- Email: [email protected]
Fish populations of Port Foster, Deception Island, Antarctica and vicinity
ARTICLE IN PRESS
Deep-Sea Research II 50 (2003) 1843–1858
Fish populations of Port Foster, Deception Island, Antarctica and vicinity Henry A. Ruhla,*, Philip A. Hastingsa, Lisa A. Zarubicka, Rachelle M. Jensena, Krzysztof Zdzitowieckib a
Marine Biology Research Division, 0202, Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA 92093-0202, USA b Institute of Parasitology, Polish Academy of Sciences, Twarda 51/55, Warszawa 00-818, Poland Received 16 September 2002; received in revised form 20 December 2002; accepted 6 January 2003
Abstract The fish populations of Port Foster, Deception Island, South Shetland Islands, Antarctica, were investigated as part of the Erupt Antarctic ecosystem study. Surveys were conducted on five cruises between March 1999 and November 2000. Samples also were collected off Livingston Island and King George Island of the South Shetland Islands. Specimens were collected or observed using a multiple opening and closing net and environmental sampling system, otter trawls, benthic line-transect photography, and remotely operated vehicle video. Species composition, length, weight, reproductive condition, diet, habitat, and parasitic infestation were examined for the dominant fish species. Eleven species were collected, all in the suborder Notothenioidei. The fishes found in the survey are known to occur in the region and had diets similar to those found in other studies. Abundances of demersal fishes in Port Foster ranged from 0.05 to 0.10 individuals m2 over the study period. Inshore shallow-water (o30 m) and inshore deep-water (>30 m) habitats are identified in Port Foster and described. Port Foster may be a refuge for juvenile fishes such as Champsocephalus gunnari. Limited exchange with the surrounding waters also may limit the influence of recruitment and prey abundance fluctuations outside Port Foster. Trematomus scotti had heavy body cavity parasite infestation from Port Foster, possibly due in part to decreased benthic scour from large icebergs, allowing benthic parasites to persist. r 2003 Elsevier Ltd. All rights reserved.
1. Introduction The fishes of Port Foster, Deception Island, Antarctica, and vicinity were investigated as part of the Erupt Antarctic ecosystem study. Fishes were collected on five cruises in March and November 1999, and February, June, and No*Corresponding author. Tel.: +1-858-534-4858; fax: +1858-534-7313. E-mail address: [email protected] (H.A. Ruhl).
vember 2000. While many fish surveys have been conducted in the region, relatively little is known about the fish populations of inshore deep-water habitats such as Port Foster. Notothenioid fishes were the only fishes noted during the Erupt survey. Deception Island is located at the southwest end of the South Shetland Islands (Fig. 1) in a region of seasonal pack-ice coverage. It is a flooded volcanic caldera, which creates an almost entirely enclosed body of water with only a narrow shallow connection to the Bransfield Strait and
0967-0645/03/$ - see front matter r 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0967-0645(03)00094-8
ARTICLE IN PRESS 1844
H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
Fig. 1. Chart of the South Shetland Islands, Antarctica. The black box indicates Deception Island represented in Fig. 2. The black dots indicate the location of otter trawl surveys conducted off Livingston and King George Islands.
surrounding waters (Fig. 2). The connection is 550 m wide at the narrowest point and has a depth of 11 m. The protected embayment within the caldera, Port Foster, is 9.8 km long 5.7 km wide. The sheltered nature of Port Foster also limits the routinely intense wave energy of the Southern Ocean, benthic habitat scour due to large drifting icebergs, and the flow of seasonal pack ice. Habitat destruction due to the calving and movement of large icebergs has been shown to cause niche separation in some notothenioid fishes (Brenner et al., 2001). Port Foster is thus likely to have a less variable benthic habitat and epipelagic habitat than more exposed communities in the region. However, the caldera is subject to active volcanic and seismic activity. For a full description of Port Foster, Deception Island, and the Erupt program see Smith et al. (2003). Livingston Island is located north of Deception, and King George Island is located further to the northeast along the South Shetland Island chain (Fig. 1). Fishes of the suborder Notothenioidei dominate the diversity and biomass of the demersal fishes
found in the Southern Ocean (Gon and Heemstra, 1990; Miller, 1993). Of the approximately 260 fish species known to occur in the Southern Ocean, nearly half are in the suborder Notothenioidei and represent roughly 90% of all individuals collected in shelf and slope waters (Eastman and Clarke, 1998). Some commercially important species in the South Shetland Islands include Champsocephalus gunnari, Chaenocephalus aceratus, Notothenia rossii, and Gobionotothen gibberifrons (=Notothenia gibberifrons) (Kock, 1992; Jones et al., 2001). The fishery for these species was closed in the region in 1989/1990 (Jones et al., 2001) due to overfishing. Numerous phylogenetic, ecological, physiological, and biochemical studies have examined several characteristics unique to notothenioid fishes, such as the reduction or lack of hemoglobin and swim bladders, production of glycopeptide antifreeze, and greatest species richness at 300–600 m (Eastman, 1990; Miller, 1993; Kock, 1992; Clarke and Johnston, 1996). Most of the fish species observed during the Erupt cruises are commonly found in all Southern
ARTICLE IN PRESS H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
1845
Fig, 2. Deception Island, Antarctica, with Port Foster in the center. The pelagic and benthic trawl transect is located along the deepest portion of Port Foster running northwest to southeast.
Ocean sectors (Atlantic, Indian, and Pacific) (Gon and Heemstra, 1990; Miller, 1993). The inshore deep-water ecosystems (>30 m) (Kock, 1992), such as Port Foster and Admiralty Bay, have not been studied to the same extent as the more
typical inshore sublittoral and offshore slope and shelf systems. Our study describes the biology of fish populations observed in the study area, with a brief review of available background information.
ARTICLE IN PRESS 1846
H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
2. Methods During the five Erupt cruises in March and November 1999, and February, June, and November 2000 several methods were employed. Fishes were collected or observed using a multiple opening/closing net and environmental sampling system (MOCNESS), otter trawls, bottom camera sled based line-transect photography, and remotely operated vehicle (ROV) video. Fishes were identified using Gon and Heemstra (1990). When fishes were collected in sufficient number, diet, reproductive condition, prey selectivity, and parasite infestation were examined. The MOCNESS was used to sample pelagic fish fauna at 50-m depth intervals from 0 to 150 m depth once within 2 h of mid-day and once within 2 h of midnight on each of the five cruises with 30 tows total. All of the MOCNESS tows were conducted along the Pelagic and Benthic Trawl Transect (Fig. 2) in Port Foster. The nets had a 10-m2 opening and a 4-mm circular mesh with a 505-mm mesh cod end and were towed typically at 3.7 km h1. Fishes caught in the nets were sorted in the field and representative sub-samples were fixed in 10% formalin in seawater and returned to the lab. Otter trawls were deployed once per cruise along the Pelagic and Benthic Trawl Transect (Fig. 2) to sample the demersal fish fauna. Bottom trawls were kept to a minimum to avoid excessive habitat disturbance within Port Foster. One otter trawl was also deployed at Livingston Island in March 1999 and one at King George Island in November 2000 (Fig. 1), with seven trawls in total. The semi-balloon trawl had a 6.1-m opening and 3.8-cm stretch mesh net with 1.3-cm mesh cod-end liner and was towed behind a benthic sled (Wakefield and Smithey, 1989) at a speed of approximately 2.8 km h1 across the sea floor between 150 and 160 m depth. The specimens caught in the otter trawl were sorted in the field and representative sub-samples were fixed in 10% formalin in seawater and returned to the lab. These specimens were then identified and used, in part, as a voucher collection to identify species present in the line-transect photography.
Line-transect photography was conducted only along the Pelagic and Benthic Trawl Transect (Fig. 2) in Port Foster using a Benthos 372 camera and Benthos 382 strobe mounted to a benthic sled, at a height of 82 cm and 22.5 below horizontal (Wakefield and Smithey, 1989). These image data were evaluated using a Canadian grid system (Wakefield and Genin, 1987) and the computer program DISTANCE (Laake et al., 1994), which is based on line-transect theory (Buckland et al., 1993). The total abundance of demersal fishes (typically >1 cm in size) was calculated. DISTANCE estimates the visibility of an object at a distance perpendicular to the centerline of the transect and provides a probability density function and an effective strip width. Transect length was calculated using underway ship speed and location information combined with the time stamp on each photo frame (Cranmer et al., 2003). The effective strip width is then multiplied by the transect length in DISTANCE and an estimation of abundance with percent coefficient of variance and a 95% confidence interval are provided. For a more detailed description of linetransect photography methods, see Lauerman et al. (1996). A Deep Ocean Engineering Corporation Phantom DS-4 ROV was used with a Sanyo closed circuit TV camera to survey five benthic habitat areas within Port Foster in March 1999. Video transects were made from an altitude of approximately 0.5–1 m off the bottom. Video information was used to describe the habitats and fish behavior at Port Foster. Complications with the ROV tether and thrusters limited the ROV maneuverability and the structure of the transects. Samples returned to the lab were fixed in 10% formalin in seawater and subsequently preserved in 70% isopropyl alcohol. This process can dehydrate the samples and limits their comparability with samples processed before preservation in other studies. Fishes returned to the lab were weighed (total wet weight) (TW), and measured (standard length) (SL). For selected specimens the gonosomatic index (GSI) was computed (Kock, 1989), and gonad maturation stage (Kock and Kellermann, 1991) and stomach contents were examined. The number of food types (n), percent
ARTICLE IN PRESS H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
total number (%N), percent total weight (%W), and percent frequency of occurrence (%FO) were also determined for selected species. Cumulative prey curves were made to estimate the effectiveness of stomach gut content sampling. The mean number of prey taxa in successive stomachs was plotted with the number of stomachs examined as in Ferry (1997). The absolute importance index (AI), and relative importance index (RI) (George and Hadley, 1979), and index of relative importance (IRI) (Pinkas et al., 1971; Prince, 1975) were then computed using the following formulae: AI ¼ %FO þ %N þ %W;
RI ¼ 100AI=
n X
1847
T. scotti, and two specimens of T. bernacchii were identified. All parasites were put into 70% ethanol, then dehydrated in ethanol to 85% then 96% and cleared in beechwood creosote without staining. Parasite samples were examined with a stereomicroscope and identified to species or higher taxonomic category where necessary. Determinations of Digenea are based on descriptions in Zdzitowiecki (1997), Acanthocephala are based on Zdzitowiecki (1991), and larval Cestoda and Nematoda are based on references listed in Zdzitowiecki et al. (1998).
AI;
1
3. Results and discussion
IRI ¼ %FOð%N þ %WÞ: 3.1. Distribution and maturity The RI and IRI create a value of importance that reduces the individual biases of numerical or mass importance to create a comparable value. A detailed discussion of the assumptions and limitations of these indices can be found in Hyslop (1980). Each occurrence of fish eggs in a stomach was considered a single feeding event since notothenioids are known to lay benthic eggs in clusters (Kock and Kellermann, 1991). Selectivity in prey choice also was examined using the Ivlev Index of Electivity (E) (Ivlev, 1961). Prey abundances (p) were estimated from eight piston operated grab respirometer (POGR) samples from within Port Foster and were compared with the abundances found in the fish stomachs using E: E¼
%N p : %N þ p
It produces an index of selectivity that ranges from one to negative one indicating strong prey choice or prey avoidance, respectively. Detailed descriptions of the benthic infauna and methods for data collection are presented in Lovell and Trego (2003). The presence or absence of parasites in the body cavity was noted for C. gunnari, Lepidonotothen larseni, L. nudifrons, and Trematomus scotti, and two specimens of T. bernacchii. The body cavity and intestine parasites of six randomly selected specimens each of L. larseni, L. nudifrons, and
Eleven species of fishes were collected using the MOCNESS and otter trawl (Table 1). There were two species of Bathydraconidae: Gymnodraco acuticeps, Prionodraco evansii; two species of Channichthyidae: C. aceratus, C. gunnari; and seven species of Nototheniidae: G. gibberifrons, L. larseni, L. nudifrons, N. coriiceps, Pleuragramma antarcticum, T. bernacchii, and T. scotti. The species list should be considered partial for the study area because of the relatively small number of collections, especially at Livingston and King George Island. Only one G. acuticeps specimen (21.2 cm) was collected in Port Foster during these surveys. The adult G. acuticeps was collected in the otter trawl at 160 m water depth in June 2000. The benthic G. acuticeps is typically found at depths of less than 50 m and has been collected in all Southern Ocean sectors (Gon and Heemstra, 1990) to a depth of 663 m (Eastman and Hubold, 1999). Two adult P. evansii were collected in the otter trawl in Port Foster and one in the MOCNESS in the 100–150 m depth horizon all measuring approximately 15 cm. Though relatively rare, P. evansii is found in all Southern Ocean sectors at depths from 70 to 550 m (Gon and Heemstra, 1990). A recent Ross Sea survey collected individuals to 910 m (Eastman and Hubold, 1999). P. evansii has not been observed in previous recent surveys around Port Foster (Everson, 1987),
ARTICLE IN PRESS 1848
H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
Table 1 Table showing fish species collected, location, and method All identified species (family/species)
Bathydraconidae G. acuticeps P. evansii Channichthyidae C. aceratus C. gunnari Nototheniidae G. gibberifrons L. larseni L. nudifrons N. coriiceps P. antarcticum T. bernacchii T. scotti
Location (method) Port Foster (MOCNESS)
Port Foster (Otter Trawl)
X
X X
X X
X
X
X X X
Livingston Island (Otter Trawl)
Admiralty Bay (Otter Trawl)
X X
X X X
X X X
Admiralty Bay (Skora and Neyelov, 1992), or the entire region (Jones et al., 2001). One juvenile C. aceratus (8.3 cm) was caught in the 0–50 m MOCNESS net in Port Foster. C. aceratus have been observed to reach maturity at around 57.1 cm in females and 45.7 cm in males (Kock, 1989) and is typically found at 200–400 m depth (Kock and Jones, 2002) throughout the lower Atlantic Southern Ocean sector (Gon and Heemstra, 1990). C. aceratus was recently observed in Admiralty Bay (Skora and Neyelov, 1992), and in a survey of the entire region (Jones et al., 2001). Mostly juvenile C. gunnari were observed (Fig. 3a) in the MOCNESS samples from 0 to 150 m depth and few were collected in the otter trawl. Only one maturing female was found with developing gonads (stage three) at 21.3 cm. Spawning is known to occur from March to May in the Antarctic Peninsula region, with length at first spawning approximately 25 cm (Kock and Kellermann, 1991) and an age of 2.8–3 years (Kock and Everson, 1997). Three year-classes were identified during the November 2000 survey (Fig. 3a). No C. gunnari were observed outside Port Foster during the Erupt surveys. Common to the
X X X
X X
waters surrounding the Antarctic Peninsula and the lower Antarctic islands, C. gunnari has been collected at depths to 700 m (Gon and Heemstra, 1990). C. gunnari has been previously collected in Port Foster during nighttime net hauls (Everson, 1987) at depths of o80 m, as well as in surveys in nearby Admiralty Bay (Skora and Neyelov, 1992), at Elephant Island (61 S, 55 W) (Kock and Stransky, 2000), and the South Shetland Islands (Jones et al., 2001). C. gunnari was notably absent in a recent trawl survey of the Ross Sea (Eastman and Hubold, 1999). Although some stocks were estimated to be greatly reduced by fishing, it is still a relatively abundant species (Kock and Stransky, 2000). Five G. gibberifrons specimens were collected among all three survey locations in otter trawls. G. gibberifrons length at maturity was noted to be 36–38.6 cm in Kock (1989) and 33–36 cm in Jones et al. (2001). The specimens collected during the Erupt surveys all had lengths less than 33 cm (Fig. 3b) and were presumably juveniles. G. gibberifrons is an abundant species in the region, and it dominated the biomass of the fauna around Elephant Island during a recent survey (Kock and Stransky, 2000) and previous surveys of Admiralty Bay (Skora and Neyelov, 1992).
ARTICLE IN PRESS H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
1849
Fig. 3. Length (cm) vs. weight (g) for C. gunnari (a); G. gibberifrons (b); L. larseni (c); L. nudifrons (d); P. antarcticum (e); T. bernacchii (f); and T. scotti (g) for all Erupt cruises and locations. Note the three size classes seen in C. gunnari.
Additionally, G. gibberifrons was the second most abundant fish a recent survey of the South Shetland Islands (Jones et al., 2001). Many specimens of L. larseni were collected in Port Foster, Admiralty Bay, and off Livingston Island in benthic otter trawls during the Erupt survey. Length at first maturity stage four was found to be 9.9 cm during the Erupt surveys (Table 2) and has been previously observed to be 11–13 cm (Duhamel and Pletikosic, 1983). Adults and juveniles were caught during the Erupt study (Fig. 3c). L. larseni is found from 30 to 550 m
depth in the lower latitude Antarctic islands in all ocean sectors (Gon and Heemstra, 1990). It also was found in a recent survey of Elephant Island (Kock and Stransky, 2000) but was not observed at Admiralty Bay previously by Skora and Neyelov (1992). L. nudifrons was frequently caught in the deeper soft bottom areas in the otter trawl. Fewer were caught in the MOCNESS collections at 0–100 m depth. Large juveniles and adults were observed in Port Foster and Admiralty Bay during the Erupt surveys (Fig. 3d). Length at first maturity in the
ARTICLE IN PRESS H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
1850
Table 2 Mean female gonosomatic index (with sample number n) and length at first maturity (LFM) (stage four after Kock and Kellermann, 1991) for all Erupt locations Examined species
Collection date (month/year)
(family/species)
3/1999
L. larseni L. nudifrons T. scotti
0.036 (22) 0.108 (1)
11/1999
0.024 (8)
Antarctic Peninsula region is known to be 9–11 cm (Hourigan and Radtke, 1989; Jones et al., 2001), 13 cm at Elephant Island (Kock, 1989), and was observed at 9.5 cm at stage four in the Erupt study (Table 2). Males have been noted as having a lower average mass per unit length than females (Skora and Neyelov, 1992). The mass difference also was observed during the Erupt study, with the average male weighing 21.9 g and female weighing 26.4 g (n ¼ 45 and 36, respectively). Average lengths were similar at 11.0 and 11.7 cm, respectively. L. nudifrons has a limited known distribution from the lower Antarctic Peninsula to South Georgia at depths from 5 to 350 m (Gon and Heemstra, 1990). It has been collected recently throughout the South Shetland Islands (Skora and Neyelov, 1992; Kock and Stransky, 2000; Jones et al., 2001; Kamler et al., 2001). One adult of the common N. coriiceps (33.6 cm) was caught off Livingston Island in an otter trawl and was the only species observed solely outside Port Foster. N. coriiceps reaches maturity at roughly 34–35 cm (Everson, 1970; Kock, 1989) and is pelagic as a juvenile and demersal later in life. N. coriiceps is found in all Southern Ocean sectors and mid-upper Antarctic latitudes at 0–550 m depth, usually above 200 m (Gon and Heemstra, 1990) and has been observed in several recent surveys and collections in the region (Skora and Neyelov, 1992; Kock and Stransky, 2000; Jones et al., 2001; Kamler et al., 2001). The common and generally pelagic fish P. antarcticum was found only in Port Foster during the Erupt study and was caught throughout the water column and once in the otter trawl. Length at maturity was noted by Hubold (1985) to be 12.5 cm. The fifteen specimens collected in the
2/2000
6/2000
11/2000
LFM (cm)
0.036 (9)
0.111 (8) 0.123 (5)
0.003 (2) 0.019 (27) 0.022 (6)
9.9 9.5 9.0
Erupt study were juveniles, with the largest being 10.5 cm (Fig. 3e). One juvenile and three adult T. bernacchii were collected in otter trawls in Port Foster and one adult in Admiralty Bay during the Erupt study (Fig. 3f). Length at maturity has been reported by Hureau (1970) to be about 17 cm. Many adult and juvenile T. scotti were collected in otter trawls in Port Foster and Admiralty Bay (Fig. 3g). Few T. scotti were collected in the 100–150 m MOCNESS tows during the Erupt cruise series. Length at first maturity stage four was found to be 9 cm in the Erupt surveys (Table 2), the only reported maturation data for T. scotti to our knowledge. A peak in GSI occurred between June and November 2000, indicating that spawning occurred during that period. Larval hatching is known to occur typically in January (Gon and Heemstra, 1990), suggesting that the time of egg laying to hatching for T. scotti may be one or more months. P. antarcticum, T. bernacchii, and T. scotti have been found in all ocean sectors at depths from surface waters to 700 m or more in pelagic settings over the continental shelf (Gon and Heemstra, 1990) and in several recent surveys in the region (Skora and Neyelov, 1992; Eastman and Hubold, 1999; Kock and Stransky, 2000; Jones et al., 2001). 3.2. Abundance Demersal fish abundance estimates for March and November 1999, and June and November 2000 ranged from 0.05 to 0.10 fish m2 (Fig. 4). There was no clear temporal trend in demersal fish abundance within the observations made. Fishes observed in the photography showed little
ARTICLE IN PRESS H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
1851
0.12
6-Nov-99
Density (fish m-2)
0.1
5-Jun-00 0.08
28-Nov-00 0.06
4-Mar-99 0.04
0.02
0 1-Nov-98
9-Feb-99
20-May-99
28-Aug-99
6-Dec-99
15-Mar-00
23-Jun-00
1-Oct-00
9-Jan-01
Fig. 4. The abundance of fishes observed in line-transect photography at Port Foster during the Erupt cruises. The error bars indicate the 95% confidence interval of the abundance estimate.
indication of avoidance behaviors similar to findings of Ekau and Gutt (1991). The identification of fish to species in the photography was aided in part by the voucher collection provided by the otter trawl samples. Specimens collected in the otter trawl are considered representative of fish observed in the photography in terms of species composition. Identification to species was not consistently possible in all the photographs as in Ekau and Gutt (1991). Based on the line-transect photography and the otter trawl voucher collections, the abundance estimate for March 1999 includes primarily the notothenioids L. larseni, L. nudifrons, and T. scotti combined. Estimates from November 1999 and June 2000 are principally for T. scotti. The abundance estimate for November 2000 principally includes L. larseni, L. nudifrons, and T. scotti. The use of line-transect photography methods provides a good estimate of the demersal fish abundance and avoids some of the errors associated with estimates of effort in terms of exact bottom time and distance traversed in otter trawls, and provide some estimation of avoidance behavior. The use of line-transect photography in areas of greater water clarity could improve the species determination in the photographs. Ekau and Gutt
(1991) used still photography and video transecting methods and estimated total demersal fish abundance to be 0.08 and 0.06 fish m2, respectively, in the Weddell Sea. The estimates from the Weddell Sea, however, were over a much larger study area and depth range than was examined in Port Foster and used different methods to estimate the area surveyed. 3.3. Habitat Two generalized benthic habitats were observed, a deeper soft bottom and a shallower ophiuroidcovered benthos. Observed during four ROV video surveys and four photographic line transects, the deeper soft-bottom habitat made up the majority of the seafloor of Port Foster. Large rocks and boulders were also sparsely present. Dominant epibenthic megafaunal invertebrates observed in the video included large euphausiidlike crustaceans, brittlestars: Ophionotus victoriae, urchins: Sterechinus neumayeri, asteroids: Odontaster validus, and nemerteans: Parbolasia corrugatus, as well as numerous tunicates and sponges (Cranmer et al., 2003). The infauna was dominated by foraminifera, nematodes, and polychaetes (Lovell and Trego, 2003). Of the major taxa
ARTICLE IN PRESS 1852
H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
observed, only euphausiids and polychaetes were major prey items for notothenioids. Euphausiids are not readily apparent in the line-transect photography and may have been attracted to the constant ROV lighting. There are, however, many apparent euphausiids utilizing the benthos. Fishes observed frequently by the ROV in the softbottom locations included T. scotti and C. gunnari. Many appeared in small depressions in the soft bottom, with the fish often partially curled. One small shallow-water region, Stanley Patch (Fig. 2), was surveyed with the ROV. With a depth of approximately 20 m, Stanley Patch was different from the deeper soft bottom area in several ways. In addition to many of the fauna observed in the deeper areas, there was an abundance of smaller ophiuroids. At some points on Stanley Patch, the bottom was so completely covered by ophiuroids that the sediment was obscured. The abundances of urchins, nemerteans, asteroids, tunicates, sponges, and L. nudifrons were also relatively higher than in the deeper areas. Large swimming crustaceans were relatively less abundant. Fishes also were found among the sponges and tunicates as observed by Ekau and Gutt (1991). 3.4. Diet C. gunnari, L. larseni, L. nudifrons, and T. scotti were collected in sufficient numbers to examine their diet (Table 3). Cumulative prey curves (Fig. 5) illustrate that enough stomachs were sampled to describe the broad taxonomic prey groups. No curve was made for C. gunnari as there were only two principle prey items. There was no definitive trend in prey choice or %FO between sampling periods for those species examined. A brief review of known diet analyses for the remaining fishes is also presented to provide a more complete description of the importance of the fishes observed in the food web of the study area. The diet of the mostly juvenile C. gunnari observed in Port Foster consisted almost exclusively of Euphausia crystallorophias and E. superba. Other studies have shown that euphausiids generally make up 90–99% of C. gunnari prey items (Kock and Everson, 1997; Jones et al., 2001).
Euphausiids were abundant in the MOCNESS tows (Kaufmann et al., 2003) and euphausiid-like crustaceans were visible in the ROV video of the Port Foster benthos. The mostly juvenile specimens in previous surveys of Admiralty Bay had an approximately 50%FO of empty stomachs (Skora and Neyelov, 1992) compared with 17.5%FO in a recent NOAA survey (Jones et al., 2001), and 15%FO empty stomachs during the Erupt survey (Table 3). Euphausiids dominated the diet and prey choice for L. larseni in the Erupt collections. Other crustaceans such as amphipods and isopods, as well as polychaetes were also important prey items (Table 3). The bivalve Nuculana inaequisculpta and nematodes, also were identified as prey items. Bivalves and nematodes were strongly avoided in prey choice (Table 3) and may have been eaten incidentally with other benthic prey. Prey items observed in previous surveys are similar and consist principally of euphausiids, amphipods, mysids, calanoid copepods, and salps (Permitin and Tarverdiyeva, 1972; Target, 1981; Daniels, 1982; Gorelova and Shandikov, 1988; Jones et al., 2001). No empty stomachs were found in the L. larseni Erupt collections, which may indicate that feeding typically occurs before the stomach is emptied, as was observed by Gorelova and Shandikov (1988). The diet of L. nudifrons during the Erupt survey was dominated by euphausiids, with other crustaceans, and fish eggs also making up a portion of the diet (Table 3). Crustaceans such as amphipods and isopods may be a favored food item as indicated by the limited selectivity data (Table 3). L. nudifrons is generally known to eat benthic fauna such as polychaetes, amphipods, isopods, fish eggs, and euphausiids (Target, 1981; Daniels, 1982; Jones et al., 2001). Small specimens also feed on copepods and other zooplankton (Richardson, 1975). As with the closely related L. larseni, no empty stomachs were observed in L. nudifrons, again indicating that feeding may typically occur before full digestion of previously consumed food. The diversity of the major prey taxa was greater for T. scotti than the other fishes examined here. Polychaetes, euphausiids, and other crustaceans
ARTICLE IN PRESS H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
1853
Table 3 Results from the diet analysis of fishes from all Erupt cruises and locations showing percent frequency of occurrence (%FO), percent of total prey number (%N), percent of total prey weight (%W), absolute importance index (AI), the relative importance index (RI), index of relative importance (IRI), and the Ivlev Index of Electivity (E) Fish species Prey items
Diet indices %FO
%N
%W
AI
RI
IRI
C. gunnari (n ¼ 122) E. crystallorophias E. superba Unidentified euphausiids Other Empty stomachs
21 15 58 1 15
17 14 68 o1
26 39 35 {1
64 68 161 1
22 23 55 {1
903 795 5974 0
L. larseni (n ¼ 45) Euphausia sp. Other crustacea Polychaetea Bivalvia Nematoda Other (mostly sediment) Empty stomachs
40 22 9 2 4 71 0
40 42 12 2 4
43 2 1 {1 {1 54
123 66 22 4 8
53 28 10 2 3
3320 968 117 4 16
0.87 0.54 0.75 0.82
L. nudifrons (n ¼ 72) Euphausia sp. Other crustacea Polychaetea Bivalvia Gastrapoda Fish eggs Other (mostly sediment) Empty stomachs
45 18 4 7 7 8 42 0
54 29 6 3 3 5
69 4 o1 o1 o1 5 21
168 51 10.3 10.3 10.3 18
63 19 4 4 4 7
5535 594 24 21 21 80
0.81 0.74 0.65 1 1
T. scotti (n ¼ 72) Euphausia sp. Other crustacea Polychaetea Bivalvia Nematoda Priapulida Fish eggs Other (mostly sediment) Empty stomachs
22 25 29 44 20 6 10 10 12
7 4 52 33 3 o1 1
17 3 34 13 {1 10 11 12
46 32 115 90 22 16 22
13 9 33 26 7 5 6
528 175 2494 2024 60 60 120
dominated the diet, while bivalves, nematodes, and priapulids also made up significant portions of the diet (Table 3). T. scotti primarily fed on benthic polychaetes, euphausiids, amphipods, and isopods in previous studies as well (Target, 1981; Daniels, 1982; Pakhomov, 1997). Although Pakhomov (1997) found no empty stomachs, the Erupt study found a 21%FO for empty stomachs.
E
0.14 0.13 0.40 0.87
The diets of remaining fishes consist of both pelagic and benthic prey. G. acuticeps is piscivorous as an adult, eating P. antarcticum, myctophids, and other fishes, as well as fish eggs, amphipods, and polychaetes (Takahashi, 1983; Eastman, 1985; Pakhomov, 1997). P. evansii has been shown to feed on benthic polychaetes, crustaceans, and amphipods (Kock et al., 1984). C. aceratus is
ARTICLE IN PRESS H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
1854 7
L. larseni
No. prey taxa
6 5 4 3 2 1 0
10
20
30
40
50
No. stomachs analyzed 8
L. nudifrons
7
No. prey taxa
6 5 4 3 2 1 0 0
20
40
60
80
No. stomachs analyzed 9
T. scotti
8
No. prey taxa
7 6 5
known to migrate vertically as juveniles feed on pelagic invertebrates (Kock and Jones, 2002). They then become more sedentary and piscivorous with age and are ambush feeders by a length of 30 cm (Jones et al., 2001). The benthic G. gibberifrons has been observed to ambush feed from rock perches and soft mud sediments (Daniels, 1982). G. gibberifrons also has been noted to feed in part on errant and sedentary polychaetes, amphipods, ophiuroids, and pycnogonids in the Antarctic Peninsula region (Daniels, 1982; Jones et al., 2001). N. coriiceps has been observed as a benthic ambush predator, often consuming large prey items with occasional watercolumn feeding, as well as grazing of fish, isopods, amphipods, and mollusks (Blankley, 1982; Daniels, 1982; Burchett et al., 1983; Pakhomov, 1997; Jones et al., 2001). N. coriiceps also has been observed feeding selectively on macroalgae as adults (Daniels, 1982; Iken et al., 1997). P. antarcticum has been noted to feed in the water column on euphausiids, cumaceans, and copepods (Daniels, 1982; Pakhomov, 1997). Typically described as a benthic browser and ambush feeder, T. bernacchii has been noted to feed on amphipods, polychaetes, isopods, and macroalgae with an increasing diversity of prey with growth (Daniels, 1982; Kiest, 1993). Vacchi et al. (1994) observed that bivalves and euphausiids were also important prey items. Animals known to feed on fish in the region include other fishes, squid, cetaceans, seabirds, and pinnipeds (Kock, 1992). Several of the seabirds and pinnipeds observed at Deception Island are known to feed on notothenioid fishes and compete for euphausiids as a major prey item (Kendall et al., 2003).
4
3.5. Parasites
3 2 1 0
20
40
60
80
No. stomachs analyzed Fig. 5. Cumulative prey curves for L. larseni, L. nudifrons, and T. scotti illustrating the asymptotic relationship between the number of stomachs analyzed and the number of prey taxa observed. The error bars represent one standard error.
Body cavity and alimentary tract parasites are frequently observed in notothenioids (Palm et al., 1994; Zdzitowiecki et al., 1998; Zdzitowiecki, 2001, 2002a, 2002b) and are thought to adversely affect fishes in a variety ways (Barber et al., 2000). Pelagic feeding fishes such as juvenile C. gunnari typically have low infestation frequencies and endoparasite diversity (Hoogesteger and White,
ARTICLE IN PRESS H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
1855
In L. larseni, all specimens above 11 cm had a frequency of occurrence of 100% (n ¼ 38=38) of body cavity parasites and specimens smaller than 11 cm had an occurrence of 56% (n ¼ 9=16). With age, L. larseni changes from a pelagic to a benthic habitat (Gorelova and Shandikov, 1988; Kellermann, 1989), which is another indication that these parasites are likely residing in the benthos and benthic prey items and infect fish as they begin benthic feeding. L. larseni had a higher diversity of parasites than the others examined with nine or more species recorded (Table 4). The common nematode Pseudoterranova decipiens was the most abundant of the parasites identified in L. larseni. The body cavity parasite infestation for L. nudifrons was lower (22%) than the other nototheniids examined here. L. nudifrons had similar occurrence of infestation in both juveniles and adults. The two T. bernacchii specimens examined for parasites had at least eight species of parasites in the body cavity and lumen of the intestine (Table 4). Four species of parasites were identified in six specimens of T. scotti with the common P. decipiens being dominant (Table 4). Body cavity parasites were present in all examined specimens
1981; Kock and Everson, 1997; Zdzitowiecki, 2002a). In support of these studies no body cavity parasites were observed in the 133 mostly juvenile C. gunnari specimens dissected from the Erupt surveys. Mid-stage nematode parasite worms are not known to occur in euphausiids (Kagei et al., 1978). The C. gunnari diet of nearly exclusively euphausiids may preclude heavy infestation and subsequent fitness burdens (Kock, 1992). Previous work has shown channichthyid fishes have a higher diversity of digenea in areas with larger accessible benthic habitats such as the South Shetland Islands than the relatively open waters of the Weddell Sea (Zdzitowiecki, 2002b). The benthic feeding L. larseni, L. nudifrons, T. bernacchii, and T. scotti were commonly infested with body-cavity parasites with a frequency of occurrence of 87% (n ¼ 47=54), 22% (n ¼ 17=81), 40% (n ¼ 2=5), and 100% (n ¼ 210=210), respectively. L. larseni, L. nudifrons, T. bernacchii, and T. scotti, for which body-cavity and intestine parasites were identified (Table 4), all had infestations of multiple species of parasites known to be abundant in fishes in the shallow waters of western Antarctica (K. Zdzitowiecki, personal communication).
Table 4 List of observed parasite species for randomly selected fishes from all Erupt cruises and locations. The mean number of parasites observed for each type are noted. Metacanthocephalus sp. is likely to be one or all of M. dalmori, M. johnstoni, and M. campbelli Parasites Larval Cestoda Tetraphyllidean cercoid bilocular Diphyllobothriid plerocercoid Digenea Macvicaria georgiana Neolebouria antarctica juv. Lepidapedon garrardi Larval Nematoda Contracaecum spp. P. decipiens Acanthocephala adults Aspersentis megarhynchus Metacanthocephalus spp. Acanthocephala cystacanths Corynosoma hamanni C. pseudohamanni C. arctocephali.
Tissue type
L. larseni n¼6
Intestine Body cavity
0.5 2.0
Intestine Intestine Intestine
4.7 0.2 1.0
Body cavity Body cavity
7.3
13.2 2.7
Intestine Intestine
0.3
11.7
0.5 1.5
0.3 0.3
1.7 4.0 2.2
1.5 13.0 4.0
Body cavity Body cavity Body cavity
L. nudifrons n¼6
3.8
T. bernacchii n¼2 1.0 2.5
1.5
T. scotti n¼6
0.2
4.8 8.0
0.2
ARTICLE IN PRESS 1856
H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
from Port Foster, implying heavy parasite infestation. However, no juvenile T. scotti were sampled for parasites. Decreased benthic habitat scour from large icebergs may allow parasites with benthic life stages to persist and become more abundant than in areas with more frequent scouring. A tissue analysis found that there was no consistent increase in heavy metals in the nematode parasites of T. scotti when compared to other tissues including muscle, liver, and gills (D. Deheyn, personal communication). These nematodes then are not likely to play a role in metal detoxification for the fish and probably do not act as a bioaccumulator of heavy metals at this stage in the parasites’ life cycle (D. Deheyn, personal communication).
4. Summary Fishes surveyed during the Erupt study of Port Foster, Deception Island and vicinity are known to occur in the region and have diets similar to those found in previous studies. Fishes within Port Foster are predators of invertebrates and small fishes and are likely prey items for the seabirds and pinnipeds observed around the shores of Port Foster. The unique habitat of Port Foster may provide refuge for juveniles of some species such as C. gunnari, which were frequently observed there. Limited exchange with the surrounding waters also may limit the influence of recruitment and prey abundance fluctuations outside Port Foster. T. scotti had heavy body cavity parasite infestation from Port Foster, possibly due in part to decreased benthic scour from large icebergs. Not recorded in many recent surveys of the region, P. evansii was notably observed in Port Foster. The overall abundances of fishes observed in Port Foster show maximum in November 1999 and range from 0.05 to 0.10 fish m2, similar to those found over a larger region and depth range in the Weddell Sea. The 1.5-year time-series did not reveal any clear pattern in abundance. The use of line-transect photography combined with otter trawl collections can be useful in determining the abundance of demersal notothenioid fishes in areas where water clarity is sufficient. Further
multi-year and diel time-series investigations, which include diet studies, estimations of digestion time, and fecundity information would help to better describe population dynamics and feeding habits of Antarctic fishes.
Acknowledgements We would like to thank K.L. Smith Jr. for initiating and coordinating the Erupt series; H.J. Walker, C. Klepadlo, L.L. Lovell, A.W. Townsend, K.D. Trego, and the Scripps Institution of Oceanography vertebrate and invertebrate collections for aid in fish and prey item identifications; J.C. Drazen and three anonymous reviewers for their helpful insights and suggestions; the science parties and crews of the R.V. L.M. Gould during the Erupt cruise series. This research was funded by the US National Science Foundation grant OPP-97-27077 to K.L. Smith.
References Barber, I., Hoare, D., Krause, J., 2000. Effects of parasites on fish behavior: a review and evolutionary perspective. Reviews in Fish Biology and Fisheries 10, 131–165. Blankley, W.O., 1982. Feeding ecology of the three inshore fish species at Marion Island (Southern Ocean). South African Journal of Zoology 17, 164–170. Brenner, M., Buck, B.H., Cordes, S., Dietrich, L., Jacob, U., . Mintenbeck, K., Schroder, A., Brey, T., Knust, R., Arntz, W., 2001. The role of iceberg scours in niche separation within the Antarctic fish genus Trematomus. Polar Biology 24, 502–507. Buckland, S.T., Anderson, D.R., Burnham, K.P., Laake, J.L., 1993. Distance Sampling: Estimating Abundance of Biological Populations. Chapman & Hall, London, 446pp. Burchett, M.S., Sayers, P.J., North, A.W., White, M.G., 1983. Some biological aspects of the nearshore fish populations as South Georgia. British Antarctic Survey Bulletin 59, 63–74. Clarke, A., Johnston, I.A., 1996. Evolution and adaptive radiation of Antarctic fishes. Trends in Ecology and Evolution 11, 212–218. Cranmer, T., Ruhl, H.A., Kaufmann, R.S., Baldwin, R.J., 2003. Spatial and temporal variation in the abundance, distribution and population structure of epibenthic megafauna in Port Foster, Deception Island. Deep-Sea Research II, this issue (doi: 10.1016/S0967-0645(03)00093-6).
ARTICLE IN PRESS H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858 Daniels, R.A., 1982. Feeding ecology of some fishes of the Antarctic Peninsula. Fishery Bulletin, United States Department of Commerce 80, 575–588. Duhamel, G., Pletikosic, M., 1983. Donnes biologiques sur les Nototheniidae les Nototheniidae des #ıles Crozet. Cybium 7, 43–57. Eastman, J.T., 1985. Pleuragramma antarcticum (Picies, Nototheniidae) as food for other fishes in McMurdo Sound, Antarctica. Polar Biology 4, 155–160. Eastman, J.T., 1990. The biology and physiological ecology of notothenioid fishes. In: Gon, O., Heemstra, P.C. (Eds.), Fishes of the Southern Ocean. J. L. B. Smith Institute of Ichthyology, Grahamstown, South Africa, pp. 34–51. Eastman, J.T., Clarke, A., 1998. A comparison of adaptive radiations of Antarctic fish with those of non-Antarctic Fish. In: di Prisco, G., Pisano, E., Clarke, A. (Eds.), Fishes of Antarctica. Springer, Milano, Italia, pp. 5–26. Eastman, J.T., Hubold, G., 1999. The fish fauna of the Ross Sea, Antarctica. Antarctic Science 11, 293–304. Ekau, W., Gutt, J., 1991. Notothenioid fishes from the Weddell Sea and their habitat, observed by underwater photography and television. Proc. NIPR Symp. Polar Biology 4, 36–49. Everson, I., 1970. Reproduction in Notothenia neglecta Nybelin. British Antarctic Survey Bulletin 23, 81–92. Everson, I., 1987. Some aspects of the small scale distribution of Euphausia crystallorophias. Polar Biology 8, 9–15. Ferry, L.A., 1997. Food habits of the two-line eelpout (Bothrocara brunneum, Zoarchidae) at two deep-sea sites in the eastern North Pacific. Deep-Sea Research I 44, 521–531. George, E.L., Hadley, W.F., 1979. Food and habitat partitioning between rock bass (Amploplites rupestris) and smallmouth bass (Micropterus dolomieui) young of the year. Transactions of the American Fisheries Society 108, 253–261. Gon, O., Heemstra, P.C., 1990. Fishes of the Southern Ocean. J. L. B. Smith Institute of Ichthyology, Grahamstown, South Africa, 462pp. Gorelova, T.A., Shandikov, G.A., 1988. Age-related changes in the composition of the food and daily feeding rhythm of Nototheniops tchizh tchizh in the Lena Bank region (Indian Ocean sector of the Southern Ocean). Journal of Ichthyology 28, 86–92. Hoogesteger, J.N., White, M.G., 1981. Notes on the parasite infestation of inshore fish at Signy Island, South Orkney Islands. British Antarctic Survey Bulletin 54, 23–31. Hourigan, T.J., Radtke, R.L., 1989. Reproduction of the Antarctic fish Nototheniops nudifrons. Marine Biology 100, 277–283. Hubold, K.G., 1985. Stomach contents of the Antarctic silverfish Pleuragramma antarcticum from the southern and eastern Weddell Sea (Antarctica). Polar Biology 5, 43–48. Hureau, J.C., 1970. Biologie compar!ee de quelques poissons antarctiques (Nototheniidae). Bulletin de l’Institut Oce! anography, Monaco 68, 1–250.
1857
Hyslop, E.J., 1980. Stomach contents analysis—a review of methods and their application. Journal of Fish Biology 17, 411–429. Iken, K., Barrera-Oro, E.R., Quartino, M.L., Casaux, R.J., Brey, T., 1997. Grazing by the Antarctic fish Notothenia coriiceps, evidence for selective feeding on macroalgae. Antarctic Science 9, 386–391. Ivlev, V.S., 1961. Experimental ecology of the feeding of fishes. Yale University Press, New Haven, 302pp. Jones, C.D., Kock, K.-H., Wilhems, S., Ramm, D., Ashford, J., Near, T., Emery, J.H., Gong, N., Flores, H., Banks, A.R., Prowse, M., 2001. Bottom trawl survey and finfish research in the South Shetland Islands, In: Lipsky, J. (Ed.), AMLR 2000/2001 Field Season Report, NOAA-TM-NMFSSWFSC-314. Kagei, N., Asano, K., Kihata, M., 1978. On the examination against parasites of Antarctic krill, Euphausia superba. Scientific Reports of the Whales Research Institute, Tokyo 30, 311–313. Kamler, E., Krasicka, B., Rakusa-Suszczewski, S., 2001. Comparison of lipid content and fatty acid composition in muscle and liver of two notothenioid fishes from Admiralty Bay (Antarctica), an eco-physiological perspective. Polar Biology 24, 735–743. Kaufmann, R.S., Fisher, E.C., Gill, W.H., King, A.L., Laubacher, M., Sullivan, B., 2003. Temporal patterns in the distribution, biomass and community structure of macrozooplankton and micronekton within Port Foster, Deception Island, Antarctica. Deep-Sea Research II, this issue (doi: 10.1016/S0967-0645(03)00092-4). Kellermann, A., 1989. The larval fish community in the zone of seasonal pack-ice cover and it’s seasonal and interanual variability. Archiv Fuer Fischereiwissenschaft. 39 (Suppl. 1), 81–110. Kendall, K, Ruhl, H.A., Wilson, R.C., 2003. Distribution and abundance of marine bird and pinniped populations within Port Foster, Deception Island, Antarctica. Deep-Sea Research II, this issue (doi: 10.1016/S0967-0645(03)00096-1). Kiest, K.A., 1993. A relationship of diet to prey abundance and the foraging behavior of Trematomous bernacchii. Polar Biology 13, 291–296. Kock, K.-H., 1989. Reproduction in fish around . Fischereiwissenschaft 39, Elephant Island. Archive fur 171–210. Kock, K.-H., 1992. Antarctic Fish and Fisheries. Cambridge University Press, Cambridge, 359pp. Kock, K.-H., Everson, I., 1997. Biology and ecology of mackerel icefish, Champsocephalus gunnari, an Antarctic fish lacking hemoglobin. Comparative Biochemistry and Physiology 118A, 1067–1077. Kock, K.-H., Jones, C.D., 2002. The biology of the icefish Cryodraco antarcticus dollo, 1990 (pisces, channichthyidae) in the southern Scotia Arc (Antarctica). Polar Biology 25, 416–424. Kock, K.-H., Kellermann, A., 1991. Reproduction in Antarctic notothenioid fishes—a review. Antarctic Science 3, 125–150.
ARTICLE IN PRESS 1858
H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
Kock, K.-H., Stransky, C., 2000. The composition of the coastal fish fauna around Elephant Island (South Shetland Islands, Antarctica). Polar Biology 23, 825–832. Kock, K.-H., Schneppenheim, R., Siegel, V., 1984. A contribution to the fish fauna of the Weddell Sea. Archive fur . Fischereiwissenschaft 34, 103–120. Laake, J.L., Buckland, S.T., Anderson, D.R., Burnham, K.P., 1994. Distance users guide V 2.1. Colorado Cooperative Fish and Wildlife Research Unit, Colorado State University, Fort Collins, CO, 84pp. Lauerman, L.M.L., Kaufmann, R.S., Smith Jr., K.L., 1996. Distribution and abundance of epibenthic megafauna at a long time-series station in the abyssal northeast Pacific. Deep-Sea Research I 43, 1075–1104. Lovell, L., Trego, K., 2003. The epibenthic megafaunal and benthic infaunal invertebrates of Port Foster, Deception Island (South Shetland Islands, Antarctica). Deep-Sea Research II, this issue (doi: 10.1016/S0967-0645(03)00087-0). Miller, R.G., 1993. History and Atlas of the Fishes of the Antarctic Ocean. Foresta Institute, Carson City, NV, 792pp. Pakhomov, E.A., 1997. Feeding and exploitation of the food supply by demersal fishes in the Antarctic part of the Indian Ocean. Journal of Ichthyology 37, 360–380. Palm, H., Anderson, K., Kl.oser, H., Pl.otz, J., 1994. Occurrence of Pseudoterranova decipiens (Nematoda) in fish from the southeastern Weddell Sea (Antarctic). Polar Biology 14, 539–544. Permitin, Y.Y., Tarverdiyeva, M.I., 1972. The food of some Antarctic fish in the South Georgia area. Journal of Ichthyology 12, 104–114. Pinkas, L., Oliphant, M.S., Iverson, I.L.K., 1971. Food habits of albacore, bluefin tuna, and bonito in California waters. California Department of Fish and Game, Fish Bulletin 152, 1–105. Prince, E.D., 1975. Pinnixid crabs in the diet of young-of-theyear copper rockfish (Sebastes caurinus). Transactions of the American Fisheries Society 99, 440–443. Richardson, M.G., 1975. The dietary composition of some Antarctic fish. British Antarctic Bulletin 41/42, 113–120. Skora, K.E., Neyelov, A.V., 1992. Fish of Admiralty Bay (King George Island, South Shetland Islands, Antarctica). Polar Biology 12, 476–496.
Smith Jr., K.L., Baldwin, R.J., Kaufmann, R.S., Sturz, A., 2003. Ecosystem studies at Deception Island, Antarctica, an overview. Deep-Sea Research II, this issue (doi: 10.1016/ S0967-0645(03)00081-X). Takahashi, M., 1983. Trophic ecology of demersal fish communities north of South Shetland Islands, with notes on the ecological role of krill. Memoirs of the National Institute of Polar Research 27, 183–192. Target, T.E., 1981. Trophic ecology and structure of coastal Antarctic fish communities. Marine Ecology Progress Series 4, 243–263. Vacchi, M., La Mesa, M., Castelli, A., 1994. Diet of two coastal nototheniid fish from Terra Nova Bay, Ross Sea. Antarctic Science 6, 61–65. Wakefield, W.W., Genin, A., 1987. The use of a Canadian (perspective) grid in deep-sea photography. Deep-Sea Research I 34, 469–478. Wakefield, W.W., Smithey, W., 1989. Two camera sleds for quantitative study of deep-sea megafauna. Scripps Institution of Oceanography Reference Series 89-14, 25pp. Zdzitowiecki, K., 1991. Antarctic Acanthocephala, parasites of fishes. In: W.agele, J.W., Sieg, J. (Eds.), Synopses of the Antarctic Benthos, Vol. 3. Koeltz Scientific Books, . Koenigstein, Germany. Zdzitowiecki, K., 1997. Antarctic Digenea, parasites of fishes. In: W.agele, J.W., Sieg, J. (Eds.), Synopses of the Antarctic . Benthos, Vol. 8. Koeltz Scientific Books, Koenigstein, Germany. Zdzitowiecki, K., 2001. New data on the occurrence of fish endoparasitic worms off Adelie Land, Antarctica. Polish Polar Research 22, 159–165. Zdzitowiecki, K., 2002a. Occurrence of Digenea in fishes of the family Nototheniidae in the Weddell Sea. Acta Parasitologica 47, 154–158. Zdzitowiecki, K., 2002b. Occurrence of Digenea in fishes of the family Channichthyidae in the Weddell Sea and other subcontinental areas of the Antarctic. Acta Parasitologica 47, 159–162. Zdzitowiecki, K., Rocka, A., Pisano, E., Ozouf-Costaz, C., 1998. A list of fish parasitic worms collected off Adelie Land (Antarctic). Acta Parasitologica 43, 71–74.
Deep-Sea Research II 50 (2003) 1843–1858
Fish populations of Port Foster, Deception Island, Antarctica and vicinity Henry A. Ruhla,*, Philip A. Hastingsa, Lisa A. Zarubicka, Rachelle M. Jensena, Krzysztof Zdzitowieckib a
Marine Biology Research Division, 0202, Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA 92093-0202, USA b Institute of Parasitology, Polish Academy of Sciences, Twarda 51/55, Warszawa 00-818, Poland Received 16 September 2002; received in revised form 20 December 2002; accepted 6 January 2003
Abstract The fish populations of Port Foster, Deception Island, South Shetland Islands, Antarctica, were investigated as part of the Erupt Antarctic ecosystem study. Surveys were conducted on five cruises between March 1999 and November 2000. Samples also were collected off Livingston Island and King George Island of the South Shetland Islands. Specimens were collected or observed using a multiple opening and closing net and environmental sampling system, otter trawls, benthic line-transect photography, and remotely operated vehicle video. Species composition, length, weight, reproductive condition, diet, habitat, and parasitic infestation were examined for the dominant fish species. Eleven species were collected, all in the suborder Notothenioidei. The fishes found in the survey are known to occur in the region and had diets similar to those found in other studies. Abundances of demersal fishes in Port Foster ranged from 0.05 to 0.10 individuals m2 over the study period. Inshore shallow-water (o30 m) and inshore deep-water (>30 m) habitats are identified in Port Foster and described. Port Foster may be a refuge for juvenile fishes such as Champsocephalus gunnari. Limited exchange with the surrounding waters also may limit the influence of recruitment and prey abundance fluctuations outside Port Foster. Trematomus scotti had heavy body cavity parasite infestation from Port Foster, possibly due in part to decreased benthic scour from large icebergs, allowing benthic parasites to persist. r 2003 Elsevier Ltd. All rights reserved.
1. Introduction The fishes of Port Foster, Deception Island, Antarctica, and vicinity were investigated as part of the Erupt Antarctic ecosystem study. Fishes were collected on five cruises in March and November 1999, and February, June, and No*Corresponding author. Tel.: +1-858-534-4858; fax: +1858-534-7313. E-mail address: [email protected] (H.A. Ruhl).
vember 2000. While many fish surveys have been conducted in the region, relatively little is known about the fish populations of inshore deep-water habitats such as Port Foster. Notothenioid fishes were the only fishes noted during the Erupt survey. Deception Island is located at the southwest end of the South Shetland Islands (Fig. 1) in a region of seasonal pack-ice coverage. It is a flooded volcanic caldera, which creates an almost entirely enclosed body of water with only a narrow shallow connection to the Bransfield Strait and
0967-0645/03/$ - see front matter r 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0967-0645(03)00094-8
ARTICLE IN PRESS 1844
H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
Fig. 1. Chart of the South Shetland Islands, Antarctica. The black box indicates Deception Island represented in Fig. 2. The black dots indicate the location of otter trawl surveys conducted off Livingston and King George Islands.
surrounding waters (Fig. 2). The connection is 550 m wide at the narrowest point and has a depth of 11 m. The protected embayment within the caldera, Port Foster, is 9.8 km long 5.7 km wide. The sheltered nature of Port Foster also limits the routinely intense wave energy of the Southern Ocean, benthic habitat scour due to large drifting icebergs, and the flow of seasonal pack ice. Habitat destruction due to the calving and movement of large icebergs has been shown to cause niche separation in some notothenioid fishes (Brenner et al., 2001). Port Foster is thus likely to have a less variable benthic habitat and epipelagic habitat than more exposed communities in the region. However, the caldera is subject to active volcanic and seismic activity. For a full description of Port Foster, Deception Island, and the Erupt program see Smith et al. (2003). Livingston Island is located north of Deception, and King George Island is located further to the northeast along the South Shetland Island chain (Fig. 1). Fishes of the suborder Notothenioidei dominate the diversity and biomass of the demersal fishes
found in the Southern Ocean (Gon and Heemstra, 1990; Miller, 1993). Of the approximately 260 fish species known to occur in the Southern Ocean, nearly half are in the suborder Notothenioidei and represent roughly 90% of all individuals collected in shelf and slope waters (Eastman and Clarke, 1998). Some commercially important species in the South Shetland Islands include Champsocephalus gunnari, Chaenocephalus aceratus, Notothenia rossii, and Gobionotothen gibberifrons (=Notothenia gibberifrons) (Kock, 1992; Jones et al., 2001). The fishery for these species was closed in the region in 1989/1990 (Jones et al., 2001) due to overfishing. Numerous phylogenetic, ecological, physiological, and biochemical studies have examined several characteristics unique to notothenioid fishes, such as the reduction or lack of hemoglobin and swim bladders, production of glycopeptide antifreeze, and greatest species richness at 300–600 m (Eastman, 1990; Miller, 1993; Kock, 1992; Clarke and Johnston, 1996). Most of the fish species observed during the Erupt cruises are commonly found in all Southern
ARTICLE IN PRESS H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
1845
Fig, 2. Deception Island, Antarctica, with Port Foster in the center. The pelagic and benthic trawl transect is located along the deepest portion of Port Foster running northwest to southeast.
Ocean sectors (Atlantic, Indian, and Pacific) (Gon and Heemstra, 1990; Miller, 1993). The inshore deep-water ecosystems (>30 m) (Kock, 1992), such as Port Foster and Admiralty Bay, have not been studied to the same extent as the more
typical inshore sublittoral and offshore slope and shelf systems. Our study describes the biology of fish populations observed in the study area, with a brief review of available background information.
ARTICLE IN PRESS 1846
H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
2. Methods During the five Erupt cruises in March and November 1999, and February, June, and November 2000 several methods were employed. Fishes were collected or observed using a multiple opening/closing net and environmental sampling system (MOCNESS), otter trawls, bottom camera sled based line-transect photography, and remotely operated vehicle (ROV) video. Fishes were identified using Gon and Heemstra (1990). When fishes were collected in sufficient number, diet, reproductive condition, prey selectivity, and parasite infestation were examined. The MOCNESS was used to sample pelagic fish fauna at 50-m depth intervals from 0 to 150 m depth once within 2 h of mid-day and once within 2 h of midnight on each of the five cruises with 30 tows total. All of the MOCNESS tows were conducted along the Pelagic and Benthic Trawl Transect (Fig. 2) in Port Foster. The nets had a 10-m2 opening and a 4-mm circular mesh with a 505-mm mesh cod end and were towed typically at 3.7 km h1. Fishes caught in the nets were sorted in the field and representative sub-samples were fixed in 10% formalin in seawater and returned to the lab. Otter trawls were deployed once per cruise along the Pelagic and Benthic Trawl Transect (Fig. 2) to sample the demersal fish fauna. Bottom trawls were kept to a minimum to avoid excessive habitat disturbance within Port Foster. One otter trawl was also deployed at Livingston Island in March 1999 and one at King George Island in November 2000 (Fig. 1), with seven trawls in total. The semi-balloon trawl had a 6.1-m opening and 3.8-cm stretch mesh net with 1.3-cm mesh cod-end liner and was towed behind a benthic sled (Wakefield and Smithey, 1989) at a speed of approximately 2.8 km h1 across the sea floor between 150 and 160 m depth. The specimens caught in the otter trawl were sorted in the field and representative sub-samples were fixed in 10% formalin in seawater and returned to the lab. These specimens were then identified and used, in part, as a voucher collection to identify species present in the line-transect photography.
Line-transect photography was conducted only along the Pelagic and Benthic Trawl Transect (Fig. 2) in Port Foster using a Benthos 372 camera and Benthos 382 strobe mounted to a benthic sled, at a height of 82 cm and 22.5 below horizontal (Wakefield and Smithey, 1989). These image data were evaluated using a Canadian grid system (Wakefield and Genin, 1987) and the computer program DISTANCE (Laake et al., 1994), which is based on line-transect theory (Buckland et al., 1993). The total abundance of demersal fishes (typically >1 cm in size) was calculated. DISTANCE estimates the visibility of an object at a distance perpendicular to the centerline of the transect and provides a probability density function and an effective strip width. Transect length was calculated using underway ship speed and location information combined with the time stamp on each photo frame (Cranmer et al., 2003). The effective strip width is then multiplied by the transect length in DISTANCE and an estimation of abundance with percent coefficient of variance and a 95% confidence interval are provided. For a more detailed description of linetransect photography methods, see Lauerman et al. (1996). A Deep Ocean Engineering Corporation Phantom DS-4 ROV was used with a Sanyo closed circuit TV camera to survey five benthic habitat areas within Port Foster in March 1999. Video transects were made from an altitude of approximately 0.5–1 m off the bottom. Video information was used to describe the habitats and fish behavior at Port Foster. Complications with the ROV tether and thrusters limited the ROV maneuverability and the structure of the transects. Samples returned to the lab were fixed in 10% formalin in seawater and subsequently preserved in 70% isopropyl alcohol. This process can dehydrate the samples and limits their comparability with samples processed before preservation in other studies. Fishes returned to the lab were weighed (total wet weight) (TW), and measured (standard length) (SL). For selected specimens the gonosomatic index (GSI) was computed (Kock, 1989), and gonad maturation stage (Kock and Kellermann, 1991) and stomach contents were examined. The number of food types (n), percent
ARTICLE IN PRESS H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
total number (%N), percent total weight (%W), and percent frequency of occurrence (%FO) were also determined for selected species. Cumulative prey curves were made to estimate the effectiveness of stomach gut content sampling. The mean number of prey taxa in successive stomachs was plotted with the number of stomachs examined as in Ferry (1997). The absolute importance index (AI), and relative importance index (RI) (George and Hadley, 1979), and index of relative importance (IRI) (Pinkas et al., 1971; Prince, 1975) were then computed using the following formulae: AI ¼ %FO þ %N þ %W;
RI ¼ 100AI=
n X
1847
T. scotti, and two specimens of T. bernacchii were identified. All parasites were put into 70% ethanol, then dehydrated in ethanol to 85% then 96% and cleared in beechwood creosote without staining. Parasite samples were examined with a stereomicroscope and identified to species or higher taxonomic category where necessary. Determinations of Digenea are based on descriptions in Zdzitowiecki (1997), Acanthocephala are based on Zdzitowiecki (1991), and larval Cestoda and Nematoda are based on references listed in Zdzitowiecki et al. (1998).
AI;
1
3. Results and discussion
IRI ¼ %FOð%N þ %WÞ: 3.1. Distribution and maturity The RI and IRI create a value of importance that reduces the individual biases of numerical or mass importance to create a comparable value. A detailed discussion of the assumptions and limitations of these indices can be found in Hyslop (1980). Each occurrence of fish eggs in a stomach was considered a single feeding event since notothenioids are known to lay benthic eggs in clusters (Kock and Kellermann, 1991). Selectivity in prey choice also was examined using the Ivlev Index of Electivity (E) (Ivlev, 1961). Prey abundances (p) were estimated from eight piston operated grab respirometer (POGR) samples from within Port Foster and were compared with the abundances found in the fish stomachs using E: E¼
%N p : %N þ p
It produces an index of selectivity that ranges from one to negative one indicating strong prey choice or prey avoidance, respectively. Detailed descriptions of the benthic infauna and methods for data collection are presented in Lovell and Trego (2003). The presence or absence of parasites in the body cavity was noted for C. gunnari, Lepidonotothen larseni, L. nudifrons, and Trematomus scotti, and two specimens of T. bernacchii. The body cavity and intestine parasites of six randomly selected specimens each of L. larseni, L. nudifrons, and
Eleven species of fishes were collected using the MOCNESS and otter trawl (Table 1). There were two species of Bathydraconidae: Gymnodraco acuticeps, Prionodraco evansii; two species of Channichthyidae: C. aceratus, C. gunnari; and seven species of Nototheniidae: G. gibberifrons, L. larseni, L. nudifrons, N. coriiceps, Pleuragramma antarcticum, T. bernacchii, and T. scotti. The species list should be considered partial for the study area because of the relatively small number of collections, especially at Livingston and King George Island. Only one G. acuticeps specimen (21.2 cm) was collected in Port Foster during these surveys. The adult G. acuticeps was collected in the otter trawl at 160 m water depth in June 2000. The benthic G. acuticeps is typically found at depths of less than 50 m and has been collected in all Southern Ocean sectors (Gon and Heemstra, 1990) to a depth of 663 m (Eastman and Hubold, 1999). Two adult P. evansii were collected in the otter trawl in Port Foster and one in the MOCNESS in the 100–150 m depth horizon all measuring approximately 15 cm. Though relatively rare, P. evansii is found in all Southern Ocean sectors at depths from 70 to 550 m (Gon and Heemstra, 1990). A recent Ross Sea survey collected individuals to 910 m (Eastman and Hubold, 1999). P. evansii has not been observed in previous recent surveys around Port Foster (Everson, 1987),
ARTICLE IN PRESS 1848
H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
Table 1 Table showing fish species collected, location, and method All identified species (family/species)
Bathydraconidae G. acuticeps P. evansii Channichthyidae C. aceratus C. gunnari Nototheniidae G. gibberifrons L. larseni L. nudifrons N. coriiceps P. antarcticum T. bernacchii T. scotti
Location (method) Port Foster (MOCNESS)
Port Foster (Otter Trawl)
X
X X
X X
X
X
X X X
Livingston Island (Otter Trawl)
Admiralty Bay (Otter Trawl)
X X
X X X
X X X
Admiralty Bay (Skora and Neyelov, 1992), or the entire region (Jones et al., 2001). One juvenile C. aceratus (8.3 cm) was caught in the 0–50 m MOCNESS net in Port Foster. C. aceratus have been observed to reach maturity at around 57.1 cm in females and 45.7 cm in males (Kock, 1989) and is typically found at 200–400 m depth (Kock and Jones, 2002) throughout the lower Atlantic Southern Ocean sector (Gon and Heemstra, 1990). C. aceratus was recently observed in Admiralty Bay (Skora and Neyelov, 1992), and in a survey of the entire region (Jones et al., 2001). Mostly juvenile C. gunnari were observed (Fig. 3a) in the MOCNESS samples from 0 to 150 m depth and few were collected in the otter trawl. Only one maturing female was found with developing gonads (stage three) at 21.3 cm. Spawning is known to occur from March to May in the Antarctic Peninsula region, with length at first spawning approximately 25 cm (Kock and Kellermann, 1991) and an age of 2.8–3 years (Kock and Everson, 1997). Three year-classes were identified during the November 2000 survey (Fig. 3a). No C. gunnari were observed outside Port Foster during the Erupt surveys. Common to the
X X X
X X
waters surrounding the Antarctic Peninsula and the lower Antarctic islands, C. gunnari has been collected at depths to 700 m (Gon and Heemstra, 1990). C. gunnari has been previously collected in Port Foster during nighttime net hauls (Everson, 1987) at depths of o80 m, as well as in surveys in nearby Admiralty Bay (Skora and Neyelov, 1992), at Elephant Island (61 S, 55 W) (Kock and Stransky, 2000), and the South Shetland Islands (Jones et al., 2001). C. gunnari was notably absent in a recent trawl survey of the Ross Sea (Eastman and Hubold, 1999). Although some stocks were estimated to be greatly reduced by fishing, it is still a relatively abundant species (Kock and Stransky, 2000). Five G. gibberifrons specimens were collected among all three survey locations in otter trawls. G. gibberifrons length at maturity was noted to be 36–38.6 cm in Kock (1989) and 33–36 cm in Jones et al. (2001). The specimens collected during the Erupt surveys all had lengths less than 33 cm (Fig. 3b) and were presumably juveniles. G. gibberifrons is an abundant species in the region, and it dominated the biomass of the fauna around Elephant Island during a recent survey (Kock and Stransky, 2000) and previous surveys of Admiralty Bay (Skora and Neyelov, 1992).
ARTICLE IN PRESS H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
1849
Fig. 3. Length (cm) vs. weight (g) for C. gunnari (a); G. gibberifrons (b); L. larseni (c); L. nudifrons (d); P. antarcticum (e); T. bernacchii (f); and T. scotti (g) for all Erupt cruises and locations. Note the three size classes seen in C. gunnari.
Additionally, G. gibberifrons was the second most abundant fish a recent survey of the South Shetland Islands (Jones et al., 2001). Many specimens of L. larseni were collected in Port Foster, Admiralty Bay, and off Livingston Island in benthic otter trawls during the Erupt survey. Length at first maturity stage four was found to be 9.9 cm during the Erupt surveys (Table 2) and has been previously observed to be 11–13 cm (Duhamel and Pletikosic, 1983). Adults and juveniles were caught during the Erupt study (Fig. 3c). L. larseni is found from 30 to 550 m
depth in the lower latitude Antarctic islands in all ocean sectors (Gon and Heemstra, 1990). It also was found in a recent survey of Elephant Island (Kock and Stransky, 2000) but was not observed at Admiralty Bay previously by Skora and Neyelov (1992). L. nudifrons was frequently caught in the deeper soft bottom areas in the otter trawl. Fewer were caught in the MOCNESS collections at 0–100 m depth. Large juveniles and adults were observed in Port Foster and Admiralty Bay during the Erupt surveys (Fig. 3d). Length at first maturity in the
ARTICLE IN PRESS H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
1850
Table 2 Mean female gonosomatic index (with sample number n) and length at first maturity (LFM) (stage four after Kock and Kellermann, 1991) for all Erupt locations Examined species
Collection date (month/year)
(family/species)
3/1999
L. larseni L. nudifrons T. scotti
0.036 (22) 0.108 (1)
11/1999
0.024 (8)
Antarctic Peninsula region is known to be 9–11 cm (Hourigan and Radtke, 1989; Jones et al., 2001), 13 cm at Elephant Island (Kock, 1989), and was observed at 9.5 cm at stage four in the Erupt study (Table 2). Males have been noted as having a lower average mass per unit length than females (Skora and Neyelov, 1992). The mass difference also was observed during the Erupt study, with the average male weighing 21.9 g and female weighing 26.4 g (n ¼ 45 and 36, respectively). Average lengths were similar at 11.0 and 11.7 cm, respectively. L. nudifrons has a limited known distribution from the lower Antarctic Peninsula to South Georgia at depths from 5 to 350 m (Gon and Heemstra, 1990). It has been collected recently throughout the South Shetland Islands (Skora and Neyelov, 1992; Kock and Stransky, 2000; Jones et al., 2001; Kamler et al., 2001). One adult of the common N. coriiceps (33.6 cm) was caught off Livingston Island in an otter trawl and was the only species observed solely outside Port Foster. N. coriiceps reaches maturity at roughly 34–35 cm (Everson, 1970; Kock, 1989) and is pelagic as a juvenile and demersal later in life. N. coriiceps is found in all Southern Ocean sectors and mid-upper Antarctic latitudes at 0–550 m depth, usually above 200 m (Gon and Heemstra, 1990) and has been observed in several recent surveys and collections in the region (Skora and Neyelov, 1992; Kock and Stransky, 2000; Jones et al., 2001; Kamler et al., 2001). The common and generally pelagic fish P. antarcticum was found only in Port Foster during the Erupt study and was caught throughout the water column and once in the otter trawl. Length at maturity was noted by Hubold (1985) to be 12.5 cm. The fifteen specimens collected in the
2/2000
6/2000
11/2000
LFM (cm)
0.036 (9)
0.111 (8) 0.123 (5)
0.003 (2) 0.019 (27) 0.022 (6)
9.9 9.5 9.0
Erupt study were juveniles, with the largest being 10.5 cm (Fig. 3e). One juvenile and three adult T. bernacchii were collected in otter trawls in Port Foster and one adult in Admiralty Bay during the Erupt study (Fig. 3f). Length at maturity has been reported by Hureau (1970) to be about 17 cm. Many adult and juvenile T. scotti were collected in otter trawls in Port Foster and Admiralty Bay (Fig. 3g). Few T. scotti were collected in the 100–150 m MOCNESS tows during the Erupt cruise series. Length at first maturity stage four was found to be 9 cm in the Erupt surveys (Table 2), the only reported maturation data for T. scotti to our knowledge. A peak in GSI occurred between June and November 2000, indicating that spawning occurred during that period. Larval hatching is known to occur typically in January (Gon and Heemstra, 1990), suggesting that the time of egg laying to hatching for T. scotti may be one or more months. P. antarcticum, T. bernacchii, and T. scotti have been found in all ocean sectors at depths from surface waters to 700 m or more in pelagic settings over the continental shelf (Gon and Heemstra, 1990) and in several recent surveys in the region (Skora and Neyelov, 1992; Eastman and Hubold, 1999; Kock and Stransky, 2000; Jones et al., 2001). 3.2. Abundance Demersal fish abundance estimates for March and November 1999, and June and November 2000 ranged from 0.05 to 0.10 fish m2 (Fig. 4). There was no clear temporal trend in demersal fish abundance within the observations made. Fishes observed in the photography showed little
ARTICLE IN PRESS H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
1851
0.12
6-Nov-99
Density (fish m-2)
0.1
5-Jun-00 0.08
28-Nov-00 0.06
4-Mar-99 0.04
0.02
0 1-Nov-98
9-Feb-99
20-May-99
28-Aug-99
6-Dec-99
15-Mar-00
23-Jun-00
1-Oct-00
9-Jan-01
Fig. 4. The abundance of fishes observed in line-transect photography at Port Foster during the Erupt cruises. The error bars indicate the 95% confidence interval of the abundance estimate.
indication of avoidance behaviors similar to findings of Ekau and Gutt (1991). The identification of fish to species in the photography was aided in part by the voucher collection provided by the otter trawl samples. Specimens collected in the otter trawl are considered representative of fish observed in the photography in terms of species composition. Identification to species was not consistently possible in all the photographs as in Ekau and Gutt (1991). Based on the line-transect photography and the otter trawl voucher collections, the abundance estimate for March 1999 includes primarily the notothenioids L. larseni, L. nudifrons, and T. scotti combined. Estimates from November 1999 and June 2000 are principally for T. scotti. The abundance estimate for November 2000 principally includes L. larseni, L. nudifrons, and T. scotti. The use of line-transect photography methods provides a good estimate of the demersal fish abundance and avoids some of the errors associated with estimates of effort in terms of exact bottom time and distance traversed in otter trawls, and provide some estimation of avoidance behavior. The use of line-transect photography in areas of greater water clarity could improve the species determination in the photographs. Ekau and Gutt
(1991) used still photography and video transecting methods and estimated total demersal fish abundance to be 0.08 and 0.06 fish m2, respectively, in the Weddell Sea. The estimates from the Weddell Sea, however, were over a much larger study area and depth range than was examined in Port Foster and used different methods to estimate the area surveyed. 3.3. Habitat Two generalized benthic habitats were observed, a deeper soft bottom and a shallower ophiuroidcovered benthos. Observed during four ROV video surveys and four photographic line transects, the deeper soft-bottom habitat made up the majority of the seafloor of Port Foster. Large rocks and boulders were also sparsely present. Dominant epibenthic megafaunal invertebrates observed in the video included large euphausiidlike crustaceans, brittlestars: Ophionotus victoriae, urchins: Sterechinus neumayeri, asteroids: Odontaster validus, and nemerteans: Parbolasia corrugatus, as well as numerous tunicates and sponges (Cranmer et al., 2003). The infauna was dominated by foraminifera, nematodes, and polychaetes (Lovell and Trego, 2003). Of the major taxa
ARTICLE IN PRESS 1852
H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
observed, only euphausiids and polychaetes were major prey items for notothenioids. Euphausiids are not readily apparent in the line-transect photography and may have been attracted to the constant ROV lighting. There are, however, many apparent euphausiids utilizing the benthos. Fishes observed frequently by the ROV in the softbottom locations included T. scotti and C. gunnari. Many appeared in small depressions in the soft bottom, with the fish often partially curled. One small shallow-water region, Stanley Patch (Fig. 2), was surveyed with the ROV. With a depth of approximately 20 m, Stanley Patch was different from the deeper soft bottom area in several ways. In addition to many of the fauna observed in the deeper areas, there was an abundance of smaller ophiuroids. At some points on Stanley Patch, the bottom was so completely covered by ophiuroids that the sediment was obscured. The abundances of urchins, nemerteans, asteroids, tunicates, sponges, and L. nudifrons were also relatively higher than in the deeper areas. Large swimming crustaceans were relatively less abundant. Fishes also were found among the sponges and tunicates as observed by Ekau and Gutt (1991). 3.4. Diet C. gunnari, L. larseni, L. nudifrons, and T. scotti were collected in sufficient numbers to examine their diet (Table 3). Cumulative prey curves (Fig. 5) illustrate that enough stomachs were sampled to describe the broad taxonomic prey groups. No curve was made for C. gunnari as there were only two principle prey items. There was no definitive trend in prey choice or %FO between sampling periods for those species examined. A brief review of known diet analyses for the remaining fishes is also presented to provide a more complete description of the importance of the fishes observed in the food web of the study area. The diet of the mostly juvenile C. gunnari observed in Port Foster consisted almost exclusively of Euphausia crystallorophias and E. superba. Other studies have shown that euphausiids generally make up 90–99% of C. gunnari prey items (Kock and Everson, 1997; Jones et al., 2001).
Euphausiids were abundant in the MOCNESS tows (Kaufmann et al., 2003) and euphausiid-like crustaceans were visible in the ROV video of the Port Foster benthos. The mostly juvenile specimens in previous surveys of Admiralty Bay had an approximately 50%FO of empty stomachs (Skora and Neyelov, 1992) compared with 17.5%FO in a recent NOAA survey (Jones et al., 2001), and 15%FO empty stomachs during the Erupt survey (Table 3). Euphausiids dominated the diet and prey choice for L. larseni in the Erupt collections. Other crustaceans such as amphipods and isopods, as well as polychaetes were also important prey items (Table 3). The bivalve Nuculana inaequisculpta and nematodes, also were identified as prey items. Bivalves and nematodes were strongly avoided in prey choice (Table 3) and may have been eaten incidentally with other benthic prey. Prey items observed in previous surveys are similar and consist principally of euphausiids, amphipods, mysids, calanoid copepods, and salps (Permitin and Tarverdiyeva, 1972; Target, 1981; Daniels, 1982; Gorelova and Shandikov, 1988; Jones et al., 2001). No empty stomachs were found in the L. larseni Erupt collections, which may indicate that feeding typically occurs before the stomach is emptied, as was observed by Gorelova and Shandikov (1988). The diet of L. nudifrons during the Erupt survey was dominated by euphausiids, with other crustaceans, and fish eggs also making up a portion of the diet (Table 3). Crustaceans such as amphipods and isopods may be a favored food item as indicated by the limited selectivity data (Table 3). L. nudifrons is generally known to eat benthic fauna such as polychaetes, amphipods, isopods, fish eggs, and euphausiids (Target, 1981; Daniels, 1982; Jones et al., 2001). Small specimens also feed on copepods and other zooplankton (Richardson, 1975). As with the closely related L. larseni, no empty stomachs were observed in L. nudifrons, again indicating that feeding may typically occur before full digestion of previously consumed food. The diversity of the major prey taxa was greater for T. scotti than the other fishes examined here. Polychaetes, euphausiids, and other crustaceans
ARTICLE IN PRESS H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
1853
Table 3 Results from the diet analysis of fishes from all Erupt cruises and locations showing percent frequency of occurrence (%FO), percent of total prey number (%N), percent of total prey weight (%W), absolute importance index (AI), the relative importance index (RI), index of relative importance (IRI), and the Ivlev Index of Electivity (E) Fish species Prey items
Diet indices %FO
%N
%W
AI
RI
IRI
C. gunnari (n ¼ 122) E. crystallorophias E. superba Unidentified euphausiids Other Empty stomachs
21 15 58 1 15
17 14 68 o1
26 39 35 {1
64 68 161 1
22 23 55 {1
903 795 5974 0
L. larseni (n ¼ 45) Euphausia sp. Other crustacea Polychaetea Bivalvia Nematoda Other (mostly sediment) Empty stomachs
40 22 9 2 4 71 0
40 42 12 2 4
43 2 1 {1 {1 54
123 66 22 4 8
53 28 10 2 3
3320 968 117 4 16
0.87 0.54 0.75 0.82
L. nudifrons (n ¼ 72) Euphausia sp. Other crustacea Polychaetea Bivalvia Gastrapoda Fish eggs Other (mostly sediment) Empty stomachs
45 18 4 7 7 8 42 0
54 29 6 3 3 5
69 4 o1 o1 o1 5 21
168 51 10.3 10.3 10.3 18
63 19 4 4 4 7
5535 594 24 21 21 80
0.81 0.74 0.65 1 1
T. scotti (n ¼ 72) Euphausia sp. Other crustacea Polychaetea Bivalvia Nematoda Priapulida Fish eggs Other (mostly sediment) Empty stomachs
22 25 29 44 20 6 10 10 12
7 4 52 33 3 o1 1
17 3 34 13 {1 10 11 12
46 32 115 90 22 16 22
13 9 33 26 7 5 6
528 175 2494 2024 60 60 120
dominated the diet, while bivalves, nematodes, and priapulids also made up significant portions of the diet (Table 3). T. scotti primarily fed on benthic polychaetes, euphausiids, amphipods, and isopods in previous studies as well (Target, 1981; Daniels, 1982; Pakhomov, 1997). Although Pakhomov (1997) found no empty stomachs, the Erupt study found a 21%FO for empty stomachs.
E
0.14 0.13 0.40 0.87
The diets of remaining fishes consist of both pelagic and benthic prey. G. acuticeps is piscivorous as an adult, eating P. antarcticum, myctophids, and other fishes, as well as fish eggs, amphipods, and polychaetes (Takahashi, 1983; Eastman, 1985; Pakhomov, 1997). P. evansii has been shown to feed on benthic polychaetes, crustaceans, and amphipods (Kock et al., 1984). C. aceratus is
ARTICLE IN PRESS H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
1854 7
L. larseni
No. prey taxa
6 5 4 3 2 1 0
10
20
30
40
50
No. stomachs analyzed 8
L. nudifrons
7
No. prey taxa
6 5 4 3 2 1 0 0
20
40
60
80
No. stomachs analyzed 9
T. scotti
8
No. prey taxa
7 6 5
known to migrate vertically as juveniles feed on pelagic invertebrates (Kock and Jones, 2002). They then become more sedentary and piscivorous with age and are ambush feeders by a length of 30 cm (Jones et al., 2001). The benthic G. gibberifrons has been observed to ambush feed from rock perches and soft mud sediments (Daniels, 1982). G. gibberifrons also has been noted to feed in part on errant and sedentary polychaetes, amphipods, ophiuroids, and pycnogonids in the Antarctic Peninsula region (Daniels, 1982; Jones et al., 2001). N. coriiceps has been observed as a benthic ambush predator, often consuming large prey items with occasional watercolumn feeding, as well as grazing of fish, isopods, amphipods, and mollusks (Blankley, 1982; Daniels, 1982; Burchett et al., 1983; Pakhomov, 1997; Jones et al., 2001). N. coriiceps also has been observed feeding selectively on macroalgae as adults (Daniels, 1982; Iken et al., 1997). P. antarcticum has been noted to feed in the water column on euphausiids, cumaceans, and copepods (Daniels, 1982; Pakhomov, 1997). Typically described as a benthic browser and ambush feeder, T. bernacchii has been noted to feed on amphipods, polychaetes, isopods, and macroalgae with an increasing diversity of prey with growth (Daniels, 1982; Kiest, 1993). Vacchi et al. (1994) observed that bivalves and euphausiids were also important prey items. Animals known to feed on fish in the region include other fishes, squid, cetaceans, seabirds, and pinnipeds (Kock, 1992). Several of the seabirds and pinnipeds observed at Deception Island are known to feed on notothenioid fishes and compete for euphausiids as a major prey item (Kendall et al., 2003).
4
3.5. Parasites
3 2 1 0
20
40
60
80
No. stomachs analyzed Fig. 5. Cumulative prey curves for L. larseni, L. nudifrons, and T. scotti illustrating the asymptotic relationship between the number of stomachs analyzed and the number of prey taxa observed. The error bars represent one standard error.
Body cavity and alimentary tract parasites are frequently observed in notothenioids (Palm et al., 1994; Zdzitowiecki et al., 1998; Zdzitowiecki, 2001, 2002a, 2002b) and are thought to adversely affect fishes in a variety ways (Barber et al., 2000). Pelagic feeding fishes such as juvenile C. gunnari typically have low infestation frequencies and endoparasite diversity (Hoogesteger and White,
ARTICLE IN PRESS H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
1855
In L. larseni, all specimens above 11 cm had a frequency of occurrence of 100% (n ¼ 38=38) of body cavity parasites and specimens smaller than 11 cm had an occurrence of 56% (n ¼ 9=16). With age, L. larseni changes from a pelagic to a benthic habitat (Gorelova and Shandikov, 1988; Kellermann, 1989), which is another indication that these parasites are likely residing in the benthos and benthic prey items and infect fish as they begin benthic feeding. L. larseni had a higher diversity of parasites than the others examined with nine or more species recorded (Table 4). The common nematode Pseudoterranova decipiens was the most abundant of the parasites identified in L. larseni. The body cavity parasite infestation for L. nudifrons was lower (22%) than the other nototheniids examined here. L. nudifrons had similar occurrence of infestation in both juveniles and adults. The two T. bernacchii specimens examined for parasites had at least eight species of parasites in the body cavity and lumen of the intestine (Table 4). Four species of parasites were identified in six specimens of T. scotti with the common P. decipiens being dominant (Table 4). Body cavity parasites were present in all examined specimens
1981; Kock and Everson, 1997; Zdzitowiecki, 2002a). In support of these studies no body cavity parasites were observed in the 133 mostly juvenile C. gunnari specimens dissected from the Erupt surveys. Mid-stage nematode parasite worms are not known to occur in euphausiids (Kagei et al., 1978). The C. gunnari diet of nearly exclusively euphausiids may preclude heavy infestation and subsequent fitness burdens (Kock, 1992). Previous work has shown channichthyid fishes have a higher diversity of digenea in areas with larger accessible benthic habitats such as the South Shetland Islands than the relatively open waters of the Weddell Sea (Zdzitowiecki, 2002b). The benthic feeding L. larseni, L. nudifrons, T. bernacchii, and T. scotti were commonly infested with body-cavity parasites with a frequency of occurrence of 87% (n ¼ 47=54), 22% (n ¼ 17=81), 40% (n ¼ 2=5), and 100% (n ¼ 210=210), respectively. L. larseni, L. nudifrons, T. bernacchii, and T. scotti, for which body-cavity and intestine parasites were identified (Table 4), all had infestations of multiple species of parasites known to be abundant in fishes in the shallow waters of western Antarctica (K. Zdzitowiecki, personal communication).
Table 4 List of observed parasite species for randomly selected fishes from all Erupt cruises and locations. The mean number of parasites observed for each type are noted. Metacanthocephalus sp. is likely to be one or all of M. dalmori, M. johnstoni, and M. campbelli Parasites Larval Cestoda Tetraphyllidean cercoid bilocular Diphyllobothriid plerocercoid Digenea Macvicaria georgiana Neolebouria antarctica juv. Lepidapedon garrardi Larval Nematoda Contracaecum spp. P. decipiens Acanthocephala adults Aspersentis megarhynchus Metacanthocephalus spp. Acanthocephala cystacanths Corynosoma hamanni C. pseudohamanni C. arctocephali.
Tissue type
L. larseni n¼6
Intestine Body cavity
0.5 2.0
Intestine Intestine Intestine
4.7 0.2 1.0
Body cavity Body cavity
7.3
13.2 2.7
Intestine Intestine
0.3
11.7
0.5 1.5
0.3 0.3
1.7 4.0 2.2
1.5 13.0 4.0
Body cavity Body cavity Body cavity
L. nudifrons n¼6
3.8
T. bernacchii n¼2 1.0 2.5
1.5
T. scotti n¼6
0.2
4.8 8.0
0.2
ARTICLE IN PRESS 1856
H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
from Port Foster, implying heavy parasite infestation. However, no juvenile T. scotti were sampled for parasites. Decreased benthic habitat scour from large icebergs may allow parasites with benthic life stages to persist and become more abundant than in areas with more frequent scouring. A tissue analysis found that there was no consistent increase in heavy metals in the nematode parasites of T. scotti when compared to other tissues including muscle, liver, and gills (D. Deheyn, personal communication). These nematodes then are not likely to play a role in metal detoxification for the fish and probably do not act as a bioaccumulator of heavy metals at this stage in the parasites’ life cycle (D. Deheyn, personal communication).
4. Summary Fishes surveyed during the Erupt study of Port Foster, Deception Island and vicinity are known to occur in the region and have diets similar to those found in previous studies. Fishes within Port Foster are predators of invertebrates and small fishes and are likely prey items for the seabirds and pinnipeds observed around the shores of Port Foster. The unique habitat of Port Foster may provide refuge for juveniles of some species such as C. gunnari, which were frequently observed there. Limited exchange with the surrounding waters also may limit the influence of recruitment and prey abundance fluctuations outside Port Foster. T. scotti had heavy body cavity parasite infestation from Port Foster, possibly due in part to decreased benthic scour from large icebergs. Not recorded in many recent surveys of the region, P. evansii was notably observed in Port Foster. The overall abundances of fishes observed in Port Foster show maximum in November 1999 and range from 0.05 to 0.10 fish m2, similar to those found over a larger region and depth range in the Weddell Sea. The 1.5-year time-series did not reveal any clear pattern in abundance. The use of line-transect photography combined with otter trawl collections can be useful in determining the abundance of demersal notothenioid fishes in areas where water clarity is sufficient. Further
multi-year and diel time-series investigations, which include diet studies, estimations of digestion time, and fecundity information would help to better describe population dynamics and feeding habits of Antarctic fishes.
Acknowledgements We would like to thank K.L. Smith Jr. for initiating and coordinating the Erupt series; H.J. Walker, C. Klepadlo, L.L. Lovell, A.W. Townsend, K.D. Trego, and the Scripps Institution of Oceanography vertebrate and invertebrate collections for aid in fish and prey item identifications; J.C. Drazen and three anonymous reviewers for their helpful insights and suggestions; the science parties and crews of the R.V. L.M. Gould during the Erupt cruise series. This research was funded by the US National Science Foundation grant OPP-97-27077 to K.L. Smith.
References Barber, I., Hoare, D., Krause, J., 2000. Effects of parasites on fish behavior: a review and evolutionary perspective. Reviews in Fish Biology and Fisheries 10, 131–165. Blankley, W.O., 1982. Feeding ecology of the three inshore fish species at Marion Island (Southern Ocean). South African Journal of Zoology 17, 164–170. Brenner, M., Buck, B.H., Cordes, S., Dietrich, L., Jacob, U., . Mintenbeck, K., Schroder, A., Brey, T., Knust, R., Arntz, W., 2001. The role of iceberg scours in niche separation within the Antarctic fish genus Trematomus. Polar Biology 24, 502–507. Buckland, S.T., Anderson, D.R., Burnham, K.P., Laake, J.L., 1993. Distance Sampling: Estimating Abundance of Biological Populations. Chapman & Hall, London, 446pp. Burchett, M.S., Sayers, P.J., North, A.W., White, M.G., 1983. Some biological aspects of the nearshore fish populations as South Georgia. British Antarctic Survey Bulletin 59, 63–74. Clarke, A., Johnston, I.A., 1996. Evolution and adaptive radiation of Antarctic fishes. Trends in Ecology and Evolution 11, 212–218. Cranmer, T., Ruhl, H.A., Kaufmann, R.S., Baldwin, R.J., 2003. Spatial and temporal variation in the abundance, distribution and population structure of epibenthic megafauna in Port Foster, Deception Island. Deep-Sea Research II, this issue (doi: 10.1016/S0967-0645(03)00093-6).
ARTICLE IN PRESS H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858 Daniels, R.A., 1982. Feeding ecology of some fishes of the Antarctic Peninsula. Fishery Bulletin, United States Department of Commerce 80, 575–588. Duhamel, G., Pletikosic, M., 1983. Donnes biologiques sur les Nototheniidae les Nototheniidae des #ıles Crozet. Cybium 7, 43–57. Eastman, J.T., 1985. Pleuragramma antarcticum (Picies, Nototheniidae) as food for other fishes in McMurdo Sound, Antarctica. Polar Biology 4, 155–160. Eastman, J.T., 1990. The biology and physiological ecology of notothenioid fishes. In: Gon, O., Heemstra, P.C. (Eds.), Fishes of the Southern Ocean. J. L. B. Smith Institute of Ichthyology, Grahamstown, South Africa, pp. 34–51. Eastman, J.T., Clarke, A., 1998. A comparison of adaptive radiations of Antarctic fish with those of non-Antarctic Fish. In: di Prisco, G., Pisano, E., Clarke, A. (Eds.), Fishes of Antarctica. Springer, Milano, Italia, pp. 5–26. Eastman, J.T., Hubold, G., 1999. The fish fauna of the Ross Sea, Antarctica. Antarctic Science 11, 293–304. Ekau, W., Gutt, J., 1991. Notothenioid fishes from the Weddell Sea and their habitat, observed by underwater photography and television. Proc. NIPR Symp. Polar Biology 4, 36–49. Everson, I., 1970. Reproduction in Notothenia neglecta Nybelin. British Antarctic Survey Bulletin 23, 81–92. Everson, I., 1987. Some aspects of the small scale distribution of Euphausia crystallorophias. Polar Biology 8, 9–15. Ferry, L.A., 1997. Food habits of the two-line eelpout (Bothrocara brunneum, Zoarchidae) at two deep-sea sites in the eastern North Pacific. Deep-Sea Research I 44, 521–531. George, E.L., Hadley, W.F., 1979. Food and habitat partitioning between rock bass (Amploplites rupestris) and smallmouth bass (Micropterus dolomieui) young of the year. Transactions of the American Fisheries Society 108, 253–261. Gon, O., Heemstra, P.C., 1990. Fishes of the Southern Ocean. J. L. B. Smith Institute of Ichthyology, Grahamstown, South Africa, 462pp. Gorelova, T.A., Shandikov, G.A., 1988. Age-related changes in the composition of the food and daily feeding rhythm of Nototheniops tchizh tchizh in the Lena Bank region (Indian Ocean sector of the Southern Ocean). Journal of Ichthyology 28, 86–92. Hoogesteger, J.N., White, M.G., 1981. Notes on the parasite infestation of inshore fish at Signy Island, South Orkney Islands. British Antarctic Survey Bulletin 54, 23–31. Hourigan, T.J., Radtke, R.L., 1989. Reproduction of the Antarctic fish Nototheniops nudifrons. Marine Biology 100, 277–283. Hubold, K.G., 1985. Stomach contents of the Antarctic silverfish Pleuragramma antarcticum from the southern and eastern Weddell Sea (Antarctica). Polar Biology 5, 43–48. Hureau, J.C., 1970. Biologie compar!ee de quelques poissons antarctiques (Nototheniidae). Bulletin de l’Institut Oce! anography, Monaco 68, 1–250.
1857
Hyslop, E.J., 1980. Stomach contents analysis—a review of methods and their application. Journal of Fish Biology 17, 411–429. Iken, K., Barrera-Oro, E.R., Quartino, M.L., Casaux, R.J., Brey, T., 1997. Grazing by the Antarctic fish Notothenia coriiceps, evidence for selective feeding on macroalgae. Antarctic Science 9, 386–391. Ivlev, V.S., 1961. Experimental ecology of the feeding of fishes. Yale University Press, New Haven, 302pp. Jones, C.D., Kock, K.-H., Wilhems, S., Ramm, D., Ashford, J., Near, T., Emery, J.H., Gong, N., Flores, H., Banks, A.R., Prowse, M., 2001. Bottom trawl survey and finfish research in the South Shetland Islands, In: Lipsky, J. (Ed.), AMLR 2000/2001 Field Season Report, NOAA-TM-NMFSSWFSC-314. Kagei, N., Asano, K., Kihata, M., 1978. On the examination against parasites of Antarctic krill, Euphausia superba. Scientific Reports of the Whales Research Institute, Tokyo 30, 311–313. Kamler, E., Krasicka, B., Rakusa-Suszczewski, S., 2001. Comparison of lipid content and fatty acid composition in muscle and liver of two notothenioid fishes from Admiralty Bay (Antarctica), an eco-physiological perspective. Polar Biology 24, 735–743. Kaufmann, R.S., Fisher, E.C., Gill, W.H., King, A.L., Laubacher, M., Sullivan, B., 2003. Temporal patterns in the distribution, biomass and community structure of macrozooplankton and micronekton within Port Foster, Deception Island, Antarctica. Deep-Sea Research II, this issue (doi: 10.1016/S0967-0645(03)00092-4). Kellermann, A., 1989. The larval fish community in the zone of seasonal pack-ice cover and it’s seasonal and interanual variability. Archiv Fuer Fischereiwissenschaft. 39 (Suppl. 1), 81–110. Kendall, K, Ruhl, H.A., Wilson, R.C., 2003. Distribution and abundance of marine bird and pinniped populations within Port Foster, Deception Island, Antarctica. Deep-Sea Research II, this issue (doi: 10.1016/S0967-0645(03)00096-1). Kiest, K.A., 1993. A relationship of diet to prey abundance and the foraging behavior of Trematomous bernacchii. Polar Biology 13, 291–296. Kock, K.-H., 1989. Reproduction in fish around . Fischereiwissenschaft 39, Elephant Island. Archive fur 171–210. Kock, K.-H., 1992. Antarctic Fish and Fisheries. Cambridge University Press, Cambridge, 359pp. Kock, K.-H., Everson, I., 1997. Biology and ecology of mackerel icefish, Champsocephalus gunnari, an Antarctic fish lacking hemoglobin. Comparative Biochemistry and Physiology 118A, 1067–1077. Kock, K.-H., Jones, C.D., 2002. The biology of the icefish Cryodraco antarcticus dollo, 1990 (pisces, channichthyidae) in the southern Scotia Arc (Antarctica). Polar Biology 25, 416–424. Kock, K.-H., Kellermann, A., 1991. Reproduction in Antarctic notothenioid fishes—a review. Antarctic Science 3, 125–150.
ARTICLE IN PRESS 1858
H.A. Ruhl et al. / Deep-Sea Research II 50 (2003) 1843–1858
Kock, K.-H., Stransky, C., 2000. The composition of the coastal fish fauna around Elephant Island (South Shetland Islands, Antarctica). Polar Biology 23, 825–832. Kock, K.-H., Schneppenheim, R., Siegel, V., 1984. A contribution to the fish fauna of the Weddell Sea. Archive fur . Fischereiwissenschaft 34, 103–120. Laake, J.L., Buckland, S.T., Anderson, D.R., Burnham, K.P., 1994. Distance users guide V 2.1. Colorado Cooperative Fish and Wildlife Research Unit, Colorado State University, Fort Collins, CO, 84pp. Lauerman, L.M.L., Kaufmann, R.S., Smith Jr., K.L., 1996. Distribution and abundance of epibenthic megafauna at a long time-series station in the abyssal northeast Pacific. Deep-Sea Research I 43, 1075–1104. Lovell, L., Trego, K., 2003. The epibenthic megafaunal and benthic infaunal invertebrates of Port Foster, Deception Island (South Shetland Islands, Antarctica). Deep-Sea Research II, this issue (doi: 10.1016/S0967-0645(03)00087-0). Miller, R.G., 1993. History and Atlas of the Fishes of the Antarctic Ocean. Foresta Institute, Carson City, NV, 792pp. Pakhomov, E.A., 1997. Feeding and exploitation of the food supply by demersal fishes in the Antarctic part of the Indian Ocean. Journal of Ichthyology 37, 360–380. Palm, H., Anderson, K., Kl.oser, H., Pl.otz, J., 1994. Occurrence of Pseudoterranova decipiens (Nematoda) in fish from the southeastern Weddell Sea (Antarctic). Polar Biology 14, 539–544. Permitin, Y.Y., Tarverdiyeva, M.I., 1972. The food of some Antarctic fish in the South Georgia area. Journal of Ichthyology 12, 104–114. Pinkas, L., Oliphant, M.S., Iverson, I.L.K., 1971. Food habits of albacore, bluefin tuna, and bonito in California waters. California Department of Fish and Game, Fish Bulletin 152, 1–105. Prince, E.D., 1975. Pinnixid crabs in the diet of young-of-theyear copper rockfish (Sebastes caurinus). Transactions of the American Fisheries Society 99, 440–443. Richardson, M.G., 1975. The dietary composition of some Antarctic fish. British Antarctic Bulletin 41/42, 113–120. Skora, K.E., Neyelov, A.V., 1992. Fish of Admiralty Bay (King George Island, South Shetland Islands, Antarctica). Polar Biology 12, 476–496.
Smith Jr., K.L., Baldwin, R.J., Kaufmann, R.S., Sturz, A., 2003. Ecosystem studies at Deception Island, Antarctica, an overview. Deep-Sea Research II, this issue (doi: 10.1016/ S0967-0645(03)00081-X). Takahashi, M., 1983. Trophic ecology of demersal fish communities north of South Shetland Islands, with notes on the ecological role of krill. Memoirs of the National Institute of Polar Research 27, 183–192. Target, T.E., 1981. Trophic ecology and structure of coastal Antarctic fish communities. Marine Ecology Progress Series 4, 243–263. Vacchi, M., La Mesa, M., Castelli, A., 1994. Diet of two coastal nototheniid fish from Terra Nova Bay, Ross Sea. Antarctic Science 6, 61–65. Wakefield, W.W., Genin, A., 1987. The use of a Canadian (perspective) grid in deep-sea photography. Deep-Sea Research I 34, 469–478. Wakefield, W.W., Smithey, W., 1989. Two camera sleds for quantitative study of deep-sea megafauna. Scripps Institution of Oceanography Reference Series 89-14, 25pp. Zdzitowiecki, K., 1991. Antarctic Acanthocephala, parasites of fishes. In: W.agele, J.W., Sieg, J. (Eds.), Synopses of the Antarctic Benthos, Vol. 3. Koeltz Scientific Books, . Koenigstein, Germany. Zdzitowiecki, K., 1997. Antarctic Digenea, parasites of fishes. In: W.agele, J.W., Sieg, J. (Eds.), Synopses of the Antarctic . Benthos, Vol. 8. Koeltz Scientific Books, Koenigstein, Germany. Zdzitowiecki, K., 2001. New data on the occurrence of fish endoparasitic worms off Adelie Land, Antarctica. Polish Polar Research 22, 159–165. Zdzitowiecki, K., 2002a. Occurrence of Digenea in fishes of the family Nototheniidae in the Weddell Sea. Acta Parasitologica 47, 154–158. Zdzitowiecki, K., 2002b. Occurrence of Digenea in fishes of the family Channichthyidae in the Weddell Sea and other subcontinental areas of the Antarctic. Acta Parasitologica 47, 159–162. Zdzitowiecki, K., Rocka, A., Pisano, E., Ozouf-Costaz, C., 1998. A list of fish parasitic worms collected off Adelie Land (Antarctic). Acta Parasitologica 43, 71–74.