Parasitological Records of Eight Rockfish Species (Scorpaeniformes:Scorpaenidae) from Pacific Baja California, Mexico

Abstract

This study reports parasitological records of eight species of marine rockfishes (Sebastes auriculatus, S. chlorostictus, S. umbrosus, S. miniatus, S. atrovirens, S. constellatus, S. serranoides, and Scorpaena guttata) collected from Todos Santos bay and San Quintin coast, Baja California, Mexico. The vermilion rockfish, S. miniatus, showed the highest parasite species richness (two species of monogeneans, two species of digeneans, three species of nematodes and one species of copepods), while the lowest richness was found in S. atrovirens and S. umbrosus (one species of copepod and one species of nematode, respectively). The species S. auriculatus, S. chlorostictus, S. constellatus, S. serranoides, and S. guttata showed a richness of up to four parasite species. Seven of the eight fish species (except S. atrovirens) presented larval stages of nematodes Anisakis sp., Pseudoterranova sp. and Hysterothylacium sp. (prevalences ranging from 8.3 to 100%), which were found in the fish mesentery (guts). The parasite species with the highest prevalence values (>80%) were found in S. miniatus (Anisakis sp.), S. guttata (Anisakis sp. and Hysterothylacium sp.), S. umbrosus (Anisakis sp.), S. auriculatus (Anisakis sp.), and S. constellatus (Anisakis sp.). The most abundant parasite species (>4 ind./host) were recorded in S. guttata (Anisakis sp. and Hysterothylacium sp.), S. umbrosus (Anisakis sp.), S. constellatus (Parabothriocephalus sagitticeps), and S. miniatus (Anisakis sp.). The parasite species with the highest intensity of infection values (>5 ind./host) were found in S. constellatus (P. sagitticeps), followed by S. guttata (Anisakis sp., Hysterothylacium sp.), S. umbrosus (Anisakis sp.), and S. serranoides (Microcotyle sebastis). The present study, in addition to listing the helminths and parasitic copepod species (and providing quantitative data on them) of eight commercially important scorpaenid fish species in the northwestern Mexico, can also serve as a baseline for future parasitological studies on these fish species.

Rockfish (Scorpaenidae) inhabit depths up to 1,000 m, and due of their slow growth, long lifespan, and late sexual maturity are sensitive to over-exploitation, and some species are considered endangered along the California coast (Love et al. 2002). From the North Pacific to Gulf of California there are currently 102 species of rockfish, while 67 of them are reported from Baja California, Mexico (Love et al. 2000). In California, USA, the rockfish catch began in 1849 (Gold Rush) and until now continues, although it has substantially declined (Love et al. 1998, 2000). Rockfish are valued resources in the North Pacific around Baja California, contributing 30% of the total commercial fish catch (Rosales-Casián and González 2003); also, rockfishes are valued for sportfishing, with the vermilion (Sebastes miniatus) as the most abundant species (Rodríguez-Santiago and Rosales-Casián 2008). However, few studies of parasites of rockfish are available.

A study from California-Baja California border to "San Quintin" (300 km south) examined three rockfish species (Sebastes elongatus, S. helvomaculatus, and S. rosaceus) and identified at least eight parasite species with nematodes as dominant group (Alvarado-Villamar and Ruíz-Campos 1992). At the "San Quintin" coast, the parasite community was studied in the vermilion rockfish (S. miniatus), and a total of 12 parasite species was found, with nematodes as the most prevalent group (Rodríguez-Santiago et al. 2014). In similar studies of other fish species from Northern Baja California, such as California halibut (Paralichthys californicus), 14 parasite species were identified (Castillo-Sánchez et al. 1998), among them a new genus and new species of trematode, Cicesetrema unami (Pérez-Ponce de León et al. 1999). In the ocean whitefish Caulolatilus princeps, six species of parasites were identified (Rodríguez-Santiago and Rosales-Casián 2011).

The aim of this study was to document parasitological records in eight Scorpaeniform marine fish species (belong to the genera Sebastes and Scorpaena) from the "Todos Santos" bay and the "San Quintin" coast at Pacific Baja California, Mexico. This study, in addition to including a list of parasite species, also reports their infection parameters (prevalence, intensity, and abundance) for each of the examined hosts.

Materials and methods

The individuals of rockfish were obtained from the commercial catch at "Todos Santos" bay (30° 29′ 52″ N–116° 07′ 5400″ W) and from sportfishing along "San Quintin" coast (30° 20′ 25″ N–115° 59′ 20″ W), Baja California, Mexico (Figure 1). In the laboratory, the specimens were measured (total length in millimeters) and weighed (g). The chosen rockfish species were: brown rockfish (Sebastes auriculatus), greenspotted rockfish (S. chlorostictus), honeycomb rockfish (S. umbrosus), vermilion rockfish (S. miniatus), kelp rockfish (S. atrovirens), starry rockfish (S. constellatus), olive rockfish (S. serranoides), and California scorpionfish (Scorpaena guttata). Fish organs (gills, intestinal caeca, stomach, intestine, mesentery, skin, fins, and coelomic cavity) were separated using a dissection microscope and placed on petri dishes with saline solution at 0.65% and fixed using 96% ethanol (see detailed method in Guzmán-Cornejo et al. 2012) at the Fisheries Ecology Laboratory at the Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE), Baja California, Mexico.

Samples were transported to the Environmental Laboratory at the Centro de Investigación de Ciencias Ambientales de la Facultad de Ciencias Naturales, Universidad Autónoma del Carmen, Ciudad del Carmen, Campeche for the parasitological assessment. The organs were reviewed by compression between 10 cm square glasses using a Discovery V8 Zeiss stereoscopic microscope and a Motic compound microscope. Helminths were fixed in acetic acid–formaldehyde–alcohol (AFA) solution for 2–24 h. Then, they were preserved in ethyl alcohol (70%) and stained with Gomori's trichromic stain. Nematodes were fixed in Berland's liquid, preserved in ethyl alcohol (70%), and cleared with a solution of phenol–ethanol (Lent's solution) and mounted on slides covered with glycerin-gelatin. Copepods were first fixed in

Figure 1.

Location of the study area at "Todos Santos" bay and "San Quintin" coast, Baja California, Mexico. Dots (●) show the locations of catches.

ethyl alcohol (70%), and then, they were cleared using a solution of glycerin-alcohol and mounted on slides covered with glycerin-gelatin (Guzmán-Cornejo et al. 2012). After obtaining the morphological data, identification of helminths was identified according to keys proposed by Yamaguti (1958, 1961, 1963); Schell (1970), and Crane (1972) for Trematoda; Yamaguti (1959, 1963) for Cestoda and Acanthochephala, respectively; Yamaguti (1961), for nematodes Davey (1971) and Anderson et al. (1974–1983). To identify the parasitic copepods keys of Cressey and Boyle-Cressey (1980, 1985); Kabata (1970a, 1970b, 1979, 1992a, b) and Boxshall (2004) were used. The parasitological material was deposited in the Laboratory of Parasitology, Faculty of Natural Sciences, of the Universidad Autónoma del Carmen and a voucher of specimens was also deposited at the Colección Nacional de Helmintos, Instituto de Biología, Universidad Nacional Autónoma de México (Mexico). The prevalence, intensity of infection and abundance was determined for each parasite species according to Bush et al. (1997).

To determine whether the parasite species richness is influenced by the host size and weight, Spearman rank correlation analyses were performed for each scorpaenid species (Rodríguez-Santiago et al. 2014).

Table 1.

Parasite Species of Rockfishes from "Todos Santos" bay and "San Quintin" coast, Baja California, Mexico

Results

A total of 96 fish host from the eight species (n = 12 individuals each species) were examined. From all fish, 12 parasite species was identified (Table 1), three monogeneans (Microcotyle sebastis, Megalobenedenia derzhavini and Neobenedenia melleni), two digeneans (Fellodistomum sebastodis and Parahemiurus merus), three nematodes (Anisakis sp., Pseudoterranova sp., and Hysterothylacium sp.), one cestode (Parabothriocephalus sagitticeps), and three copepod species (Neobrachiella robusta, Caligus hobsoni, and Lepeoptheirus sp.). The nematode Anisakis sp. parasitized six host fish species, except S. atrovirens and S. guttata; while the nematode Hysterothylacium sp. infected five species except S. atrovirens, S. umbrosus, and S. constellatus (Table 1). The monogenean Microcotyle sebastis was located in four fish species (Table 1). The highest parasite species richness was found in S. miniatus with eight species, while the lowest richness was in S. umbrosus and S. atrovirens with only one species (Table 2). The most abundant parasite (Anisakis sp.) was located in the stomach, mesentery, intestine, and intestinal caeca. Digenea and Cestoda were found at the digestive tract, mainly at the stomach. The most infected organs were the stomach, pyloric caeca and intestine (Table 1). The parasite species with the highest prevalence values (>80%) were found in S. miniatus (Anisakis sp. = 92% and M. sebastis = 93%), S. guttata (Anisakis sp. = 87.5% and Hysterothylacium sp. = 87.5%), and S. umbrosus (Anisakis sp. = 83.3%) (Table 2). The most abundant parasite species were recorded in S. guttata (Anisakis sp. = 4.8 ind./host and Hysterothylacium sp. 4.5 ind./host), followed by S. umbrosus (Anisakis sp. = 4.3 ind./host), S. constellatus (P. sagitticeps = 4.2 ind./host), and S. miniatus (Anisakis sp. = 4.0 ind./host) (Table 2). The parasite species with the

Table 2.

Prevalence (P%), Abundance (Ab), and Intensity of Infection (I) of the Parasites Found in the Eight Rockfish Species Collected from "Todos Santos" bay and "San Quintin coast," Baja California

highest intensity of infection values were found in S. constellatus (P. sagitticeps = 5.6 ind./ host), followed by S. guttata (Anisakis sp. = 5.5 ind./host and Hysterothylacium sp. = 5.1 ind./ host) and S. umbrosus (Anisakis sp. = 5.2 ind./ host) (Table 2).

The parasite species richness data were not related with the host size and weight for each scorpaenid species (p > 0.05 in all cases).

Discussion

The members of genus Sebastes are found from the intertidal zone to the margin of the continental shelf, occupying nearly all the types of bottom and with a wide bathymetric distribution (Love and Moser 1983, Love et al. 1990). In the analysis of the eight Sebastes and Scorpaena species from Pacific Baja California, Mexico, there were differences in the taxa composition of macroparasites at inter- and intra-specific level. It has been inferred that the possible causes of the difference in the composition of macroparasites in different scorpaenids are due to the bionomical and ecological characteristics of the species and not to physiological differences (Love and Moser 1983). Important ecological factors may include differences in their feeding habits and individual movement (Love et al. 2000), as well as habitat selection (Love and Moser 1983).

All six rockfish species in the present study are carnivores, consuming small invertebrates and fish, and their feeding variations may be a reflection of the differences in food availability between upwelling and non-upwelling seasons, as small fishes feed on recruiting zooplankters (such as the euphausid Euphausia pacifica), which also increase with upwelling. However, there were some species which may not depend on upwelling for increased food (such as the benthic feeder S. chlorostictus), but exhibit feeding seasonality (Love et al. 1990).

The diet of Sebastes includes a variety of species (fishes, skids, octopuses, shrimps, copepods, isopods, squids, polychaetes, etc.), many of which are potential hosts for initial stages of cestodes (Rojas-Herrera et al. 2003). Similarly, adult stages of parasites also inhabit predators such as elasmobranches (Schmidt 1986) and sea lions (Lowry et al. 1991). In this respect, the Sebastes species are a part of an intermediate food web permitting the parasites to reach their maturity in the final host (Jensen 2001, Love et al. 2002). Some parasites found is these rockfishes (digeneans, cestodes, nematodes, and acanthocephalans) are possibly transmitted via ingestion of larval forms or by the presence of free-living stages of larvae in the plankton, which often determines the parasitic fauna of the host (Dogiel 1964). Monogeneans and parasitic copepods (ectoparasites), for example, can be acquired by being in contact with other intermediate hosts such as fish and crustaceans.

In the present study, the parasites found in S. auriculatus, S. atrovirens, S. serranoides, and Scorpaena guttata are first records for this geographic area. For S. constellatus, S. umbrosus, and S. chlorostictus a single parasite species (Anisakis sp.) was previously recorded at Baja California (Alvarado-Villamar and Ruíz-Campos 1992). Another study with S. miniatus reported 12 parasite species, nematodes being the most prevalent (Rodríguez-Santiago et al. 2014, 2015). Moreover, the rockfish species in the present study showed a relatively low parasite species richness compared with other species such as S. nebulosus (Southeastern Pacific) with 26 parasite species, primarily Digenea (Holmes 1990). In S. capensis (North of Chile) and S. caurinus (Pacific and Atlantic oceans) a parasite species richness of 16 and 50 was found, respectively (González and Acuña 1998). For S. serranoides at Oregon coast, the richness of 36 parasite species was correlated with host age and size, and the parasite specificity was for intestine, stomach, intestine walls, and gills (Holmes 1990). This organ specificity was also recorded in S. capensis (González and Acuña 1998). In this study, the species richness was variable between and within the rockfish species, and no relationship was found between this parasite community descriptor and the host size and weight. This may have been due to the size of the examined individuals being similar and/ or because the sample size was not large enough to detect patterns.

Similar to other Sebastes members, in the present study the nematodes (Anisakis and Hysterothylacium) and monogeneans (Microcotyle sp.) were the dominant parasite groups in terms of abundance. Only in S. serranoides, the cestodes were dominant (Love and Moser 1983, Love et al. 1984). In other Baja California rockfish (S. constellatus, S. elongatus, S. rosaceus, S. umbrosus, S. helvomaculatus, and S. chlorostictus) the nematodes (Anisakis, 65–90% of prevalence) were the dominant group, followed by the digeneans with 4.1–25% of prevalence (González and Acuña 1998). In the present study, the parasite species richness was relatively smaller than previously recorded for other scorpaenid species. However, to have a better understanding of the community of parasites that infect these host species, further studies that include more sampling locations and different times of the year are necessary. Nevertheless, this study, in addition to contributing to knowledge of the parasite biodiversity of commercially important marine fish in the northwestern Mexico, provides quantitative data that can serve as a baseline for future parasitological studies on these fish species.