The Larval Development and Juvenile Growth of the Silver Mouth Turban, Turbo argyrostomus.

Item Type Thesis/Dissertation

Authors Kimani, Edward Ndirui

Publisher University of the Ryukyus, Japan

Download date 28/09/2021 18:53:19

Link to Item http://hdl.handle.net/1834/7409 The Larval Development and Juvenile Growth of the

Silver Mouth Turban, Turbo argyrostomus

A THESIS SUBMITTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF THE RYUKYUS IN PARTIAL FULFILLMENT FOR THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE IN MARINE SCIENCES

August 1996

by

Edward Ndirui Kimani

Adviser: Masashi Yamaguchi ------

•

• ":' We certifY that we have read this thesis and found it satisfactory in scope and • content for the degree of Master of Science in Marine Sciences

•

• Thesis committee

•I I J

• J Masashi Y

• j

] 52;2~¥H ~ - Shigemitsu Shokita ....J

., · I

:..J ~i~~ ~

l I Tetsuo Yoshino ..J J ] ]

] ] ~

] 11 ] l .] .J

.J Dedication .J I dedicate this report to my dear wi fe Sarah, and son Kirnani, for their .J patience and understanding during this work. J ] J ] ] ] } ] ] ] ] ] ]

J 111 ]

J ~ J ] Abstract ] The si lver mouth turban, Turbo argyrostomus L. 1758, is an ] archeogastropod widely distributed throughout the Indo-Pacific regIon. It is an important marine resource, harvested for food, ] marIne souvenirs and ornamental items. Mass seed production J techniques for Turbo marmoratus and T. argyrostomus, based on the techniques developed for Trochus niloticus in Palau, are J currently being developed in the Okinawa prefecture, Japan, to J replenish the declining populations of these commercial turbinids. Here, I report on the larval development, metamorphosis and the J effect of diet on growth and shell characters of silver mouth turban ] juveniles, raised in the laboratory. ] I studied the larval developlnent, metamorphosis and juvenile ] growth of T. argyrostomus between August 1995 and July 1996. ] Adults collected from Komesu, southern Okinawa Island, were induced to spawn by packing and UV sterilised seawater treatment ] on 9 August 1995. The green eggs (180-190 Jlm in diameter) ] hatched within 18 hours, underwent torsion a few hours later and metamorphosed in 3-4 days after fertilization in the presence of ] metamorphosis inducing cues. Forty-eight percent of 200 ] competent veligers spontaneously metamorphosed in the absence of metamorphosis inducing cues between 7 days and 21 days after ] J J l fertilization without feeding. The protoconch, 170-185 J.!rn diameter, was colorless and globose in shape with irregular articulations. The juveniles grew to a mean shell length of 3.7 mm in 5 months (mean growth rate of 0.7 mm per month) feeding on microalgae growing on coral rubble and the sides of the aquaria,

and grew to 11.5 mm in 9 months (mean growth rate of2.7 mm per .~

" month) feeding on macroalgae.

Small juveniles of mean shell length 3.9 mm, reared on a small fleshy red algae, Gelidiella acerosa, grew approximately 2 times faster than those reared on the green algae, VIva purtusa, over 18

,.; weeks. The combined diet of these two algae species gave higher growth rates than either algae individually, but did not improve

,..J growth significantly in large juveniles with an initial shell length of i J 5.8 mIn. Percentage survival after 18 weeks was higher for ] juveniles reared on red algae (92.2 oj(,) compared to green algae (81.] 0/0). The shell color of the snails depended on the algal diet. J The shells ofjuveniles collected from the reef were heavier, for the ] same size, than those reared in the laboratory. The juveniles reared on mixed algae growing on coral rubble, collected from the reef, J and the green algae had higher mean shell weights than snails

'I J reared on red algae alone or on a combination of green and red algae. ]

] 2 ] l J ] Introduction ] ] Large turbinids are conspicuous members of the shallow coral reef habitats where they graze on detritus film and algae. They are J valued ornamental and food items in the Indo-Pacific region. The ] shells of turbinids are used in 'Raden', a traditional Japanese craftwork dating back to the 600 A. D. Consequently the ] population of the green snail, Turbo marmoratus, the largest (25 ] cm diameter) and most valued turbinid, has been depleted in the Ryukyu Islands (Yamaguchi 1993). In an attempt to restore the ] population of the commercial turbinids, mass seedling production ] techniques are being developed in the Ryukyu Islands (Murakoshi ] et al. 1993) based on the techniques developed for raising juveniles i] of the top shell, Trochus niloticus (Heslinga 1980). The silver mouth turban, Turbo argyrostomus is widely distributed between j - the intertidal zone and 3 m depth throughout the Indo-Pacific I ] region. Although it is a target species for the reef seeding program I ] in the Ryukyu Islands, little is known of the larval development and juvenile growth of T argyrostomus. I ] ] I Larval development and reproductive biology are central to understanding the biogeography, ecology and evolution of fossil I ] and present marine benthic communities. Gene flow between I ] 3 I ] ] I 1 J '] shallow water populations by means of pelagic larvae is dependent OJ on the length of larval life and the number of larvae produced by

OJ the parent ° population (Scheltema ]971). These factors also determine the possibilities of successful colonization and re­ OJ colonization of depleted habitats, and therefore the geographic ] distribution and evolution of shallow water species. The larval development of T. marmoratus has been described by Murakoshi et 'J al. (1993). Grange (1976) reared the larvae of Lunella smaragda, a I) small turbinid, up to the veliger stage. Experimental larval and I) juvenile rearing of T. argyrostomus have been conducted by the Okinawa Prefectural Sea Farming Center (Murakoshi and J Yamamoto 1991) but details of larval and juvenile growth are J lacking. J The gastropod larval life is divided into two parts: the pre­ ] competent period during which the larvae cannot be induced to metamorphose to the sedentary form and the competent period J when metamorphosis can be induced by providing some chemical ] and/or physical cues of the adult environment (Hadfield 1977, Crisp 1974, Scheltema 1974). The dispersal potential of larvae is ] therefore a function of the rate of development to metamorphic ] competence and the maxinlum length of time that metamorphosis can be delayed in absence of a suitable substrate. Temperature and ]

] 4 ] 1 .J I J I the related rates of growth and differentiation are principle factors J in delaying metamorphosis of gastropod larvae (e.g. Pechenik I J 1984, Lima and Pechenik 1985). The potential for delaying I­ metamorphosis, and therefore the fate of the larvae of J lecithotrophic species, depends on temperature and is limited by ] the amount of yolk in the eggs. Despite widespread occurrence and obvious ecological importance of the ability of larvae to delay ] metamorphosis, delaying capabilities are so far unknown for most ] specIes. ] The mode of larval development in prosobranch gastropods is ] related to the morphology and ornamentation of the larval shell ] (Thorson 1950). Species with plantotrophic larvae have a small protoconch I and a clearly demarcated protoconch II reflecting J planktonic existence. Species with non-planktotrophic larvae have ] large eggs and a large protoconch I (larval shell) with little or no protoconch II reflecting the short time, if any, spent in the ] plankton. The 'Apex Theory' developed by Thorson (1950) and · ] later expanded by Shuto (1974) is based on the observation that I most shells with narrow, high protoconchs and pointed apices are I ] those of species with planktotrophic development, whereas those I ] with globose, low protoconchs and blunt apices are those of species I .. with non-planktotrophic development. Shuto (1974) observed that ] I­ 5 I ] I ] I 1 J ] protoconchs with distinct reticulation and close axial sculpture '] generally had planktotrophic larvae. To infer larval development ] accurately from shell morphology, the protoconchs of a given I • species should be compared with those of congenerics or 'J confamilial species of known larval development. Few records of

, ] larval shell morphology of gastropods exist to pennit such comparIsons. ]

] Mass seed production techniques of the top shell, Trochus niloticus, were developed in Palau, Caroline Islands (Heslinga ] 1980, Heslinga and Hillmann 1981). Juveniles of the green snail ] have been raised to seed coral reefs in the Okinawa prefecture ] based on the spawning and juvenile rearing techniques developed for the top shell (Murakoshi et at. 1993). The sessile diatoms, -J Navicula ramosissima, grown on corrugated PVC plates are used J to feed the juveniles for the first 3 to 4 lTIonths. Fresh green algae, VIva pertusa, is then used until release of the 1 to 1.5 years old ] juveniles on the reefs. Diet determines growth rate (Uki et at. 1986, ] Murakoshi et al. 1993) and the shell coloration of gastropods (Ino 1949, Ino 1952, Olsen 1968, Murakoshi et al. 1993). Red, brown ] and green algae were found to progressively attract young top ] shell, Batillus cornutus (Fuj ii et al. 1988). Although species of Enteromolpha, Monostroma and soft varieties of VIva are taken ]

] 6 ] 1 J 1 by T marmora/us juveniles, red algae with soft tissues such as ] Hypnea, Gelidium, Graci/aria, Eucheuma, which are carrangeenan ] or agar producing genera, are preferred (Yamaguchi 1993). Comparative studies on diet preference and growth of juveniles J have economic relevance in reef seeding programs. ] Despite the recent advances in larval and juvenile rearing of coral J reef gastropods, outgrowing success on the reefs has been very J liJnited. The main problem is poor survival after release on the reef. Predation and dispersion by strong waves were the main j causes of poor survival of T marmora/us juveniles (Nakamura • J 1992). Many factors may lead to high predation rates of released gastropod juveniles. Among them are poorly developed shell, un­ •I J natural shell coloration reducing camouflage, and poor escape j response developed in the absence of natural water rhythms and J predators. The turban shell, Turbo cornu/us, developed no spines and changed shell color when removed from the normal habitat to a · J calm dark habitat (Tno 1943). Shell and body form determines predation and the adhesion power of Nucella (Kitching et al. J· · 1966). In this study, ] determined the effect of macroalgae diet on J shell thickness, by comparing shell weights, of juveniles fed on

·i different diets in the laboratory. I _.1

I _..J_ j· 7

J , J ]

] The aim of this study was to describe the larval development of ] Turbo argyrostomus, and to examine some aspects the of juvenile development, growth and survival, relevant to mass production of ] juveniles. This report describes the larval development and ] metamorphosis of T argyrostomus and the effect of macroalgal diets on the growth and shell characteristics ofthe juveniles. J ] ] ] ] ] ] ] ] ] ] ]

] 8 ] 1 J

_l Materials and Methods .l ] Spmvning, larval andjuvenile development

] This study was conducted at the University of the Ryukyus, in J Okinawa Island, southern Japan from May 1995 to August 1996. Between 15 and 40 individuals of T. argyrostomus were collected, J regularly from May to September 1995 close to the full moon, J around Okinawa Island. They were kept in strongly aerated seawater overnight in the laboratory until the following evening. ] Induced spawning was then attempted by changing the mucus ] fouled seawater with fresh UV treated seawater at room ] temperature without aeration. Snails were removed as soon as they started to spawn, and males were separated from females to avoid J multiple fertilization. The eggs were retained at the bottom of ] beakers and excess mucous was removed by decanting several times. The eggs were then inoculated by introducing a small ] amount of sperm into the holding beakers and stirring gently. To ] document early development, embryos and larvae samples were periodically observed, sketched using camera lucida attached to a

] compound microscope, photographed and preserved in 70 o~ ] alcohol. Egg and larval shell diameters were measured with the aid of calibrated ocular microscope. Red algae encrusted coral rubble ]

] 9 ] 1 J 1 was introduced on the second day to induce metamorphosis and ] settlement. ] An experiment to determine the rate and timing of metamorphosis ] in the absence of a stimulating substrate was undertaken. Two ] hundred vigorously swimming veligers were held in 10 f.!m filtered seawater at 23-25 °C, in ten glass petri dishes (6 cm diameter) on ] the second day after fertilization. Metamorphosed, dead and ] surviving larvae were counted and the seawater in the dishes was ] changed daily. All the dead and metamorphosed snails were also removed daily. Shell specimens of the larvae and early juveniles ] were examined and photographed by scanning electron microscope ] to visualize ornamentation in detail. Dry shell specimens were mounted on tape on metal screws and gold coated in a Polaron ] coater. The coated specimens were then examined with a Hitachi ] S-530 scanning electron Inicroscope at an accelerating voltage of 20 kv and micrographs were taken. ] ] Diet andjuvenile growth ] Five months old juveniles were fed on two algae specIes In ] isolation, and on a combination of both species to determine the effect of algal diet on growth. The juveniles were separated into 2 ]

] IO ] 1 J ] size groups: 208 individuals of mean shell length 3.9 + 0.6 mm and ] 41 individuals of mean shell length 5.8 + 0.6 mm. Each group was J divided into 3 sets which were reared on different algal diets for 18 weeks (Table 2). One set in each group was reared on the soft J green algae, VIva pertusa, collected from reef lagoons. The second ] set was reared on the small fleshy red algae Gelidiella acerosa ] found attached to coral rubble in shallow water and the third set was reared on a combination of the two algae species. The snails J were held in 2 mm nylon mesh enclosures in a 200 Ire-circulation ] aquarium with sand filter, maintained at 22-23 °C and 35 ppt salinity in the laboratory. Fresh algae was provided every other ] day. Droppings were removed weekly by siphoning approximately ] 20-30 % of the water to avoid fouling and maintain water quality. Growth was monitored by measuring the shell lengths of all ] surviving snails, on 3 week intervals using vernier calipers to 0.1 ] mm.

] The shell thickness (measured as shell weight) of the laboratory ] reared juveniles were compared to shells of juveniles collected from shallow reefs on the west coast of Okinawa Island by SCUBA ] diving. Shell samples of 1 year old snails, raised by M. Yamaguchi - J on mixed algae growing on coral rubble collected from the reef, ] were also compared with shells of the snails raised in this study.

] 11 ] l I J ] The snails were killed by boiling gently. All the flesh and attached ] Inaterial were then carefully cleaned off, and the shells were dried J for 6 hours at 50°C. Shell lengths were measured to 0.1 mm by calipers and weight to O.OOlg on a top loading balance. ] ] Data analysis

J The effect of diet on growth was determined by comparing shell J lengths using one way ANOVA and Turkey's honest significant difference test for unequal numbers. To compare shell weight, J analysis of covariance was done on square root transformed data, ] with diet as the main effect and shell length as the covariate. ] Homogeneity of variances was tested using Levene's test and the distribution of data was tested by the Kolmogorov-Smirnov one ] sample test. ] ] ] ] ] ]

] 12 ] l J J Results ] J Spawning and larval development

J A total of 6 (3 males and 3 females) out of 13 individuals spawned .'] on 3 July and 9 (6 males and 3 females) out of 15 individuals on 9 August 1995. The males spawned approximately 30 minutes after ] changing the mucus fouled seawater. The sperm was discharged J with stream of water by suddenly closing the operculum. The females spawned approximately 1 hour after changing the water. ] The green eggs were spawned with copious amounts of mucus that ] settled to the bottom of the vessels. Approximately 90,000 eggs ] were collected fronl the 3 females that spawned on 9 August. After washing repeatedly in 10 J.!m filtered seawater, they were ] inoculated with a small amount of sperm. The larvae obtained on ] 9 August were used for all studies. A summary of larval development stages and sizes are shown in Table 1. ] ] The green eggs were spherical, with a maximum egg cell diameter of 180-190 J.!m and were covered by a 20-30 J.!m thick jelly layer ] (Fig. 1A). The first cleavage started within 30 minutes after ] fertilization, making two macromeres of equal size (Fig. 1B). ] Consecutive cleavages into 4, then 8 macromeres occurred within

] 13 ] 1 J ]

J Table 1. The embryonic and larval development stages of Turbo

] argyrostomus reared in the laboratory at 24-27 °c. ] Development stage Widest diameter (~m) Time after fertilization ] J Unfertilized egg 180-190 0 2 cell stage " 30-40 minutes J 4 cell stage " 60-90 minutes ] 8 cell stage " 120-150 minutes Morula stage " 4-5 hours ] Trochophore stage " 9-12 hours Pre-torsion ve1iger 170-180 14-18 hours ] Post-torsion stage " 20-30 hours Metamorphosed J juvenile " 3-4 days J J J J J J J 14 J l J ] increasing time spans (Table 1). A clearer animal and a densely ] pigmented vegetal pole could be distinguished at the morula stage, ] 4-5 hours after fertilization (Fig. 1D). The apical invagination was also evident at this stage. 1 ] Gastrulation occurred 5-6 hours after fertilization and the prototroch and apical tuft cilia were evident 9-12 hours after 1 fertilization (Fig. 1E). Intermittent beating of the prototroch and J apical tuft cilia kept the trochophore larvae moving within the egg. The protoconch appeared in the early trochophore, 9-12 hours after ] fertilization and was three-quarters complete at the late ] trochophore stage (Fig. IF). ] The larvae hatched within 14-18 hours after fertilization to pre­ ] torsion veligers. The veligers had two eye spots on the inner edge ] of the single-lobed vela (Fig. 2A) and swam near the water surface. Protoconch was transparent and four-fifths complete at hatching. ] The developlnent of protoconch was complete within a few hours

] after hatching, and was 180-190 ~tm at the greatest width. The veliger was uniform green in color with a slight bulge of the ] propodium. The post-torsion bi-lobed veligers with a small foot ] and opercullum (Fig. 2B) were observed 20-30 hours after fertilization. The veligers were transferred to aquaria in which red ]

] 15 ] 1 J J algae encrusted coral rubble had been put when they were J observed to creep at the bottom of the beakers with well developed J sticky feet, 2 days after fertilization (Fig. 2C).

J Metamorphosis and early shell development J Metamorphosis occurred within 3-4 days after fertilization in the J presence of coral rubble encrusted with red algae. Metamorphosed J juveniles lost their vela and developed tentacles and eyestalks (Fig. 2D). J J Fifty-eight percent of 200 veHgers held in dishes without a settlement substrate died between 2 days and 6 days after J fertilization (Fig. 3). No metamorphosed individuals were observed ] until 7 days after fertilization. Only a few veligers metamorphosed ] or died between 6 days and 10 days after fertilization. The number of metamorphosed juveniles increased to a total of 86 individuals ] (43 % of the total) 21 days after fertilization. Only 8 individuals J died 6 days after fertilization. It was not possible to differentiate metamorphosed and non-metamorphosed veligers when dead due J to the rapid disintegration of tissues. It is therefore possible some ] individuals died after nletamorphosis. ]

"] 16 ] 1 J 1

] The shells of newly settled juvenile were transparent, globose, with ] irregular ornamentation and a prominent sinusigera lib (Figs. 4A, 4B). Developlnent of a transparent teleoconch was observed 5 days ] after metamorphosis, and 8 days after fertilization (Figs. 4 C, 4D). J No protoconch II was evident between the protoconch and the teleoconch. Half the first teleoconch whorl developed as irregular ] rectangles bound by longitudinal and transverse ridges, J approximately 2 weeks after metamorphosis (Figs. 5A, 5B). A second, wider whorl was complete by the second month (Figs. 5C, J 5D). Reddish brown bloches appeared on the third whorl. J J oJ J J J J J J J 17 J .., J 1 1 I J A 8

1

I 1 ] , .. I J 1 1 c D I J apical invagination I J I J I J I J E F apical tuft I ' ] prototroch I J - early protoconch ,J -

Figure I. The embryonic and larval development of J'urho urgvroslol1llls reared in the ~J laboratory at 24-27 "c. A: Newly spawned egg. B: Two-cell stage, 30-40 minutes after

fertilization. C: Four-cell stage, 60-90 minutes after fertilization. D: Morula stage, 4-5 I~ I hours after fertilization. E: Early trochophore with cilia and early protoconch, 9-12 hours J after fertilization F: Late trochophore with three-fourths of the protoconch complete, 14­ I 18 hours after fertilization Scale bar = )00 11m. ] ] 18 l J 1 J bi-Iobed velum A

1 ~eyespots

...... operculum J '\\~'~': ·x: ."/ '4 propodium J 1 J c /'01?17- tentacles ]

eye ] ] - ] ] Figure 2. The larval development of Turbo art,7)'ros·tomus reared in the ] laboratory at 24-27 cle. A: Pre-torsion veligcr. 14-18 hours after fertilization. B: Early post-torsion veliger, 20-30 hours aftcr fcrtilization. C: Late post­ ] torsion veliger, 30-45 hours aner fertilization. D: Metamorphosed juvenile, 2­

] 3 days after fertilization. Scale bar = I00 ~lm. ] .' ] ] ] 19 1 l l J ,

I 220 ~,~~-~-~~-~~~~--~~-~~~~--~J j -0- Number surviving -0- Number metamorphosed 180 l

.J

Vl 140

~ .~ ] 100

J 13 ~ .0 § 60 ] Z

] 20 -~~-~~--~-~~. -20 LI ] 2 3 4 5 (, 7 8 9 10 II 12 13 14 15 16 17 18 )9 20 21 Days ] Figure 3. Number of metatnorphosed and surviving Turbo argyrostomus veliger larvae, held in glass dishes in absence of J metamorphosis inducing cues at 23-24 °C in the Laboratory, 2 days ] after fertilization . .J ] ] J ] J 20 ] 1 Ful!~ FiguL"+ Scanning electron micrographs of'the- larval and early .iuvenile shelis of Tun'h Clrg:"i"nS!OI17US .~,

de\eloped lanal shell (prowcol1ch: Scale bar = i 25 11m. B Full~ d\?veloped larval shelL \cak bar = 5() pm C ~_~fl b~r' RIQhl \'ie\\ of earh jU\enik she]1 sllO\\inC'. initial she]] 2ro\\'th. 8 dm's after fenilJz[Hion SC~1k = ::2:::LLIll U ...... • • ...... '""-' ~ I sho\\lI1~ \In\ or~al!:, .1uve11lle sheli lI1ilia! sheIl grO\vth. 8 days a!l(:: fertilization Scale bar = ::) Lll1i

:1 ,---. ..-----, ,--, II r~ II rI fI .,---, r-. .---. II --, . --" ....----, --, Figure 5. Scanning electron micrographs of the early juvenile shells Turbo Clr;"'~Tost()IJlUs. A: Right vie\v of half of the first whorL Scale bar =125 11m. B: Left view of half of the first whorl. Scale bar = 125 11m. C: Right vievl"of 2 ~)cale ~lm. month old juvenile shell. Scale bar = 500 ~lm. D: Left view of 2 month old juvenile shell. bar = 500

')'l ,...... , ~ ..., ...., ...., ~ ~'" ~ r---1 ..., rI r1' It' " II It It I"' r-l r-l r J J Juvenile growth, diet and survival ] ] The mean growth rate of T. argyrostomus juveniles was 0.72 + 0.3 mm per month for the first 5 months, feeding on microalgae ] growing on coral rubble and aquaria walls, and 2.7 + 0.6 mm per ] month for the next 4.5 months, feeding on macroalgae. Variation of size increased with age (Fig. 6). The largest individual was 2.9 ] times larger than the smallest by the 9th month. ] ] Mean shell lengths of the small size juveniles reared on different algal diets were significantly different after 6 weeks (one way

] ANOVA, F = 14.96, P < 0.001) and after 9 weeks for the large ] juveniles (one way ANOVA, F = 17.68, P < 0.001). The mean growth rate of small juveniles reared on the red algae, Gelidiella J acerosa, was approximately 2 times higher than the mean growth ] rate of the juveniles reared on green algae, Viva pertusa (Table 2). The juveniles reared on combined red and green algae had the ] highest mean shell length after 18 weeks. The same pattern was ] observed for the large size group; the mean growth rate of the juveniles reared on red algae was higher than that of juveniles ] reared on green algae, and highest for the juveniles reared on a ] combined red and green algae diet. The general growth pattern is shown on Figures 7A and 7B. ] ] 23 J 1 J '] I '] ]

22 ] 111

14

I] S ~

..cl ~1O ..!:!= I] ...... cl

] -2 0 2 3 4 5 6 7 8 9 ] Months

, 1 ] Figure 6. The growth pattern of Turbo argyrostomus juveniles ] reared on n1icroalgae growing on coral rubble and aquaria walls (first 5 months) and macroalgae (last 4 months) in the laboratory. ] Vertical bars = size range. I] ]

I I] J I·, ,I] I] 24

• I ] :1 J I] I] 16 1 IA "0. Gn.-en algae 14 -'''''' Red algae I] """l::l.... Gn.-cn+Red algae

12 I· 6' ] -! 10 oJ: "til c I- J! 8 = oJ:.. ] Vl 6

I) 4

2 I) 0 3 6 <) 12 15 18 Weeks

I) \8 B "0.. Green algae I 16 -'''''' Red algae I """l::l.... Grecn+Red algae J 14 e I oS 12 ..c: 'ell c J J! 10 -.:; ..c: I] '" 8

I. ~ ~---~___ ...J I J () (, 9 12 15 18 Weeks

1 J Figure 7. The growth pattern of Turbo argyrostomus juveniles reared on I J different types of macroalgae diets in the laboratory at 22-24 DC. Vertical bar I J = size range; A = small size group (3.9 ± 0.6 mm); B = large size group (5.8 J ± 0.6 mm); Green algae = VIva pertusa; Red algae = Gelhdiella acerosa. I_ I) J 25 I ] 1 1 J ]

] Growth rates were similar for snails reared on red and cOlnbined 1 green and red algae in both groups (Table 2). Paired comparisons of the mean shell lengths of the small size juveniles, after 18 1 weeks, indicate significant differences between the snails reared on ] the 3 algal diet regimes (one way ANOVA, F = 131.84, P < 0.001). However, the mean shell lengths of the large juveniles reared on 1 red algae and conlbined green and red algae were not significantly ] different (F = 3.96, P = 0.57). Size variation of the small size group, was highest for snails reared on green algae (coefficient of ] variation: 22, 12 and 13 % for green, red and the combined green ] and red algae respectively) with some of the smallest individuals ] hardly growing at all after 18 weeks. Size variation of the large juveniles reared on different diets was similar (6.0, 8.0, and 8.0 for J green, red and combined green and red algal diets respectively). ] The percentage survival of snaHs reared on green algae and the ] conlbination of red and green dropped to about 93 0/0, 3 weeks after ] cOlnlnencing the feeding experiment (Fig. 8). The survival of snails reared on green algae ':llone continued to drop to 81 % after 15 ] weeks. Survival of those reared on the combination of the two ] algae species leveled off after 9 weeks at 90 0/0. None of snails reared on red algae were lost during the first 6 weeks of the ]

] 26 ] 1 Table 2. The initial and final (after 18 weeks) mean shell lengths (+ s.d. mm), numbers (in parenthesis) and growth rates of Turbo argyrostomus juveniles reared on green (Viva purtusa), red (Gelidiella acerosa) algae and a combination of both algae species.

Algae diet Initial shell length Final shell length Growth rate (Jlrn) day"I

A B A B A B

Green algae 3.9 ± 0.6 (69) 5.8 ± 0.3 (13) 6.8 ± 1.5 (56) 10.6 ± 0.6 (13) 25.6 40.7

Red algae 3.9 ± 0.6 (68) 5.7 ± 0.5 (14) 9.5 ± 1.2 (62) I4.I±1.I(14) 47.5 71.2

Green +Red algae 3.9 ± 0.6 (71) 5.8 ± 0.4 (14) 10.9 ± 1.4 (64) 15.1 ± 1.2 (14) 59.3 78.8

A = small size group; B = large size group.

27 ~ ~ ~ ~ ...., --- w--'I .J ,J.-, r-'l r-'l r---"'1 ,..--, ,r--1I r--1I ,--, ,--, '--'. r--t' r--J r--t r­ i - -'

_--i 102 ,------,------~~----~- ~------~------~

98 f \ . 10G=.'-0- Red algae... \ . --t>. Green+Red algae '\ 941 'fl.­

I '

~ i ­ - "'ll._

'-' ~ ------~ ----- t> ;> -'"c: 'Q. ::>

78 ,------.--.-----.----~.----~-----.------J o 3 6 9 12 15 18 J Weeks

..i . Figure 8. The percentage survival pattern of Turbo argyrostomus ..i juveniles reared on different algae diets in the laboratory for 18 . . I weeks. Green algae = VIva pertusa; Red algae = Gelidiella , J acerosa. J

J

· .­ ! ·I

l• l 28 -J

l J I] I] experiment. Although some individuals died thereafter, more snails I] reared on red algae survived than those reared on either the green i or the combined red and green algal diet. Survival during the last 6 "] weeks of the feeding experiment was 100 % for all diets. No snails ] died in the large size group during the entire feeding experiment. ] Effect ofdiet on shell color and weight ] The shells of T argyrostomus juveniles reared on green algae were ] characteristically light green while those of snails reared on red ] and the combined green and red algal diet were light-green with ] mottled reddish blotches. The shell color of juveniles collected from the reef were mainly mottled red with greenish blotches (Fig. ,] 9). '] Shell weights of silnilar-sized juveniles, 10.5 + 3.7 mm and 0.39 + ] 0.36 g collected frOln the reef and 11.3 + 3.5 mm and 0.35 + 0.29 ] g reared in the laboratory, were compared. The elevation of the regression line of shell weights upon shell length of juveniles J collected from the reef was higher than that of juveniles reared in J the laboratory (Fig. 10). Shell weights of juvenile snails collected J from the reef were significantly higher than those of snails reared J 29 J 1 ,I :1 '] I

'1, 1 ] ] ,J ']

] Figure 9. The shell color variation of Turbo argyrostomus juveniles reared on different algae (the algae diet was the left to , ] right; Viva pertusa, Gelidiella acerosa, and a combination of V. -] pertusa and G. acerosa in the laboratory) and a shell of a T .] argyrostomus juvenile collected frotTI the reef. Shell lengths: 16, 17, 15 and 22 mm respectively. ,] ] ] ] J ] 30 ] 1 J :1 :1 :1 1.4 I I :] 1.2 0] § 0.8 .c -011 0.6 '

0.2 '''0.. Reef " ] "0.... Lab, reared 0

:l -0.2 4 6 8 10 12 14 16 18 20 '] Shell length (mm)

'], Figure 10. The regression lines of shell weights upon shell lengths :] of Turbo argyrostomus juveniles collected from the reef and reared in the laboratory. Regression formulas: Y = - 0.609 + 0.096 X and "] , Y = - 0.561 + 0.081 X for shells of juveniles collected from the I '] reef and reared in the laboratory respectively. ] ] ] " ] ] 31 ] 1 I ']

:1 in the laboratory (ANCOYA of square root transfonned data, F = '] 305.75, P < 0.001). The adjusted mean shell weight of juveniles collected from the reef was 34 % higher than that of juveniles '] reared in the laboratory (0.432 and 0.323 g respectively). The '] differences between the regression lines increased with increasing shell length. ']

'] The regression lines of shell weights upon shell lengths of similar­ I sized juveniles: 9.5 + 1.4 tum and 0.200 + 0.056 g, 10.0 + 1.2 mm '] and 0.190 + 0.063 g, 10.2 + 0.9 mm and 0.212 + 0.048 g, 10.2 + i] 0.9 mm and 0.200 + 0.064 g for the juveniles reared on green I] algae, red algae, combined green and red and mixed algae growing on coral rubble respectively; with shell length as the covariate, ] were significantly different (ANCOVA of square root transfonned ] data, F = 281.95, P < 0.001). The regression lines were heterogeneous (parallelism test, p = 0.061, Fig. 11). Pairwise ] cOlnparisons revealed that the regression line of snails reared on ] red algae was not significantly different from that of juveniles reared on combined green and red algae (F = 0.076, P = 0.78). The ] adjusted shell weights were: 0.217,0.191,0.185,0.205 for shells ] ] ] 32 ] 1 J · .] , of juveniles reared on green, red, combined green and red and · I]

, mixed algae diet, respectively. · ~] •

The absolute differences of the adjusted shell weight means were - ~ ] - , small. The difference between the shell weight upon length _I] regression lines of snails reared on green algae and other diets r _l] decreased with increasing shell length (Fig. 11). The difference , between the shell weights upon length regression lines of snails - I] , reared on red and combined green and red algae diet and that of

snails reared on a mixed diet, increased with increase in shell - ~ ] r length. - I ] I

I - ~ ] ! _ vi ]

- , ='~ J

- ! ] ] _ '] i I] -J (J

[ : ] 33

[ I ] r 1 J ] ]

O.W , " '" ' ' ] "...... -:

AA ":-,, Q o.~ ~

0 0 66':"

g ,~

~.."

] o.~

o t. , ' ~ 0 W"'" _,~oe 0

§

O~

~ o 0,'",';.Al." nA 0

~

] ,," ~,,4 6 ~

~ ",~

0.2 040 0

~ o 0 ,,'Ot. ,oa B 0 ~ I] 00 80 ,','" "t:>" 00'0.. Q16 " 0 0 Green algae o ", ,,0 °0 ''0..... Red algae o ,," 0 0 0 " 0 8 0 I] 0.12 o '0..... Green+Red algae '0t..• Mixed algae

O.M 7 8 9 10 11 12 13 I] Shell length (mm) I] Figure] 1. The regression lines of shell weights upon shell lengths I] of Turbo argyrostomus juveniles reared on different algal diets in I] the laboratory. Regression formulas; Y = - 0.269 + 0.049 X; Y = ­ 0.342 + 0.053 X; Y = - 0.331 + 0.052 X; Y = - 0.386 + 0.059 X I] for shell weights of juveniles reared on the green algae, VIva I] pertusa, the red algae, Gellidiella acerosa, the combined green and red algae species and mixed algae growing on cora] rubble I] collected from the reef. I ] I J 1­ -] \ ­ ,] 34 I J 1 1 J ] Discussion ] ] Spawning and lan'al development

] Packing and UV sterilized seawater method has been used to ] induce spawning in gastropods with varyIng success. Approxitnately 50 % of Turbo argyrostomus individuals stitnulated ] in this study spawned. This rate is higher than the 1.5-35.8 % achieved for the top shell using the still water and UV treated I] water method (Kubo et al. 1989) and lower than the 27-100 % I] achieved for green snail, using the same method (Murakoshi et al. I] 1993). The nUInber of eggs spawned by individual an T. argyrostomus females, approximately is less than the number I] obtained from an individual Turbo marmoratus (Table 3). Among ] the individuals that spawned, the proportion of females was 50.0 0/0 I. for T. lnarmoratus and 33.3 % for T. argyrostomus. This I] proportion is higher than for T. niloticus, of which only 7.7 % of J the number that spawned were females (Kubo et al. 1989). I J I Larval and reproductive aspects of some larger tropical manne J archeogastropods are compared in Table 4. The egg diameter of T. I

J argyrostomus is on the outer limit of the 100-170 ~lm size range, I_ while the protoconch I diameter lies within the 125.9-369.4 /-lm

-J I ~ 35 1 ] J I 1 Table 4. Reproductive and larval development aspects of some tropical marine archeogastropods.

Species Number of eggsx 103 Egg Diameter(J.lm) Hatching stage Maximum length of Reference larval life

Turbo argyrostomus 30 (Ind) 180-190 veliger 21 days This study

Turbo marmoratus 1500-24000 (Ind) 230-270 trochophore ? Murakoshi et al. 1993

Trochus niloticus 100-1000 (Nat) 185.2±3.2 trochophore 21 days Kubo et al. 1989

Cittarium pica ? 170-175 trochophore 14 days Bell 1992

Ind = induced spawning; Nat = natural spawning.

36 ~~~~~~~""""''''''''''''''''''''''''''''''r--l~r-1'''''''r-Ir-1r- --_. ' • • J '] size range, estimated for gastropods with a planktonic larval life ] (Lima 1990). The jelly layer on the eggs of T argyrostoma and ] Lunella smaragda (Grange 1976) is smooth unlike that of T niloticus eggs, which is pitted (Heslinga 198]). However, the jelly J layer of the eggs of the West Indian top shell, Cittarium pica, was J smooth (Bell 1992) and therefore a pitted jelly layer is not a general character of Trochus. The larvae of T argyrostomus hatch J as veligers, unlike the other species which hatch as trochophores. J The velum of pre-torsion T argyrostomus is single lobed similar to that of pre-torsion 1. smaragda. The velum of T argyrostomus J post-torsion veliger is bi-lobed while the trochids, T niloticus and ] C. pica have single lobed vela. Adult trochids have single lobed ,] feet while T argyrostomus has double lobed feet.

] Metamolphosis and geographical range ] The ability to delay metamorphosis by competent larvae in the ] absence of appropriate cues should increase the probability of ] metanl01-phosis in an environment favorable for juvenile survival and subsequent repr~ductive success (Thorson 1950, Scheltema ] 196], Crisp ]974). The type of larval development and the ] capacity for dispersal determines geographical ranges, extinction and speciation rates in prosobranch gastropods (Scheltema 1977). ]

] 37 J 1 ,J

:1 The gastropod species compared in Table 3 have similar larval :1 biology but their geographic distribution is different. Turbo :l argyrostomus is distributed throughout the Indo-Pacific regIon while the T marmoratus is distributed in the Indo-Pacific west of

:l Fiji (Abbott and Dance 1982). T niloticus is distributed in the ~] eastern Indian ocean and the western Pacific; from Sri-Lanka (Rao I l] 1936) to Wallis Island (Gillett 1986a) and the Ryukyu Islands of southern Japan (Hedley 1917) to New Calendonia (Bour et al. I] 1982) and the Swain reefs complex at the southern end of the I] Great Barrier Reef (Moorhouse 1933). The distribution of Cittarium pica is restricted to the Bahamas and the Caribbean I] south of Trinidad (Abbott 1974). Hatching as a veliger with a well I] developed protoconch may give some survival advantage in the open sea. Other mechanisms of dispersal, including passive I] drifting aided by mucous and byssal threads and rafting of I­ postlarvae and small adults have been implicated in the wide ,] geographical distribution of some small bivalves and gastropods I] species (Martel and Chia 1991 ). The effectiveness of these mechanisms depends on behavioral and growth characteristics of I] the juveniles. Four months old T niloticus juveniles, reared in the ,] laboratory (Heslinga and Hillmann 1981), are approximately 4 fold the size of T argyrostomus (this study) of same age. Differences in I] -] I" ,] 38 I] 1 J ] juvenile growth rates may determine the probability of effective ] juvenile dispersal by rafting and drifting. :l I] The larval shell

r I ~ i] The globose shape and irregular ornamentation of Turbo I] argyrostomus protoconch is usually a characteristic of non­ planktotrophic larval development (Thorson 1950, Shuto 1974). ,] However, the trochid, Calliostoma granulatum, with direct I] development has a regularly ornamented protoconch (Ramon 1990) a character associated with planktotrophy. The distinct sinusigera I] lib is a characteristic of larvae with extended, large or multi-lobed I] velar lobes, common in teleplanic larvae (Scheltema 1971, Robertson 1976, Laursen 1981). The velum of T. argyrostoma is '1 bi-Iobed and the protoconch is uncalcified, morphological I- adaptations for survival in the open sea (Scheltema 1971). The I] large yolky eggs and possible absorption of dissolved organic I] matter from seawater may enable non-planktotrophic larvae to live for extended periods therefore considerably increase their dispersal I] capability. I] I] J I ] 39 ]

i "1 J I] I] Diet and growth

I] During intennediate rearing, feeding Turbo mannoratus juveniles I­ on macroalgae improved growth up to 4 fold compared to feeding .] on sessile diatoms (Murakoshi et al. 1993). The size range of nine 1-. ] month old T. argyrostomus juveniles reared on macroalgae in this I ] study was 5.9-17.0 mm. This is higher than the 6.0-12.0 mm size range that was attained in 13 months, feeding on the sessile I] diatoms, Navicula rasmosissima, at the Okinawa Prefectural Sea I] Fanning Center (Murakoshi and Yamamoto 1991). Herbivorous gastropods will accept several species of macroalgae, but the effect I] on growth depends on species. Although both macroalgae species I] were readily taken by T. argyrostomus juveniles, after reaching 2.8 mm, red algae gave higher growth rates than green algae. The same I.] green algae, Viva pertusa, gave higher growth rates than the red I: ] algae, Gelidium amansii, for the abalone, H. discus hannai (Uki et al. 1986). Abalone usually prefer brown algae, particularly I] Undaria and Laminaria. However, Haloitis iris and H. australis I] ate Macrocystis pyrtfera, when abundant although they preferred I] red algae in New Zealand (Poore 1972). Juvenile and adult food preference are different in some species. The adult abalone, H. iris I] preferred M. pyrifera but juveniles reared on Graci/aria sp. grew I i 2 times faster than juveniles reared on M pyrifera (Tong 1982). '., ] I

i] 40 , I '] 1 J I] I] The stomach contents of adult T argyrostomus were found to contain a carrageenan like jelly substance and the remains of a red 1] algae, Gelidium sp. (Yamaguchi and Kikutani 1989). Unlike the

trochids which mainly feed on detritus, the turbinids are capable of ~]

holding and eating high vertical growing macroalgae by holding ~] them between the two halves of the specialized foot (Yamaguchi I] 1993).

I] Shell color depends on algal diet but varies depending on the I] gastropod species. The shell color of snails reared on red algae or a combination of red and green was the same, while snails reared on I ] green algae alone had a different shell color. The shells of T. l ] marmoratus juveniles reared on the green algae, U. pertusa were green, and white when reared on diatoms (Murakoshi et al. 1993). 1] .1 Shell color of abalone reared on green algae varies from green for H. diversicolor (Chiu 1981), whitish or greenish white for H - ] l ] rufenscens (Shibui ]97]) to bluish green for H. gigantea (Sakai • r 1960). Shell color of abalone reared on red algae varies from

, - ~] brown (Ino ]952, Leighton and Blootian 1963, Olsen ]968 and , Chiu 198]) to red (Leighton 1961, Olsen 1968) depending on - .] , speCIes.

_ ']

- I

- .' ] - . :l 41

! '] -!, '1 J I ] The physiological basis to explain the effect of diet on shell weight I] is not clear. Algal diet affected shell length and body weight

I ] increases differently in the abalone Haliotis discus hannai (Uki et 1~ - al. 1986). Viva pertusa gave a higher body weight increase, -1 relative to shell length increase. The red algae, G. amansii, gave a I· ] similar shell weight and body weight increase for the same abalone I] species. Mixed and green algae diets gave slower shell growth rates and higher shell thickness relative to red algae in this study. I] The effect of diet on shell development ofgastropods will therefore I] depend on species and probably on other rearing conditions.

I] Body and shell form affect predation and adhesion in the small I] intertidal gastropod, Nucella lapillus (Kitching et al. 1966). In a , wave exposed site, with few predatory crabs, thin shelled snails '- ] , with bigger feet and stronger adhesion power were favored. In a

,. ] sheltered site, with loose rocks which serve as shelter for crabs, , thick shelled snails were favored. Shell thickness may determine '] · predation mortality by crushing. The hemlit crab, Dardanus '] sanguinolentus may be a natural predator of the top shell (Nash • 1985). Although the hermit crabs did not attack juvenile green '] f snails released in shallow water (Nakamura 1992), they are 0] frequently observed occupying shells of the turbinids of all sizes. • The difference between the shell weight of juveniles collected ". , ]

oJ 42 ·

"J • ~l J ]

] from the reef and those reared in the laboratory, and the increasing ] trend suggest considerable shell weight difference in larger individuals. There is more overlap between the weights of small ] individuals collected in the reef and reared in the laboratory than ] between larger individuals (Fig. 10). Individuals with thin shells are either selectively predated on, leaving only those that develop ] thicker shells, or the shell thickness increase with size more rapidly ] on the reef, compared to the laboratory reared individuals. A thinner than natural shell may considerably affect the survival of ] juveniles released on the reef. ] I ] I]I . ] ] ] 'J 'J 'J :J 43 ']

" J ]

] Acknowledgrnents ] I thank my academic adviser, Dr. Yamaguchi for the constant .l . guidance, encouragement and moral support during this study and ] Iny stay in Okinawa. Assistance by many students in the Coral Reef Studies Laboratory, in particular Mr. Ozawa Hiroyuki, Ms. ] I Suzuki Yumiko, Mr. Nagata Tomofumi and Ms. Nomura Junko I ] during the collection of the study materials and their constant I ] concern and interest in this study is gratefully appreciated. Cheryl Lewis made useful comments on the initial manuscript, for which I I ] am deeply indebted. I thank Dr. Yamasu who assisted with the I ] SEM. Comments and suggestions by Dr. Van Woesik and Mr. Yoshino throughout the experiments and writing of the this report . '] are appreciated. I would also like to thank the director of the Kenya 0] Marine and Fisheries Institute, Dr. Okemwa, who kindly released me from my duties in order to undertake this course. Finally, the ] assistance by the Japan Ministry of Education, without which my ] study and stay in Okinawa would not have been possible, is gratefully acknowledged. I] ] .]

] 44 ] 1 References

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45 ill I

J Gillett, R. (1986a). The transplantation of trochus from Fiji to 1 Tokelau. UNDP/OPE Integrated Atoll Development Project. ] 28 pp.

~. Grange, K. R. (1976). Larval development in Lunella smaragda J (Gastropoda: Turbinidae). New Zealand Journal ofmarine ] and Fresh Water Research, 10 (3), 517-25. Hedley, C. (1917). The economics of Trochus niloticus. Australian J Zoologist 1,69-73. I I) Hadfield, M. G. (1977). Chemical interactions in larval settling of I) a marine gastropod. In: Marine natural products chemistry. D. J. Faulkner and W. H. Fenical (Eds), Plenum, New York. pp I] 403-13. I) Heslinga, G. A. (1980). Report on Palaus trochus hatchery project. The South Pacific Fisheries Newsletter, 20, 4-8. I] Heslinga, G. A. (1981). Growth and maturity of Trochus niloticus !- :, 1 in the Laboratory. Proceedings of the Fourth International Coral Reef Symposium, Manila, 1981, Vol. 1, 39-45. 'J Heslinga, G. A. and Hillmann, A. (1981). Hatchery culture ofthe '] conunercial top snail Trochus niloticus in Palau, Caroline Islands. Aquaculture, 22, 35-43. ] '] 'J .: ] 46 :l '1

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r 47 \] II 1 J Leighton, D. L. (1961). Observations of the effect of diet on shell J coloration in the red abalone, Haliotis rufescens Swainson. 1 The Veliger,4 (1), 29. , Lima, G. W. and Pechenik, J. A. (1985). The influence of 'J . temperature on growth and length of larval life of the J gastropod, Crepidula plana Say. Journal ofExperimental Marine Biology and Ecology, 90, 57-91 '] Lima, G. W. and Lutz, R. A. (1990). The relationship of larval '] shell morphology to mode of development in n1arine prosobranch gastropods. Journal ofMarine Biology, 70, 611­ J 37. J Martel, A. and Chia, F. (1992). Drifting and dispersal of bivalves J and gastropods with direct development. Journal of F-..xperimental Marine Biology and Ecology, 150, 131-147. J Moorhouse, F. W. (1933). The commercial trochus. Reports ofthe j Great Barrier ReefCommittee, 4(1), 23-9. Murakoshi, M. and Yamamoto. T. (1991). Experimental ] production of Turbo argyrostomus juveniles. Okinawa ] Prefecture Sea Fanning Center Report for the fiscal year 1987-1989 No.2, 73-74. ] ] . ]

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] Yamaguchi, M. and Kikutani, K. (1989). Feasibility Study of ] Green Snail Transplantation to the Federated States of ,.. Micronesia. A report prepared for Marine Resource Division, .. Department of Resource and Development, FSM. FAO/ ] South Pacific Aquaculture Development Project, Suva, 25 pp. ] Yanlaguchi, M. (1993). Green snail. In: Wright, A. and Hill, L. ] (Eds) Nearshore Marine Resources ofthe South Pacific. 497­ 512. V.S.P, F.A.A and I. C. O. D., Canada. ] ] ]

-~~ ..

~ ] ] ] ] ;] I -.: I ~I ,] 52 ] j -,