The use of parasites in discriminating stocks of Pacific halibut (Hippoglossus stenolepis) in the northeast Pacific.Abstract--The use of parasites as indicators of the stock structure of Pacific halibut Noun 1. Pacific halibut - a righteye flounder found in the Pacific
righteye flounder, righteyed flounder - flounders with both eyes on the right side of the head (Hippoglossus stenolepis) in the northeast Pacific was investigated by using 328 adult (>55 cm fork length) halibut halibut: see flatfish.
Any of various flatfishes, especially the Atlantic and Pacific halibuts (genus Hippoglossus, family Pleuronectidae), both of which have eyes and colour on the right side. from 15 composite localities ranging from northern California Northern California, sometimes referred to as NorCal, is the northern portion of the U.S. state of California. The region contains the San Francisco Bay Area, the state capital, Sacramento; as well as the substantial natural beauty of the redwood forests, the northern to the northern Bering Sea Bering Sea, c.878,000 sq mi (2,274,020 sq km), northward extension of the Pacific Ocean between Siberia and Alaska. It is screened from the Pacific proper by the Aleutian Islands. The Bering Strait connects it with the Arctic Ocean. and 96 juvenile (10-55 cm) halibut from five localities ranging from the northern Queen Charlotte Islands Queen Charlotte Islands, archipelago of several large and many small islands, off the coast of W British Columbia, Canada. The main islands are Graham and Moresby. Masset on Graham Island is the main settlement. to the Bering Sea. Counts of eight selected parasite parasite, plant or animal that at some stage of its existence obtains its nourishment from another living organism called the host. Parasites may or may not harm the host, but they never benefit it. species (the juvenile acanthocephalans Corynosoma strumosum and C. villosum, the metacestode Nybelinia surmenicola, the digenean metacercaria Otodistomum sp., and the larval larval
1. pertaining to larvae.
see cutaneous and visceral larva migrans. nematodes Anisakis simplex, Pseudoterranova decipiens, Contracaecum sp., and Spirurid gen. sp.) that produce infections of long duration, do not multiply in the host, and that have a relatively high abundance in at least one geographic locality 1. locality - In sequential architectures programs tend to access data that has been accessed recently (temporal locality) or that is at an address near recently referenced data (spatial locality). This is the basis for the speed-up obtained with a cache memory.
2. were subjected to discriminant function analysis Discriminant function analysis involves the predicting of a categorical dependent variable by one or more continuous or binary independent variables. It is statistically the opposite of MANOVA. . Juvenile Pacific halibut showed no separation and, even though they were not heavily infected in·fect
tr.v. in·fect·ed, in·fect·ing, in·fects
1. To contaminate with a pathogenic microorganism or agent.
2. To communicate a pathogen or disease to.
3. To invade and produce infection in. with parasites, the analysis suggested that juveniles could be a mixed stock. Three groups of adults were identified: fish from California to the southern Queen Charlotte Islands, those from the northern Queen Charlotte Islands to the central Bering Sea, and those from the central and northern Bering Sea. These groups suggest that the single stock concept be more thoroughly evaluated.
The Pacific halibut (Hippoglossus stenolepis) is an Arctic-Boreal Pacific pleuronectid flatfish ranging throughout the North Pacific from southern California to northern Japan, but is most abundant in the Gulf of Alaska Noun 1. Gulf of Alaska - a gulf of the Pacific Ocean between the Alaska Peninsula and the Alexander Archipelago
Pacific, Pacific Ocean - the largest ocean in the world . The halibut supports one of the top five commercial fisheries in North America North America, third largest continent (1990 est. pop. 365,000,000), c.9,400,000 sq mi (24,346,000 sq km), the northern of the two continents of the Western Hemisphere. , with average annual landings of approximately 25,000 metric tons from 1991 to 1995 (IPHC IPHC International Pacific Halibut Commission
IPHC International Pentecostal Holiness Church
IPHC Internet Protocol Header Compression
IPHC Intermediate Point Headway Control (subway signaling) , 1996), and is also widely sought in the sport fishery, thus contributing significantly to west coast economies. The International Pacific Halibut Commission (IPHC) is responsible for management of the resource. From the 1930s through the 1950s the IPHC recognized at least three stocks of halibut from tagging experiments, egg and larval drift, anatomical anatomical /ana·tom·i·cal/ (an?ah-tom´i-kal) pertaining to anatomy, or to the structure of an organism.
an·a·tom·i·cal or an·a·tom·ic
1. Concerned with anatomy.
2. differences, and differences in growth rate: 1) those in the Bering Sea; 2) those from the Gulf of Alaska south to Cape Spencer Cape Spencer can refer to
1. Arrangement or formation in zones; zonate structure.
2. Ecology The distribution of organisms in biogeographic zones. in the North Pacific. Skud (1977) re-analyzed the data and concluded that there was extensive intermingling of fish among areas and that there was no evidence to indicate that fish north and south of Cape Spencer, Alaska, constituted different stocks. Available biochemical bi·o·chem·is·try
1. The study of the chemical substances and vital processes occurring in living organisms; biological chemistry; physiological chemistry.
2. evidence (Tsuyuki et al., 1969; Grant et al., 1984), although limited in scope and by sampling effort, suggests little genetic variation throughout the northeast Pacific. As a result, the IPHC manages halibut as a single population, but with statistical divisions for management of data.
Parasites have been used successfully to distinguish populations or stocks of fishes and, as a result, provide information useful in fisheries management (see reviews by Lester, 1990; Moser, 1991; Williams et al., 1992). With respect to flatfish, Gibson (1972) used parasitological parasitological
pertaining to or emanating from parasitology.
includes examination of feces for protozoa, worm eggs or larvae and for tapeworm segments, skin scrapings for arthropod parasites, blood data to distinguish three groups of Platichthys flesus Noun 1. Platichthys flesus - important food fish of Europe
righteye flounder, righteyed flounder - flounders with both eyes on the right side of the head
genus Platichthys, Platichthys - a genus of Pleuronectidae and Krzykawski and Wierzbicka (1982) used parasitological data and other information to distinguish between Barents Sea Barents Sea, arm of the Arctic Ocean, N of Norway and European Russia, partially enclosed by Franz Josef Land on the north, Novaya Zemlya on the east, and Svalbard on the west. and Labrador stocks of Greenland halibut The Greenland halibut (Reinhardtius hippoglossoides, Walbum 1792) belongs to the Pleuronectidae family (the right eye flounders), of the Pleuronectiformes (the flatfishes). , Reinhardtius hippoglossoides. Khan khan
Historically, the ruler or monarch of a Mongol tribe. Early on a distinction was made between the title of khan and that of khakan, or “great khan.” Later the term khan was adopted by the Seljuq and Khwarezm-Shah dynasties as a title for the highest et al. (1982) and Arthur and Albert (1993) used parasites to distinguish between Atlantic and Gulf of St. Lawrence Noun 1. Gulf of St. Lawrence - an arm of the northwest Atlantic Ocean off the southeastern coast of Canada
Gulf of Saint Lawrence
Atlantic, Atlantic Ocean - the 2nd largest ocean; separates North and South America on the west from Europe and Africa on the east stocks of R. hippoglossoides, and Boje et al. (1997) used parasites to indicate differences among Greenland stocks of Greenland halibut and stocks from the western Atlantic. No similar work on flatfishes has been done in the Pacific and, with the exception of Krzykawski and Wierzbicka (1982) and Boje et al. (1997), there has been no attempt to distinguish between stocks of a species across a significant portion of the species' range.
In this article, we use discriminant dis·crim·i·nant
An expression used to distinguish or separate other expressions in a quantity or equation. analysis on counts of some of the parasites from adult Pacific halibut to determine if they form discrete groups or stocks in the northeast Pacific. We do a similar analysis on the juvenile fish and compare the results to the adult analysis to determine when separation is likely to occur.
Materials and methods
A total of 328 adults (>55 cm fork length) from 15 composite localities, ranging from northern California to the vicinity of St. Matthew's Island in the Bering Sea and 96 juveniles (10-55 cm) from five localities ranging from the northern Queen Charlotte Islands to the Bering Sea (Fig. 1), were caught by staffs of the IPHC and the U.S. National Marine Fisheries Service during the summers of 1990-92 (using longlines and trawls). Most localities (for the adult samples) included fish taken from several hauls; however, 202 fish came from 13 individual hauls, each of which contained at least 10 fish. Fish were bagged individually and immediately frozen at sea for later examination.
[FIGURE 1 OMITTED]
Fish and parasites were processed by using standard parasitological techniques (see Blaylock et al., 1998a). We followed Bush et al.'s (1997) definitions for prevalence, abundance, and intensity. Parasites used in the analyses were chosen according to according to
1. As stated or indicated by; on the authority of: according to historians.
2. In keeping with: according to instructions.
3. the guidelines guidelines,
n.pl a set of standards, criteria, or specifications to be used or followed in the performance of certain tasks. of Arthur and Albert (1993). Only those species with infections of long duration, that do not multiply in the host, and that have a relatively high abundance in at least one geographic locality were used. Of the 59 parasite taxa identified from Pacific halibut (Blaylock et al., 1998a), eight taxa met these criteria: the juvenile acanthocephalans Corynosoma strumosum (body cavity body cavity
See coelom. ) and C. villosum (body cavity), the metacestode Nybelinia surmenicola (stomach wall), the digenean metacercaria Otodistomum sp. (stomach wall), and the larval nematodes Anisakis simplex (body cavity, organs, musculature musculature /mus·cu·la·ture/ (mus´kul-ah-cher) the muscular apparatus of the body or of a part.
The arrangement of the muscles in a part or in the body as a whole. ), Pseudoterranova decipiens (body cavity, organs, musculature), Contracaecum sp.(body cavity), and Spirurid gen. sp. (stomach wall). A ninth taxon taxon (pl. taxa), in biology, a term used to denote any group or rank in the classification of organisms, e.g., class, order, family. , the larval nematode nematode
Any of more than 15,000 named and many more unnamed species of worms in the class Nematoda (phylum Aschelminthes). Nematodes include plant and animal parasites and free-living forms found in soil, freshwater, saltwater, and even vinegar Hysterothylacium aduncum (body cavity and organs) was included for the analysis of juveniles.
Because individual fish varied extensively in size (fork length), and the number of a parasite individuals was strongly correlated cor·re·late
v. cor·re·lat·ed, cor·re·lat·ing, cor·re·lates
1. To put or bring into causal, complementary, parallel, or reciprocal relation.
2. with fish size (Blaylock et al., 1998a), parasite numbers were corrected for differences in host size. Counts of individual parasites were first log-transformed (ln(x+1)). To adjust for the effect of fish length, a regression of the transformed parasite numbers on fish length for each species in each locality (and haul) was calculated. This relationship was then used to adjust the number of parasite individuals within each fish in each locality (and haul) to that expected for the average-size fish in the overall sample (80.9 cm for adults, 39.2 cm for juveniles). These data were then used in discriminant function discriminant function
A function of a set of variables used to classify an object or event. analyses. We applied the most widely used (and available) method of discriminant function analysis, in which the data were divided into training and test sets, and a discriminant function calculated on the training set was used to classify clas·si·fy
tr.v. clas·si·fied, clas·si·fy·ing, clas·si·fies
1. To arrange or organize according to class or category.
2. To designate (a document, for example) as confidential, secret, or top secret. the test set. Interpretations were based on patterns in the test sets. To insure Insure can mean:
Our training set consisted of six fish randomly selected from each haul ("haul" training set) or these fish plus four from the northern Queen Charlotte Islands and six from Unimak Pass ("locality" training set). Discriminant functions calculated from data on these "training" fish were used to classify each of the remaining fish from each haul ("haul" test set) or those fish plus all remaining fish ("locality" test set). The test set fish were first classified into one of the 13 hauls or 15 localities. Classification matrices were examined for the degree of misclassification. Hauls or localities were then grouped and regrouped into four and three groups based on patterns in the 13 or 15 category analyses and the zoogeographic zones from Blaylock et al. (1998b). Analyses were then repeated. Classifications were examined for misclassification, and boundaries adjusted for retesting. Results presented are those from the best fit "test" classifications. Statistical analyses were performed in SYSTAT for Windows version 5.05 (Wilkinson et al., 1992). The entire data set from which the data for this analysis came is available for purchase from the Depository The place where a deposit is placed and kept, e.g., a bank, savings and loan institution, credit union, or trust company. A place where something is deposited or stored as for safekeeping or convenience, e.g., a safety deposit box. of Unpublished Data, Document Delivery, CISTI CISTI Canada Institute for Scientific and Technical Information
CISTI Civil Space Technology Initiative
CISTI Canadian Institute of Telecommunications Engineers , National Research Council of Canada, Ottawa, ON K1A 0S2, Canada.
Of the taxa that met the Arthur and Albert (1993) criteria, N. surmenicola was most common and abundant in northern localities and fairly common and abundant in central localities. Corynosoma strumosum, although variable in prevalence and abundance, was much more common in the northernmost localities. Corynosoma villosum, although prevalent everywhere, was more abundant in northern fish. Otodistomum sp. and Spirurid gen. sp. were more common and abundant in southern localities. Anisakis simplex, although present in virtually every fish from every locality, was more abundant in southern fish. Pseudoterranova decipiens and Contracaecum sp. appeared to be more common in central areas (Table 1). In the juveniles, A. simplex and P. decipiens were more common in central localities, whereas C. villosum, C. strumosum, and Hysterothylacium aduncum were more common in northern localities (Table 2).
The haul analyses indicated that the majority of fish from some hauls (12/14 Vancouver Island Vancouver Island (1991 pop. 579,921), 12,408 sq mi (32,137 sq km), SW British Columbia, Canada, in the Pacific Ocean; largest island off W North America. It is c.285 mi (460 km) long and c. [VI] fish, 3/4 Southeast Alaska 1 [SA1] fish, 3/5 from the Pribilof Islands Pribilof Islands (prĭb`ĭlŏf'), group of four volcanic islands, off SW Alaska in the Bering Sea, c.230 mi (370 km) N of the Aleutian Islands; explored and named in 1786 by Gerasim Pribilof, a Russian navigator. The larger islands, St. [PI], and all 4 from St. Matthew's Island [SMI (1) (Storage Management Initiative) The initiative developed by the SNIA in 2003 to create a single standard interface for storage management technologies used by multiple vendors and networking communities. ]) could be correctly classified but that fish from surrounding areas also were incorrectly classified to these hauls. Moreover, the percentage of fish correctly classified by the haul functions was, in all cases, within only a few percentage points of that correctly classified by the equivalent locality function. Thus, patterns do not appear to be associated with independent hauls. Therefore, we present only the results of the locality analyses.
Fifteen category discriminant analyses revealed severe misclassification in most areas. Only 39% were correctly classified to locality (Table 3). The functions did assign correctly the majority of test fish from two localities (19/26 from Vancouver Island [VI] and 14/22 from the southern Bering Sea [SB]). However, misclassification of fish from surrounding areas to these localities indicated less than accurate discrimination. The clearest indications from these analyses were that localities from the vicinity of the Queen Charlotte Islands south should be grouped together and that there is a suggestion that the two northern Bering Sea locations (PI and SMI) should be grouped.
Regrouping the localities into four categories by using boundaries from zoogeographic analyses (Blaylock et al., 1998b) plus the apparent northern Bering Sea grouping (PI-SMI), considerably improved the predictive ability of the functions. The "best fit" four-category grouping gave approximately 62% correct classification at the locality level (Table 4). The four-category functions were good predictors for the California-Oregon (OR) to southern Queen Charlotte Islands (SQC SQC Statistical Quality Control
SQC Singapore Quality Class
SQC Software Quality Control
SQC Sediment Quality Criteria
SQC Scottish Qualifications Certificate (record of student's academic achievements)
SQC Surface Quality Control ) fish; over 80% of these southern fish were correctly classified, and only about 6% of the other fish were misclassified to this group. Over 70% of the Pribilof-St. Matthew Island (PI-SMI) fish were correctly classified, and only 7% of the other fish were incorrectly classified to this group. There was much misclassification in the two central groups, and adjustment of the boundary between these two groups did not produce marked improvement (not shown).
Grouping into three categories by combining the two central groups resulted in substantial improvement in discrimination (83% correct) (Table 5). Shifting of the boundary between the northern and central group revealed that discrimination broke down when the southern Bering Sea (SB) was included in the northern group (not shown). Inclusion of the northern Queen Charlotte Islands (NQC NQC Not Quite C (programming language; released under Mozilla Public License)
NQC National Quartet Convention (Louisville, Kentucky)
NQC Net Qualifying Capacity (electricity) ) in the southern group had little effect (81% correct classification) (not shown). These analyses indicated a southern (OR-SQC) group, a central (NQC-SB) group, and a northern (PI-SMI) group.
Classification into two categories (with SQC as the dividing line Noun 1. dividing line - a conceptual separation or distinction; "there is a narrow line between sanity and insanity"
demarcation, contrast, line
differentiation, distinction - a discrimination between things as different and distinct; "it is necessary to ) provided no substantial improvement (87% correct) (not shown). Inclusion of NQC in the southern group had little effect (88% correct classification).
Discrimination of juveniles was poor with any organization of localities. The "best fit" classification correctly classified only 66% of the fish and there was substantial misclassification among the localities (Tables 6 and 7). Fish from the northern Queen Charlotte Islands (NQC) through Nagai Island Nagai Island is one of the largest of the Shumagin Islands in the Gulf of Alaska, south of the Alaska Peninsula considered a part of the NE Aleutian Range. It is located at , and is 31 miles long. (NI) separated reasonably well, but the majority of fish from the northernmost locality were also misclassified to this group. Note that parasite numbers and prevalences were low in the juveniles (Table 2).
Our results show four things: 1) parasites clearly differentiate a group of southern adults; 2) parasites provide some evidence for a separation of the northernmost adults; 3) the differentiation is not always unequivocal; and 4) parasites do not differentiate groups of juvenile fish.
Skud (1977) concluded that southern and northern groups mixed extensively at all ages of their life history and that, although populations of adults may be largely discrete in the summer, any such discreteness was temporary because tagging evidence suggested more extensive winter migrations associated with spawning. Our data, on the other hand, suggest that there is some merit to the IPHC's early recognition of three stocks of adult halibut. Parasite data support the existence of two major groups of halibut and suggest the possibility of a third group in the central and northern Bering Sea. The high proportion of correct classifications based on parasites suggest that these differences are well established.
Recognition of three such groups is also supported by several of Skud's (1977) observations. He presented data suggesting that after fish home to spawning areas, southern and northern fish maintain reasonably separate migration circuits between feeding and spawning grounds. Data from Skud (1977) and more recent tagging data (Geernaert, 1996) also suggest that southern fish move less than their northern counterparts. Skud also recognized a resident population in the Bering Sea. These conclusions pose two questions. First, do fish from different groups mix extensively? Second, do such groups represent reproductive units or stocks?
Our analysis was based on a small set of larval parasites, all of which are known to be long-lived and do not multiply in the host. Other long-lived parasites such as the myxosporeans have been used in stock discrimination but were not included here because of a lack of abundance data. However, the decreased ability to detect differences because of the small data set was offset by an increased ability to detect the host's past activities. Most of these parasites live for at least several years; therefore, the presence and abundance of these parasites may indicate where the host has been over that time period. At least some of the individuals of each of the parasite species, however, were probably short-term acquisitions (lasting a few years); thus, there may be some bias in the data of the recent past.
Our data suggest less extensive movement of Pacific halibut in southern areas. Because parasites are generally more abundant in the south, southern fish may be more easily classified. Nevertheless, if the southern fish mingle extensively with more northern fish, there should be more similarity Similarity is some degree of symmetry in either analogy and resemblance between two or more concepts or objects. The notion of similarity rests either on exact or approximate repetitions of patterns in the compared items. in the parasite faunas. In particular, central area fish should develop characteristics of southern fish. This did not happen, as is shown by the very low proportion of central fish misclassified as southern fish (Table 5). Our information cannot completely rule out the movement of southern fish to central areas during the spawning season, and then back to southern areas for the feeding season. Their long-lived parasite fauna fauna
All the species of animals found in a particular region, period, or special environment. Five faunal realms, based on terrestrial animal species, are generally recognized: Holarctic, including Nearactic (North America) and Paleartic (Eurasia and northern Africa); , having been established in the distinct southern areas, would probably not lose their southern character. Winter sampling could potentially determine if this is the case.
With respect to the Bering Sea, we suggest that the majority of the mixing occurs in the southern Bering Sea because classification breaks down when the southern Bering Sea is included in the northern region. This mixing is consistent with larval studies that show that larvae Larvae, in Roman religion
Larvae: see lemures. enter the Bering Sea through the Aleutian chain. Those fish may not disperse disperse /dis·perse/ (dis-pers´) to scatter the component parts, as of a tumor or the fine particles in a colloid system; also, the particles so dispersed.
1. far into the Bering Sea. Rather, they either remain in the southern Bering Sea or migrate back to the Gulf of Alaska area (Skud  believed that both occurred). A migration may explain why fish tagged in the Bering Sea tend to be recovered at greater distances from the tagging site than those tagged elsewhere (Geernaert, 1996). Migrations of the central and northern Bering Sea group appear to be in a more northerly direction (Skud, 1977), which would preclude mixing in the Aleutians and the Gulf of Alaska. Zoogeographic analysis with patterns of prevalence showed that Bering Sea parasites are rarely found outside the Bering Sea (Blaylock et al., 1998b).
The patterns identified in our analysis agree only in part with zoogeographic analyses (Blaylock et al., 1998b). The southern boundaries in both studies are in the vicinity of the Queen Charlotte Islands, providing additional support for the existence of a southern group of halibut. However, this analysis, unlike the zoogeographic analyses, indicated no sign of a division in the vicinity of Kodiak Island Kodiak Island (kō`dēăk'), 5,363 sq mi (13,890 sq km), c.100 mi (160 km) long and 10–60 mi (16–96 km) wide, off S Alaska, separated from the Alaska Peninsula by Shelikof Strait. , suggesting that the division near Kodiak Island depends on short-lived species not included in this analysis. The evidence for the existence of a northern Bering Sea group is equivocal EQUIVOCAL. What has a double sense.
2. In the construction of contracts, it is a general rule that when an expression may be taken in two senses, that shall be preferred which gives it effect. Vide Ambiguity; Construction; Interpretation; and Dig. ; it was supported by the clustering of localities by using prevalences and, to some degree, the clustering of individuals, but was not supported by any other analyses (Blaylock et al., 1998b).
With respect to juveniles, Skud's (1977) analysis clearly indicates compensatory movement from the Gulf of Alaska and southern Bering Sea to southern areas, and, as such, predicts that juveniles should have more similar parasite faunas among areas. Our data show this similarity, but there are significant caveats. First, our samples of juveniles came from areas that form a single group in the classification of adults. The sample from the northern Queen Charlottes is near the southern boundary of that group, and the sample from Nunivak Island Nunivak Island, the second largest island in the Bering Sea, is a permafrost-covered volcanic island lying about 48 km (30 miles) offshore from the delta of the Yukon and Kuskokwim rivers in the state of Alaska, at about 60° North latitude. Nunivak Island is 4,226.78 km² (1,631. is near the northern boundary. Samples of juveniles from other areas, particularly the southern area, should be examined to help clarify this issue. Second, and maybe more important, in these smaller fish, prevalences and intensities are low and perhaps hinder hin·der 1
v. hin·dered, hin·der·ing, hin·ders
1. To be or get in the way of.
2. To obstruct or delay the progress of.
v.intr. separation. However, because halibut at this stage are susceptible to bycatch in other fisheries (IPHC, 1996), management should probably consider juveniles a mixed stock to prevent impacts on future halibut populations in distant localities.
Overall, our analysis provides a less clear picture than that of Arthur and Albert (1993) for Greenland halibut in the northwest Atlantic. Part of the lack of clarity may be due to our use of the training and test set method rather than the bootstrapping Bootstrapping
A procedure used to calculate the zero coupon yield curve from market figures.
Since the T-bills offered by the government are not available for every time period, the bootstrapping method is used to fill in the missing figures in order to derive the method used by Arthur and Albert, which would increase the likelihood of correctly classifying similar fish. Also, Arthur and Albert were dealing with a very different system. Geological and oceanographic conditions around the Gulf of St. Lawrence are quite complex and create great potential for the isolation of stocks. The northeast Pacific is more open and has fewer isolating mechanisms Isolating Mechanisms are features of behavior, morphology, or genetics which serve to prevent breeding between species. Reproductive isolation of populations is established. than the northwest Atlantic. Further, the system is clinal (Blaylock et al., 1998b) and Pacific halibut are quite capable of migrating along the entire Pacific coast; therefore, less clear cut divisions are expected. Nevertheless, we successfully identified groups of fish, some with a high degree of accuracy.
Skud (1977) suggested that juveniles will, as adults, home to the areas in which they were spawned, making the existence of reproductive stocks at least possible. Modern molecular methods could address the issue. For example, molecular methods could potentially address the existence of separate stocks in the south and in the northern Bering Sea. The limited molecular studies done to date, however, have not elucidated any indentifiable stock structure because of limited sampling localities, the limited number of loci loci
[L.] plural of locus.
loci Plural of locus, see there examined, and the use of juveniles only. Tsuyuki et al. (1969) examined a single serum hemoglobin hemoglobin (hē`məglō'bĭn), respiratory protein found in the red blood cells (erythrocytes) of all vertebrates and some invertebrates. transferrin locus in halibut from ten sites from Vancouver Island to the Bering Sea and found that only one southeast Alaska locality was different. Grant et al. (1984) found no differences between Gulf of Alaska and Bering Sea halibut at five loci but were able to distinguish northeast Pacific halibut from Japanese halibut. However, it is important to note that biochemical and genetic information measures differentiation at a different time scale than that reflected in parasite data (Lester et al., 1988). According to Grant (1984), movement of only a few Atlantic herring herring, common name for members of the large, widely distributed family Clupeidae, comprising many species of marine and fresh-water food fishes, including the sardine (Sardinia), the menhaden (Brevoortia), and the shad (Alosa). (Clupea harengus) may be sufficient to obscure true differences between different breeding stocks. Thus, even limited gene flow could obscure any differences in the loci examined.
Parasite or tagging information alone, however, can not determine whether or not the groups we identified are reproductive stocks. Therefore, all potential factors that might refine the halibut stock concept should be considered. The parasite data suggest a conservative approach to management that recognizes a mixed stock of juveniles and three potential stocks of adults--one in the south, another in the northern Bering Sea, and a third and largest centered in the Gulf of Alaska.
Table 1 Summary of parasites used for discrimination of stocks of adult Pacific halibut by locality. OR = Oregon-northern California, WA = Washington, VI = southern Vancouver Island, SQC = southern Queen Charlotte Islands, NQC = northern Queen Charlotte Islands, SA1 = southeast Alaska 1, SA2 = southeast Alaska 2, KP = Kenai Peninsula, KI = Kodiak Island, NI = Nagai Island, WAI = western Aleutian Islands, SB = southern Bering Sea, PI, Pribilof Island (central Bering Sea), SMI = St. Matthew Island (northern Bering Sea). bc = body cavity, o = organs, m = musculature, sw = stomach wall. Intensity = mean number of parasites per infected host. OR (n=23) Parasite Site Stage % Intensity Anisakis simplex bc, o, m larva 100 258.2 [+ or -] 520.2 Corynosoma villosum bc juvenile 74 7.9 [+ or -] 5.4 Corynosoma strumosum bc juvenile 52 5.6 [+ or -] 6.4 Nybelinia sw metacestode 17 2.8 [+ or -] 2.9 surmenicola Otodistomum sp. sw metacercaria 44 14.3 [+ or -] 13.8 Pseudoterranova bc, o, m larva 44 2.5 [+ or -] 2.1 decipiens Contracaecum sp. bc larva 0 0 Spirurid gen. sp. sw larva 22 1.4 [+ or -] 0.5 WA (n=14) Parasite % Intensity Anisakis simplex 100 122.2 [+ or -] 101.0 Corynosoma villosum 71 6.3 [+ or -] 7.3 Corynosoma strumosum 50 6.3 [+ or -] 5.2 Nybelinia 14 4.0 [+ or -] 4.2 surmenicola Otodistomum sp. 36 32 [+ or -] 55.7 Pseudoterranova 21 2.3 [+ or -] 1.5 decipiens Contracaecum sp. 0 0 Spirurid gen. sp. 50 11 [+ or -] 24.7 VI (n=32) Parasite % Intensity Anisakis simplex 100 381.4 [+ or -] 357.1 Corynosoma villosum 94 8.8 [+ or -] 7.4 Corynosoma strumosum 44 3.6 [+ or -] 5.2 Nybelinia 19 16.0 [+ or -] 31.9 surmenicola Otodistomum sp. 9.4 18.3 [+ or -] 30.0 Pseudoterranova 16 1.2 [+ or -] 0.4 decipiens Contracaecum sp. 3 1.0 [+ or -] 0 Spirurid gen. sp. 3 1.0 [+ or -] 0 SQC (n=31) Parasite % Intensity Anisakis simplex 100 167.8 [+ or -] 101.4 Corynosoma villosum 94 13.7 [+ or -] 24.3 Corynosoma strumosum 39 1.8 [+ or -] 1.5 Nybelinia 3 1.0 [+ or -] 0.0 surmenicola Otodistomum sp. 39 8.3 [+ or -] 13.9 Pseudoterranova 13 1.5 [+ or -] 0.6 decipiens Contracaecum sp. 0 0 Spirurid gen. sp. 0 0 NQC (n=8) Parasite % Intensity Anisakis simplex 100 76.1 [+ or -] 47.6 Corynosoma villosum 100 5.9 [+ or -] 7.4 Corynosoma strumosum 25 2.0 [+ or -] 0.9 Nybelinia 50 13.3 [+ or -] 23.8 surmenicola Otodistomum sp. 38 4.7 [+ or -] 2.3 Pseudoterranova 25 2.0 [+ or -] 0.0 decipiens Contracaecum sp. 50 3.8 [+ or -] 4.9 Spirurid gen. sp. 0 0 SA1 (n=20) Parasite % Intensity Anisakis simplex 100 81.8 [+ or -] 141.1 Corynosoma villosum 90 10.9 [+ or -] 16.6 Corynosoma strumosum 15 1.7 [+ or -] 0.6 Nybelinia 30 11.8 [+ or -] 25.1 surmenicola Otodistomum sp. 35 13.0 [+ or -] 11.0 Pseudoterranova 25 3.2 [+ or -] 4.4 decipiens Contracaecum sp. 40 3.5 [+ or -] 2.2 Spirurid gen. sp. 15 2.3 [+ or -] 1.2 SA2 (n=29) Parasite % Intensity Anisakis simplex 100 44.0 [+ or -] 57.0 Corynosoma villosum 93 16.1 [+ or -] 32.0 Corynosoma strumosum 52 1.9 [+ or -] 1.0 Nybelinia 52 4.1 [+ or -] 2.0 surmenicola Otodistomum sp. 21 8.3 [+ or -] 11.0 Pseudoterranova 69 3.1 [+ or -] 3.0 decipiens Contracaecum sp. 45 2.0 [+ or -] 2.0 Spirurid gen. sp. 10 2.8 [+ or -] 2.0 KP (n=21) Parasite % Intensity Anisakis simplex 100 33.6 [+ or -] 22.1 Corynosoma villosum 95 11.1 [+ or -] 12.4 Corynosoma strumosum 19 1 [+ or -] 0.0 Nybelinia 43 4.2 [+ or -] 3.9 surmenicola Otodistomum sp. 14 2.0 [+ or -] 1.7 Pseudoterranova 29 1.5 [+ or -] 1.2 decipiens Contracaecum sp. 62 3.0 [+ or -] 3.08 Spirurid gen. sp. 9 1.0 [+ or -] 0 KI (n=26) Parasite % Intensity Anisakis simplex 100 29.5 [+ or -] 27.3 Corynosoma villosum 100 11.2 [+ or -] 18.4 Corynosoma strumosum 27 1.3 [+ or -] 0.5 Nybelinia 65 29.5 [+ or -] 106.6 surmenicola Otodistomum sp. 4 1 [+ or -] 0 Pseudoterranova 50 1.9 [+ or -] 1.4 decipiens Contracaecum sp. 50 3.2 [+ or -] 3.2 Spirurid gen. sp. 4 1 [+ or -] 0.0 NI (n=13) Parasite % Intensity Anisakis simplex 100 80.3 [+ or -] 62.0 Corynosoma villosum 85 12.6 [+ or -] 15.0 Corynosoma strumosum 8 2.0 [+ or -] 0.0 Nybelinia 39 42.2 [+ or -] 89.0 surmenicola Otodistomum sp. 8 1 [+ or -] 0.0 Pseudoterranova 61 2.5 [+ or -] 2.0 decipiens Contracaecum sp. 0 0 Spirurid gen. sp. 0 0 UP (n=20) Parasite % Intensity Anisakis simplex 100 53.3 [+ or -] 43.8 Corynosoma villosum 85 29.6 [+ or -] 57.4 Corynosoma strumosum 30 2.0 [+ or -] 1.5 Nybelinia 55 2.7 [+ or -] 2.1 surmenicola Otodistomum sp. 0 0 Pseudoterranova 45 1.4 [+ or -] 0.7 decipiens Contracaecum sp. 15 2.0 [+ or -] 1.0 Spirurid gen. sp. 5 1.0 [+ or -] 0.0 WAI (n=20) Parasite % Intensity Anisakis simplex 100 41.5 [+ or -] 55.0 Corynosoma villosum 95 13.8 [+ or -] 14.0 Corynosoma strumosum 40 2.1 [+ or -] 2.0 Nybelinia 35 16.1 [+ or -] 33.8 surmenicola Otodistomum sp. 5 1 [+ or -] 0 Pseudoterranova 45 2.3 [+ or -] 2.0 decipiens Contracaecum sp. 30 1.3 [+ or -] 1.0 Spirurid gen. sp. 0 0 SB (n=29) Parasite % Intensity Anisakis simplex 100 40.6 [+ or -] 33.6 Corynosoma villosum 97 16.8 [+ or -] 18.3 Corynosoma strumosum 38 8.5 [+ or -] 20.2 Nybelinia 52 6.7 [+ or -] 13.1 surmenicola Otodistomum sp. 0 0 Pseudoterranova 38 2.3 [+ or -] 1.5 decipiens Contracaecum sp. 38 3.0 [+ or -] 4.5 Spirurid gen. sp. 4 1 [+ or -] 0.0 PI (n=14) Parasite % Intensity Anisakis simplex 100 21.5 [+ or -] 22.3 Corynosoma villosum 86 34.4 [+ or -] 37.0 Corynosoma strumosum 79 9.0 [+ or -] 9.3 Nybelinia 57 34.6 [+ or -] 69.2 surmenicola Otodistomum sp. 0 0 Pseudoterranova 29 2.3 [+ or -] 1.3 decipiens Contracaecum sp. 14 1.0 [+ or -] 0 Spirurid gen. sp. 0 0 SMI (n=28) Parasite % Intensity Anisakis simplex 84 10.9 [+ or -] 10.0 Corynosoma villosum 90 34.4 [+ or -] 55.9 Corynosoma strumosum 77 23.2 [+ or -] 25.4 Nybelinia 58 25.0 [+ or -] 69.8 surmenicola Otodistomum sp. 0 0 Pseudoterranova 23 2.4 [+ or -] 1.8 decipiens Contracaecum sp. 7 4.0 [+ or -] 3.5 Spirurid gen. sp. 0 0 Table 2 Summary of parasites used for discrimination of stocks of juvenile Pacific halibut. NQC = northern Queen Charlotte Islands, NI = Nagai Island, UP = Unimak Pass, PI = Nunivak Island (central Bering Sea). bc = body cavity, o = organs, m = musculature, sw = stomach wall. Intensity = mean number of parasites per infected host. NQC (n=20) Parasite Site Stage % Intensity Anisakis simplex bc, o, m larva 25 1.2 Corynosoma bc juvenile 5 1 [+ or -] 0.0 villosum Corynosoma bc juvenile 0 0 strumosum Hysterothylacium bc, o juvenile 15 1 [+ or -] 0.0 aduncum Nybelinia sw metacestode 0 0 surmenicola Pseudoterranova bc, o, m larva 0 0 decipiens Contracaecum sp. bc larva 0 0 Spirurid gen. sp. sw larva 0 0 KI (n=13) Parasite % Intensity Anisakis simplex 8 1.0 [+ or -] 0 Corynosoma 46 1.3 [+ or -] 2.4 villosum Corynosoma 8 1.0 [+ or -] 0 strumosum Hysterothylacium 92 4.4 [+ or -] 3.2 aduncum Nybelinia 0 0 surmenicola Pseudoterranova 8 1.0 [+ or -] 0 decipiens Contracaecum sp. 15 1.0 [+ or -] 1O Spirurid gen. sp. 0 0 NI (n=20) Parasite % Intensity Anisakis simplex 65 3.1 [+ or -] 1.9 Corynosoma 75 3.4 [+ or -] 2.6 villosum Corynosoma 0 0 strumosum Hysterothylacium 95 8.7 [+ or -] 10.7 aduncum Nybelinia 0 0 surmenicola Pseudoterranova 25 1.4 [+ or -] 0.9 decipiens Contracaecum sp. 10 5 [+ or -] 5.7 Spirurid gen. sp. 5 2.0 [+ or -] 0.0 UP (n=20) Parasite % Intensity Anisakis simplex 70 3.6 [+ or -] 3.1 Corynosoma 80 5.8 [+ or -] 7.4 villosum Corynosoma 5 1 [+ or -] 0.0 strumosum Hysterothylacium 85 5.4 [+ or -] 8.8 aduncum Nybelinia 5 1 [+ or -] 0.0 surmenicola Pseudoterranova 15 1 [+ or -] 0.0 decipiens Contracaecum sp. 0 0 Spirurid gen. sp. 0 0 PI (n=23) Parasite % Intensity Anisakis simplex 30 1.7 [+ or -] 0.8 Corynosoma 9 1.5 [+ or -] 0.7 villosum Corynosoma 48 1.2 [+ or -] 0.4 strumosum Hysterothylacium 74 2.8 [+ or -] 1.5 aduncum Nybelinia 26 1.3 [+ or -] 0.8 surmenicola Pseudoterranova 4 6 [+ or -] 0.0 decipiens Contracaecum sp. 0 0 Spirurid gen. sp. 0 0 Table 3 Cross validation results of a 15-category discriminant function classification of adult Pacific halibut in the northeast Pacific based on parasite data. Numbers of fish assigned to each locality and the corresponding percentage of the sample assigned to that category are shown. See Table 1 legend for key to abbreviations. Correct classifications are shown in bold (28% of 240). Assigned category True category OR WA VI SQC NQC SA1 SA2 OR 4 2 1 2 17% 9% 4% 9% WA 2 2 1 25% 3% 13% VI 1 19 2 3 4% 73% 8% 12% SQC 1 1 10 11 4% 4% 40% 44% NQC 2 2 50% 50% SA1 1 1 4 7% 7% 29% SA2 1 1 2 1 4% 4% 9% 4% KP 7 1 50% 7% KI 7 2 35% 10% NI 1 1 14% 14% UP 2 1 14% 7% WAI 3 1 21% 7% SB 1 1 4 3 7% 7% 29% 21% PI SMI 1 5% Assigned category True category KP KI NI UP WAL SB PI SMI OR 2 3 9% 13% WA 1 2 13% 25% VI 1 4% SQC 2 8% NQC SA1 1 1 1 3 7% 7% 7% 21% SA2 3 3 1 1 8 1 1 13% 13% 4% 4% 35% 4% 4% KP 1 1 1 2 1 7% 7% 7% 14% 7% KI 1 2 1 2 3 2 5% 10% 5% 10% 15% 10% NI 2 1 1 29% 14% 14% UP 2 2 1 2 3 1 14% 14% 7% 14% 21% 7% WAI 1 2 2 0 5 7% 14% 14% 36% SB 1 2 1 2 5 1 2 7% 14% 7% 14% 36% 7% 14% PI 1 3 4 13% 38% 50% SMI 3 3 1 14 14% 14% 5% 64% Table 4 Cross validation results of a four-category discriminant function classification of adult Pacific halibut in the northeast Pacific based on parasite data. Numbers of fish assigned to a category and the corresponding percentage of the sample in that category are shown. Correct classifications are shown in bold (63% of 240). OR-SQC = Oregon-northern California to southern Queen Charlotte Islands, NQC-KP = northern Queen Charlotte Islands to Kenai Peninsula, KI-SB = Kodiak Island to southern Bering Sea, PI-SMI = Pribilof Islands to St. Matthew Island. Assigned category True category OR-SQC NQC-KP KI-SB PI-SMI OR-SQC 60 3 7 6 79% 4% 9% 8% NQC-KP 3 28 21 4 5% 50% 42% 7% KI-SB 7 23 41 7 9% 30% 53% 9% PI-SMI 1 6 23 3% 20% 77% Table 5 Cross validation results of a three-category discriminant function classification for adult Pacific halibut in the northeast Pacific based on parasite data. Numbers of fish assigned to a category and the corresponding percentage of the sample in that category are shown. Correct classifications are shown in bold (83% of 240). OR-SQC = Oregon-northern California to southern Queen Charlotte Islands, NQC-SB = southeast Alaska to southern Bering Sea, PI-SMI = Pribilof Islands to St. Matthew Island. Assigned category True category OR-SQC NQC-SB PI-SMI OR-SQC 63 7 6 83% 9% 8% NQC-SB 10 112 12 7% 84% 9% PI-SMI 5 25 17% 83% Table 6 Cross validation results of five-category discriminant function classification for juvenile Pacific halibut in the northeast Pacific based on parasite data. Numbers of fish assigned to a category and the corresponding percentage of the sample in that category are shown. Correct classifications are shown in bold (44% of 62). NQC = northern Queen Charlotte Islands, NI = Nagai Island, UP = Unimak Pass, and PI = Nunivak Island (central Bering Sea). Assigned category True category NQC KI NI UP PI NQC 9 4 69% 31% KI 1 5 1 14% 71% 14% NGI 5 3 3 2 39% 23% 23% 15% UP 5 2 5 1 39% 15% 39% 8% PI 6 4 1 5 38% 25% 6% 31% Table 7 Cross validation results of a three-category discriminant function classification for juvenile Pacific halibut in the northeast Pacific based on parasite data. Numbers of fish assigned to a category and the corresponding percentage of the sample in that category are shown. Correct classifications are shown in bold (66% of 62). NQC = northern Queen Charlotte Islands, NI = Nagai Island, UP = Unimak Pass, PI = Nunivak Island (central Bering Sea). Assigned category True category NQC-NI UP PI NQC-NI 30 3 91% 9% UP 6 6 1 46% 46% 8% PI 10 1 5 63% 6% 31%
We thank the International Pacific Halibut Commission, Seattle, WA, for coordinating sampling and for financial support. Mark Higgins and John Quintero provided invaluable assistance in the laboratory. Tom McDonald
Thomas Bayne McDonald (b. 12 September 1907, d. 26 March 1987) was a pioneering New Zealand wine-maker. and Dave Whitaker provided technical assistance. We also thank Al Shostak and Jeff Lotz for advice and comments.
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Manuscript accepted 10 July 2002. Fish. Bull. 101: 1-9 (2003)
Reginald B. Blaylock Department of Biological Sciences University of Alberta Edmonton, AB T6G 2E9, Canada and Department of Fisheries and Oceans Pacific Biological Station Nanaimo, B.C. V9R 5K6, Canada Present address: College of Marine Sciences The University of Southern Mississippi 703 East Beach Blvd. P.O. Box 7000 Ocean Springs, Mississippi 39566-7000 E-mail address: email@example.com Leo Margolis (deceased) Department of Fisheries and Oceans Pacific Biological Station Nanaimo, B.C. V9R 5K6, Canada John C. Holmes Department of Biological Sciences University of Alberta Edmonton, AB T6G 2E9, Canada