Data on pink abalone, Haliotis corrugata (Gray 1828) with infested shells from the San Benito archipelago, Baja California, Mexico.

ABSTRACT This work presents abundance estimations of pink abalone (Haliotis corrugata, Gray 1828) with shells infested by epibionts from the San Benito archipelago (Baja California, Mexico). The first quantifications, undertaken at the end of the 80s, revealed that the highest abundances of infested abalone were concentrated around one of the three islands of the archipelago, where notorious differences in aspect and sizes between infested and normal exemplars were observed. Between 1989 and 1992, infested pink abalones from this location were commercially extracted, attempting to clean up the population. Extractions resulted in the dominance of normal exemplars. Nevertheless, 10 y later (year 2001), the abundance of infested pink abalone was again higher than that of normal pink abalone, and normal and infested organisms seemed to be bathymetrically segregated. In year 2001, differences in aspect between infested and normal organisms remained notorious, but differences in size were practically absent. Most of the infested exemplars were adults. Two morphotypes of infested pink abalone were identified: (a) abalone which shells are dome-shaped and which growth is vertically directed, with the surface homogeneously covered by epibionts and (b) abalone with flat and oval-shaped shells, which growth is horizontally directed, and edges usually free of epibionts.

KEY WORDS: abalone, Haliotis corrugata, epibionts, shell, infestation, Mexico

INTRODUCTION

In Mexico, all abalone species have high economic value. Nowadays, the production of meat and shell is supported by green Haliotis fulgens (Philippi 1854) and pink abalone H. corrugata (Gray 1828). Sometimes, shells of green abalone can be as expensive as the meat itself, whereas those of pink abalone usually occupy the second place in importance, because they accumulate high densities of epibionts. The presence of epibionts does not affect the quality of the meat, but some can perforate the shell destroying the mother-of-pearl. This kind of damage is typical for the sponge Cliona (Kojima & Imajima 1982), the spionid polychaete Polydora (Clavier 1992), and some sabellid polychaetes (Leighton 1998, Kuris & Culver 1999).

The knowledge about the effect of epibionts over Mexican abalone species is scarce. Alvarez-Tinajero et al. (2000) reported about the incidence of the boring clam Lithophaga over pink abalone and its repercussions over the shell marketing at Cedros Island. Caceres-Martinez and Tinoco-Orta (2001) analyzed the effect of spionid and serpulid polychaetes over H. rufescens. Nothing is known about the frequency of infested abalone at wild populations. Ortiz-Quintanilla (1974) reported for the first time about a population of pink abalone from the middle island of the San Benito archipelago, where the incidence of infested abalone with sizes below the minimum legal size of capture (140 mm of shell length) was particularly high. Due to the appearance of the infested organisms, the local fishermen named them "dwarf abalones." Between 1989 and 1992 special permissions were granted for extracting infested abalones from the archipelago, attempting to clean up the population.

Here, we present the most important results of the quantifications of infested pink abalone undertaken between 1988 and 1991 at the San Benito archipelago, which up to now have remained unpublished. Additionally, results of the latest quantification undertaken in July 2001 will allow us to know about the persistence of the infestation phenomenon in this area.

MATERIALS AND METHODS

The most important features of the San Benito archipelago (Fig. 1) were described by Rodriguez-Valencia and Caballero-Alegria (2002). The first quantification of infested pink abalone was undertaken in February 1988, randomly locating sampling points inside the fishing area (0-30 m depth) around the three islands, and using a 1 [m.sup.2]-quadrant as sampling unit. All abalone found inside the quadrant were collected. In this survey, 200 [m.sup.2] were explored around the westerly island, 225 [m.sup.2] at the easterly island, and 450 [m.sup.2] at middle island. After this attempt, quantifications for infested pink abalone were restricted to the middle island (October 1989, March 1990, and October 1991) using the method described by Rodriguez-Valencia and Caballero-Alegria (2002). The most recent survey was done in July 2001, again applying the method described by Rodriguez-Valencia and Caballero-Alegria (2002), at 86 randomly located sampling points (Fig. 1).

[FIGURE 1 OMITTED]

RESULTS

The Abundance of Infested Pink Abalone During 1988 to 1991

In February 1988, the abundance of infested pink abalone at the middle island of the archipelago was higher (0.3 [abalone.sup.*][m.sup.-2]) than at the westerly and easterly islands (0.1 and 0.08 [abalone.sup.*][m.sup.-2], respectively). Sixty percent of all the pink abalone captured during this survey was infested, and 96% of them were smaller than the minimum legal size of capture (140 mm of shell length). In October 1989, the abundance of infested pink abalone at the middle island was 0.2 [abalone.sup.*][m.sup.-2], whereas at the other two islands was 0.1 [abalone.sup.*][m.sup.-2]. Ninety-eight percent of all the abalone collected around the middle island (36996 exemplars) was infested, and 89% of them were below the minimum legal size of capture. The most common epibionts observed over the shells were Corallina spp., hydrozoans, bryozoans, serpulid and spionid polychaetes, Cliona celata, and Litophaga plumula. Normal and in tested abalone differed markedly in size. In 1989, the modal size of infested organisms was 118 mm versus 140 mm in normal ones. In 1990, modal sizes were 124 mm versus 135 mm, respectively.

As a result of the special capture permissions for infested pink abalone granted to the local fishermen, 6.9, 12.9, 10.0, and 5.8 tones of meat were extracted from the middle island of the archipelago, in 1989, 1990, 1991, and 1992 respectively. In consequence, the abundance of infested pink abalone decreased (0.2 [abalone.sup.*][m.sup.-2] in March 1990 vs. 0.05 [abalone.sup.*][m.sup.-2] in October 1991), whereas the abundance of normal pink abalone remained between 0.2-0.3 [abalone.sup.*][m.sup.-2]. The contribution of normal pink abalone to the total catch increased from 2% in 1989, to 34% in 1992, whereas that of infested pink abalone below the minimum legal size of capture decreased from 40% to 4% for the same period. The modal shell length of infested pink abalone increased from 127 mm to 142 mm.

The Abundance of Infested Pink Abalone 10 Years Later

In July 2001, the abundance of infested organisms at the middle island was significantly higher than that of normal organisms (0.1 [abalone.sup.*][m.sup.-2] + 0.03 vs. 0.07 [abalone.sup.*][m.sup.-2] [+ or -] 0.03, respectively; [F.sub.(1,170)] = 5.0, P < 0.05). Fifty-seven percent of all the pink abalone collected (294 exemplars) was infested. The highest abundance of normal pink abalone was concentrated between 10-20 m deep (52% of their total abundance), whereas 40% of the total abundance of infested pink abalone was found between 20-30 m deep.

Differences in appearance between normal and infested pink abalone were still marked (Fig. 2). In dorsal view, infested shells differ by having only one pair of open respiratory orifices; in ventral view their edges lacked a marked Ca[Co.sub.3] accumulation band, reflecting a decreased horizontal growth. Nevertheless, differences between the mean shell lengths of normal and infested pink abalone were absent (127.6 mm [+ or -] 1.6 in infested abalone vs. 129.1 mm [+ or -] 2.2 in normal abalone; [F.sub.(1,167)] = 1.2, P > 0.05). Significant differences between the mean weight of muscle were also absent (143.7 g [+ or -] 7.0 for infested abalone vs. 145.6 g [+ or -] 9.0 for normal abalone; [F.sub.(1,167)] = 0.1, P > 0.05).

[FIGURE 2 OMITTED]

In pink abalone, the size of the muscular scar over the ventral face of the shell increases as the organism gets older; therefore, exemplars without or with small scars are younger than those with large and well-defined scars. This allowed us to build groups of relative age (Fig. 3): (1) Juveniles I, as exemplars, which shells lack of muscular scar; (2) Juveniles II, as organisms which shells have small muscular scars; and (3) Adults, as organisms which shells have large and well-defined scars. Four percent of the infested pink abalone was Juveniles I (120 mm [+ or -] 8.0 of mean shell length), 25% were Juveniles II (128.5 mm [+ or -] 3.0 of mean shell length), and 73% were Adults (128.6 mm [+ or -] 1.0 of mean shell length). The mean shell length between these three groups differed significantly ([F.sub.(2,166)] = 4.1, P < 0.05), but differences were caused by the mean length of Juveniles 1 (after Tukey HSD Test).

[FIGURE 3 OMITTED]

Two morphotypes were recognized among infested abalones (Fig. 4). Organisms with almost perfectly rounded and dome-shaped shells represent the first type. The surface of these shells is homogeneously covered by epibionts. Flatted and oval-shaped shells, without dome appearance, represent the second type. Edges of these shells are usually free of epibionts. Morphotypes were named "vertical growth" and "horizontal growth," respectively. Sixty percent of all the infested pink abalone belonged to "vertical growth" being their abundance concentrated between 10-20 m in depth (55% of their total). The rest of the infested pink abalone (40%) belonged to the "horizontal growth" type, being mainly concentrated between 10-30 m deep (89% of their total).

[FIGURE 4 OMITTED]

DISCUSSION

Unfortunately, raw data of the first surveys were not captured and got lost, being only summarized in technical reports of our institution. This hinders the extraction of more information through additional analyses. It is probable that this data set represents the unique documentation about the temporal persistence of the infestation phenomenon by epibionts in abalone, since any other similar information has been published until now. As far as we know, any other attempt to clean up populations of infested organisms, as the one described here, has been done. This strategy, applied until 1992, apparently succeeded because the incidence of infested organisms decreased and the abundance of normal pink abalone remained practically constant. Nevertheless, the absence of the raw data set hinders the statistical confirmation. Ten years later, the abundance of infested abalone again surpassed that of normal exemplars at the middle island of the archipelago, but both showed lower abundance levels than those observed during 1988 to 1991 due to the regional decline in abalone populations (Guzman-del-Proo 1992: Shepherd et al. 1998). Based on the yearly surveys undertaken at the archipelago (Rodriguez-Valencia & Caballero-Alegria 2002), we know that the incidence of infestation by epibionts remains highest around the middle island of the archipelago.

We believe that the abundance turnaround of infested abalone and the absence of differences in size between normal and infested organisms, observed in July 2001, are by-products of the fishery. This may have occulted because infested pink abalone are not preferred by commercial divers, because their shells will not sell well; therefore, they are focused on the extraction of normal pink abalone. This leads to the reduction of abundance of normal organisms and the reduction of the mean size of normal abalone to sizes similar to those of infested pink abalone. This is supported by findings of Rodriguez-Valencia and Caballero-Alegria (2002), indicating that between 1989 and 1999 the modal size of pink abalone at the archipelago has decreased.

We still do not have a clear explanation for the occurrence of two morphotypes of infested pink abalone. We hypothesize, that organisms showing "vertical growth" were infested at early ages and small sizes; therefore the epibionts crust covered the whole shell surface and hindered the continuation of horizontal growth. On the other hand, organisms with "horizontal growth" could have been infested when they were older and their shells were already oval-shaped. It is probable that the epibionts crust did not cover the whole surface, allowing the continuation of horizontal expansion. At the present, we are trying to find a method suitable to test this hypothesis.

This topic leads to the following interesting open questions that would be worthy to asses through experimental approaches: What are the reasons for the bathymetric segregations between normal and infested pink abalone, as well as between morphotypes of infested abalone? Are meroplanktonic larvae of some of the epibionts passively or actively retained around the middle island of the archipelago, leading to a higher larval settlement at this location? How comparable are densities and species composition of epibionts over the abalone shells with those over other hard substrata around the middle island (e.g. boulders, shells of other mollusks, and/or crabs exoskeletons)? Are there seasonal/yearly changes in the specific composition of epibionts over the pink abalone shells? Are there physiologic and/or genetic differences between normal and infested pink abalone? Are there chemical differences in shell composition between normal and infested abalone? Is the infestation degree dependent on ontogeny?

During these years we have been willing to find a method to get more accurate age estimations. Nevertheless, as Munoz-Lopez (1976) reported, deformed spires and damaged periostracs hinder the age determination using growth rings. Our relative age categories are similar to those defined by Munoz-Lopez (1976), after finding a good correlation between gonadal maturity and development of muscular scars (he used prejuveniles, lacking of muscular scar; preadults, with muscular scars slightly marked; and adults, with complete and well defined muscular scars). Talmadge (1964) also used similar classifications.

Fortunately, there are no differences in taste of the meat between normal and infested pink abalone. Nevertheless, shell deformations and shell weakness induced by boring epibionts (Oakes & Fields 1996) do have economic repercussions (Alvarez-Tinajero et al. 2000). We believe that the assessment of the remaining open questions and the analysis of temporal dynamics of infesting by epibionts at a fixed location are worthy tasks.

ACKNOWLEDGMENTS

We dedicate this work to the memory of our colleague A. L. Lelevier-Grijalva, who strongly contributed in the conception and development of the first versions of this manuscript. The authors sincerely thank our colleagues from the National Institute for Fisheries (Mexico) that helped during all the surveys. This work has been made possible thanks to the logistic support of the fishermen cooperative S.C.P.P. "Pescadores Nacionales de Abulon". A. Cota-Villavicencio provided valuable suggestions for this manuscript.

LITERATURE CITED

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F. CABALLERO-ALEGRIA, J. A. RODRIGUEZ-VALENCIA, ** AND J. CASTRO-GONZALEZ

Instituto Nacional de la Pesca, CRIP-Ensenada, Carretera Tijuana-Ensenada Km 107, Parque Industrial Fondeport, El Sauzal, Baja California, Mexico

** Correspondence author. E-mail: [e-mail]