Common deep-benthic skates (Rajidae) of the northwestern Pacific

Common deep-benthic skates (Rajidae) of the northwestern Pacific:
Basic ecological and biological features
by
Alexei ORLOV (1), Alexei TOKRANOV (2) & Raf FATYKHOV (3)
ABSTRACT. - Deep-benthic rajid skates represent an important component of bottom ichthyofauna of the western North
Pacific. In some areas they comprise up to 10% of fish biomass. Skates play significant role in food webs, consuming variety of fish and invertebrates including commercially important species. Russian fishery for skates in the northwestern
Pacific is poorly developed due to lack of domestic demand. Though skates are very promising target of inshore fisheries
with export to Asian fish markets. Their fishery should be based on intimate knowledge of their ecology and biology, which
are still poorly understood even for most common species inhabited the northwestern Pacific. The data on some ecological
parameters and biological features of seven most abundant and common species (Aleutian skate Bathyraja aleutica, whiteblotched skate B. maculata, Matsubara skate B. matsubarai, whitebrow skate B. minispinosa, Alaska skate B. parmifera,
Okhotsk skate B. violacea, and mud skate Rhinoraja taranetzi) were sampled in the Pacific waters off the northern Kuril
Islands and southeastern Kamchatka (47°50’N-52°10’N, depth range 85-850 m) during 1992-2002 bottom trawl surveys
and commercial fishing operations. The spatial and vertical distributions are presented, bottom temperature preferences are
shown, and dynamics of relative abundance are considered. Data on length frequencies, length-weight relationships, and
sex ratios in different size classes are presented. Data on sexual dimorphism in skate sizes are given as well. The study of
vertical ontogenetic shifts of skate species considered was attempted.
RÉSUMÉ. - Raies (Rajidae) bathyales communes du nord-ouest Pacifique : principales caractéristiques écologiques et
biologiques.
Les raies bathyales représentent un élément important de l’ichtyofaune profonde dans le Pacifique nord-ouest. Dans
certaines zones, elles constituent jusqu’à 10% de la biomasse en poisson. Les raies jouent un rôle significatif dans les
chaînes alimentaires, car elles consomment une grande variété de poissons et d’invertébrés, incluant des espèces commercialement importantes. Les pêches russes de raies dans le Pacifique nord-ouest sont peu développées car il n’existe aucune
demande domestique. Cependant, les raies sont des cibles prometteuses pour les pêches côtières car elles peuvent être
exportées vers les marchés asiatiques. Leur pêche devrait être fondée sur une connaissance précise de leur écologie et biologie, qui sont encore peu connues, même pour les espèces les plus communes du Pacifique nord-ouest. Les principaux
paramètres écologiques et biologiques de sept espèces communes et abondantes (la raie aléoutienne Bathyraja aleutica, la
raie à points blancs B. maculata, la raie de Matsubara B. matsubarai, la raie à sourcil blanc B. minispinosa, la raie d’Alaska
B. parmifera, la raie d’Okhotsk B. violacea, et la raie de vase Rhinoraja taranetzi) ont été déterminés à partir d’échantillons
collectés au nord des îles Kouriles et dans les sud-est du Kamchatka (47°50’N-52°10’N, intervalle de profondeurs : 85850 m) au cours de campagnes de chalutages et d’opérations de pêche commerciale effectuées entre 1992 et 2002. Les distributions spatiales et bathymétriques sont présentées, les preferendums thermiques sont mis en évidence, et la dynamique
des abondances relatives est analysée. Pour les différentes classes de tailles, les paramètres suivants sont donnés: les fréquences de tailles, les relations taille-poids, et le sex-ratio. Des informations sur le dimorphisme sexuel sont aussi présentées. L’étude des changements bathymétriques en fonction des stades ontogéniques est abordée.
Key words. - Rajidae - Skates - PNW - Kuril Islands - Kamchatka - Deepwater - Ecology - Biology .
The skates (Rajidae) are an important element of the bottom ichthyocoenes in the North Pacific. They feed on commercial fish species such as the Pacific herring Clupea pal lasii, walleye pollock Theragra chalcogramma, flathead
sole Hippoglossoides elassodon, yellowfin sole Limanda
aspera, northern rock sole Lepidopsetta polyxystra, Atka
mackerel Pleurogrammus monopterygius, Pacific cod
Gadus macrocephalus, shortraker rockfish Sebastes
borealis, popeye grenadier Coryphaenoides cinereus, and
invertebrates like red squid Berryteuthis magister, octopi
Octopoda, golden king crab Lithodes aequispinis, Tanner
crabs Chionoecetes spp. and shrimp (Mito, 1974; Brodeur
and Livingston, 1988; Livingston and deReynier, 1996;
Orlov, 1998a, 2003a; Chuchukalo et al., 1999; Chuchukalo
and Napazakov, 2002). In many countries, especially those
in Southeast Asia, skates are significant as commercial
species in coastal fisheries where their wings are dried up for
human consumption while meat is processed into fish meat
(1) Russian Federal Research Institute of Fisheries and Oceanography (VNIRO), 17 V. Krasnoselskaya, Moscow, 107140, RUSSIA.
[[email protected]]
(2) Kamchatka Branch of Pacific Institute of Geography, Far East Branch of Russian Academy of Science (KB PIG FEB RAS), 6
Partizanskaya St., Petropavlovsk-Kamchatsky, 683000, RUSSIA.
(3) Sakhalin Research Institute of Fisheries and Oceanography (SakhNIRO), 196 Komsomolskaya St., Yuzhno-Sakhalinsk, 693016,
RUSSIA.
Cybium 2006, 30(4) suppl.: 49-65.
ORLOV ET AL.
Deepwater skates of NW Pacific
jelly (Ishihara, 1990). To some extent, skates are promising
for Russian fisheries as well since in some areas they make
up about 10% of the total groundfish biomass, with a notable
upward trend in recent years (Orlov, 2003b). Skates show
some biological characteristics common for most of elasmobranch fishes (slow growth rate, late maturation and low
reproductive rate), which make them vulnerable to fishing
(Orlov, 2004). Optimum exploitation of stocks of the North
Pacific skates is obstructed by the lack of reliable catch
statistics and scarceness of data on their biology. Given this
background, the increased fishing pressure may affect the
stock condition of these fishes.
Despite the greater attention given recently to the study
of the North Pacific skates, most of publications cover only
some aspects of their biology and ecology (Teshima and
Tomonaga, 1986; Dolganov, 1998a, 1998b, 1998c, 1998d,
1999a, 1999b; Orlov, 1998a, 1998b, 1998c, 2003a;
Fatykhov et al., 2000; Chuchukalo et al., 1999; Chuchukalo
and Napazakov, 2002; Ebert, 2005) while the habitat of
skates in the North Pacific, trends in abundance variations,
and many features of their biology have been studied most
inadequately.
The purpose of this paper is to analyze spatial and vertical distribution of seven species of skates, which are the
most abundant ones in the North Kuril and Southeast Kamchatkan waters of the Pacific Ocean (Aleutian Bathyraja
aleutica, whiteblotched B. maculata, Matsubara B.
matsubarai, whitebrow B. minispinosa, Alaska B.
parmifera, Okhotsk B. violacea, and mud Rhinoraja
taranetzi skates) and to consider their distribution depending
on the bottom temperature, evaluate the relative abundance
of these species in the area surveyed with bottom trawl; analyze the size composition and body length/weight relations,
sex ratios in different size groups, sexual dimorphism in size
and stomach fullness based on the data sampled during bottom trawl surveys and commercial fishing operations in
1992-2002. Besides, an attempt was made to assess vertical
ontogenetic and diurnal migrations.
MATERIAL AND METHODS
The material for the analysis of the conditions of skates’
habitats, their spatial and vertical distribution and abundance
changes were obtained from 19 bottom trawl surveys totalizing 1,480 hauls, made from 1993 to 2000. The biological
parameters were examined from the materials collected in
50 exploratory cruises (over 10,000 bottom tows at 85850 m) in April-December, 1992-2002 in the Pacific near the
North Kuril Islands and Southeast Kamchatka (47°50’N to
52°10’N) as a joint project between VNIRO (Russian Federal Research Institute of Fisheries and Oceanography,
Moscow, Russia), SakhNIRO (Sakhalin Research Institute
50
of Fisheries and Oceanography, Yuzhno-Sakhalinsk, Russia)
and KamchatNIRO (Kamchatka Research Institute of Fisheries and Oceanography, Petropavlovsk-Kamchatsky, Russia). The volume of biological material collected for each
species of skate is indicated in table I. The species were
identified with the use of available identification sheets and
keys (Dolganov, 1983; Ishihara and Ishiyama, 1985; Dolganov and Tuponogov, 1999).
Round o’clock tows were made using bottom trawls with
vertical and horizontal openings of 5-7 m and c.a. 25 m
respectively (trawl opening parameters were monitored
instrumentally), the average speed being 3.6 knots. Since the
haul duration during cruises varied between 0.5 and 10
hours, all catches were later recalculated for standard one
hour hauls. In most cruises, the bottom temperature was
measured at each tow. The distribution of each species by
depth and as dependent on bottom temperature was analyzed
by the frequency of their occurrence (percent) estimated by
the mean catches per one hour haul.
The ontogenetic vertical migrations were analyzed using
distribution data by depths and mean body weight obtained
by dividing each total catch weight for the species of skate
examined by the number of individuals in the catch at the
check-point station of the bottom trawl survey. The analysis
of the daily vertical migrations was done by comparing
catch rate data at different time of the day using the results of
bottom trawlings too.
Stomach fullness index was defined according to a 5number scale: 0 = stomach empty to 4 = full stomach.
RESULTS
Spatial distribution.
Skates in question exhibited different patterns of spatial
distribution. B. aleutica was most abundant in the area
from central part of Shiashkotan Isl. coast to central part of
Paramushir Isl. Maximum catches comprised 100-300
specimens per h were recorded at the western slope of
underwater plateau and off neighboring seamounts, off the
central Onekotan Isl. and opposite the Fourth Kuril Strait
(Fig. 1A). B. maculata was the most abundant species in
area surveyed with maximum catches up to 1,200 individuals per hour. It was most numerous within the southern part
of the study area south of the Fourth Kuril Strait while its
maximum catches were registered from southern coast of
Shiashkotan Isl. to northern coast of Onekotan Isl.
(Fig.1B). B. matsubarai formed most dense aggregations
in two areas: north of the First Kuril Strait (southeastern
Kamchatkan coast) and south of the Fourth Kuril Strait
(from northern coast of Onekotan Isl. to central part of
western slope of underwater plateau). In both areas, catches of B. matsubarai comprised up to 250 specimens per
Cybium 2006, 30(4) suppl.
ORLOV ET AL.
Deepwater skates of NW Pacific
Table I. - Some biological features of common skates of the Pacific waters off the northern Kuril Islands and southeastern Kamchatka
(above the line minimum and maximum value of the feature are given, while under the line the average value and standard error are provided). [Quelques caractéristiques biologiques des raies communes des eaux du Pacifique au nord des îles Kouriles et au sud-est du Kamchat ka (les minima et les maxima sont au-dessus de la line, les moyennes et les écarts-types sont au-dessous ).]
hour but in the southern part of study area abundance of
species considered was considerably higher (Fig. 1C). B.
minispinosa occurred predominantly in the southern part
south of the Fourth Kuril Strait. Maximum catches exceeded 25 individuals per hour (Fig. 1D) were noted at northeastern slope of underwater plateau and between Onekotan
and Shiashkotan Islands. B. parmifera was less abundant
among species considered. The majority of its catches did
not exceed 10 specimens per hour (Fig. 1E). The single
catch exceeded 25 ind./h was registered in the area
between Shiashkotan and Onekotan Islands. B. violacea
occurred mostly within central and northern parts of the
area surveyed. It formed most dense concentrations with
catches ranged 151-300 specimens per hour opposite the
Fourth Kuril Strait and north of northern part of Paramushir Isl. (Fig. 1F). R. taranetzi was most abundant in
central part of study area from Onekotan Isl. to the First
Kuril Strait (Fig. 1G) though its maximum catches up to
300 specimens per h occurred opposite the First and Fourth
Kuril Straits and off central Paramushir Isl.
Cybium 2006, 30(4) suppl.
Vertical distribution
Our research shows that the B. parmifera, B. violacea
and R. taranetzi are the species found at lesser depths; they
did not occur at places deeper than 700, 650 and 700 m
respectively (Fig. 2). The B. minispinosa and B. matsubarai
were most deepwater species since 22.4% and 10.1% of the
total number of their individuals were caught deeper 700 m.
The vertical distribution of B. aleutica and B. maculata was
between the two above groups.
Bottom temperature
According to our data, between April and December the
skates in the Kuril and Kamchatkan waters of the Pacific
Ocean are found in bottom temperature range of about 0°C
and nearly 4°C, except for B. matsubarai, which occurred
near the bottom at up to 5.5°C (Fig. 3). The skates’ mode of
distribution as dependent on the bottom temperature has its
own features in each species. The relative abundance of B.
minispinosa in any temperature range was rather great,
though their individuals were at their maximum (48.6%) in
51
ORLOV ET AL.
Deepwater skates of NW Pacific
Figure 1. - Relative abundance and spatial distribution of B. aleutica (A),
B. maculata (B), B. matsubarai (C), B. minispinosa (D), B. parmifera (E),
B. violacea (F) and R. taranetzi (G) in the Pacific waters off the northern Kuril
Islands and southeastern Kamchatka, 1993-2000. 1: First Kuril Strait,
2: Shumshu Isl., 3: Paramushir Isl., 4: Fourth Kuril Strait, 5: Onekotan Isl.,
6: Shiashkotan Isl., 7: underwater plateau. Thin lines are 100, 200, 500 and
1000 m isobaths. [Abondance relative et distribution spatiale de B. aleutica (A),
B. maculata (B), B. matsubarai (C), B. minispinosa (D), B. parmifera (E),
B. violacea (F) et R. taranetzi (G) dans les eaux du Pacifique au nord des îles
Kouriles et au sud-est du Kamchatka, 1993-2000. 1 : Premier détroit des
Kouriles, 2 : Îles Shumshu, 3 : Île Paramushir, 4 : 4e détroit des Kouriles, 5 : Île
Onekotan, 6 : Île Shiashkotan, 7 : Plateau. Les lignes fines représentent les iso bathes 100, 200, 500 et 1000 m.]
the range of 2.5°C and 4.0°C. B. aleutica and B. maculata
distribution pattern was rather similar: both species were
most numerous within the bottom temperature range of
3.0°C-4.0°C (64.4 and 62.5% respectively). B. matsubarai
and B. parmifera were more numerous in two ranges of temperatures: 1.0°C-2.0°C (25.2%) and 2.5°C-3.5°C (46.4%) in
the case of the former species, and 1.5°C-2.5°C (32.3%) and
52
3.0°C-3.5°C (27.2%) in the case of the latter one. Unlike
them, B. violacea and R. taranetzi had the majority of their
individuals concentrate in a narrower temperature range. In
the first species, 35.3% was recorded between 3.0°C and
3.5°C while the other species in the same range had over half
of the number (54.4%). Three species (B. aleutica, B.
violacea and R. taranetzi) are the most stenothermic versus
Cybium 2006, 30(4) suppl.
ORLOV ET AL.
Deepwater skates of NW Pacific
Figure 2. - Vertical distribution of the most abundant skates in the
Pacific waters off the northern Kuril Islands and southeastern Kamchatka, 1993-2000. [Distribution verticale des raies les plus abon dantes dans les eaux du Pacifique au nord des îles Kouriles et au
sud-est du Kamchatka, 1993-2000.]
the other ones: their temperature ranges somewhat exceeds
3.5°C.
Body length and weight
B. maculata had the largest length range in the Pacific off
the Kurils and Southeast Kamchatka in 1992-2002 (Tab. I).
Its individuals in catches ranged between 17 and 134 cm
(total length). Though this skate was the longest among all
the seven species examined, its average length (62.52 cm)
was much lower than that of B. matsubarai (78.61 cm), B.
aleutica (82.40 cm) and, especially, B. parmifera (91.44 cm)
(Fig. 4). The B. minispinosa and R. taranetzi proved to be
the smallest, their average length being 54.59 cm and 51.71
cm respectively.
There was a high degree of correlation between the body
Cybium 2006, 30(4) suppl.
length and weight in all the skate species examined
(R2 > 0.95). The closeness of the linear and power coefficients (Tab. I) in the equations of the dependence considered
(2.2 x 10-3 - 5.9 x 10-3 and 3.05-3.24 respectively) makes the
curves rather similar (Fig. 5).
Our data show (Tab. I) that it was the B. aleutica, which
reached the maximum weight of body (14.1 kg). However,
in terms of respective average characteristics the leading
species was the B. parmifera (5.61 kg) whereas the mean
body weight of the B. aleutica was only 4.43 kg. According
to the linear size, B. minispinosa and R. taranetzi had the
smallest weight of body (the average 1.03 and 1.06 kg
respectively). As far as this indicator is concerned, B.
violacea was close to those two species (1.18 kg) despite its
total length of 60.66 cm, which is much bigger.
53
Deepwater skates of NW Pacific
ORLOV ET AL.
Figure 3. - Distribution of the most abundant skates in the Pacific
waters off the northern Kuril Islands and southeastern Kamchatka
depending on the bottom temperature, 1993-2000 (n = number of
observations). [Distribution des raies les plus abondantes dans les
eaux du Pacifique au nord des îles Kouriles et au sud-est du Kam chatka en fonction de la température du fond, 1993-2000 (n= nom bre d’observations).]
Vertical migrations
There was found that mean body weight of 3 of the 7
skates considered (B. aleutica, B. maculata and R. taranetzi)
decreased with depths increasing (Fig. 6). In the other
species similar tendency of mean body weight variations
was also observed but the range of variations was smaller.
Skate catch data in bottom trawl surveys made mostly
during summer/autumn period in the light time of the day
(03:00-19:00) were analyzed. There is no relationship
between the catch size and time of the day in any of the
skates studied (Fig. 7).
54
Sex ratios and sexual dimorphism
The quite equal proportions of males and females were
observed in some skates species inhabiting the Pacific
waters off the Kurils and Kamchatka (Tab. I). Females prevailed in catches of literally all species of skates. The
females of B. aleutica, B. maculata and B. violacea were
only slightly predominant in number (B. minispinosa and B.
parmifera provided too little data to be representative),
while female B. matsubarai and R. taranetzi were prevalent
in catches quite noticeably (1.4 and 1.8 times respectively).
Increasing of female proportion with the increased fish
Cybium 2006, 30(4) suppl.
ORLOV ET AL.
Deepwater skates of NW Pacific
Figure 4. - Length frequencies of the most abundant skates in the
Pacific waters off the northern Kuril Islands and southeastern
Kamchatka, 1993-2000. [Fréquences de tailles des raies les plus
abondantes dans les eaux du Pacifqiue au nord des îles Kouriles
et au sud-est du Kamchatka, 1993-2000.]
size was observed in R. taranetzi only (Fig. 8). The sex ratio
was about equal in the smallest skates < 30 cm, while the
proportion of females among the largest individuals was
88%. Females are slightly more numerous among the small
individuals of B. aleutica; in larger fish proportion between
males and females was almost equal. Data are insufficient
for the B. minispinosa and B. parmifera. In the other three
Cybium 2006, 30(4) suppl.
species there is an apparent tendency for the sex ratio to
change the bigger the fish are: females prevail in the smallsized groups, while males are more numerous among the
fish of large size.
Stomach fullness
In autumn and summer period when most studies of
55
Deepwater skates of NW Pacific
ORLOV ET AL.
Figure 5. - Relations between total length and body weight of the
most abundant skates in the Pacific waters off the northern Kuril
Islands and southeastern Kamchatka, 1993-2000. [Relations
entre la longueur totale et le poids du corps des raies les plus
abondantes des eaux du Pacifique au nord des îles Kouriles et
au sud-est du Kamchatcka, 1993-2000.]
skates’ feeding were made the stomach fullness by the
species examined was rather high (Tab. I). The B. maculata,
B. parmifera and B. violacea contained the largest number
of individual fish with the maximum fullness of stomachs,
and the smallest number of not feeding fish (Fig. 9). Stomach fullness of B. matsubarai and B. aleutica were lesser; a
56
large number of fish had empty stomachs. Virtually all the
species studied, except the B. minispinosa, had their females
having fuller stomachs than males. While B. maculata and
B. matsubarai females and males differed in stomach fullness insignificantly, among B. aleutica, B. parmifera and R.
taranetzi those differences were rather considerable.
Cybium 2006, 30(4) suppl.
ORLOV ET AL.
Deepwater skates of NW Pacific
Figure 6. - Relations between mean body weight and capture depth
of the most abundant skates in the Pacific waters off the northern
Kuril Islands and southeastern Kamchatka, 1993-2000. [Relations
entre le poids moyen du corps et la profondeur de capture des raies
les plus abondantes das eaux du Pacifique au nord des îles
Kouriles et au sud-est du Kamchatka, 1993-2000.]
Dynamics of abundance
The results of the bottom trawl surveys made in the area
of study in 1993-2000 indicate that there is general growth
in the abundance of skates (Fig. 10). The data available
allow us to make some conclusions regarding the relative
abundance of each of the species examined, and their
dynamics during the period of consideration. The results of
the surveys show that it is B. maculata that is the most abundant in the survey area. B. aleutica and B. violacea rank second and third, followed by R. taranetzi and B. matsubarai.
Cybium 2006, 30(4) suppl.
B. parmifera and B. minispinosa are least abundant species
in the area surveyed.
The survey results relating to the four more easily identifiable species in catches show that the relative abundance of
the B. aleutica and B. parmifera went down in recent years.
The number of B. maculata went up notably in 1999 and
2000. In B. matsubarai, despite the increased catches in
2000 against the previous year, the relative abundance
shows some decline.
57
Deepwater skates of NW Pacific
DISCUSSION
Spatial distribution
Spatial distribution of the North Pacific skates is studied
insufficiently. Patterns of spatial distribution were previously reported in the Pacific waters of the North Kurils and
Southeast Kamchatka waters only (Orlov, 1999; Fatykhov et
al., 2000). However, the first paper briefly described spatial
distribution of six species based on limited data obtained
from about 1,000 commercial bottom trawl hauls conducted
in 1992-1996, while in the second paper, the spatial distribution of only four largest skates are presented based on data
obtained during very short period (1996-1997). Despite the
limited data used in both above
papers, they show that in general
the higher aggregations of skates
species studied have been occurred
at the same places during the whole
period of investigations.
ORLOV ET AL.
the North Kurils has been reviewed in several papers (Orlov,
1998b; Fatykhov et al., 2000; Moukhametov and Poltev,
2003); but the data are fragmentary. In publications of Orlov
(1998b) and Fatykhov et al. (2000), the bathymetrical characteristics were reviewed on the basis of combined data
from bottom trawl surveys and commercial fishing tows (in
the latter case the initial and final depths of fishing might
vary notably) made during a relatively short period of time
(1993-1996 and 1996-1997 respectively). Besides, the paper
of Fatykhov et al. (2000) considers the vertical distribution
pattern of four largest species only: B. aleutica, B. maculata,
B. parmifera and B. matsubarai. Moukhametov and Poltev
(2003) used the data based on the results of a single survey
Vertical distribution
Although vertical distribution
of the North Pacific skates has been
reviewed in a number of papers, it
still remains not studied adequately
enough. Only depth ranges of some
species, and capture depths can be
found in some publications (Eschmeyer et al., 1983; Dudnik and
Dolganov, 1992; Nakaya and Shirai, 1992; Amaoka et al., 1995;
Dolganov, 1999b; Fedorov, 2000;
Sheiko and Fedorov, 2000; Parin,
2001; Ebert, 2003). The single
paper (Fedorov, 2000) provides the
preferred depth ranges for several
species. More detailed data on the
vertical distribution of some of the
North Pacific skates are given in
Dolganov (1998b), who reviews
the bathymetric features of five
species in the western Bering Sea
and, moreover, considers them with
200 m increment. The vertical distribution of skates in the Pacific off
Figure 7. - Diurnal changes of catch
rates of the most abundant skates in the
Pacific waters off the northern Kuril
Islands and southeastern Kamchatka,
1993-2000. [Variations diurnes des
taux de capture des raies les plus abon dantes des eaux du Pacifique au nord
des îles Kouriles et au sud-est du Kam chatka, 1993-2000.]
58
Cybium 2006, 30(4) suppl.
ORLOV ET AL.
Deepwater skates of NW Pacific
Figure 8. - Proportion of females within different length classes of
the most abundant skates in the Pacific waters off the northern
Kuril Islands and southeastern Kamchatka, 1993-2000. [Propor tion des femelles dans les différentes classes de tailles des raies les
plus abondantes des eaux du Pacifique au nord des îles Kouriles et
au sud-est du Kamchatka, 1993-2000.]
made in February-April 2002.
There is no common view regarding bathymetric ranges
of skate species in question. Some authors (Sheiko and
Fedorov, 2000; Moukhametov and Poltev, 2003) consider all
the skates mesobenthic, i.e. occurring mainly in the upper
bathyal zone (mesobenthal), namely between 200 and 500 m
depth. Orlov (1998b) refers B. matsubarai to bathybenthal
species; Dolganov (1998b) includes B. aleutica in the same
category. According to our data, B. aleutica should be considered mesobenthic. Off the west coast of the USA, all of
captures of this skate were recorded within 438-613 m
depth, the average capture depth being 499.5 m (Hoff,
2002). Our research showed that all the species of skates
considered belong to the mesobenthal ichthyocoene except
B. matsubarai which has to be referred to the bathybenthal
grouping since 46.7% of its individuals were recorded within the lower bathyal layer while only 43.7% of the relative
abundance was found in the upper bathyal layer. The most
Cybium 2006, 30(4) suppl.
skates of the other species were recorded within the
mesobenthal layer: 57.5% B. aleutica, 65.0% B. maculata,
51.8% B. minispinosa, 48.6% B. parmifera, 74.2% B.
violacea, 84.1% R. taranetzi.
Bottom temperature
The distribution of the North Pacific skates in relation to
the bottom temperature is largely unknown. Dolganov
(1998c) indicates the temperature range where various
species occur in the West Bering Sea and shows the summer
and winter distribution patter depending on the bottom temperature of four species: B. parmifera, B. violacea, B.
aleutica and B. matsubarai. The distribution patterns of four
largest skates in terms of the bottom temperature in the
Kamchatkan and Kuril waters in various time periods of
1996 (May, October) and 1997 (May, August) was analyzed
by Fatykhov et al., (2000) using a small set of catch rates of
skates in different temperature ranges.
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Deepwater skates of NW Pacific
ORLOV ET AL.
Figure 9. - Stomach fullness of the most abundant skates in the Pacific waters off the northern Kuril Islands and southeastern Kamchatka,
1993-2000. [Taux de remplissage des estomacs des raies les plus abondantes des eaux du Pacifique au nord des îles Kouriles et au sud-est
du Kamchatka, 1993-2000.]
There are virtually no data on bottom temperatures at
which deep-benthic skates occur in other areas of the North
Pacific. There are only data available that B. aleutica off the
U.S. west coast were recorded within the bottom temperatures of 5.2°C-5.9°C, while the average was 5.47°C (Hoff,
2002).
Body length and weight
The data on sizes of the North Pacific skates available
from the literature is mostly referred to their maximum body
60
length. The following values of maximum length appeared
in published sources: 151 cm for B. aleutica (Ishiyama,
1958), 120 cm for B. maculata and 83 for B. minispinosa
(Mecklenburg et al., 2002), 77 cm for R. taranetzi (Ebert,
2005), 129 cm for B. parmifera, 126 for B. matsubarai and
84 cm for B. violacea (Dolganov and Tuponogov, 1999).
Most of our specimens did not exceed known maximum
length, except for B. maculata and B. violacea whose TL
reached of 134 and 102 cm respectively.
The larger average length of B. parmifera in comparison
Cybium 2006, 30(4) suppl.
ORLOV ET AL.
Deepwater skates of NW Pacific
Figure 10. - Multi-annual changes of relative abundance of skates
in the Pacific waters off the northern Kuril Islands and southeastern Kamchatka, 1993-2000. [Variations pluri-annuelles de
l’abondance relative des raies les plus abondantes des eaux du
Pacifique au nord des îles Kouriles et au sud-est du Kamchatka,
1993-2000.]
Cybium 2006, 30(4) suppl.
61
Deepwater skates of NW Pacific
to B. maculata and B. aleutica can be explained by the fact
that latter two species have the larger amount of juveniles in
catches. The lesser number of juvenile skates found in B.
parmifera is likely related to their inhabitation at shallower
depths. Small number of juvenile B. matsubarai in the catches is probably associated with a more deepwater distribution
pattern of the immature individuals in this bathybenthal
species.
As for the weight and relationships between length and
weight of skates, no data were found in literature. The similarity of linear and power coefficients in the length-weight
relationships probably shows that in all these species of
skates the growth mechanisms are alike.
Vertical migrations
The knowledge of vertical migrations of the North Pacific skates is scant. Dolganov (1998b) stated that some upper
and lower bathyal species migrate seasonally, leaving for
greater depths in winter; the magnitude of such migrations in
youngs and adults being different.
Our data on changes of body weight with depth show
that the large individuals inhabit shallower places than the
young fish, and the skates do make ontogenetic vertical
migrations. Their egg capsules being attached to the substrate with horny projections and fibrillar filaments (Dolganov, 1998d), they cannot be carried away to deeper layers
by currents, thus females have to migrate to spawning sites
for laying eggs, while the young have to shift themselves
gradually to shallower places with growth. A transport of the
hatched embryos from the shelf to bigger depths by the nearbottom currents is not likely since the empty egg capsules
are more often found at the concentration sites of the young,
i.e. the juvenile skates do not abandon the spawning ground
at once and stay for some more time. Such logics disagree
with the existing concept of a continuous conveyor method
of reproduction of the Far East deep-benthic skates all the
year round (Dolganov, 1998d) since otherwise, given this
way of breeding, the females would have to migrate from
shallow to deeper places several times a year. The incubation
period and hatching are unknown in the Far Eastern deepbenthic skates. In some other species of Bathyraja incubation lasts for 6-9 months (Bor, 2002) while the incubation
period of the North Atlantic Raja species takes from 9 weeks
to 15 months (Wourms, 1977). Based on those data, it could
be assumed that the females lay eggs twice a year at the
most, hence making as many spawning migrations. The
complex population structure of the skate species examined
includes individuals of various ages, which probably results
from the time difference in laying egg by the females. Therefore, the spawning time disparity in individual females
extends the process of spawning among the entire population to the whole year, which given the limited food resource
on the continental slope, ensures a better food supply to the
62
ORLOV ET AL.
progeny and, as consequence, its improved survival rate.
Skates are capable of preying on pelagic prey (Orlov,
1998a,c, 2003a; Chuchukalo and Napazakov, 2002).
Epipelagic and even mesopelagic captures of skates have
been reported by Shuntov and Bocharov (2003). This shows
the ability of skates to migrate vertically into water column,
though it was unclear if these migrations are regular (diurnal) or incidental. In our study the captures of skates in midwater layers were incidental; pelagic fish and squids were
found sporadically in their stomachs.
Sex ratios and sexual dimorphism
Dolganov (1998d) suggests about equal ratio between
females and males in most populations of skates in the
Northwest Pacific with the prevalence of the females in the
older age groups only. In the Eastern Bering Sea, proportion
of females and males in catches is almost equal in each
species except for B. parmifera, where males prevailed 27
times over females (Ebert, 2005). In our study, almost equal
sex ratio occurred in the B. aleutica and B. violacea while in
other species females were predominant. These differences
are probably related to the variation of the sex ratio with
depth, latitude, habitat, season, and bottom temperature
(McEachran and Musick, 1975; Compagno et al., 1991).
Many species are known to segregate by sex, size and maturity status, and this may have some influence on sex ratio
(Ebert, 2003).
Data regarding the sex ratios of skates considered in different size groups appeared in two recent papers (Dolganov,
1998d; Ebert, 2005). First author noted that the females prevail in the largest skates irrespective of species. Second
author showed that almost equal sex ratio occur in all
species examined among juveniles in the eastern Bering Sea.
Adolescent male B. maculata were caught in greater number
than females. Among adults, females of the B. aleutica were
notably abundant in catches in comparison to males while in
other species males prevailed over females. These data differ
somewhat from our observations. These discrepancies may
be related to the presence of sexual dimorphism in the body
length and weight of the species considered (Tab. I) as pointed out by Orlov (1998a, 1998c, 2003) and by Ebert (2005).
Four of the seven species examined (B. maculata, B.
parmifera, B. matsubarai and R. taranetzi) had their females
of greater length than males. Mean length differences of B.
maculata and B. matsubarai were weak (0.2-1.3 cm). In the
other species males are greater than females. The body
weight differences are observed in some species. For
instance, female B. maculata were larger than males in body
length, but weighed somewhat less. Conversely, the males of
B. violacea were somewhat larger but weighed less than
females, in average.
As for the relationship of sexual demorphism in sizes of
the skates studied and sex ratio in different size groups, we
Cybium 2006, 30(4) suppl.
ORLOV ET AL.
can make some tentative judgment. As was shown above
(Fig. 8), the increasing of female proportion with size
increasing was characteristic for R. taranetzi only. Females
of this species are much longer (by about 6 cm) and heavier
(by about 400 g) than males, in average. Given the mean
sizes of males and females, it constitutes the difference
between them of over 10% in the length and about 38% in
the body weight. The prevalence of females in all size
groups is likely to determine such a great relative differences. The sex ratio of B. aleutica and B. maculata is about
the same in all size groups, and the relative difference in size
between males and females is weak. The results obtained in
B. matsubarai and B. violacea probably do not reflect the
actual situation since the data on sex ratios within larger size
groups are very limited.
Stomach fullness
Despite the large number of publication on food habits of
the Far Eastern skates which appeared in recent years (Dolganov, 1998a; Orlov, 1998a, 1998c, 2003a; Chuchukalo et
al., 1999; Chuchukalo and Napazakov, 2002) it is the first
one that considers, besides diet composition, the intra-annual variations of stomach fullness, and its changes depending
on the bottom temperature, though these data were given
only in respect of the B. violacea and B. parmifera.
The difference in stomach fullness by fish of both sexes
may result from their different physiological condition.
However, since the life history of the Far Eastern skates has
been studied most insufficiently, it would be impossible to
determine with certainty the causes for the differences found
in stomach fullness of males and females of individual
species.
Dynamics of abundance
Skates are considered as a potential target for Russian
fisheries, and some assessment containing TAC estimations
began to be generated in recent years. However, the problems of their stock dynamics remain to be unexplored. The
data on the total biomass of skates in some parts of the Russian Far Eastern EEZ are found in several papers: Dolganov
(1999a) and Fatykhov et al. (2000) provide data on biomass
by species. The first paper deals with ten of the most abundant species within the entire Russian Far Eastern zone, by
areas; the second paper covers four species in the Pacific off
the North Kurils and Southeast Kamchatka. The biomass
data result from trawl surveys, but stock dynamics data are
not available.
Our results disagree considerably with Dolganov data
(1999a) that the biomass of B. parmifera off the East Kamchatka and Kuril Islands is the largest, decreasingly followed
by the biomass of B. matsubarai, B. violacea, B. aleutica, B.
maculata, R. taranetzi and B. minispinosa. This disagreement might result from the smaller area of our study, and
Cybium 2006, 30(4) suppl.
Deepwater skates of NW Pacific
smaller depth range examined (100-850 vs 50-2000 m).
The fact that skate species in each haul during our surveys began to be identified in the recent two years only complicates the analysis. Prior to 1999 the species of skates were
not identified during individual surveys, or the largest and
easily recognizable species were recorded: B. aleutica, B.
parmifera, B. maculata and B. matsubarai. That is why in
some years B. violacea, B. minispinosa and R. taranetzi
were actually not recorded in catches at all. The exclusively
high catches of B. minispinosa made in 1996 can hardly be
recognized as true. Most likely, they were heavily exaggerated because of the incorrect species identification. Even if the
catch data for the current year are excluded, the relative
abundance trend generally is pointed upward in a stable way.
At present it is difficult to make assumptions regarding the
quantity of B. violacea and R. taranetzi since it is only the
two recent year’s data that can be recognized reliable for the
above reasons.
Abundance of some skates species exhibit a similar trend
in any other areas of the North Pacific too. For instance, the
abundance of B. parmifera and B. aleutica in the Gulf of
Alaska increased by many times throughout the period of
study according to the trawl survey data of 1984-2003
(Gaichas et al., 2003).
Acknowledgements. - Authors would like to express their gratitude to all scientists of VNIRO, KamchatNIRO, SakhNIRO and
other institutions who participated in 1992-2002 in sampling of
data used in this paper. Special thanks go to our colleagues and
friends Yu.N. Poltev and I.N. Moukhametov (SakhNIRO) who provided us with some data on R. taranetzi. We also appreciate valuable comments on the manuscript of anonymous reviewer and Dr.
Bernard Séret (Museum national d’Histoire naturelle, Paris,
France) who considerably improved it.
REFERENCES
AMAOKA K., NAKAYA K. & M. YABE, 1995. - The Fishes of
Northern Japan. 390 p. Sapporo: Kita Nihon Kayo Center Co.
Ltd.
BOR P., 2002. - Egg-capsules of sharks and skates. World Wide
Web Electronic Publication. http://www.rajidae.tmfweb.nl/
rogtable.html.
BRODEUR R.D. & P.A. LIVINGSTON, 1988. - Food habits and
diet overlap of various Eastern Bering Sea fishes. U.S. Dep.
Commer., NOAA Tech. Memo. NMFS F/NWC, 127: 1-76.
CHUCHUKALO V.I. & V.V. NAPAZAKOV, 2002. - Feeding and
trophic status of abundant skate species (Rajidae) of the western Bering Sea. Izv. TINRO, 130: 424-428. [In Russian]
CHUCHUKALO V.I., LAPKO V.V., KUZNETSOVA N.A. et al.,
1999. - Feeding of groundfishes on the shelf and continental
slope of the northern Sea of Okhotsk. Izv. TINRO, 126: 24-57.
[In Russian]
COMPAGNO L.J.V., EBERT D.A. & P.D. COWLEY, 1991. - Distribution of offshore demersal cartilaginous fishes (Class Chondrichthyes) off the west coast of Southern Africa, with notes on
their systematics. S. Afr. J. Mar. Sci., 11: 43-139.
63
Deepwater skates of NW Pacific
DOLGANOV V.N. & V.N. TUPONOGOV, 1999. - Identification
sheets of skates of genera Bathyraja and Rhynoraja (family
Rajidae) of the Russian Far East Seas. Izv. TINRO, 126: 657664. [In Russian]
DOLGANOV V.N., 1983. - Guide to the Diagnostic Characters of
Cartilaginous Fishes from the Far East Seas of the U.S.S.R. and
Neighboring Waters. 92 p. TINRO: Vladivostok. [In Russian]
DOLGANOV V.N., 1998a. - Feeding of skates of the family Rajidae and their role in the ecosystems of Russian Far East seas.
Izv. TINRO, 124: 417-424. [In Russian]
DOLGANOV V.N., 1998b. - Distribution and migration of skates
of family Rajidae of the Far-Eastern Seas of Russia. Izv.
TINRO, 124: 433-437. [In Russian]
DOLGANOV V.N., 1998b. - Reproduction of skates of the family
Rajidae and their role in the ecosystems of Russian Far East
seas. Izv. TINRO, 124: 425-428. [In Russian]
DOLGANOV V.N., 1998c. Environmental abiotic conditions of
skates of the family Rajidae of Russian Far East seas. Izv.
TINRO, 124: 429-432. [In Russian]
DOLGANOV V.N., 1999a. - Abundance of skates in Russian economic zone of the Far Eastern seas. Izv. TINRO, 126: 650-652.
[In Russian]
DOLGANOV V.N., 1999b. - Geographic and bathymetric distribution of skates of the family Rajidae in the Russian Far East seas
and adjacent waters. Vopr. Ikhtiol., 39: 428-430. [In Russian]
DUDNIK Yu.I. & V.N. DOLGANOV, 1992. - Distribution and
stocks of fishes on the continental slope of the Sea of Okhotsk
and Kuril Islands in summer of 1989. Vopr. Ikhtiol., 32: 83-98.
[In Russian]
EBERT D.A., 2003. - Sharks, Rays and Chimaeras of California.
284 p. Berkeley, California: Univ. of California Press.
EBERT D.A., 2005. - Reproductive biology of skates, Bathyraja
(Ishiyama), along the eastern Bering Sea continental slope. J.
Fish. Biol., 66: 618-649.
ESCHMEYER W.N., HERALD E.S. & H. HAMMAN, 1983. - A
Field Guide to Pacific Coast Fishes. 336 p. Boston: Houghton
Mifflin Co.
FATYKHOV R.N., POLTEV Yu.N., MOUKHAMETOV I.N. et al.,
2000. - Spatial distribution of skate mass species, Bathyraja, in
the region of the Northern Kuril Islands and Southeastern Kamchatka in different seasons of 1996-1997. In: Commercial and
Biological Studies of Fishes in the Pacific Waters of the Kurils
Islands and Adjacent Areas of the Okhotsk and Bering Seas in
1992-1998 (Kotenev B.N., ed.), pp. 104-120. Moscow:
VNIRO. [In Russian]
ORLOV ET AL.
HOFF G.R., 2002. - New records of the Aleutian skate, Bathyraja
aleutica from northern California. Calif. Fish Game, 88: 145148.
ISHIHARA H. & R. ISHIYAMA, 1985. - Two new North Pacific
skates (Rajidae) and revised key to Bathyraja in the area. Jpn. J.
Ichthyol., 32: 1-23.
ISHIHARA H., 1990. - The skates and rays of the western North
Pacific: An overview of their fisheries, utilization, and classification. U.S. Dept. Commer., NOAA Tech. Rep. NMFS, 90: 485-497.
ISHIYAMA R., 1958. - Studies on the rajid fishes (Rajidae) found in
the waters around Japan. J. Shimonoseki Coll. Fish., 7: 193-394.
LIVINGSTON P.A. & Y. DE REYNIER, 1996. - Groundfish food
habits and predation on commercially important prey species in
the Eastern Bering Sea from 1990 to 1992. U.S. Dep. Commer.,
NOAA/NMFS, Alaska Fish. Sci. Cent. Proc. Rep., 9604: 1-214.
MCEACHRAN J.D. & J.A. MUSICK, 1975. - Distribution and relative abundance of seven species of skates (Pisces: Rajidae)
which occur between Nova Scotia and Cape Hatteras. Fish.
Bull., 73: 110-136.
MECKLENBURG
C.W.,
MECKLENBURG
T.A.
&
L.K.THORSTEINSON, 2002. - Fishes of Alaska. 1037 p.
Bethesda, Maryland: American Fisheries Society.
MITO K., 1974. - Food relationships among benthic fish populations in the Bering Sea on the Theragra chalcogramma fishing
grounds in October and November of 1972. M.S. Thesis. Hakodate: Hokkaido Univ. Graduate School, 135 p.
MOUKHAMETOV I.N. & Yu.N. POLTEV, 2003. - Results of faunistic studies conducted aboard R/V “Dmitry Peskov”
(SakhNIRO) in February-April 2002 off the Kuril Islands
(marine fishes). Trudy SakhNIRO, 5: 25-46. [In Russian]
NAKAYA K. & S. SHIRAI, 1992. - Fauna and zoogeography of
deep-benthic chondrichthyan fishes around the Japanese
archipelago. Jpn. J. Ichthyol., 39: 37-48.
ORLOV A.M., 1998a. - Materials on the feeding of mass species of
deep-sea skates (Bathyraja spp., Rajidae) from the Pacific
waters of the northern Kurils and southeastern Kamchatka.
Vopr. Ikhtiol., 38: 659-668. [In Russian]
ORLOV A.M., 1998b. - The diets and feeding habits of some deepwater benthic skates (Rajidae) in the Pacific waters off the
northern Kuril Islands and southeastern Kamchatka. Alaska
Fish. Res. Bull., 5: 1-17.
FEDOROV V.V., CHERESHNEV L.A., NAZARKIN M.V. et al.,
2003. - Catalog of Marine and Freshwater Fishes of the Northern Part of the Sea of Okhotsk. 204 p. Vladivostok: Dal’nauka.
[In Russian]
ORLOV A.M., 1998c. - Demersal ichthyofauna of Pacific waters
off the northern Kuril Islands and southeastern Kamchatka.
Biol. Morya, 24: 146-160. [In Russian]
ORLOV A.M., 1999. - Trophic relationships of commercial fishes
in the Pacific waters off southeastern Kamchatka and the northern Kuril Islands. In: Ecosystem Approaches for Fisheries
Management. pp. 231-263. Fairbanks, Univ. of Alaska. Alaska
Sea Grant Coll. Prog., AK-SG-99-01.
ORLOV A.M., 2003a. - Diets, feeding habits, and trophic relations
of six deep-benthic skates (Rajidae) in the western Bering Sea.
Aqua, J. Ichthyol. Aquat. Biol., 7: 45-60.
ORLOV A.M, 2003b. - Ichthyocoenes of the lower shelf and upper
bathyal of the Pacific waters off the northern Kuril Islands and
southeastern Kamchatka. Ph.D. Thesis, 47 p. Moscow:
VNIRO. [In Russian]
GAICHAS S., RUCCIO M., STEVENSON D., & R. SWANSON,
2003. - Stock assessment and fishery evaluation of skate
species (Rajidae) in the Gulf of Alaska. In: Stock Assessment
and Fishery Evaluation Report for the Groundfish Resources of
the Gulf of Alaska. pp. 719-756. Anchorage: North Pacific
Fishery Management Council.
ORLOV A.M., 2004. - Deep-water chondrichthyan species: Problems of biodiversity conservation and fisheries management some results of FAO and IUCN workshop (Dunedin, New
Zealand, 27-29 November 2003). Ecology- XXIcentury.World
Wide Web Electronic Publication. http://www.ecology21.info/
_order/_html_publication/00004.html (In Russian).
FEDOROV V.V., 2000. - Species composition, distribution and
habitation depths of the Northern Kuril Islands fish and fishlike species. In: Commercial and Biological Studies of Fishes
in the Pacific Waters of the Kuril Islands and Adjacent Areas of
the Okhotsk and Bering Seas in 1992-1998 (Kotenev B.N.,
ed.), pp. 7-41. Moscow: VNIRO. [In Russian]
64
Cybium 2006, 30(4) suppl.
ORLOV ET AL.
PARIN N.V., 2001. - An annotated catalog of fishlike vertebrates
and fishes of the seas of Russia and adjacent countries. Part 1.
Orders Myxiniformes-Gasterosteiformes. J. Ichthyol.,
41(Suppl. 1): S51-S131.
SHEIKO B.A. & V.V. FEDOROV, 2000. - Chapter 1. Class Cephalaspidomorphi - Lampreys. Class Chondrichthyes - Cartilaginous Fishes. Class Holocephali - Chimaeras. Class Osteichthyes - Bony Fishes. In: Catalogue of Vertebrates of Kamchatka and adjacent Waters. (Moiseev R.S. & A.M. Tokranov,
eds.), pp. 7-69. Petropavlovsk-Kamchatsky: Kamchatskii
Pechatnyi Dvor. [In Russian]
Cybium 2006, 30(4) suppl.
Deepwater skates of NW Pacific
SHUNTOV V.P. & L.N. BOCHAROV (Eds.), 2003. - Atlas of
quantitative distribution of nekton in the Sea of Okhotsk.
1040 p. Moscow: Izdatel’stvo “FGUP Natsional’nyie Rybnyie
Resursy”. [In Russian]
TESHIMA K. & S. TOMONAGA, 1986. - Reproduction of Aleutian skate, Bathyraja aleutica, with comments on embryonic
development. In: Proc. Second Internat. Conf. Indo-Pacific
Fish (Uyeno T., Arai R., Taniuchi T. & K. Matsuura, eds),
pp. 303-309. Tokyo: Tokyo National Museum.
WOURMS J.P., 1977. - Reproduction and development of chondrichthyan fishes. Am. Zool., 17: 379-410.
65