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Larval settlement of haliotis tuberculata coccinea in response to different inductive cues and the effect of larval density on settlement, early growth, and survival.

ABSTRACT Settlement and metamorphosis of Haliotis tuberculata coccinea larvae were examined in the presence of different settlement cues reported effective in larval settlement of other abalone species (crustose coralline algae, Ulvella lens, conspecific mucus, [gamma]-aminobutyric acid, and 4 benthic diatom species). In addition, larval density effect was tested on crustose coralline algae substrate. Larval settlement was highest on crustose coralline algae followed by U. lens. Settlement was very low on conspecific mucus and [gamma]-aminobutyric acid, varying between 1% and 2%. U. lens inoculated with the diatom Navicula incerta induced a reduced settlement of 9% compared with the 22% obtained on films of U. lens alone. The settlement induction efficiency of all the benthic diatoms tested (Amphora sp., N. incerta, Proschkinia sp. and Nitzschia sp.) was very low and not significantly different among diatom species. Larval settlement at 48 h after addition and survival after l mo were higher for the lower larval density, whereas postlarval growth rates were not influenced by larval density.

KEY WORDS: abalone larvae, crustose coralline algae, Ulvella lens, diatoms, GABA, mucus, settlement, early growth, survival, Haliotis tuberculata coccinea

INTRODUCTION

The induction of larval settlement is a critical stage in abalone seed production. Abalone larvae require specific cues for attachment and stimulation of metamorphosis (Morse & Morse 1984, Roberts 2001). The absence of such cues leads to low settlement and survival rates in early post larvae (Searcy-Bernal et al. 1992, Slattery 1992, Daume et al. 1999, Roberts et al. 1999, Takami et al. 2002).

Substances that have been reported to induce settlement in abalone larvae include crustose coralline algae (CCA), benthic diatom biofilms, spores of the green algae Ulvella lens, chemicals like [gamma]-aminobutyric acid (GABA), abalone mucus trails, or bacterial films (Morse & Morse 1984, Searcy-Bernal et al. 1992, Slattery 1992, Seki 1997, Takami et al. 1997, Bryan & Qian 1998, Roberts 2001, Gordon et al. 2004, Daume 2006). Published literature documents many contradictions and wide variation in abalone settlement rates, on the settlement cues previously cited, depending on the abalone species or the methodology selected for each study.

On one hand, benthic diatom biofilms have been traditionally used in abalone hatcheries worldwide to induce larval settlement, but its effectiveness is unpredictable and larval settlement rates are frequently low (1-10% of larvae) (Daume et al. 2000). On the other hand, abalone hatcheries in Japan successfully settle abalone larvae (Haliotis discus hannai) on the green algae U. lens (Takahashi & Koganezawa 1988) and its use has been spread recently to other countries.

In addition, abalone settlement rates and early growth and survival have been recently suggested to be markedly affected by larval and postlarval density (Daume et al. 2004).

Because Haliotis tuberculata coccinea Reeve, 1846 is a new candidate species for aquaculture, studies related to that species are scarce and have focused on spawning techniques (Pena 1986, Viera et al. 2003), larval development (Courtois de Vicose et al. 2007), ecology (Perez & Moreno 1991), as well as culture techniques and nutrition (Toledo et al. 2000, Viera et al. 2005). To date, there is no information available about the settlement process of its larvae or on the adequate settlement cues and larval densities, and their effect on postlarval growth and survival.

Hence, a better understanding of H. tuberculata coccinea settlement processes and the identification of a reliable approach for efficient recruitment and early growth are therefore of great importance for furthering the development of culture techniques and the production of this species. Both arouse public interest, because they would contribute to the recovery of wild H. tuberculata coccinea populations.

The current study investigates the settlement induction efficiency of substrates, reported to induce settlement in other abalone species, on H. tuberculata coccinea larvae to identify suitable settlement substrates for this abalone species. The objectives of the current study were (1) to evaluate the effectiveness of GABA, abalone mucus, CCA, U. lens, Navicula incerta, and its combination with U. lens on larval settlement of H. tuberculata coccinea; and (2) to assess the efficiency of 4 strains of diatoms for larval settlement of H. tuberculata coccinea. This study also examines whether larval density influences overall settlement rate and later postlarval performance.

MATERIALS AND METHODS

Experimental Protocol

Captive H. tuberculata coccinea broodstock were kept in 60-L tanks with a flow-through system at the Instituto Canario de Ciencias Marinas (Canary Islands, Spain). Ripe H. tuberculata coccinea were induced to spawn (male to female ratio, 1:2) by the hydrogen peroxide technique (Morse et al. 1977), and all the larval experiments were run at the Instituto Canario de Ciencias Marinas in 2008. Larvae used in each experiment were from the same batch and were obtained from fertilized gametes from various males and females. They were judged to be competent for settlement when the third tubule of the cephalic tentacle could be observed (Hahn 1989, Courtois de Vicose et al. 2007).

Settlement plates consisted of 50-[m.sup.2] plastic squares colonized by settlement cues to be tested for experimental plates; control plates were not colonized. Each replicate consisted of 4 settlement plates placed vertically in 12-L containers filled with 1-[micro]m filtered seawater, supplied with low aeration. After 24 h of introduction of the larvae, flow was initiated at a 1% exchange rate per hour and was increased up to a 20% exchange rate per hour after 72 h. The seawater outlet was fitted with 125-[micro]m mesh screens to prevent the loss of larvae. Seawater temperature in the rearing containers was 19 [+ or -] 0.5[degrees]C, with an artificial photoperiod of 12 h light/12 h dark provided at a light intensity of 2,000 lux, measured using a digital light meter (HT170N, HT ITALIA, Italy).

Settled larvae were counted, on every settlement plate of each replicate (a total of 12 per treatment), under a dissecting microscope 48 h after the larvae were added. Plates were kept immersed at all times during observation. Larvae were considered as settled when permanently attached to the substrate after shedding the velum to complete metamorphosis.

Algal Cultures

Four species of diatoms N. incerta, Proschkinia sp., Nitzschia sp., and Amphora sp. were grown in f/2 medium (Guillard 1975) plus silicate at ambient temperature and under continuous light of 62 [+ or -] 8 [micro]mol photon/[m.sup.2]/sec. Photon flux density (irradiance) was measured using a digital light meter (HT ITALIA). The cultures were not axenic.

For each diatom treatment, individual diatom species were cultured with initial inoculums of [10.sup.5] cells/mL for 5 days and allowed to attach to settlement plates until they reached a density of approximately [10.sup.5] cells/[m.sup.2]. For the CCA treatment, settlement plates were left to be colonized by CCA in nursery tanks until reaching approximately 57% cover.

Ten-day-old U. lens germlings, which colonized the settlement plates with 27% cover, were obtained from mature (spore-producing) U. lens according to the methods for spore collection of Takahashi and Koganezawa (1988).

To colonize the plates with N. incerta in combination with U. lens, settlement plates with germlings of U. lens were placed in N. incerta culture and grown for 5 days so that they were inoculated with the diatom at a density of approximately [10.sup.5] cells/[m.sup.2].

Larval Settlement

Four different experiments were conducted to test GABA, abalone mucus, CCA, U. lens, the combination of U. lens and N. incerta, 4 different diatoms and 2 larval densities on larval settlement of H. tuberculata coccinea. Algal colonization of experimental plates is described earlier. Regarding the conspecific mucus treatment, specimens of H. tuberculata coccinea (3-4-cm shell length) were allowed to crawl on the settlement plates for 24 h before the introduction of the larvae.

In the first experiment, the larval response to 1 [micro]M GABA (Morse et al. 1979), conspecific mucus, U. lens, and CCA was tested. Each type of substrate was tested in triplicate at a larval density of 2,000 larvae/12-L container, representing 10 larvae/ [m.sup.2] of substrate.

The following treatments were tested during the second experiment: a negative, bare control; U. lens, diatom film of N. incerta; and U. lens in combination with N. incerta and as a positive control of the CCA. Each type of substrate was tested in triplicate with a larval density of 2,000 larvae/12-L container representing 10 larvae/[m.sup.2] of substrate.

In the third experiment, settlement plates colonized by CCA were tested against settlement plates colonized by monospecific diatom films of N. incerta, Proschkinia sp., Nitzschia sp., and Amphora sp. Each type of substrate was tested in triplicate at a larval density of 2,000 larvae/12 L, representing 10 larvae/[m.sup.2] of substrate.

In the fourth experiment, 2 larval densities were tested: 2,000 larvae/12 L and 200 larvae/12 L, representing 10 larvae/[m.sup.2] and 1 larva/[m.sup.2] of CCA substrate, respectively.

Postlarval Growth and Survival

Postlarvae from the fourth larval settlement experiment were fed weekly with 200 mL mixed diatom inoculum ([10.sup.6] cells/mL) cultured as described earlier. Their growth and survival were followed 4 wk after settlement. The number of live postlarvae was counted on every settlement plate of each replicate (a total of 12 per treatment) using a dissecting microscope at weekly intervals. The shell length of 10 randomly selected postlarvae per treatment was measured weekly with a profile and measuring projector (model PJ-H3000, MITUTOYO, Japan). Plates were kept immersed at all times, except during observation and measurement, and were replaced immediately thereafter.

Daily growth rate was calculated according to the formula

Lf - Li / t

where Lf is final shell length in micrometers, Li is initial shell length in micrometers, and t is time in days.

Estimates of Cell Density and Percent Cover of Algae

Ten randomly chosen fields of view of the settlement plates were photographed at a magnification of 400x. Number of diatoms cells per square centimeter as well as percent cover of CCA and U. lens were calculated by processing the images with Image J Software (National Institutes of Health, USA, Image J 1.42q).

Data Analysis

Statistical analysis was performed using the Statgraphics Plus 5.1 software. One-way analyses of variance (ANOVAs) were performed for settlement rate, survival rate, and daily growth rate. Data showing significant differences (P < 0.05) were analyzed by paired comparisons using Tukey's HSD test. Equality of variance was assessed with Bartlett's test. When data were not normally distributed, a nonparametric one-way ANOVA on Kruskal--Wallis ranks was tested.

RESULTS

Larval Settlement

The number of settled larvae was significantly higher on the CCA than on U. lens ([F.sub.4,10] = 142.97, P = 0.000), and both treatments induced a significantly higher settlement (P < 0.05) of larvae than mucus film, GABA, and the control (Fig. 1). After 48 h, a settlement rate of 31% was achieved on CCA, followed by a settlement rate of 22% on U. lens, and less than 2% on mucus film, GABA, and the control. There was no significant difference between the mucus film, the GABA treatment, and the control (P > 0.05).

[FIGURE 1 OMITTED]

A similar result was obtained when larval settlement was compared between CCA, U. lens, U. lens combined with N. incerta, and a film of N. incerta. A significantly higher number of larvae settled on CCA ([F.sub.4,10] = 29.57, P = 0.000) compared with U. lens, and both treatments induced a significantly higher settlement (P < 0.05) of larvae than U. lens inoculated with N. incerta, a film of N. incerta, and the control (Fig. 2). Settlement was significantly higher (P = 0.000) on plates with U. lens combined with N. incerta than on film of N. incerta alone, and the control. Settlement rates of 34% on CCA, 22% on U. lens, 10% on U. lens inoculated with the diatom N. incerta, and 1% on a film of N. incerta were determined after 48 h.

[FIGURE 2 OMITTED]

In the third experiment, significantly more larvae settled on CCA than on films of N. incerta, Proschkinia sp., Nitzschia sp., or Amphora sp. ([F.sub.5,12] = 215.71, P = 0.000). Indeed, a settlement rate of 30% was calculated on CCA after 48 h whereas settlement on the monospecific diatom films remained less than 1%. There was no significant difference in the settlement rates between the monospecific diatom films and the control (P > 0.05; Fig. 3).

Settlement of H. tuberculata coccinea larvae was significantly higher on the low-density treatment when induced to settle on CCA, with 57% average percentage cover ([F.sub.1,4] = 17.61, P = 0.013; Fig. 4). Thus, after 48 h, 49% of larvae settled in the low-density treatment whereas only 30% of larvae settled in the high-density treatment.

Postlarval Growth and Survival

There was no significant difference in survival ([F.sub.1,4] = 2.75, P = 0.17) between high- and low-larval density treatments on CCA, although postlarval survival was slightly higher at the lower larval density, with 73.94 [+ or -] 3.42% survival 4 wk after settlement (Table 1; Fig. 5).

After week 4 of the experiment, postlarvae grown on CCA substrate, at low and high density, and fed weekly 200 mL [10.sup.6] cells/mL diatom mix (N. incerta, Proschkinia sp., Nitzschia sp., and Amphora sp.) reached an average of 891 [micro]m and 758 [micro]m in shell length, respectively (Fig. 6). When daily growth rates were analyzed, there was no significant difference between the low- and high-density treatments during the 4 wk after settlement (([F.sub.1,18] = 1.13, P = 0.30; Table 1).

DISCUSSION

The current study was performed to test, for the first time, the settlement induction efficiency of substrates reported to induce settlement in other abalone species on H. tuberculata coccinea larvae and to determine their suitability for this abalone species.

The results obtained demonstrate that larval H. tuberculata coccinea will settle at a higher rate on CCA than all other substrates tested, confirming that CCA are among the best settlement-inducing substrates (Roberts 2001). The settlement rate on CCA (30-34%) is similar to that reported by Daume et al. (1999) for H. rubra larvae (25%).

[FIGURE 3 OMITTED]

[FIGURE 4 OMITTED]

Larvae of the same batch, and across experiments, have also settled well on U. lens. These results are in concordance with the settlement rates obtained for H. rubra on U. lens (20%) as noted by Daume et al. (2000). The settlement rates observed on U. lens that was inoculated with N. incerta (10%) are consistent with the results of Daume et al. (2000) (9%), lending support to the conclusion that diatom colonization on U. lens reduces settlement induction potential of this alga.

The settlement trials on conspecific mucus led to low settlement rates. Similarly, Bryan and Qian (1998) also reported low settlement rates (12%) on conspecific mucus alone whereas they observed increased settlement rates (> 50%), as did Slattery (1992), on a diatom plus conspecific mucus treatment. Hence, the absence of diatoms in the conspecific mucus treatment of the current study could probably explain the low settlement rates obtained.

The controversial efficiency of GABA as settlement inducer (Roberts 2001) is reflected in this study given that the low settlement rates observed, with 1 [micro]M GABA in this study, are consistent with the poor results from GABA reported by Slattery (1992) but contradictory to the ones of Searcy-Bernal et al. (1992). In all cases, the experiments were conducted in the absence of antibiotics, at 1-[micro]M GABA concentration and with settlement plates previously colonized by diatoms. According to Searcy-Bernal and Anguiano-Beltran (1998), these last 2 factors reduce GABA's efficiency as an inducer of larval settlement. In addition, GABA's efficiency could be species dependent, as reported by Roberts and Nicholson (1997) for H. iris and H. virginea.

[FIGURE 5 OMITTED]

Not many diatoms are known to be consistently suitable for abalone larval recruitment (Roberts 2001). The low settlement observed on monospecific diatom films across experiments, a system traditionally used in abalone hatcheries, is consistent with the one reported by Daume et al. (1999) for H. rubra and is unlikely to be related to diatom abundance, as densities of [10.sup.5] cell/[m.sup.2] were reached. More likely explanations involve the age, or growth phase, of the diatom biofilm, because cells were only allowed to grow for 5 days to reach this density. On the other hand, Kawamura and Kikuchi (1992) obtained a successful settlement of H. discus hannai postlarvae with N. ramosissima. Nevertheless, other types of diatom could be successful for the settlement requirements of H. tuberculata coccinea.

In the current study, survival was not significantly higher at the low larval density, but was higher than that obtained by Gordon et al. (2006) using much higher larval densities on mixes of diatoms. The effect of larval density on settlement was tested on CCA substrate, and this experiment also showed significantly higher settlement for the low-density treatment. These results are bolstered by those of Daume et al. (2004), who showed higher settlement of H. rubra at low larval density on U. lens.

[FIGURE 6 OMITTED]

Growth rates obtained in the current study were within the range reported in earlier studies for other abalone postlarvae conducted by Takami et al. (1997) and Gordon et al. (2006), but lower than the ones obtained by Strain et al. (2006) and Viana et al. (2007). These differences could be explained considering that the settlement substrates, diatom species as well as their densities, and finally the larval densities tested varied among all these experiments. Moreover, the sloughing of surface layers observed for most crustose species (Giraud & Cabioch 1976) could be contributing to the reduction of attached diatom cells on the CCA substrate and might therefore affect growth rates of postlarvae, given that corallines present a low food value for abalone postlarvae (Roberts 2001).

This study demonstrates that larvae of H. tuberculata coccinea will settle at a high rate on CCA and suggests that U. lens, which is easier to manage than CCA, can be used as an efficient and consistent settlement substrate for H. tuberculata coccinea larvae. To the contrary, none of the diatom species tested were successful in the induction of H. tuberculata coccinea larval settlement. In addition, this study shows that larval density has an effect on settlement rates and postlarval survival of H. tuberculata coccinea.

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GERCENDE COURTOIS DE VICOSE, * MAPI VIERA, AMAIA BILBAO AND MARISOL IZQUIERDO

Grupo de Investigacion en Acuicultura (GIA) Instituto Canario de Ciencias Marinas (ICCM) & Instituto Universitario de Sanidad Animal (IUSA), PO Box 56, 35200 Telde, Las Palmas, Islas Canarias, Espana

* Corresponding author. E-mail: gtricor@hotmail.com
TABLE 1.
Mean daily growth and survival rates of H. tuberculata
coccinea postlarvae on crustose coralline algae at high and low
larval density (n = 3 and n = 10, respectively).

                                       Daily Growth
              Survival Rate           Rate at Week 4
Larval          at Week 4           ([micro]m/day (1)
Density      (% [+ or -] SE)           [+ or -] SE)

High       58.64 [+ or -] 8.58     19.58 [+ or -] 1.67
Low        73.94 [+ or -] 3.42     23.04 [+ or -] 4.47
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Author:De Vicose, Gercende Courtois; Viera, Mapi; Bilbao, Amaia; Izquierdo, Marisol
Publication:Journal of Shellfish Research
Article Type:Report
Geographic Code:1USA
Date:Nov 1, 2010
Words:4076
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