ISSN 1063-0740, Russian Journal of Marine Biology, 2008, Vol. 34, No. 5, pp. 276–287. © Pleiades Publishing, Ltd., 2008. Original Russian Text © A.M. Orlov, V.F. Savinyh, D.V. Pelenev, 2008, published in Biologiya Morya.
ICHTHYOLOGY
Features of the Spatial Distribution and Size Structure of the Pacific Lamprey Lampetra tridentata in the North Pacific A. M. Orlova, V. F. Savinyhb, and D. V. Peleneva aRussian
Federal Research Institute of Fisheries and Oceanography (VNIRO), Moscow, 107140 Russia Scientific Research Fisheries Center (TINRO Center), Vladivostok, 690950 Russia e-mail:
[email protected]
bPacific
Accepted March 26, 2008
Abstract—Results of long-term research on the spatial and vertical distribution of the Pacific lamprey Lampetra tridentata (Richardson, 1836) (the family Petromyzontidae) in the North Pacific, and data on its size structure are submitted. It was shown, that L. tridentate reached its greatest number in the Bering Sea. The maximum concentration of the Pacific lamprey was observed all year round about Navarin Cape, in the Koryak shelf area, at the East Aleutian Islands and at the west coast of the USA, which, apparently, spoke of the increased number of its prey there. On the bottom, the Pacific lamprey was the most numerous at depths of less than 500 m, and in the pelagic, in the upper 100-meter layer. The length of individuals varied in catches from 12 up to 85 cm. The existence of several size groups may indicate that the Pacific lamprey spend several years in the sea. No correlation was revealed between the length of body and fishing depth. The correlations between body length and body weight, body length and condition factor were analyzed. Seasonal dynamics of these parameters were considered. DOI: 10.1134/S1063074008050039 Keywords: Pacific lamprey, distribution, length, mass, North Pacific, Bering Sea.
The Pacific lamprey Lampetra tridentata is an endemic species of anadromous parasitic lampreys, widespread in the North Pacific. The Pacific waters from North Hokkaido (Japan) and South California (USA) in the south and up to northern part of the Bering Sea in the north were considered the range of this species up to the recent time [8, 60, 70]. In recent years, data indicating an increase in the number of the Pacific lamprey [15] and expansion of its range to the south [41, 67] up to the central part of Honshu (prefecture Tochigi) and Mexico (Santo-Domingo River) were published. The Pacific lamprey is considered the most numerous species of parasitic lamprey at the west coast of Canada [64], this species was considered endemic to the North American waters for a long time [3]. In the Russian waters of the Northwest Pacific, the Pacific lamprey was considered a rare species [12, 19, 24, 25, 62]. The Pacific lamprey plays an important and multifaceted role in marine and fresh-water ecosystems of the North Pacific. On the one hand, at different stages of its life cycle, it serves as food for various aquatic animals, from crayfish up to piscivorous birds and sea mammals [1, 20, 31, 35, 45, 46, 50, 61, 66, 70], on the other hand, it is the most serious threat to other fish among all North Pacific species [64]. The Pacific lamprey parasitizes many fish species and even whales, causing significant harm to trade stocks of such species as the Pacific herring Clupea pallasii, North Pacific hake Merluccius productus, Pacific cod Gadus macro-
cephalus, Alaska pollock Theragra chalcogramma, Pacific salmons Oncorhynchus spp., rockfish, Sebastes spp., halibuts (Pacific halibut Hippoglossus stenolepis, Greenland halibut Reinhardtius hippoglossoides matsuurae,), Kamchatka, Atheresthes evermanni, and arrowtooth A. stomias, flounders, and others [1, 14, 19, 31, 45, 53, 70]. As well, it is of interest to fishery, being now an object of commercial fishing only in the waters of the state of Oregon in the USA [53]. In spite of the fact that the Pacific lamprey is widespread in the North Pacific and already for many years has attracted the great attention of researchers, only the fresh-water period of its life cycle may be considered to be well studied. The data on its sea period of life, when the Pacific lamprey leads a parasitic way of life, are extremely limited and fragmentary. In the submitted paper, the data on the spatial and vertical distribution of the Pacific lamprey in the North Pacific are adduced, and features of its size structure are considered. MATERIAL AND METHODS The data from trawl surveys and commercial trawling by bottom and variable–depth trawls in various regions of the North Pacific carried out during 1975– 2007 by employees of the Pacific Scientific Research Fisheries Center (TINRO Center, Vladivostok), Alaska Fisheries Science Center, Seattle, USA, Russian Federal (VNIRO, Moscow) and regional Sakhalin (Sakh-
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NIRO, Yuzhno-Sakhalinsk) and Kamchatka (KamchatNIRO, Petropavlovsk-Kamchatsky) research institutes of fisheries and oceanography, concurrently with the Chukchi Branch of the TINRO-Center (ChukotTINRO, Anadyr) were used as the material for this paper. The materials we used (according to inquiry) were the samples of the above-named datasets and included data only about those catches in which the lamprey were recorded. In total, the data from 3832 catches of the Pacific lamprey taken by bottom and variable–depth trawls, including 3818 with depth records, were analyzed. All catches with a known depth at the location and water layer of trawling were conventionally divided into the bottom, if the depth of location and layer of trawling coincided, and to the pelagic, if the depths of location and of layer of trawling differed by 10 m and more. Thus, the numbers of bottom and pelagic catches were 700 and 3118 respectively. The analysis of the size structure was based on measuring the length of 725 individuals and weighing 332 of them. The diagrams of spatial distribution were constructed using SURFER 8 software (Golden Software, Inc. 2005). RESULTS AND DISCUSSION Spatial distribution Until recently, there was practically no information on the spatial distribution of the Pacific lamprey in Russian waters, except for the data on the coordinates or locations of catches of some individuals of that species [1, 14, 19, 24], and its occurrence in Bering Sea between 60°−61°N and 171°–173°E, and in Kuril waters of the Pacific, from 45° up to 49°N [62]. Unlike our materials, the published diagrams of distribution of the Pacific lamprey [4, 5, 21], which are based on the long-term data of the TINRO Center, were constructed based on GIS technology with one degree generalization squares, and therefore reflected only the general character of the distribution of the considered species. As well, they united the data on catches of the lamprey by midwater trawls in epi- and mesopelagical, which did not enable them to judge the features of its distribution at the bottom. Finally, the specified diagrams were confined by the limits of the Northwest Pacific and did not give any data concerning distribution of the Pacific lamprey in the Northeast Pacific. The analysis of our data on the spatial distribution of the Pacific lamprey (Fig. 1a) corroborated data obtained rather recently that it was widespread to the south to the coast of central Honshu (Japan) at the Asian coast [41]. The available information did not allow specifying the southern boundary of the range of the Pacific lamprey at the American coast, as we had no materials on its occurrence in Mexican waters. This species reached the greatest number in the Bering Sea, inhabiting it practically everywhere. Within the limits of the Russian waters the largest catches (exceeding RUSSIAN JOURNAL OF MARINE BIOLOGY
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10 ind.) were recorded in the Bering Sea in the Navarin Cape vicinity and in the central part at the Koryak Coast. This does not contradict the data on the locations of the maximum concentration of this species obtained previously [4, 21]. The large catches of the Pacific lamprey in the specified areas most likely were caused by an increased number of its victims, primarily, the Alaska pollock Theragra chalcogramma and Greenland halibut Reinhardtius hippoglossoides matsuurae [22, 26]. Now it is difficult to judge the occurrence of the Pacific lamprey in the south part of Bering Sea to the east and to the west of 180 longitude, as registration surveys were few in this area. However, in spite of the fact that bottom trawling occurred in the Bowers Ridge region, there was no data submitted from observers on lamprey catches by fishing vessels from that area (Fig. 1a). In the east part of the Bering Sea, the greatest number of the Pacific lamprey was recorded in the slope area, in shallow water areas its occurrence was rather rare. The biomass of the most usual prey fishes (Alaska pollock, cod, herring, and halibut) in the east part of Bering Sea was about 4.2 million tn for 2006 [51]. Thus, the main concentration of the specified species was related to the continental slope, which may explain the increased number of the lamprey in this area. The shallow water areas, within whose limits it practically did not occur, were characterized by a high ichthyomass (about 5 million tons for 2006), compounded, however, by the account of three flatfish species, (the yellowfin sole Limanda aspera, the rock sole Lepidopsetta bilineata and the Alaska plaice Pleuronectes quadrituberculatus); no attacks by lamprey have been recorded on these species yet. The herring was the only prey occurring in the shallow water area of the sea. However, its number was rather low (23 thousand tons for 2006) and during the surveys it was distributed mostly between the St. Lawrence, St. Matthew, and Nunivak Islands [51], where rare catches of the Pacific lamprey were recorded. In the Northeast Pacific, the greatest catches of the Pacific lamprey were recorded along the west coast of North America, from south of Vancouver Island to San Francisco, this apparently was related to the increased number of the North Pacific hake [10], which is, as well as salmon, one of the basic prey species of the lamprey in this area [31]. Despite the rather high abundance of mass prey fishes (Alaska pollock, cod, and halibuts), whose biomass was estimated for 2002 at a value of about 630 thousand tons [76], catches of the Pacific lamprey occurred very rarely over the greater part of the water area belonging to the Aleutian Islands. The probable causes for this may be the remoteness of the islands from the reproduction areas of lamprey and the connection of basic fish congregations to a narrow coastal strip (the bottom relief was a poorly developed shelf and abrupt slope), where the number of pinnipeds, which are active fish consumers, was high [31, 45, 70]. No. 5
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ORLOV et al. 70° N Russia
(a)
U.S.A
60°
50° PASIFIC OCEAN Catches, specimens per catch 1 6–10 2–5 > 10
40° 70° (b)
Russia
U.S.A
60°
50° Catches, specimens per catch 1
40° 70°
PASIFIC OCEAN
(c) Russia U.S.A
60°
50° PASIFIC OCEAN Catches, specimens per catch 40°
1
E 140° 150°
160°
170°
180°
170°
160°
150°
140°
130°
120°W
Fig. 1. The spatial distribution of the Pacific lamprey Lampetra tridentata in the North Pacific. The trawl survey data: (a)—bottom and pelagic, (b)—pelagic, (c)—bottom.
We cannot speak of the distribution of the considered species in the British Columbia area, as we have no data on trawl surveys in the Canadian waters. The rare records of the Pacific lamprey in the Gulf of Alaska, both pelagic and bottom, are impossible to explain, as within the limits of that area, regular trawl
surveys are conducted and there is large-scale trawl fishing. The number of mass prey species in the Gulf of Alaska (Alaska pollock, cod and halibuts) by the results of a 1996 survey [56] was estimated as about 3.5 million tons. The densest aggregations of cod and halibut were recorded to the southwest of Kodiak Island, and
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those of the Alaska pollock around that island. This corresponded to the distribution pattern of maximum catches of the Pacific lamprey in Gulf of Alaska. However, there is a lack of correlation between the number of prey fish in this area and the number of catches of the lamprey. Probably, this is related to the small number of rivers running into Gulf of Alaska and to the flow regulation of many rivers of the western coast of USA and Canada by construction of hydroelectric dams [33, 43, 57, 58, 59, 65], that limit the opportunity for normal reproduction and preservation of high number of the Pacific lamprey in the Gulf of Alaska and adjacent areas. It is also not impossible that such a break in the distribution of the lamprey is caused by the existence of two subspecies—northern and southern [47]. The results of the analysis of catches of the Pacific lamprey with variable–depth trawls (Fig. 1b) showed that the species was rather widespread in the pelagic zone. Thus numerous catches of the Pacific lamprey at a sufficient distance from coasts, e.g., in the central part of the Bering Sea and at the Kamchatka coast, corroborated the conclusions of Beamish [31] on its ability to migrate long distances to open waters. At the same time, our data testified to the occurrence of the Pacific lamprey in the eastern part of the Sea of Okhotsk at the southwest coast of Kamchatka. Formerly, it was known there only from individual finds [21]. Finding the Pacific lamprey at the east coast of Sakhalin is quite probable, but may be unreliable because of inaccurate species identification, although, taking into account the structure of the oral sucker it would be difficult to confuse it with the other lamprey species inhabiting this area, the Arctic lamprey Lethenteron camtschaticum. On the bottom, the Pacific lamprey occurs mostly in the Bering Sea along the continental slope from the Africa Cape to the east part of the Aleutian Archipelago, and at the west coast of North America, to the south from Vancouver Island (Fig. 1c), and the overwhelming majority of its catches are related to the shelf and continental slope waters. Vertical Distribution Little is known concerning the vertical distribution of the considered species. There is an opinion [1] that the Pacific lamprey inhabits greater depths (300–400 m and deeper). Its recent catches [19] have shown that it can parasitize herring at a depth of about 5 m. Some American researchers [35] consider 800 m as the maximum depth of inhabitation of this species. Domestic experts [25] believe that the Pacific lamprey can occur at depths from 0 to 1100 m, its catches at the surface often occur in the Kurile waters of the Pacific [11, 24]. A range of 200–1000 m was referred as the preferred depths in [23]. We established that the Pacific lamprey occurred in the catches of bottom trawls at the depths of 16–1193 m, and about 80% of the individuals were caught at depths RUSSIAN JOURNAL OF MARINE BIOLOGY
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of less than 500 m (Fig. 2a). The number of finds from depths exceeding 400 m considerably decreased as the depth increases, and most of the individuals (21.4%) were caught from depths of less than 100 m. At the same time in the pelagical, the lamprey was caught by trawls at depths from 0 to 1485 m, and about 83% of all the catches occurred at depths of less than 200 m (Fig. 2b). As well, the size of the average catches and frequency of occurrence of lamprey decreased with an increase of depth. Nevertheless, a significant number of individuals (about 8%) was recorded in the mesopelagical at a depth of 400–500 m, which corroborated the data on the common occurrence of the considered species in the mesopelagical of the Bering Sea published previously [6, 7]. An analysis of the variation of the catch size within daylight hours showed that the Pacific lamprey made daily vertical migrations (Fig. 2c). From midnight up to 9 a.m. catches increased in the pelagical, and decreased at the bottom. Probably, it rose from bottom into the pelagic zone during this time. From 9 a.m. to 6 p.m., i.e., during the daytime, the reverse picture was observed, catches at the bottom increased, and decreased in the pelagical, indicating migration of the lamprey from the pelagic layers to the bottom ones. Movement of the considered species during the day from the bottom into the water column and back might be caused by vertical migration of the lamprey’s prey, planktophage fishes, e.g., the Alaska pollock, which has characteristic vertical feeding migrations during the day [27]. From 6 p.m. to midnight the lamprey catches increased, both in the pelagical, and at the bottom, which is not yet explainable. There is no common opinion concerning the ecological status of the Pacific lamprey. Some authors suppose that this species leads a bottom dwelling way of life at greater depths [14], others attribute it to neritipelagic [62] or mesopelagical species [25, 35]. The Pacific lamprey may occur also in the epipelagical [11], thus, it is able to migrate far into the open ocean [31]. In the mesopelagical, at depths less than 500 m, the Pacific lamprey occurs significantly more often, than in the deeper layers [7, 75], this was also corroborated by our research. Similar contradictions obviously can be caused by the poor status of the study of lamprey migrations and, probably, by the specifics of its behavior. Some authors [30] have hypothesized that it started to parasitize fishes already in the estuary before exiting into the sea, right after the end of metamorphosis or during its last phase. The other researchers [35] considered that after migration into the sea the lamprey moves to the depth exceeding 70 m. These considerations contradicted the data on catches of mature individuals of the Pacific lamprey of 41–65 cm in length at a depth of about 5 m parasitizing herring [19]. Our data (Fig. 3a) also did not find a reliable correlation (R2 = 0.149) between the body length of lamprey and the catch depth, there were individuals of various lengths, from the minimal to the maximal at practically all studied ranges of depths. Probably, the Pacific lamNo. 5
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ORLOV et al. 4.5 4.0 20 3.5 mean catch 3.0 15 2.5 2.0 10 1.5 1.0 5 0.5 0 0 0–100101– 201– 301– 401– 501– 601– 701– 801– 901–1001–1101– 200 300 400 500 600 700 800 900 1000 1100 1200 70 3.5 (b) 3.0 60 (a)
% of catches
50
2.5
40
2.0
30
1.5
20
1.0
10
0.5
0
Mean catch, specimens
0–100 101– 201– 301– 401– 501– 601– 701– 801– 901– 1001– 200 300 400 500 600 700 800 900 1000 1500 Depth, m 3.0 (c)
Mean catch, specimens
Percentage of catches
25
0
1 2.5 2
2.0 1.5 1.0 0.5
0–3
3–6
6–9
9–12 12–15 Hour, h
15–18
18–21
21–24
Fig. 2. Vertical distribution of the Pacific lamprey Lampetra tridentata in the North Pacific according to trawl survey with bottom and midwater trawls. Trawling: (a)—bottom, (b)—pelagic, (c)—daily dynamics of catches at bottom (1) and in the pelagical (2).
prey is such a plastic species that it can occupy practically any sea biotope. If it is possible to explain its presence in epipelagic Kuril waters and in the open ocean by connection to the distribution of Pacific salmon, which it attacks [21, 31, 48], and at the bottom by its parasitizing many bottom and benth-pelagic fishes [15], the high frequency of occurrence the Pacific lamprey in the mesopelagical has not found an explanation yet. It is not impossible that at a greater depth the lamprey can feed on the mass meso- and bathypelagic Myctophidae lantern fish and the Bathylagidae deepsea smelts. There is an opinion that lampreys can
intensely feed on dense aggregations of small fish, eating them entirely, which enables them to quickly find new prey [37]. At the present, numerous data on the feeding of various species of parasitic lamprey on juveniles and small fish species, such as the sprat Sprattus sprattus, Baltic herring Clupea harengus membras, alewife Alosa pseudoharengus, Atlantic menhaden Brevoortia tyrannus (Clupeidae), rainbow trout Oncorhynchus mykiss (Salmonidae), white sucker Catostomus commersonii, northern hog sucker Hypentelium nigricans (Catostomidae), bluegill Lepomis macrochirus (Centrarchidae), stonecat Noturus flavus (Ictalu-
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Length, cm
FEATURES OF THE SPATIAL DISTRIBUTION 90 80 70 60 50 40 30 20 10 0
281
(a)
R2 = 0.1491 100
200
300
400
500
600 700 Depth, cm
800
900 1000 1200 1400
30
Number of specimens
25
N = 725 specimens M = 48.65 cm
(b)
20 15 10 5
Length, cm
0 90 80 70 60 50 40 30 20 10 0
12 15 18 21 24 27 30 33 36 39 42 45 48 51 54 57 60 63 66 69 72 75 78 81 84 Length, cm (c)
R2 = 0.5369 4
5
6
7
8 Month
9
10
11
12
Fig. 3. Length of the Pacific lamprey Lampetra tridentata in the North Pacific. (a)—body length at different depths, (b)—size structure, (c)—body length in different months. Vertical lines—fluctuations of an attribute, circlets—average values, dash line—average weighted values.
ridae), wounded darter Etheostoma vulneratum (Percidae), Creek chub Semotilus atromaculatus, common shiner Luxilus cornutus, blacknose dace Rhinichthys atratulus, Eurasian minnow Phoxinus phoxinus (Cyprinidae), three-spined stickleback Gasterosteus aculeatus (Gasterosteidae) and European smelt Osmerus eperlanus (Osmeridae) [28, 34, 36, 39, 42, 52, 55, 74] RUSSIAN JOURNAL OF MARINE BIOLOGY
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have been collected. It is practically impossible to trace the attacks of lamprey on small fish because of their total consumption, it is possible to judge such facts only by the contents of the digestive tract of the lamprey. Unfortunately, there is no data on the contents of the stomachs of the Pacific lamprey caught in the mesoand bathypelagical. No. 5
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ORLOV et al.
Length and Body Weight The information on the size structure of the Pacific lamprey caught in the sea is extremely poor. Despite the numerous catches of this species in the mesopelagical of the Bering Sea [7], the data on its size structure are practically absent in the literature. Thus, data on the length of several individuals caught by various fishing gear [1, 14, 19, 24], and of one individual found in a sperm whale stomach [20] have been published. There is no common opinion also on the maximum length of the Pacific lamprey; it is thought that it may reach 69 cm [8, 45], 73.1 cm [29] or 76 cm [53]. In our data (Fig. 3b), the Pacific lamprey was represented by individuals with body lengths from 12 up to 85 cm (48.65 on the average) in trawl catches. The transformation in this species occurs at a body length of 12–30 cm [70], about 14 cm on the average [45]. Hence, in catches in the sea, concurrently with mature individuals, there was recently transformed lamprey, which had just left the river. Respectively, the individuals with a body length from 40 up to 63 cm dominated in number, 57.2%. The presence of several peaks in the size structure diagram presumes a complex size–age structure of the population with several age groups present. Kostlow’s [49] research showed that lamprey coming to spawn into the Willamette River (Oregon State) consisted of individuals of three peak dimension series, which probably indicates the participation of representatives of different (at least, three) generations. There is no common point of view on the duration of the sea period of the life of this species. Some authors suppose that it continues for 12–20 months [70], while others [31] state the ambiguity of the period of occurrence of lamprey in the sea and believe that there probably are different durations of the sea period in various populations. Experimental research indicates that under laboratory conditions the duration of the stay in saline water for individuals of the Pacific lamprey may reach 3.5 years [31], which corresponds to the data published in [49, 72] and to our data on its size structure. The variation of body length during the year also speaks in favor of the assumption of a long occurrence of the lamprey in the sea (Fig. 3c). The positive significant trend (R2 = 0.537) of an increase in average body length from about 36.5 cm in April to 53.0 cm in December corroborates the data previously obtained [31, 53, 70], indicating the high rates of linear growth of individuals during the year: from 12–16 up to 30 cm during migration down rivers and up to 54 cm on the average during the return of spawning migrations. Nevertheless, during the research there were individuals of various body lengths recorded in the catches, from the minimum to the maximum, which probably indicated the presence of different generations. An analysis of the correlation between length and the weight of the lamprey body has been carried out only for 8 of the 47 existing species (Table 1). The data on correlation between length and weight of body of the
Pacific lamprey were obtained only for ammocoetes, transformers and adult individuals from the rivers of the states of Washington and Oregon [49, 73], and are absent for the sea period of life. Moreover, in the latter work only graphic materials on adult lamprey, without calculation of the correlation between the length and weight of the body, were submitted. Meanwhile, such data allow us to have some idea of the character of lamprey growth and probably of interpopulation distinctions. Our research revealed a significant correlation (R2 = 0.706) between the total length (TL) and weight (W) of the Pacific lamprey (Fig. 4a), described by the formula: W = 4.6 × 10–5 TL2.1648. As a whole, during our research the power factor of this equation varied within a wide range from 1.762 to 3.080 (Table 2). From May it consistently increased, reaching the maximum value in November. As comparison of the parameters of the equation for the dependence reveals (Table 1), the value of the power factor b in the overwhelming majority of lamprey is within the limits of normal (2.5–3.5) for most of the marine fishes [40]. In our case, the values of the power factor for the dependence were within the limits of this interval only in August and November and were significantly lower for the rest of the time. At the same time, at lesser than a –3 value of the common logarithm of the linear coefficient a of the correlation equation between length and weight, the form of fish body approached being eel–like [40]. In the Pacific lamprey the value of loga varied from –3.368 up to –5.959 from May till November (Table 2), which corresponded well with Froese’s conclusions [40]. The consecutive increase in the value of the power factor of the considered correlation may be connected to several causes. At the Canadian coast, after transformation young lamprey leave the rivers for the sea from December till June, with maximum from the middle of March up to the middle of May [31, 32]. After the transformation, they eat intensely during the entire feeding period. This is connected to the necessity of accumulation of an energy reserve before coming to the rivers, which will be spent later for wintering and migration to spawning grounds in the following spring [45]. As well, the growth of the power factor may be caused by an increase in gonad weight during maturation, as has been observed in other lamprey species [2]. Considering the within-year dynamics of Fulton’s condition factor (Table 3), it is possible to note that its average values, from 0.25 to 0.49, occurred in the spring–summer season (from March until July). A similar dynamics of growth of the condition factor during the spring–summer season was also displayed by the Caspian lamprey [2, 9]. The correlation between the condition and body length of the Pacific lamprey (Fig. 4b) implied that the increase of its linear size was accompanied by a decrease of the condition factor. It is known that during the sea period of life the Pacific lamprey grows very quickly and its condition decreases in
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Table 1. Length–weight parameters of various species of lamprey Length (min. max.)
n
33.0–46.0
108
0.0023
2.531
[9]
Low Volga River
36.0–53.0
50
0.0015
2.610
[2]
Kura River
31.7–43.2
50
0.007
3.117
[17]
Volga Estuary
30.1–55.3
100
0.0008
3.071
[18]
Mid Volga
–
145
0.0015
2.660
[71]
Adult, spawning migration in river
–
31
0.0012
3.080
[71]
Adult, parasitic phase
Chestnut lamprey Icthyomyzon castaneus
–
–
0.00000058
3.215
[69]
Michigan Lake
European river lamprey Lampetra fluviatilis
31.0–45.0
0.0011
3.141
[68]
Estonia
–
0.0000041
2.836
[69]
Michigan Lake
Species Caspian lamprey Caspiomyzon wagneri
Silver lamprey Icthyomyzon unicupsis
Brook lamprey Lampetra lamottei
a
7
–
b
Reference
Note
European brook lamprey Lampetra planeri
2.5–19
17
0.0017
3.000
[44]
Great Britain
Pacific lamprey Lampetra tridentata
~2...~12
–
0.00005
2.738
[73]
Ammocoete and transformers, river
14.0–85.0
332
0.00007
2.066
Our data
Adult, sea
31.0–93.0
25
0.0008
3.196
[38]
Sea
–
0.000019
2.631
[69]
Michigan Lake
Sea lamprey Petromyzon marinus
–
Note: n—number of the measured individuals, a and b—parameters of the correlation equation between length and weight of body; “–”—no data available.
Table 2. Parameters of the correlation equation between length (L) and weight (W) of body of the Pacific lamprey Lampetra tridentata in the Northwest Pacific W = aLb in various months Month
a
log a
b
R2
n
May June July August September October November
2.3 × 10–4 1.3 × 10–4 1.2 × 10–4 9.3 × 10–6 2.2 × 10–5 4.6 × 10–5 1.1 × 10–6
–3.63827 –3.88606 –3.92082 –5.03152 –4.65758 –4.33724 –5.95861
1.7619 1.9349 1.9309 2.5638 2.3354 2.1666 3.0796
0.779 0.743 0.634 0.770 0.740 0.707 0.820
25 35 21 29 81 70 36
Note: R2—determination factor, n—number of the measured individuals. RUSSIAN JOURNAL OF MARINE BIOLOGY
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Table 3. Fulton’s condition factor in the Pacific lamprey Lampetra tridentata from the North Pacific for various months Month January February March April May June July August September October November December
Minimum Maximum 0.14 0.21 0.49 0.14 0.12 0.11 0.11 0.10 0.10 0.10 0.10 0.10
0.20 0.21 0.49 0.62 1.71 1.54 2.44 1.17 0.81 0.81 0.51 1.30
Average
n
0.17 0.21 0.49 0.25 0.30 0.29 0.27 0.20 0.20 0.20 0.16 0.28
7 1 1 9 46 41 50 73 99 90 39 37
Note: n—number of the measured individuals. No. 5
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ORLOV et al. 1.0 0.9 Body weigth, kg
0.8
(a)
W = 0.000046 TL2.16477 R2 = 0.706 n = 332
0.7 0.6 0.5 0.4 0.3 0.2 0.1 0 10 3.0
20
30
40
50 60 Length, cm
70
80
90 (b)
Condition
2.5 2.0 1.5 1.0 0.5 0 10
20
30
40
50 60 Mean length, cm
70
80
90
Fig. 4. Correlation between length and body weight (a), average body weight and condition (b) in the Pacific lamprey Lampetra tridentata in the North Pacific.
that relation. As we have established the fact of an increase in the average size of this species from spring to winter, this may also explain the decrease in the condition factor from spring to autumn. As a whole, the values of the condition factor we obtained for the Pacific lamprey were difficult to compare to those obtained for other lamprey species, because of discrepancies in the published data. Thus, according to Abdurakhmanov [2], the condition factor of the Caspian lamprey was 1.36–1.74 in January–April. According to Ginzburg [9], from December until June it varied within the limits of 0.12–0.16. The condition factor of the Pacific lamprey at the northwest coast of Sakhalin Isl. was 1.2–1.7 in August, and increased with an increase in the length of individuals [13]. In ammocoetes of the Pacific lamprey the condition factor varied within the limits of 0.88–2.52 (1.49–1.54 on the average) and decreased with growth, varying from 0.59 to 2.66 in transformers (1.21–1.41 on the average) [54],
significantly exceeding our data. In the Western brook lamprey Lampetra richardsoni the condition factor of ammocoetes was 1.13–1.60 (1.41–1.44 on the average) and, increasing with growth, reached 1.64–1.83 (1.70 on the average) in adult individuals [54]. ACKNOWLEDGEMENTS The authors are highly grateful to their colleagues from the NOAA Alaska Fisheries Science Center: Drs. James Orr, Duane Stevenson and Robert Lauth for the data on catches of the Pacific lamprey in the Pacific waters of the USA. We are also indebted to our colleagues from the TINRO Center, VNIRO, KamchatNIRO, and ChucotNIRO, who participated in the sampling of the Pacific lamprey in the North Pacific in 1975–2006, the data from which was used in this paper.
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REFERENCES 1. Abakumov, V.A., Concerning the Sea Period of Life of the Pacific Lamprey Enthosphenus tridentatus (Richardson)), Tr. VNIRO, 1964, vol. 49, pp. 253–256. 2. Abdurakhmanov, Yu.A., Ryby presnyh vod Azerbaidzhana (Fishes of Fresh Waters of the Azerbaijan), Baku: Izdatel’stvo AN Azerbaidzhanskoi SSR, 1962. 3. Andriyashev, A.P., Ocherk zoogeografii i proishozhdeniya fauny ryb Beringova morya i sopredel’nyh vod (Outline of Zoogeography and Origin of Fauna of Fishes of the Bering Sea and Adjacent Waters, Leningrad: Izdatel’stvo LGU. 1939. 4. Atlas kolichestvennogo raspredeleniya nektona v severo-zapadnoi chasti Tihogo okeana T. 3. Karty (The Atlas of Quantitative Distribution of Nekton in the Northwest Pacific Vol. 3. Maps) (Shuntov V.P., Bocharov L.N., eds), Moscow: Izdatel’stvo FGUP “Natsional’nye rybnye resursy”, 2005. 5. Atlas kolichestvennogo raspredeleniya nektona v zapadnoi chasti Beringova morya T. 4. Karty (The Atlas of Quantitative Distribution of Nekton in the Western Part of the Bering Sea Vol 4. Maps) (Shuntov V.P., Bocharov L.N., eds), Moscow: Izdatel’stvo FGUP “Natsional’nye rybnye resursy”, 2006. 6. Balanov, A.A. and Ilyinsky, E.N., Species Composition and Biomass of Mesopelagical Fishes of the Okhotsk and Bering Seas, Vopr. Ikhtiol., 1992, vol. 32, 1, pp. 56–63. 7. Balanov, A.A. and Radchenko, V.I., The Composition and Distribution of Fishes in the Meso– and Bathipelagical of the Bering and Okhotsk Seas, Kompleksnye issledovaniya ekosistemy Beringova morya. (Complex Researches of the Bering Sea Ecosystem), Moscow: Izdatel’stvo VNIRO, 1995, pp. 335–343. 8. Borets, L.A., Annotirovannyi spisok ryb dal’nevostochnyh morei (Annotated List of Fishes of the Far East Seas), Vladivostok: TINRO-Center, 2000. 9. Ginzburg, Ya.I., Spawning Population of the Lamprey Caspiomyzon wagneri (Kessler) after Regulating of Volga River by the Dam of Volgograd Hydroelectric Power Station, Vopr. Ikhtiol., 1969, vol. 9, no. 6, pp. 1022–1031. 10. Yermakov, J.K., Hakes, Biologicheskie resursy Tikhogo okeana (Biological Resources of the Pacific), Moscow: Nauka, 1986, pp. 221–228. 11. Ivanov, O.A., The Epipelagic Community of Fishes and Cephalopods of Kuril Waters of the Pacific in 1986– 1995, Izv. TINRO, 1998, vol. 124, pp. 3–54. 12. Myagkov, N., Far East Lamprey, Rybovodstvo i rybolovstvo, 1983, no. 11, p. 10. 13. Nikolsky, G.V., Some Data Concerning Sea Period of Life of the Arctic Lamprey Lampetra japonica (Martens), Zool. Zhurn., 1956, vol. 35, no. 4, pp. 588–591. 14. Novikov, N.P., The Incidents of Attack the Pacific Lamprey Enthosphenus tridentatus (Gairdner) on Halibuts and Other Fishes of the Bering Sea, Vopr. Ikhtiol., 1963, vol. 3, no. 3, pp. 567–569. 15. Orlov, A.M, The Present Condition, Temporary Variations of Structure, Fisheries Potential and Prospects of Fisheries Management of Fish Communities of the Upper Bathyal of Kuril and Kamchatka Waters of the Pacific, Vodnye biologicheskie resursy, ikh sostoyanie i ispol’zovanie: analiticheskaya i referativnaya inforRUSSIAN JOURNAL OF MARINE BIOLOGY
Vol. 34
16.
17. 18.
19.
20.
21.
22. 23.
24.
25.
26. 27.
No. 5
285
matsiya (Water Biological Resources, Their Condition and Use: Analytical and Abstract Information), Moscow: VNIERKH, 2004, issue 1, pp. 2–34. Orlov, A.M., Vinnikov, A.V., and Pelenev, D.V., Concerning the Methods of Study of Sea Period of Life of Parasitic Lamprey at Example of the Pacific lamprey Lampetra tridentata (Gairdner, 1836), Fam. Petromyzontidae, Vopr. Rybovodstva, 2007, vol. 8, no. 2, pp. 287–312. Pravdin, I.F., Observation on the Caspian Lamprey (Caspiomyzon wagneri Kessler) in Spring of 1912, Tr. Astrakhan. Ikhtiol. Lab., 1913a, vol. 2, issue 6, pp. 1–17. Pravdin, I.F., The Autumn Migration of the Lamprey (Caspiomyzon wagneri Kessler) from the Caspian Sea into the Volga River, Tr. Astrakhan. Ikhtiol. Lab., 1913b, vol. 2, issue 6, pp, 19–43. Prohorov, V.G. and Grachev, LE., On the Find of the Pacific Lamprey Enthosphenus tridentatus (Gairdner) in the West part of the Bering Sea, Vopr. Ikhtiol., 1965, vol. 5, no. 4, pp. 723–726. Svetovidova, A.A., On the find of the Pacific Lamprey Enthosphenus tridentatus (Gairdner) in the Soviet Part of the Bering Sea, Dokl. AN SSSR, 1948, vol. 61, no. 1, pp. 151–152. Sviridov, V.V., Spatial–Time Variability of Distribution of the Main Species of Predatory Fishes and Fishlike Fishes, Consumers of Pacific Salmons in the Far East Sas, Byul. no. 1 realizatsii “Kontseptsii dal’nevostochnoi basseinovoi programmy izucheniya tihookeanskih lososei (Bull.nNo 1 of Actualization of the Concept of the Far East Basin Program of Study of Pacific Salmons), Vladivostok: TINRO-Center, 2006, pp. 266– 276. Fadeyev, N.S., The Alaska Pollock, Biologicheskie resursy Tikhogo okeana (Biological Resources of the Pacific), Moscow: Nauka, 1986, pp. 187–201. Fedorov, V.V., Species Composition, Distribution and Depths of Habitation of Species of Fishlike and Bony Fishes at the North Kurils, Promyslovo-biologicheskie issledovaniya ryb v tihookeanskih vodah Kuril’skih ostrovov i prilezhaschikh raionah Ohotskogo i Beringova morei v 1992–1998 gg (Fishery–Biological Researches of Fishes in Pacific Waters of the Kurils and Adjacent Areas of Okhotsk and Bering Seas 1992–1998, Moscow: Izdatel’stvo VNIRO, 2000, pp. 7–41. Fedorov, V.V. and Parin, N.V., Pelagicheskie i bentopelagicheskie ryby tihookeanskih vod Rossii (Pelagic and Benthopelagic Fishes of the Pacific Waters of Russia), Moscow: Izdatel’stvo VNIRO, 1998. Sheiko, B.A. and Fedorov, V.V., Class Cephalaspidomorphi—Lampreys. Class Chondrichthyes—Cartilaginous Fishes. Class Holocephali, Class Osteichthyes— Bone Fishes, Katalog pozvonochnyh zhivotnyh Kamchatki i sopredel’nyh morskih akvatorii (Catalogue of Vertebrate Animals of Kamchatka and Adjacent Sea Areas), Petropavlovsk-Kamchatsky: Kamchatskii Pechatnyi Dvor, 2000, pp. 7–69. Shuntov, V.P. Distribution of Greenland Halibut and Arrowtooth Flounder in the North Pacific, Tr. VNIRO, vol. 58 (Izv. TINRO, vol. 53), 1965, pp. 155–163. Shuntov, V.P., Volkov, A.F., Temnyh, O.S., and Dulepova, E.P., Mintai v ekosistemakh dal’nevostochnykh 2008
286
28. 29. 30.
31.
32.
33.
34. 35.
36. 37. 38.
39.
40. 41.
42.
ORLOV et al. morei (Alaska Pollock in Ecosystems of Far Eastern Seas. Vladivostok: TINRO, 1993. Eglite, R.M., Feeding of the European River Lamprey Lampetra fluviatilis (L.) in the Sea, Zool. Zhurn., 1958, vol. 37, no. 10, pp. 1509–1514. Amaoka, K., Nakaya, K., and Yabe, M., The Fishes of Northern Japan, Sapporo: Kita-Nihon Kaijo Center Co., 1995. Anderson, J.W., A Description of Pacific Lamprey Life History, Physical Habitat and Water Quality Criteria, and Their Current Status Downstream of the Hells Canyon Complex (E.3.1–3, chapter 4), Rept. to Oregon and Idaho Bureau of Land Management. November, 2002, http://www.or.blm.gov/vale/ferc/ferc-internet/29A.pdf. Beamish, R.J., Adult Biology of the River Lamprey (Lampetra ayresi) and Pacific Lamprey (Lampetra tridentata) from the Pacific Coast of Canada, Can. J. Fish. Aquat. Sci., 1980, vol. 37, pp, 1906–1923. Beamish, R.J. and Levings, C.D., Abundance and Freshwater Migrations of the Anadromous Parasitic Lamprey, Lampetra tridentata, in a Tributary of the Fraser River, British Columbia, Can. J. Fish. Aquat. Sci., 1991, vol. 48, pp. 1250–1263. Beamish, R.J. and Northcote, T.G., Extinction of a Population of Anadromous Parasitic Lamprey, Lampetra tridentata, Upstream of an Impassable Dam, Can. J. Fish. Aquat. Sci., 1989, vol. 46, pp. 420–425. Bond, C.E. and Kan, T.T., Lampetra (Enthosphenus) minima n. sp., a Dwarfed Parasitic Lamprey from Oregon, Copeia, 1973, pp. 568–574. Close, D.A., Fitzpatrick, M., Li, H., et al., Status Report of the Pacific Lamprey (Lampetra tridentata) in the Columbia River Basin, Tech. Rept. DOE/BP–39067-1 (Contract 95BI39067). U.S. Department of Energy Bonneville Power Administration. Environment, Fish and Wildlife, 1995. Cochran, P.A. Size-Selective Attack by Parasitic Lamprey: Consideration of Alternative Null Hypothesis, Oecologia, 1985, vol. 67, pp. 137–141. Cochran, P.A., Small Fishes as Hosts for Parasitic Lamprey, Copeia, 1994, no. 2, pp. 499–504. Coull, K.A., Jermin, A.S., Newton, A.W., et al., Length/Weight Relationships for 88 Species of Fish Encountered in the North Atlantic, Scott. Fish. Res. Rept., 1989, no. 43, pp. 1–80. Davis, R.M., Parasitism by Newly Transformed Sea Lamprey on Landlocked Salmon and Other Fishes in a Coastal Maine Lake, Trans. Amer. Fish. Soc., 1967, vol. 96, pp. 11–16. Froese, R., Cube Law, Condition Factor and Weight– Length Relationships: History, Meta-Analysis and Recommendations, J. Appl. Ichthyol., 2006, vol. 22, pp. 1–13. Fukutomi, N., Nakamura, T., Doi, T., et al., Records of Enthosphenus tridentatus from Naka River System, Central Japan; Physical Characteristics of Possible Spawning Redds and Spawning Behavior in the Aquarium, Jap. J. Ichthyol., 2002, vol. 49, no. 1, pp. 53–58. Hall, J.D., An Ecological Study of the Chestnut Lamprey, Ichthyomyzon castaneus (Girard), in the Manistee River, Michigan, Ph. D. Dissertation, Ann Arbor: University of Michigan, 1963.
43. Hamilton, J.B., Curtis, G.L., Snedaker, S.M., and White, D.K., Distribution of Anadromous Fishes in the Upper Klamath River Watershed Prior to Hydropower Dams—A Synthesis of the Historical Evidence, Fisheries, 2005, vol. 30, no. 4, pp. 10–20. 44. Hardisty, M.W., The Life History and Growth of the Brook Lamprey, (Lampetra planeri), J. Anim. Ecol., 1944, no. 13, pp. 110–122. 45. Hart, J.L., Pacific Fishes of Canada, Bull. Fish. Res. Bd. Can., 1973, no. 180, pp. 1–740. 46. Harvey, J.T., Food Habits, Seasonal Abundance, Size, and Sex of the Blue Shark, Prionace gluaca, in Montery Bay, California, Calif. Fish Game, 1989, vol. 75, no. 1, pp. 33–44. 47. Hubbs, C.L., Occurrence of the Pacific Lamprey, Entosphenus tridentatus, off Baja California and in Streams of Southern California; with Remarks on Its Nomenclature, San Diego Soc. Nat. Hist., 1967, vol. 20, pp. 303–311. 48. Klovach, N. and Gruzevich, A., Results of 2003 Salmon Research Cruise of the SRTMK “Sovremennik”, NPAFC Doc. No. 767, 2004. 49. Kostow, K. Oregon Lamprey: Natural History Status and Problem Analysis, Salem: Oregon Department of Fish and Wildlife, 2002. 50. Lamb, A. and Edgell, P., Coastal Fishes of the Pacific Northwest, Madeira Park, B.C., Canada: Harbour Publishing Co., 1986. 51. Lauth, R.R. and Acuna, E., Results of the 2006 Eastern Bering Sea Continental Shelf Bottom Trawl Survey of Ground and Invertebrate Resources, U. S. Dep. Commer., NOAA Tech. Memo. NMFS–AFSC–176, 2007 52. Lennon, R.E., Feeding Mechanism of the Sea Lamprey and its Effect on Host Fishes, Fish. Bull. Fish Wildlife Serv., 1954, vol. 56, no. 98, pp. 247–293. 53. Love, M., Probably More than You Want to Know About the Fishes of the Pacific Coast, Santa Barbara: Really Big Press, 1996. 54. Lucier, C. and Silver, G., Evaluate Habitat Use and Population Dynamics of Lamprey in Cedar Creek, Annual Report for 2004 Sampling Season (BPA Project no. 2000–014–00), 2005. 55. Mansueti, R.J., Distribution of Small, Newly Metamorphosed Sea Lamprey, Petromyzon marinus, and Their Parasitism on Menchaden, Brevootria tyrannus, in MidChesapeake Bay During Winter Months, Chesapeake Sci., 1962, no. 3, pp. 137–139. 56. Martin, M.H., Data Report: 1996 Gulf of Alaska Bottom Trawl Survey, U.S. Dept. Commer., NOAA Tech. Memo, NMFS–AFSC–82, 1997. 57. Mesa, M.G., Annual Physiological Profiles of Pacific Lamprey: Implications for Migrations Past Dams, The Biology of Lamprey, Proc. Int. Congr. Biol. Fish, Vancouver, Canada: University of British Columbia, 2002, pp. 17–19. 58. Moser, M.L., Cavender, W.P., Ogden, D.A., and Peery, C., Effects of Light on Migrating Adult Pacific Lamprey, The Biology of Lamprey, Proc. Int. Congr. Biol. Fish, Vancouver, Canada: University of British Columbia, 2002, pp. 37–40.
RUSSIAN JOURNAL OF MARINE BIOLOGY
Vol. 34
No. 5
2008
FEATURES OF THE SPATIAL DISTRIBUTION 59. Moser, M.L. and Close, D.A., Assessing Pacific Lamprey Status in the Columbia River Basin, Northwest Sci., 2003, vol. 77, no. 2, pp. 116–125. 60. Nagasawa, K. and Torisawa, M., Fishes and Marine Invertebrates of Hokkaido: Biology and Fisheries, Sapporo: Kita–Nihon Kayo Center Co., 1991. 61. Pacific Lamprey, 2001, http://streamnetorg/pub-ed/ ff/Lifehistory/lamprey_fact.html http://streamnet.org/pubed/ ff/Lifehistory/lamprey_fact.html 62. Parin, N.V., An Annotated Catalog of Fishlike Vertebrates and Fishes of the Seas of Russia and Adjacent Countries. Part 1. Order Myxiniformes–Gasterosteiformes, J. Ichthyol., 2001, vol. 41, suppl. 1, pp. S51– S131. 63. RACE Groundfish Survey Data, AFSC, Alaska Fisheries Science Center, www.afsc.noaa.gov, December 2007. 64. Richards, J.E., Beamish, R.J., and Beamish, F.W.H., Descriptions and Keys for Ammocoetes of Lamprey from British Columbia, Canada, Can. J. Fish. Aquat. Sci., 1982, vol. 39, pp. 1484–1495. 65. Robinson, T.C., Bayer, J.M., and Seelye, J.G., Upstream Migration of Pacific Lamprey in the John Day River: Behavior, Timing, and Habitat Use, The Biology of Lamprey, Proc. Int. Congr. Biol. Fish., Vancouver, Canada: University of British Columbia, 2002, pp. 69–72. 66. Roffe, T.J. and Mate, B.R., Abundance and Feeding Habits of Pinnipeds in the Rough River, Oregon, J. Wildl. Manag., 1984, vol. 48, no. 4, pp. 1262–1274. 67. Ruiz-Campos, G. and Gonzalez-Guzman, S., First Freshwater Record of Pacific Lamprey, Lampetra tridentata, from Baja California, Mexico, Calif. Fish Game, 1996, vol. 82, no. 6, pp. 144–146.
RUSSIAN JOURNAL OF MARINE BIOLOGY
Vol. 34
287
68. Saat, T., Tambets, J., and Pihu, E., Lampern River Lamprey, Lampetra fluviatilis (L.), Fishes of Estonia, Tallinn: Estonian Academic Publishing, 2003, pp. 48–51. 69. Schneider, J.C., Laarman, P.W., and Gowing, H., Length–Weight Relationships, Manual of Fisheries Survey Methods II: With Periodic Updates, Ann Arbor: Michigan Department of Natural Resources, 2000, chapter 17, pp. 1–16. 70. Scott, W.B. and Crossman, E.J., Freshwater Fishes of Canada, Bull. Fish. Res. Bd. Can., 1973, no. 184, pp. 1–966. 71. Secor, D.H., Gunderson, T.E., and Karlsson, K., Effect of Temperature and Salinity on Growth Performance in Anadromous (Chesapeake Bay) and Non-Anadromous (Santee–Cooper) Strains of Striped Bass (Morone saxatilis), Copeia, 2000, no. 1, pp. 291–296. 72. Stone, J. and Barndt, S., Spatial Distribution and Habitat Use of Pacific Lamprey (Lampetra tridentata) Ammocoetes in a Western Washington Stream, J. Freshwat. Ecol., 2005, vol. 20, no. 1, pp. 171–185. 73. Stone, J., Sundlov, T., Barndt, S., and Coley, T., Evaluate Habitat Use and Population Dynamics of Lamprey in Cedar Creek, Annual Rept. (BPA Contract no. 200001400), U.S. Fish Wildlife Service, 2001. 74. The Freshwater Fishes of Europe, vol. 1, part 1: Petromyzontiformes (ed. J. Holcˇik), Wiesbaden: AULA–Verlag, 1986. 75. Willis, J.M., Pearcy, W.G., and Parin, N.V., Zoogeography of Midwater Fishes in the Subarctic Pacific, Bull. Ocean Res. Inst. Univ. Tokyo, 1988, no. 26, part 2, pp. 79–142. 76. Zender, H.H., Jr., Data report: 2002 Aleutian Islands Bottom Trawl Survey, U.S. Dep. Commer. NOAA Tech. Memo., NMFS–AFSC–143, 2004.
No. 5
2008
