As Abalone Grow, They Change Their Habitat and Be- Haviour

S. Afr. J. mar. Sci. 22: 145Ð156 2000 145

EVIDENCE FOR A POSITIVE RELATIONSHIP BETWEEN JUVENILE ABALONE HALIOTIS MIDAE AND THE SEA URCHIN PARECHINUS ANGULOSUS IN THE SOUTH-WESTERN CAPE, SOUTH AFRICA

E. DAY* and G. M. BRANCH*

Previous field observations have suggested an association between the urchin Parechinus angulosus and juveniles of the abalone Haliotis midae. To test the generality and nature of this association, surveys were carried out at five sites between Cape Point and Danger Point in the kelp beds of the South-Western Cape, South Africa. These showed that both species occupy primarily hard substrata, showing preferences for encrusting coralline algae. They also confirmed a strong, positive relationship between urchins and juvenile abalone. Of the juvenile abalone sampled, more than 98% were found beneath sea urchins. All small (3Ð10 mm) and medium-sized (11Ð20 mm) juvenile abalone were under urchins, whether on flat or vertical reef, or in crevices. A small proportion (~10%) of larger juveniles (21Ð35 mm) was not found under urchins, and in these instances they occupied crevices instead. These findings are of particular importance in terms of their implications for the lucrative commercial abalone fishery in South Africa, indicating that urchins are of critical importance to the continued survival of viable abalone populations. There has been a dramatic decrease in natural populations of sea urchins over the past five years in the heart of the abalone fishing grounds, and the present findings suggest that this will lead to recruitment failure of abalone, because juvenile abalone seem dependent on the urchins. The long-term consequences for the industry may be crucial.

As abalone grow, they change their habitat and be- The specific behaviour patterns of juveniles when haviour (Shepherd and Turner 1985, Prince et al. they outgrow their association with corallines is largely 1988, Tutschulte and Connell 1988). In general, at the dependent on the type of habitat available to them end of the larval phase, competent larvae settle preferen- (Tegner and Levin 1982). This probably accounts for tially on encrusting coralline substrata (Morse et al. the diversity of biotic associations and habitats of juve- 1980, Saito 1981, Shepherd and Turner 1985), and both nile abalone, which differ among areas, species and the specificity of this relationship and the mechanisms communities. Research in several areas has high- involved have been the subject of numerous experi- lighted the fact that the availability of shelter beneath ments and debates (Morse et al. 1984, Johnson et al. boulders or in crevices is critical for the survival of post- 1991, Morse 1991). Once established on encrusting recruits of several abalone species (Haliotis laevigata corallines, they feed primarily on benthic diatoms and in southern Australia, Shepherd and Turner 1985; H. iris bacteria (Kawamura et al. 1995), and are also im- in New Zealand, McShane and Naylor 1995; H. cor- bued with a pink coloration from the coralline algae rugata and H. fulgens in southern California, Tutschulte themselves, rendering them relatively cryptic against and Connell 1988; H. walallensis in California, Lowry the pale corallines (Garland et al. 1985, McShane and Pearse 1973; and several haliotid species in New 1992). As they grow, however, their diet changes and South Wales, Australia, Andrew 1993). their shell markings darken, making them more visible The juveniles of some haliotid species, however, (Tegner and Butler 1989). Lacking both the protective shelter beneath adult sea urchins, rather than under thick shell of larger abalone and the advantages of rocks and boulders (Kojima 1981, Tegner and Dayton small size and cryptic coloration (Shepherd and Turner 1981, Tegner and Levin 1982, Tegner and Butler 1985), it is surmised that they must then rely on inacces- 1989, Tarr et al. 1996). Tegner and Butler (1989) be- sibility to predators (Sloan and Breen 1988, Tegner lieve that this behaviour is primarily a defence against and Butler 1989) and move to habitats offering more predators, but drift seaweed caught by sea urchins concealment (Tegner and Butler 1989, McCormick may also benefit the abalone (Tegner and Dayton et al. 1994). This transition marks the end of what is 1977). In South Africa, a positive relationship has defined here as the “recruit” stage and the beginning been reported between juveniles of the commercially of the “juvenile” stage, the latter covering individuals exploited abalone Haliotis midae and the sea urchin of 3Ð35 mm shell length. Parechinus angulosus (Tarr 1989, Wood 1993, Tarr

* Marine Biology Research Institute, Zoology Department, University of Cape Town, Rondebosch 7701, South Africa. E-mail [email protected] Manuscript received November 1999; accepted July 2000 146 South African Journal of Marine Science 22 2000

1 Millers Point SOUTH 2 Pyramid Rock AFRICA 3 Boordjiesrif CAPE TOWN 4 Buffels Bay 5 Betty’s Bay 6 Gans Bay

False Bay

1 34°15′ 2

3 4

ATLANCTIC 5 OCEAN Cape Hangklip

N 6

24 km

18°18′ 18°30′ E

Fig. 1: Map of the South-Western Cape, South Africa, showing the location of the study sites et al. 1996), with juvenile H. midae occurring pre- change with abalone size (McCormick et al. 1994), dominantly under the tests or spine canopies of adult size-based relationships between abalone and habitats sea urchins on shallow subtidal reefs (Tarr 1995). were examined, within the specified size range of Tarr et al. (1996) showed that juvenile abalone have “juveniles” (i.e. 3Ð35 mm shell length). virtually disappeared from areas where urchins are The investigations took the form of surveys, so they depleted. The reason for the decline in urchin numbers provide correlations from which causality at best can is uncertain, but purported increases in populations of only be inferred. Nevertheless, they provided a foun- rock lobster Jasus lalandii, which eat sea urchins, dation from which more detailed experimental work, have been mooted as the cause (Tarr et al. 1996). It is reported on elsewhere (Day 1998, Day and Branch in critical for the management of the fast-dwindling prep.), could then be based. abalone resource that the nature and significance of the association between urchins and juvenile abalone be elucidated. MATERIAL AND METHODS The primary aim of this paper was to test the generality of the evidence for a close positive relationship between juvenile abalone and sea urchins. As habitat Sites availability influences the behaviour and associations formed by juvenile abalone (Tegner and Levin 1982), Five sites were selected between Cape Point and the habitat preferences of both species were investi- Danger Point for initial surveys of the habitats and gated, in relation to habitat availability. Moreover, ecological associations of abalone juveniles: Millers because the preferences of abalone for different habitats Point, Boordjiesrif, Buffels Bay, Betty’s Bay and Gans 2000 Day & Branch: Juvenile Abalone and Sea Urchins 147

Bay (Fig. 1). A sixth site, at Pyramid Rock, was later numbers involved. A more useful comparison was sampled (Fig. 1). All sites lay within kelp beds (pri- derived, however, by calculating proportions of abalone marily Ecklonia maxima, with some Laminaria pallida), found under urchins against the proportion of area and either currently or previously supported populations occupied by urchins, to test whether juvenile abalone of sea urchins P. angulosus and abalone H. midae. are specifically associated with urchins. χ2 tests were performed to compare the numbers of abalone found under urchins in each quadrat (observed) with those Associations between juvenile abalone, urchins and predicted by the null hypothesis that abalone should substratum occur beneath urchins in proportion to the area occupied by urchins. An initial set of surveys between May and July 1995 The total area occupied by urchins was estimated was designed to determine the preferred habitat of using the formula: juvenile abalone and, specifically, to test the generality Area π r2 N of any relationship between juvenile abalone and sea = , urchins. where r is the mean radius of an urchin (including A preliminary dive at Betty’s Bay failed to detect spine canopy) and N is the total number of urchins either urchins or juvenile abalone. At each of the re- found. For a random sample of 60 urchins, r was 35 mm maining four sites, 38 randomly dropped 50 × 50 cm (range 20Ð45 mm). quadrat samples were read by divers on SCUBA. The patchy distribution of abalone juveniles meant Quadrats were restricted to reef areas dominated by that a square-root transformation of abalone densities rock, although where sand patches intruded into the (x«=√(x+0.5)) was necessary before two-way ANOVAs quadrats, they were included in the assessment. could be run on both abalone and urchin data. Tukey Surveys were carried out at depths of 1.0Ð2.5 m at a posteriori tests were used on any significantly dif- mean spring low water (MSLW), and were therefore ferent data. concentrated on the depth range in which the majority of juvenile H. midae are found (Newman 1968, Tarr 1989). Use of indices For each quadrat, the percentage cover of each substratum type was recorded, along with the numbers Gabriel’s (1978) index of selectivity (W) was used of urchins and the numbers and sizes of abalone ju- to determine the relationship between the availability veniles found on each particular substratum. Substrata of different substratum types and the proportional were broadly classified into nine categories, each relating abundance of animals on each. This assessed whether to a texturally or structurally different type of surface. urchins or juvenile abalone displayed any selectivity The categories were: (1) sponge, (2) sand, (3) foliar for particular substrata. In logarithmic form, the index algae, (4) polychaete mat (primarily Paronuphis antarc- (W) yields values that range between Ð∞ (negative se- tica), (5) bare rock, (6) the encrusting alga Hilden- lection) and +∞ (positive selection), with values of 0 brandia lecanellierii, (7) colonial ascidians, (8) pink indicating an absence of any selection. It is calculated encrusting corallines <1 mm thick (grouped as “thin” as follows: corallines) and (9) “thick corallines” (thickly layered W p q p q corallines >1 mm thick and consisting predominantly = 1 2/ 2 1 , of Heydrichia woelkerlingii). Within each substratum where p1 is the percentage of urchins or juvenile type, the numbers and sizes of abalone exposed, hidden abalone occupying a particular substratum; p2 is the under rocks or in crevices, or under urchins were noted. percentage of area covered by that particular substra- Percentage cover data were converted into actual tum; q1 = (100 Ð p1), and q2 = (100 Ð p2). areas of each substratum type, and urchin and abalone counts could thus be expressed in terms of densities per unit area of each substratum category. Habitat effects on the distribution of juvenile abalone of different sizes

Data analysis Following the initial surveys, in which “thin” and “thick” encrusting corallines were identified as being The number of abalone juveniles found in each preferred by juvenile abalone, more detailed surveys quadrat (y) was regressed against the number of urchins of these substrata were undertaken at Pyramid Rock, in that quadrat (x), using the square-root transformations Boordjiesrif, Buffels Bay and Millers Point (Fig. 1). y«=√ (y+0.5) and x«=√ (x+0.5), in view of the low This set of surveys examined the possibility that, 148 South African Journal of Marine Science 22 2000

Sand (a) (b)

Rock

Hildenbrandia

Sponge

Polychaete mat

Foliar algae

Thin coralline

Thick coralline 0.1 0.2 0.3 0.4 0.1 0.2 0.3 0.4 SUBSTRATUM AVAILABILITY (mÐ2)

Sand (c) (d)

Rock

Hildenbrandia

Sponge

Polychaete mat

Foliar algae

Thin coralline

Thick coralline 10 20 30 40 50 2 4 6 8 10 12 14 16 DENSITY OF URCHINS DENSITY OF ABALONE (numberámÐ2 substratum)

Fig. 2: Results of the broad-scale survey Ð (a) composition of substratum by area at the Betty’s Bay site, (b) composition of substratum by area at sites excluding Betty’s Bay, (c) density of urchins on different substrata, excluding Betty’s Bay, and (d) density of abalone on different substrata, excluding Betty’s Bay. Vertical bars link densities of urchins or abalone on different substrata that were not significantly different (Tukey test, p > 0.05). Error bars denote +1SE within the substrata preferred by abalone juveniles, under the rope was recorded (to the nearest 5 cm). there might be more specific preferences for particular Habitats included sand, shale, gravel, small rocks habitat types, related to the degree of shelter provided (with longest side <10 cm), flat rock, vertical rock, by each. First, the proportional availability of all habitat kelp holdfasts, crevices (which included sheltered types was assessed. At each site, a total of 12 × 8-m areas formed between adjoining rocks), “under rock” transects were swum along a weighted, demarcated area, sponge, Hildenbrandia patches and polychaete rope. The length of each habitat type falling directly mats. Because shelter was the primary variable being 2000 Day & Branch: Juvenile Abalone and Sea Urchins 149 investigated, the categories were subsequently simpli- was also overgrown by thick stands of foliar algae fied for analysis by retaining the categories flat rock, (Fig. 2a). Consequently, this site was excluded from vertical rock and crevices (including all under-rock the analysis of habitat preferences of urchins and juve- surfaces beneath movable boulders), but merging the nile abalone. other categories as “unsuitable habitat”, because they Figure 2bÐd summarizes the results obtained at did not support juvenile abalone. the remaining four sites in the initial broad-scale survey. At each site, stratified random sampling was applied The data have been pooled for clarity, because there to habitats, which were classified into three types, ac- were no significant differences between these sites cording to degree of exposure: crevice habitat (including (p > 0.05). In terms of substratum availability (Fig. 2b), accessible “under rock” habitat), flat (i.e. horizontal) thin corallines occupied a greater area than did any exposed rock surfaces and vertical exposed rock other substratum. Sand pockets comprised a fairly faces. Any boulder too large to roll was classified as a high proportion of reef area too, although they occurred flat or vertical rock surface. Quadrat size was reduced mainly on the reef periphery. Bare rock occupied a to 25 × 25 cm to allow more specific coverage of the surprisingly small area, with most available reef area restricted habitat types. In all, 30 quadrats were read being covered by encrusting coralline or foliar algae. for each habitat category, at each of the four sites. The Densities of urchins on different substrata suggested percentage area constituting each particular habitat a preference for coralline-covered hard substrata, with was recorded, as well as the size and number of juvenile all urchins occurring on them, except for a very small abalone found in that habitat and whether or not they number on sand patches (Fig. 2c). Densities of urchins were under urchins. Numbers of juvenile abalone were were high, averaging 45.5.m-2 on thin corallines and recorded in three size categories: small (3Ð10 mm), 23.m-2 on thick corallines. There were no significant medium (11Ð20 mm) and large (21Ð35 mm). differences between sites (df = 3, p > 0.05), but there were differences between different substrata (df = 8, p < 0.02). There were no significant interactions be- Data analysis tween sites and substrata (p > 0.05). Tukey a posteriori tests, run on data pooled between sites, showed that The availability of different habitat types at each site densities of urchins on thick and thin corallines was compared, using a two-way fixed-effects ANOVA, differed significantly from those on other substrata on arcsin-transformed data. Because urchins also and from each other (p < 0.05), with highest densities represented an important habitat type for abalone, on thin corallines. their densities in each of the habitats were compared by Densities of juvenile abalone on different substrata means of a two-way ANOVA, after square-root trans- followed a similar pattern to those of urchins, with the formation. Abalone densities in each habitat were highest densities being found on thin corallines, fol- similarly compared. lowed by thick corallines. Juvenile abalone were not Data were also expressed in terms of the frequencies found on any of the other substrata (Fig. 2d). Distri- of small, medium-sized and large juvenile abalone pre- butions were, however, extremely patchy. A two-way sent in each habitat, and standardized as the number ANOVA showed no significant differences in abalone per m2 of each habitat to allow for differences in the densities between sites (df = 3, p > 0.05), although amount of habitat available in any particular quadrat. differences among substrata did differ significantly Two-way ANOVAs were run on the data for each (df = 8, p < 0.01). There were no significant interactions size-class, to test for differences in the distribution of between sites and substrata (p > 0.05). Abalone densi- each size-class of juveniles among different habitats. ties on both thick and thin corallines were significantly different (p < 0.05) from each other, and from all other substrata. RESULTS Substratum selectivity Associations between abalone juveniles, urchins and substrata Figure 3 shows the proportions of urchins and abalone juveniles found on different substrata, plotted Both abalone juveniles and urchins were absent against the relative availability of each substratum, as from Betty’s Bay. Most of the reef there, with the ex- well as the selectivity indices for the two species. ception of small, well-grazed rings around adult Negative selectivity was shown by both urchins and abalone, had been colonized by a polychaete tube abalone for most substrata, with the exception of worm Paronuphis antarctica, whose tubes produce a thick and thin corallines, for which there was strong, dense mat of shale and sand. Most of the reef at this site positive selection. Whereas thin corallines occupied 150 South African Journal of Marine Science 22 2000

PROPORTION OF URCHINS ON SUBSTRATUM (a) 10 20 30 40 50 60 Sand Rock Substrate Urchins Hildenbrandia Sponge Polychaete tubing Thin coralline Thick coralline Foliar algae Ð∞ Ð4 Ð2 0 2 10 20 30 40 50 60 SELECTIVITY INDEX AVAILABLE SUBSTRATUM (%)

PROPORTION OF ABALONE JUVENILES ON SUBSTRATUM (b) 10 20 30 40 50 60 Sand Rock Substrate Abalone Hildenbrandia Sponge Polychaete tubing Thin coralline Thick coralline Foliar algae Ð∞ Ð4 Ð2 0 2 10 20 30 40 50 60 SELECTIVITY INDEX AVAILABLE SUBSTRATUM (%)

Fig. 3: Substratum selection by (a) urchins and (b) juvenile abalone. The left-hand graphs show the selectivity indices of urchins and juvenile abalone for each substratum. The right-hand graphs show the proportional distribution of urchins and juvenile abalone on different substrata, compared to the proportional availability of each substratum. Negative selectivity values indicate rejection or avoidance and positive ones show preferences for a particular substratum approximately 36% of the total available reef surface, cupied by urchins. A strong, positive relationship exists 66% of urchins and 61% of juvenile abalone occupied between urchins and juvenile abalone, virtually all juve- this substratum. Similarly, only 14% of the reef was nile abalone being found under urchins, even though occupied by thick corallines, but 33% of urchins and urchins occupied only 18Ð25% of the substratum 38% of abalone were found on them. area. This finding was consistent and significant at all sites (χ2 test: p < 0.001). Associations between juvenile abalone and urchins Distribution of abalone and urchins in different Most juvenile abalone were found under urchins. habitats Figure 4 illustrates the significant relationship between urchin and juvenile abalone densities at different sites There were no differences in urchin densities be- (r2 = 0.2878 for transformed data, n = 152, p < 0.05). tween sites (df = 3, p > 0.05) and no significant inter- Table I compares the proportion of abalone found actions between sites and substrata (p > 0.05). How- under urchins with the percentage of substratum oc- ever, urchin densities differed significantly between 2000 Day & Branch: Juvenile Abalone and Sea Urchins 151

to the total exposed habitat (vertical and flat rocks), 1 1 there was, however, significantly less sheltered than 10 exposed habitat (df = 1, p < 0.005). The crevice area, 1 2 which is the only one offering physical cover to urchins and abalone, was in fact a fairly small component of 8 n = 152 the whole reef environment, constituting <25%. 1 2 r 2 = 0.2878 2 2 6 p = <0.05 1 3 Effect of abalone size on habitat choice

1 1 1 2 4 When juvenile abalone were considered in terms of 1 1111 1 3 1 three size groups, there were also differences in the ABALONE/QUADRAT 1 1 1 1 3 1 1 1 1 types of habitat that they occupied. Figure 5b shows 2 the frequencies of small, medium-sized and large juve- 1 2234226 2 1 1 nile abalone in the three habitat-types, separating 3 9 5511 766 2 6 5 1 1 those that were under urchins from those that were 5 10 15 not. Small and medium-sized juveniles all occurred URCHINS/QUADRAT under urchins. A small proportion of large juveniles was not found under urchins, all occupying crevices. All juveniles were thus cryptic, only being found on Fig. 4: Relationships between juvenile abalone and urchin exposed flat or vertical surfaces if they were concealed densities. The number above each point indicates the number of samples with this value under urchins. In general, more large juveniles were found in the crevice habitat than in any other habitat. Two-way ANOVAs were run separately on the dis- habitats (df = 2, p < 0.05), being highest in crevices tributions of each of the three size-classes of juvenile (112.4 ± 46.4.m-2; Tukey test, p < 0.05), but similar abalone in flat, vertical and crevice habitats. Although on flat and vertical rock faces (75.88 ± 24.57.m-2 and some differences in densities between sites were evi- 75.7 ± 26.40.m-2 respectively, Tukey test, p > 0.05). dent, overall, only large animals were found in signifi- Similarly, densities of abalone juveniles (of all sizes) dif- cantly higher densities in crevices, as opposed to vertical fered significantly between habitats (df = 2, p < 0.01), or flat rock faces (df = 2, p < 0.001), whereas there higher densities being found in crevices than on flat were no significant differences in the distribution of or vertical rock faces (p < 0.05). Densities of juvenile small and medium-sized abalone between the three abalone at Pyramid Rock and Buffels Bay were sig- habitats. nificantly different from each other. Figure 5a shows the relative availability of crevices, flat and vertical rock faces, pooling data across sites DISCUSSION because there were no significant differences between them (df = 3, p > 0.05). Availability of these three habitat types, however, differ significantly (df = 2, Associations between juvenile abalone, urchins and p < 0.05), flat rock being the most abundant habitat substrata (Tukey test, p < 0.05), and crevice and vertical rock habitat being equally abundant (p > 0.05). If the avail- The importance of encrusting corallines as a sub- ability of sheltered habitat (i.e. crevices) is compared stratum for both the urchin P. angulosus and juvenile

Table I: Results of χ2 tests run on the number of abalone juveniles found under urchins versus the expected number, based on the proportion of the area of each quadrat occupied by urchins

Percentage of juvenile abalone under Number of Percentage cover of urchins p Site quadrats substratum by urchins (±SE) Predicted Actual (±SE) Boordjiesrif 15 23.47 (3.86) 23.47 100.00 (0) < 0.001 Buffels Bay 24 20.95 (2.02) 20.95 000n99.17 (0.83) < 0.001 Millers Point 20 22.47 (2.55) 22.47 100.00 (0) < 0.002 Gans Bay 07 23.79 (2.98) 23.79 100.00 (0) < 0.001 152 South African Journal of Marine Science 22 2000

(a)

20 HABITAT (%)

AVAILABILITY OF 10

Crevices Flat rock Vertical rock HABITAT TYPE

(b)

10 Under urchins Not under urchins 8 Small (3-10 mm) 6 Medium (11-20 mm) Large (21-35 mm) OF HABITAT

2 4 M 2 NUMBER OF ABALONE PER NUMBER OF Crevices Flat rock Vertical rock Crevices Flat Vertical rock rock HABITAT TYPE

Fig. 5: Variations in size frequencies of juvenile abalone with different habitats Ð (a) proportional availability of hard-reef habitats occupied by juvenile abalone, out of total reef habitat (“unsuitable habitat” not shown here), and (b) numbers of abalone in each size-class in each habitat type. The numbers of abalone from each size-class that were not found under urchins in each habitat are shown. Error bars denote +1SE

H. midae is clearly evident from the results (Figs 2, 3). the two possibilities. In many parts of the world, urchins have been attributed The absence of both abalone juveniles and urchins the role of maintaining coralline cover, often linked to from virtually all non-coralline substrata sampled was their ability to overgraze kelp forests or foliar algae not surprising, owing to the unsuitability of such sub- (reviewed by Lawrence 1975, Harrold and Pearse 1987). strata for grazing and occupation. Shepherd (1973) This role has, however, been debated (Contreras and observed extremely low densities of urchins on alcyo- Castilla 1987), particularly where urchins are reputed naria-covered reef, and none at all on sponges, whereas to trap drift seaweeds rather than actively graze on Fricke (1979) found that hard substrata were of prime the substratum. Nevertheless, urchins frequently do importance in explaining densities of P. angulosus in play a role in defining their habitat structure (Fletcher False Bay. However, it is noteworthy that the densities 1987, Andrew and Underwood 1992, Hagen 1995). In reported by Fricke (1979) are considerably higher (up the present case, whereas the occurrence of urchins to 72.m-2) than those found in the present survey. on encrusting corallines might reflect habitat prefer- Tegner and Butler (1989) noted that juvenile abalone ence, it could also be explained by habitat creation, if do not attach well to silty surfaces and are therefore the urchins themselves are responsible for maintaining found only on clean rock surfaces. Shepherd and these corallines. Because the present surveys yield Turner (1985) also observed no juvenile abalone on only correlative data, they cannot distinguish between upright corallines or foliar algae, possibly because 2000 Day & Branch: Juvenile Abalone and Sea Urchins 153 smooth, hard surfaces are necessary for secure pedal Size-related associations between abalone juveniles, adhesion and attachment (Shepherd and Daume 1996). urchins and habitat There are two plausible reasons for the habitat “choice” exhibited by juvenile abalone. The first implies Two possible causes of the correlative relationship selection by juveniles for the coralline substratum itself, between abalone juveniles and sea urchins emerge as circumstantially suggested by the positive selectivity from a consideration of different sized abalone. All indices in Figure 3b. Alternatively, the occurrence of small and medium-sized abalone juveniles were beneath juveniles on corallines may be incidental, and juve- urchins. Although not all large abalone juveniles were niles may actually be selecting urchins that happen to found under urchins, those that were not were con- inhabit that substratum. There was a significant corre- cealed in cracks and crevices. The association between lation between urchin and abalone densities (Fig. 4). abalone juveniles and urchins therefore appears to be This correlation does not, however, answer the question predominantly shelter-related, a view shared by of whether juvenile abalone and urchins merely select Breen et al. (1985) and Tegner and Butler (1989). the same kind of habitat, or whether one is actively The importance of shelter for the survival of juvenile seeking out the other. By contrast, Table I shows that, abalone cannot be overestimated. Caddy and Stamato- not only are abalone juveniles correlated with densities poulos (1990) suggest that the carrying capacity of of urchins, but almost all of them (98Ð100% at all four different habitats is largely dependent on the availability sites) are found under urchins, even though urchins of shelter for individuals of different sizes. Kojima covered only 18Ð25% of the substratum. Conversely, (1981) noted that juvenile survival varied directly although most of the habitat not covered by urchins with the degree of shelter provided by the environment. still consisted of encrusting corallines, extremely few In the present case, it appears to be urchins that are ful- juveniles were found there. filling this role, rather than physical shelters. The most Further circumstantial evidence to reinforce the compelling indication for this comes from the fact suggestion that a close association exists between that the juveniles most vulnerable to predation (i.e. abalone juveniles and urchins was the lack of both at small and medium-size) invariably occurred under Betty’s Bay. Their joint absence corroborated the results urchins (Fig. 5a). Juveniles of other abalone species that of surveys in the area by Marine & Coastal Management do not conceal themselves under urchins all shelter under (MCM, formerly Sea Fisheries Research Institute), boulders (Lowry and Pearse 1973, Dayton 1975). At which previously regularly recorded large populations the sites surveyed in this study, there was a paucity of there (Newman 1968), but which have declined consid- this under-boulder habitat, largely because dense mats erably in recent years (Tarr et al. 1996). The abundance of sand and shale cemented rocks to the substratum. of foliar algae and extensive polychaete mats (Fig. 2a) These mats were created by tubiferous polychaete at Betty’s Bay during the present survey contrasts worms, primarily P. antarctica. The sparsity of “under- with the sparsity of both at all other sites (Fig. 2b), rock” habitat reinforces the potential importance of and also with previous surveys at Betty’s Bay. Field the urchins as a shelter, particularly for small abalone. et al. (1980) recorded virtually no foliar algae or For large juvenile abalone, crevices provide some polychaete mats there in 1976. The marked decline of protection, whether or not urchins are present. It is after both urchins and juvenile abalone at Betty’s Bay may this “large-juvenile” stage that sub-adult abalone therefore be associated with this dramatic change in (>35 mm shell length) begin to lose the photophobia habitat structure and suggests that, in the complete of juvenile abalone and emerge from cryptic habitats to absence of urchins, abalone juveniles either fail to re- inhabit areas of exposed reef. By that stage, their shells cruit or, if they recruit, failed to survive to juvenile are sufficiently robust to offer protection against at sizes. least some predators (Tegner and Butler 1989). The apparent selectivity displayed by juvenile abalone for encrusting corallines at the remaining four sites may therefore be a surrogate for their selection of Implications of the association between juvenile urchins, which happen themselves to live on encrusting abalone and urchins corallines. Consequently, the relationship between H. midae juveniles and P. angulosus suggested by Tarr Thus far, the association observed between abalone et al. (1996) appears to be a direct and causal one, juveniles and sea urchins has been attributed largely and of considerable ecological importance. Of more to the degree of protection from predation offered by practical relevance, these findings validate the protocols the urchins. Witman (1985) affirms that the ability of followed during previous MCM surveys of abalone “structures” to provide refuges from predation can ex- juveniles, in which the only habitat searched to obtain plain local distribution and abundance patterns. Tegner estimates of the densities of juvenile abalone was and Dayton (1977) found that juvenile urchins protected that under urchins. by adult spine canopies survived far longer than un- 154 South African Journal of Marine Science 22 2000 protected juveniles. Tegner and Butler (1989) and grazed by abalone is in limited supply, such dispersal Breen et al. (1985) believe that the occurrence of juve- will ensure that grazing is not restricted to crevices nile abalone and juvenile urchins under adults of the and their immediate vicinity. In addition, if abalone urchin Strongylocentrotus franciscanus is primarily to juveniles are able to derive food from kelp trapped by avoid predation. urchins, they may be able to shorten or even do away There are, however, several additional advantages with periods when they would otherwise have to that such a relationship might hold for juvenile abalone. leave the protection of an urchin to forage (Shepherd One possibility is that abalone might benefit from and Daume 1996). drift kelp caught by urchins (Tegner and Butler 1989). In summary, this paper has shown: Clearly, in the present context, this would depend on whether P. angulosus feeds predominantly by grazing, (i) that both urchins and juvenile abalone are found or by trapping kelp. Wood and Buxton (1996), working predominantly on encrusting corallines; on H. midae in the Eastern Cape, South Africa, suggested (ii) a strong, positive relationship between urchins and that P. angulosus is a nocturnal grazer. However, their abalone juveniles, which seems to be attributable region of study lies beyond the geographic range of to a positive selection of urchins by juvenile aba- subtidal kelp beds, and urchins might therefore be lone; expected to favour a different mode of feeding there. (iii) that both urchins and juveniles are found in higher Although Fricke (1979) described P. angulosus in False densities in crevices than on exposed surfaces; Bay as a “grazer”, he expanded this definition to note (iv) that large juvenile abalone are predominantly that it does feed on pieces of drift kelp, a phenomenon crevice-dwellers, where they may or may not also observed in the present study. The extent to shelter directly under urchins; and which P. angulosus makes use of drift seaweeds is (v) that small and medium-sized abalone juveniles therefore of importance in determining its potential in kelp-dominated ecosystems are almost always impacts on algae, as well as its possible contribution found under urchins and show no preferences to the diet of juvenile abalone. As abalone grow, they for physical shelters, such as crevices and cracks. move onto a diet of macro-algae (Wood and Buxton The practical import of the findings is considerable. 1996), and it is at this point that additional food The association between juvenile abalone and urchins trapped by urchins might be of value, particularly if is so strong in the region investigated that, were urchins juvenile abalone would otherwise be too small to be to be eliminated or substantially reduced, a complete able to trap it themselves. Tegner and Levin (1982) collapse of juvenile abalone can be forecast. Indeed, noted increased growth rates of abalone associated the surveys of Tarr et al. (1996) have shown just this with urchins. at many sites east of Cape Hangklip (Fig. 1), where There are also other potential advantages that might increases in the density of the West-Coast rock lobster accrue to abalone from their association with urchins. J. lalandii have been held responsible. Whatever the At the sites surveyed here, sea urchins were found in cause, these declines have taken place in the heart of shallow subtidal aggregations on coralline-encrusted the commercial abalone fishing grounds and constitute reefs, mainly within beds of the kelp Ecklonia maxima. a serious threat to future recruitment to the fishable These kelp beds may have considerable implications stocks. for the distribution of sea urchins and, hence, abalone juveniles. For example, kelp beds have an important breakwater effect on subtidal communities (Velimirov ACKNOWLEDGEMENTS et al. 1977). Urchin populations that occur in exposed areas lacking kelp beds are frequently controlled by the availability of crevices in which they can shelter Many divers helped with collecting the data for from the surge (Shepherd 1973, see Farquhar 1994 these surveys, and special thanks are due to Messrs for P. angulosus in the Eastern Cape). However, in the M. Farquhar, W. O. Meyer, C. Smith, P. Hanekom, J. A. areas surveyed here, urchins were usually encoun- Bloomer and Y. Lechanteur, Ms J. L. Fowler, C. A. tered on exposed rock surfaces, both flat and vertical, Parkins and C. Heijnis, and Drs K. Prochazka, S. May- with only a minority clustering in crevices. Only in field and B. A. Clark. The Abalone Research Unit at conditions of extreme swell did divers observe urchins MCM, and Mr R. J. Q. Tarr in particular, provided aggregating in crevices, presumably for shelter. There- the initial impetus for this study through their early fore, the normally sheltered conditions in kelp beds observations, and were generous with their time and may enable urchins to spread out away from crevices. additional suggestions regarding this work. Funding Incidentally, this may also disperse the abalone that was provided by grants from the South African take refuge under these urchins. 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