Perkinsus sp. on Crassostrea gigas performance cultivated in the southeastern Gulf of California

A. M. Góngora-Gómez3; F. Rubio-Zepeda1; A. Santamaría-Miranda1; B. P. Villanueva-Fonseca1; A. L. Domínguez-Orozco2; L.C. Villanueva-Fonseca1; J. A. Hernández-Sepúlveda2; H. Rodríguez-González1; L. G. Espinosa-Alonso3; M. García-Ulloa1*

1. Departamento de Acuacultura, del Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional-Unidad Sinaloa, Instituto Politécnico Nacional, Guasave, Sinaloa, México, Instituto Politécnico Nacional, Departamento de Acuacultura, Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional-Unidad Sinaloa, Instituto Politécnico Nacional,

<city>Guasave</city>
<state>Sinaloa</state>
, Mexico , 2. Departamento de Medio Ambiente, Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional-Unidad Sinaloa, Instituto Politécnico Nacional, Guasave, Sinaloa, México, Instituto Politécnico Nacional, Departamento de Medio Ambiente, Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional-Unidad Sinaloa, Instituto Politécnico Nacional,
<city>Guasave</city>
<state>Sinaloa</state>
, Mexico ,
3. Departamento de Biotecnología Agrícola, Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional-Unidad Sinaloa, Instituto Politécnico Nacional, Guasave, Sinaloa, México., Instituto Politécnico Nacional, Departamento de Biotecnología Agrícola, Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional-Unidad Sinaloa, Instituto Politécnico Nacional,
<city>Guasave</city>
<state>Sinaloa</state>
, Mexico

Correspondence: *. Corresponding Author: Manuel García-Ulloa, Instituto Politécnico Nacional, Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional-Unidad Sinaloa, Departamento de Acuacultura, Blvd. Juan de Dios Bátiz Paredes # 250, CP 81101, Guasave, Sinaloa, México. E-mail.: E-mail: .


Abstract:

We studied the relation between the presence of Perkinsus sp. with growth performance (shell height - SH, body weight - BW), condition index, and biochemical composition (triglycerids, proteins, lipids, and carbohydrates) of the oyster Crassostrea gigas cultivated in two farms from Sinaloa, Mexico. Perkinsus sp. Was detected in both farms throughout (June 2013 to June 2014). The oysters had diverse degrees of prevalence fluctuating from 26.7 to 83.3 %. According to the Mackin’s scale, the intensity of infection was light to very light (0.1 to 1.2). There were not significant correlations between the prevalence with all studied parameters. Oyster survival at both farms was not affected by the presence of the protozoan. Intensity of Perkinsus infection was positively correlated with the biochemical composition of oyster. The influence of environmental parameters on the incidence the parasite in C. gigas is discussed. The overall results suggest that the presence of Perkinsus sp. in C. gigas from the two farms did not affect the health of the cultivated oysters, however, periodic monitoring of this pathogen in the farms should be continued.

Received: 2019 February 7; Accepted: 2019 May 5

revbio. 2020 Mar 20; 6: e681
doi: 10.15741/revbio.06.e681

Keywords: Key words: Parasite occurrence, Pacific oyster, condition index, proximal composition, Farming.

Introduction

As many parasites, the protozoa of the genus Perkinsus is transmitted horizontally via the water column (Andrews, 1996), thus, it has been widely reported infecting different oysters and clams species, and in some cases, associated with drastic mortalities of commercially important bivalves throughout the world. For instance, Goggin & Lester, (1995) identified the protozoan Perkinsus olseni as the causative agent of severe mortalities of the green-lip abalone Haliotis laevigata in Australia, meanwhile, Park et al. (2008) confirmed the occurrence of the same Perkinsus species in the Japanese short-neck clam Ruditapes philippinarum. Park & Choi (2001) confirmed the presence of Perkinsus-like parasites associated with mass mortalities on the clam Tapes philippinarum in Korea. Along the Atlantic coast of North America, from Canada to the coastal lagoons of the central and southern Gulf of Mexico, P. marinus has infected both cultivated and natural populations of the eastern oyster Crassostrea virginica (Ford, 1996; Soniat, 1996; Aguirre-Macedo et al., 2007). In Brazil, Brandão et al. (2013) found Perkinsus sp. infecting the mangrove oyster Crassostrea rhizophorae. Oyster production in the Pacific Northwest of Mexico relies on the culture of Crassostrea gigas and for two decades Perkinsus sp. have been reported in farms located in the Gulf of California (Chávez-Villalba, 2014; Chávez-Villalba et al., 2007, 2010; Enríquez-Espinoza et al., 2010; Villanueva-Fonseca & Escobedo-Bonilla, 2013). The same has occurred in other species such as the pleasure oyster C. corteziensis (Cáceres-Martínez et al., 2008) and the rock oyster Saccostrea palmula (Cáceres-Martínez et al., 2012) in southern locations of the Mexican coastline.

The level of affection in bivalves caused by Perkinsus is dependent on several factors such as the species (native, non-native), latitude, environmental parameters, host immune system, parasite activity, and stressors as pollutants (Villalba et al., 2004), and it is commonly evaluated by means of the infection prevalence and intensity (Park et al., 1999; Encomio et al., 2005; da Silva et al., 2016). For instance, Cáceres-Martínez et al. (2008) observed low prevalence and moderate infection of P. marinus in C. corteziensis from the central Pacific coast of Mexico, and mention that a possible origin of the parasite in natural populations may be associated with introductions of infected C. virginica from the East coast of United States of America or the Gulf of Mexico. Meanwhile, Villanueva-Fonseca & Escobedo-Bonilla, (2013) studied the occurrence of Perkinsus sp. in a Pacific oyster farm from the southeastern coast of the Gulf of California, recording moderate prevalence and low infection intensity of parasite, which increased in the warmest months of the culture cycle.

The level of incidence of this parasite in bivalve mollusks can vary from an innocuous occurrence, to a severe infection that damages the tissues. When the latter happens, the metabolism of the bivalve is compromised by affecting its energy flow and performance (Paynter, 1996). The reduction in the soft tissue growth (and consequently of the condition index) and changes in the biochemical composition of the host, are some of the systemic effects provoked by infections of Perkinsus sp. in oysters (Dittman et al., 2001; Encomio et al., 2005). Then, the incidence of Perkinsus sp. in these bivalves could deplete their net energy that should be used for growth and reproduction.

Most of the reports on the presence of Perkinsus in C. gigas are related to juvenile and adult specimens collected from commercial farms (Kennedy et al., 1995; Samain et al., 2007; Enríquez-Espinoza et al., 2010, 2015). Specific studies on determining the effect of the Perkinsus sp. occurrence in C. gigas from seed to harvest represent useful tools to better understand such biological association. Therefore, the purpose of this study was to assess the relation between the presence of Perkinsus sp. with growth performance, condition index, and biochemical composition of C. gigas oysters cultivated in two localities from the southeastern Gulf of California, during a single culture cycle.

Material and Methods

The study was carried out in two cultivation sites located at the north-central shoreline of Sinaloa: El Colorado Bay (CB), (25°39’-25°47’N, and 109°16’-109°24’W), and Las Aguamitas Estuary (AE), (24°20’-24°40’N, and 107°30’-107°58’W) (Figure 1).


[Figure ID: f1] Figure 1.

Culture sites. CB = El Colorado Bay, AE = Las Aguamitas Estuary, Sinaloa, Mexico.


A total of 6,000 Japanese oysters (3000 for each site, certified as pathogen-free) were obtained from Centro de Investigaciones Biológicas del Noroeste (CIBNOR), Sonora, Mexico, and cultured in racks suspended in a long-line system 0.15 m beneath the water surface. Initial shell height (SL) and body weight (BW) were 6.8 ± 0.9 mm and 0.02 ± 0.00 g. Young oysters were acclimated as mentioned by Gallo-García et al. (2004), placed in a plastic mesh bags (2 mm diameter) and then, into the racks suspended in a long-line system (n = 500 oysters rack-1). When reached 30-40 mm SL, oysters were grown out of the mesh (n = 42 oysters rack-1) until the end of the trial. The study started in June 2013 and finished in June 2014.

Oysters (n = 390, 30 month-1) were opened and soft tissues removed from the shell. The tissue fraction (10 g) used for Perkinsus sp. diagnosis was homogenized in a buffer solution (0.2 M phosphate buffer) and placed in tubes containing Ray’s fluid thioglycollate medium (RFTM) (Karolus et al., 2000). The tubes were placed in the dark at room temperature (28 °C) for seven days. After incubation, tissues were chopped into small pieces, stained with Lugol’s solution (1 ml, 4%), and the presence and number of Perkinsus sp. hypnospores were examined by light microscopy (100X, Leica®, DM750). The prevalence of infection was calculated as the percentage of infected oysters in each sampling month (Thrusfield, 1995). The intensity of infection in oysters was classified according to Mackin’s scale (Mackin, 1962) modified by Craig et al. (1989) (Table 1).

Table 1.

Degree of infection intensity in oysters according to Mackin’s scale (Mackin, 1962) modified by Craig et al. (1989).


Description of the Scale Mackin’s scale # Hypnospores Tissue covered by hypnospores (%)
Negative/No infection 0 0
Very light - 0.3 1-10
Very light + 0.7 11-74
Ligth - 1.0 75 - 125
Ligth 1.3 > 125 but < 25
Ligth + 1.7 < 25
Ligth/moderate - 2.0 25
Ligth/moderate 2.3 > 25 but much < 50
Ligth/moderate + 2.7 > 25 but < 50
Moderate - 3.0 50
Moderate 3.3 > 50 but much < 75
Moderate + 3.7 > 50 but < 75
Moderately heavy - 4.0 75
Moderately heavy 4.3 > 75 but much less than 100
Moderately heavy + 4.7
> 75, oyster tissue still visible
Heavy 5.0 100 oyster tissue covered

Biometrics and survival

Oyster biometrics and survival were obtained monthly. Total SL and BW of 60 specimens from each culture site were measured in situ with a vernier caliper (0.2 mm) and a portable balance (0.00 g), respectively. The growth rate of oyster was reported as body weight gain month-1 (Rodríguez-Quiroz et al., 2016). Survival was calculated by counting dead animals at each sampling and expressed as a percentage of the original number of oysters (Góngora-Gómez et al., 2012).

Condition index

Additionally, 30 specimens were sampled monthly to obtain the condition index (CI). After shucking and removing of tissues, the total oyster shell weight (g, TW) and the total fresh weight of soft tissues (g, SW) were registered with a portable balance (OHAUS, Scout Pro SP 2001). The shells and soft tissues were dried by using a draft oven (100° C, Riossa EC-41) during 24 hours. The CI was calculated with the formula proposed by Lucas & Beninger (1985): CI = (SW/TW) x 100.

Biochemical composition

At each sampling date, whole-oyster wet flesh weight of 30 oysters was measured and soft tissue samples were combined in 3 pools of ten animals each. Tissue samples were individually analyzed for protein, lipid, and carbohydrate content each month. Due to their small size, the biochemical composition of oysters from the three first months was determined using a pool (n = 30). Each tissue sample was triturated and placed in individual 2.0 ml Eppendorf microtubes, frozen at -70 °C for 24 h, lyophilized for 24 h, and pulverized. Finally, tissues were homogenized in 1 ml saline solution (35 UPS). All results were expressed as mg g-1, dry weight (DW).

Triglicerids were calculated by using the GEO-PAP (Randox) commercial kit at 460 nm absorbance. Total protein concentration was determined according to the procedure of Bradford (1976) at 595 nm absorbance. Lipids were extracted from freeze-dried oyster tissue using the sulphophosphovanillin method (Barnes & Blackstock, 1973) and assayed at 540 nm absorbance. Carbohydrates were analyzed using the anthrone reagent method (Roe, 1955) at 630 nm absorbance.

Water parameters

Water parameters were sampled every month to obtain temperature and dissolved oxygen (DO) with an oximeter (YSI 55/12FT, Ohio, USA), salinity with a refractometer (ATAGO, S/Mill), pH by using a pHmeter (HANNA, HI 8314, USA), depth and transparency with a Secchi disk, and total suspended solids (TSS) and particulate organic matter (POM) by the gravimetric method (APHA, 1995). Chlorophyll a (Cla) analysis was performed after filtration with Whatman GF/F filters (0.7 µm pore size) using Millipore vacuum filtration and was determined by standard spectrophotometric methods (Strickland & Parsons, 1972).

Data analysis

All dataset were tested for normality, and statistical tests were chosen accordingly. Comparison of means by one-way analysis of variance (ANOVA) and Tukey’s test was practiced at each site monthly for the incidence of Perkinsus sp. Student´s t-test was used to assay significant difference between means of all variables from both culture sites. Correlations of prevalence and intensity of Perkinsus sp. with oyster biometrics, condition index, biochemical content, and environmental parameters were computed at each culture site. The Statgraphic Plus 5.0 software package (Statistical Graphics Corp., Herndon, VA, USA) was used to perform these analyses. Differences were considered significant at p = 0.05.

Results and discussion

Perkinsus sp. was detected in CB and AE throughout culturing months. The oysters sampled in both places had diverse degrees of prevalence and intensity of infection (Table 2).

Table 2.

Prevalence and intensity of Perkinsus sp. infection in the oyster Crassostrea gigas cultivated in The Colorado Bay (CB) and Las Aguamitas Estuary (AE), Sinaloa, Mexico


2013-2104 Prevalence (%) Intensity (Mackin’s scale*)
CB AE CB AE
July 56.7 53.3 0.3ª 0.5a
(17)§ (16) (0.1) (0.1)
August 80 63.3 0.4a 0.9b
(24) (19) (0.1) (0.1)
September 60 50 1.2b 0.5a
(18) (15) (0.2) (0.1)
October 36.7 46.7 0.5a 0.4a
(11) (14) (0.1) (0.1)
November 56.7 43.3 0.5a 0.2a
(17) (13) (0.1) (0.1)
December 60 80 0.4a 0.6a
(18) (24) (0.1) (0.1)
January 70 60 0.4a 0.3a
(21) (18) (0.1) (0.1)
February 43.3 46.7 0.2a 0.3a
(13) (14) (0.04) (0.1)
March 43.3 56.7 0.4a 0.3a
(13) (17) (0.1) (0.1)
April 26.7 46.7 0.1a 0.2a
(11) (14) (0.04) (0.1)
May 83.3 73.3 0.6a 0.3a
(25) (22) (0.1) (0.1)
June 46.7 40 0.2ª 0.2a
(14) (12) (0.04) (0.1)
Mean 55.3 55 0.4 0.4
(16.58) (16.5) (0.1) (0.1)

TFN1*Mackin (1962) modified by Craig et al. (1989). §Mean (± standard error). Different superscripts between sites per month, mean significant differences (p≤0.05).


Prevalence of the parasite in CB fluctuated from 26.7 ± 8.0 % found in April, to 83.3 ± 25.0 % obtained in May, meanwhile, the lowest and highest prevalence values in AE were registered in June 2014 (40.0 ± 12.0 %) and December 2013 (80.0 ± 24.0 %), respectively. The intensity of infection in CB varied from 0.1 ± 0.04 in April, to 1.2 ± 0.2 found in September. For the AE farm, the lowest intensity (0.2 ± 0.1) was obtained in June and the highest value (0.9 ± 0.1) in August. There were no significant differences comparing prevalence (t = 0.07, p = 0.94) and incidence of parasite (t = 0.32, p = 0.75) in both culture sites.

Since Perkinsus-like organisms have been described parasitizing, and in some cases, causing massive mortalities in a large number of wild (Choi et al., 2002; Casas et al., 2004) and cultivated mollusks from around the world (Aguirre-Macedo et al., 2007; da Silva et al., 2016) and that many factors (internal and external) are involved in the parasite-host interaction, the study on the occurrence of Perkinsus sp. with host physiological condition and ambient parameters represents a valuable contribution to properly evaluate the effects of this parasite in cultivated bivalves.

Although Perkinsus sp. was detected at both CB and AE farms, the overall growth and physiological results obtained in this experiment suggest that the C. gigas strain possessed resistance to the pathogen. This because any drastic reduction in the oyster survival was observed, coinciding with Villanueva-Fonseca & Escobedo-Bonilla, (2013) working with C. gigas in the Gulf of California and with Encomio et al. (2005) comparing Perkinsosis-resistance oyster stocks from the Gulf of Mexico. In addition to high survival, resistant populations may maintain low-to-moderate prevalence and intensities of infections (Villalba et al., 2004), as was observed in this study. Perkinsus sp. incidence was determined from the first culture month, which indicated that oyster could have acquired the parasite by direct contact with the water, where wild and cultivated bivalves populations possibly already infected could be found. For instance, Góngora-Gómez et al. (2016) reported wild specimens of the pen shell Atrina maura infected with Perkinsus sp. close to one of the studied farm located at the north coast of Sinaloa. Meanwhile, Villanueva-Fonseca & Escobedo-Bonilla (2013) Escobedo-Bonilla the parasite in C. gigas cultivated in one of the experimental farms from this study. It suggests that although the oyster seed used in this work was guaranteed pathogen-free by the CIBNOR lab, Sonora, the prevalence results pointed out that the parasite was already present in the farm locations.

In this study, the range of prevalence found in the CB (26.6-83.3 %) and AE (40-73.3 %) farms were higher than those reported by Villanueva-Fonseca & Escobedo-Bonilla (2013) and Enríquez-Ezpinoza et al. (2015) in C. gigas (3-40 % and 3-60 %, respectively) by Cáceres-Martínez et al. (2008) in C. corteziensis (1-6 %), and by Cáceres-Martínez et al. (2012) in Sacosstrea palmula (7-20%). Nevertheless, our values are comparable with found by Luz & Boehs (2016) in C. rhizophorae (50-88 %), but lower than those obtained by Huicab-Pech et al. (2012) in C. virginica (70-100 %). For the intensity of infection, our results at both sites showed a very light to light range (0.2-1.2), which was lower than those aforementioned studies.

Perkinsus sp. incidence and biometrics, survival and CI

Shell heights continuously increased over time until the ninth culture month in both locations. In March, oysters from CB and AE reached 101.6 ± 6.5 and 96.1 ± 9.1 mm in SH, respectively, and there were no differences (t = 1.25, p = 0.24) between the farms. Prevalence displayed negative correlation values with SH for oysters cultivated in CB (r = -0.25, p = 0.22) and AE (r = -0.00, p = 0.52), but no relation was detected between these parameters (Fig. 2). Body weights (t = 2.55, p = 0.03) and survivals (t = -4.64, p = 0.00) varied significantly at both farms. Weight values at the end of cultivation were 117 and 101 g for CB and AE, respectively. Prevalence of Perkinsus sp. and oyster BW were no correlated at both sites (CB r = -0.29, p = 0.28; AE r = -0.05, p = 0.52) (Figura 2).


[Figure ID: f2] Figure 2.

Oyster shell height (mm) and total weight (g) and prevalence (%) of Perkinsus sp. in Crassostrea gigas cultivated at El Colorado Bay (CB) and Las Aguamitas Estuary (AE), Sinaloa, Mexico.


Survival higher than 90 % was recorded in oysters from CB and AE after 13 cultivation months. Survival did not showed significantly correlation with the prevalence of the parasite at CB (r = -0.06, p = 0.45) nor at AE (r = 0.09, p = 0.42).

Condition index of C. gigas cultivated at CBand AE displayed two (September = 72.1 and April = 60.9) and three peaks (September = 59.5, November = 64.0, and May = 54.1), respectively. However, CI were similar at both farms (t = 0.19, p = 0.85). Prevalence of Perkinsus at both locations were no correlated with the CI (CB r = -0.18, p = 0.58; AE r = -0.11, p = 0.52).

Previous experiences cultivating C. gigas in the southeastern of the Gulf of California (Góngora-Gómez et al., 2012; Rodríguez-Quiroz et al., 2016) indicate that commercial size of the Japanese oyster is reached between 7 and 8 months, which coincide with this work in both culture sites. The rapid SH growth of the oyster seeds suggests that the progeny from the CIBNOR broodstock may be a useful aquaculture strain, particularly in oyster farms from the southeastern Gulf of California, where Perkinsus spp. has been detected (Villanueva-Fonseca & Escobedo-Bonilla, 2013; Góngora-Gómez et al., 2016). The higher condition index values obtained in this study during the first months in oysters from both farms, maybe attributed to the continuous increase in both SH and BW (Encomio et al., 2005), which was related to the food availability. At the same time, the CI was correlated with food sources and nutrient content of oysters suggesting nutrient utilization for somatic and shell growth. However, there is not clear evidence that Perkinsus sp. presence had a significantly negative effect on CI. It seems that environmental influences on CI were likely greater than effects of the parasite, coinciding with findings by Dittman et al. (2001) and Encomio et al. (2005).

Perkinsus sp. incidence and biochemical composition

Triglycerids, lipids, and proteins were significantly different (t= -3.12, p=0.01; t= -2.98, p = 0.01; t = 3.00, p = 0.01, respectively) at the two culture sites showing the higher values in September for CB (81.7, 288.7 and 540.7 mg g-1, resp.), and in December (45.3 mg g-1 for triglycerids), September (184.8 mg g-1 for lipids), and February (564.1 mg g-1 for proteins) for the oysters cultivated at AE farm. Carbohydrates were similar (t=1.69, p=0.12) at both locations.

Perkinsus sp. prevalence was not significantly correlated with triglycerides (CB r = 0.26, p = 0.61; AE r = 0.32, p = 0.26), lipids (CB r = 0.26, p = 0.58; AE r = 0.15, p = 0.49), proteins (CB r = 0.28, p = 0.65; AE r = -0.12, p = 0.70), nor with carbohydrates composition of oysters at both farms (CB r = -0.10, p = 0.87; AE r = 0.19, p = 0.84) (Figura 3).


[Figure ID: f3] Figure 3.

Concentration of triglycerides, lipids, proteins, and carbohydrates (mg g-1, dw), and prevalence (%) of Perkinsus sp. in Crassostrea gigas cultivated at El Colorado Bay (CB) and Las Aguamitas Estuary (AE), Sinaloa, Mexico.


The Spearman’s rank order correlations (r) for the parasite and environmental parameters for the oysters from the CB and AE farms indicated that incidence of Perkinsus sp. in CB was correlated with the oyster protein (r = 0.62, p = 0.03), lipids (r = 0.65, p = 0.02), and triglycerids (r = 0.67, p = 0.02) concentrations, meanwhile, incidence of the protozoan in AE was correlated with oyster survival (r = 0.72, p = 0.01), but shown negative correlation with BW and SH (r = -0.70, p = 0.01 and r = -0.72, p = 0.01, respectively).

Biochemical studies with bivalves state that when food is abundant, it is used for growth and stored for reproduction in the form of proteins, lipids, and carbohydrates (Ojea et al., 2004; Dridi et al., 2007). As observed by Berthelin et al. (2000), proteins were the major component throughout the cycle in the oysters cultivated in CB and AE sites, and registered a peak during the summer-autumn months in a similar trend of the CI, suggesting mobilization of that nutrient source during growth. Then, subsequent two smaller peaks of proteins were obtained. Although at a lower level, the similar pattern was observed for lipids increasing the first three months when oyster gonads are developed (Berthelin et al., 2000). Carbohydrate content can be considered as bioindicators of environmental status reflecting the oyster capacity to sustain exogenous stress (Dridi et al., 2007) including Perkinsus sp. incidence. Although no significant correlation was found between the presence of parasite with the carbohydrate level of oysters, their curves displayed coincidences for some months suggesting a possible effect of this energy source in the parasite. The concentration values for all biochemical components tested suggest an adequate amount of energy for supporting the general oyster metabolism, including the presence of Perkinsus sp at the prevalence and intensity levels.

Perkinsus sp. occurrence and water parameters

With exception of depth and transparency, all water parameters were similar at both CB and AE farms. Temperatures were not significantly different (t = -1.88, p = 0.09) at the two culture sites showing the maximum values in the summer months (30.3 °C in June-July 2013 for CB, and 30.8 °C in June 2014 for AE), and minimum in December (CB = 19.7 °C, AE = 22.5 °C). In both farms, Perkinsus sp. prevalence was not related to the temperature (CB r = 0.28, p = 0.68; AE r = -0.34, p = 0.25). Salinities were not different (t = -0.59, p = 0.57) between CB and AE, ranging from 30 to 38.6, and 30.3 to 35.6 UPS, respectively. There was no correlation between prevalence of the parasite and salinity in both farms (CB r = 0.25, p = 0.64; AE r = 0.23, p = 0.67).

The concentrations of DO in CB and AE were similar (t = 0.40, p = 0.70) and fluctuated from 3.1 mg L-1 found in autumn, to 8.1 mg L-1 obtained in spring. Prevalence of parasite in CB (r = 0.16, p = 0.83) and AE (r = -0.04, p = 0.90) was not influenced by the OD level. The pH tendency showed similar performances between both farms (t = 0.14, p = 0.89) ranging from 6.5 to 8.2 for CB, and from 7.5 to 8.1 for AE. No significant correlation was found between the prevalence of Perkinsus sp. and the pH values in both farms (CB r = 0.08, p = 0.59; AE r = 0.19, p = 0.43).

Depth and transparency were different at both Colorado Bay and Estero Las Aguamitas (t = -11.58, p = 0.00 and t = -3.69, p = 0.00, respectively); the higher values were obtained for the AE farm (3.9 m depth and 1.9 m transparency). As for the aforementioned physical and chemical parameters, prevalence of the parasite was not correlated with depth (CB r = 0.46, p = 0.15; AE r = 0.21, p = 0.39) nor transparency (CB r = 0.45, p = 0.12; AE r = 0.47, p = 0.19) in both farms.

There were no significant differences between the concentration of Cla (t = 0.59, p = 0.56), TSS (t = -1.50, p = 0.16) and POM (t = -0.77, p = 0.46) in the CB and AE locations; the higher values of these food sources were observed during the winter months. Prevalence of Perkinsus sp. was not correlated with Cla (CB r = 0.09, p = 0.79; AE r = -0.23, p = 0.82), TSS (CB r = -0.22, p = 0.44; AE r = 0.51, p = 0.19), and POM (CB r = -0.21, p = 0.36; AE r = 0.69, p = 0.05) in both farms.

The presence of the genus Perkinsus is associated to surface mean water temperatures above 25 °C (Guo & Ford, 2017) that reaches until 30 to 32 °C in summer, which is characteristic in the oyster farms located in the southeastern of the Gulf of California (Rodríguez-Quiroz et al., 2016; Villanueva-Fonseca et al., 2017). In fact, moderate fluctuations of temperature and salinity can be found during annual culture cycles in such region (Góngora-Gómez et al., 2015, 2016), which was confirmed in this work. The higher temperatures (29.7-30.7 °C) during the first three months could also have promoted the fast occurrence of Perkinsus sp. on both sites, which was reflected in higher prevalence values (between 60 to 80%) obtained from July to August 2013. This coinciding with Ragone Calvo et al. (2003) and Villanueva-Fonseca & Escobedo-Bonilla, (2013), whose observed the higher parasite proliferation during the warmest culture months in C. virginica and C. gigas, respectively. Salinities above 12 UPS are associated with the presence of Perkinsus sp. in oysters (Ragone & Burreson, 1993). La Peyre et al. (2006) concluded that salinities above 15 UPS promote Perkinsus sp. metabolic activity, which coincides with the obtained results in both farms. Since water temperature and salinity are considered the key environmental factors that govern the incidence of this protozoan (Choi & Park, 2010), there is not available punctual information that study the relationship of this pathogen (Fernández-Robledo et al., 2014) for adequate comparisons.

With regard to food quantity and quality, the nutrient levels found in C. gigas suggest that the energy content was enough to fulfill oyster physiological requirements even with the presence of the parasite at the incidences found in both farms. Lucas & Beninger (1985) and Oliver et al. (1998) mention that the quantity of food may improve the oyster physiological condition reinforcing its immunology. Still, both food aspects (quality and quantity) should be studied in relation to the presence of Perkinsus in wild and cultivated bivalve populations.

Conclusions

The Pacific oyster cultivated at the north-central shoreline of Sinaloa showed a low susceptibility to Perkinsus sp. The overall results suggest that the occurrence of Perkinsus sp. in C. gigas was due to the previous presence of the parasite in the farm locations. Similarly, the low rates of Perkinsus sp. incidence in the oyster studied at both farms indicate that the presence of this pathogen would not threaten the aquaculture industry within the study area. Finally, it is recommended to integrate other techniques such as PCR and histology to better evaluate and understand the effect of this parasite on oyster performance and continue with monitoring of this parasite.


1.

fn1Cite this paper: Góngora-Gómez, A. M., Rubio-Zepeda, F., SantamaríaMiranda, A., Villanueva-Fonseca, B. P., Domínguez-Orozco, A. L., Villanueva-Fonseca, L.C., HernándezSepúlveda, J. A., Rodríguez-González, H., Espinosa-Alonso, L. G., García-Ulloa, M. (2019). Perkinsus sp. on Crassostrea gigas performance cultivated in the southeastern Gulf of California. Revista Bio Ciencias 6, e681. doi: https://doi.org/10.15741/revbio.06.e681

Acknowledgments

The authors wish to express their gratitude to the Instituto Politécnico Nacional (IPN), the Secretaría de Investigación y Posgrado (SIP-IPN), the Comisión de Operaciones y Fomento de Actividades Académicas (COFFA-IPN), and the Estímulo para el Desempeño de los Investigadores (EDI-IPN) for funding and logistic support (SIP-IPN 20160455 and 20160456)

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Revista Bio Ciencias, Año 12, vol. 8,  Enero 2021. Sistema de Publicación Continua editada por la Universidad Autónoma de Nayarit. Ciudad de la Cultura “Amado Nervo”,  Col. Centro,  C.P.: 63000, Tepic, Nayarit, México. Teléfono: (01) 311 211 8800, ext. 8922. E-mail: revistabiociencias@gmail.com, revistabiociencias@yahoo.com.mx, http://revistabiociencias.uan.mx. Editor responsable: Dr. Manuel Iván Girón Pérez. No. de Reserva de derechos al uso exclusivo 04-2010-101509412600-203, ISSN 2007-3380, ambos otorgados por el Instituto Nacional de Derechos de Autor. Responsable de la última actualización de este número Dr. Manuel Iván Girón Pérez. Secretaria de Investigación y Posgrado, edificio Centro Multidisciplinario de Investigación Científica (CEMIC) 03 de la Universidad Autónoma de Nayarit. La opinión expresada en los artículos firmados es responsabilidad del autor. Se autoriza la reproducción total o parcial de los contenidos e imágenes, siempre y cuando se cite la fuente y no sea con fines de lucro.

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