Will providing a filamentous substratum in the water column and shell litter on the bottom increase settlement and post-larval survival of the scallop Argopecten purpuratus?

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Abstract

The marked variability in the natural recruitment of Argopecten purpuratus, a common characteristic for many marine invertebrates with a pelagic larval stages, with important consequences for community functioning, is a problem for the fishery on this species. We ran experiments in the subtidal zone in Tongoy Bay, Chile, to test whether providing a filamentous settlement substratum in the water column and shell litter on the bottom would increase the settlement and post-larval survival of scallops. We placed collectors made of Netlon® 50 cm above the sand and mud bottoms, and three and a half months later there were significantly more scallop spat on the bottom under the collectors (38.5 ind m 2), than in areas without collectors (0 ind m 2), or in controls where collectors were installed but a bag around the collector prevented the juveniles from falling to the bottom (4.8 ind m 2). Also, the addition of either entire or broken scallop shells to the bottom resulted in increased settlement of juveniles on the bottom (33.7 ind m 2 with entire shells and 48.1 ind m 2 with broken shells), compared to plots where no shell debris was added (0 ind m 2). The 2 week survival rate of juveniles (< 3 mm shell height) added to plots covered with entire scallop shells (12.4%) and to plots covered with broken shells (15.1%) was greater than in plots where we did not add shells (3.5%). These results suggest that substrate availability explains spatial variability of recruitment for this species, while temporal variability (between years) is mainly the consequence of larval supply. The manipulation of substrates can locally increase settlement, but will not remove the temporal variability. Whereas our experiments provide useful insights into strategies for managing or establishing local scallop populations, experiments over a longer term and at a large scale are needed to further understand the community functioning in order to develop a strategy for managing this fishery resource.

Introduction

Recruitment variability, produced by diverse processes (larval supply and its underlying larval advection mechanisms, settlement cues, availability of suitable settlement sites, post-settlement mortality, etc.) is considered a key factor explaining the dynamics of near shore benthic populations of invertebrates with pelagic larval stages (Roughgarden et al., 1988, Botsford et al., 1994, Young, 1997, Morgan, 2001, Underwood and Keough, 2001), and has been a central issue in marine ecology in the last decades. The availability of suitable settlement sites, even when competent larvae are abundant, may limit larval settlement and thus affect recruitment (Morgan, 2001). On soft bottom communities biogenic reefs or habitats (mussels, oysters, polychaete tubes, maerl, etc.), and materials (as shells and shell litter), which increase habitat heterogeneity, favour settlement, post-settlement survival and recruitment (Lenihan and Peterson, 1998, Gutiérrez et al., 2003, Kamenos et al., 2004). Shells and shell litter provide substrate for attachment of epibionts, as algae, bryozoa and hydrozoa which are settlement sites for many larvae, provide refuges from predation, reduce physical or physiological stress, and influence the transport of solutes and particles in the benthic environment (Gutiérrez et al., 2003, Guay and Himmelman, 2004, Lenihan and Peterson, 2004). Human activities, principally the use of bottom fishing gear, can affect these materials, having important effects on populations, communities and biodiversity (Dayton et al., 1995, Lenihan and Micheli, 2000, Coleman and Williams, 2002, Lenihan and Peterson, 1998, Lenihan and Peterson, 2004). Artificially adding shells to the bottom, and thus recovering materials or reefs, has proven to be effective to recover the ecosystem services of these habitats, and thus biodiversity (Lenihan et al., 2001, Lenihan and Peterson, 1998, Lenihan and Peterson, 2004, Guay and Himmelman, 2004). Besides the natural materials, as shells, artificial materials, as the collector bags used for recruitment studies and in the aquaculture (Brand et al., 1980, Ventilla, 1982, Wilson, 1987, Ambrose and Lin, 1991, Ruiz-Verdugo and Caceres-Martínez, 1991, Peterson and Summerson, 1992, Pouliot et al., 1995, Arnold et al., 1998, Marelli et al., 1999), which artificially may recover functions of filamentous algae, hydrozoa or bryozoa as settlement substrata, could prove to be favourable for recruitment in natural habitats too. To evaluate the effect on recruitment of both types of materials, shells and artificial filamentous substrata, will be the issue addressed in the present paper.

Much discussion has been around of which of the processes, recognized to produce variability in the recruitment, is the most important (Morgan, 2001, Underwood and Keough, 2001). At least five processes are recognized: larval production, larval dispersal, larval survival while in the plankton, settlement, and growth and survival of recently settled juveniles (Underwood and Keough, 2001). For a benthic species, larval production will depend strongly on adult stocks, the dispersal and survival in the plankton on oceanographic dynamics, and the settlement and post-settlement survival mainly on bottom characteristics and community structure to which settlers arrive. If adult stocks do not vary, and bottom characteristics are proven to produce predictable effects on recruitment, the importance of dispersion and larval survival in the plankton as a factor causing variability could be assessed.

The commercially valuable scallop, Argopecten purpuratus, occurs in shallow bays from near Paita, Peru (5°S, 81°W), to Tongoy, Chile (30°S, 71°W). Its abundance fluctuates greatly, in part due to variations in recruitment related to El Niño events (El Niño Southern Oscillation, ENSO) which produce conditions favourable to “explosive” population growth (Wolff, 1988, Arntz and Fahrbach, 1996, Wolff and Mendo, 2000). As a result the fishery is often not sustainable (Navarro et al., 1991, Stotz and Gonzáles, 1997, Stotz, 2000, Stotz and Mendo, 2001), in spite of the fisheries regulations in Chile and in Peru aimed at preventing collapses (Stotz and Mendo, 2001). In recent years, techniques for mass culture of A. purpuratus, using Japanese technology, were developed to avoid the fluctuations of natural production. At present, most of the production of this species in Chile comes from growing scallops in suspended culture. The culture produces 4–5 times more scallops than the highest landings from the bottom in the past (Stotz, 2000). Also scallop stocks maintained in cultures in Tongoy Bay are at least ten times greater compared to former natural stocks in the Bay, showing fluctuations, but which in general maintain stocks at levels much above natural stocks in the past (Stotz, 2000). Given there are nearly 300 million scallops in culture in the bay, (Stotz, 2000), which represent ca 50% of the estimated carrying capacity of the bay for this scallop species (Uribe and Blanco, 2001), we expect there is an abundant larval production, much higher than formerly in the natural situation, thus probably not being an important source of recruitment variability. According to unpublished data, collected by aquaculture companies in the bay in their regular larval monitoring programs, densities during spawning periods are between 50–1500 larvae·m 3 during normal years. With ENSO values up to 6000 larvae·m 3 can be observed. For coastal areas, not associated to scallop cultures, larval densities between 30–200 larvae·m 3 were reported for normal years, increasing up to 1000–4000 larvae·m 3 during years with ENSO (Narvarte et al., 2001). The larval period can last between 16 to 25 days, depending upon water temperature and the amount and quality of food (von Brand et al., in press). Retention of larvae, and thus larval supply within the bay is probably very variable, as water exchange of the bay may vary greatly, depending on wind intensity and direction. The Bay exchanges its entire water every 1.5 to 20. 6 days depending on wind intensity and direction (Uribe and Blanco, 2001).

Considering the temporal variability of spat obtained in collector bags in aquaculture (Stotz, 2000), settlement within the bay shows to be very variable. Many interacting factors govern recruitment of scallops and these include the degree of synchronous spawning to ensure fertilization, favourable food and physical conditions for the larvae, and the role of currents in bringing competent larvae to appropriate settlement sites (Eckman, 1983, Eckman, 1996, Orensanz et al., 1991, Roberts et al., 1991, Hurlburt, 1992, Anderson and Underwood, 1994, James and Underwood, 1994, Keough and Raimondi, 1995, Marelli et al., 1999, Arnold et al., 1998). Once the larvae arrives to a potential settlement site, temperature, depth, food availability, salinity, turbidity, and the occurrence of competitors and predators affect the success of scallop settlement (Brand, 1991). Another important factor is the availability of suitable substrata for metamorphosis and early survival (Ambrose et al., 1992, Defeo, 1996). The preferred settlement substrata reported for scallops include filamentous algae and invertebrates, small rocks and shells of conspecifics (Caddy, 1972, Thayer and Stuart, 1974, Brand et al., 1980, Pohle et al., 1991, Minchin, 1992, Stokesbury and Himmelman, 1995, Arnold et al., 1998, Marelli et al., 1999). Although few studies have specifically examined the preferred natural settlement substrata for A. purpuratus, recently settled juveniles have been observed on the alga Rhodymenia sp. (Hogg, 1977), the bryozoan Bugula sp. (Di Salvo et al., 1984), small algal covered stones (Wolff and Alarcon, 1993), tubes of the polychaete Diopatra sp. and the sea grass Heterozostera tasmanica (Aguilar and Stotz, 2000).

Studies of numerous scallop species demonstrate that artificial collectors made with filamentous plastic materials are effective at capturing spat (Pecten maximus, Brand et al., 1980, Wilson, 1987; Chlamys opercularis, Brand et al., 1980; Placopecten magellanicus, Pouliot et al., 1995; Aequipecten opercularis, Acosta et al., 1999; Argopecten irradians,Ambrose and Lin, 1991; Argopecten circularis and Pecten vogdesi, Ruiz-Verdugo and Caceres-Martınez, 1991). Also, the collector material used for the Japanese scallop Patinopecten (Mizuhopecten) yessoensis (Ventilla, 1982) has been shown to be equally effective for A. purpuratus (Illanes et al., 1985, Pereira et al., 1987, Avendaño and Cantillánez, 1989). Such techniques support large scallop culture industries. Artificial filamentous substrata have also been used as collectors in assessing the presence of larvae in the water, in quantifying recruitment levels, and in estimating the stock levels required to sustain fisheries, for example for the scallops Chlamys varia and P. maximus (Cano et al., 1999), Aequipecten tehuelchus (Ciocco and Monsalve, 1999) and A. irradians (Peterson and Summerson, 1992, Arnold et al., 1998, Marelli et al., 1999).

In the present study, we predict that natural settlement and early survival of A. purpuratus can be increased by providing filamentous substrata in the water column and by adding shell litter (entire and broken scallop shells) to soft bottoms that are normally unsuitable for settlement. The shell litter will be advantageous to settlers as it offers substrate to attach to, prevents to become buried in the sediment and confers refuge from predators. The area chosen for the study, Puerto Aldea, at the southern end of Tongoy Bay (Chile), is habitat for a natural scallop bed that is managed and harvested by local fishers under a recently developed resource management legislation (the fishers have acquired property rights over the bed). In this area the recruitment has fluctuated greatly, indicating that the larval production from cultured scallops in Tongoy Bay does not always lead to recruitment into the natural bed (Stotz, 2000), suggesting the importance of other processes, not merely the larval supply, to affect recruitment success, the question this paper deals with.

Contributions to the knowledge regarding settlement will favour aquaculture, but also the development of strategies for the recovery of natural beds, which remain in very bad shape (Stotz, 2000). While aquaculture recovered and increased production of scallops, natural beds were completely destroyed (Stotz, 2000), raising the question regarding conservation of the species and its related community. Extensive culture operations can lead to problems, such as pollution and mass mortalities from disease (Ventilla, 1982). Also, there may be a loss of genetic variability of the scallop due to the selection involved in the production in the water column or to the use of a limited brood stock for producing juveniles in the hatchery (Stotz, 2000). Thus, it is desirable to re-establish and manage natural scallop beds to maintain genetic variability of the scallop (Avendaño and Cantillánez, 1997, Stotz, 2000) and in general to re-establish biodiversity. It is preferable to make use of natural recruitment in re-establishing natural scallop beds, which makes the study involved in that process, necessary.

Section snippets

Study area

The study was carried in front of Puerto Aldea (30°17′S;71°36′W; Fig. 1) which is a small fishing village located in the southern side of Tongoy Bay, Chile and 60 km south of Coquimbo. The area consists of four distinct habitats, of which the two naturally least attractive for scallop settlement where used for the experiments: (A) a sand bottom habitat, between 6 and 11 m, made of coarse sand (grain diameter of 0.775 mm), with some patches of sand-tube-forming polychaetes (Diopatra sp.) and

Effect of suspending a filamentous spat collector above the bottom

Experiment 1 showed there was increased settlement of scallops on the bottom when a Netlon® collector was placed above the bottom, compared to when a bag was placed around a suspended collector to prevent spat from dropping from the collector (control 1) or when there was no collector at all (control 2). For the two bottom types together, there were on average 38.5 spat m 2 on areas below a collector compared to 4.0 spat m 2 in control 1 and none in control 2 (Fig. 4). The ANOVA indicated

Discussion

Our experiments show that the number of scallops settling onto sand and mud bottom can be increased by suspending a filamentous substratum in the water column above the bottom, and also by adding shell litter to the bottom. We further show that the addition of shell material to the bottom increases post-settlement survival (culture reared juveniles added to the bottom in our trials). These trials provide insights which should be useful in planning methods for enhancement of scallop populations,

Acknowledgements

We are grateful to friends and colleagues who assisted in this study. Nelson Plaza and Ricardo Hidalgo, directives of the Fisher Association of Puerto Aldea, allowed us to dive and work in their Management Area. María Antonieta Zuñiga, Nicole Piaget, Pablo Araya, Claudio Cerda and Juan Carlos Flores were of great help in different parts of the field and laboratory work. Joel Barraza and Carlos Solar from the Aquaculture Laboratory provided spat for the experiments from their cultures. The

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