxa appear to be circumpolar in distribution activity of four species of Antarctic Bryozoa in relation to envi but our biogeographic under.;tanding is based on relatively ronmenial faciOrS, J. Exp. Mar. Bioi. &01., 181, 117-133, 1994. few and scattered data. The role of historical processes in Barnes, D.K.A., and A. Clarke, Seasonality of feeding ecology in producing many of the patterns we see in Antarctica today polar suspension feeders, Polar BioI., 15,335-340, 1995. is better under.;tood than in many other areas, but we need Barthel. D .. 1. Gutt, and O.S. Tendal. New information on the bi to utilize modem molecular techniques to distinguish the ology of Antarctic deep-water sponges derived from underwater impact of history and the physical environment in, for exam pholOgnlphy, Mar. &oL Progr. Su. . 69,303-307, 1991. ple, determining patterns of distribution in the Antarctic Bone, D.G .. AspeelS of the biology of the Antarctic arnphipod Peninsula area. Borollia giganlea Pfeffer at Signy Island, South Orkney Islands, Ecological studies are generally limited, for reasons of Bull. Bril. Anlarel. Surv .. 27, \05-122, 1972. Bosch, I., and 1.S. Pearse, Developmental types of shallow-water It logistics, to the austral summer. is becoming clear, how asteroids of McMurdo Sound, Antarctica. Mar. BioI., 104,41-46, ever, that winter is an important time in the ecology of many 1990. species, and further year-round studies are badly needed. Brand, T.E., Trophic relationships of selected benthic marine in Biological work in the Southern Ocean has also revealed the vertebrates and foraminifera in Antarctic, Antoret. J. U.S., II, 24- importance of long-term data sets both for unaer.;tanding the 26, 1976. biology itself and for relating this to variability in the physi Bmnd~ A., Origin of Antarctic 1sopoda (Cruslacea, Malacostraca), cal environment. Key areas for future work are thus year Mar. Bioi., 113, 415-423, t992. round studies, the use of modem molecular techniques, the Bregazzi, P.K., Life cycles and seasonal movements of Cheiri medon femoratus (Pfeffer) and Tryphoselill Icerg~/eni (Miers) further development of remote techniques such as photog (Crustacea: Amphipoda), Bull. Bril. An/arct. Surv., 30, 1-34, raphy. and (perhaps most important of all), continued unin 1972. tetTUpted work to build long-term data. Brey, T., and A. Clarke, Population dynamics of marine benthic invertebrates in Antarctic and subantarctic environments: are there unique adaptations?, Ant. Sci., 5, 253-266, 1993 . Acknowledgements. Work on the physiology and ecology of Brey, T., and S. Hain, Growth, reproduction and production of Lis benthic marine invertebrates at Signy Island has been undertaken as sarca notorcad.ensis (Bivalvia: Philobryidae) in the Weddell Sea, part of the British Antarctic Survey Nearshore Marine Biology Antarctica, Mar. Ecol. Progr. Ser.. 82, 219-226, 1992. program. Thanks are due to the many biologists, assistants and div Brey, T., M. Klages, C. Dahm, M. Gorny, I. GUI~ S. Hoin, M. Stit ing officers who have contributed to thi s program from J962 to its ler. W.E. Arntz, 1.-W. WJlgele, and A. Zimmerman, Antarctic c10sure in 1995; the program will restan further south at Rothero benthic diversity, Nature, 368, 297 only, 1994. station in 1996. Thanks are also due to many colleagues who have Brouwer, P.E.M., E.F.M. Geilen, NJ.M. Gremmen, and F. van provided inspiration and advice over the years, in particular Wolf Lent, Biomass. cover and zonation patterns of sublittoral macro Arntz., David Barnes. Thomas Beey, Paul Dayton, John Dearborn , algae at Signy Island, South Orkney Islands, Antal 1980. bridge University Press, in press. Clarke, A., Life in cold water: the physiological ecology of polar Curtis, M.A, The marine benthos of Arctic and subarctic conti marine ectoIherms, Ocwrwgr. Mar. BioL Ann. Rev., 2 I, 341-453, nenllli sbelves, Polar Rec" 17, 595-626,1975. 1983. Dayton, P.K., Interdecadal variation in an Antarctic sponge and its Clarke, A., Temperature, latihlde and reproductive effort, Mar. &0[. predators from oceanographic climate shifts. Scienu. 245, 1484- Progr. Ser" 38, 89-99, 1987. 1486, 1989. Clarke, A" Seasonality in the Antarctic marine environment. Compo Dayton, P.K., Polar benthos. in Polar Oceanography, Part B: Biochem. Physio[" 9OB, 461-473, 1988. Chemistry, Bio[ogy and Geology, edited by W.O . Smith, lr" pp. Darke, A, What is <>lId adaptation and how should we measure it7, 631-685, Academic Press, London, 1990. Am. 7.00[" 31, 81-92, 1991. Dayton, P.K" G.A. Robilliard, R. T. Paine, and L.B . Dayton, Bio Clarke, A.. Is there a latitudinal diversity cline in the sea? Trends logical accommodation in the benthic conununity at McMurdo &0[. EvoL, 7, 286-287, 1992a. Sound, Antarctica, &0[. Monogr., 44, 105-128, 1974. Clarke, A., Reproduction in the cold: Thorson revisited, Ilivert. Dell, R.K., Antarctic benthos, Adv. Mar. Bioi., /0, 1-216. 1972. Reprod. Deve[op" 22, 175-184, 1992b. Dunton, K., Arctic biogeography: the paradox of the marine ben Clarke, A.• Egg size and egg composition in polar shrimps thic fauna and flom, Trends &0[. Evo[" 7, 183-189, 1992. (Caridea: Decapeda), J. Exp. Mar. Bio[. &0[., 168, 189-203, Eastman, J.T., Antarctic Fish Biology: EvolUlion In A Unique En 1993a. vironment, 322 pp., Academic Press, San Diego, 1993. Darke, A., Reproductive trade-offs in caridean shrimps, Funct. Ekau, W., and J. Gua., Notolhenioid fishes from the Weddell Sea &oL, 7,411-419, 1993b. and their habitat. observed by underwater photography and tele Oarke, A. t Temperature and extinction in the sea: a physiologist's vision, Proc. NIPR Symp. Polar BioL, 4, 36-49. view, Paleobio[ogy, 19, 499-518, 1993c. Everson, I., Antarctic marine secondary production and the phe Clarke, A" The Distribution of Antarctic Marine Benthic Conunu nomenon of cold adaptation, Phil. Tr(lllJ. Roy. Soc. Lond. B., nities. this volume. 279,55-66, 1m. Clarke. A., and lA. Crame. The origin of the Southern Ocean Fell, FJ" The Cidamida (Echinodermata: Echinoidea) of Antarctica marine fauna, in Originr and Evolution of the Amarctic Biota, and the Southern Oceans, Ph.D. thesis, University of Maine. edited by l.A. Crame, pp. 253-268, Geological Society Special Fraser, W.R.. WI Trivelpiece. D.G. Ainley, and 5.0 . Trivelpiece, Publication No. 47, The Geological Society, London, 1989. Increases in Antarctic penguin populations: reduced competition Clarke, A., and lA. Crame. The Southern Ocean benthic fauna and with whales or loss of sea ice due to environmental warming 7~ climate change: an historical perspective, Phil. TrailS. Roy. Soc. Polor Bio[., II, 525-553, 1992. !..ond. B, 338, 299-309, 1992. Gallardo, V.A" l .G. Castillo, M.A. Retamal, A YiIilez, H.l. Clarke, A , and J.A CraIne, Divenity, latitude and time: patterns in Moyano, and J.G. HennosiUa., Quantitative studies on the soft the shallow sea, in MarinI! Biodivl!rs;ty: Causes and Conse bottom macrobenthic animal communities of shallow Antarctic quences, edited by R.F.G. Ormond and J. Gage, Cambridge Uni bays, in Adaptalions WiUUn Antarctic Ecosystems, edited by G.A. versity Press, in press. Llano. pp. 361-387. The Smithsonian Institution. Washington Clarke, A., and D.J. Gore, Egg size and composition in Ceralo D.C., 1m. strolis (Crustacea: [sopeda) from the Weddell Sea, Polar Bio[., Gaston, K.J., Rariry, 205 pp" Chapman & Hall, London. 1994. 12, 129-134, 1992. Oilbert, N.S .. Microphytobenthic seasonality in nearshore marine Clarke, A, and K.H. Lakhani, Measures of biomass. moulting sediments at Signy Island, South Orkney Islands, Antarctica., behaviour and the pattern of em:1y growth in Chorismus antarc Estuar. Coastal Shelf Sci., 33, 89-104, 1991. ticus (Pfeffer), BulL Brit. Antarct. Surv., 47, 6~-88, 1979. Gorny, M., W.E. Arntz., A. Clarke and DJ. Gore, Reproductive Clarke, A" and R.l.G. Leakey, The seasonal cycle of phyto biolngy of caridean decapods from the Weddell Sea, Polor Bio[" pJankton, macronutrients and the microbial community in a near 12, 111-120, 1992. shore Antarctic marine ecosystem, Limnol. Oceanogr., in press. Gray, J.S., Species-abundance patterns, in Organisarion ofCommu Darke, A, and AW.;Ncxth, Is the growth of polar fish limited by nitil!s Pasl and Presenl, edited by J.H.R. Gee and P.S. Giller, pp. temperature? in Biology of Antarctic Fish, edited by G. di 53-67, Blackwell Scientific, Oxford, 1987. Prisco, B. Maresca, and B. Tota, pp. 54-69, Springer-Verlag, Grosberg, R.K., and D.R. Levitan, For adults only? Supply-side Berlin. ecology and the history of larval biology, Trends Eeol. Evol., 7, Clarke, A" and L.S . Peck, The physiology of polar zooplankton, 130-133, 1992. Polar Res" 10, 355-369, 1991. Gut!, J., and D. Pipenburg, Dense aggregations of three deep-sea Clayton, M.N., Evolution of the Antarctic marine benthic algal holothurians in the southern Weddell Sea, Antarctica, Mar. EcoL flom, Phycology, 30, 897-904, 1994. Progr. Ser" 68, 2n-285, 1991. Crame, J.A., Latitudinal range fluctuations in the marine rerum Gua., J., M. Gorny, and W.E. Arntz., Spatiru distribution of Antarctic tluougb geological time, Trends &0[. Evo[" 8, 162-166, 1993. shrimps (Crustacea: Decapoda) by underwater pho'ogmphy, Ant Cr.une, J.A .. Evolution of high-latitude molluscan faunas. in Origin Sd, 3, 363-369, 1991. and EvolUlionary Radiation of 1M Mollusca. edited by J.D. Gutl, J., W. Flam, and M. Gorny, New results on the fi sh and Taylor, pp. 119-131, Oxford Univer.;ity Press, 1995. shrimp fauna of the Weddell Sea and Laz.arev Sea (Antarctic), Crame. J.A, An evolutionary framework for the polar regions, J. Proc. NIPR Symp. Polor Bio[" 7,91-102, 1994. Biogeogr. . in press. Hedgpeth, J.W., Perspectives of benthic ecology in Antarctica, in Crame, J.A, and A. Clarke, The historical component of marine Research in 1M Anlarclie, edited by L.O. Quam, pp. 93-136, taxonomic diversity gradients, in MarilU! Biodiversity: Causes American Association for the Advancement of Science, Wash and Consequmce3, edited by R.F.G. Ormond and J. Gage, Cam- ington. 1971. CLARKE: BENTHIC POPULA nONS 387 HOlljo, S. , Fwtide fluxes and modem sedimentation in the polar 8th Inlemarionai ~chinodenn conje~nc~j, edited by B. David, A. oce&I1, in P{Jlar Oc~ancgraphy, ParI B: Chemistry. Diologyarul Guille, I.P. Ftral, and M. Roux, pp. 111-120, Balkerna, Rotto' Geology, edited by W.O. SmiUI, Ir . pp. 687-739,1990. darn, 1!I94. lohn, D.M., J. Tittley. G.W. Law,:"" """ PJ.A. Pugh, Distributior, Ficken, G.B., Non-pelagic reproduction of some Antarctic prose of seaweed floras in the Southern Ocean, Boranica Marina, 37, brancb gastropods from Signy Island, South Orkney Islands, 235-239, 1994. Ma/4cologia, 19, 109-128, 1979a. Kendall. M.A.. and M. Aschan. l..3.titudin:lJ gr..!dients in the struc Picken, G.B., Growth, production and biomass of the Antarctic ture of macrobenthic communi(es: a comparison of Arctic, [em gastropod LaeviIavunario anuur:tica Marten; 1885. J. Exp. Mar. penile and tropical silOS, J. Exp. Mar. BioL Ecol.. 172, 157-169, Bioi. Ecol.. 40, 71-79, 1979b. 1993. Picken, G.B., The nearshore prosobranch gastropod epifauna of K16ser, H.. G. Mercuri, F. LatW1lUS. M.L. Quartino, and C. Signy Island, South Orkney Islands, Ph,D. thesis, University of Wieneke, Gn the competitive baJance of macroalgae at Potter Aberdeen, Scotland, 1980a. Cove (King George Island, South Shetland), Polm Bioi., 14, 11- Picken, G.B., The distribution, growth and reproduction of the Ant 16, 1994. arctic limpet Nocella (Palinigeraj concinna (Strebel. 1908), J. Lipps, J.H., and C.s. Hickman, Origin, age and evoI.H!~n of Ant Exp. Mar. Bioi. Ecol .. 42. 71-85, 198Ob. arctic and deep-sea faunas, in Environment of rhe Deep Sea, Picken, G.B., Reproductive adaptations of Antarctic benthic in Volwne 2, edited by W.G. Ernst and lG. Monn, pp. 324-356, vettebraleS, BioI. J. Linn. Soc., 14.67-75, 198Oc. Prentice-Hall, Englewood Cliffs, New lersey, 1982. Pielou, E.C., An InrroductilJn to Mathematical &ology. 286 pp .. Uttlcpage. J.L., Oceanographic investigations in McMurdo Sound, lohn Wiley, New York, 1969. Antarctic, in Biology oj Antarclic Seas //, edited by G.A. Llano, Poore, G.e.B., and GD.F. Wilson, Marine species richness, Nature, pp. 1-37, A.,lIarcl;c Research Series, 5, American Geophysical . 361, 597-598, 1993. Union. WasbiDgton, D.C .. 1965. FfC3ton, F.W., The canonical distribution of conunonness and rar Luxmoore. RA., Moulting and growth in serolid isopcx1s. J. Exp. ity, Ecology. 43, 185-212, 1962. MOl". Bioi. Ecol .• 56, 6?-85, 1982. P..aJS(".hert, 1'.1., Ecgebmisse der faunistischen Arbeiten im Bentha! Macpherson, E., The marine Mollusca of Arctic Canada, Nat. Mus. 'ton King George Island (SiJdshetlandinseln. AnlarCtis), Bu. Canada Publ. Bioi. Oceanogr., 3, 1··149, 1971. Pola,jorsch., 76, 1-75, 1991. Magurran, A.E., Ecolog"caj Diversity and ilS Measurement, 179 I'p .. Rel, M.A., C.T. Stuan, R.R. ~:cssler, I.A. Allen, lA. Sanders, and Princeton Universily, New Jersey, 1988. G.D.F. Wilson, Global-scale latitudinal patterns of species di Mileikovsky, S.A., Types of larval development in marine bottom versity in the deep-sea benthos, Nature, 365, 636-639, 1993. invertebrates, their distribution and ecological significance: a re Richardson, M.D., The classification and structure of macrobenthic evaluation. Mar. Bioi., 10, 193-213, 1971. assemblage! of Arthur Harbour, Anvers Island. Antarctica. Ph.D. Minelli, A., Biological Systematics: The Slale OJ 1 he Art. 387 pp .. thesis, Oregon State University, t 976. Cbapman & Hall, London, 1993. Richardson, M.D., and I.W. Hedgpeth, Antarctic soft-bullorn, rna Moe, R.L., and T.E. DeLaca, Occurrence of macroscopic algae crobenthic community adapu:.tions to a cold, highly productive, along the Antan:tic peninsula, Antarct. J. U.s.. 11(5), 20-24, glacially affected environment.. in Adaplations Within Amarctic 1976. Ecosystems, edited by G.A. Llano, pp. 18!-195, The Smithsonian Mortensen. T., Studies oj the Development and Larval Fonns oj Institution, Washington D.C. , 1977. Echinoderm.;, G.E.C. Gad, Copenhagen, 1921. Richardson, M.G., The ecology and reproduction of the brooding Monensen, T., Echinoidea and Ophiuroidea. Discovery' Rep., 12, Antarctic bivalve Lissarca miliaris. Bull. Brit. Amarc/. Surv .. 49, 199-348, 1936. 91-115, 1979. Murphy, E.I., A. Clatk C. Symon, and I. fuddle, Temporal vari· Ross, R.M., and L.B. Quetin, Ecological physiology of larval ation in Antarctic sea-ice: analysis of a long-tenn fast-ice record euphausiids, Euphausia superba (Euphausiacea), Mem. Quuns. from the South Orkney Islands, Deep-Sea Res .. 42. 1045-1062, MILr .. 31, 321-333, 1991. 1995. Ross, R.M., L.B. Quetin, and E. Kirsch, Effect of temperature on Nicol, D., An assay on the size of marine pelecypods, J. Paleont. developmental times and survival of larval stages of Eup"awia 38,968-974, 1964. superba Dana, J. Exp. Mar. Bioi. Ecol., 121,55-71. 1988. Nicol. D .. Size of pelecypods in recent marine faunas, Nautilus. 79. Ross, R.M .. L.B. Quetin. and C.M. l..ascara, Distribution of Ant 109-113, 1966. arctic krill and Dominant Zooplankton West of the Antarctic Nicol, D., Size trends in living pelecypods and gastropods with cal Peninsula.. this volume. careous shells, Nauli/w. 92. 70-79, 1978. Roy, K., D. Jablonski, and 1.W. Valentine, Eastern Pacific mol North, A. W., and M.G. White, Reproductive strategies of Antarctic luscan provinces and latitudinal diversity gradient: no evidence fish, in Proceedings of the Fifth Congress oj Ellropean Ichthy for "Rapoport's Rule", Proc. Nat. Acad. Sci. U.S .. 9/, 8871-8874, ologists, Stocklwlm 1985, edited by S.O. Kullandcr and B. Fern 1994. holm, pp. 381-390, Swedish Museum of Natural History, Stock Shabicn, S.V., The natural history of the Antarctic limpet Patinigera holm, 1987. polaris (Hombron and Jacquinot). Ph.D. thesis, University of Pearse. 1.S., Cold-water echinodenru break. 'Thorson's rule', in Oregon, 1976. Reproduction, Larval Biology and Recruitment in the Deep-Sea Smith, W.O., Jr., and E. Sakshaug, Polar phytoplankton, in Polar Benthos, edited by C.M. Young and K.I. F.ckelbargcr, pp. 2643, Oceanography. Pan B: Chemistry, Biology ami Geology, edited Columbia University Press. New York, 1994. by W.O. Smith, Ir., pp. 477-525, 1990. Pearse, 1.S., and I. Bosch, bnxxling in the Antarctic: Ostergren had Somero, G.N., and A.L. DeVries, Temperature tolerance of some it nearly right, in Echinodenns Through Tune (Proceedings of the Antan:tic fishes, Science, 156. 257-258, 1967. 388 ECOLOGICAL RESEARCH WEST OF THE PENINSULA Spigh~ T.M., CensustS of rocky she", prosobranchs from Wash Rabitti. and M. Vincx, Deep-sea meiofauna communities in Ant ington and Costa Rica. Am. Nat., Ill, IDn-I097, 1976. arctica: structural analysis and relation with the environment, TtOtIl, l .w., G. Oehlet, D.G. Ainley, lL. Bengston, D.B. Siniff, Mar. EcoL Prog. Ser .. in press. R.M. Laws, and D. Roonsevell. TempornJ variability in Antarctic Venneij. OJ .. Anatomy of an invasion: the trans-Arctic interchange, marine ecosystems: periodic fluctuations in th e phocid seals, Pal.obiology, 17. 281-307, 1991. Can. J. Fish Aquat. Sci., 48. 631-{i39, 1991. Wagele, lW., On the reproductive biology of Ceratoserolis (rila lborson. G .. The tarnll development, grcwth, and meiliINlism ~{ bitoides (Crustacea: Isopoda): latitudinal variation of fecundity Arctic marine bottom inv!%tebrates compared wi th t!:0se Gl o(i1er and embryonic development, Polar Bioi .• 7. 11-24. 1987. seas. Med1- Cr~n/and.. 100, 1-155, 1936. White, M.G., Marine benthos, in Antarctic Ecology, Volume 2, edit Thorsen. G., Reproductive and hrvil1 ecology of marine bonom in ed by R.M. Laws, pp. 421-461, Academic fuss, London, 1984. vertebratf.s, 3io!. Rev" 25, 145, 1950. Winston. lE.. Systematics and marine conservation, in Systematics, Thorson. G., Bottom c:mununitl:£ (sublittoraJ or shallow shelf), in Ecology and /11< Biodiversity Cri.!is. edited by N. Eldn:dge, pp. Trearise on Marine Ecology and Paleoecology. edited by J.W. 144-168, Columbia University Press, New York, 1992. Hedgpeth, pp. 461-534, Geological Society of America. New York. 1957. Thtm;ton, M.H., The Crustacea Amphipoda of Signy Island, South Andrew Clarke, Marine Life Sciences Division, British Antarctic Orlcney Islands, Br. Antaret. Surv. Sd Rep .. 7 J, 1-133, 1971, Survey, High Cross, Madingley Road, Cambridge CB 3 OET, UK Vanhofe, S., l. Wittocclc. G. Desme~ B. Van den Berghe, i{.L. He=, R.P.M. Bal<, G. Nieuwland, 1.H. Vosjan, A. Boldric., S. (Received September 5, 1995; accepted October 25, 1995.)