l MARINE ECOLOGY PROGRESS SERIES Vol. 118: 179-186.1995 ; Published March 9 Mar. Ecol. Prog. Ser. l

Pattern of spatial distribution of a brood-protecting schizasterid echinoid, cordatus, endemic to the Kerguelen Islands

Glie Poulin, Jean-Pierre Feral

Observatoire Oceanologique de Banyuls, U.R.A. C.N.R.S. 117, F-66650 Banyuls-sur-Mer, France

ABSTRACT. This study examined the spatial distribution at different geographic scales of the echinoid which is endemic to the Kerguelen Islands. Special attention was paid to the non- dispersal strategy of the specles. Itlives burrowed in the sediment and females brood the~ryoung in dorsal pouches. The dispersal of this species is therefore characterised by a limited mobility among adults and the lack of a free-swimming larval phase. Using SCUBA and dredging, A. cordatus was sampled all around Kerguelen. The spatial distribution from the island scale to the bay scale shows dis- continuities at 2 levels: (1) at the island level favourable sectors (princ~pallycharacterised by jagged coastline with numerous sheltered bays) are separated by linear coastline or swell exposed sectors; (2) at the bay scale A. cordatus lives in high density, isolated demes in shallow water of sheltered bays. A. cordatus was most numerous in sediments that ranged from medium to fine sand. The granulometry of the sed~mentand the lack of predation determine this aggregated spatial distrlbution pattern. Con- sidering that the scale of larval dispersal is the consequence of spatial and temporal habitat structure, the non-dispersal strategy of A. cordatus is associated with a spatially varying but temporally constant habitat as predicted by theoretical models.

KEY WORDS: Abatus. Brooding . Habitat limits. Kerguelen . Non-dispersal strategy. Spatial distribution . Subantarctic

INTRODUCTION Studies on the spatial distribution of organisms are important for several reasons (Thrush 1991). Firstly, Species spatial distribution is the result of the inter- the knowledge of distribution patterns is necessary to act~onof biotic and abiotic constraints (Thrush 1991). investigate population dynamics and genetics and, In soft-bottom marine invertebrates and particularly more generally, population biology. The different dis- deposit-feeders, functions such as feeding, respiration tribution patterns (aggregated, random or regular and motility are strongly linked to the sediment char- distribution) will determine the choice of a sampling acteristics of the habitat. Generally, granulometry and design, in order to avoid bias in statistical analysis. the organic content of the sediment are the main fac- Secondly, it is important to identify the factors respon- tors that determine habitat (Lopez & Levinton 1987). sible for the distribution patterns. Thirdly, there is the However the range of the habitat can be modified by potential to understand the relationships between the biotic constraints, such as interspecific competition and spatial distribution and life-history traits, particularly predation; life-history factors may also influence for species without larval dispersal and that have low spatial distribution (Thrush 1991). Larval dispersal and motility (Carlon & Olson 1993). recruitment processes are also important factors re- The schizastend echinoid Abatus cordatus (Verrill, lated to spatial distribution. Indeed, factors such as 1876) is endemic to the Kerguelen Islands (49" 21'S, length of larval stage duration, currents and site selec- 70" 12' E) and 1s a deposit feeder that burrows a few tion by larvae affect the spatial pattern of species centimetres below the surface of the sediment. The (Thrush 1991). development of A. cordatus is direct (Schatt 1985, P.

O lnter-Research 1995 Resale of full article not permitted 180 Mar. Ecol. Prog. Ser. 118: 179-186. 1995

Schatt & J.-P. Feral unpubl.) and the females brood METHODS their young. The juveniles are released on the sea floor near their mother. Some information on the distribu- Exploratory phase. Exploration using SCUBA diving tion of A. cordatus is available (Magnicz 1980, Schatt and dredging (Charcot dredge) was made at different 1985, Mespoulhe 1992). This burrowing echinoid is scales (Fig. 1):firstly at the island scale to evaluate the often very abundant and high densities are found at overall distr~butionof Abatus cordatusaround Kergue- shallow depth (0 to 2 m) near beaches. Individuals in len; secondly at the scale of a large gulf with numerous dense aggregations often touch or nearly touch each scattered islands (Golfe du Morbihan); and thirdly at a other. The goal of the present study was to establish bay scale. Densities of A. cordatuswere estimated and the spatial distribution of A. cordatusat different spa- density indices were attributed to each site: low tial scales. (<5 ind. m-'), medium (5 to 20 ind. m'-2)and high den- sity (>20 ind. m-'). The type of substratum was recorded. Density transects: density and vertical ------. , and horizontal patterns of distribution. After the exploratory phase, 3 major study ' -1areas (Ile Haute, Anse du Halage and Port . - Couvreux, respectively Sites 5,12 and 17 ir? Fig. l), were selected for their high popula- tion densities. These are the locations of eco- logical and physiological studies (Magniez I I 1980, Schatt 1985, Mespoulhe 1992). At the 3 l , . sites, we examined a transect of 50 or 100 m

: ./ length from the beach towards the open sea, until the echinoid density was zero.

,L> C-i 3 l, + L-: - c .-.!,,33 6'-. - . c . _I i, m .--> nigr donqtry .-\ . r. -. c- - . F*.. f. , '. , ,,l5 , 5llU aP-ztry ', ' ..- ,. '- A lnedurn r " t \? \, - ZZ +.m de-7 :y l1-..- ::c> -2: .. 8 a>,,> P ,. a3sence I -- & -;, ,.?l,-.------::l', I >- f~ -+& drcdgi-g - ,-..a: , U *1 I, ' L: ".lf.,. , , .- .-. . - .-a- v-- .-.. . I ,. ,. .., -L1 .-._-... -- -- -p- ' - ,. --- p- Pan --: Cor~vteua 1 ,,:'>I5 I" 7?"

Fig. 1. Distribution pattern of Abatus cordatus around the Kcrguelen Islands. (a) Golfe du hlorbi- han. (b) Bras de la Fondene. Numbers correspond to thc sitcs descnbed In Table l Poulin & Feral: Spatial distribution of Abatus cordat~ls 181

Quadrats (0.5 m') were made every 10 m, or more fre- RESULTS quently if a topographical change occurred (e.g slope break, substrate texture, algal cover). All individuals Distribution patterns found were removed from each quadrat and counted. This procedure of sampling by hand could under- Abatus cordatus is distributed all around the Ker- estimate the density of small individuals. Correspond- guelen Islands (Fig. 1, Table 1). However, high density lng depth.s were regularly recorded with an electronic populations are found principally in sectors where the depth gauge in order to draw bottom profiles. Depths coastline IS lagged and where bays are abundant were calculated from the equinoctial low water Major (northwestern sector and Golfe du Morbihan). Only features of the substratum and of algal composition scattered and isolated individuals were found on the and density were also noted. west coast (Site 29) which is swept by strong swell, and At Ile Haute a second perpendicular transect was on the poorly jagged east coastline. carried out to circumscribe the population. Data from Investigations on the spatial distribution of Abatus the 2 perpendicular transects were extrapolated to pro- cordatusat different scales indicate that discontinuities duce 3-dimensional plots of density and of bottom in the distribution occur at 2 levels: firstly, at the island topography at this site. We used a gndding method, level, where favourable sectors are separated by linear which uses geostatistical techniques to calculate the coastline or swell exposed sectors; secondly, at a autocorrelation between data points and produce a smaller scale, where A. cordatusis distributed in small minimal variance unbiased estimate ('kriging' option, populations. Indeed, populations are generally charac- SURFER Access System, Golden Software, Inc., terised by high-density, isolated aggregations (up to Golden, CO, USA). 70 mature ind. per 0.5 m2)in favourable sites, in shal- At Port Couvreux we repeated the same transect 1 yr low water at the bottom of sheltered bays (Fig. lb). later to establish the stability of the spatial distribution However, lsolated individ.uals were observed during of high population densities. SCUBA diving at up to 25 m depth on muddy sand, and Sediment sampling and analysis. Substrate samples have been reported down to 560 m depth (De Ridder et (core-box, 5 cm2) from the upper 5 to 6 cm were al. 1993) around Kerguelen. taken at the location of the highest density of Abatus cordatusat Ile Haute, Anse du Halage and Port Cou- vreux to evaluate the particle size composition of Transects the substratum. The localities of these sites are shown in Fig. 1. The particle-size frequency distribution Fig. 2 shows densities of mature Abatus cordatus were obtained by sieving the dried sediment through along bottom profiles. At Ile Haute (Fig.2a), the density a sel-les of sieves (50, 100, 250, 400, 630, 1000 and increases rapidly in the subtidal zone to a maximum 2000 pm). (34ind. per 0.5 m2) at 0.2 m depth. Twenty metres from

Distance from the coast line (m) Distance from the coast line (m)

Fig. 2. Density (top line) and topo- graphy (bottom line) profiles along transects. (a) Ile Haute; (b) Anse du Halage; [c) Port Couvreux (1991); (d) Port Couvreux (1992) Distance from the coast line (m) Distance from the coast line (m) 182 Mar. Ecol. Prog. Ser. 118: 119-186, 1995

Table 1 Characteristics of sites where Abatus cordattls was found by SCUBA divers. Density index: low, <5 ~ndm-', medium, 5 to 20 ind m-'; h~gh,> 20 ind, m-'. Site numbers are shocvn In Fig. 1. 'Sites from this study

No. Si.te Presence Depth (m) B~otope -- - l A Port Aux Franqais No Kelp forest 1B Port Aux Franca~s No - Mud 1C Port Aux Fran~ais Yes Medium Muddy sand 1D Port Aux Fran~ais No Mud 2A Port Raymond Yes High Sand 28 Port Raymond Yes Low Mud 3 Anse de Saint Malo No - Mud 4 Bras Karl Luyken No Mud 5A Ile Haute ' Yes High- Sand 5B Ile Haute No - Kelp forest 5 C Ile Haute No Rocks 5D Anse des Rennes No Rocks 6 Ile Heugh No Mud 7 Ile Mayes No Mud 8 Ile Blackney Yes Muddy sand 9 Ile du Chat No Rocks !on !!e Shum Yes bteiiiunl Muddy sand 1OB fle Shum No - Mud 11 Port Bizet Yes Low muddy sand 12 Anse du Halage ' Yes High Sand 13A Port Jeanne D'Arc Yes High Sand 13B Port Jeanne D'Arr No :V; U il 14A llots Glenan Yes Medium Mud 14B Ilots Glenan No Mud 15A Chateau d'If No Muddy sand 15B Baie Norvegienne Yes Medium Sand 16A Anse Caron Yes High Sand 16B Anse Caron Yes Low Mud 17 Port Couvreux ' Yes H1gh Sand 18A Anse Aldebert Yes High Sand 18B Anse Aldebert Yes Medium Sand 18C Anse Aldebert No - Kelp forest 19A Anse Thomas Yes Medium Sand 19B Anse Thomas No Muddy sand 20 Ilot des Trois Bergers No Rocks 2 1 Baie du Hopful Yes Low Muddy sand 22A Port Matha Yes High Sand 22B Port Matha Yes Medium Mud 22C Port Matha No Muddy sand 23A Baie du Brise-Lames Yes High Sand 23B Baie du Brise-Lames Yes High Sand 23C Baie du Brise-Lames No Kelp forest 24A Anse du Jardin Yes High Sand 24B Anse du Jardin Yes Low Muddy sand 25 Port Chrismas No Muddy sand 26 Baie des Swains Yes Sand 27A Fjord des Portes Noires No Mud 27B Fjord des Portes Noires Yes Mud 28 Anse de Larmor No Sand 29A Baie du Noroit No Sand 29R Baie du Noroit No Sand 29C Pointe Berger Yes Low Sand 30 Baie de la Mouche Yes H1gh Sand

the coast, the bottom drops rapidly from 0.5 to 2.5 m and sity area is much wider and the density itself is twice as A. cordatusbecome progressively more isolated great (70 ind. per 0.5 m2).Again, the decrease of Aba- At Anse du Halage (Fig. 2b), the distribution profile tus cordatusdensity is correlated with a change in the is similar to the preceding one, although the hlgh den- bottom profile. Poulin & Feral: Spatial distribution of Abatuscordatus 183

Distance along beach (m)

v-5- l[ 5-10 I 10-20- C Density (individuals 10.5 m')

Fig. 3 Three-dimensional plot of (a) Abatuscordatus density and (b) topography of the site based on 2 perpendicular transects at the Ile Haute (SURFER 'kriging' option) (c) Two-dimensional representation of A. cordatusdensity distribution at Ile Haute. Levels of grey show density (~nd.per 0.5 m'); (- ) so baths (m);I-----) transect lines

At Port Couvreux (Fig. 2c), the peak of density is Particle size distribution deeper (1.5 m) and the first individuals encountered are 20 m from the coastline. However, the lower limit The particle size distributions of the substrata of the is unchanged and the density also decreases greatly 3 high density areas are shown in Fig. 4. At Ile Haute when the depth reaches 2 m. One year later (Fig. 2d), and Anse du Halage the sediment in which Abatus the distribution profile was relatively unchanged but cordatus was found falls within the limits of sand (2.0 to the bottom profile shows some differences along the 0.063 mm grain size) with medium to finehedium first 30 m of the transect, indicating a marked influence of the hydrodynamic activity of the area. This was con- firmed by the observation of deep ripple marks in 1991 Silt and clay Sand Granule and 1992. f~ne rned~urn coarse In all areas, Abatus cordatus showed a peak of den- sity in the shallow subtidal zone. At Ile Haute and Anse du Halage, these peaks began not far below the lower tide level while it was typically deeper at Port Couv- reux. Field observations showed that A. cordatus was not found in high energy sites (west and northeastern coasts). The occurrence of Abatus cordatus is shown in terms of 3-dimensional plots of density (Fig. 3a), bottom topography (Fig. 3b) at Ile Haute, and 2-dimensional projections (Fig. 3c). Most of the population is localised on a small plateau between 0.2 and 1 m depth and the entire population lives on a 2500 m2 surface. The esti- Particle size log (~nmicrons) mated density was 10 '0 15 X 103 mature ind'viduals at ~i~,4. size frequency distribution (ill percent) this site (test length '27 mm for females and 19 mm for of the substrata of: A. Ile Haute (I); B, Anse du Halage (A); males; Magniez 1980). C. Port Couvreux (a) 184 Mar. Ecol. Prog. Ser.

sand grades predominant. At Port Couvreux samples iment becomes finer with increasing depth. Therefore, were characterised by a finer sand, with a low percent- the substratum particle size may be a limiting factor age of silt and clay (<20%). controlling the localisation of high density populatlons. In addition to abiotic constraints which determine the range of the habitat, biotic factors such as interspe- DISCUSSION cific competition (Thompson 1982) and predation can affect distribution patterns. Generally, when prey dis- Distribution pattern and habitat limits play an aggregated spatial pattern, predators concen- trate their feeding in the richest patches and tend to The spatial distribution of Abatus cordatus is charac- equalise prey density (Schneider 1978, Sih 1982, Bot- terised by numerous, dense, isolated populations in ton 1984). Predation on Abatus cordatus was never shallow water (0 to 3 m) and scattered individuals to observed in the field but organic parts of broken spec- 560 m depth. This dispersed distribution in high den- imens are rapidly eaten by Serolis spp. (Isopoda: Crus- sity demes appears to be the consequence of a specific tacea) that are very abundant in the subtidal area. It habitat. The upper limit is the lowest tide level in shel- seems unlikely that they attack healthy individuals but tered sites, or the depth limit of swell action in less perhaps they prey on very young ones. Gulls Larus sheltered sites, as in Port Couvreux. Indeed Ile Haute dominicanus are potential predators because of the and Anse du Halage are very sheltered but Port Couv- low depth at low tide at which the highest densities of reux is more exposed to the swell. These data indicate A. cordatus are found, but predation has not been that A. cordatus is intolerant of wave action and the observed. The burrowing habits of A. cordatus make displacement of the peak of density to a deeper zone at them invisible for predatory birds. Gastropods are fre- Port Couvreux may be related to this factor. Generally quently described as important predators for irregular density decreases ~dpidiyat less than 2 m depth. The echinoids (Chesher 1969, Dix 1970, Hughes & Hughes particle size composition of the substratum is usually 1971 1981, Gladfelter 1978, McClintock & Marion a primary factor determining the habitat of deposit- 1993) but the lack of holes in beached tests indicates feeders. It influences both respiratory and locomotory that they are not predators of A. cordatus. It is there- functions (Lopez & Levinton 1987). fore probable that predation does not contribute to Since Abatus cordatus lacks a sophisticated respira- the spatial distribution of A. cordatus. Likewise inter- tory-current-producing mechanism such as a respira- specific competition certainly does not play a role on tory funnel or sanitary drain, it could be limited to spatial pattern because of the quasi-monospecific pat- coarse sediments in shallow waters because of the tern of populations. need to maintain sufficient water flow (Higgins 1974). The presence of high density populations of Abatus The relatively large pore space in coarse, well-sorted cordatus is probably determined by the nature of the sediment probably allows a better flow of oxygenated substrata and lack of turbulence. The occurrence of water. As in many other spatangoids (see Chesher scattered individuals in the adjacent deeper zones and 1969 for a review; Ferber & Lawrence 1976, Schinner generally with different types of substrata (often 1993), A. cordatus emerges from the san.d under condi- muddy sediments] indicate that A. cordatus can live in tions of oxygen deprivation in aquaria, when water very different habitats, but these individuals are often circulation stops. In general, irregular echinoids, which found on the surface of the sediment (Fig. 5).More- inhabit fine sediments, excavate specialised respira- over, the absence of small individuals in these areas tory connections with the surface (De Ridder 1982, suggests recruitment is very low or absent in such Kanazawa 1991). The oxygen consumption rate of A. places and that high density zones function as nurs- cordatus (Guille & Lasserre 1979, Magniez & Feral eries. The movement towards deeper zones could arise 1988) is comparable to that of the urchin Cassidulus when the individuals are large enough to manipulate canbbearum (Gladfelter 1978). This is relatively high different substrata, as suggested by Lawrence & Fer- compared to other burrowing echinoids (Webster 1975, ber (1971) for Lovenia elongata, or young could remain Gladfelter 1978, Magniez & Feral 1988). It also sup- stationary during the early period of growth as pro- ports the idea that, like Cassidulus spp., A. cordatus posed by Chesher (1969) for ~Vleomaventricosa. is limited to well-aerated substrata (Gladfelter 1978, Freire et al. 1992). A number of irregular echinoid species show a Distribution pattern and non-dispersal strategy decrease of burrowing and locomotory abilities in finer sediments (Lawrence & Ferber 1971, Ferber & Some authors (Jackson 1968, Carlon & Olson 1993) Lawrence 1976, Lawrence & Murdoch 1977). Abatus have considered larval dispersal distance as an expla- cordatus could also have such problems when the sed- nation for adult spatial patterns. From this point of Poul~n& Feral. Spat~aldistribution of Abatus cordalus 185

Table 2. Optlmal d~spersalstrategies under varying habitat heterogeneity and instability

No perturbdtion Perturbations

No spatial No Dispersal heterogeneity selection Spatial No Mixed heterogeneity dispersal

habitat heterogeneity and instability. The non-disper- sal strategy is favoured only if the habitat is heteroge- neous (in terms of low and high density sites) and if habitat is stable in time (in the sense of persistence). In Abatus cordatus, if spatial heterogeneity seems clearly established because of the discontinuity of the habitat (dense, isolated demes), it is more difficult to prove the time-stability of those populations. How- ever, we have some indications: (1) The high density populations are always found in sheltered bays where tidal currents and wave action are weak. Indeed this region is known for frequent storms, and the swells Flg. 5. V~deotapeframe showing 2 specimens of Abatus cor- can be devastating for shallow sea-floor and beaches. datus (45 mm length) on the surface of a muddy sediment at Kerguelen (Pointe du Zodiac, extremity of the north coast of (2) An indication of the time stability is given by a the Anse du Halage, 7 m depth) and 1 just below the surface 10 yr study at the reference site Anse du Halage. We of the sediment (arrow) observed during this time neither a crash, nor an im- portant variation in the density of A, cordatus.More- over, a replicate of the transect in Port Couvreux 1 yr view, an aggregated distribution may result from short later showed no difference in the general distribution larval dispersal time, simultaneous or gregarious set- pattern of this species in spite of a modification of the tlement, or habitat selection by larvae. In the case of topographic profile probably due to a limited swell. Abatus cordatus,if the brood-protecting strategy and (3) Another indication is given by the age structure of the release of young on the bottom near their mother the population observed at the Anse du Halage in could produce high-density, isolated populations, the December 1992. An exhaustive sampling of quadrats mobility of the burrowing echinoid would prevent (2 m2) allows us to reconstruct an age pyramid that population discontinuities. This hypothesis is therefore indicates a regular recruitment for at least 5 yr (Feral conceivable only for sessile organisms. & Poulin 1994). As a result, A. cordatusfits the predic- Another approach considers the scale of larval dis- tion of such models, and its non-dispersal strategy, in persal as the consequence of spatial and temporal this case, is associated with a spatially varying but habitat structure. Indeed, from a number of models, temporally constant habitat. Our case study thus con- the heterogeneity and/or the instability of habitat have tributes to an evaluation of models of dispersion, but been recognised as fundamental features which ac- does not substantially support them. Other examples cord with optimal dispersal strategies (Cadgil 1971, are needed to validate the importance of temporal Roff 1974, Frank 1981, Hastings 1983, Hardin et al. and spatial habitat structure on evolution of the dis- 1990, McPeek & Holt 1992). Temporal variation of car- persal strategies. rying capacities (which reaches zero in the case of ex- tinction) will favour dispersion because of the necessity Acknowledgements. This work was supported by specific grants from the lnstitut Fran~aispour la Recherche et la Tech- to recolonize free habitats. On the other hand, when nologie Polaires (formerly T.A.A.F. Mission de Recherche) spatial variability of carrying capacities increases, the 'BENTHOS/MAC' program. We thank the I.F.R.T.P. for facili- probability for a propagule to reach a 'good' site de- ties In Kerguelen. We are grateful to M.-J.Bodiou for drawing creases. Thus, the balance of temporal and spatial vari- the maps. Thanks are also due to P. Schatt for discussions and help in the field and to V. Andersen for allowing us to use her ations of carrying capacities of habitat determines an SURFERsoftware. We are grdteful to J. M. Lawrence for read- optimal dispersal strategy for the species. Table 2 ing the manuscript. M't? also thank him and 2 anonymous ref- shows the optimal dispersal strategies under varying erees for help~ngus to improve the English text. 186 Mar. Ecol Prog. Ser. 118: 179-186, 1995

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This article was submitted to the edrtor (vfannscnpt first received: June 23, 1994 Revlsed verslon accepted December 5, 1994