Taxonomy, Identification, and Distribution

Oysters are members of the family Ostreidae (Rafinesque-Schmaltz 1815), order Ostreida (Férussac 1821–1822), subclass Pteriomorphia (Beurlen 1944), and class Bivalvia (Linnaeus 1758). Sixteen living genera with about 75 species are known. Six genera are currently documented in the tropical eastern Pacific. The family occurs as early as the Triassic period.

Despite being one of the most common and economically important bivalve molluscs consumed around the world, oysters are exceptionally difficult to identify. Oyster shell shape is greatly influenced by the substratum to which they attach. They also are frequently covered with epibionts, including other oysters. That being said, there are reliable shell features that will assist in the identification of most specimens.

Some molecular studies have reorganized the taxonomy of oysters in the eastern Pacific. For instance, Polson et al. (2009) demonstrated that Ostrea lurida (Carpenter 1864) and Ostrea conchaphila (Carpenter 1857) are two distinct species despite having nearly identical shell morphology. Raith et al. (2016) have further defined the distribution of this species complex, as well as synonymizing the genus Myrakeena (Harry 1985), and the species Ostrea tubifera (Dall 1914). It is hopeful that these landmark studies will be pushed forward to all oysters in the eastern Pacific, and will also yield additional morphological characteristics to separate them.

Additional genetic studies have led to the creation of new generic and higher level names in the Ostreidae (Salvi & Mariottini 2016, Guo et al. 2018). Following suggestions by Bayne et al. (2017), the generic allocations have been maintained as outlined in Coan and Valentich-Scott (2012) and Valentich-Scott et al. (2020) until the taxa defined in these genetic studies have stabilized. A diagnostic characteristic for each species and an explanation of the current taxonomy are provided. Detailed descriptions of each species are modified from Valentich-Scott et al. (2020), Coan and Valentich-Scott (2012), and Coan et al. (2000).

In the taxonomic synonyms in the following text, we use the term “of authors.” This implies that an author or authors have misapplied a species name in the literature.

Description of Shell Characteristics

Identification of oyster shells requires an understanding of a few specific terms (Fig. 1A–E). The left/right orientation of an oyster shell is not immediately apparent. The right valve is almost always the upper valve, whereas the attached valve is almost always the left valve (Fig. 1D), and the convexity is frequently a useful diagnostic characteristic. The height of the shell extends from the beaks above the hinge margin (dorsal) to the opposite (ventral) side (Fig. 1E). The length is the maximum dimension approximately 90° from the height measurement. In oysters the height is usually greater than the length. The adductor muscle scar is mostly posterior of the midline of the shell (Fig. 1E). Thus, the left valve has the adductor muscle scar mostly to the left of the midline, and the right valve has a scar mostly to the right of the midline.

The amount of shell attachment to the substratum is sometimes diagnostic. Some species have only a slight area of attachment on the left valve, whereas others have extensive areas of attachment. The shell margin might be strongly undulate (Fig. 1C), or not undulate (Fig. 1D). The exterior valve sculpture can be useful in identification if not heavily eroded or encrusted with epibionts. Several species have strong radial plicae (ribs) (Fig. 5E, F, I), some have lamellate sculpture (Fig. 3H, K), and others are mostly smooth (Fig. 2A).

Internal shell characteristics are often more helpful than external ones in separating the tropical eastern Pacific oysters. The presence or absence of small denticulations (chomata) along the shell margin near the hinge can be very useful to separate genera (Fig. 1A, B); however, sometimes chomata are greatly reduced in certain specimens (e.g., Ostrea conchaphila). One must be careful to make an immediate or hasty identification based on a single shell character. Using the entire suite of the aforementioned characteristics leads to an accurate identification.

Crassostrea aequitorialis

Crassostrea columbiensis

Figure 1.

Shell characteristics of Ostreidae. (A) Hinge with smooth margins and long ligament groove; (B) Hinge with chomata and broad ligament; (C) Left (bottom) valve nearly flat, margin strongly undulate; (D) Left valve deeply convex, margins not undulate; (E) right (top) valve, adductor muscle scar mostly posterior of midline.

Crassostrea corteziensis

Crassostrea gigas

Figure 2.

Oyster species of the eastern Pacific: (A–F) Crassostrea aequatorialis, Ecuador, Guayaquil, Isla Luna. BMNH 1854.12.4.823 (holotype), length 44 mm, height 80 mm. (G–L) Crassostrea columbiensis, Ecuador, Guayas, Santa Elena. SBMNH 120,192 (neotype), length 62 mm, height 59 mm. (A, G) Exterior right valve; (B, H) Exterior left valve with mangrove root adhering to shell; (C, I) Interior of the right valve; (D, J) Interior of the left valve; (E, K) Lateral view of both valves; (F, L) Hinge of the left valve.

Figure 3.

Oyster species of the eastern Pacific: (A–F) Crassostrea corteziensis, México, Sonora, Bahía Kino. CAS 064,947 (holotype), top valve length 83 mm, height 140 mm and bottom valve length 103 mm, height 152 mm. (G–L) Crassostrea gigas, Mexico, Sonora, Bahía la Choya, intertidal. SBMNH 359915, length 61 mm, height 119 mm. (A, G) Exterior right valve; (B, H) Exterior left valve; (C, I) Interior of the right valve; (D, J) Interior of the left valve; (E, K) Lateral view of both valves; (F, L) Hinge of the left valve.

Crassostrea sikamea

Dendostrea folium

Dendostrea sandvichensis

Ostrea angelica

Figure 4.

Oyster species of the eastern Pacific: (A–F) Crassostrea sikamea, USA, OR, Lincoln County, Yaquina Bay. SBMNH 145309, length 48 mm, height 66 mm. (A) Exterior right valve; (B) Exterior left valve; (C) Interior of the right valve; (D) Interior of the left valve; (E) Lateral view of both valves; (F) Hinge of the left valve. (G–J) Dendostrea folium, Mexico, Baja California Sur, Punta Pescadores, attached to urchin, 3–6 m. SBMNH 83500, length 8 mm, height 17 mm. (G) Exterior right valve; (H) Urchin host with figured oyster attached to the top spine; (I) Interior of the right valve; (J) Interior of the left valve.

Figure 5.

Oyster species of the eastern Pacific: (A–D) Dendostrea sandvichensis, Mexico, Baja California Sur, Bahía de los Muertos, 3–6 m. SBMNH 149691, length 18 mm, height 28 mm. (A) exterior left valve, (B) oyster attached to coral branch, (C) interior of right valve, (D) interior of left valve. (E–J) Ostrea angelica, Mexico, Sonora, NE of Guaymas, Bahía Batuecas, intertidal. SBMNH 135082, length 41 mm, height 42 mm. (E) exterior right valve, (F) exterior left valve attached to rock, (G) interior of right valve, (H) interior of left valve, (I) lateral view of both valves, (J) hinge of left valve.

Ostrea conchaphila

Figure 6.

Oyster species of the eastern Pacific: (A–F) Ostrea conchaphila, Mexico, Sonora, Estero El Soldado. SBMNH 20357, length 39 mm, height 51 mm. (G–L) Saccostrea palmula, Mexico, Oaxaca, Golfo de Tehuantepec. BMNH 74.12.11.260 (syntype of Ostrea mexicana), length 39 mm, height 51 mm. (A, G) Exterior right valve; (B, H) Exterior left valve; (C, I) Interior of the right valve; (D, J) Interior of the left valve; (E, K) Lateral view of both valves; (F, L) Hinge of the left valve. (M) S. palmula, Mexico, Baja California, Puertecitos. SBMNH 468301, length 52 mm, height 62 mm, depth 34 mm, lateral view depicting the deep left valve and concave right valve fitting inside left.

Figure 7.

Oyster species of the eastern Pacific: (A–F) Striostrea prismatica, Panama, Veraguas, Guacamya. BMNH 1912.6.18.40 (syntype), length 63 mm, height 80 mm. (A) Exterior right valve; (B) Exterior left valve; (C) Interior of the right valve; (D) Interior of the left valve; (E) Lateral view of both valves; (F) Hinge of the left valve. (G–L) Undulostrea megodon, Peru (precise locality unknown). BMNH unnumbered (syntype), length 43 mm, height 102 mm. (A, G) Exterior right valve; (B, H) Exterior left valve; (C, I) Interior of the right valve; (D, J) Interior of the left valve; (E, K) Lateral view of both valves; (F, L) Hinge of the left valve.

Saccostrea palmula

Striostrea prismatica

Undulostrea megodon

General Anatomy

Internal anatomy of the oysters in the tropical and subtropical regions of the American Pacific is similar to that of other Ostreidae molluscs, and we take Crassostrea corteziensis as an oyster model. According with Chávez-Villalba et al. (2005) and Flores-Higuera (2011), two lobes forming the mantle cover the organs and shape the pallial cavity. The gills divide the space in inhalant and ex-halant chambers where seawater circulation takes place. The mouth is covered by the labial palps and is oriented to the ligament, whereas the anus borders the adductor muscle. The gonad is largely diffused within the digestive gland and both surround the pericardium and part of the adductor muscle. A representative of organs and tissues of C. corteziensis is in Figure 8.

Life Cycle

Few studies have been conducted on the biology of oysters in the West American tropics and the subtropical eastern Pacific, and knowledge of the life cycle, particularly the early stages, is still to be determined in most native species. Embryogenesis, larval, and postlarval development of Crassostrea corteziensis and Striostrea prismatica have been described during spat production in controlled conditions (Mazón-Suástegui 2014, Lodeiros et al. 2017).

Figure 8.

Main internal anatomical features of the Cortez oyster Crassostrea corteziensis.

In these species, fertilization is external, and once the eggs are fertilized, the embryonic development begins quickly, reaching the trochophore larval stage in a few hours (12–18 h), resulting in “D” veliger mixotrophic larvae before 24 h. The planktonic life stage lasts 2 to 3 wk, during which time the larva grows and modifies its shape and behavior with very active swimming; then, the eye spot appears and the foot is developed (pediveliger larvae). At this time, the larval swimming stops, passing into a benthic phase, and then the larvae acquire a creeping displacement until obtaining an adequate substrate where they are cemented and metamorphosed to acquire their sessile lifestyle.

From this point forward (18–22 days for Crassostrea corteziensis and 22 days for Striostrea prismatica), the larva undergoes metamorphosis, loses the velum, and develops its gills. During this process, the larva chooses the substratum and cements with the left valve, thus initiating its sessile life, similar to that of the adult. Figure 9 schematically shows the life cycle details of S. prismatica from its fertilization, production of juveniles (in laboratory conditions), and adult stages. Although the embryonic and larval development in these oysters is similar to that of many oysters, and shows the characteristics of many bivalves, the umboned larva in S. prismatica has a reddish distal spot, which can be used for identification in zooplankton samples (Lodeiros et al. 2017).

Population and Ecological Interactions

Population studies and the ecological interactions of these species are intended for the evaluation of the resource for fishery and exploitation purposes, and oyster reef conservations and restoration, so they are aimed at determining their abundance and distribution by size, sex proportion, associated species, water quality, and other parameters in the systems where they are distributed naturally (Coen & Luckenbach 2000).

The rock oyster is one of the most abundant species in the coastal and subcoastal rock systems, and, in most cases, it provides the greatest fishing biomass. Ríos-González et al. (2018) performed a revision of Striostrea prismatica describing its biology, exploitation, and conservation. On the coasts of Mexico, the species S. prismatica, together with Chama coralloides, Choromytilus palliopunctatus, and Saccostrea palmula, accounts for almost 60% of the total abundance of species, with S. prismatica representing the largest biomass (Flores-Garza et al. 2014).

Unexploited stocks can have up to 175 individuals/m², as Campos and Fournier (1989) have reported for Curú Bay in Costa Rica; however, the stocks are generally overexploited or depleted by artisanal or commercial fisheries because of the lack of extraction regulations. Additional anthropogenic factors, such as pollution, have contributed to the decline of the fishery (Grijalva-Chon et al. 2015).

In 2000, the stocks of Striostrea prismatica in the rocky coast of Tumbes, Peru, showed a size range of 7–228 mm, with densities of 6–77 oysters/m², but in subsequent surveys (2007), the densities dropped to 0.2 oysters/m² (Ordinola et al. 2010, 2013). Gonzabay (2014) recorded a density of 0.7 oysters/m² in a rocky system of the town of Ayangue, in the El Pelao nature reserve, Santa Elena Province, Ecuador, with dominant sizes of 80.0–120.0 mm (77.1%), and García and Leones (2016) report sizes of 32.5–178.0 mm with a greater predominance of 60–90 mm, in the intertidal zone of Punta Napo and Punta Gorda, province of Manabí, Ecuador. This difference in sizes, with a shortage of large specimens, is a product of the fishing pressure that exists on the species in rocky systems.

In other species such as Crassostrea columbiensis, population studies are even fewer. In Punta Morales, Puntarenas, Costa Rica (years 1984–1985), individuals showed a growth that conforms to the model of Von Bertalanffy [Lt = 8.9 (1 – e^–0.1567 (t = –0.123))], with a relationship length-weight of P = 1.04 × 10^–3 Lt = 2.3487 (Caballero et al. 1997), and for Magdalena Bay, Baja California Sur, Mexico, it is estimated they had a longevity of 6–7 y (García-Domínguez, unpublished data).

The palmate oyster Saccostrea palmula and the Arcid cockle Anadara tuberculosa are the most important components and the most conspicuous species in mangrove swamps of southern Baja California peninsula, Mexico. The palmate oyster can reach 50 mm in shell length at 1 y (Félix-Pico et al. 2015). Nonetheless, in the estuary Morales, Punta Morales, Puntarenas, and Costa Rica, the maximum total weight length found was 66.7 mm and 24.7 g, respectively, and the growth conforms to the von Bertalanffy model, with a relation Lt = 68.2 (1 – e^–0.1577t). In this locality, the length–weight population ratio is allometric and fits the equation Pt = 2.13 × 10^–2 Lt 1.6602 (Cabrera et al. 2001b); however, records of the biological-fishing status of their populations are not yet available.

In addition to growth studies of Crassostrea corteziensis during cultivation (Chávez-Villalba et al. 2005), growth in this species has been examined from two perspectives, scope of growth and use of growth models. In the first case, values of the scope for growth revealed that C. corteziensis is able to grow in different combinations of temperatures and salinities, but with superior results at 26°C and salinity of 20 (Guzmán-Agüero et al. 2013). In terms of growth modeling, growth data have been analyzed using the model of von Bertalanffy with the following relation: Lt = 114 (1 – e^–1.1t) (Chávez-Villalba et al. 2005). Another approach, implemented by Chávez-Villalba and Aragón-Noriega (2015), was multimodel inference by testing five different asymptotic growth models (von Bertalanffy, logistic, Gompertz, Schnute, and Schnute–Richards). They found that the best model to describe the individual growth of the species is that of Schnute–Richards.

Figure 9.

Life cycle of the rock oyster Striostrea prismatica, showing its planktonic (embryonic and larval) and benthonic (pediveliger and postlarval) development, from spat to adult stage. (A) Unfertilized oocyte; (B) First polar body indicating oocyte fertilization 15 min; (C) First cell cleavage 1 h 30 min; (D) Second cell cleavage 2 h; (E) Immobile morula 4 h; (F) Blastula 5 h; (G) Late gastrula 7 h 30 min; (H) Trochophore larvae 10 h; (I) Calcified early D-shaped larvae with prodissoconch I 20 h; (J) Veliger larvae 2 days; (K) Umboned larvae with a distal reddish-orange toward the ventral zone 9 days; (L) Umboned larvae with a more marked distal reddish-orange toward the ventral zone 12 days; (M) Large umboned larvae showed spot eye 18 days; (N) Pediveliger larvae 22 days; (O) Early postlarvae 3 days postmetamorphosis; (P) Visually observable postlarvae 9 days postmetamorphosis; (Q) Spat juvenile 90 days postmetamorphosis; and (R) adult. The images have different magnification scales delineated as horizontal bars.

Considering that the Japanese oyster Crassostrea gigas is an exotic species on the shores of the American Pacific, it is speculated that it is highly probable that the various causative agents of epizootics may have arrived as dispersal vehicles as larvae and C. gigas spat from hatcheries in the United States. Many lots of oysters (spat, juveniles, and adults) were illegally introduced to Mexico, without strict sanitary controls, including the minimum required by international standards (Flores-Higuera 2011).

Although there are no reports of predators in the oyster species stocks of the tropical and subtropical American Pacific, Mazón-Suástegui (2014) points out that the main predators of Crassostrea corteziensis are crabs (Callinectes spp.), the sea urchin Echinometra vanbrunti, sea stars (Heliaster kubiniji and Pentaceraster cuminigi), the puffer fish Sphoeroides annulatus, rays, and carnivorous molluscs such as Thais spp.

In the oyster stocks of Tumbes, Peru, Striostrea prismatica serves as a substrate for a variety of benthic communities (35 species) that are predominantly molluscs, within which are the genera Diodora and Crepidula, and the drilling mussels in the genus Lithophaga were the most abundant. These were followed by crustaceans, echinoderms, cnidarians, annelids, and poriferans, as well as several types of macroalgae (Ordinola et al. 2013). Similarly, Mazón-Suástegui (2014) reports that the shells of Crassostrea corteziensis house a great diversity of species of molluscs, sponges, tunicates, bryozoans, crustaceans, scales, and some macroalgae. This high diversity of species and invertebrate epibionts that use oyster shells as habitats confers the character of bioengineers to these two species.

Oysters can harbor other organisms within their mantle cavities such as the tiny soft-bodied pea crabs of the family Pinnotheridae that live commensally in the mantle of certain bivalve molluscs. A series of adaptations have evolved to cope with their symbiotic lifestyle (Peiró et al. 2011), which makes them an interesting model to study the evolution of associations between decapods and other invertebrates. Some studies (Cabrera et al. 2001a, Salas-Moya et al. 2014) of the pea crab Austinotheres angelicus, living in the palmate oyster Saccostrea palmula, have included biometric and reproductive data, adding important information about both species (commensal: A. angelicus and host: S. palmula); however, more data are needed to get a better understanding of the interactions between population dynamics of the host and adaptive responses of the symbiotic pea crab (Salas Moya et al. 2014).

In the case of Crassostrea gigas, as a cultured resource in many parts of the world, particularly in temperate zones, the species can create large hard-substrate biogenic reefs, making them one of the most transformative invaders of marine ecosystems (Crooks et al. 2015). Oyster reefs may harbor invertebrate groups, support other bivalves (Geukensia spp., Macoma spp., Ensis spp., Mya arenaria, and Mercenaria mercenaria), and are used by many fishes as a recruitment substrate, nursery habitat, and foraging ground (Coen & Luckenbach 2000, Beck et al. 2011). These reefs may influence water quality, sediment erosion rates, and hydrodynamic patterns of water in estuaries and coastal lagoons. All of this affects the distribution and abundance of other biogenic habitats, such as seagrass beds, salt marshes, algal beds, and also influences the dynamics of disease dispersal. Despite the ecological importance of oyster reefs, the large original populations in native areas had been severely affected because of overfishing, contamination, and the construction or expansion of seaports (Beck et al. 2011). Some of the efforts aimed at reestablishing natural oyster populations have focused on finding suitable alternative substrates. In this sense, Goelz et al. (2020) make an excellent review of the use of various alternative substrates used for oyster reef restoration.

Aquaculture activities pose a risk of species introductions when oysters are transplanted or introduced into different zoogeographic regions, including the introduction of new diseases. In addition, exotic oyster introduction produces competition and displacement of congener species with the same or greater capacities of negative effects on the ecosystems to which they are introduced. Although the movements of introduced oysters as in the case of Crassostrea gigas along the American coasts are almost exclusively related to aquaculture practices, this activity is recognized as one of the largest potential vectors for the transport of marine invasive species (Ruesink et al. 2005, 2006). For example, the snail Batillaria attramentaria was introduced to the west coast of the United States with C. gigas, where it outcompetes and is displacing the native snail Cerithidea californica in several estuaries (Byers 2000).

Ecological effects of nonindigenous species when introduced in native habitats are due to not only ineffective control strategies to prevent parasite and pathogen dispersion around the world but also as a natural consequence of globalization of world commerce. Every day, substantial amounts of live fishery or aquacultural products are distributed from one country to many other countries around the world. In this overall context, the species Crassostrea gigas introduced by aquaculture practices may have substantial effects in terms of biodeposits, altered flow regimes, and disturbance of the substrate (see Everett et al. 1995).

Oysters remove particles from the water column during suspension feeding and produce feces and pseudo-feces, which lead to reduced particle size and increased organic content in sediments (Ruesink et al. 2005). Although this process facilitates the action of the bacterial flora of the environment and of marine floors, Villarreal (1995) argue that in Bahía San Quintín (Baja California, Mexico), biodeposits coming from oyster cultures have been associated with eutrophication.

There are two species in the genus Dendostrea that have been reported sporadically in the tropics and subtropics of the American Pacific (Taxonomy, Identification, and Distribution), and very little information is available for these small and regionally rare species. The few reports show Dendostrea folium and Dendostrea sandvichensis from the Indo-Pacific, as species recorded in lists of Pacific islands, such as Isla Cocos in Costa Rica and the Galapagos Islands in Ecuador (Magaña-Cubillo & Espinosa 2009, Coan & Valentich-Scott 2012). It is important to mention that D. folium shows a quantitatively different karyotype (2n = 18; Ieyama 1990) the species of the family Ostreidae (n = 20), and that D. sandvichensis is called the Hawaiian oyster.

There are only a few studies on Ostrea angelica (formerly Myrakeena angelica), dealing with taxonomy (McLean & Coan 1996, Holguin-Quiñones et al. 2008, Bastida-Zavala et al. 2013) as well as paleontological and archaeological records (Laynder et al. 2013, Rugh 2014). Marcus and Harry (1982) described the planarian Zygantroplana ups associated with the mantle cavity of the Ostrea angelica, and recently, molecular phylogenetic studies confirm its integration into the genus Ostrea (Raith et al. 2016).

Reproduction

Most of the reproduction studies on tropical and subtropical oysters have been carried out in natural populations (Table 1). All species whose reproductive cycle has been studied so far, including Striostrea prismatica, Crassostrea columbiensis, Crassostrea corteziensis, and Saccostrea palmula, are gonochoric organisms, and in their populations, most of the males are smaller in size (Fournier 1992, Caballero et al. 1997, Cabrera et al. 2001b, Romo-Piñera 2005, Chávez-Villalba et al. 2008, Loor & Sonnenholzner 2014). This suggests a common characteristic of protramental hermaphroditism.

In these species, the gonad is distributed throughout the visceral mass (Fig. 9), which contains large amounts of oocytes. Spawning Striostrea prismatica individuals of 120 mm (dorsoventral axis) induced at CENAIM-ESPOL/Ecuador hatchery indicate a fecundity of 60 million oocytes/individual. This number could be higher considering that oysters of this species may reach twice that size (Lodeiros et al. 2017). Although fecundity of Crassostrea corteziensis is lower (50 million oocytes/ individual) than that of S. prismatica according to several studies at CIBNOR Mexico (Chávez-Villalba et al. 2008, Rodríguez-Jaramillo et al. 2008), both species are considered great broadcast spawners. While C. corteziensis has the ability to attain sexual maturity and carry out several partial spawnings during a breeding season (Mazón-Suástegui et al. 2011).

The size at the sexual maturity in 50% of Striostrea prismatica populations on the coasts of Nayarit, Mexico, is 87–91 mm of the dorsoventral axis (Hernández-Covarrubias et al. 2013), whereas in Crassostrea corteziensis in Las Guasimas, Sonora, and in Ceuta Bay, Sinaloa (Mexico), it is 50–60 mm (Chávez-Villalba et al. 2008, Mazón-Suástegui et al. 2011). For other species, such as Saccostrea palmula and Crassostrea columbiensis of Punta Morales, Puntarenas (Costa Rica), the size at sexual maturity is 10–11 mm (Cabrera et al. 2001b).

Ríos-González et al. (2018) described phases of reproduction of Striostrea prismatica observed in a latitudinal gradient from north to south in tropical eastern Pacific. As observed in Table 1, studies on the reproduction of S. prismatica cover a wide latitudinal range, from 03° S (Costa de Tumbes, Peru) to 27.5° N (Guaymas, Sonora, Mexico). With the exception of studies conducted in Curú, Gulf of Nicoya, Costa Rica, where temperatures are always high (29.0°C–32.7°C), significant changes related to high temperatures were always associated with reproductive processes, particularly the maturation and spawning of S. prismatica.

TABLE 1.

Studies of the reproductive cycle of populations of native Ostreidae species of the tropical and subtropical American Pacific in north-south latitudinal order.

continued

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Loor and Sonnenholzner (2014) reported that there is no correlation between phytoplankton biomass (estimated by chlorophyll a) and the reproduction of Striostrea prismatica in the two places studied on the Santa Elena peninsula, Ecuador (General Villasmil and in Ayangue). In these locations, the chlorophyll a concentrations are greater than 2 µg/mL, suggesting that food availability is not a limiting factor. Similarly, other studies conducted in tropical areas such as the Gulf of Nicoya, Costa Rica, show that food availability does not appear to be a limiting factor for the reproductive processes of the species. Although Fournier (1992) did not record data on food availability in his study at the Gulf of Nicoya, it is known that the area is highly productive (León et al. 1998). In these high-productivity tropical systems, where the temperature is stable (<4°C annual variability in our analysis, Table 1), other environmental factors could be the main modulators of reproduction (Giese & Pearse 1974). Accordingly, Fournier (1992) found a negative association between spawning periods and salinity periods. In view of this, everything seems to indicate that temperature variability is the main factor in the modulation of S. prismatica reproduction, and, when its anual variability is minimal, salinity appears to be the main modulation factor. This agrees with the protocols established by Argüello et al. (2013) for gonadic conditioning of S. prismatica at high temperatures, consequently causing induction to spawning temperature changes from 28°C to 33°C accompanied by the reduction of salinity from 32 to 15.

In the southern Gulf of California, at El Verde, Sinaloa, it has been observed that Striostrea prismatica accumulates reserves during most of the year, which it mobilizes according to reproductive demand. Lipids decrease from October to March during the resting phase, and carbohydrates have an inverse trend in the months of April to May and June to July, whereas proteins increase in May when gametogenesis is activated and, with it, sexual maturation (Páez-Osuna et al. 1993). The aforementioned suggests that the reproductive strategy in the species is conservative.

Unlike Striostrea prismatica, reproduction studies in Crassostrea corteziensis, Saccostrea palmula, and Crassostrea columbiensis (Table 1) show in general, and regardless of latitude, a year-round reproductive activity with few periods of sexual rest. Temperature is the predominant modulating factor both for maturation (average temperatures) and spawning (high temperatures). An exception, and at the same time an interesting case, is the behavior of S. palmula indicated by Romo-Piñera (2005) and Romo-Piñera et al. (2015) in Santo Domingo, Magdalena Bay, and El Conchalito in La Paz Bay, Baja California Sur, Mexico. Even though these sites have similar temperature ranges and latitudes, natural populations of this species behave reproductively different, being opportunistic at the first site and conservative in the second. This difference is possibly associated with food availability, because at Santo Domingo, chlorophyll a has always been greater than 1 µg/L, with periods of higher production (>3 µg/L and up to 9 µg/L), whereas at El Conchalito, it was always less than 1 µg/L.

Other studies on the effect of environmental variables on gonad maturation, immunology, and genetic diversity have been carried out on Crassostrea corteziensis. Rodríguez-Jaramillo et al. (2008) and Chávez-Villalba et al. (2008) described the quantitative and qualitative histology and histochemistry of C. corteziensis. Mature organisms were found during most of the year, and there were at least two strong spawning periods, first in summer and then in autumn.

The two reproductive studies reported for Crassostrea columbiensis in the Bay of Santo Domingo, Mexico (Félix-Pico et al. 2011), and at Estero Morales, Costa Rica (Caballero et al. 1997), are contrasting in terms of the distance in a latitudinal order (24° and 10°, respectively); however, both populations show reproductive activity throughout the year (Table 1). In the case of Santo Domingo, where there is a greater annual temperature range, average temperatures greater than 22°C favor gametogenesis, and high temperatures (26°C–30°C) favor maturation, with a temperature decrease inducing spawning (Félix-Pico et al. 2011).

In general, the natural or harvest habitats, where the tropical and subtropical Pacific North American oysters develop, seem to provide enough phytoplankton biomass to support their reproductive processes so that the environmental modulation of reproduction is governed mainly by temperature, particularly in the maturation and spawning processes. As was indicated, in those tropical ecosystems where the temperature variability is not high, salinity also seems to be an important factor for spawning.

There are no published data to indicate the establishment of naturally reproducing populations of the Japanese or Pacific oyster Crassostrea gigas or the Kumamoto oyster Crassostrea sikamea beyond southern California, United States, or in the subtropical and tropical countries of the American Pacific Southern Hemisphere. Recently, however, the presence of the Japanese oyster has been reported outside culture sites in the Ojo de Liebre lagoon, which corresponds to the El Vizcaíno Biosphere Reserve in the Gulf of California (Carrasco & Barón 2010). Studies detailing the reproductive processes of cultivated C. gigas have been performed in Mexico. The species behaves as a protandrous hermaphrodite (Paniagua-Chávez & Acosta-Ruíz 1995), and depending on the region (Baja California or Sonora), the gonads are in early gametogenesis from January until June, in vitellogenesis from March to July, and mature from June to October, and partial spawning occurs from August to October (Cáceres-Martínez et al. 2004, Rodríguez-Jaramillo et al. 2017). Nevertheless, Chávez-Villalba et al. (2007) indicated that the species did not spawn in Sonoran waters, and there was evidence that oocytes were reabsorbed within the gonad. It seems that temperature regimes are the main limiting factors for the normal processes of spawning, fertilization, and larval settlement, thus preventing the establishment of feral populations. Recently, histological studies to determine the reproductive condition of C. gigas culture in a tropical estuary at Bahía de Caráquez, Manabí, Ecuador (0° 36′3″ S, 80° 25′23″ O), show that oysters greater than 40 mm maintain a protrandic condition with a female to male ratio of 1:2.6 with partial spawning (Lodeiros, unpublished data). This indicates limited processes for the development of C. gigas larvae or postlarvae in subtropical and tropical regions, restricting the establishment of feral populations.

There are no reproductive studies of the Kumamoto oyster Crassostrea sikamea in the tropical and South American Pacific. Nevertheless, Cáceres-Martínez et al. (2012) reported that Kumamoto oysters start gametogenesis as young as 71 days from spawning (35 days from postsettlement), with a mean shell height of 3.0 mm. This constitutes a record in age size for gametogenesis in oysters of commercial importance and adds another biological difference comparing this species with the Pacific oyster Crassostrea gigas.

Bioacumulators

Because of the filtering characteristics of oysters and their commercial importance, various studies have been undertaken to determine whether they bioaccumulate unwanted substances, compounds, or organisms. For instance, Striostrea prismatica has been used to detect organochlorine pesticides (Ponce-Vélez & Botello 2018) and heavy metals (Páez-Osuna et al. 1995, Frías-Espericueta et al. 1999a, 1999b, Soto-Jiménez et al. 2001, Osuna-López et al. 2007). Oysters also accumulate bacterial species that can cause epizootics and pathogenic agents that affect their consumption safety at harvest. In this sense, it is necessary to remember that the microbiota associated with the intestinal digestive tract of the ostreids contributes various beneficial substances to the host; it presents antibiosis or competition for space and nutrients against pathogens and their composition, and diversity varies according to the age of the mollusc and the culture site (Trabal-Fernández et al. 2014). The distribution of S. prismatica along the rocky coasts of the tropical and subtropical eastern Pacific suggests that the species could be used as a model in ecotoxicological studies for rocky systems. Similarly, evidence of heavy metal accumulation in conspicuous oyster species (Crassostrea corteziensis, Saccostrea palmula, and Crassostrea columbiensis) in the mangrove systems of the region has allowed them to be considered (particularly C. corteziensis) as biomarker organisms (Páez-Osuna et al. 2002, Jara-Marini et al. 2008, Bernal-Hernández et al. 2010, García-Rico et al. 2010, Páez-Osuna & Osuna-Martínez 2015). Given the direct human consumption of various molluscs, including S. prismatica, some studies have been carried out to advise managers on the advisability of establishing continuous monitoring programs for toxicity because of harmful algal blooms (Barraza et al. 2004, Band et al. 2010, Alonso-Rodríguez et al. 2015).

Diseases

Few diseases have been described for tropical and subtropical oysters of the American Pacific. Most reports have been for oysters (Crassostrea gigas and Crassostrea sikamea) introduced from temperate zones (Elston & Wilkinson 1985, Bower et al. 1997, Friedman et al. 1998, Burreson & Ford 2004, Friedman et al. 2005, Burge et al. 2011, Moore et al. 2011).

In a subtropical region (Baja California, México), a virus belonging to the Herpesviridae was detected after a Crassostrea gigas mortality event in 2000, although the role of the presumable pathogens has not been clearly defined (Vásquez-Yeomans & Cáceres-Martínez 2004, Vásquez-Yeomans et al. 2004). The OsHV-1 herpesvirus was later found in the gills of the species (Vásquez-Yeomans et al. 2010). Recently, nine genotype variants of OsHV-1 were identified in the Gulf of California, and genetic analysis suggested that linear genotypic evolution had occurred from strain JF894308 present in lagoon La Cruz (Sonora, Mexico) in 2011 (Martínez-García et al. 2020). The prevalent pathogen of oysters, Perkinsus marinus, causing the dermo disease or perkinsosis, has been associated with massive mortalites of C. gigas in culture conditions along Sonoran coasts, Mexico (Enríquez-Espinoza et al. 2010). Similarly, the protozoan Marteilia refringens was detected for the first time in the Gulf of California in samples of C. gigas (Grijalva-Chon et al. 2015). The presence of parasites including ciliates (Ancistrocoma and Trichodina), the annelid Polydora sp., and trematode worms has also been detected in Pacific oysters in northwestern Mexico, but they have not been associated with mortalities (see Cáceres-Martínez & Vásquez-Yeomans 2008 for more details).

In the native oyster Crassostrea corteziensis, a series of epizootics diseases associated with parasites, bacteria, or viruses have been recorded (Grijalva-Chon et al. 2015). This problem has been associated with the presence of Perkinsus marinus, Nematopsis sp., and some protozoa such as Halteria grandinella, Hexamita spp., Bodo spp., and Marteilia refringens during the larval and juvenile stages of the species. Reports of high mortality in larval culture associated with the presence of Vibrio spp. are also common and increasingly frequent (Campa-Córdova et al. 2009, 2011). Martínez-García et al. (2017) studied the possible presence of a temporary coupling of infectious events in distant cultures of C. corteziensis in the Gulf of California considering seasonal variation, presence, and the prevalence of P. marinus, M. refringens, and OsHV-1. Results of the molecular analysis showed a higher prevalence of P. marinus in the north area and M. refringens in the southern area. The OsHV-1 herpesvirus was only present during summer and autumn with low prevalence in the two areas. The histological analysis of the PCR-positive organisms presented alteration characteristic of infections. The presence of M. refringens in a new location in the Gulf of California suggests that this pathogen is already well established in the area, and the dual presence of pathogens is reported for the first time in C. corteziensis.

Gutiérrez-Rivera (2014) compared the immune response of the Cortez oyster Crassostrea corteziensis and the eastern oyster Crassostrea virginica after their experimental infection with the protozoan Perkinsus marinus. Results indicated that the protozoan caused greater mortality in the eastern oyster. This possible resistance to Perkinsus adds consideration of C. corteziensis as a good candidate for aquaculture, in addition to its better flavor and texture (Mazón-Suástegui 2014). Conversely, Bravo-Guerra (2018) showed that the parasite could be treated therapeutically because it shows a high susceptibility to silver nanoparticles at a concentration of 0.0927 mM Ag, an order of magnitude less than the concentration known to impart negative effects on C. corteziensis.

The parasite Bonamia spp. is commonly associated with oysters from temperate zones, but Hill et al. (2014) detected a Bonamia sp. in Dendostrea sandvicensis from Hawaii. This record, together with others detected in Ostrea edulis in Australia (Morton et al. 2003) and South Africa (Haupt et al. 2010), confirms that Bonamia parasites have extended their presence in tropical climates.

Bacterial infections have been little studied in the subtropical and tropical oysters of the American Pacific, and, although there is a relationship of bacterial infection when oysters are infected with the OsHV-1 virus (Cáceres-Martínez & Vázquez-Yeomans 2013), there are no specific studies that can determine the type of these infections. Luis-Villaseñor et al. (2018) conducted a study on the communities of the oysters Crassostrea corteziensis and Crassostrea sikamea from commercial oyster farms in Mexico. They found that the Kumamoto oyster C. sikamea presented a greater diversity of species and the highest number of pathogenic bacteria for aquatic organisms, which is a probable reflection of their poor health status in tropical culture.

Saccostrea palmula

There are no population genetic studies for this species, but in the contribution by Cruz et al. (2007) on the microsatellite loci for Crassostrea corteziensis, they mention that of the 11 loci characterized for the Cortez oyster, seven can be amplified in Saccostrea palmula, which makes them suitable for population studies. Mazón-Suástegui et al. (2016) reported sequences of mitochondrial cytochrome c oxidase subunit 1 (COI) gene, the nuclear intertranscribed spacer 1 (ITS-1), and the nuclear 28S ribosomal gene. By means of a phylogenetic analysis with sequences of other species of ostreids, these authors concluded that the 28S gene was more reliable in correctly identifying species; thus, it can be used as an alternative marker. Raith et al. (2016) included S. palmula in a phylogenetic analysis with ostreids from the Gulf of California using COI and 16S ribosomal gene sequences and mentioned a lack of genetic variation in S. palmula, and validated the Saccostrea genus.

Ostrea angelica

This species also lacks studies of population genetic diversity. The phylogenetic analysis carried out by Raith et al. (2016) confirms the closeness of this species with Ostrea conchaphila and Ostrea lurida, and placed the species within the genus Ostrea while invalidating the genus Myrakeena.

Striostrea prismatica

The levels of genetic diversity and population structure are also unknown in this species. For this species, Mazón-Suástegui et al. (2016) report sequences of COI, ITS-1, and 28S that can be used in phylogenetic studies. In the phylogenetic study carried out by Raith et al. (2016), it is proposed that Striostrea is the only member of the new subfamily Striostreinae.

Ostrea conchaphila

The level of genetic diversity in this species is unknown. When analyzing 16S and COIII mitochondrial markers, Polson et al. (2009) determined that this species is not a synonym for Ostrea lurida. Subsequently, the phylogenetic study of Raith et al. (2016) confirmed the genetic closeness with O. lurida and determined that there is no sympatry between them. With this molecular identification, these authors also extended its distribution range to Laguna San Ignacio, south of Punta Eugenia, Baja California Sur (Mexico).

Crassostrea columbiensis

For this species, there is only a report of the sequences of COI, ITS-1, and 28S by Mazón-Suástegui et al. (2016).

Crassostrea corteziensis

In the tropical and subtropical eastern Pacific, Crassostrea corteziensis is the native ostreid species with the greatest aquaculture and fishing exploitation. Because of this, more attention has been paid to it than to the oyster species in the region. Thirty-one years ago, Rodríguez-Romero et al. (1979) described the karyotype of the species, determining that it has 20 chromosomes. Hedgecock and Okazaki (1984) carried out the first population genetics study with allozymes in organisms from Estero el Pozo, Nayarit (Mexico). These authors analyzed 17 loci, of which 58.8% were polymorphic, with an average of 2.12 alleles per locus and observed heterozygosity (Ho) of 13.8 and expected heterozygosity (He) of 19.6, outside the equilibrium of Hardy–Weinberg (HW). In the same state of Nayarit, Rodríguez-Romero et al. (1988) compared the electrophoretic profile of general proteins in organisms from two localities (Estero el Pozo and Estero Teacapan), finding statistically significant differences between the areas.

Cruz et al. (2007) reported 11 microsatellite loci for Crassostrea corteziensis, of which 10 proved to be polymorphic. These authors performed a test analysis with 30 wild oysters from Sinaloa and found four loci that were out of HW equilibrium, and concluded that these loci were useful for paternity tests and for population genetics studies. Later, in a study with samples from five locations within the Gulf of California, Pérez-Enríquez et al. (2008) carried out a population genetic study with allozymes and mitochondrial DNA markers. The analysis of six allozymic loci (four polymorphic) showed that Ho was in the range of 0.058–0.117 and the He was 0.089–0.129, with HW equilibrium and without evidence of a population structure because of high genetic flow. Considering the levels of diversity reported by Hedgecock and Okazaki (1984), it was concluded that diversity did not change substantially in 20 y; on the other hand, an atypical result in the genotypic frequencies of the samples taken in Topolobampo, Sinaloa (Mexico), motivated these authors to perform a sequence analysis of the 16S mitochondrial gene, which demonstrated the presence of an unknown species, and the authors considered it to be Crassostrea columbensis.

Enríquez-Espinoza and Grijalva-Chon (2010) carried out an analysis of allozymes in a sample of the F1 generation descendent from a stock of breeders of wild origin from Sinaloa, Mexico. That F1 generation was cultivated in the state of Sonora. The 13 allozymic loci studied included eight polymorphic loci that were out of HW equilibrium, with an average Ho of 0.065 and He of 0.294, and with high inbreeding values.

Regarding the inclusion of this species in phylogenetic analyses, Raith et al. (2016) included it in their analyses of ostreids from the Gulf of California, so they also reported 16S and COI sequences for this species. Mazón-Suástegui et al. (2016) also report sequences for COI, ITS-1, and 28S.

Crassostrea gigas

Although some studies indicate the possibility of feral populations of Crassostrea gigas in Ojo de Liebre lagoon, Gulf of California, Mexico (Carrasco & Barón 2010), the population genetic studies of the species are limited to cultivated populations. Enríquez-Espinoza and Grijalva-Chon (2010) carried out an analysis with allozymes in a batch of triploid organisms that arrived as spat at Sonora. Sixteen loci were analyzed, of which 12 were polymorphic, with nine of them out of HW equilibrium, and with Ho and He averages of 0.350 and 0.309, respectively. The authors discussed the quality of these organisms because the heterozygosity values were lower than those reported for triploid oysters in the United States.

Grijalva-Chon et al. (2013) used microsatellites to analyze genetic variability in a sample from a batch of breeders that were purchased as spat from France. A second sample consisted of organisms from the F1 generation of that batch. Up to 68 alleles and 168 genotypes were detected with six microsatellite loci, with differences in the averages of the heterozygosity observed and expected in both samples (Ho = 0.65 and He = 0.81 for the parental lot; Ho = 0.67 and He = 0.84 for F1), and out of HW equilibrium in almost all loci. Finally, in the phylogenetic study reported by Raith et al. (2016), organisms of this species obtained from an oyster farm in Puerto Peñasco, Sonora, Mexico, were included.