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Squid as a resource shared by fish and humans on the Falkland Islands’ shelf
Fisheries Research 106 (2010) 151–155
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Squid as a resource shared by fish and humans on the Falkland Islands’ shelf Vladimir Laptikhovsky ∗ , Alexander Arkhipkin, Paul Brickle Falkland Islands Government Fisheries Department, P.O. Box 598, Stanley, FIQQ 1ZZ, Falkland Islands
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Article history: Received 24 February 2010 Received in revised form 9 April 2010 Accepted 5 May 2010 Keywords: Falkland Islands Fish Squid Feeding ecology Fishery
a b s t r a c t Nektonic squids are the dominant group in the Falklands Islands’ fishery representing >75% of the total annual catch. Among these squids, the benthopelagic Loligo gahi is an important link between zooplankton and fish in the shelf food web. It is preyed upon by diverse and numerous demersal and benthopelagic fishes, penguins and marine mammals, and is harvested by fishermen. Pelagic squids, Illex argentinus, Onykia ingens, and Gonatus antarcticus though seasonally very abundant, are scarce in fish diet because of the absence of specialised pelagic predators. This ecological niche is shared between humans (targeting Illex) and penguins (targeting Onykia and Gonatus). Martialia hyadesi though was abundant in some years in the past, it has now virtually disappeared from the shelf ecosystem. The biomass produced by L. gahi remains in the Falkland waters, whereas that of pelagic squid is transported out of the shelf either to the northern Patagonian slope (I. argentinus) or to deeper waters around the islands (O. ingens and G. antarcticus). Generally squids occupy the ecological niche of epipelagic fish on the Falkland shelf and slope. © 2010 Elsevier B.V. All rights reserved.
1. Introduction Nowadays aquaculture, freshwater and marine fisheries supply about 10% of world population calorie intake (Nellemann et al., 2009). A total of 80–90% of the human seafood harvest in the Atlantic, Pacific and Indian oceans is represented by fish (Table 1), and only 2–6% – by cephalopods (FAO, 2009), the rest being crustaceans, miscellaneous invertebrates, etc. The actual catch composition could be biased from this general rule in some ecosystems (Rodhouse and White, 1995), and an outstanding example of this is the shelf of the Falkland Islands (southern Southwest Atlantic). It is an important fishery area with annual catch of 101,000–427,000 tonnes (FIG, 2009) on the shelf and upper slope between 100 and 350 m. In contrast to other neighbouring regions, including the adjacent Patagonian shelf with nearly the same cephalopod and fish fauna, the bulk of the total catch around the Falklands (75.3% in 1989–2009, FIG, 2005, 2009) is represented by squids. It is the only region in the world where cephalopods predominate in the total annual catch. There are five common nektonic squid species recorded on the Falkland shelf (we do not take into account such rarities as Architeuthis dux or Pholidoteuthis boschmai). The two of them are abundant commercial species. Illex argentinus (Castellanos, 1960) is a seasonal immigrant of 20–35 cm ML, being on the shelf between February and June (Haimovici et al., 1998). Loligo gahi D’Orbigny,
∗ Corresponding author. Tel.: +500 27 260; fax: +500 27 265. E-mail address: vlaptikhovsky@fisheries.gov.fk (V. Laptikhovsky). 0165-7836/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.fishres.2010.05.002
1835 lives around the Falkland Islands all year round, grows to the size of about 20 cm ML (max. 42 cm ML), reproduces in inshore waters and migrates down to the upper slope for growth and maturation (Arkhipkin et al., 2004). Other nektonic squids that occur on the shelf and upper slope in numbers (at least in some years) are Gonatus antarcticus Lönnberg, 1898 (5–15 cm ML), Onykia ingens Smith, 1881 (5–35 cm ML) and Martialia hyadesi Rochebrune & Mabile 1889 (15–35 cm ML). Juvenile O. ingens and G. antarcticus annually occur on the shelf in spring–summer (Thompson, 1994; Jackson et al., 1998; Nesis, 1999), whereas M. hyadesi is abundant on the shelf in autumn only occasionally (FIG, 2005). None of three species is of commercial importance: G. antarcticus is too small, O. ingens is not edible. M. hyadesi is a potential commercial species in Antarctica, particularly at the Antarctic Polar Front (González and Rodhouse, 1998), but attempts to organise its fishery turned out to be disappointing. This species occurs on the Falkland shelf only in years with Falkland Current spreading over the shelf (Collins and Rodhouse, 2006) as in 1997. Recently it virtually disappeared from the ecosystem; a joint trawl survey of FVs “Castello” and “Beagle” in February 2010 did not yield any Martialia over the entire shelf and upper slope between 100 and 320 m around the islands (our data). In contrast to this, commercial shelf fish species are diverse in both taxonomic and ecological aspects and are represented by hakes Merluccius hubbsi Marini, 1933 and Merluccius australis (Hutton, 1882), hoki, Macruronus magellanicus Lönnberg, 1907, kingclip, Genypterus blacodes (Forster, 1801), blue whiting, Micromesistius australis Norman, 1937, subadult Patagonian toothfish, Dissostichus eleginoides Smitt, 1898, red cod, Salilota australis (Günther, 1878),
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Table 1 Catch composition of marine fisheries in different oceans in the year 2007, % (FAO, 2009). Ocean
Crustacean
Marine fish
Cephalopods
Gastropods and bivalves
Miscellaneous aquatic invertebrates
Atlantic Indian Pacific South
6.3 7.7 6.7 82.4
81.9 89.4 83.2 17.6
6.0 2.1 6.1 0.0
5.8 0.6 3.2 0.0
0.0 0.2 0.8 0.0
rays of the family Rajidae, and small sized notothenioids Patagonotothen spp. There is no direct estimation of biomass of every commercial fish and squid in this area and this task is next to impossible, because most of these species migrate seasonally to and from the Falkland waters. Because of the predominance of squid in the total annual catch (all gears combined), we may assume that cephalopods generally are much more abundant there than both teleost fish and elasmobranchs combined, and the Falkland waters are cephalopod based fishery ecosystem. This is particularly true for the south-eastern shelf, where some 80–90% of the total annual catch by trawlers is represented by the squid L. gahi. Because of the squid abundance around the Falklands it is possible to assume that they should be the key element in the marine food web, and this paper aims to investigate their importance in fish diet and assess the scale of possible impact of fisheries. 2. Materials and methods A total of 6531 fish specimens belonging to 20 commercial and non-commercial species were collected onboard various fishing vessels and during seven research bottom surveys by the R/V Dorada on the Falkland shelf between 30 and 400 m. Sample collection was carried out between June 1999 and April 2003, excluding that of the icefish, Champsocephalus esox that lasted until February 2007. Fish were measured to the nearest 1 cm (pre-anal length, PL, in hoki; disk width, DW, in rays; and total length, TL in all other species), then dissected and analysed onboard or in the Falkland Islands Government Fisheries Department laboratory. Only markedly digested items were taken into account, net feeding was ignored. A total of 109,523 prey items were identified to the lower possible taxonomic level, including 3493 squids. The percentage of occurrence
(%O) and percentage by number (%N) of each nektonic squid species were calculated (Cortés, 1997). 3. Results All squids combined represented a total of 14.9% of prey items in fish stomachs, and mean 69.1% of the total annual catch during the sampling period. 3.1. Loligo gahi This species was a common prey of a variety of fish from different ecological groups, and represented 10.7% of prey items (excluding planktivorous blue whiting and hoki). Among large benthopelagic predators, common hake was the principal consumer of L. gahi in winter (Table 2). Demersal fish consumed an important amount of this squid, it accounted for about a quarter of the diet in frogmouth (Cottoperca gobio) and about 10–15% of that in sharks and rays and subadult Patagonian toothfish (D. eleginoides). This species represented 9.2–23.5% (mean 19.2%) of the total catch of all commercial and non-commercial species during the period of sample collection (FIG, 2009). 3.2. Illex argentinus This species was found to play an important role in the red cod diet, and occurred occasionally in the diet of common hake and kingclip (Table 2). However, it was almost not used by other predatory fish and represented 1.1% of food items. In contrast to this, I. argentinus accounted for 13.2–70.6% (mean 49.9%) of the total catch during the period of sampling.
Table 2 Occurrence of nektonic squids in stomachs of predatory fish. Predator
Ecological group
Amblyraja doellojuradoi Bathyraja albomaculata Bathyraja brachiurops Bathyraja griseocauda Bathyraja scaphiops Champsocephalus esox Cottoperca gobio Dissostichus eleginoides Genypterus blacodes Lampris immaculatusa Macruronus magellanicus Merluccius australis Merluccius hubbsib Micromesistius australis Patagonotothen guntheri Patagonotothen ramsayi Patagonotothen tesselata Salilota australis Schroederichthys bivius Squalus acanthias
Demersal Demersal Demersal Demersal Demersal Benthopelagic Demersal Benthopelagic Demersal Pelagic Pelagic Benthopelagic Benthopelagic Pelagic Benthopelagic Benthopelagic Benthopelagic Demersal Demersal Benthopelagic
a b
Fish size (cm)
7–41 8–50 8–87 9–130 21–57 12.5–37 11–80 26–84 33–134 72–142 14–47 64–84 44–88 10–61 11–23 10–37 12–35 14–84 20–81 44–98
Number of stomachs
26 201 198 154 37 235 357 610 496 69 492 20 357 922 35 394 265 574 564 525
Data from Jackson et al. (2000). June–August, the period of mass hake immigration to the Falkland shelf.
Number of food items
209 1494 981 958 169 332 535 847 1551 1370 11,763 25 1328 75,905 58 1499 293 7602 1217 1387
Loligo
Illex
Gonatus
Moroteuthis
%N
%O
%N
%O
%N
%O
%N
%O
3.4 5.4 8.1 2.1 2.4 0.0 22.2 17.2 2.8 22.6 0.2 4.0 43.3 0.2 0.0 0.9 0.0 9.5 9.6 8.1
19.2 11.4 20.2 9.1 10.8 0.0 26.3 17.7 4.6 23.2 4.1 5.0 89.4 1.0 0.0 3.3 0.0 12.7 26.9 16.0
0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.9 0.0 0.0 0.0 0.2 0.0 0.0 0.0 0.0 2.7 0.7 0.0
0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 1.6 0.0 0.0 0.0 0.6 0.0 0.0 0.0 0.0 10.5 1.4 0.0
0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.0 0.0 <0.1 0.0 0.0 0.0 <0.1 0.0 0.4
0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 1.4 0.0 0.0 0.0 <0.1 0.0 0.0 0.0 <0.1 0.0 0.4
0.5 0.0 0.0 0.0 0.0 0.0 0.0 0.9 0.0 47.0 0.5 0.0 0.2 0.0 0.0 0.0 0.0 0.1 0.7 0.0
3.8 0.0 0.0 0.0 0.0 0.0 0.0 1.3 0.0 92.8 8.5 0.0 0.6 0.0 0.0 0.0 0.0 1.4 0.3 0.0
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Fig. 1. Mean daily catches of Illex and common hake on the Falkland shelf in 1999–2008.
3.3. Gonatus antarcticus Juveniles of this species were found occasionally in the diet of several fish species (Table 2) (0.03% of food items in total). Because of its small size, they passed through the trawl mesh and were not captured by any type of commercial fishing gear. 3.4. Onykia ingens The species was of small importance in food spectra of the fish species studied (mean 3.1% of food items). Catch statistics are not reliable because it is always discarded, and observers’ presence onboard fishing boats is occasional. 3.5. Martialia hyadesi Because of its rarity on the shelf and upper slope the species was rarely found in stomachs of common hake (both %N and %O <1) and was not recorded in the diet of any other fish. A total of 147 tonnes (<0.1% of the total catch) were captured by jiggers in the year 2001; during other years the annual catch was <1 tonne (all gears combined). 4. Discussion L. gahi, which is the only resident shelf squid species in Falkland Island waters, was found to be important in the diet of demersal fish, but not in species inhabiting water column, probably because of its benthopelagic life style. The only pelagic fish preying on L. gahi is the moonfish (Lampris immaculatus) which is a rare though specialised squid feeder (Jackson et al., 2000). This squid is consumed in large numbers by penguins being an important part of their diet (Croxall and Prince, 1996; Pütz et al., 2001; Clausen and Pütz, 2003; Clausen et al., 2005), as well as is preyed upon by seals and dolphins (Clarke, 1996; Klages, 1996; Schiavini et al., 1997; Otley, 2008) and by black-browed albatrosses Thalassarche melanophris that feed on discards from fishing boats (Thompson, 1992). I. argentinus was found in the diet of gentoo and king penguins (Cherel et al., 2002; Clausen and Pütz, 2003), and is common in sea lion and dolphin diet (Koen Alonso, 1999; Otley, 2008). However, it was almost not preyed upon by fish, neither demersal not pelagic. It is very different from its important role in trophic webs of the warmer Patagonian shelf, particularly as a food of common hake in which this squid represented >50% of annual food intake (Dawe and Brodziak, 1998). This discrepancy could be explained by the relative large size of maturing and mature I. argentinus on the Falkland shelf, but also by a temporal gap in the presence of both the predator and the prey (Fig. 1). Another specialised predator of I. argentinus
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in Argentinean waters is the dogfish, Squalus acanthias in which this squid represented >40% by prey weight and occurrence (Koen Alonso, 1999; Koen Alonso et al., 2002). However, this shark was found to feed mostly on animals of 13–18 cm ML (max. 22 cm), so the Falkland squids are likely to be too big for it. They are also too big for subadult Patagonian toothfish (35–70 cm TL on the shelf). The kingclip, an eel-like browser and scavenger, is probably too slow to catch I. argentinus, and the red cod is the only demersal fish to take advantage of I. argentinus seasonal immigrations to the Falklands. The large and abundant pelagic fish around the Falklands (hoki, blue whiting) occupy the same trophic level as I. argentinus and feed on euphausiids, Themisto gaudichaudi and myctophids (Brickle et al., 2009). Small to medium sized penguins feed intensively on epipelagic juvenile G. antarcticus. The total number of squids eaten during the breeding season by a single pair of magellanic (Spheniscus magellanicus), rockhopper (Eudyptes chrysocome chrysocome) and gentoo penguins (Pygoscelis papua) from colonies of Steeple Jason and New Island varied between 5000 and 13,000 animals. A total of 5000 tonnes of G. antarcticus are consumed annually by penguins in these two colonies only (Thompson, 1994). This squid occurred occasionally in the diet of larger king penguins Aptenodyptes patagonicus and that of sea lions Otaria flavescens (Thompson et al., 1998; Cherel et al., 2002). In contrast to this, this species was not commonly found in the diet of fish, even in the diet of pelagic planktivorous blue whiting and hoki (Brickle et al., 2009). However, in a small area southwest of the Falklands, hoki stomachs were found full of juvenile G. antarcticus during a summer 2010 trawl survey, which means that occasionally it could be consumed by this fish in numbers (Laptikhovsky and Brickle, personal observation). Two other pelagic squids O. ingens and M. hyadesi are also almost unexploited by the fish community. O. ingens was reported to be the main prey of the only one fish – the moonfish, L. immaculatus (Jackson et al., 2000), which is a quite rare species. However, its juveniles are intensively hunted by Gentoo penguins (Clausen et al., 2005). M. hyadesi occurred occasionally in the diet of king penguins (Cherel et al., 2002) – the only Falkland penguin species that forage in the oceanic waters beyond the shelf edge (Pütz and Cherel, 2005), and obviously squids were captured there. The reason of low importance of pelagic squid in the fish diet is that there are no abundant large epipelagic fish predators to feed on them. In contrast to this, all of these squid species are intensively exploited by penguins that occupy this ecological niche. The absence of competition with fish around the Falkland Islands, had possibly contributed to this area as an important penguin breeding grounds in the Southern Hemisphere. The Falkland Islands have the world’s largest breeding population of southern rockhopper penguins, and the second largest population of gentoo penguins (Croxall et al., 1984). The total breeding population of the different penguin species combined is about 750,000 birds (Huin, 2007), which is 585 adult penguins/km of the coastline. Once upon a time the Falkland Islands held an even larger penguin population: 3 million of rockhoppers (Pütz et al., 2001), so squid consumption by seabirds was much higher. The Falkland Islands’ shelf ecosystem is unique, because nektonic squids, though exclusively abundant all year round, are not important in fish diet, and the principal cephalopod consumers are birds. Generally, the importance of squids in the diet of the demersal fish communities is much lower worldwide. For example, cephalopods account for 0.66% of prey by number (3% by volume) in 27 fish species of the Gulf of Biscay, they occur in 2.2% of stomachs in 23 fish species of Northeast Atlantic from Scottish waters to the English Channel (Velasco et al., 2001; Daly et al., 2001), but cephalopod abundance there is also significantly lower than that of fish. Also, in other cold-water ecosystems, fish – not birds – are main cephalopod predators. In the Sea of Okhotsk, for example,
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fishes account for 66.7% of a total consumption of squids (Lapko, 1996). In polar ecosystems with high cephalopod abundance on the slope and low on the shelf, cetaceans (particularly sperm whales) could be the most important consumers of pelagic squids, like in Bering Sea (Radchenko, 1992). Such a “basement” position of squids as medium sized predators in the Falkland shelf ecosystem is understandable, because all of them prey on zooplankton when adult and subadult. The most important diet of the squids L. gahi (Guerra et al., 1991; Pineda et al., 1998; Brickle et al., 2001), I. argentinus (Ivanovic and Brunetti, 1994; Laptikhovsky, 2002) and subadult shelf O. ingens (Phillips et al., 2003) are swarming pelagic amphipod, T. gaudichaudi and Euphausiacea (Euphausia lucens, Euphausia vallentini and others). These prey (mostly T. gaudichaudi) represented >80% of planktonic crustaceans in catches by Isaacs – Kidd trawls above the bottom deeper than 70 m (our data), and waters of the Falkland Islands are another example of a sub-Antarctic amphipod-based food web, like that of Kerguelen Island (Bocher et al., 2001). The energy of zooplankton consumed by L. gahi largely remains within the Falkland shelf ecosystem. This squid does not emigrate and is consumed by a diverse demersal predatory fish community (as well as by penguins and marine mammals), though some of these fish emigrate seasonally, as well as large amounts of the squid are removed by fisheries for human consumption in the northern hemisphere. All of the nutrients assimilated on the shelf by pelagic squids are either transported northward (I. argentinus) or into deep seas (O. ingens and G. antarcticus). Because of this, the Falkland Islands shelf is an important source of biogenic elements for adjacent waters, and pelagic squids are principal exporters of this energy into other ecosystems. With the almost total absence of pelagic fish predators, such squid abundance is intensively exploited by humans and penguins that share this resource. Humans are specialised Illex and Loligo-hunters, whereas penguins target both Onykia and Gonatus. Both groups of seafood eaters do not compete so much for pelagic squid resources though they share the same interest for the benthopelagic L. gahi. It means that the largest of Falkland fisheries – jigging fishery for I. argentinus – probably has a positive impact on ecosystem production. There is no bycatch and the fishery removes a seasonal top-predator thus making available more food resources for turnover within the Falkland shelf. The trawl fishery targeting Loligo squid obviously takes some resources otherwise available for penguins. However taking into account a drastic decline in penguin numbers during the last two centuries (probably about five times) there is no evidence that this fishery can somehow limit the ecosystem carrying capacity for penguins. Acknowledgements The authors sincerely thank observers of the Falkland Islands Fisheries Department for sample collection and two anonymous reviewers for valuable comments. References Arkhipkin, A., Grzebielec, R., Sirota, A.M., Remeslo, A.V., Polishchuk, I.A., Middleton, D.A.J., 2004. The influence of seasonal environmental changes on ontogenetic migrations of the squid Loligo gahi on the Falkland shelf. Fish. Oceanogr. 13, 1–9. Bocher, P., Cherel, Y., Labat, J.-P., Mayzaud, P., Razouls, S., Jouventin, P., 2001. Amphipod-based food web: Themisto gaudichaudii caught in nets and by seabirds in Kerguelen waters, southern Indian Ocean. Mar. Ecol. Prog. Ser. 223, 261–276. Brickle, P., Olson, P.D., Littlewood, D.T.J., Bishop, A., Arkhipkin, A., 2001. Parasites of Loligo gahi from waters off the Falkland Islands with a phyllogenetically based identification of their cestode larvae. Can. J. Zool. 79, 2297–2302. Brickle, P., Arkhipkin, A.I., Laptikhovsky, V.V., Stocks, A., Taylor, A., 2009. Resource partitioning by two large planktivorous fishes Micromesistius australis and Macruronus magellanicus in the Southwest Atlantic. Estuar. Coast. Shelf. Sci. 89, 91–98.
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Squid as a resource shared by fish and humans on the Falkland Islands’ shelf Vladimir Laptikhovsky ∗ , Alexander Arkhipkin, Paul Brickle Falkland Islands Government Fisheries Department, P.O. Box 598, Stanley, FIQQ 1ZZ, Falkland Islands
a r t i c l e
i n f o
Article history: Received 24 February 2010 Received in revised form 9 April 2010 Accepted 5 May 2010 Keywords: Falkland Islands Fish Squid Feeding ecology Fishery
a b s t r a c t Nektonic squids are the dominant group in the Falklands Islands’ fishery representing >75% of the total annual catch. Among these squids, the benthopelagic Loligo gahi is an important link between zooplankton and fish in the shelf food web. It is preyed upon by diverse and numerous demersal and benthopelagic fishes, penguins and marine mammals, and is harvested by fishermen. Pelagic squids, Illex argentinus, Onykia ingens, and Gonatus antarcticus though seasonally very abundant, are scarce in fish diet because of the absence of specialised pelagic predators. This ecological niche is shared between humans (targeting Illex) and penguins (targeting Onykia and Gonatus). Martialia hyadesi though was abundant in some years in the past, it has now virtually disappeared from the shelf ecosystem. The biomass produced by L. gahi remains in the Falkland waters, whereas that of pelagic squid is transported out of the shelf either to the northern Patagonian slope (I. argentinus) or to deeper waters around the islands (O. ingens and G. antarcticus). Generally squids occupy the ecological niche of epipelagic fish on the Falkland shelf and slope. © 2010 Elsevier B.V. All rights reserved.
1. Introduction Nowadays aquaculture, freshwater and marine fisheries supply about 10% of world population calorie intake (Nellemann et al., 2009). A total of 80–90% of the human seafood harvest in the Atlantic, Pacific and Indian oceans is represented by fish (Table 1), and only 2–6% – by cephalopods (FAO, 2009), the rest being crustaceans, miscellaneous invertebrates, etc. The actual catch composition could be biased from this general rule in some ecosystems (Rodhouse and White, 1995), and an outstanding example of this is the shelf of the Falkland Islands (southern Southwest Atlantic). It is an important fishery area with annual catch of 101,000–427,000 tonnes (FIG, 2009) on the shelf and upper slope between 100 and 350 m. In contrast to other neighbouring regions, including the adjacent Patagonian shelf with nearly the same cephalopod and fish fauna, the bulk of the total catch around the Falklands (75.3% in 1989–2009, FIG, 2005, 2009) is represented by squids. It is the only region in the world where cephalopods predominate in the total annual catch. There are five common nektonic squid species recorded on the Falkland shelf (we do not take into account such rarities as Architeuthis dux or Pholidoteuthis boschmai). The two of them are abundant commercial species. Illex argentinus (Castellanos, 1960) is a seasonal immigrant of 20–35 cm ML, being on the shelf between February and June (Haimovici et al., 1998). Loligo gahi D’Orbigny,
∗ Corresponding author. Tel.: +500 27 260; fax: +500 27 265. E-mail address: vlaptikhovsky@fisheries.gov.fk (V. Laptikhovsky). 0165-7836/$ – see front matter © 2010 Elsevier B.V. All rights reserved. doi:10.1016/j.fishres.2010.05.002
1835 lives around the Falkland Islands all year round, grows to the size of about 20 cm ML (max. 42 cm ML), reproduces in inshore waters and migrates down to the upper slope for growth and maturation (Arkhipkin et al., 2004). Other nektonic squids that occur on the shelf and upper slope in numbers (at least in some years) are Gonatus antarcticus Lönnberg, 1898 (5–15 cm ML), Onykia ingens Smith, 1881 (5–35 cm ML) and Martialia hyadesi Rochebrune & Mabile 1889 (15–35 cm ML). Juvenile O. ingens and G. antarcticus annually occur on the shelf in spring–summer (Thompson, 1994; Jackson et al., 1998; Nesis, 1999), whereas M. hyadesi is abundant on the shelf in autumn only occasionally (FIG, 2005). None of three species is of commercial importance: G. antarcticus is too small, O. ingens is not edible. M. hyadesi is a potential commercial species in Antarctica, particularly at the Antarctic Polar Front (González and Rodhouse, 1998), but attempts to organise its fishery turned out to be disappointing. This species occurs on the Falkland shelf only in years with Falkland Current spreading over the shelf (Collins and Rodhouse, 2006) as in 1997. Recently it virtually disappeared from the ecosystem; a joint trawl survey of FVs “Castello” and “Beagle” in February 2010 did not yield any Martialia over the entire shelf and upper slope between 100 and 320 m around the islands (our data). In contrast to this, commercial shelf fish species are diverse in both taxonomic and ecological aspects and are represented by hakes Merluccius hubbsi Marini, 1933 and Merluccius australis (Hutton, 1882), hoki, Macruronus magellanicus Lönnberg, 1907, kingclip, Genypterus blacodes (Forster, 1801), blue whiting, Micromesistius australis Norman, 1937, subadult Patagonian toothfish, Dissostichus eleginoides Smitt, 1898, red cod, Salilota australis (Günther, 1878),
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Table 1 Catch composition of marine fisheries in different oceans in the year 2007, % (FAO, 2009). Ocean
Crustacean
Marine fish
Cephalopods
Gastropods and bivalves
Miscellaneous aquatic invertebrates
Atlantic Indian Pacific South
6.3 7.7 6.7 82.4
81.9 89.4 83.2 17.6
6.0 2.1 6.1 0.0
5.8 0.6 3.2 0.0
0.0 0.2 0.8 0.0
rays of the family Rajidae, and small sized notothenioids Patagonotothen spp. There is no direct estimation of biomass of every commercial fish and squid in this area and this task is next to impossible, because most of these species migrate seasonally to and from the Falkland waters. Because of the predominance of squid in the total annual catch (all gears combined), we may assume that cephalopods generally are much more abundant there than both teleost fish and elasmobranchs combined, and the Falkland waters are cephalopod based fishery ecosystem. This is particularly true for the south-eastern shelf, where some 80–90% of the total annual catch by trawlers is represented by the squid L. gahi. Because of the squid abundance around the Falklands it is possible to assume that they should be the key element in the marine food web, and this paper aims to investigate their importance in fish diet and assess the scale of possible impact of fisheries. 2. Materials and methods A total of 6531 fish specimens belonging to 20 commercial and non-commercial species were collected onboard various fishing vessels and during seven research bottom surveys by the R/V Dorada on the Falkland shelf between 30 and 400 m. Sample collection was carried out between June 1999 and April 2003, excluding that of the icefish, Champsocephalus esox that lasted until February 2007. Fish were measured to the nearest 1 cm (pre-anal length, PL, in hoki; disk width, DW, in rays; and total length, TL in all other species), then dissected and analysed onboard or in the Falkland Islands Government Fisheries Department laboratory. Only markedly digested items were taken into account, net feeding was ignored. A total of 109,523 prey items were identified to the lower possible taxonomic level, including 3493 squids. The percentage of occurrence
(%O) and percentage by number (%N) of each nektonic squid species were calculated (Cortés, 1997). 3. Results All squids combined represented a total of 14.9% of prey items in fish stomachs, and mean 69.1% of the total annual catch during the sampling period. 3.1. Loligo gahi This species was a common prey of a variety of fish from different ecological groups, and represented 10.7% of prey items (excluding planktivorous blue whiting and hoki). Among large benthopelagic predators, common hake was the principal consumer of L. gahi in winter (Table 2). Demersal fish consumed an important amount of this squid, it accounted for about a quarter of the diet in frogmouth (Cottoperca gobio) and about 10–15% of that in sharks and rays and subadult Patagonian toothfish (D. eleginoides). This species represented 9.2–23.5% (mean 19.2%) of the total catch of all commercial and non-commercial species during the period of sample collection (FIG, 2009). 3.2. Illex argentinus This species was found to play an important role in the red cod diet, and occurred occasionally in the diet of common hake and kingclip (Table 2). However, it was almost not used by other predatory fish and represented 1.1% of food items. In contrast to this, I. argentinus accounted for 13.2–70.6% (mean 49.9%) of the total catch during the period of sampling.
Table 2 Occurrence of nektonic squids in stomachs of predatory fish. Predator
Ecological group
Amblyraja doellojuradoi Bathyraja albomaculata Bathyraja brachiurops Bathyraja griseocauda Bathyraja scaphiops Champsocephalus esox Cottoperca gobio Dissostichus eleginoides Genypterus blacodes Lampris immaculatusa Macruronus magellanicus Merluccius australis Merluccius hubbsib Micromesistius australis Patagonotothen guntheri Patagonotothen ramsayi Patagonotothen tesselata Salilota australis Schroederichthys bivius Squalus acanthias
Demersal Demersal Demersal Demersal Demersal Benthopelagic Demersal Benthopelagic Demersal Pelagic Pelagic Benthopelagic Benthopelagic Pelagic Benthopelagic Benthopelagic Benthopelagic Demersal Demersal Benthopelagic
a b
Fish size (cm)
7–41 8–50 8–87 9–130 21–57 12.5–37 11–80 26–84 33–134 72–142 14–47 64–84 44–88 10–61 11–23 10–37 12–35 14–84 20–81 44–98
Number of stomachs
26 201 198 154 37 235 357 610 496 69 492 20 357 922 35 394 265 574 564 525
Data from Jackson et al. (2000). June–August, the period of mass hake immigration to the Falkland shelf.
Number of food items
209 1494 981 958 169 332 535 847 1551 1370 11,763 25 1328 75,905 58 1499 293 7602 1217 1387
Loligo
Illex
Gonatus
Moroteuthis
%N
%O
%N
%O
%N
%O
%N
%O
3.4 5.4 8.1 2.1 2.4 0.0 22.2 17.2 2.8 22.6 0.2 4.0 43.3 0.2 0.0 0.9 0.0 9.5 9.6 8.1
19.2 11.4 20.2 9.1 10.8 0.0 26.3 17.7 4.6 23.2 4.1 5.0 89.4 1.0 0.0 3.3 0.0 12.7 26.9 16.0
0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.9 0.0 0.0 0.0 0.2 0.0 0.0 0.0 0.0 2.7 0.7 0.0
0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 1.6 0.0 0.0 0.0 0.6 0.0 0.0 0.0 0.0 10.5 1.4 0.0
0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.0 0.0 <0.1 0.0 0.0 0.0 <0.1 0.0 0.4
0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 1.4 0.0 0.0 0.0 <0.1 0.0 0.0 0.0 <0.1 0.0 0.4
0.5 0.0 0.0 0.0 0.0 0.0 0.0 0.9 0.0 47.0 0.5 0.0 0.2 0.0 0.0 0.0 0.0 0.1 0.7 0.0
3.8 0.0 0.0 0.0 0.0 0.0 0.0 1.3 0.0 92.8 8.5 0.0 0.6 0.0 0.0 0.0 0.0 1.4 0.3 0.0
V. Laptikhovsky et al. / Fisheries Research 106 (2010) 151–155
Fig. 1. Mean daily catches of Illex and common hake on the Falkland shelf in 1999–2008.
3.3. Gonatus antarcticus Juveniles of this species were found occasionally in the diet of several fish species (Table 2) (0.03% of food items in total). Because of its small size, they passed through the trawl mesh and were not captured by any type of commercial fishing gear. 3.4. Onykia ingens The species was of small importance in food spectra of the fish species studied (mean 3.1% of food items). Catch statistics are not reliable because it is always discarded, and observers’ presence onboard fishing boats is occasional. 3.5. Martialia hyadesi Because of its rarity on the shelf and upper slope the species was rarely found in stomachs of common hake (both %N and %O <1) and was not recorded in the diet of any other fish. A total of 147 tonnes (<0.1% of the total catch) were captured by jiggers in the year 2001; during other years the annual catch was <1 tonne (all gears combined). 4. Discussion L. gahi, which is the only resident shelf squid species in Falkland Island waters, was found to be important in the diet of demersal fish, but not in species inhabiting water column, probably because of its benthopelagic life style. The only pelagic fish preying on L. gahi is the moonfish (Lampris immaculatus) which is a rare though specialised squid feeder (Jackson et al., 2000). This squid is consumed in large numbers by penguins being an important part of their diet (Croxall and Prince, 1996; Pütz et al., 2001; Clausen and Pütz, 2003; Clausen et al., 2005), as well as is preyed upon by seals and dolphins (Clarke, 1996; Klages, 1996; Schiavini et al., 1997; Otley, 2008) and by black-browed albatrosses Thalassarche melanophris that feed on discards from fishing boats (Thompson, 1992). I. argentinus was found in the diet of gentoo and king penguins (Cherel et al., 2002; Clausen and Pütz, 2003), and is common in sea lion and dolphin diet (Koen Alonso, 1999; Otley, 2008). However, it was almost not preyed upon by fish, neither demersal not pelagic. It is very different from its important role in trophic webs of the warmer Patagonian shelf, particularly as a food of common hake in which this squid represented >50% of annual food intake (Dawe and Brodziak, 1998). This discrepancy could be explained by the relative large size of maturing and mature I. argentinus on the Falkland shelf, but also by a temporal gap in the presence of both the predator and the prey (Fig. 1). Another specialised predator of I. argentinus
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in Argentinean waters is the dogfish, Squalus acanthias in which this squid represented >40% by prey weight and occurrence (Koen Alonso, 1999; Koen Alonso et al., 2002). However, this shark was found to feed mostly on animals of 13–18 cm ML (max. 22 cm), so the Falkland squids are likely to be too big for it. They are also too big for subadult Patagonian toothfish (35–70 cm TL on the shelf). The kingclip, an eel-like browser and scavenger, is probably too slow to catch I. argentinus, and the red cod is the only demersal fish to take advantage of I. argentinus seasonal immigrations to the Falklands. The large and abundant pelagic fish around the Falklands (hoki, blue whiting) occupy the same trophic level as I. argentinus and feed on euphausiids, Themisto gaudichaudi and myctophids (Brickle et al., 2009). Small to medium sized penguins feed intensively on epipelagic juvenile G. antarcticus. The total number of squids eaten during the breeding season by a single pair of magellanic (Spheniscus magellanicus), rockhopper (Eudyptes chrysocome chrysocome) and gentoo penguins (Pygoscelis papua) from colonies of Steeple Jason and New Island varied between 5000 and 13,000 animals. A total of 5000 tonnes of G. antarcticus are consumed annually by penguins in these two colonies only (Thompson, 1994). This squid occurred occasionally in the diet of larger king penguins Aptenodyptes patagonicus and that of sea lions Otaria flavescens (Thompson et al., 1998; Cherel et al., 2002). In contrast to this, this species was not commonly found in the diet of fish, even in the diet of pelagic planktivorous blue whiting and hoki (Brickle et al., 2009). However, in a small area southwest of the Falklands, hoki stomachs were found full of juvenile G. antarcticus during a summer 2010 trawl survey, which means that occasionally it could be consumed by this fish in numbers (Laptikhovsky and Brickle, personal observation). Two other pelagic squids O. ingens and M. hyadesi are also almost unexploited by the fish community. O. ingens was reported to be the main prey of the only one fish – the moonfish, L. immaculatus (Jackson et al., 2000), which is a quite rare species. However, its juveniles are intensively hunted by Gentoo penguins (Clausen et al., 2005). M. hyadesi occurred occasionally in the diet of king penguins (Cherel et al., 2002) – the only Falkland penguin species that forage in the oceanic waters beyond the shelf edge (Pütz and Cherel, 2005), and obviously squids were captured there. The reason of low importance of pelagic squid in the fish diet is that there are no abundant large epipelagic fish predators to feed on them. In contrast to this, all of these squid species are intensively exploited by penguins that occupy this ecological niche. The absence of competition with fish around the Falkland Islands, had possibly contributed to this area as an important penguin breeding grounds in the Southern Hemisphere. The Falkland Islands have the world’s largest breeding population of southern rockhopper penguins, and the second largest population of gentoo penguins (Croxall et al., 1984). The total breeding population of the different penguin species combined is about 750,000 birds (Huin, 2007), which is 585 adult penguins/km of the coastline. Once upon a time the Falkland Islands held an even larger penguin population: 3 million of rockhoppers (Pütz et al., 2001), so squid consumption by seabirds was much higher. The Falkland Islands’ shelf ecosystem is unique, because nektonic squids, though exclusively abundant all year round, are not important in fish diet, and the principal cephalopod consumers are birds. Generally, the importance of squids in the diet of the demersal fish communities is much lower worldwide. For example, cephalopods account for 0.66% of prey by number (3% by volume) in 27 fish species of the Gulf of Biscay, they occur in 2.2% of stomachs in 23 fish species of Northeast Atlantic from Scottish waters to the English Channel (Velasco et al., 2001; Daly et al., 2001), but cephalopod abundance there is also significantly lower than that of fish. Also, in other cold-water ecosystems, fish – not birds – are main cephalopod predators. In the Sea of Okhotsk, for example,
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fishes account for 66.7% of a total consumption of squids (Lapko, 1996). In polar ecosystems with high cephalopod abundance on the slope and low on the shelf, cetaceans (particularly sperm whales) could be the most important consumers of pelagic squids, like in Bering Sea (Radchenko, 1992). Such a “basement” position of squids as medium sized predators in the Falkland shelf ecosystem is understandable, because all of them prey on zooplankton when adult and subadult. The most important diet of the squids L. gahi (Guerra et al., 1991; Pineda et al., 1998; Brickle et al., 2001), I. argentinus (Ivanovic and Brunetti, 1994; Laptikhovsky, 2002) and subadult shelf O. ingens (Phillips et al., 2003) are swarming pelagic amphipod, T. gaudichaudi and Euphausiacea (Euphausia lucens, Euphausia vallentini and others). These prey (mostly T. gaudichaudi) represented >80% of planktonic crustaceans in catches by Isaacs – Kidd trawls above the bottom deeper than 70 m (our data), and waters of the Falkland Islands are another example of a sub-Antarctic amphipod-based food web, like that of Kerguelen Island (Bocher et al., 2001). The energy of zooplankton consumed by L. gahi largely remains within the Falkland shelf ecosystem. This squid does not emigrate and is consumed by a diverse demersal predatory fish community (as well as by penguins and marine mammals), though some of these fish emigrate seasonally, as well as large amounts of the squid are removed by fisheries for human consumption in the northern hemisphere. All of the nutrients assimilated on the shelf by pelagic squids are either transported northward (I. argentinus) or into deep seas (O. ingens and G. antarcticus). Because of this, the Falkland Islands shelf is an important source of biogenic elements for adjacent waters, and pelagic squids are principal exporters of this energy into other ecosystems. With the almost total absence of pelagic fish predators, such squid abundance is intensively exploited by humans and penguins that share this resource. Humans are specialised Illex and Loligo-hunters, whereas penguins target both Onykia and Gonatus. Both groups of seafood eaters do not compete so much for pelagic squid resources though they share the same interest for the benthopelagic L. gahi. It means that the largest of Falkland fisheries – jigging fishery for I. argentinus – probably has a positive impact on ecosystem production. There is no bycatch and the fishery removes a seasonal top-predator thus making available more food resources for turnover within the Falkland shelf. The trawl fishery targeting Loligo squid obviously takes some resources otherwise available for penguins. However taking into account a drastic decline in penguin numbers during the last two centuries (probably about five times) there is no evidence that this fishery can somehow limit the ecosystem carrying capacity for penguins. Acknowledgements The authors sincerely thank observers of the Falkland Islands Fisheries Department for sample collection and two anonymous reviewers for valuable comments. References Arkhipkin, A., Grzebielec, R., Sirota, A.M., Remeslo, A.V., Polishchuk, I.A., Middleton, D.A.J., 2004. The influence of seasonal environmental changes on ontogenetic migrations of the squid Loligo gahi on the Falkland shelf. Fish. Oceanogr. 13, 1–9. Bocher, P., Cherel, Y., Labat, J.-P., Mayzaud, P., Razouls, S., Jouventin, P., 2001. Amphipod-based food web: Themisto gaudichaudii caught in nets and by seabirds in Kerguelen waters, southern Indian Ocean. Mar. Ecol. Prog. Ser. 223, 261–276. Brickle, P., Olson, P.D., Littlewood, D.T.J., Bishop, A., Arkhipkin, A., 2001. Parasites of Loligo gahi from waters off the Falkland Islands with a phyllogenetically based identification of their cestode larvae. Can. J. Zool. 79, 2297–2302. Brickle, P., Arkhipkin, A.I., Laptikhovsky, V.V., Stocks, A., Taylor, A., 2009. Resource partitioning by two large planktivorous fishes Micromesistius australis and Macruronus magellanicus in the Southwest Atlantic. Estuar. Coast. Shelf. Sci. 89, 91–98.
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