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The ecology of Evechinus chloroticus.
Edible Sea Urchins: Biology and Ecology Editor: John Miller Lawrence 9 2001Elsevier Science B.V. All rights reserved.
245
The e c o l o g y o f Evechinus chloroticus. M.F. Barker Department of Marine Science, University of Otago PO Box 56, Dunedin, New Zealand
1. INTRODUCTION
Evechinus chloroticus (Valenciennes), known locally as "kina," is a ubiquitous echinometrid endemic to New Zealand. It is one of the largest sea urchins known, with a maximum test diameter (TD) of 180-190 cm (pers. obs.). It was harvested by Maori people before the arrival of Europeans in New Zealand and more recently has been exploited in small quantities in restricted areas around New Zealand. The morphology and taxonomy are well described by (McRae 1959) and Mortensen (1922). Its morphology and distribution are also described by Cook, (in press). As the only shallow water sea urchin on hard bottoms around New Zealand, knowledge of its ecology is of great importance. The ecology of northern populations of E. chloroticus were reviewed by Andrew (1988).
2. GEOGRAPHIC DISTRIBUTION
Evechinus chloroticus is widely distributed around the main islands of New Zealand but is also found at the Chatham Islands to the west, the Snares Islands to the south (Pawson 1965) and from the Three Kings (Schiel et al. 1986) and Kermadec Islands to the north (Pawson, 1961, Cook, in press). This latter record has been questioned (Dix 1970a).
3. HABITAT
Evechinus chloroticus is generally found in water < 12 to 14 m deep although it has been collected from at least 60 m (Cook, in press). Intertidal populations also occur, mainly in the north of the North Island (Dix 1970a; McRae 1959). Dix (1970a) also noted intertidal populations at Kaiteriteri in Golden Bay at the north ofthe South Island. Although E. chloroticus is occasionally found on sandy or shingle areas (Dix, 1970a), this is not common and it is very seldom seen on fine sediments such as silt or mud (pers. obs.). Adults are normally found in areas with moderate currents and wave action, and are seldom found in areas of extreme exposure such as the surf shores that occur along much of New Zealand's west coast.
246 Evechinus chloroticus is found in somewhat different patterns of distribution and relationships with kelp and other invertebrates throughout New Zealand, and it is difficult to make broad generalisations about the habitat. In northern parts of New Zealand, E. chloroticus is most commonly found on shallow rocky reefs, dominated by encrusting coralline algae. In such areas they may be extremely abundant, with maximum densities of 40 m 2 reported by Choat and Schiel (1982) (Poor Knights Islands). When individuals are closely packed, density is strongly influenced by body size and density is less useful than biomass m. 2 Such coralline dominated reef flats are often interspersed with mature stands of laminarian algae. Within rocky reefs E. chloroticus is generally clumped, and there may be patches dominated by sea urchins which are almost devoid of kelp alongside areas where kelp is dense (Choat and Schiel 1982). The borders between such areas appear to be stable, and suggest a balance between echinoid grazing and algal colonization. In the Chatham Islands Schiel (1995),found E. chloroticus at almost every site sampled, at mean densities of 5 to15 m 2 but at maximum densities of 40 m 2 for large individuals. They tended to be abundant in sites where the deep water fucalean C.flexuosum was common. They were not seen in characteristically extensive deforested areas typical of northern N.Z. (Choat and Schiel 1982) and deforested patches larger than --25 m 2were never seen. Around the South Island E. chloroticus are less often seen on extensive rock fiats in open coast habitats, as they are in the north. More commonly they are in aggregations, either located between individual or small groups of kelp, or in barren areas of approximately 5 to 6 m diameter. On the Otago coast E. chloroticus is uncommon, although isolated aggregations of extremely large (120 to160 mm diameter) individuals do occur. The apparent rarity of E. chloroticus on this area of coast is anomalous, as the habitat would appear to be very suitable over much of the region and perhaps reflects very sporadic and low levels of recruitment. On the most southern coasts of the South Island E. chloroticus is more abundant and is very common in the sheltered inlets of Stewart Island. On the south western coast of Fiordland, E. chloroticus is abundant in the deep fiords which indent the coastline. In each fiord, steep cliffs covered with luxuriant rainforest overhang steep fiord walls that drop into deep water. This area of New Zealand is subjected to extremely high rainfall and many of the fiords have a surface low salinity layer (LSL) that may be up to 10 to 12 m in depth after several days of heavy rain in the local catchment. This fresh water layer is particularly deep in Doubtful Sound, because of additional discharge of freshwater from the tailrace of a hydro electric power station located on Lake Manapouri. In these fiords E. chloroticus is abundant, often in aggregations of up to 20 to 30 m 2 from immediately below the LSL, clinging to the steep rock faces sometimes on bare or coralline encrusted rock, sometimes on sunken trees which are often caught on ledges, or in shallower areas. Laminarians are only found towards the entrance ofthe fiord. In a survey of sea urchin abundance throughout Doubtful Sound, Wing et al. (unpub.) found mean densities varied from 5.22 at the entrance to 1.81 m 2 at Deep Cove the innermost site, with the highest density (5.98 m 2) at Espinosa Point (mid to outer reaches of the fiord). Juvenile E. chloroticus are cryptic throughout New Zealand. Dix (1970a) noted that individuals <10 mm TD are generally attached beneath both intertidal and subtidal rocks. Individuals between 10 to 40 mm TD occur in the intertidal and subtidal under rocks, or within small crevices or depressions in rocks and typically covered in debris. At around 40 mm TD individuals migrate into open habitats. The size structures of populations of Evechinus chloroticus vary over its geographic range. Populations typically have a unimodal size distribution dominated by larger individuals. Such
247 populations have been documented for the Otago coast (pers. obs.) Kaikoura and Kaiteriteri (Dix 1972), Tory Channel (Lamare and Barker, unpub.), and Dusky Sound (McShane 1992). The mean size of individuals in these populations ranges from 40 to 50 mm TD. (e.g. Kaiteriteri, Dix 1972), to 112 mm TD Dusky Sound (McShane et a1.1996). Populations with a bimodal or polymodal distribution are less common but have been described for Kaikoura (Dix 1972), Dusky Sound (McShane et al. 1994) and Doubtful Sound (Lamare and Barker unpub.). The size structure of populations of E. chloroticus can be distinctly different over relatively short distances. Along the Kaikoura Peninsula, for example, populations vary in mean body size and in the abundance of juveniles over distances of <5 km (Dix 1972).
4. ASSOCIATED SPECIES 4.1. Kelp In northern New Zealand Evechinus chloroticus is strongly associated with kelp forests often dominated by the laminarian Ecklonia radiata (Choat and Schiel 1982; Schiel 1982; Andrew and Stocker 1986) although in very shallow water they can be found in association with the fucaleans Carpophyllum mashalocarpum and C. angustifolium (Schiel 1982). In the Marlborough Sounds of the South Island they are mostly found with C. mashalocarpum and in areas subjected to high current flows Macrocystispyrifera (Dix 1970a; Brewin et al., in press). Further south on the Otago coast and at Stewart Island E. radiata only occurs as occasional isolated plants, and Macrocystis pyrifera is often the dominant kelp forest forming laminarian species (pers. obs.). In Dusky Sound in southern Fiordland (McShane et al. 1994) and further north at the entrance to Doubtful Sound (pers. obs.) E. chloroticus is found with E. radiata and Carpophyllumflexuosum. These are the most common laminarians though a number of red and green seaweeds are seasonally abundant. 4.2. Gastropods Evechinus chloroticus is often found in association with a variety of grazing gastropod species. Andrew and Choat (1982) reported a positive correlation between the abundance of E. cloroticus and the herbivorous gastropods Cellana stellifera (limpet), Trochus viridis (topshell) and Cookia sulcata (turbinid) at depths less than 12 m. Gastropod abundance was significantly lower in the absence of E. chloroticus. The effects of caging specific gastropods with E. chloroticus, supported the suggestion of a positive relationships between E. chloroticus and Cookia sulcata as the biomass (mean dry weight) ofE. chloroticus increased in the presence of the turbinid (Choat and Andrew 1986). Both Trochus viridis and Cookia sulcata occur in the South Island. Detailed relationships between E. chloroticus and other grazers have not been investigated. In some southern open coast situations E. chloroticus is often found in association with the abalone Haliotis iris especially in depths of 5 to 10 m. Wing (pers. comm.). He found that both E. chloroticus and H. iris in Paterson Inlet and Port Pegasus are found on shallow rocky reefs and the peak abundances overlap in depth. As they are rarely found together in the same quadrate (2 m 2) however, their distributions are negatively correlated at a relatively small scale.
248 5. FEEDING 5.1. Diet
(Dix 1970a) observed feeding ofE. chloroticus at both Kaikoura and Kaiteriteri. At least 11 species of algae were eaten at Kaikoura and only two at Kaiteriteri. Laboratory observations confirmed that E. chloroticus is chiefly herbivorous but eats a variety of food when algae are scarce. While E. chloroticus feeds on a wide variety of algal species, it shows preferences. Don (1975) examined this question in the laboratory and concluded that although E. chloroticus preferred E. radiata,, it grazed indiscriminately on all entrusting organisms when large brown algae were unavailable. The degree to which food choice experiments conducted in the laboratory can be extrapolated to the field is problematic. Such experiments should be conducted in natural conditions whenever possible. The study of Schiel (1982)highlights this. He presented the same seven species of algae to E. chloroticus in the laboratory and placed subtidally, on a rocky reef where E. chloroticus were relatively abundant (2.5 m 2) and randomly distributed. The amount of each alga grazed was different and the ranking of the algal species from the field experiment did not correlate with the rankings established by the laboratory choice experiment. It is clear that E. chloroticus exert a major influence on algal stands in the subtidal. Andrew and Choat (1982) used cages to exclude E. chloroticus from a 1000 sq m subtidal coralline fiat area in northern New Zealand. They found a large increase in biomass in a range of kelp species followed, especially E. radiata. The grazing activities of E. chloroticus also influence the structure of entrusting communities as well as algal stands. Ayling (1978) investigated the grazing ofE. chloroticus on encrusting communities dominated by sponges in both the field and in a laboratory study. In the field, they grazed sponge species according to abundance. In the laboratory, preferences for particular sponge species did not relate to the diet in the field. (Ayling 1981) suggest that E. chloroticus in benthic communities made up of encrusting organisms will readily graze all encrusting species except a few of the more massive sponges. Even these are grazed when food is in short supply. Although many encrusting animals produce chemical toxins or large quantities of mucus, Ayling (1978) found feeding preferences were not related to toxicity, although she did suggest that toxins of some species of sponges may influence feeding preferences. Algae contain phlorotannins (polyphenolic compounds that are the dominant secondary metabolites in temperate brown seaweeds) which are known to deter feeding by some invertebrate grazers (Van Alstyne 1988). Steinberg and Altena (1992) tested the tolerance of E. chloroticus to brown algal phlorotannins in six algal species, and found no correlation between feeding preferences and algal phenolic levels. Cole et al. (in press) found some evidence that high levels ofphlorotannins influenced grazing by E. chloroticus on certain species, particularly Carpophylummflexuosum which has two growth forms. The form which had high phlorotannin levels was not grazed by E. chloroticus in the field or in the laboratory. A more detailed investigation of the relationship of diet preferences and metabolites that deter grazers is required. Aside from the early studies by (Dix 1970a) at Kaikoura and Kaiteriteri, all the studies mentioned so far are for northern populations of E. chloroticus. Wing et al. (unpub.) found E. chloroticus near the entrances of southern fiords had a larger percentage of algae in the gut, smaller Aristotle's lantern indices and higher calorific gut content compared to populations in the inner fiords. They suggested this is evidence of nutritional limitations in inner fiord sites. The entrance and outer fiords are characterized by assemblages of laminarian kelps dominated by Ecklonia radiata, while the inner fiords with steeper rock walls only support filamentous
249 chlorophytes and small amounts of rhodophytes. Here E. chloroticus are often found grazing sunken logs (pers. obs.). Evechinus chloroticus caged at low densities and fed the more preferred alga E. radiata, had a higher reproductive output than individuals fed the less preferred species Carpophyllum sp. (Andrews 1986). This relationship broke down when individuals were caged at higher densities. Laboratory experiments using prepared artificial diets also showed that diet quality has a significant influence on reproductive output in E. chloroticus (Barker et al. 1998). A great deal more information is required from field studies before we will understand the relationship between food selection and other metabolic requirements, i.e. whether sea urchins selectively graze on algae or other organisms in order to maximize reproductive output or enhance other physiological processes. 5.2. Feeding rate Barker et al. (1998) found E. chloroticus in the laboratory ate significantly more prepared feeds than the algae Macrocystis pyrifera and Ulva lactuca. For all diets feeding rate showed a clear seasonal trend directly correlated with water temperature. Of the two algal diets, M. pyrifera was clearly preferred over U. lactuca for individuals 30 to 90 mm diameter. Schiel (1982) fed E. chloroticus, of a similar size to medium-sized individuals used by Barker et al. (60mm TD), a range of algal species in the laboratory. Although both the range of algal species and the experimental design was slightly different, the mean daily feeding rate per individual calculated from Schiel's 1982 data is 0.69 g day1 for the most preferred alga (Cystophora torulosa) compared to 0.88 for E. chloroticus feeding on M. pyrifera. This suggests that feeding rates for sea urchins may be similar, even though they are collected from widely different latitudinal locations.
6. MOVEMENT Movement in E. chloroticus, especially in relationship to levels and quality of food, is poorly understood. Dix (1970b) investigated movement of tagged individuals in aggregated populations at Kaikoura and at Kaiteriteri. At Kaikoura he found only small numbers (6% at 3 months, 10% at 6 months) had moved a maximum distance of 4.8 m. At Kaiteriteri, a site where brown algae are less abundant, movement was slightly greater. Tagged individuals had lower gonad indices, and less food in the gut than untagged ones which suggests that tagging affects feeding and is likely to influence movement. Dix (1970b) found that E. chloroticus in the laboratory moved more at night than during the day. Andrew and Stocker (1986) examined the movement of E. chloroticus in relationship to the availability ofE. radiata at two subtidal sites in northern New Zealand. Their results confirm Dix' s suggestion that movement is related to the availability of food. In the presence of drift algae, individuals increased their overnight movements. This suggests a chemosensory response to the presence of damaged kelp, although they did not appear to respond in a directional manner. Increased movement stimulated by an increase in the abundance of drift algae as has been reported for Strongylocentrotus species (e.g. Harrold and Reed 1985), has not been demonstrated in E. chloroticus and active feeding fronts of sea urchins have yet to be documented. Movement may also be affected by the presence of predators. Andrew and McDiamid (1991) report that E. chloroticus move less in habitats in which the rock lobster Jasus edwardsii (a
250 predator) are abundant than in areas where lobsters are scarse. There is a need for more studies on movement and behaviour in relation to food, especially in southern populations in fiordland. Here the fluctuating levels of the low salinity layer causes vertical migration of populations (pers. obs.) as individuals maintain their distribution within high salinitiy strata of the halocline, a physical requirement which must impact markedly on both the type and quantity of available food. Large starfish, Coscinasterias muricata and Astrostole scabra, are also abundant in this zone and their presence may also influence sea urchin behaviour.
7. REPRODUCTION Evechinus chloroticus is gonochoric, with a 1:1 sex ratio and an annual breeding cycle (Dix 1970c). The reproductive output varies with diet quality (Barker et al. 1998) and population density (Andrew 1986).
7.1. Gametogenesis The gametogenic cycle has been described in detail by (Dix 1970b; Walker 1982; Brewin et al., in press). The developmental sequence of gametogenic stages differs little in these studies and the following description can be regarded as applying to all populations: Spawning occurs during the austral summer, generally being complete by March in most populations. A build up of nutrient reserves in the form of nutritive phagocytes occurs during autumn and early winter (March-May), followed by gametogenesis during mid-late winter and into spring (June to October). Gonads are ripe during spring (October and November) although some individuals collected from the field can be spawned in the laboratory from October to March (pers. obs.).
7.2. Reproductive cycle The annual reproductive cycle has been described in detail by the calculation of monthly gonad size indices for populations from the north of New Zealand (Hauraki Gulf, Walker 1982), central regions (Wellington and Northern South Island (Dix 1970c; McShane et al. 1996); Brewin et al. (in press) and for the south west of the South Island, Dusky Sound, (McShane et al. 1996; Doubtful Sound, Lamare 1998; Lamare and Barker, unpub.) (Table 1). Male and female reproductive cycles are generally synchronous in most populations. Surprisingly, considering the wide latitudinal range covered by these studies (36 ~to 45 ~ and the marked differences in seasonal temperatures (13 to 22 ~ in the north, 8 to15 ~ in the south), there is no clear latitudinal trend in the breeding season. Gamete release occurs from November to February in most populations, the broadest season (October to May) when ripe individuals can be found being at Ranson Head, near the entrance to Doubtful Sound (Table 1). Different methods have been used to calculate gonad indices, making comparison among all populations difficult. However the maximum index is approximately 25 to 28 in populations in both the Marlborough Sounds and Doubtful Sound respectively (Table 1). There are marked differences in reproductive seasonality between populations that are often only a few km apart. Walker (1982) found significant differences in gonad volume in the Hauraki Gulf (three populations, 10 km apart) during most of the year but most pronounced during summer. Similarly Brewin et al. (in press) found temporal and spatial differences over less than 10 km in three populations in the Marlborough Sounds. In these populations there were also differences on both rates of
251 gametogenesis and recovery of individuals and gametogenic differences between sexes in these populations. Table 1. Spawning period and maximum gonad index (GI) of E. c h l o r o t i c u s arranged latitudinally from the north to south of New Zealand. Region Sampling site Year Spawning Max GI GI Author period formula 1 Walker (1982) Hauraki Gulf Noises Island 1975-76 Nov.-Jan. N/A 1975-76 Nov.-Jan. N/A 1 Walker (1982) Hauraki Gulf Rangitoto Island 1 Walker (1982) Hauraki Gulf Crusoe Island 1975-76 Jan.-Feb. N/A 2 McShane et al. 1993-94 Dec.-Feb. -- 20 Wellington Reef Bay (1996) 3 Brewin et al. 19.3 - 22.95 Marlborough PeranoHeads 1990-92 Nov.-Jan. (in press ) Sounds 3 Brewin et al. Marlborough Titi Bay 1990-92 Nov-Feb. 15.8 - 26.99 (in press) Sounds 3 Brewin et al. Marlborough Dieffenbach 1990-92 Jan.-Mar. 11.87- 20.9 (in press) Sounds Point 4 Dix (1970c) Golden Bay Kaiteriteri 1968-69 Dec. to Apr. N/A 4 Dix (1970c) Jan. to Feb. N/A Kaikoura 1968-69 3 Lamare & Barker. Doubtful Causet Cove 1993-94 Dec-Feb. 20.0 - 19.2 (unpub.) Sound (DS) 3 Knapp (pers. tom) DS Causet Cove 1999-00 Nov.- May 15 - 16 DS Espinosa Point 1993-94 3 Lamare & Barker Nov.- Apr. 18.3 - 25.5 (unpub.) DS Deep Cove 1993-94 Nov.-Jan. 14-24 3 Lamare & Barker (unpub.) DS Seymore Island 1999-00 3 Knapp (pers. com) Sept.-Jan. 28-29 DS Ranson Head 1999-00 Oct.-May 19-21 3 Knapp (pers. corn) DuskySound Anchorlsland 1992-93 Dec.-Feb. ~-8 -15 2 McShane et al. (1996) 1. Gonad volume/test diameter 2. Gonad volume/drained wet weight.x 100 3. Gonad wet weight/drained wet weight.x 100 4. Gonad volume/test volume x 10
7.3. Reproductive output Reproductive output (difference in pre and post-spawning gonad index) is a useful measure of actual gamete production. Brewin et al. (in press) found that annual mean gamete output for three populations in the Marlborough Sounds varied from 0.068 to 0.108 g y-i with no direct relationship between output and length of spawning period.
252 7.4. Size at sexual maturity The size at which E. chloroticus becomes sexually mature differs between populations, being 35 to 45 mm diameter at Kaiteriteri, and 55 to75 mm at Kaikoura (Dix 1970c). In Dusky Sound E. chloroticus reached sexual maturity at 50 to 60 mm diameter with little difference between populations (McShane et al. 1996). In the laboratory Barker et al. (1998) found that E. chloroticus as small as 30 mm diameter develop a gonad when fed prepared diets. Although the gonads were largely composed of nutritive phagocytes, they also contained either oocytes or spermatocytes confirming precocious development. This suggests that sexual maturity may be determined by nutritive input and not size. 7.5. Spawning Lamare and Stewart (1998) observed a mass in situ synchronous spawning of E. chloroticus in Doubtful Sound, on 27 January 1994. Spawning occurred between 17:30 hrs and 18:30 hrs, 20 minutes before low tide and coincided with a full moon, spring tide and the commencement of a period of rapidly cooling sea temperatures. More than 90% of both males and females formed a dense spawning aggregation with gametes clouding the water, a number of which were eaten by small labrid fish species. The spawning, which the authors suggest may have occurred over the whole fiord, was followed by a 42 to 50% decrease in gonad indices. Such synchronous spawning may be quite unusual and perhaps reflects the unique hydrological conditions within a fiord. Open coast populations probably show less synchrony. Even though gametogenesis may be synchronous, spawning is usually not as it is probably induced by very local cues. 8. LARVAL DEVELOPMENT Early development was first described by Mortensen (1921) who was able to rear larvae through to the pluteus stage only. Dix (1969) and Walker (1984) succeeded in rearing larvae through to metamorphosis in a minimum time of approximately 30 days. Both authors provided a cursory description of larval development and metamorphosis. The most rapid larval development in culture was obtained by Lamare and Barker (1999) in which larvae reached competency at 22 days post-fertilization. These laboratory observations provide information on the developmental timetable to each stage, however caution should be exercised in extrapolating them to the field. The only comprehensive field investigation of larval ecology ofE. chloroticus is provided by Lamare (1998). He followed the transport and development of larvae in Doubtful Sound following the mass spawning of E. chloroticus during the summer of 1993/94 and also 1994/95 when no mass spawning was observed. Larval densities were approximately ten times higher in 1993/94 than in 1994/95 reflecting the marked annual differences in reproductive output. Larval distribution in the water column suggests a high level of larval retention within the fiord, presumably by entrainment of larvae within the estuarine circulation (Lamare 1998). Larvae completed development between 4 and 6 weeks within Doubtful Sound, a longer period than predicted by Dix (1969) and Walker (1984). This suggests that development in the plankton was slower than potentially possible. Food limitation of larvae was examined from the comparison of larval morphometrics, the larvae sampled exhibiting a food-limited morphology (Fenaux et al. 1994). These results strongly suggest that recruitment of E. chloroticus in Doubtful Sound is by larvae that have originated, been retained, and completed development within the fiord. Lamare and Barker (1999) followed the cohort of larvae resulting from the mass
253 spawning of adults until no larvae were present in the plankton. Instantaneous mortality rates for the larvae were calculated using 3 different mathematical models. Instantaneous mortality rate (M) was found to be constant and estimated at 0.164, 0.173, and 0.085 d 1 for the 3 models, the most accurate estimate of mortality probably being M = 0.16 d-1. Larvae reach competency in Doubtful Sound between 18 and 31 d, which is 1.05- to 1.82-fold slower than maximum growth rates recorded in laboratory cultures and further evidence of food limitation in the plankton. The mortality estimates determined by Lamare and Barker (1999) are very similar to those of Rumrill (1987), 0.162 d~ for larvae of Strongylocentrotus droebachiensis.
9. RECRUITMENT Dix (1972) noted populations of E. chloroticus were often made up of single cohorts and suggested that settlement is irregular from year to year. Walker (1984) examined scrapings from rock and associated algae collected subtidally from Goat island Bay, North Auckland and found a very small number of recently settled (1.3 mm diameter) juveniles in substrata containing the turf coralline species Corallina officinalis. Andrew and Choat (1985) surveyed numbers of juveniles (21 to 30 mm) in 3 habitats in northeastern New Zealand and found that numbers were high, though variable, in coralline fiat habitats (areas devoid of large brown algae) but low in forests of E. radiata and deep reef habitats. Juveniles transplanted into deep reef habitats suffered a high mortality rate with 70% being dead after 18 weeks. Mortality was only 3% for coralline fiat habitats and 37% in E. radiata forests. The presence of conspecific adults did not significantly influence survivorship of juveniles in any habitat. The causes of mortality were undetermined. They concluded that abundance of juvenile E. chloroticus is strongly linked to habitat, and argued that successful recruitment into canopy forming algal stands of E. radiata is unlikely. These conclusions are based on data generated by manipulations of small urchins, of a size which suggests that they are two or three years old. The abundance patterns are probably profoundly influenced by earlier post-settlement processes, and may be very different from patterns of recruitment. Barker (unpub. data) transplanted recently settled (0.37 mm diameter) juvenile E. chloroticus settled on Corallina encrusted pebbles in both caged and uncaged treatments into a shallow (12 m) site outside of and a deeper (16 m) site within an E. radiata kelp forest in Doubtful Sound. Survival varied but was significantly greater in the deeper kelp forest than the shallow site. Although survival was always greater in caged treatments, the difference between caged and uncaged treatments was not statistically significant. If the hypothesis of Andrew and Choat (1985) is correct, patterns of recruitment in Doubtful Sound are clearly different from those in northern New Zealand. In a detailed study on recruitment in E. chloroticus Lamare and Barker (unpub. obs.) found settlement and recruitment were highly correlated. Relatively high settlement in Doubtful Sound was followed by an increase in juveniles during the subsequent 9 months. Settlement during the following 2 years was comparatively poor and there was a decline in the density ofjuveniles. In Tory Channel settlement and recruitment were lower. In the laboratory the rate of settlement was close to 100% on coralline algae but was significantly less on artificial substrates. Survival of laboratory reared juveniles settled onto coralline encrusted rocks was high in the laboratory but much lower on rocks transplanted into Doubtful Sound. It appears that spatial and temporal
254 variation in recruitment in the Tory Channel is linked to breeding and spawning periodicity almost certainly accentuated by the relatively open coast situation. Predictable recruitment in Doubtful Sound is a consequence of the closed nature of the population. 10. POPULATION BIOLOGY 10.1. Growth
Little is known about growth in E. chloroticus. The earliest study was by Dix (1972) who estimated the age and annual growth of individuals collected at Kaikoura and at Kaitedteri ranging in diameter from 40 to 140 mm by the use of growth lines in apical plates and the growth of juveniles (18 mm diameter) in the laboratory. Walker (1981) also used annual lines in combination with external tags to investigate seasonal growth in sea urchins at Goat Island Bay, Leigh, in the north of New Zealand. Growth estimated from growth lines determined from etched genital plates is confounded by various problems (Gage 1991). Estimating growth by the injection of a fluorescent marker such as tetracycline hydrochloride or calcein into the body cavity is more successful (Ebert 1988). Lamare and Mladenov (2000) used this method in conjunction with measurements of growth of smaller individuals (<10 mm diameter) kept in the laboratory and data gathered from newly settled cohorts, to estimate growth ofE. chloroticus, from Espinosa Point, Doubtful Sound and the Tory Channel. Recently settled juveniles (0.37 mm diameter) grew to 8.05 mm in the laboratory and 10.5 mm in the field in one year. Growth was slow for the first 200 days after settlement and then increased. Growth of calcein-tagged adults was modelled using one non-asymptotic (Tanaka) and three asymptopic growth functions (Brody-Bertalanffy, Richards and Jolicoeur). All models predicted faster growth over the first 2 to 4 years in the Tory Channel population but a larger maximum size in Doubtful Sound. Lamare and Mladenov (2000) concluded that the Richards model best describes growth in E. chloroticus (Fig. 1) because it most accurately predicts the size at year 1 and a decrease in somatic growth at reproductive maturity (30 to 40 mm TD). 120 110 100
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Age (years) Figure 1. Predicted growth of Evechinus chloroticus (Richards model, after Lamare and Mladenov 2000).
255 Growth curves using other models do not meet these criteria. The Richards model predicts a decrease in somatic growth in the Tory Channel after an age of 1.76 years (22 mm TD) and 2.31 years (30 mm TD) in Doubtful Sound, with growth decreasing rapidly after ages 3 to 4 years (40 to 50mm TD). Not surprisingly the growth curves calculated by Dix (1972) show considerably faster growth for two of the three populations studied. While it is possible the suggested sizes at age are correct, it is likely Dix (1972) over-estimated the growth rate. McShane and Anderson (1997) also used calcein tagging to model growth in E. chloroticus from populations in Dusky Sound and from Arapawa Island in the Marlborough Sounds. They concluded that individuals in Dusky Sound reached a larger size than conspecifics elsewhere but provided no growth curve that would allow size at age comparisons with other populations. 10.2 Mortality 10.21 Rates of mortality Mortality is most accurately determined from tagging and recapture or from population sizefrequency analysis. Very few studies have calculated mortality for E. chloroticus. Lamare (1997) applied Ebert and Russell's (1973) model based on analysis of population size-structure to calculate instantaneous mortality (Z) in Doubtful Sound and Tory Channel populations. These analyses suggest mortality is higher in Doubtful Sound than Tory Channel. Annual mortality and mean longevity were calculated as 9.21% and 10.38 y in the Doubtful Sound populations and 5.01% and 19.44 y for Tory Channel. 10.22 Causes of mortality Mortality could result from predation (natural and human), disease, morbidity or from physical damage due to environmental perturbations. Lamare (1997) ascribed higher mortality in Doubtful Sound to a number of predators including benthic feeding fishes, asteroids, molluscs, and lobsters. The most conspicuous and probably the most important being the large asteroids, Coscinasterias muricata and Astrostole scabra, which were often observed feeding on E. chloroticus. In comparison, Tory Channel has lower densities of most of these predators, particularly benthic invertebrates. Periodic rapid intrusions of low salinity water could also contribute to mortality in Doubtful Sound, particularly for juveniles which commonly occur at shallower depths than adults. Some harvesting of E. chloroticus also occurs in Tory Channel, however harvesting is very low or absent in the Doubtful Sound and probably only accounts for a minor proportion of total mortality in this population (Lamare 1997). Andrew and Choat (1982) used exclusion cages to evaluate fish predation on juvenile E. chloroticus at a subtidal coralline fiat site where invertebrate predators occurred in low numbers. The abundance of juveniles within the cages increased significantly over the experimental period, presumably as a result of recruitment into the caged areas, indicating that fish are important predators on recently recruited juvenile E. chloroticus. On rocky reefs throughout New Zealand E. chloroticus and the rock lobster Jasus edwardsii have a loose association, although they are seldom seen in close proximity in southern New Zealand (pers. obs.). Andrew and MacDiarmid (1991) investigated the interaction between E. chloroticus and the rock lobster jr. edwardsii in the shallow subtidal zone of northern rocky reefs. During the day rock lobsters were cryptic, and spatially segregated on a small scale from the sea urchins which were generally
256 exposed. However both species were active during the night. Lobsters moved considerable distances and are likely to prey on sea urchins. Large lobsters in the laboratory ate all sizes of sea urchins. All sizes of lobster ate small sea urchins (<50 mm diameter) in preference to larger ones. Sea urchins are found in the guts of lobsters and broken tests are found in lobster dens (Andrew and McDiamid, 1991). Clearly lobsters prey on E. chloroticus. However as lobsters are rare in areas of barrens where E. chloroticus is most abundant, and sea urchins are absent from reefs deeper than 12 m where rock lobsters are abundant, Andrew and McDiamid (1991) doubt that rock lobsters regulate sea urchin numbers. If regulation does occur they believed it is mainly on sea urchins of 40-50 mm diameter when they become less cryptic and move from crevices into open rock habitat. Lamare (1997) observed a few individuals ofE. chloroticus with spine loss resembling "baldsea-urchin disease" (Maes et al. 1986) in both Doubtful Sound and the Tory Channel. During the summer of 1999/2000 diseased sea urchins in northern New Zealand were also reported to be dying of 'bald-sea-urchin disease'. The incidents of infection were widespread, from Cape Reinga, Mayor Island, Leigh and the Bay of Plenty. Deaths were higher in areas where sea urchins were present in higher densities (Babcock, pers. comm.).
10.3. Population genetics With a latitudinal distribution of over 1500 km on both east and west coasts of New Zealand, and with the established differences between populations, (size, recruitment, habitat preferences) it might be expected that populations of E. chloroticus vary genetically over their range. Mladenov et al. (1997) found few genetic differences at five polymorphic enzyme loci in six widely separated populations (Leigh in the north to Stewart Island in the south). Mladenov et al. (1997) suggested that long larval life ensures high gene flow between populations, despite hydrographic features of the coast (southward flowing East Cape Current and the Subtropical Convergence) that might be expected to impede larval transport. Individuals collected from Doubtful Sound showed slight evidence of genetic differentiation, possibly the result of larval retention within the fiord.
II. CONCLUSIONS Evechinus chloroticus is the most common, largest and most widely distributed New Zealand sea urchin, occurring on shallow rocky reefs from sheltered sites to those of moderate exposure. It has an important ecological role by grazing kelp, creating extensive deforested areas particularly in the north of New Zealand. In the absence of kelp, they also feed on sessile invertebrates such as sponges. Evechinus chloroticus breeds through the spring and summer. Planktotrophic larvae spend between 3 to 4 weeks in the plankton and are widely dispersed along open coasts ensuring high gene flow between populations. Based on studies in the Marlborough Sounds and Doubtful Sound, recruitment is temporally and spatially variable in open coast situations but more predictable in southern fiords with patterns of estuarine circulation. Evechinus chloroticus grows slowly reaching reproductive maturity at a test diameter of 40 to 50 mm at 3 to 4 years of age. Maximum size of 80 to 100ram is attained after 8 to 9 years in the Marlborough Sounds and Doubtful Sound. Based on data from these two populations, annual
257 mortality varies from 5 to 10% and mean longevity is between 10 and 20 years. Information on recruitment, growth and mortality from other regions is needed. Although E. chloroticus has been a traditional food of Maori people since before the arrival of Europeans the gonads have not yet been harvested extensively for export markets because of poor colour and taste. This has proved to be a significant problem in establishing a fishery for this species. ACKNOWLEDGMENT: I am grateful to Miles Lamare for critically reading a draft of this review. REFERENCES
Andrew, N. L. (1986) The interaction between diet and density in influencing reproductive output in the echinoid Evechinus chloroticus (Val.). J Exp Mar Biol Eco197:63-79 Andrew NL (1988) Ecological aspects of the common sea urchin, Evechinus chloroticus, in northern New Zealand: A review. N Z J Mar Freshwat Res 22:415-426 Andrew NL, Choat JH (1982) The influence of predation and conspecific adults on the abundance of juvenile Evechinus chloroticus (Echinoidea: Echinometridae). Oecologia 54" 80-87 Andrew NL, Choat JH (1985) Habitat related differences in the survivorship and growth of juvenile sea urchins. Mar Ecol Prog Ser 27:155-161 Andrew NL, MacDiarmid AB (1991) Interrelations between sea urchins and spiny lobsters in northeastern New Zealand. Mar Ecol Prog Ser 70:211-222 Andrew NL, Stocker LJ (1986) Dispersion and phagokinesis in the echinoid Evechinus chloroticus (Val.). J Exp Mar Biol Ecol 100:1-3 Ayling AL (1978) The relation of food availability and food preferences to the field diet of an echinoid Evechinus chloroticus (Valenciennes). J Exp Mar Biol Ecol 33:223-235 Ayling AM (1981) The role of biological disturbance in temperate subtidal encrusting communities. Ecology 62:830-847 Barker MF, Keogh JA, Lawrence JM, Lawrence AL (1998) Feeding rate, absorption efficiencies, growth, and enhancement of gonad production in the New Zealand sea urchin Evechinus chloroticus Valenciennes (Echinoidea: Echinometridae) fed prepared and natural diets. J of Shellfish Res 17:1583-1590 Brewin PE, Lamare MD, and JA Keogh, Mladenov PV (in press) Reproductive variability over a four year period in the sea urchin, Evechinus chloroticus (Echinoidea: Echinodermata) from differing habitats in New Zealand. Mar Biol Choat JH, Andrew NL (1986) Interactions amongst species in a guild of subtidal benthic herbivores. Oecologia 68" 387-394 Choat JH, Schiel DR (1982) Patterns of distribution and abundance of large brown algae and invertebrate herbivores in subtidal regions of northern New Zealand. J Exp Mar Biol Eco160: 129-162 Cole RG, Haggitt T, Babcock RC (in press) Dietary preferences of Evechinus chloroticus. In Barker MF (ed) Proceedings 10th Intemational Echinoderm Conference, Balkema, Rotterdam Cook S (in press) In: Cook S (ed.) New Zealand Coastal Invertebrates. Echinoids. Canterbury University Press, Christchurch
258 Dix TG (1969) Larval life span of the echinoid Evechinus chloroticus (Val.). N Z J Mar Freshwat Res 3:13-16 Dix TG (1970a) Biology of Evechinus chloroticus (Echinodermata:Echinometridae) from different localities. 1. General. N Z J Mar Freshwat Res 4:91-116 Dix TG (1970b) Biology of Evechinus chloroticus (Echinodermata:Echinometridae) from different localities. 2. Movement. N Z J Mar Freshwat Res 4:267-277 Dix TG (1970c) Biology of Evechinus chloroticus (Echinodermata:Echinometridae) from different localities. 3. Reproduction. N Z J Mar Freshwat Res 4:385-405 Dix TG (1972) Biology of Evechinus chloroticus (Echinodermata:Echinometridae) from different localities. 4, Age, Growth and Size. N Z J Mar Freshwat Res 6" 48-68 Don GL (1975) The effects of grazing by Evechinus chloroticus (Val.) on populations of Ecklonia radiata (Ag.). M Sc thesis, University of Auckland Ebert TA (1988) Calibration of natural growth lines in ossicles of two sea urchins, Strongylocentrotus purpuratus and Echnometra mathaei, using tetracycline. In: Burke RD, Mladenov PD, Lambert P, Parsley RL (eds) Echinoderm biology, Balkema, Rotterdam, pp 435-443 Ebert TA, Russell MP (1993) Growth and mortality of subtidal red sea urchins (Strongylocentrotus franciscanus) at San Nicolas Island, California, USA: Problems with models. Mar Biol 117:79-89 Fenaux L, Strathmann MF, Strathmann RR (1994) Five tests of food-limited growth of larvae in coastal waters by comparisons of rates of development and form of echinoplutei. Limnol Oceanogr 39:84-98 Gage JD (1991) Skeletal growth zones as age-markers in the sea urchin Psammechinus miliaris. Mar Biol 110:217-228 Harrold C, Reed, D.C. (1985) Food availability, sea urchin grazing, and kelp forest community structure. Ecology 66:1160-1169 Hyman LH (1955) The Invertebrata. 4. Echinodermata. McGraw Hill, New York Lamare MD (1997) Population biology, pre-settlement processes and recruitment in the New Zealand sea urchin Evechinus chloroticus Valenciennes (Echinoidea: Echinometddae) PhD thesis, University of Otago, Dunedin Lamare MD (1998) Origin and transport of larvae of the sea urchin Evechinus chloroticus (Echinodermata: Echinoidea) in a New Zealand fiord. Mar Ecol Prog Ser 174:107-121 Lamare MD (2000) Modelling somatic growth in the sea urchin Evechinus chloroticus (Echinoidea:Echinometridae). J Exp Mar Biol Ecol 243:17-43 Lamare MD, Barker MF (1999) In situ estimates of larval development and mortality in the New Zealand sea urchin Evechinus chloroticus (Echinodermata: Echinoidea). Mar Ecol Prog Ser 180:197-211 Lamare MD, Mladenov PV (2000) Modelling somatic growth in the sea urchin Evechinus chloroticus (Echinoidea: Echinometridae). J Exp Mar Biol Eco1243" 17-43 Lamare MD, Stewart BG (1998) Mass spawning by the sea urchin Evechinus chloroticus (Echinodermata: Echinoidea) in a New Zealand fiord. Mar Biol 132:135-140 Maes P, Jangoux M, Fenaux L (1986) The "bald-sea-urchin" disease: Ultrastructure of the lesions and nature of their pigmentation. Ann Inst Oceanogr, Paris Nouv Ser 62" 37-45 McRae A (1959) Evechinus chloroticus (Val.), an endemic New Zealand echinoid. Trans Roy Soc N Z 86:205-267
259 McShane PE (1992) Sea urchins in Dusky Sound-Prospects for a major kina industry in New Zealand. N Z Professional Fisherman December 92:34-40 McShane PE, Anderson O, Gerring PK, Stewart RA, Naylor JR (1994) Fisheries biology ofkina (Evechinus chloroticus). MAF Fisheries, New Zealand Fisheries Assessment Research Document 94/17 McShane PE, Gerring PK, Owen AA, Stewart RA (1996) Population differences in the reproductive biology of Evechinus chloroticus (Echinoidea: Echinodermetridae). N Z J Mar and Freshwat Res 30:333-339 McShane PE, Anderson OF (1997) Resource allocation and growth rates in the sea urchin Evechinus chloroticus (Echinoidea: Echinometridae). Mar Biol 128:657-663 Miller ILl (1985) Seaweeds, sea urchins, and lobsters: A reappraisal. Can J Fish Aquat Sci 42: 2061-2072 Mladenov PV, Allibone RM, Wallis GP (1997) Genetic differentiation in the New Zealand sea urchin Evechinus chloroticus (Echinodermata: Echinoidea). N Z J Mar Freshwat Res 31: 261269 Mortensen T (1921) Studies on the development and larval forms of echinoderms. G.E.C Gad, Copenhagen Mortensen T (1922) Echinoderms of New Zealand and the Auckland Campbell Islands. I. Echinoidea. Vidensk Meddr dansk naturh Foren 73:139-198 Pawson DL (1961) Distribution patterns of New Zealand echinoderms. Tuatara 9:9-18 Pawson DL (1965) New records of echinoderms from the Snares Islands to the south of New Zealand. Trans Roy Soc N Z (Zool) 6:9-18 RumriU SS (1987) Differential predation upon embryos and larvae of temperate Pacific echinoderms. PhD thesis, University of Alberta, Edmonton Scheibling RE, Stephenson RL (1984) Mass mortality of Strongylocentrotus droebachiensis (Echinodermata: Echinoidea) offNova Scotia, Canada. Mar Biol 78:153-164 Scheibling RE, Raymond BG (1990) Community dynamics on a subtidal cobble bed following mass mortalities of sea urchins. Mar Ecol Prog Ser 63" 127-145 Schiel DR (1982) Selective feeding by the echinoid, Evechinus chloroticus, and the removal of plants from subtidal algal stands in northern New Zealand. Oecologia 54:379-388 Schiel DR, Kingsford MJ, Choat JH (1986) Depth distribution and abundance of benthic organisms and fishes at the subtropical Kermadec Islands. N Z J Mar Freshwater Res 20:521535 Schiel DR, Andrew NL, Foster MS (1995) The structure of subtidal algal and invertebrate assemblages at the Chatham Islands, New Zealand. Mar Biol 123:355-367 Steinberg PD, Altena IV (1992) Tolerance of marine invertebrate herbivores to brown algal phlorotannins in temperate Australasia. Ecol Monogr 62:189-222 Van Alstyne KL (1988) Herbivore grazing increases polyphenolic defenses in the intertidal brown alga Fucus distichus. Ecology 69:655-663 Walker MM (1981) Influence of season on growth of the sea urchin Evechinus chloroticus. N Z J Mar Freshwat Res 15:201-205 Walker MM (1982) Reproductive periodicity in Evechinus chloroticus in the Hauraki Gulf. N Z J Mar Freshwat Res 16:19-26 Walker MM (1984) Larval life span, larval settlement, and early growth of Evechinus chloroticus (Valenciennes). N Z J Mar Freshwat Res 18:393-397
260 Wing SR, Lamare MD, Vasques J (in press). Population structure of sea urchins (Evechinus chloroticus) along gradients in benthic productivity in the New Zealand fjords. In Barker MF (ed) Proceedings 10th International Echinoderm Conference, Balkema, Rotterdam
245
The e c o l o g y o f Evechinus chloroticus. M.F. Barker Department of Marine Science, University of Otago PO Box 56, Dunedin, New Zealand
1. INTRODUCTION
Evechinus chloroticus (Valenciennes), known locally as "kina," is a ubiquitous echinometrid endemic to New Zealand. It is one of the largest sea urchins known, with a maximum test diameter (TD) of 180-190 cm (pers. obs.). It was harvested by Maori people before the arrival of Europeans in New Zealand and more recently has been exploited in small quantities in restricted areas around New Zealand. The morphology and taxonomy are well described by (McRae 1959) and Mortensen (1922). Its morphology and distribution are also described by Cook, (in press). As the only shallow water sea urchin on hard bottoms around New Zealand, knowledge of its ecology is of great importance. The ecology of northern populations of E. chloroticus were reviewed by Andrew (1988).
2. GEOGRAPHIC DISTRIBUTION
Evechinus chloroticus is widely distributed around the main islands of New Zealand but is also found at the Chatham Islands to the west, the Snares Islands to the south (Pawson 1965) and from the Three Kings (Schiel et al. 1986) and Kermadec Islands to the north (Pawson, 1961, Cook, in press). This latter record has been questioned (Dix 1970a).
3. HABITAT
Evechinus chloroticus is generally found in water < 12 to 14 m deep although it has been collected from at least 60 m (Cook, in press). Intertidal populations also occur, mainly in the north of the North Island (Dix 1970a; McRae 1959). Dix (1970a) also noted intertidal populations at Kaiteriteri in Golden Bay at the north ofthe South Island. Although E. chloroticus is occasionally found on sandy or shingle areas (Dix, 1970a), this is not common and it is very seldom seen on fine sediments such as silt or mud (pers. obs.). Adults are normally found in areas with moderate currents and wave action, and are seldom found in areas of extreme exposure such as the surf shores that occur along much of New Zealand's west coast.
246 Evechinus chloroticus is found in somewhat different patterns of distribution and relationships with kelp and other invertebrates throughout New Zealand, and it is difficult to make broad generalisations about the habitat. In northern parts of New Zealand, E. chloroticus is most commonly found on shallow rocky reefs, dominated by encrusting coralline algae. In such areas they may be extremely abundant, with maximum densities of 40 m 2 reported by Choat and Schiel (1982) (Poor Knights Islands). When individuals are closely packed, density is strongly influenced by body size and density is less useful than biomass m. 2 Such coralline dominated reef flats are often interspersed with mature stands of laminarian algae. Within rocky reefs E. chloroticus is generally clumped, and there may be patches dominated by sea urchins which are almost devoid of kelp alongside areas where kelp is dense (Choat and Schiel 1982). The borders between such areas appear to be stable, and suggest a balance between echinoid grazing and algal colonization. In the Chatham Islands Schiel (1995),found E. chloroticus at almost every site sampled, at mean densities of 5 to15 m 2 but at maximum densities of 40 m 2 for large individuals. They tended to be abundant in sites where the deep water fucalean C.flexuosum was common. They were not seen in characteristically extensive deforested areas typical of northern N.Z. (Choat and Schiel 1982) and deforested patches larger than --25 m 2were never seen. Around the South Island E. chloroticus are less often seen on extensive rock fiats in open coast habitats, as they are in the north. More commonly they are in aggregations, either located between individual or small groups of kelp, or in barren areas of approximately 5 to 6 m diameter. On the Otago coast E. chloroticus is uncommon, although isolated aggregations of extremely large (120 to160 mm diameter) individuals do occur. The apparent rarity of E. chloroticus on this area of coast is anomalous, as the habitat would appear to be very suitable over much of the region and perhaps reflects very sporadic and low levels of recruitment. On the most southern coasts of the South Island E. chloroticus is more abundant and is very common in the sheltered inlets of Stewart Island. On the south western coast of Fiordland, E. chloroticus is abundant in the deep fiords which indent the coastline. In each fiord, steep cliffs covered with luxuriant rainforest overhang steep fiord walls that drop into deep water. This area of New Zealand is subjected to extremely high rainfall and many of the fiords have a surface low salinity layer (LSL) that may be up to 10 to 12 m in depth after several days of heavy rain in the local catchment. This fresh water layer is particularly deep in Doubtful Sound, because of additional discharge of freshwater from the tailrace of a hydro electric power station located on Lake Manapouri. In these fiords E. chloroticus is abundant, often in aggregations of up to 20 to 30 m 2 from immediately below the LSL, clinging to the steep rock faces sometimes on bare or coralline encrusted rock, sometimes on sunken trees which are often caught on ledges, or in shallower areas. Laminarians are only found towards the entrance ofthe fiord. In a survey of sea urchin abundance throughout Doubtful Sound, Wing et al. (unpub.) found mean densities varied from 5.22 at the entrance to 1.81 m 2 at Deep Cove the innermost site, with the highest density (5.98 m 2) at Espinosa Point (mid to outer reaches of the fiord). Juvenile E. chloroticus are cryptic throughout New Zealand. Dix (1970a) noted that individuals <10 mm TD are generally attached beneath both intertidal and subtidal rocks. Individuals between 10 to 40 mm TD occur in the intertidal and subtidal under rocks, or within small crevices or depressions in rocks and typically covered in debris. At around 40 mm TD individuals migrate into open habitats. The size structures of populations of Evechinus chloroticus vary over its geographic range. Populations typically have a unimodal size distribution dominated by larger individuals. Such
247 populations have been documented for the Otago coast (pers. obs.) Kaikoura and Kaiteriteri (Dix 1972), Tory Channel (Lamare and Barker, unpub.), and Dusky Sound (McShane 1992). The mean size of individuals in these populations ranges from 40 to 50 mm TD. (e.g. Kaiteriteri, Dix 1972), to 112 mm TD Dusky Sound (McShane et a1.1996). Populations with a bimodal or polymodal distribution are less common but have been described for Kaikoura (Dix 1972), Dusky Sound (McShane et al. 1994) and Doubtful Sound (Lamare and Barker unpub.). The size structure of populations of E. chloroticus can be distinctly different over relatively short distances. Along the Kaikoura Peninsula, for example, populations vary in mean body size and in the abundance of juveniles over distances of <5 km (Dix 1972).
4. ASSOCIATED SPECIES 4.1. Kelp In northern New Zealand Evechinus chloroticus is strongly associated with kelp forests often dominated by the laminarian Ecklonia radiata (Choat and Schiel 1982; Schiel 1982; Andrew and Stocker 1986) although in very shallow water they can be found in association with the fucaleans Carpophyllum mashalocarpum and C. angustifolium (Schiel 1982). In the Marlborough Sounds of the South Island they are mostly found with C. mashalocarpum and in areas subjected to high current flows Macrocystispyrifera (Dix 1970a; Brewin et al., in press). Further south on the Otago coast and at Stewart Island E. radiata only occurs as occasional isolated plants, and Macrocystis pyrifera is often the dominant kelp forest forming laminarian species (pers. obs.). In Dusky Sound in southern Fiordland (McShane et al. 1994) and further north at the entrance to Doubtful Sound (pers. obs.) E. chloroticus is found with E. radiata and Carpophyllumflexuosum. These are the most common laminarians though a number of red and green seaweeds are seasonally abundant. 4.2. Gastropods Evechinus chloroticus is often found in association with a variety of grazing gastropod species. Andrew and Choat (1982) reported a positive correlation between the abundance of E. cloroticus and the herbivorous gastropods Cellana stellifera (limpet), Trochus viridis (topshell) and Cookia sulcata (turbinid) at depths less than 12 m. Gastropod abundance was significantly lower in the absence of E. chloroticus. The effects of caging specific gastropods with E. chloroticus, supported the suggestion of a positive relationships between E. chloroticus and Cookia sulcata as the biomass (mean dry weight) ofE. chloroticus increased in the presence of the turbinid (Choat and Andrew 1986). Both Trochus viridis and Cookia sulcata occur in the South Island. Detailed relationships between E. chloroticus and other grazers have not been investigated. In some southern open coast situations E. chloroticus is often found in association with the abalone Haliotis iris especially in depths of 5 to 10 m. Wing (pers. comm.). He found that both E. chloroticus and H. iris in Paterson Inlet and Port Pegasus are found on shallow rocky reefs and the peak abundances overlap in depth. As they are rarely found together in the same quadrate (2 m 2) however, their distributions are negatively correlated at a relatively small scale.
248 5. FEEDING 5.1. Diet
(Dix 1970a) observed feeding ofE. chloroticus at both Kaikoura and Kaiteriteri. At least 11 species of algae were eaten at Kaikoura and only two at Kaiteriteri. Laboratory observations confirmed that E. chloroticus is chiefly herbivorous but eats a variety of food when algae are scarce. While E. chloroticus feeds on a wide variety of algal species, it shows preferences. Don (1975) examined this question in the laboratory and concluded that although E. chloroticus preferred E. radiata,, it grazed indiscriminately on all entrusting organisms when large brown algae were unavailable. The degree to which food choice experiments conducted in the laboratory can be extrapolated to the field is problematic. Such experiments should be conducted in natural conditions whenever possible. The study of Schiel (1982)highlights this. He presented the same seven species of algae to E. chloroticus in the laboratory and placed subtidally, on a rocky reef where E. chloroticus were relatively abundant (2.5 m 2) and randomly distributed. The amount of each alga grazed was different and the ranking of the algal species from the field experiment did not correlate with the rankings established by the laboratory choice experiment. It is clear that E. chloroticus exert a major influence on algal stands in the subtidal. Andrew and Choat (1982) used cages to exclude E. chloroticus from a 1000 sq m subtidal coralline fiat area in northern New Zealand. They found a large increase in biomass in a range of kelp species followed, especially E. radiata. The grazing activities of E. chloroticus also influence the structure of entrusting communities as well as algal stands. Ayling (1978) investigated the grazing ofE. chloroticus on encrusting communities dominated by sponges in both the field and in a laboratory study. In the field, they grazed sponge species according to abundance. In the laboratory, preferences for particular sponge species did not relate to the diet in the field. (Ayling 1981) suggest that E. chloroticus in benthic communities made up of encrusting organisms will readily graze all encrusting species except a few of the more massive sponges. Even these are grazed when food is in short supply. Although many encrusting animals produce chemical toxins or large quantities of mucus, Ayling (1978) found feeding preferences were not related to toxicity, although she did suggest that toxins of some species of sponges may influence feeding preferences. Algae contain phlorotannins (polyphenolic compounds that are the dominant secondary metabolites in temperate brown seaweeds) which are known to deter feeding by some invertebrate grazers (Van Alstyne 1988). Steinberg and Altena (1992) tested the tolerance of E. chloroticus to brown algal phlorotannins in six algal species, and found no correlation between feeding preferences and algal phenolic levels. Cole et al. (in press) found some evidence that high levels ofphlorotannins influenced grazing by E. chloroticus on certain species, particularly Carpophylummflexuosum which has two growth forms. The form which had high phlorotannin levels was not grazed by E. chloroticus in the field or in the laboratory. A more detailed investigation of the relationship of diet preferences and metabolites that deter grazers is required. Aside from the early studies by (Dix 1970a) at Kaikoura and Kaiteriteri, all the studies mentioned so far are for northern populations of E. chloroticus. Wing et al. (unpub.) found E. chloroticus near the entrances of southern fiords had a larger percentage of algae in the gut, smaller Aristotle's lantern indices and higher calorific gut content compared to populations in the inner fiords. They suggested this is evidence of nutritional limitations in inner fiord sites. The entrance and outer fiords are characterized by assemblages of laminarian kelps dominated by Ecklonia radiata, while the inner fiords with steeper rock walls only support filamentous
249 chlorophytes and small amounts of rhodophytes. Here E. chloroticus are often found grazing sunken logs (pers. obs.). Evechinus chloroticus caged at low densities and fed the more preferred alga E. radiata, had a higher reproductive output than individuals fed the less preferred species Carpophyllum sp. (Andrews 1986). This relationship broke down when individuals were caged at higher densities. Laboratory experiments using prepared artificial diets also showed that diet quality has a significant influence on reproductive output in E. chloroticus (Barker et al. 1998). A great deal more information is required from field studies before we will understand the relationship between food selection and other metabolic requirements, i.e. whether sea urchins selectively graze on algae or other organisms in order to maximize reproductive output or enhance other physiological processes. 5.2. Feeding rate Barker et al. (1998) found E. chloroticus in the laboratory ate significantly more prepared feeds than the algae Macrocystis pyrifera and Ulva lactuca. For all diets feeding rate showed a clear seasonal trend directly correlated with water temperature. Of the two algal diets, M. pyrifera was clearly preferred over U. lactuca for individuals 30 to 90 mm diameter. Schiel (1982) fed E. chloroticus, of a similar size to medium-sized individuals used by Barker et al. (60mm TD), a range of algal species in the laboratory. Although both the range of algal species and the experimental design was slightly different, the mean daily feeding rate per individual calculated from Schiel's 1982 data is 0.69 g day1 for the most preferred alga (Cystophora torulosa) compared to 0.88 for E. chloroticus feeding on M. pyrifera. This suggests that feeding rates for sea urchins may be similar, even though they are collected from widely different latitudinal locations.
6. MOVEMENT Movement in E. chloroticus, especially in relationship to levels and quality of food, is poorly understood. Dix (1970b) investigated movement of tagged individuals in aggregated populations at Kaikoura and at Kaiteriteri. At Kaikoura he found only small numbers (6% at 3 months, 10% at 6 months) had moved a maximum distance of 4.8 m. At Kaiteriteri, a site where brown algae are less abundant, movement was slightly greater. Tagged individuals had lower gonad indices, and less food in the gut than untagged ones which suggests that tagging affects feeding and is likely to influence movement. Dix (1970b) found that E. chloroticus in the laboratory moved more at night than during the day. Andrew and Stocker (1986) examined the movement of E. chloroticus in relationship to the availability ofE. radiata at two subtidal sites in northern New Zealand. Their results confirm Dix' s suggestion that movement is related to the availability of food. In the presence of drift algae, individuals increased their overnight movements. This suggests a chemosensory response to the presence of damaged kelp, although they did not appear to respond in a directional manner. Increased movement stimulated by an increase in the abundance of drift algae as has been reported for Strongylocentrotus species (e.g. Harrold and Reed 1985), has not been demonstrated in E. chloroticus and active feeding fronts of sea urchins have yet to be documented. Movement may also be affected by the presence of predators. Andrew and McDiamid (1991) report that E. chloroticus move less in habitats in which the rock lobster Jasus edwardsii (a
250 predator) are abundant than in areas where lobsters are scarse. There is a need for more studies on movement and behaviour in relation to food, especially in southern populations in fiordland. Here the fluctuating levels of the low salinity layer causes vertical migration of populations (pers. obs.) as individuals maintain their distribution within high salinitiy strata of the halocline, a physical requirement which must impact markedly on both the type and quantity of available food. Large starfish, Coscinasterias muricata and Astrostole scabra, are also abundant in this zone and their presence may also influence sea urchin behaviour.
7. REPRODUCTION Evechinus chloroticus is gonochoric, with a 1:1 sex ratio and an annual breeding cycle (Dix 1970c). The reproductive output varies with diet quality (Barker et al. 1998) and population density (Andrew 1986).
7.1. Gametogenesis The gametogenic cycle has been described in detail by (Dix 1970b; Walker 1982; Brewin et al., in press). The developmental sequence of gametogenic stages differs little in these studies and the following description can be regarded as applying to all populations: Spawning occurs during the austral summer, generally being complete by March in most populations. A build up of nutrient reserves in the form of nutritive phagocytes occurs during autumn and early winter (March-May), followed by gametogenesis during mid-late winter and into spring (June to October). Gonads are ripe during spring (October and November) although some individuals collected from the field can be spawned in the laboratory from October to March (pers. obs.).
7.2. Reproductive cycle The annual reproductive cycle has been described in detail by the calculation of monthly gonad size indices for populations from the north of New Zealand (Hauraki Gulf, Walker 1982), central regions (Wellington and Northern South Island (Dix 1970c; McShane et al. 1996); Brewin et al. (in press) and for the south west of the South Island, Dusky Sound, (McShane et al. 1996; Doubtful Sound, Lamare 1998; Lamare and Barker, unpub.) (Table 1). Male and female reproductive cycles are generally synchronous in most populations. Surprisingly, considering the wide latitudinal range covered by these studies (36 ~to 45 ~ and the marked differences in seasonal temperatures (13 to 22 ~ in the north, 8 to15 ~ in the south), there is no clear latitudinal trend in the breeding season. Gamete release occurs from November to February in most populations, the broadest season (October to May) when ripe individuals can be found being at Ranson Head, near the entrance to Doubtful Sound (Table 1). Different methods have been used to calculate gonad indices, making comparison among all populations difficult. However the maximum index is approximately 25 to 28 in populations in both the Marlborough Sounds and Doubtful Sound respectively (Table 1). There are marked differences in reproductive seasonality between populations that are often only a few km apart. Walker (1982) found significant differences in gonad volume in the Hauraki Gulf (three populations, 10 km apart) during most of the year but most pronounced during summer. Similarly Brewin et al. (in press) found temporal and spatial differences over less than 10 km in three populations in the Marlborough Sounds. In these populations there were also differences on both rates of
251 gametogenesis and recovery of individuals and gametogenic differences between sexes in these populations. Table 1. Spawning period and maximum gonad index (GI) of E. c h l o r o t i c u s arranged latitudinally from the north to south of New Zealand. Region Sampling site Year Spawning Max GI GI Author period formula 1 Walker (1982) Hauraki Gulf Noises Island 1975-76 Nov.-Jan. N/A 1975-76 Nov.-Jan. N/A 1 Walker (1982) Hauraki Gulf Rangitoto Island 1 Walker (1982) Hauraki Gulf Crusoe Island 1975-76 Jan.-Feb. N/A 2 McShane et al. 1993-94 Dec.-Feb. -- 20 Wellington Reef Bay (1996) 3 Brewin et al. 19.3 - 22.95 Marlborough PeranoHeads 1990-92 Nov.-Jan. (in press ) Sounds 3 Brewin et al. Marlborough Titi Bay 1990-92 Nov-Feb. 15.8 - 26.99 (in press) Sounds 3 Brewin et al. Marlborough Dieffenbach 1990-92 Jan.-Mar. 11.87- 20.9 (in press) Sounds Point 4 Dix (1970c) Golden Bay Kaiteriteri 1968-69 Dec. to Apr. N/A 4 Dix (1970c) Jan. to Feb. N/A Kaikoura 1968-69 3 Lamare & Barker. Doubtful Causet Cove 1993-94 Dec-Feb. 20.0 - 19.2 (unpub.) Sound (DS) 3 Knapp (pers. tom) DS Causet Cove 1999-00 Nov.- May 15 - 16 DS Espinosa Point 1993-94 3 Lamare & Barker Nov.- Apr. 18.3 - 25.5 (unpub.) DS Deep Cove 1993-94 Nov.-Jan. 14-24 3 Lamare & Barker (unpub.) DS Seymore Island 1999-00 3 Knapp (pers. com) Sept.-Jan. 28-29 DS Ranson Head 1999-00 Oct.-May 19-21 3 Knapp (pers. corn) DuskySound Anchorlsland 1992-93 Dec.-Feb. ~-8 -15 2 McShane et al. (1996) 1. Gonad volume/test diameter 2. Gonad volume/drained wet weight.x 100 3. Gonad wet weight/drained wet weight.x 100 4. Gonad volume/test volume x 10
7.3. Reproductive output Reproductive output (difference in pre and post-spawning gonad index) is a useful measure of actual gamete production. Brewin et al. (in press) found that annual mean gamete output for three populations in the Marlborough Sounds varied from 0.068 to 0.108 g y-i with no direct relationship between output and length of spawning period.
252 7.4. Size at sexual maturity The size at which E. chloroticus becomes sexually mature differs between populations, being 35 to 45 mm diameter at Kaiteriteri, and 55 to75 mm at Kaikoura (Dix 1970c). In Dusky Sound E. chloroticus reached sexual maturity at 50 to 60 mm diameter with little difference between populations (McShane et al. 1996). In the laboratory Barker et al. (1998) found that E. chloroticus as small as 30 mm diameter develop a gonad when fed prepared diets. Although the gonads were largely composed of nutritive phagocytes, they also contained either oocytes or spermatocytes confirming precocious development. This suggests that sexual maturity may be determined by nutritive input and not size. 7.5. Spawning Lamare and Stewart (1998) observed a mass in situ synchronous spawning of E. chloroticus in Doubtful Sound, on 27 January 1994. Spawning occurred between 17:30 hrs and 18:30 hrs, 20 minutes before low tide and coincided with a full moon, spring tide and the commencement of a period of rapidly cooling sea temperatures. More than 90% of both males and females formed a dense spawning aggregation with gametes clouding the water, a number of which were eaten by small labrid fish species. The spawning, which the authors suggest may have occurred over the whole fiord, was followed by a 42 to 50% decrease in gonad indices. Such synchronous spawning may be quite unusual and perhaps reflects the unique hydrological conditions within a fiord. Open coast populations probably show less synchrony. Even though gametogenesis may be synchronous, spawning is usually not as it is probably induced by very local cues. 8. LARVAL DEVELOPMENT Early development was first described by Mortensen (1921) who was able to rear larvae through to the pluteus stage only. Dix (1969) and Walker (1984) succeeded in rearing larvae through to metamorphosis in a minimum time of approximately 30 days. Both authors provided a cursory description of larval development and metamorphosis. The most rapid larval development in culture was obtained by Lamare and Barker (1999) in which larvae reached competency at 22 days post-fertilization. These laboratory observations provide information on the developmental timetable to each stage, however caution should be exercised in extrapolating them to the field. The only comprehensive field investigation of larval ecology ofE. chloroticus is provided by Lamare (1998). He followed the transport and development of larvae in Doubtful Sound following the mass spawning of E. chloroticus during the summer of 1993/94 and also 1994/95 when no mass spawning was observed. Larval densities were approximately ten times higher in 1993/94 than in 1994/95 reflecting the marked annual differences in reproductive output. Larval distribution in the water column suggests a high level of larval retention within the fiord, presumably by entrainment of larvae within the estuarine circulation (Lamare 1998). Larvae completed development between 4 and 6 weeks within Doubtful Sound, a longer period than predicted by Dix (1969) and Walker (1984). This suggests that development in the plankton was slower than potentially possible. Food limitation of larvae was examined from the comparison of larval morphometrics, the larvae sampled exhibiting a food-limited morphology (Fenaux et al. 1994). These results strongly suggest that recruitment of E. chloroticus in Doubtful Sound is by larvae that have originated, been retained, and completed development within the fiord. Lamare and Barker (1999) followed the cohort of larvae resulting from the mass
253 spawning of adults until no larvae were present in the plankton. Instantaneous mortality rates for the larvae were calculated using 3 different mathematical models. Instantaneous mortality rate (M) was found to be constant and estimated at 0.164, 0.173, and 0.085 d 1 for the 3 models, the most accurate estimate of mortality probably being M = 0.16 d-1. Larvae reach competency in Doubtful Sound between 18 and 31 d, which is 1.05- to 1.82-fold slower than maximum growth rates recorded in laboratory cultures and further evidence of food limitation in the plankton. The mortality estimates determined by Lamare and Barker (1999) are very similar to those of Rumrill (1987), 0.162 d~ for larvae of Strongylocentrotus droebachiensis.
9. RECRUITMENT Dix (1972) noted populations of E. chloroticus were often made up of single cohorts and suggested that settlement is irregular from year to year. Walker (1984) examined scrapings from rock and associated algae collected subtidally from Goat island Bay, North Auckland and found a very small number of recently settled (1.3 mm diameter) juveniles in substrata containing the turf coralline species Corallina officinalis. Andrew and Choat (1985) surveyed numbers of juveniles (21 to 30 mm) in 3 habitats in northeastern New Zealand and found that numbers were high, though variable, in coralline fiat habitats (areas devoid of large brown algae) but low in forests of E. radiata and deep reef habitats. Juveniles transplanted into deep reef habitats suffered a high mortality rate with 70% being dead after 18 weeks. Mortality was only 3% for coralline fiat habitats and 37% in E. radiata forests. The presence of conspecific adults did not significantly influence survivorship of juveniles in any habitat. The causes of mortality were undetermined. They concluded that abundance of juvenile E. chloroticus is strongly linked to habitat, and argued that successful recruitment into canopy forming algal stands of E. radiata is unlikely. These conclusions are based on data generated by manipulations of small urchins, of a size which suggests that they are two or three years old. The abundance patterns are probably profoundly influenced by earlier post-settlement processes, and may be very different from patterns of recruitment. Barker (unpub. data) transplanted recently settled (0.37 mm diameter) juvenile E. chloroticus settled on Corallina encrusted pebbles in both caged and uncaged treatments into a shallow (12 m) site outside of and a deeper (16 m) site within an E. radiata kelp forest in Doubtful Sound. Survival varied but was significantly greater in the deeper kelp forest than the shallow site. Although survival was always greater in caged treatments, the difference between caged and uncaged treatments was not statistically significant. If the hypothesis of Andrew and Choat (1985) is correct, patterns of recruitment in Doubtful Sound are clearly different from those in northern New Zealand. In a detailed study on recruitment in E. chloroticus Lamare and Barker (unpub. obs.) found settlement and recruitment were highly correlated. Relatively high settlement in Doubtful Sound was followed by an increase in juveniles during the subsequent 9 months. Settlement during the following 2 years was comparatively poor and there was a decline in the density ofjuveniles. In Tory Channel settlement and recruitment were lower. In the laboratory the rate of settlement was close to 100% on coralline algae but was significantly less on artificial substrates. Survival of laboratory reared juveniles settled onto coralline encrusted rocks was high in the laboratory but much lower on rocks transplanted into Doubtful Sound. It appears that spatial and temporal
254 variation in recruitment in the Tory Channel is linked to breeding and spawning periodicity almost certainly accentuated by the relatively open coast situation. Predictable recruitment in Doubtful Sound is a consequence of the closed nature of the population. 10. POPULATION BIOLOGY 10.1. Growth
Little is known about growth in E. chloroticus. The earliest study was by Dix (1972) who estimated the age and annual growth of individuals collected at Kaikoura and at Kaitedteri ranging in diameter from 40 to 140 mm by the use of growth lines in apical plates and the growth of juveniles (18 mm diameter) in the laboratory. Walker (1981) also used annual lines in combination with external tags to investigate seasonal growth in sea urchins at Goat Island Bay, Leigh, in the north of New Zealand. Growth estimated from growth lines determined from etched genital plates is confounded by various problems (Gage 1991). Estimating growth by the injection of a fluorescent marker such as tetracycline hydrochloride or calcein into the body cavity is more successful (Ebert 1988). Lamare and Mladenov (2000) used this method in conjunction with measurements of growth of smaller individuals (<10 mm diameter) kept in the laboratory and data gathered from newly settled cohorts, to estimate growth ofE. chloroticus, from Espinosa Point, Doubtful Sound and the Tory Channel. Recently settled juveniles (0.37 mm diameter) grew to 8.05 mm in the laboratory and 10.5 mm in the field in one year. Growth was slow for the first 200 days after settlement and then increased. Growth of calcein-tagged adults was modelled using one non-asymptotic (Tanaka) and three asymptopic growth functions (Brody-Bertalanffy, Richards and Jolicoeur). All models predicted faster growth over the first 2 to 4 years in the Tory Channel population but a larger maximum size in Doubtful Sound. Lamare and Mladenov (2000) concluded that the Richards model best describes growth in E. chloroticus (Fig. 1) because it most accurately predicts the size at year 1 and a decrease in somatic growth at reproductive maturity (30 to 40 mm TD). 120 110 100
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Age (years) Figure 1. Predicted growth of Evechinus chloroticus (Richards model, after Lamare and Mladenov 2000).
255 Growth curves using other models do not meet these criteria. The Richards model predicts a decrease in somatic growth in the Tory Channel after an age of 1.76 years (22 mm TD) and 2.31 years (30 mm TD) in Doubtful Sound, with growth decreasing rapidly after ages 3 to 4 years (40 to 50mm TD). Not surprisingly the growth curves calculated by Dix (1972) show considerably faster growth for two of the three populations studied. While it is possible the suggested sizes at age are correct, it is likely Dix (1972) over-estimated the growth rate. McShane and Anderson (1997) also used calcein tagging to model growth in E. chloroticus from populations in Dusky Sound and from Arapawa Island in the Marlborough Sounds. They concluded that individuals in Dusky Sound reached a larger size than conspecifics elsewhere but provided no growth curve that would allow size at age comparisons with other populations. 10.2 Mortality 10.21 Rates of mortality Mortality is most accurately determined from tagging and recapture or from population sizefrequency analysis. Very few studies have calculated mortality for E. chloroticus. Lamare (1997) applied Ebert and Russell's (1973) model based on analysis of population size-structure to calculate instantaneous mortality (Z) in Doubtful Sound and Tory Channel populations. These analyses suggest mortality is higher in Doubtful Sound than Tory Channel. Annual mortality and mean longevity were calculated as 9.21% and 10.38 y in the Doubtful Sound populations and 5.01% and 19.44 y for Tory Channel. 10.22 Causes of mortality Mortality could result from predation (natural and human), disease, morbidity or from physical damage due to environmental perturbations. Lamare (1997) ascribed higher mortality in Doubtful Sound to a number of predators including benthic feeding fishes, asteroids, molluscs, and lobsters. The most conspicuous and probably the most important being the large asteroids, Coscinasterias muricata and Astrostole scabra, which were often observed feeding on E. chloroticus. In comparison, Tory Channel has lower densities of most of these predators, particularly benthic invertebrates. Periodic rapid intrusions of low salinity water could also contribute to mortality in Doubtful Sound, particularly for juveniles which commonly occur at shallower depths than adults. Some harvesting of E. chloroticus also occurs in Tory Channel, however harvesting is very low or absent in the Doubtful Sound and probably only accounts for a minor proportion of total mortality in this population (Lamare 1997). Andrew and Choat (1982) used exclusion cages to evaluate fish predation on juvenile E. chloroticus at a subtidal coralline fiat site where invertebrate predators occurred in low numbers. The abundance of juveniles within the cages increased significantly over the experimental period, presumably as a result of recruitment into the caged areas, indicating that fish are important predators on recently recruited juvenile E. chloroticus. On rocky reefs throughout New Zealand E. chloroticus and the rock lobster Jasus edwardsii have a loose association, although they are seldom seen in close proximity in southern New Zealand (pers. obs.). Andrew and MacDiarmid (1991) investigated the interaction between E. chloroticus and the rock lobster jr. edwardsii in the shallow subtidal zone of northern rocky reefs. During the day rock lobsters were cryptic, and spatially segregated on a small scale from the sea urchins which were generally
256 exposed. However both species were active during the night. Lobsters moved considerable distances and are likely to prey on sea urchins. Large lobsters in the laboratory ate all sizes of sea urchins. All sizes of lobster ate small sea urchins (<50 mm diameter) in preference to larger ones. Sea urchins are found in the guts of lobsters and broken tests are found in lobster dens (Andrew and McDiamid, 1991). Clearly lobsters prey on E. chloroticus. However as lobsters are rare in areas of barrens where E. chloroticus is most abundant, and sea urchins are absent from reefs deeper than 12 m where rock lobsters are abundant, Andrew and McDiamid (1991) doubt that rock lobsters regulate sea urchin numbers. If regulation does occur they believed it is mainly on sea urchins of 40-50 mm diameter when they become less cryptic and move from crevices into open rock habitat. Lamare (1997) observed a few individuals ofE. chloroticus with spine loss resembling "baldsea-urchin disease" (Maes et al. 1986) in both Doubtful Sound and the Tory Channel. During the summer of 1999/2000 diseased sea urchins in northern New Zealand were also reported to be dying of 'bald-sea-urchin disease'. The incidents of infection were widespread, from Cape Reinga, Mayor Island, Leigh and the Bay of Plenty. Deaths were higher in areas where sea urchins were present in higher densities (Babcock, pers. comm.).
10.3. Population genetics With a latitudinal distribution of over 1500 km on both east and west coasts of New Zealand, and with the established differences between populations, (size, recruitment, habitat preferences) it might be expected that populations of E. chloroticus vary genetically over their range. Mladenov et al. (1997) found few genetic differences at five polymorphic enzyme loci in six widely separated populations (Leigh in the north to Stewart Island in the south). Mladenov et al. (1997) suggested that long larval life ensures high gene flow between populations, despite hydrographic features of the coast (southward flowing East Cape Current and the Subtropical Convergence) that might be expected to impede larval transport. Individuals collected from Doubtful Sound showed slight evidence of genetic differentiation, possibly the result of larval retention within the fiord.
II. CONCLUSIONS Evechinus chloroticus is the most common, largest and most widely distributed New Zealand sea urchin, occurring on shallow rocky reefs from sheltered sites to those of moderate exposure. It has an important ecological role by grazing kelp, creating extensive deforested areas particularly in the north of New Zealand. In the absence of kelp, they also feed on sessile invertebrates such as sponges. Evechinus chloroticus breeds through the spring and summer. Planktotrophic larvae spend between 3 to 4 weeks in the plankton and are widely dispersed along open coasts ensuring high gene flow between populations. Based on studies in the Marlborough Sounds and Doubtful Sound, recruitment is temporally and spatially variable in open coast situations but more predictable in southern fiords with patterns of estuarine circulation. Evechinus chloroticus grows slowly reaching reproductive maturity at a test diameter of 40 to 50 mm at 3 to 4 years of age. Maximum size of 80 to 100ram is attained after 8 to 9 years in the Marlborough Sounds and Doubtful Sound. Based on data from these two populations, annual
257 mortality varies from 5 to 10% and mean longevity is between 10 and 20 years. Information on recruitment, growth and mortality from other regions is needed. Although E. chloroticus has been a traditional food of Maori people since before the arrival of Europeans the gonads have not yet been harvested extensively for export markets because of poor colour and taste. This has proved to be a significant problem in establishing a fishery for this species. ACKNOWLEDGMENT: I am grateful to Miles Lamare for critically reading a draft of this review. REFERENCES
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260 Wing SR, Lamare MD, Vasques J (in press). Population structure of sea urchins (Evechinus chloroticus) along gradients in benthic productivity in the New Zealand fjords. In Barker MF (ed) Proceedings 10th International Echinoderm Conference, Balkema, Rotterdam