Introduction

Molluscs mainly inhabit the marine environment, on coral and rocky substrates, soft bottoms, algae and even on other marine organisms (^{Ruppert & Barnes, 1996}; ^{Lodeiros et al., 1999}; ^{Prieto et al., 2001}). The organisms that live on marine bivalves are epibionts, both plants and animals, which live attached to the substrate, walk on it or crawl (^{Guartatanga et al., 2003}), while endobionts are those organisms that live below the external surface of their basibiont, which provides substrate for both epibionts and endobionts (^{Taylor & Wilson, 2002}). The organism serving as a basibiont usually has a large and strong shell that allows attachment or protection to other species (^{Schejter & Bremec, 2007}). Aggregation-forming bivalves are known as bioengineers as they create conditions for the maintenance of other organisms in shallow and deep environments (^{Turnipseed et al., 2004}; ^{Beck et al., 2009}, ²⁰¹¹).

The rock oyster Striostrea prismatica (Gray, 1825), is a bivalve that feeds on phytoplankton and suspended organic matter (^{Keen, 1971}), has an oval to dorsoventrally elongated, heavy and thick shell. The shell is brownish-purple on the outside and iridescent white on the inside with bright brown patches, the left valve has a purple muscular scar and the right one is slightly lighter, reaching a maximum length of 190 mm (^{Coan & Valentich-Scott, 2012}). This species is known as Crassostrea iridescens in the Mexican Fisheries Chart (^{DOF, 2017}), and is a synonym of S. prismatica. This mollusk is distributed along the eastern Pacific coast from southern Baja California to northern Peru (^{Mora, 1990}). It is found on shallow rocky intertidal and subtidal substrates (^{Fournier, 1992}; ^{Coan & Valentich-Scott, 2012}; ^{Loor & Sonnenholzner, 2014}).

The S. prismatica fishery is coastal artisanal, and is caught from 2 to 10 meters deep from Baja California to Oaxaca in the Mexican Pacific, as well as in other countries such as Ecuador (^{Argüello-Guevara et al., 2013}). S. prismatica has the highest catch volumes and is the main source of market supply in some coastal cities such as the municipality of Acapulco, Guerrero, as it is the species that is mostly caught by the Fisheries Production Cooperative Societies (FPCS). The amount of rock oysters caught per season is approximately 700 thousand organisms, leaving a total income of almost $6.5 million pesos to the cooperatives in the municipality (^{Castro-Mondragon et al., 2015}).

In addition to studies where it refers to taxonomy, economic aspects, reproductive, abundances or biogeographic distribution of the species (^{Ríos-González et al., 2018}). S. prismatica is an ecological engineer that forms large reefs where many other organisms inhabit and develop, but these interactions have not been studied for the species. This oyster possesses large, thick valves that serve as substrates for other mollusks. Studying these structures may allow the identification of substrate-organism relationships that will contribute to determine the ecological role of the rock oyster. In this context, the aim of the study was to analyze the mollusks associated with the shell (right valve) of S. prismatica, in addition to determining the species richness, relative abundance and frequency of occurrence of the species and families of associated mollusks, as well as estimating the diversity. This is the first record of this type in the Mexican Tropical Pacific with S. prismatica as the subject of study. This study will allow us to understand the ecological relationships that arise in the right valve of S. prismatica.

The Mexican Transitional Pacific (MTP) is a tropical sea influenced by the California Current. The MTP has a complex geomorphology, its narrow continental shelf is 10 to 15 km wide, and has several marine canyons from the coasts of Jalisco to Oaxaca. It is a region of high productivity due to its temperature, tropical marine fauna and an enormous diversity of species, with more than 189 species of mollusks (^{Wilkinson et al., 2009}).

Marine ecoregion number 17 of the MTP comprises the states of Jalisco, Colima, Michoacán, Guerrero, Oaxaca and the tip of the southernmost tip of Baja California Sur. This classification was given by the National Oceanic and Atmospheric Administration (NOAA) in 2002 (^{Wilkinson et al., 2009}).

Playa Corrales is located in the municipality of Cabo Corrientes in southeastern Jalisco (20°10’55’’ and 20°31’00’’ N; 105°10’00’’ and 105°41’25’’ W). The 98 % of the municipality of Cabo Corrientes has a warm sub-humid climate. The average annual temperature is 24.6°C, with a maximum of 36.0°C and a minimum of 13.3°C. The average annual precipitation is 1,624 mm (^{IIEG, 2018}).

Material and Methods

Methodology

This study was carried out on 12 right valves of rock oysters, these valves were chosen because this part of the body is where there is mostly sediment accumulation and the habitat becomes more complex, allowing the existence of a greater diversity and abundance of epibiont organisms, the left valve is cemented to the rock and the growth of epibionts is scarce. The oysters were acquired at a seafood market in Melaque Jalisco in June 2016, which came from Playa Corrales, in the Municipality of Cabo Corrientes, Jalisco, Mexico (Figure 1) and was the total number of oysters for sale. The specimens were fresh, recently extracted from the oyster bed, and it was observed that they had associated fauna on their valves. The size of the oysters corresponded to those normally caught for sale at this location > 60 mm. Each of the oysters was stored in plastic vessels with their respective labels and preserved in 96 % alcohol, which keeps the tissues in better condition for possible genetic analysis (^{Nagy, 2010}). They were then transferred to the Coastal Ecology and Sustainability laboratory of the Facultad de Ecología Marina - Universidad Autónoma de Guerrero for sample processing.

Figure. 1 Extraction site for Striostrea prismatica rock oysters analyzed in this study (Melaque, Jalisco). 

In the laboratory, the valves were disarticulated with the aid of a razor; the shapes were half-round or subtringular. Only the right (unattached) shell of the rock oyster S. prismatica was analyzed in the present research. The valves were cleaned of epiphytes, and mollusks associated with S. prismatica were separated with dissection material, quantified and classified as epibiont or endobiont according to their position on the valve. Further, they were identified with taxonomic keys of ^{Keen (1971)}, and the nomenclature was updated with the World Register of Marine Species (^{WORMS, 2020}). After the organisms were separated and the valves were cleaned, the length of each shell was measured with a digital caliper (0.1 mm).

Results

The analyzed valves of S. prismatica ranged in length from 61.1 to 84.2 mm. A total of 164 organisms of the phylum Mollusca associated with the 12 valves were quantified, which were represented by the classes Bivalvia (141 specimens) and Gastropoda (23 specimens), corresponding to 12 species of which 11 were considered epibionts and 1 endobiont (Table 1). For the class Bivalvia, 5 families, 7 genera and 8 species were identified (Figure 2). Gastropoda was represented by 3 families, 4 genera and 4 species (Figure 3).

Figure. 2 Bivalves associated with the rock oyster Striostrea prismatica in Corrales Beach, Jalisco, Cabo Corrientes, Mexico. A. Leiosolentus aristatus *. Scale bar = 2 mm. B. Divalinga peripavula. Scale bar = 0.5 mm. C. Brachidontes adamsianus. Scale bar = 2 mm. D. Zeptifer zeteki. Scale bar = 0.5 mm. E. Chama coralloides. Scale bar = 10 mm. F. Chama echinata. Scale bar = 10 mm. G. Pinctada mazatlanica. Scale bar = 1 mm. H. Striostrea prismatica. Scale bar = 10 mm. 

Figure. 3 Gastropods associated to the rock oyster Striostrea prismatica in Corrales beach, Cabo Corrientes, Jalisco, Mexico. A. Crucibulum concameratum. Scale bar = 2 mm B. Pilosabia trigona. Scale bar = 2 mm. C. Parvanachis pygmaea. Scale bar = 0.5 mm. D. Crepidula excavata. Scale bar = 10 mm. 

The family with the highest number of Bivalvia species was Mytilidae (3 species) and also obtained the highest relative abundance with 64 % (Table 2), while the most abundant species was the mussel Leiosolenus aristatus with 59.8 % and likewise the one with the highest frequency of occurrence with 91.3 %. Regarding Gastropoda was Calyptraeidae (2 species), in terms of relative abundance was Hipponicidae with 11.6 %. The most abundant species was the hoofed snail Pilosabia trigona with 11.6 % (Table 3).

An average species richness of 4.8 species/valve and an average abundance of 13.7 mollusks/valve were obtained. The total Shannon-Wiener diversity index was H’=2.2 bits/ind, while the Pielou’s evenness index (J’) was J’=0.6 (Table 4).

In this study, it was observed that the perforator bivalve L. aristatus caused a number of marks on the inner valve of S. prismatica (Figure 4), therefore, L. aristatus was considered endobiont. A possible association was observed between the number of marks and abundance of L. aristatus (Figure 5), with a Spearman correlation value of 0.42 (P = 0.41).

Figure. 4 Marks in the valve of the rock oyster Striostrea prismatica produced by the perforator Leiosolenus aristatus. A. Perforator L. aristatus, B. and C. Close view of the marks produced by L. aristatus in the external and internal valve, respectively, and D. Valve showing the mark produced by L. aristatus. 

Figure. 5 Scatter plot between number of the perforator Leiosolenus aristatus and number of internal marks in the right valve of the rock oyster Striostrea prismatica. 

Discussion

In this study it was determined that the most abundant class associated with S. prismatica was Bivalvia with 86 % of the organisms in relation to Gastropoda. The high dominance of bivalves compared to Gastropoda associated with other bivalve mollusks seems to be a common pattern. ^{De León et al. (1993)}, ^{Villafranca & Jiménez (2006)} and ^{Rodríguez Perera (2011)} found a higher abundance of bivalves with 51.8 %, 73.1 % and 61 %, in Spondylus princeps, Perna Viridis and Atrina seminuda respectively, in the Gulf of California (Mexico) and the North Coast of the Araya Peninsula (Venezuela). However, ^{Acosta et al. (2007)} determined that gastropods dominated with 68.5 % of organisms in Arca zebra in Chacopata, Venezuela. In addition, it was observed that bivalve valves tend to be more favorable for the settlement of bivalve organisms than gastropods.

According to the families present, Mytilidae was the most abundant, similar to other studies (^{Acosta et al., 2007}; ^{Rodríguez Perera, 2011}). The Mytilidae, Calyptraeidae and Ostreidae families present in this study have been commonly associated with other bivalves such as Pinctada imbricata, Arca zebra, Perna viridis, Atrina seminuda, Mytilus edulis platensis, Pinna nobilis, Spondylus princeps in Venezuela, Argentina, the Mediterranean Sea and Mexico (^{De León et al., 1993}; ^{Bremec & Roux, 1997}; ^{Villafranca & Jiménez, 2006}; ^{Acosta et al., 2007}; ^{Addis et al., 2009}; ^{Rodríguez Perera, 2011}; ^{Hernández-Ávila et al., 2013}). Other families have also been reported to be occasionally associated with bivalves, for example; Lucinidae, Pteriidae, Columbellidae and Chamidae in the basibiont species Pinctada imbricata, Arca zebra, Perna viridis, Atrina seminuda and Spondylus princeps (^{De León et al., 1993}; ^{Villafranca & Jiménez, 2006}; ^{Acosta et al., 2007}; ^{Rodríguez Perera, 2011}; ^{Hernández-Ávila et al., 2013}), the frequent association of these mollusc families with the different species of basibiont bivalves recorded, may be due to the wide geographic distribution of these families as well as the fact that both parties usually share similar habitat characteristics, which would promote the emergence of some kind of association.

In this study, 12 species of bivalves and gastropods were identified in only 12 organisms sampled from S. prismatica, while for Spondylus princeps 8 species in 30 organisms (^{De León González et al. 1993}), Arca zebra 50 species in 363 organisms (^{Acosta et al., 2007}), Pinna nobilis 2 species in 530 organisms (^{Addis et al., 2009}), Mytilus edulis platensis 24 species (^{Bremec & Roux 1997}), Perna viridis 47 species (^{Villafranca & Jiménez, 2006}), Arca zebra 19 species (^{Licet et al., 2009}), Atrina seminuda 59 species (^{Rodríguez Perera, 2011}), and for the aggregations of Pinctada imbricata and Arca zebra 40 species (^{Hernández-Ávila et al., 2013}). The highest richness of associated species belonged to the Gastropoda class (^{Vlilafranca & Jiménez 2006}; ^{Acosta et al., 2007}; ^{Licet et al., 2009}; ^{Hernández-Ávila et al., 2013}), however, in the present study the highest species richness belonged to Bivalvia as in ^{Bremec & Roux (1997)} and ^{Rodríguez Perera (2011)}.

Comparisons of the associated species were made with other species such as Spondylus princeps and Atrina seminuda, because there is no study related to S. prismatica. However, it must be considered that these species are very different morphologically and ecologically, since their range of distribution with respect to the depth and type of substrate they inhabit is different. S. princeps has long, thin spines favoring organisms to attach to it, and inhabits between 10 and 30 m depth in sandy substrates (^{De León González et al., 1993}). On the other hand, A. seminuda has a long byssus with which it remains fixed to the substrate and presents tubular spiny ornamentations on its shell and inhabits sandy-muddy bottoms (^{Rodríguez Perera, 2011}). Unlike S. prismatica which is attached to the rocky substrate, and with one of the valves exposed to a larger surface.

These differences can be marked by the type of sampling employed, sample size, sampling effort, type of environment, geographic area of the study and type of substrate offered by the basibiont valves. Most studies have collected mollusks by trawling (^{Acosta et al., 2007}; ^{De León Gónzalez et al. 1993}), which allows them to collect a large number of specimens, but in this study the oysters are extracted by means of a barrette since they are embedded in the rocky substrate. The sample size is related to the aim of the study, in this case the objective was to determine the species associated with S. prismatica, further studies should cover the spatial and temporal part of the associated fauna. The sampling effort to compare was adequate for this study. Studies that test specific hypotheses should make use of quadrats (^{Hernández-Ávila et al., 2013}, ^{Villafranca & Jiménez 2006}), trawls (^{Licet et al., 2009}, ^{Bremec & Roux 1997}) or non-extractive methods (^{Addis et al., 2009}), as long as the conditions of the marine environment allow it.

The total value for the Shannon-Wiener index corresponded to H’= 2.2 bits/ind (in 12 organisms), a value lower than that shown by ^{Acosta et al. (2007)}, in their analysis with Arca zebra as the object of study, in which they obtained for H’= 4.6 bits/ind (in 363 organisms), and for the Pielou evenness index J’=0.8, while in S. prismatica the species were found to be distributed mostly uniformly with a value of J’= 0.6, it can be observed that the values obtained are close to those obtained by Acosta et al. (2007) if it is considered that in the present study the sample size was smaller.

L. aristatus was the species with the highest frequency of occurrence in the analysis with 91.3 %, being also the only endobiont and species that has been found associated with other basibiont bivalves (^{Acosta et al., 2007}; ^{Hernández-Ávila et al., 2013}). However, in none of these cases was any damage to the basibiont shell reported, as it was observed in this study and where a total of 21 marks were quantified on the inner shell of 41.7 % of the valves. There are other endobionts that cause damage to basibiont bivalves, for example, ^{González Ortiz et al. (2017)} have reported that the polychaete Polydora sp. caused an average of 1.77 (013 blisters) blisters per valve in the clam Nodipecten subnodosus. In this study, an average of 1.75 (0-7 marks) marks per valve caused by the perforator L. aristatus on the right valve of S. prismatica was recorded in this study. Spearman’s correlation showed that the relationship between the increase in the number of perforating organisms and the increase in the number of internal marks is not significant, which may be due to the low number of organisms examined. Therefore, it is suggested to follow up this possible association with a greater number of organisms in the sample and a greater number of samples, in order to evaluate valve damage that the perforator bivalve L. aristatus may cause in S. prismatica.

Conclusions

Bivalves are more likely to be found associated with the basibiont S. prismatica than gastropods. This could be associated with the fact that larvae of some bivalve species prefer oyster shells as a substrate for attachment and development (^{Chuku et al., 2020}), but further studies are needed to verify this. The bivalve most commonly associated with S. prismatica was the mussel L. aristatus while the gastropod most commonly associated was the hoofed snail P. trigona. With respect to species richness, 91.7 % of the molluscan species associated with S. prismatica have not been reported to be associated with other bivalves. This is the first study that contributes to the knowledge of the associations (epibiont, endobiont), species richness, abundances, frequency of occurrence of mollusks associated with S. prismatica in the Mexican Tropical Pacific.

It is advisable to continue with the study of S. prismatica as an ecological engineer and creator of habitats in the Mexican Transitional Pacific, the evaluation of mollusks and other invertebrates such as annelids, crustaceans S. prismatica, abarcando and echinoderms associated with S. prismatica, covering different spatial and temporal scales. The extraction of S. prismatica leads to the destruction of these habitats that other species use as a place of refuge, breeding or feeding.