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Notice: ©1989 Elsevier B.V. The final published version of this manuscript is available at http://www.sciencedirect.com/science/journal/00220981 and may be cited as: Cameron, J. L., & Fankboner, P. V. (1989). Reproductive biology of the commercial Parastichopus californicus (Stimpson) (Echinodermata: Holothuroidea). II. Observations on the ecology of development, recruitment and the juvenile life stage. Journal of Experimental Marine Biology and Ecology, 127(1), 43-67.doi:10.1016/0022-0981(89)90208-6 I i'V ) J. Exp. Mar. BioI. £Col., 1989, Vol. 127, pp. 43-67 43 Elsevier

JEM 01229

Reproductive biology of the commercial sea cucumber Parastichopus californicus (Stimpson) (Echinodermata: Holothuroidea). II. Observations on the ecology of development, recruitment, and the juvenile life stage

J. Lane Cameron and Peter V. Fankboner Department ofBiological Sciences. Simon Fraser University. Burnaby, British Columbia, Canada

(Received 17 November 1987; revision received 9 January 1989; accepted 23 January 1989)

Abstract: Evidence from in vitro culture of embryos and larvae of Parastichopus califomicus (Stimpson) suggests that asynchronization of development through metamorphosis and settlement results in a variable pelagic period for larvae within a particular cohort. Additionally, considerable variation in size of 0 + yr recruits observed in situ may indicate that settlement had occurred continuously for some months within the population studied. Recruitment of at least seven of (including P. californicus} was observed at distinct sites that were notably free of the predatory sea stars dawsoni (Verrill), S. stimpsoni (Verrill), and S. endeca (L.). The swimming response characteristic of adult P. californicus when touched by the sunflower star Pycnopodia helianthoides (Brandt) did not occur with the same regularity or intensity in juveniles. S. dawsoni preyed upon small (:S;2 yr of age) P. califomicus in aquaria; sea cucumbers > 2 yr avoided predation by swimming. Periodic collections of P. californicus recruits revealed a pattern of somatic weight loss in the fall and winter that is coincident with a similar pattern reported for the adults of this species. Visceral atrophy was observed in juvenile collected in the late fall. The polynoid wormArctonoepulchra (Johnson) and the endoparasitic gastropod ComenteroxenousparastichopoliTikasingh, common symbionts of adult P. californicus, were also noted on or within juvenile animals.

Key words: ; Ecology; Holothurian; Juvenile; Parastichopus califomicus

INTRODUCTION

The California sea cucumber Parastichopus californicus (Stimpson) is commonly found in rocky low-intertidal and subtidal areas away from strong wave action or in quiet bays and on pilings from Baja California to British Columbia (Ricketts & Calvin, 1968; Brumbaugh, 1980; Kozloff, 1983). This sea cucumber is a relatively large (60-100 em long) epibenthic detritivore, that may reach population densities as high as 0.5' m - 2, and has recently become the focus ofa limited commercial fishery within the

Harbor Branch Oceanographic Institution Contribution No. 656. Correspondence address: Department of Larval Ecology, Harbor Branch Oceanographic Institution, 5600 Old Dixie Highway, Ft. Pierce, FL 34946, U.S.A.

0022-0981/89/$03.50 © 1989.Elsevier Science Publishers B.V. (Biomedical Division) 44 J.L. CAMERON AND P.V. FANKBONER inland waters of British Columbia, Canada, and Puget Sound, Washington (McDaniel, 1984; Sloan, 1985, 1986). Various aspects of the development ofP. califamicus have been examined. Mortensen (1921) reared the larvae to the early auricularia, while Courtney (1927) examined the fertility of excised gametes at various lengths of time after collection. Johnson & Johnson (1950) report on the maturity of gametes collected by dissection. M. Strathmann (1978) outlines processes for the collection and fertilization of the gametes. Smiley & Cloney (1985) discuss oogenesis and ovulation in Stichapus (= Parastichopus) califamicus (cf. Smiley, 1988). Smiley (1986) discusses metamorpho­ sis of the larvae, while Burke et al. (1986) describe the structure of the larval nervous system. Cameron & Fankboner (1984) describe tentacle structure and feeding processes in adult and juvenile animals, and describe seasonal reproductive processes (Cameron & Fankboner, 1986). Swan (1961) reports that adult P. californicus expel their visceral organs in the fall and early winter ofeach year. Fankboner & Cameron (1985), however, have shown that this process is actually visceral atrophy, not evisceration. Additionally, Margolin (1976) reports that adult P. califamicus respond by swimming to the touch of many predatory sea stars. Interestingly, none ofthe sea stars known to elicit swimming behavior prey regularly upon this sea cucumber (Greer, 1961; Mauzey et al., 1968; Shivji et aI., 1983). While much of the biology and ecology of aspidochirote holothurians in general (Mitsukuri, 1903; Trefz, 1958; Ricketts & Calviri, 1968; Jespersen & Lutzen, 1971; Bakus, 1973; Lawrence, 1979; Roberts, 1979; Sloan, 1979; Conand, 1981; Roberts & Bryce, 1982; and others) and P. califamicus specifically is well known, little has been reported on the ecology of development, recruitment, or the juvenile life stage from this group of sea cucumbers (Bakus, 1973; cf. Sloan, 1980; Conand, 1981, 1983). The occurrence and distribution of new recruits and juveniles, size and growth of recruits, predator-prey interactions among juveniles and co-occurring sea stars, and behavior of newly settled and juvenile animals warrants investigation. With the discovery of apparent nursery areas where recruits and juveniles of P. califamicus were regularly observed, and by rearing the larvae through settlement in vitro, we undertook a study of various aspects of the biology and ecology of development, recruitment, and the juvenile life stage of this sea cucumber.

METHODS

COLLECTION AND FERTILIZATION OF OOCYTES

Adult individuals of P. califamicus were collected by scuba from Woodlands, Indian Arm Fjord, British Columbia, at 5-15 m depth. Portions of the excised ovaries from numerous female animals were placed into beakers containing 1200 ml of Millipore­ filtered (0.45 }lm) seawater and stirred at 60 rpm for 2 h. Ovarian fragments were JUVENILE HOLOTHURIAN ECOLOGY 45 removed by filtering the cultures through 500-pm mesh Nitex screen after which 5 ml dilute sperm solution (Strathmann, 1978) were added to each culture. After ~4 h oocytes exposed to sperm were washed and placed into fresh Millipore-filtered seawater. Prior to fertilization some cultures were treated with echinoderm, Pycnopodia helianthoides (Brandt), radial nerve factor (RNF) (Strathmann & Sato, 1969) or with 10- 3 M dithiothreitol (DTT) (Maruyama, 1980) to induce germinal vesicle breakdown. On one occasion naturally spawned oocytes were collected in situ by pipette as they exited the gonopore of a spawning female. This spawning sea cucumber was then placed, while under water, into a large plastic bag and transported to the laboratory.

CULTURING TECHNIQUES Developing embryos and larvae were maintained at 10-12 °C and aerated by stirring with glass paddles attached to slow turning electric motors (60 rpm). Culture salinity was maintained at in situ levels of 27-28%0. Developing larvae were fed equal amounts, in excess, of the marine flagellates Dunaliella tertiolecta, Pavlova lutheri, and Isochrysis galbana (see Hinegardner, 1969; Strathmann, 1971).

OCCURRENCE AND DISTRIBUTION OF JUVENILE ECHINODERMS 228 scuba dives were made from May 1979 through December 1984 to observe or collect P. califomicus in various locations around: San Juan Island (Cantilever Pier and Shady Cove) and Shaw Island (Pt. George), Washington; and Indian Arm Fjord (Woodlands Bay and Croker Island), Howe Sound (Kelvin Grove), and Clayoquot Sound (Ritchie Bay), British Columbia (Fig. 1). The presence or absence of juvenile echinoderms, especially P. califomicus, and potentially important predatory sea stars were qualitatively observed on each dive.

SIZE AND GROWTH OF RECRUITS Traditionally, the juvenile sea cucumber that arises from the metamorphosis of a doliolaria or vitellaria larva has been termed a pentactula because it possesses five primary buccal tentacles (MacBride, 1914; Hyman, 1955). Even though this stage is morphologically similar to the adult, and generally found in the same habitat, it has been called a larva (Barnes, 1980, p. 995). For the purposes of this paper these newly settled animals are termed larvae as long as they possess no more than their five original buccal tentacles. When one additional buccal tentacle appears, we consider the a juvenile of the 0 + year class. Holothurians are quite plastic in their body dimensions, so single measurements of linear size, such as length, are unreliable. Additionally, because of the nature of their respiratory process (the filling and emptying of internal fluid-filled respiratory trees) repeat measurements of mass in individual adult P. califomicus can vary as much as 100g (J. L. Cameron, unpub!. data). Therefore, a bidimensional index of size was determined from the relationship of contracted length (em) times contracted width (em) 46 J.L. CAMERON AND P.V. FANKBONER

A BRITISH COLUMBIA

Fig. 1. (A) Primary study areas within the inland waters of mainland British Columbia (Howe Sound, Indian Arm), the west coast of Vancouver Island (Clayoquot Sound), and the U.S. San Juan Islands. (B) Study sites within U.S. San Juan Islands showing the locations of (1) Pt. George, (2) Cantilever Pier, and (3) Shady Cove. (C) Location of study sites within the inland waters of mainland British Columbia: (4) Croker Island, (5) Woodlands Bay, and (6) Kelvin Grove. JUVENILE HOLOTHURIAN ECOLOGY 47 times a scaling factor of 0.1 (ef. Yingst, 1982). Measurements were taken from animals that were teased to stimulate contraction until the body wall became rigid from internal coelomic pressure. All measurements were made with a ruler 10 or 50 em long on animals submerged in seawater. The smallest animals were measured to the nearest 0.1 em, while larger animals were measured to the nearest 0.5 em. The size index was correlated with the damp weight of the body wall. This weight included the body wall, buccal bulb and longitudinal muscles. The gut, gonad (when present), respiratory trees, polian vesicle, and coelomic fluid were all excised prior to weighing the body wall. Pentactula larvae (up to ~ 5 months postsettlement) reared in vitro were measured with an ocular reticule through a Wild M5A stereomicroscope. Growth within cohorts of P. califamicus discovered in the late spring of 1982 and again in 1984 was observed by periodic collection (every 2-3 months) and sizing. The number of animals collected on each sampling trip was dependent upon the accessibility of sites where juveniles were known to occur, and a desire to collect a sufficient number of animals for experimen­ tation without significantly depleting the juvenile population. With this in mind, divers swimming predetermined routes collected all juvenile sea cucumbers < 5 em in length discovered within 25 min of diving time. It was felt that the 5 cm length constraint might bias the mean individual growth rate downward slightly, but seemed a natural cutoff point from qualitative observations ofjuvenile size distribution within the population. Size indices from two samples ofjuvenile P. califamicus were pooled and divided into size (age) classes by probability paper analysis (Cassie, 1954; Birkeland et aI., 1982), and compared with the size of juveniles ofknown age (Fankboner & Cameron, 1988).

BEHAVIOR

Feeding and locomotory behavior of newly settled pentactula larvae reared in vitro, and of 0 + year class animals collected at Kelvin Grove was observed with a stereo­ microscope. The response of 0 + year class juveniles to being touched by the predatory sea star P. helianthoides was observed in three trials with each of 10 different animals. The tip ofa single ray from a small ( < 10 em diameter, ray tip to ray tip) star was placed mid-dorsally on the experimental animal. The ray was removed after 20 s ofcontact or when a response was observed. Response time and duration of the response was noted for each application in each trial. The intensity of the response was subjectively assigned to one of four categories: no response within the 20-s stimulation period (NR); local contraction of the body wall at the site of stimulation (CONT); arching of the body (ARCH); and undulating contractions of the body or "swimming" (SWIM) (cf. Margolin, 1976).

PREY-PREDATOR INTERACTIONS

Prey-predator interactions between juvenile P. californicus, and predatory sea stars were observed in flow-through seawater aquaria (60 em wide by 90 em long by 15 em 48 J.L. CAMERON AND P.V. FANKBONER deep) at the University of Washington's Friday Harbor Laboratories. The aquaria were devoid of inclusions that could have provided refugia for the sea cucumbers. Adult specimens of the sea star (L.) were starved for 2-6 wk, then offered P. californicus of various sizes (ages). For each trial three or five sea cucumbers of uniform size were placed into an aquarium in which a starved sea star was already present.

RESULTS

DESCRIPTION OF OOCYTES

Mature oocytes of P. californicus are translucent spheres measuring 150 Jlm in diameter and are surrounded by a jelly coat 30 Jlm in thickness. Oocytes collected from excised ovaries are generally enclosed within a follicleof ciliated squamous cells (Smiley & Cloney, 1985). After a few minutes exposure to seawater ovulation occurs. Pre- and postovulation oocytes generally possess a distinct germinal vesicle and nucleolus. < 1% of the hundreds of thousands of oocytes, collected as above, had undergone germinal vesicle breakdown within the ovarian tubules prior to collection. Examination of naturally spawned oocytes 2 h after collection in situ showed the germinal vesicle to be intact with the nucleolus distinctly visible. None of these oocytes was enclosed within follicles, and visually did not appear to be different from oocytes observed two hours after collection by dissection.

FERTILIZATION Treatment ofoocytes with RNF or with DTT did not appear to facilitate fertilization in any of the cultures. In vitro fertilization levels were consistantly quite low ( < 5%).

DEVELOPMENT

Development in P. californicus proceeds in a manner typical for aspidochirote holo­ thurians with planktotrophic larvae (Fig. 2). First cleavage is completed 4 h after insemination. Second cleavage is completed at 6 h after fertilization, while subsequent divisions follow at ~ 2-3 h intervals (Table I) to 16 h after fertilization (64-cellblastula). After 16 h asynchrony in both cleavage pattern and time elapsed to major developmental benchmarks (i.e., gastrula, auricularia, etc.) was noted. 24 h after fertilization> 50% of the embryos in aliquots pipetted from the cultures were at the 128-cellstage, and by 24 h after fertilization > 50% of the embryos in culture were prehatched blastulae. After 40 h invagination of the blastular wall began. 24 h later (64 h after fertilization) an entirely ciliated hatched gastrula was the most common embryonic form in culture. 6-day-old larvae display distinct bilateral symmetry. A ciliated band encircles this stage from the anterior to the posterior in roughly lateral position enclosing the oral field. In some of the larvae the ciliated band has begun to form lobes characteristic of the early auricularia larvae. By Day 13 the larvae have developed into feeding auricularia. JUVENILE HOLOTHURIAN ECOLOGY 49

Fig. 2. Representation of spawning and development through settlement and metamorphosis of P. califomi­ cus. Development does not deviate significantly from that expected for an aspidochirote holothurian with planktotrophic larvae. Drawing is not to scale.

Auricularia were fed in excess as described above. The presence of algal material within the guts was noted during all microscopic examinations, Metamorphosis of the auricularia may begin at ~ 65 days after fertilization or may be delayed upwards of another 60 days. Older auricularia change very little except in overall size, several ofwhich (120 days old) were nearly 1 mm long. Metamorphosis to the pentactula includes a brief transitional barrel-shaped larva called a doliolaria. The doliolaria represents a nearly 90%decrease in body volume from the 60-day auricularia. Metamorphosis to the pentactula occurs quite rapidly, and is a continual process beginning at metamorphosis ofthe auricularia. As the auricularia reduces in size forming the doliolaria the ciliated band of the auricularia breaks into segments forming rings around the larva. These rings persist until after the eruption of the five buccal podia and the first posterioventral pedicle. These early pentactula larvae alternately swim over the substratum or drop to the bottom attaching via their single pedicle. The ciliated bands disappear in completely metamorphosed pentactulae, with the larvae taking up the benthic existence of the adults (J. L. Cameron, unpubl. data). 50 J.L. CAMERON AND P.V. FANKBONER

TABLE I Composite developmental schedule derived from five separate in vitro cultures of the embryos and larvae

of P. califamicus reared at 10-12 0 C.

Developmental stage Time after fertilization

First cleavage 3-4 h Second cleavage 5-6 h Fifth cleavage (32 cell) 13-14 h Most embryos* 64 cells** 16-17 h Most embryos* 128 cells** 19-20 h Pre-hatched blastula 24 h Early gastrula 40 h Hatched gastrula 64h Early auricularia 6 days Feeding auricularia 13 days Metamorphosis to doliolaria 65-125 days Metamorphosis to pentactula 24-48 h post-doliolaria

* Asynchrony of development in simultaneously fertilized ova was common. ** Asynchrony of cleavage common after 32-cell stage (fifth cleavage).

OCCURRENCE AND DISTRIBUTION OF JUVENILE ECHINODERMS

Newly settled sea stars, Pisaster brevispinus (Stimpson), P.ochraceus (Brandt), P. helianthoides, Evasterias troschelli (Stimpson), and others, and the sea urchins Strongylocentrotus franciscanus (Agassiz) and S. droebachiensis (Muller) were regularly observed in the summer and early fall of each sampling year at Kelvin Grove and Indian Arm (both Woodlands Bay and the northern tip near Croker island) (Table II). P. brevispinus, P. ochraceus, P. helianthoides and E. troschelli were all observed at Woodlands Bay, while P. ochraceus and others were observed at Kelvin Grove. Adults of these sea stars, as well as others, commonly occurred at the same sites. Recently settled S.franciscanus (test diameter < 1 em) were observed in great numbers (25-50' m - 2) in each spring we sampled at Kelvin Grove. A late 1st or possible 2nd yr specimen (test diameter ~ 3 em) (cf. Kato & Schroeter, 1986)was seen on one occasion, but no adult S. franciscanus were ever observed in this area. In the late summer, while searching for juvenile P. califomicus, numerous empty tests of these juvenile urchins were noted. In the summers of 1982 and 1983 massive settlements (estimated at > 300 ind . m - 2) of S. droebachiensis were noted in the shallow subtidal at the northern tip of Indian Arm opposite the west side of Croker Island. Rainwater runoffduring the very wet winter season turns the top 1.5-2.5 m of water in Indian Arm to virtually fresh water (Gilmartin, 1962). Massive mortality, which almost equalled recruitment, was observed among these young echinoids at this time (see Himmelman et al., 1975). Occasionally older S. droebachiensis ~ 3-6 em test diameter were observed under rocks and within the interstices between rocks within this area. Juvenile and adult P. californicus were regularly observed at these same locations (Table II). Juvenile animals (presumed late 0+ and 1st yr) at Woodlands Bay and JUVENILE HOLOTHURIAN ECOLOGY 51

TABLE" Study locations within the San Juan Islands, Indian Arm Fjord, Howe Sound, and Clayoquot Sound.

Location Number of Time span of dives Presence or absence" dives Juvenile Solaster": Pycnopodia holothurians

SAN JUAN ISLANDS Cantilever Pier 39 May 79-Mar 80 + + Pt. George'?" 45 May 79-Dec 84 + + Shady Cove 6 May 79-Mar 80 + + HOWE SOUND Kelvin Grove 22 Jun 82-Dec 84 + CLAYOQOUT SOUND Ritchie Bay 7 Jan 81 + INDIAN ARM Croker Island 32 Jun 82-0ct 83 + Woodlands Bay···· 77 Sep 80-0ct 83 + + +++

• + indicates presence of 0 + through adult age classes of P. californicus - indicates animals were all adults of approximately the same size. •• The presence of any combination of the three predatory sea stars , S. dawsoni, or S. endeca are noted in this column. ••• One juvenile, probably early 1st year class, was collected at Pt. George in November 1979. No other juveniles were discovered at this location. •_•• A single Solaster dawsoni was observed on one dive in the summer of 1981 at this location.

Croker Island were commonly found within dense mats of the filamentous red alga Sarcodiotheca gaudichaudii (Montagne) Gabrielson or attached to the thalli and stipes of S.furcata (Setchell & Gardner) Kylin (Croker Island only). At Ritchie Bay (Clayoquot Sound) 0 + yr P. califomicus were found on the parchment tubes of the sedentary polychaete Phyllochaetopterus prolifica Potts which also support a significant growth of the red alga Callophylis jlabellulata Harvey. Juvenile P. califomicus (0 + year class) collected at Kelvin Grove were most often found in fissures or crevices that afforded overhang protection on a nearly vertical rock wall extending from 2 to 20 m in depth. Most of these young were observed in ~ 10 m of water. Divers collected 11-42 0 + year class individuals' 25 min diving time - 1.

SIZE AND GROWTH Measured within a few days ofmetamorphosis, pentactula larvae with no ossification are ~ 250 Jlm long (inclusive of their tentacles). Pentactulae reared in vitro for ~5 months averaged 1.11 mm in length (SD = 0.83, n = 7 [average size in­ dex = 8.59 x 10- 4, SD = 12.42]). ~ 50 days after first settlement, a single juvenile was observed with seven tentacles. This was the only instance of development of secondary podia on pentactulae reared in vitro. Growth within two populations of juveniles at Kelvin Grove was observed periodi­ cally during the months following settlement in 1981 and 1983. Juveniles were first noted 52 J.L. CAMERON AND P.V. FANKBONER in the early spring of 1982 (probably 4-8 months postsettlement), when they were between 0.3 and 1.0 em in contracted length, and were first collected in the summer of 1982 when they were between 0.5 and 1.9 em in contracted length. Over the next 11 months their average size index increased ~ 750%. Growth of the 1981 cohort was greatest in the summer and spring, but slower in the winter (Fig. 3). The 1983 cohort

0.6

X 0.4 Q) U ...... c

Q) N if) 0.2

JASONDJFMAMJJASONDJFMAMJJASONDJ 1983 1984 Fig. 3. In situ growth within two cohorts ofjuvenile P. californicus from Kelvin Grove, Howe Sound, British Columbia. Asterisks denote means that are not significantly different.

(discovered at this same location in the summer of 1984) was sampled approximately every other month until December 1984. In this second group, body size decreased between October and December (Fig. 3). We do not know ifthis decrease is due to an actual reduction in body size or to the loss of larger individuals through predation or migration. In both cohorts the probability that all sample means were equal was P = 0.0000 (Table III). Growth in recently settled juveniles (as observed from field collected specimens) appears to result from the lengthening ofthe body in the anterior direction. At settlement, a single tube foot is present on the ventral surface. As young sea cucumbers grow, this

TABLE III One-way ANOVA of postsettlement growth in two cohorts of recently settled P. californicus from Kelvin Grove.

Source of variation df ss MS P

1982 postsettlement growth Mean size index 4 0.7648 0.1912 0.0000 Error 108 1.5182 0.0141 1984 postsettlement growth Mean size index 3 0.0373 0.0124 0.0000 Error 68 0.0905 0.0013 JUVENILE HOLOTHURIAN ECOLOGY 53

primary tube foot retains its terminal position near the anus. Additional tube feet appear anteriorly to this first pedicle alternating irregularly across the ventral surface among the radii of the trivium. Near the end of the 1st yr postsettlement, a small cluster of tube feet appears terminally around the primary tube foot. Little proliferation of the appendages associated with the water vascular system was noted on pentactulae reared in vitro, but culturing was interrupted by a fatal electrical failure within the culture refrigeration system 5 months after settlement had first begun. 100 + year class animals coIlected from Kelvin Grove in June of 1985 had numerous tube feet (8-48), dorsal papiIlae (15-44), and buccal tentacles (13-17). Probability paper analysis of the pooled size frequency data from two samples of juvenile P. califomicus collected near Croker Island indicates the probable age structure within these animals (Table IV). Juvenile P. califomicus from these samples are from the

TABLE IV Probability paper analysis of pooled size index frequency data from two samples of juvenile P. califomicus collected at Croker Island, Indian Arm Fjord, British Columbia.

Year class' Size index Range n Percentage x SD of total

1 1.01 (0.83) 0.00- 2.50 34 34.3 2 4.45 (1.69) 2.51- 7.50 52 52.5 3 8.97 (1.38) 7.51-11.50 II Il.l 4 13.40 (0.61) 11.51-14.50 4 4.0

• In this analysis the .Ist year class would appear to include newly settled animals. New recruits of 0 + juveniles were not obvious in these samples. See Fig. 3 for representative size indices of juvenile animals from the 0 + year class.

1st year class through 4th year class. Correlation analysis of the relationship of size index to stripped body weight of juvenile P. califomicus < 5-yr-old collected at Croker Island was highly significant (r = 0.96, n = 61). The prediction equation is y = 7.796x - 7.339, x = size index, Y = predicted body weight. Comparison of these data with size indexes of juvenile P. californicus of known age (Fankboner & Cameron, 1988)showed a very close fit, verifyingthe presence of at least four year classes in these samples of juvenile sea cucumbers (Fig. 4). Mature animals are > 56 months old (Fankboner & Cameron, 1988).Collection of smaller animals at Kelvin Grove suggests a 0 + year class in which animals are < 12 months old.

SEASONAL DYNAMICS OF VISCERA Of63juvenile animals collected in August of 1983 at Croker Island, all but three had . complete viscera with their guts full of ingested material (Fig. 4). In a similar sample collected at the same location in October of the same year (n = 36) the viscera were in a state of flux; many individuals were undergoing atrophy and regeneration (Fig. 5). 54 J.L. CAMERON AND P.Y. FANKBONER

15

12

x Q) 9 "D C

Q) N 6 (f)

3

0

Age in Years

Fig.4. Comparison of mean size indexes of juvenile P. californicus derived from probability paper analysis (solid bars) with those of juvenile P. californicus of known age (hashed bars) (Fankboner & Cameron, 1988).

JUVENILE VISCERAL CONDITION

100 l 80 60 40 20 f- Z O-'---~ w o 2 3 4+ ffi 100 _ Complete n. 80 I2Zl Degenerating Q2I Regenerating OCTOBER 28, 1983 601 ::1 at. 2 3 4+ AGE IN YEARS Fig. 5. Condition of the viscera in juvenile Parastichopus califomicus ~4 yr of age collected from Croker Island, Indian Arm, British Columbia. JUVENILE HOLOTHURIAN ECOLOGY 55

BEHAVIOR OF PENTACTULAE AND JUVENILES

The newly settled and growing pentactulae were quite active; larvae ofP. californicus moved and fed with their buccal podia. When feeding, pentactulae sweep the sur­ rounding substratum collecting microorganisms and detritus from the bottom of the culture vessels. Strings of fecal material were often noted in the culture vessels or being evacuated from the cloaca of pentactula larvae. :::::; 90 days after settlement, cloacal pumping was observed, suggesting that respiratory trees were present and functional. Pentactulae were often observed standing up-right on their single tube foot, waving their tentacles above them in a hydra-like manner as described for Holothuria floridana Portales (Edwards, 1909), or by releasing the grip of their tube foot, they sometimes walked across the substratum on their tentacles (cf. Young & Chia, 1982; Cameron & Fankboner, 1984). Juvenile P. californicus (0 + year class) observed in situ at Kelvin Grove fed by firmly attaching themselves to the substratum with their tube feet while sweeping the surrounding rock surfaces with their tentacles. These animals were often difficult to dislodge with a suction pipette. The terminal cluster of tube feet maintained such a grip on the substratum that many animals could be collected only by prying them free with a dissecting probe.

PREY-PREDATOR INTERACTIONS

When stimulated with a ray from the predatory sea star P. helianthoides, juvenile P. califomicus responded with varying levels of intensity and duration of response (Table V). Swimming was not observed in all of the trials. The smallest P. califomicus offered to the predatory sea star S. dawsoni were readily consumed, whereas larger (older) animals escaped predation more easily. The largest of the trial animals (mean size index = 5.26, y = 33.7 g, age re3 yr postsettlement) were never captured by a foraging sea star even after 12 h of continuous and repeated attacks (Table VI). Adult P. californicus maintained in laboratory aquaria for 2-6 months with one or two specimens of either S. dawsoni or S. stimpsoni were occasionally attacked but never consumed (J. L. Cameron, unpubl. data). Juvenile sea cucumbers in the 1st yr after settlement are quite variable in color. The smallest animals are uniformly white, whereas larger and presumable older-0 + age class animals are pink dorsally. During the 2nd yr after settlement (Ist year class) the body wall becomes intensly red-maroon in color. This red-maroon coloration is very similar to the coloration ofthe red algae with which juveniles were sometimes associated, and was especially so in situ where ambient light conditions often rendered the juveniles on red algae nearly invisible.

SYMBIONTS

Of the 14 different samples of juvenile P. califomicus collected at various locations in only one sample were animals found hosting the scale worm Arctonoe pulchra V> 0--

TABLE V Response of juvenile P. californicus to contact of a ray from P. helianthoides. Each animal was stimulated three times for a maximum period of 20 s. Data are reported as length of stimulation (s), length of response (s), and intensity of response". :- Trial 2** r Animal Trial 1** Trial 3** n > Stimulus Response Response Stimulus Response Response Stimulus Response Response :s: tTl time time intensity time time intensity time time intensity :::0 0 Z I 20 45 CONT 20 - NR 20 - NR > 2 8 19 CONT 8 172 ARCH 20 112 SWIM Z 3 3 62 CONT 16 79 CONT 20 40 CONT 0 :'" 4 7 88 SWIM 6 62 SWIM 2 43 CONT -< 5 18 37 CONT 17 55 ARCH 8 30 CONT .." 6 11 68 SWIM 8 92 SWIM 5 30 CONT > Z 7 5 50 ARCH 10 50 ARCH 10 25 CONT ;>': 8 5 79 SWIM 7 103 SWIM 20 NR O:l - 0 9 20 - NR 18 92 ARCH 20 - NR Z tTl 10 20 - NR 3 30 CONT 15 30 CONT :::0 * NR, no response; CONT, local contraction of the body wall at the site of stimulation, ARCH, arching of the body; and SWIM, sinusoidal undulations of the body that result in "swimming" behavior. ** Trials 1 and 2 were done the same day separated by a 30-min rest period. Trial 3 was run the following day.

.. JUVENILE HOLOTHURIAN ECOLOGY 57

TABLE VI Predation on P. californicus by S. dawsoni" in aquaria.

Size index of Number of Duration of Duration of Time to first Number prey X(SD) prey experiment (h) predator attack consumed foraging (h)

0.91 (0.12) 5 24 24 14 min 5 1.67 (0.05) 3 48 48 4h 3 3.68 (0.48) 5 48 43 35 min 3** 5.26 (0.73) 3 48 12 0***

* Stars were starved for 2-6 wk before this experiment. ** After consuming three sea cucumbers in 43 h the star stopped all foraging activity. *** Star actively foraged for 12 h making numerous unsucessful attacks, then ceased all foraging activity.

(Johnson). On 19 October 1982, 42~ 1st yr animals (assumed August-December 1981 settlement) were collected from Kelvin Grove, three of which hosted a single small specimen of A. pulchra each. Two samples of juvenile sea cucumbers (1st through 4th year class) collected at Croker Island were dissected for visceral examination. Six of the 63 animals collected on 8 August 1983 (size index 4.20-9.36, encompassing 2nd, 3rd, and 4th yr juveniles) had single specimens of the endoparasitic gastropod Comenteroxenous parastichopoli Tikasingh attached to their guts. One of these sea cucumbers lacked viscera and the parasite was attached to the anterior region of the esophagus (cf. Lutzen, 1978), a portion of the gut never lost during atrophy or evisceration (Fankboner & Cameron, 1985). Pale white blisters on the gut of one animal were the encysted stage of an unidentified sporozoan that is occasionally observed on the gut of adult P. califomicus prior to the onset of, or during early visceral atrophy (Fankboner & Cameron, 1985).

DISCUSSION

ECOLOGY OF DEVELOPMENT Reliable methods for induction of spawning in holothurians are virtually unknown (McEuen, 1987),and Mortensen (1921) has suggested that next to crinoids holothurians are the poorest of all echinoderms for successful artificial fertilization. McEuen (1987) outlines the procedures for inducing oocyte maturation, but cautions against the likelihood of polyspermy and subsequent abnormal development. In three efforts to rear the embryos and larvae of Parastichopus califomicus only a very small percentage of the ova and oocytes exposed to sperm fertilized and developed to the auricularia. In all instances, the cultures developed to healthy active auricularia that metamorphosed to doliolaria then pentactulae and settled within culture. Development as observed should therefore be representative of normal in situ development of this sea cucumber. Rustad (1938) and Holland (1981) report asynchrony in the development of S. tremulus embryos. Holland considered this normal, while Rustad attributed it to poor 58 J.L. CAMERON AND P.V. FANKBONER

culture conditions. Because Rustad collected spawned ova from containers in which the adults had been transported after collection, he was only able to determine the timing of fertilization to within 0.5 h, and felt that this could account for the observed asynchrony. While the onset of asynchronus development in holothurians is quite variable, its existence is relatively common (see references in Holland, 1981) and should not be considered a result of inadequate or improper culture techniques. The pattern of embryonic and larval development in P. califomicus does not deviate significantly from that for aspidochirote holothurians possessing a planktotrophic larval phase (Hyman, 1955; Kume & Dan, 1968). Metamorphosis and settling were first observed 65 days after fertilization and continued for upwards of another 60 days (cf. McEuen, 1987). When this pattern of asynchronous development is correlated with in situ spawning observations spanning a 3-month mating season (Cameron & Fankboner, 1986), settlement from the first cohort of the season could begin in early August and continue for a least 2 months. Settlement from the fmal cohort of the season would not begin until early November and potentially would not terminate until the end ofthe year. This would result in a potential recruitment period of ~ 5 months duration with pentactulae probably settling out continuously over this period. In other laboratory studies, Strathmann (1978) observed different initial and terminal settlement times for P. califomicus from those reported herein. His observations would result in a settlement period shorter than we have suggested, but still of sufficient duration that a significant extension of the recruitment period is possible. On the other hand, Rutherford (1973) has noted a very short breeding period for the brooding sea cucumber Cucumaria pseudocurata which he suggests is common among holothurians generally (see also Boolootian, 1966). However, McEuen (pers. comm.) states that the young of C. pseudocurata, which are brooded under the trivium of the female, are actually released over an extended period of time possibly comparable to the recruitment period suggested for P. californicus. Marine invertebrates with feeding planktonic larvae, as exemplified by P. californicus, generally have the longest pelagic period of all larval types (Emlet et aI., 1987), and asynchronization of the developmental period of P. californicus embryos and larvae would extend this pelagic period among sibling larvae. This extended settlement period. may be further increased if release of larvae or spawning of gametes is spread over time.. Such is the case with P. californicus in that spawning occurs throughout the late spring and summer (Cameron & Fankboner, 1986). Life in the plankton is generally considered to be quite hazardous for invertebrate larvae (Jackson & Strathmann, 1981). In temperate or boreal marine environments where physical parameters vary greatly and are presumed to affect the timing of reproductive patterns (Thorson, 1950; Barnes, 1975) stochastic environmental pertur­ bations, such as unusual storm activity, anomalous temperature conditions (i.e., El Nino), and predation, may be significant direct or indirect sources of mortality among developing embryos, larvae, and early postsettlement juveniles of many benthic inverte­ brates. JUVENILE HOLOTHURIAN ECOLOGY 59

Life history tactics that extend planktonic larval life and thereby increase the exposure of larvae to the risks associated with a planktonic existence should be considered maladaptive. Strathmann (1974) though suggests that dispersal of sibling larvae by benthic invertebrates may increase the parental cumulative rate of increase if by such dispersal, variation from year to year in the survival and reproduction of siblings is reduced. He also notes that increasing the length of the planktonic period, extending larval release time (spawning period), or varying the length of the larval planktonic period are possible methods of increasing the spread of sibling larvae. Palmer & Strathmann (1981), after modeling the costs and benefits of increasing the scale of dispersal by the larvae of benthic invertebrates, state generally that little advantage lies in an increased scale of dispersal, and that an extended larval life may therefore be a consequence of producing a large number of small eggs. However, Obrebski (1979) has suggested that the evolutionary trend in reproductive strategies of benthic invertebrates where the adult habitats are widely scattered and rare is to retain a long-lived pelagic larva. If environmental processes such as hydrographic conditions were to limit settle­ ment of invertebrate larvae to a few "nursery" sites that were rare in proportion to the adult habitats then selection should operate in the same manner as if the adult habitats were rare and widely distributed. The result being the same in both situations, i.e., the retention of a small long-lived feeding larva. Pennington et al. (1986) have observed stage-specific predation among some common planktonic predators upon the developing larvae of the Pacific sand dollar, Dendraster excentricus (Eschscholtz). Earlier stages (i.e., gastrula, blastula, and prism) are preferen­ tially selected by some predators over later stages (4- and 8-a:m plutei). Rumrill & Chia (1985) report similar results for the embryos of Ss franciscanus and S. purpuratus. P. californicus, with its long-lived pelagic larva, could ameliorate or spread the risk to its developing young from environmental processes, and predation, by varying in time and space the number of embryos, larvae, and newly settled young exposed to the environment at any given time. It is apparent that the extended period of spawning and asynchronous development in P. califomicus significantly expands the planktonic period ofits larvae. This flexibility in spawning and development strategy would appear to be well tuned to the dispersal of sibling larvae and to the spreading of the risk from environmental and biological factors that could cause mortality among the planktonic larvae of P. califomicus. The most obvious reward of such action would appear to be an increased potential, to at least some degree, for successful recruitment in a potentially variable and unpredictable environment.

RECRUITMENT AND JUVENILE ECOLOGY

The discovery of newly recruited (0 + year class) P. californicus at Kelvin Grove allowed us to examine the growth, biology, and ecology ofyoung sea cucumbers in order to evaluate the significance of the juvenile stage in the life history of this sea cucumber.

L 60 J.L. CAMERON AND P.V. FANKBONER < 1 em This study was somewhat opportunistic as juvenile P. californicus < 1 yr old and in length are seldom encountered in situ (cf. Conand, 1983). Populations of P. californicus at Kelvin Grove, Croker Island, and, to a lesser extent, that successful Woodlands Bay regularly included numerous small animals, suggesting recruitment into these areas was common. Recruitment at Kelvin Grove during 1981 and and 1983 was noted with the appearance of 0 + yr animals in the summers of 1982 in the summer of 1984. No juveniles that could have been 0 + animals were observed 1983. This may not be the regular pattern of recruitment at Kelvin Grove though, as that qualitative observations of this population of sea cucumbers included animals settlement had appeared to be of all year classes between 0 + and adult. Apparently occurred regularly each season over the previous four or five years at least. associated The processes of metamorphosis from a planktonic to benthic existence and with the settlement of marine invertebrate larvae can include morphological physiological changes of monumental proportions (Burke, 1983). Additionally, the factors that commonly cue metamorphosis are generally species specific (Burke, 1983; Crisp, 1984). The noteworthy occurrence of numerous echinoderm species settling into subsequent high areas where young P. californicus were commonly found, and the environmental mortality among some of these young, would indicate that some parameter, and not a chemical or biological cue, was instrumental in the congregation Hydrographic and settlement oflarvae at these sites (Barker, 1979; Chia et al., 1984). ecologyof pelagic factors may playa major roll in recruitment patterns. In a review ofthe coast lines help larvae Young & Chia (1987) state that nearshore eddies along irregular ~ that coastal retain larvae in specific areas. Additionally, Ebert Russell (1988) suggest America may gyres resulting from upwelling at headlands along the west coast of North & Nichols (1983) direct settlement of S. purpuratus into specific locations. Barker congregated suggest that "swarms" of the larvae ofAsterias rubens L., which had been Reef) by hydrographic conditions, repeatedly settled into a specific site (Hollicombe while adjacent areas to the north and south had not experienced the same massive recruitment. Tidal generated internal waves and surface slicks have also been shown (Shanks, to transport patches of the pelagic stages of marine invertebrates shoreward that are only 1983, 1985). Physical processes then may trap competent larvae in habitats partially to have marginally suitable for the adults (Thorson, 1950, 1966). This appears been the case at Kelvin Grove, Woodlands, and Croker Island as massive settlements of numerous species of echinoderms occurred in these areas, yet for some species few of these settlers survived for very long. The seasonal loss of visceral organs by evisceration (Swan, 1961; Byrne, 1985) or in adult visceral atrophy (Fankboner & Cameron, 1985) has been observed processes of holothurians. Our examination of 1st through 4th year classes showed the visceral degeneration and subsequent regeneration that occurs in adult animals also • throughout occurs in all age classes of P. californicus. However, this process is staggered the population, with only a portion of the animals with either degenerating or population regenerating viscera at anyone time. All ages of sea cucumbers in a given • JUVENILE HOLOTHURIAN ECOLOGY 61

undergo visceral atrophy and subsequent regeneration seasonally (cf. Fankboner & Cameron, 1985). The frequent observation ofjuvenile P. califomicus closely associated with various red algae suggests that these animals are cryptic in this situation. If this is indeed the case, it is possible that selective settlement ofthe larvae, or some postsettlement process, such as increased survival of young that had randomly settled onto or near a red alga, may account for the establishment ofthe association. Whatever the cause, the resultant effect appears to be a refuge from predators that may use vision as one means of detecting their prey. Bingham & Braithwaite (1986) report the presence of Stichopus ( = Parasti­ chopus) californicus tissues in the guts of three of 47 Hexagrammos decagrammus collected from various locations around the San Juan Islands. On one occasion a hermit crab, Pagurus hirsutiusculus (Dana), was observed to attack and consume an early Ist-yr P. califomicus in an aquarium (J. L. Cameron, unpub!. data). These observations suggest that predation upon P. californicus by visually active predators may be common. The significance of this predation is not known. Adult P. califomicus display an interesting response when touched by many predatory sea stars (Margolin, 1976), yet none ofthe stars that stimulate this response are reported to feed regularly upon this holothurian (Mauzey et al., 1968). The behavior reported as swimming by Margolin (1976) consists ofrapid undulating or sinusoidal movements of the body which propel the sea cucumber across the bottom. Often the sea cucumber is elevated off the bottom for short periods oftime. Juvenile sea cucumbers also respond to the touch of a predatory sea star, but not with the same level ofintensity as reported for the adults. The large sun star P. helianthoides, which is known to be a voracious predator of numerous benthic invertebrates (Greer, 1961; Mauzey et al., 1968; Paul & Feder, 1975; Shivji et al., 1983), elicits the most intense and regular response in adult P. californicus(100 %swimming, 100%oftimes contacted; Margolin, 1976), yet appears seldom if ever to consume P. californicus in situ (Fisher, 1928; Greer, 1961; Mauzey - et al., 1968; Paul & Feder, 1975). At the Woodlands Bay site the density of P. helianthoides reaches 15-20' m - 2 (J. L. Cameron, unpub!. data). Quiescent P. helianthoides were often seen with one or more rays draped across the dorsal surfaces ofP. califomicus. This contact elicited no unusual behavior of any kind in the sea cucumber. Prodding or handling of the star by a diver initiated active movements in the star, and stars so stimulated invariably elicited typical swimming behavior in the sea cucumbers they touched. This suggests that some factor associated with active or excited stars somehow stimulates swimming behavior in the • cucumbers whereas quiescent stars do not (cf. Sloan, 1980). Three congeneric species of predatory sea stars, Solaster dawsoni, S. endeca, and S. stimpsoni, which sometimes occur in areas inhabited by P. califomicus, also elicit a • significant swimming response in adults of this species (56-91 % of contacts resulted in swimming; Margolin, 1976). A considerable portion ofthe diets ofthese three species of sea star are known to consist of holothurians from 1-3 cm long, Cucumaria lubrica up to 10-15 cm long, spp., though not P. califomicus (Mauzey et al., 1968; • Birkeland et al., 1982).

• 62 J.L. CAMERON AND P.Y. FANKBONER

Juvenile P. califamicus were readily consumed by S. dawsani in laboratory predation experiments up to a specific size (size index of ::::; 5). Above this threshold the stars appeared unable to capture the sea cucumbers (cf. Fisher, 1928). Protection from predation due to size is common among marine invertebrates; older animals often attain a size large enough to avoid being consumed by predators that feed upon smaller individuals (Paine, 1976). It appears that P. califamicus > 2 yr of age are immune to predation by S. dawsani, and probably other predatory sea stars as well. Juvenile P. califamicus are conspicuously absent in most areas where adult animals are found (Table II). Qualitative observations of community structure in these areas showed that various species of sea stars of the genus Salater were common in these areas. Inversely, in areas where recruits and juveniles were commonly encountered these sea stars were seldom ifever encountered. These observations circumstantially support the hypothesis that predation upon recruits and juveniles limits their occurrence, and that areas where predatory sea stars are absent may also provide refuges wherein recruits can survive after settlement. Swimming behavior is displayed by all size classes of sea cucumbers but is most effectivein older (larger) animals (Sloan, 1980).The distance that a sea cucumber moves while swimming is a function of its overall length. The sweep of the sinusoidal or undulating motion is much more vigorous in longer animals, and results in a greater displacement with increased thrust off the substratum. This same behavior in animals of the 0 + year class results in a negligible displacement of the animals, especially in aquaria with virtually no water motion. The efficiency of the swimming escape behavior undoubtedly increases with size (age), and may be a factor in providing the apparent size refuge from predatory sea stars. Numerous macroscopic symbionts ofholothurians are known (Jespersen & Lutzen, 1971). Yet, their presence and or prevalence in juvenile animals has not been reported. The purpose of this study was not to account for the varied and numerous symbiotic relationships that may occur in juvenile P. califamicus, but some of the more obvious symbionts could not be ignored. The presence of A. pulchra, C. parastichapali, and an unidentified sporozoan gut parasite, infesting various year classes of this sea cucumber indicates that juvenile animals are not immune to infestation by these symbionts. The presence of presumedly juvenile A. pulchra on 0 + year class P. califamicus would be interesting to follow to determine if growth in this polynoid is arrested by the size of its host or if the worm outgrows its host and seeks a larger one.

SIZE AND GROWTH Adult size among holothurians generally appears to be determinate, with all sea cucumbers in anyone population often being the same size (Bakus, 1973; Con and, 198I). Adult P. califamicus in a given population do appear to be nearly the same size during any given season, yet, Fankboner & Cameron (1985) observed that up to 25% of the maximum summer body weight in one population of adult P. califamicus was lost JUVENILE HOLOTHURIAN ECOLOGY 63

during the winter when feeding had stopped and visceral atrophy and subsequent regeneration ofthe viscera was occurring (cf. Choe, 1963). Similarily, growth in juvenile P. califomicus < 2 yr old appears to be most rapid in the spring and early summer, slowing down in late summer and stopping and regressing in the winter. A similar pattern of growth has been reported for juvenile A. rubens from temperate waters (Barker & Nichols, 1983) along the southwest coast of Britain (see also Choe, 1963). Growth, as we have measured herein, may be confounded with mortality and or dispersion, if one or the other of these factors are age or size dependent, then the observed winter reduction in size may be an artifact caused by these processes. Differen­ tial mortality between larger and smaller individuals within a cohort would bias these data toward lower or higher growth rates depending upon the direction ofthe mortality. However, we feel that a significant portion ofsuch mortality would result from predation and, if occurring, would be most intense throughout the spring and summer. Dispersion ofpost-settlement juveniles (Engstrom, 1982) could also bias the measured growth, but should also be most significant in the spring and summer when the animals are most active (Fankboner & Cameron, 1985; da Silva et al., 1986). The winter reduction in growth rate observed in juvenile animals may be best explained on the basis of somatic tissue resorption resulting from cessation offeeding and visceral atrophy (cf. F ankboner & Cameron, 1985). JuvenileP. califomicus are subject to many ofthe same physiological and environmen­ tal processes that are significant factors in the life history of the adults. Juveniles, .' however, appear to be more susceptible to predation. Recruitment ofjuveniles would . appear to occur regularly in some areas and irregularly or not at all in others. Whether or not those areas where recruitment occurred regularly could be classified as nurseries is enigmatic. There was no identifiable resource that was uniquely important for the survival of sea cucumber recruits in these areas, and indeed the recruits of many other echinoderms did not survive in these areas. Some areas, though, were most certainly predisposed to settlement of the larvae and survival of the recruits of P. califomicus.

ACKNOWLEDGMENTS

We thank Dr. A. O. D. Willows for providing space at the Friday Harbor Laboratories ofthe University ofWashington. Various versions ofthe manuscript benefitted from the comments of B. Bingham, R. Burke, G. Gheen, B. Hartwick, S. McEuen, J. Mc­ Clintock, S. Rumrill, N. Sloan, M. Smith, C. Young, and one anonymous reviewer. The final version of the manuscript was proofread by P. A. Linley. G. I. Hansen identified the algae. Portions of this research were supported by the Science Council of British Columbia and by the National Science and Energy Research Council of Canada. 64 J.L. CAMERON AND P.V. FANKBONER

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