Southern California Bight 2003 Regional Monitoring Program: IV. Demersal Fishes and Megabenthic Invertebrates
VII. Ectoparasitism of Fishes Introduction
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VII. Ectoparasitism of FishesIntroductionEffluent pollution, generally organic material, has the potential to adversely affect fishes and invertebrates through effects such as oxygen depletion (Tsai 1973). Exposure to pollution may result in stress, which could potentially decrease the immune response in fishes and increase their susceptibility to diseases and parasites (Ellis 1981, Adams 1990). A variety of organisms have been evaluated as potential biological indicators of pollution in the aquatic environment, such as polychaetes, mollusks, and fishes (Wolfe 1992 Doherty et al. 1993, Wilson 1994, George-Nascimento et al. 2000). However, due to the range of contaminants, concentrations, and exposure time that marine organisms experience, it is unclear which organisms and which anomalies are best used as indicators. Many of these studies measured the amount of toxins, such as heavy metals, accumulated in the tissues of the indicator species (Doherty et al. 1993, Cross et al. 2001). Cross et al. (2001) found that the quality of the larval stage of a parasitic marine trematode (the cercariae), in terms of horizontal swimming rate and longevity, was reduced when development occurred within a metal-accumulating host. They speculated that the cercarial tegument, which is specialized for absorption in the endoparasitic environment, was responsible for quick metal accumulation and thus suggested that cercariae may be excellent indicator organisms for heavy metal pollution. Others have used low reproductive output (k) factors, anemia, and low blood hemoglobin and lymphocyte levels as indicators of stress in fish (Barker et al. 1994, George-Nascimento et al. 2000). Perkins (1995) illustrated effects of wastewater on three target species of marine fishes: bigmouth sole, hornyhead turbot, and white croaker. The fishes collected close to the outfall suffered severe liver neoplasms compared to those collected further away from the outfall. In addition, fin erosion in some flatfishes appears to be directly associated with discharge of municipal effluent (Mearns and Sherwood, 1977). Many studies have used fin erosion, tumors, and lesions as indicators of environmental stress (Mearns and Sherwood 1977, Siddall et al. 1994, Sures et al. 1997; Landsberg et al. 1998, George-Nascimento et al. 2000). George-Nascimento et al. (2000) found lesions and impaired blood values, such as low hemoglobin, total plasma protein, and lymphocytes, in flounder (Paralichthys spp.) at heavily polluted sites. The historical decrease in abundance or complete absence of a species, such red brittlestar, has also been used as an indicator of sediment contamination (OCSD, 2006). Conversely, the presence and consistent abundance of specific organisms in routine monitoring indicate stable habitat quality (OCSD, 2006). More than a hundred papers have established a correlation between parasitism and pollution in marine fishes (Khan and Thulin, 1991). Williams and MacKenzie (2003) discuss eight major reviews and give a literature update for the period 1995-2001 on the use of marine parasites as potential indicators of pollution. They proposed 10 criteria for selecting parasites as indicator/monitoring species, as follows: 1) the ecology of the study areas should be well known from research over a long period, 2) both host and parasite should be readily available for study throughout the year and over a number of years using cost-effective methods, 3) host and parasite should be readily identifiable without the aid of time-consuming methods, 4) problems regarding possible sampling of different host and parasite populations should be taken into consideration, 5) the ecology and life-cycles of both host and parasite should be well known, 6) there should be consistency in the use of ecological terms, for example those in Bush et al. (1997), 7) the pollutant(s) should be identifiable and their possible effects on both host and parasite considered relative to those of almost 30 biotic and abiotic factors, 8) selection should focus on host/parasite systems with large geographical and ecological ranges, but also where populations might be restricted in their migrations within this range, and sampling should occur where conditions are thought to be optimal for host and parasite as well as near the limits of the parasite’s geographical range, 9) wherever possible the indicator parasite(s) should be used in conjunction with one or more of about 50 other techniques used for monitoring the biological effects of pollution, and 10) host/parasite systems for which it might be possible to investigate the complex interactions between pollutant, immune response and parasites when interpreting results should be selected (Williams and MacKenzie 2003). Few have used host organisms and ectoparasites as indicators of effluent pollution in southern California (Mearns and Sherwood 1977; Perkins and Gartman 1997; Kalman 2001, 2006a,b; Hogue and Paris 2002; Hogue and Peng 2003). Parasites are potentially good candidates for indicator species in the marine environment because 1) there are more parasitic than free-living species, 2) many have complex life cycles with multiple stages, each with potential as an indicator, and 3) there is likely varying species resistance to pollution (MacKenzie 1999). A change in parasite levels of infection may serve as an early warning of deteriorating environmental conditions before a large number of species are seriously affected (MacKenzie 1999). Many biotic and abiotic factors influence the prevalence and mean intensity of fish parasites. Field and laboratory research indicates that the incidence and intensity of infestation of ectoparasites are enhanced by exposure to environmental pollution (Mearns and Sherwood, 1977, Siddall et al. 1994, Perkins and Gartman 1997, Landsberg et al. 1998, MacKenzie 1999). However, many of these studies were conducted on a small scale in terms of location (i.e., restricted to a single location or area) or targeted a single host and/or parasite species. Perkins and Gartman (1997) determined the prevalence (percentage of fishes parasitized) of the eye copepod (Phrixocephalus cincinnatus), on the Pacific sanddab in southern California to be highest at areas nearest to effluent discharge. However, Mearns and Sherwood (1977) found the prevalence of the eye copepod on Pacific sanddab to be lowest in more polluted areas (Santa Monica Bay to San Pedro Bay) and highest in cleaner areas to the north and south. They speculated that because the parasite feeds on the vascular supply of choroid tissue of the eye of the fish host, the elevated levels of chlorinated hydrocarbons in the tissues of the host may have been related to the absence of parasitized individuals in more polluted areas. Landsberg et al. (1998) showed that ecto- and endoparasites of the silver perch (Bairdiella chrysoura) respond differently to different environmental stressors. They found that responses of specific parasite groups vary according to different environmental stressors; monogeneans with temperature, nematodes with contaminants, protists with low dissolved oxygen, and crustaceans with salinity and metal contaminants (Landsberg et al. 1998). They suggested that parasites of fishes are useful biomarkers because the parasites themselves appeared to be more sensitive to environmental stressors than did the fishes. MacKenzie (1999) concluded that as a general rule, endoparasites, with complex indirect life cycles, tend to decrease with increasing levels of pollution, whereas ectoparasites, with direct single-host life cycles, tend to increase with increasing levels of pollution. The present study evaluates the conditions around wastewater outfalls in terms of infestation of ectoparasites on fishes and examines whether specific parasite and/or host species can be used as bioindicators of environmental stress. The Southern California Bight (SCB) provides an ideal area in which to examine the impact of effluent pollution on fishes and their corresponding parasites. While it is widely known that the southern California marine environment has been subjected to numerous inputs of pollution, such as wastewater effluent, storm runoff, Dichloro-diphenyl-trichloroethane (DDT), and Polychlorinated Biphenyls (PCBs; Dorsey et al. 1995, Stull 1995, Schiff 2000, Schiff et al. 2000, Allen 2006b), little is known about the effects of pollution on parasites of marine fishes in the SCB. In addition, it is unclear to what degree parasites cause stress to their host and what long-term damage occurs to host physiological responses. Chronic stress can inhibit an organism’s normal physiological response to the environment. Thus, fishes may be subjected to two major forms of environmental stress in the SCB: parasites and poor water quality. A detailed investigation of the parasite community in outfall areas may provide important knowledge about the influence of environmental variables on parasite-host relationships. Because of the importance of the soft-bottom fish fauna to fisheries and to environmental assessments of human activities on the continental shelf, the biology and ecology of soft-bottom fishes have been relatively well studied (Allen 2006a). In addition, studies have shown flatfishes and scorpionfishes to be infested with monogeneans, leeches, copepods, and isopods (Causey 1960; Cressey 1969; Ho 1972a, 1972b; Mearns and Sherwood, 1977; Dojiri, 1979, 1981; Dojiri and Brantley 1991; Allen et al. 1998; Kalman 2001, 2003, 2006a,b). In 2003 (July through September), through a joint project with University of California Los Angeles (UCLA), the Orange County Sanitation District-Ocean Monitoring Program, and SCCWRP, fishes collected during Bight '03 and the permit-required monitoring programs of the four major sanitation districts (HY, LA, OC, and SD) were examined for ectoparasites. The goals of this project were to assess the parasite community 1) in the SCB, 2) regionally, 3) by outfall type (large, small, and nonoutfall), and 4) across the four large-outfalls. Furthermore, the use of specific parasite and host species as bioindicators of environmental stress in the SCB was investigated. Additional detail on the results given below can be found in Kalman (2006b). ResultsOtter trawl sampling occurred at 79 stations at depths of 22-198 m in the SCB. Nominal coordinates and start depth for each station were reported in Appendix E-E1. Sampling encompassed the mainland shelf and northern Channel Islands from Point Conception, California, to the United States-Mexico International Border (Figure II-3). A total of 15,848 individual fish representing 34 species (including six families, 17 genera) were examined (Table VII-1). Host vouchers were deposited in the Natural History Museum of Los Angeles County (LACM 56324-1 through 56348-2). A total of 14,620 parasites composed of monogeneans (681 individuals), leeches (97 individuals), branchiurans (six individuals), copepods (12,795 individuals), and isopods (1,041 individuals) infected the host fishes (Table VII-2). The parasites consisted of three species of monogeneans (representing two orders, three families, three genera), four species of leeches (representing one order, one family, one genus), one species of branchiuran (Argulidae), 26 species of adult copepods (representing two orders, six families, 12 genera), one larval copepod (chalimus) representing a single family (Caligidae), two species of adult isopods (representing one order, one family, one genus), and two larval isopods (aegathoid and praniza) representing two families (Cymothoidae and Gnathiidae, respectively; Appendix E-E2). Host-parasite and parasite-host tables are presented in Appendix E-E3 and E-E4, respectively. Parasite vouchers were deposited at the U.S. National Parasite Collection (monogeneans; USNPC 97856 through 97858), the Smithsonian National Museum of Natural History (leeches; USNM 1086228 through 1086230), and the Natural History Museum of Los Angeles County (crustaceans; LACM CR 2003-018.1 through 2003-041.1). Southern California Bight (SCB)Total parasitization was calculated for individual host fishes collected at 79 stations throughout the SCB and ranked in order of highest to lowest prevalence (Table VII-3). The prevalence ranged from 0% to 100% and the mean intensity ranged from 0.0 to 48.2. Of fishes with parasites, longspine combfish had the lowest prevalence (0.2%) and fantail sole had the highest prevalence (100%); C-O sole, Gulf sanddab, and rex sole had the lowest mean intensity (1.0) and California scorpionfish had the highest mean intensity (48.2). No parasites were found on 11 host species. However, other species, such as Pacific sanddab, bigmouth sole, and California halibut, carried as many as 11 species of parasites (Appendix E-E3). Three new species of leeches (Austrobdella spp. 1-3) and one new species of parasitic copepod (Parabrachiella spp. 1) were found in this study. In addition, 56 new host records are reported (Appendix E-E3 and E-E4). RegionHost species totals were separated by four regions within the SCB (Northern Channel Islands, Northern Mainland Shelf, Central Mainland Shelf, and Southern Mainland Shelf; Table VII-4). Six of 34 species of hosts were collected in all four Regions: longspine combfish, Pacific sanddab, speckled sanddab, Dover sole, English sole, and curlfin sole. Northern Channel Islands consisted of 13 stations, Northern Mainland Shelf consisted of one station, Central Mainland Shelf consisted of 44 stations, and Southern Mainland Shelf consisted of 21 stations (Figure II-3). The total number of stations in which each host was collected was calculated for each Region (Table VII-5). Total parasite prevalence and mean intensity were calculated for each host species for each Region in which it was collected (Tables VII-6 and VII-7, respectively). There was a significant difference in median prevalence for three host species by Region (p ≤0.05: Pacific sanddab, p=0.0281; speckled sanddab, p=0.0293; hornyhead turbot, p=0.0002), and there was a significant difference in median mean intensity for three host species by Region (p ≤0.05: Pacific sanddab, p=0.0051; bigmouth sole, p=0.0296; English sole, p=0.0449). The total prevalence and mean intensity for Pacific sanddab in all four Regions was 12.7% and 1.4 (n=497, 3 stations) on the Northern Channel Islands, 19.4% and 1.1 (n=36, 1 station) on the Northern Mainland Shelf, 5.5% and 1.1 (n=4,132, 43 station) on the Central Mainland Shelf, and 5.0% and 1.2 (n=1,437, 18 stations) on the Southern Mainland Shelf (Tables VII-5 to VII-7). The total prevalence for speckled sanddab in all four Regions was 18.2% (n=55, 1 station) on the Northern Channel Islands, 10.9% (n=165, 1 station) on the Northern Mainland Shelf, 44.2% (n=443, 17 stations) on the Central Mainland Shelf, and 28.7% (n=522, 10 stations) on the Southern Mainland Shelf (Tables VII-4 through VII-6). The total mean intensity for bigmouth sole in the two Regions in which it was collected was 2.6 (n=101, 33 stations) on the Central Mainland Shelf, and 4.6 (n=32, 11 stations) on the Southern Mainland Shelf (Tables VII-5, VII-6, and VII-8). The total mean intensity for English sole in all four regions was 2.6 (n=24, 4 stations) on the Northern Channel Islands, 1.2 (n=19, 1 station) on the Northern Mainland Shelf, 2.2 (n=396, 32 stations) on the Central Mainland Shelf, and 1.4 (n=124, 7 stations) on the Southern Mainland Shelf. The total prevalence for hornyhead turbot in the two Regions in which it was collected was 64.5% (n=313, 41 stations) on the Central Mainland Shelf and 97.1% (n=35, 12 stations) on the Southern Mainland Shelf (Tables VII-5 through VII-7). Host-parasite prevalence and mean intensity were calculated for each Region (Appendix E-E5 and E-E6, respectively). There was a significant difference in median prevalence for three parasite species by Region (p ≤0.05: the copepod Clavella parva on stripetail rockfish, p=0.0453; the copepod Holobomolochus prolixus on speckled sanddab, p=0.0497; the leech Austrobdella spp. 2 on hornyhead turbot, p=0.0272). The Kruskal-Wallis test showed a significant difference in median mean intensity for five parasite species by Region (p ≤0.05: the copepod Naobranchia scorpaenae on California scorpionfish, p=0.0009; the eye copepod (Phrixocephalus cincinnatus) on Pacific sanddab, p=0.0006, the monogenetic trematode Neoheterobothrium hippoglossini on bigmouth sole, p=0.0260; gnathiid isopod praniza on bigmouth sole, p=0.0374; the copepod Taeniacanthodes haakeri on hornyhead turbot, p=0.0285). Table VII-1. Host fish taxa collected at depths of 22-198 m in the Southern California Bight, July-October 2003. 
Table VII-2. Classification and group totals of parasites on fishes collected at depths of 22-198 m in the Southern California Bight, July-October 2003. 
Table VII-3. Total parasite prevalence and mean intensity for all host fish species collected from 79 stations at depths of 22-198 m in the Southern California Bight (SCB), July through October 2003, with host fishes ranked in order of highest to lowest prevalence. 
Table VII-4. Host totals by region collected at depths of 22-198 m in the Southern California Bight, July-October 2003. . 
Table VII-5. Number of stations each host was collected by Region in the Southern California Bight at depths of 22-198 m, July through October 2003. 
Table VII-6. Total parasite prevalence by Region collected at depths of 22-198 m in the Southern California Bight, July through October 2003. 
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