Interannual variations in cephalopod consumption ... - CSIRO Publishing

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Marine and Freshwater Research, 2007, 58, 1136–1143

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Interannual variations in cephalopod consumption by albatrosses at South Georgia: implications for future commercial exploitation of cephalopods J. C. XavierA,B,C , A. G. WoodA , P. G. RodhouseA and J. P. CroxallA A British

Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, CB3 OET, Cambridge, UK. B Centre of Marine Sciences (CCMAR), University of Algarve, Faculty of Marine and Environmental Sciences, Campus Gambelas, 8000-139 Faro, Portugal. C Corresponding author. Email: [email protected]

Abstract. Assessing the consumption of prey by predators in the marine environment is key to fisheries assessment and management. Although environmental and ecological variations can affect the consumption of certain prey by albatrosses interannually, this issue has not been addressed to date. In the present study, the interannual consumption of cephalopods by grey-headed and black-browed albatrosses was assessed while breeding at South Georgia between 1996 and 2000, by comparing consumption estimates from a reparameterised version of the South Georgia Seabird Impact Assessment (SGSIA) model. The reparameterised model showed that there are considerable interannual variations in cephalopod consumption in both albatross species, with the highest consumption occurring in 1996 (5787 tonnes; for black-browed albatrosses) and 1997 (11 627 tonnes; for grey-headed albatrosses), and the lowest in 2000 (2309 tonnes and 772 tonnes for grey-headed and black-browed albatrosses respectively). These interannual variations were linked to oceanographic conditions and changes in cephalopod abundance/availability to predators. The cephalopod species with the most commercial potential (Martialia hyadesi, Kondakovia longimana, Moroteuthis knipovitchi and Gonatus antarcticus) also showed considerable differences in their consumption by predators. Owing to the importance of these squid species in the diet of albatrosses, precautionary measures for future commercial exploitation are suggested. Additional keywords: Antarctic cephalopods, diet analysis, fisheries, trophic interactions.

Introduction Antarctic top predators provide a unique insight into the size of stock of numerous prey species, including cephalopods, in the Southern Ocean. Indeed, top predators have been considered an excellent aid to the management and assessment of fisheries in the Antarctic (Rodhouse 1990). At present, estimates of prey consumption by predators have been made (e.g. Croxall et al. 1984; Rodhouse 1990) but no studies have included interannual variability of prey consumption, nor have they assessed how that could affect fisheries assessment and management. In Antarctic Ocean waters, most exploitation of natural resources has focussed on seals (18th and 19th centuries), whales (until the mid 20th century) and more recently fish (marbled rockcod Notothenia rossii, the mackerel icefish Champsocephalus gunnari, the Patagonia toothfish Dissostichus eleginoides) and Antarctic krill Euphausia superba (Kock 1992; Everson 2000). Of these, krill and the latter two fish species are still exploited under strict regulations set by the Commission for the Conservation of Antarctic Marine Living Resources (CCAMLR). Consequently there is a need not only to assess and manage the species that are already being targeted commercially, but also species that have the potential to be targeted in the future, such as cephalopods. © CSIRO 2007

Although the Southern Ocean contains large stocks of cephalopods, these have never been exploited commercially other than on an exploratory basis (González and Rodhouse 1998). Within the Scotia Sea (which includes South Georgia) in the Atlantic Sector of the Southern Ocean, the total annual cephalopod consumption by predators is estimated to be 3.7 million tonnes (Croxall et al. 1985). Among cephalopod species known to occur in Antarctic waters, the ommastrephid squid Martialia hyadesi is the most likely candidate for future commercial exploitation (Rodhouse et al. 1993). Indeed, M. hyadesi is very abundant in the diet of top predators and exploratory fishing surveys in certain years (Rodhouse 1990). Other cephalopods that may have commercial value include Kondakovia longimana, Moroteuthis knipovitchi and Gonatus antarcticus (Rodhouse 1990). Cephalopods of the Southern Ocean are poorly understood owing to the small number of scientific cruises devoted to their collection and the difficulty in sampling active squids (Cherel et al. 2004); most individuals caught are at larval or juvenile stages and adults are rarely sampled (Rodhouse 1990; Cherel and Weimerskirch 1999). Estimates of the consumption of cephalopods by seabirds are among the most reliable data on natural predation of these 10.1071/MF06237

1323-1650/07/121136

Cephalopod consumption by albatrosses at South Georgia

Marine and Freshwater Research

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Table 1. Values for key parameters in the original and our reparameterised the South Georgia Seabird Impact Assessment (SGSIA) model runs Model parameter Number of years in an activity cycle Number of breeding attempts Initial population (pairs) Day number (from 1 Sep.) at egg laying Egg loss rate Day number (from 1 Sep.) at egg hatching Chick loss rate Day number (from 1 Sep.) at fledging Chick feed size (g) Chick feed frequency (per adult, per day) Flight speed (m s−1 ) Flight zigzag factor Foraging range (km) Proportion of foraging trip spent on water

molluscs in the Antarctic (Rodhouse 1997). Squid are an important food for grey-headed Thalassarche chrysostoma and blackbrowed Thalassarche melanophrys albatrosses breeding at Bird Island, South Georgia (54◦ S, 38◦W) (Prince and Morgan 1987; Croxall and Prince 1996; Croxall et al. 1999; Xavier et al. 2003a, 2005; Xavier and Croxall 2007). Croxall et al. (1984, 1985) provided an estimate of food consumption by these seabirds for South Georgia waters according to the nature and timing of breeding activities (incubating, brooding or chick-rearing); the model included parameters such as arrival date of the birds to Bird Island, laying date, share of incubation duties, hatching date, duration of brooding and fledging date. Since the timing and duration of activities were determined by the ‘input specification’(i.e. data were estimated for each day) of the annual cycle, the energy consumption by birds of each sex on each day of the year was calculated. This was converted to food consumption using the known diet composition and energy content of prey, and assuming an assimilation efficiency of 75% (Croxall et al. 1985). Only breeding albatrosses were included in the model and black-browed albatrosses were assumed to leave the region immediately after their chicks fledged. Croxall et al. (1984) estimated 7.8 million tonnes of prey were consumed each year by breeding seabirds at South Georgia (including albatrosses, penguins, petrels, prions, terns and shags) of which 73% was krill, 13% copepods, 6% squid, 5% fish and 3% amphipods. Greyheaded and black-browed albatrosses consumed 20.6 (4.4% of the total squid consumed by seabirds) and 4.6 (0.9%) thousand tones of squid respectively. Within other seabird species, the white-chinned petrel Procellaria aequinoctialis consumed more squid; 365.8 thousand tonnes (78.5% of the total squid consumed by seabirds). Black-browed, and particularly greyheaded, albatrosses are sensitive to the availability of squid in South Georgia waters; if M. hyadesi are not present in Antarctic waters, these albatrosses have a very low breeding success (Xavier et al. 2003a). The aims of the present study are to provide: (i) a revised estimate of consumption of Martialia hyadesi, Kondakovia longimana, Moroteuthis knipovitchi and Gonatus antarcticus by

Black-browed albatross

Grey-headed albatross

1 1

2 1 60 000

57 0.0057 125 0.004 241 570 0.415

49 0.0046 121 0.002 262 600 0.45 12.4

1.54 428 0.49

1.47 615 0.24

grey-headed and black-browed albatrosses in the period between hatching and fledging, by comparing the South Georgia Seabird Impact Assessment (SGSIA) model (Croxall et al. 1985) and a reparameterised version of the SGSIA model; and (ii) a discussion of the implications of our results for proposed precautionary measures to regulate commercial fishing of M. hyadesi. Material and methods The original SGSIA model and a reparameterised version were used to estimate the consumption of cephalopods, including Martialia hyadesi, Kondakovia longimana, Moroteuthis knipovitchi and Gonatus antarcticus by grey-headed and blackbrowed albatrosses at South Georgia. Both model runs used the same parameters (Table 1), but differ in values of diet components between years (see below; data used here was from food samples (i.e. stomach contents were from forced regurgitations, after one of the chicks had been fed by one of the parents)). Both models were run, following Croxall et al. (1985), for 5 years (1996–2000), and consumptions were estimated for all of the study period (Fig. 1). The time period of interest is between hatching and fledging of black-browed and grey-headed albatross chicks (Prince et al. 1994b), from February to May for each year. The original SGSIA model run estimated the overall cephalopod consumption by albatrosses, but did not allow for interannual variations in the diet of albatrosses (Croxall et al. 1985). Therefore, the proportion of M. hyadesi consumed by mass (in food samples) was considered constant between years: 91% and 76% of all cephalopods for grey-headed and blackbrowed albatrosses respectively (Rodhouse et al. 1993). For other squid species, the average contribution by mass was considered to be: K. longimana 32.1% and 39.2%, M. knipovitchi 3% and 10.4%, G. antarcticus 2% and 2.7% of the diets of grey-headed and black-browed albatrosses respectively (Xavier et al. 2003a). The reparameterised version of the SGSIA model used yearspecific values for diet components and meal sizes for both albatross species (Table 2). The diet component values were obtained from food samples collected from chicks between


J. C. Xavier et al.

Grey-headed albatross 8000

Black-browed albatross 8000

Martialia hyadesi

4000 2000 0

0

Kondakovia longimana Tonnes

Tonnes

2000

4000 2000 0 1000

Moroteuthis knipovitchi

800

Tonnes

Tonnes

Kondakovia longimana

6000

4000

600 400


800 600 400 200

200

0 300

Gonatus antarcticus Tonnes

0 300

4000 2000

6000

0 1000

Martialia hyadesi

6000 Tonnes

Tonnes

6000

Tonnes

1138

200

Gonatus antarcticus

200 100

100

0

0 1996 1997 1998 1999 2000

1996 1997 1998 1999 2000

Year

Year

Fig. 1. Estimation of squid consumption between hatching and fledging of grey-headed and black-browed albatrosses for each year breeding at Bird Island, South Georgia based on the original South Georgia Seabird Impact Assessment (SGSIA) model run (in dots) and a reparameterised version (in bars) between 1996 and 2000.

Table 2. Values (percentages) for albatross diet and meal size used in the reparameterised and in the original the South Georgia Seabird Impact Assessment (SGSIA) model runs (in brackets) Importance in weight (%) Year

Fish

Cephalopods

Crustaceans

Others

Meal size (g)

Grey-headed albatrosses 1996 25 (35) 1997 12 (35) 1998 21 (35) 1999 22 (35) 2000 19 (35)

60 (49) 75 (49) 53 (49) 68 (49) 17 (49)

15 (15) 6 (15) 15 (15) 9 (15) 61 (15)

0 (1) 7 (1) 11 (1) 1 (1) 3 (1)

615 (600) 781 (600) 721 (600) 760 (600) 640 (600)

Black-browed albatrosses 1996 21 (39) 1997 19 (39) 1998 32 (39) 1999 40 (39) 2000 23 (39)

49 (21) 47 (21) 26 (21) 25 (21) 7 (21)

30 (38) 31 (38) 31 (38) 34 (38) 63 (38)

1 (2) 3 (2) 11 (2) 1 (2) 7 (2)

571 (570) 571 (570) 571 (570) 571 (570) 571 (570)



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Table 3. Consumption of cephalopods with commercial potential, by weight (g), found in the diet of grey-headed and black-browed albatrosses at Bird Island, South Georgia (mean ± s.e.) Year

Number of food samples

Cephalopods per food sample (g)

All cephalopods Weight (g)

Martialia hyadesi %

Kondakovia longimana %

Moroteuthis knipovitchi %

Gonatus antarcticus %

Grey-headed albatrosses 1996 41 1997 40 1998 38 1999 40 2000 120 Mean

3300 3124 6369 11 349 4117 5652 ± 1537

135 314 124 952 242 026 453 973 494 059

60.1 55.8 9.4 61.6 7.7 38.9 ± 12.4

24.1 26.5 51.0 14.6 44.5 32.1 ± 6.8

0.7 2.9 2.2 5.3 4.0 3.0 ± 0.8

0.8 1.9 2.6 1.5 3.3 2.0 ± 0.4

Black-browed albatrosses 1996 20 1997 39 1998 46 1999 30 2000 120 Mean

1286 2585 1290 5511 1668 2468 ± 797

25 711 100 796 59 356 165 333 200 149

65.4 40.1 1.9 16.7 0.0 24.8 ± 12.4

3.4 41.0 60.5 30.9 60.0 39.2 ± 10.6

0.0 6.2 2.6 34.1 9.1 10.4 ± 6.1

2.7 0.9 2.6 2.5 4.7 2.7 ± 0.6

February and May in five consecutive years (1996–2000). The meal sizes for grey-headed albatrosses were based on 1996– 2000 data, whereas the meal size for black-browed albatrosses was obtained from an average value obtained from five consecutive years of data (Table 2) (Huin et al. 2000). The proportion of squid consumed by both albatross species between 1996 and 2000 was estimated from reconstructed mass (Table 3). The population sizes were not changed between models in order to facilitate comparison of model runs (Table 1). Therefore, the mean value of 60 000 pairs for grey-headed and black-browed albatrosses for South Georgia were used, based on the mean population estimations by Croxall et al. (1984). Results The consumption of cephalopods by grey-headed and blackbrowed albatrosses at South Georgia varied considerably between 1996 and 2000. For grey-headed albatrosses, the reparameterised model showed a higher consumption of total cephalopods in 1996 (8900 tonnes), 1997 (11 627 tonnes), 1998 (7842 tonnes) and 1999 (10 451 tonnes) in comparison with the original model run (1996–2000 was 7151 tonnes). In 2000, the consumption of cephalopods (estimated by the reparameterised model) decreased sharply to 2310 tonnes, approximately five times less than the previous year. The quantities of the cephalopod species with most commercial interest (Martialia hyadesi, Kondakovia longimana, Moroteuthis knipovitchi, and Gonatus antarcticus) consumed by grey-headed and black-browed albatrosses between 1996 and 2000 are shown in Table 3. Comparison between models The estimates of cephalopod consumption calculated using the original SGSIA model run (Croxall et al. 1985) and our reparameterised version are shown in Fig. 1. The original model run showed a constant consumption of each cephalopod species between years, whereas the reparameterised version

shows marked interannual variations. However, when those interannual variations are averaged for all years, there are no significant differences between the average cephalopod consumption values obtained from either model run for grey-headed (two sample Wilcoxon rank sum test, W = 17, P = 0.885) and black-browed albatrosses (two sample Wilcoxon rank sum test, W = 17, P = 0.885). For grey-headed albatrosses, the reparameterised version of the model estimated that the ommastrephid M. hyadesi was the most consumed cephalopod in 1996, 1997 and 1999, and the onychoteuthid K. longimana in 1998 and 2000. It showed M. hyadesi consumption to be lower than the original model run estimates (6507 tonnes) in all years: it increased from 1996 (5316 tonnes) to 1997 (6488 tonnes), decreased in 1998 (737 tonnes), increased again in 1999 (6443 tonnes) and finally decreased to 178 tonnes in 2000, the lowest value estimated for M. hyadesi. Kondakovia longimana consumption estimated by the reparameterised model showed higher values in 1997 and 1998 when compared with the original model run, whereas M. knipovitchi consumption estimates were higher in 1997 and 1999 (Fig. 1). Gonatus antarcticus consumption estimated by the reparameterised model showed higher values in 1997 (221 tonnes), 1998 (204 tonnes) and 1999 (157 tonnes) than the original results (143 tonnes). Results from generalised linear models (using data from the reparameterised model) showed that the consumption of the main cephalopod species did not differ between years (F4,3 = 1.07, P = 0.41) but it differed significantly between squid species (F4,3 = 5.75, P = 0.01). For black-browed albatrosses, the reparameterised model results showed that K. longimana was the most consumed cephalopod in 1997 and 1998, with M. hyadesi the most consumed cephalopod in 1996, and M. knipovitchi in 1999 (Fig. 1). Martialia hyadesi estimates from the reparameterised model showed higher values in 1996 (3784 tonnes) and 1997 (2235 tonnes) than the original results (1829 tonnes). Kondakovia longimana consumption estimates from the reparamaterised model showed higher values in 1997 (2285 tonnes) and 1998

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(1811 tonnes) than the original results (944 tonnes), whereas M. knipovitchi estimates were higher in 1997 (346 tonnes) and 1999 (986 tonnes) than the original results (250 tonnes). Gonatus antarcticus consumption estimates from the reparameterised model showed higher values in 1996 (156 tonnes) and 1998 (78 tonnes) than the original results (65 tonnes). Results from generalised linear models (using data from the reparameterised model) showed that the consumption of the main cephalopod species did not differ between years (F4,3 = 0.77, P = 0.57) nor between squid species (F4,3 = 1.91, P = 0.18). Prey consumption comparisons between albatross species According to the reparameterised model results, the consumption of cephalopods are not correlated between grey-headed and black-browed albatrosses, with the exception of M. knipovitchi (Pearson correlation = 0.97, P = 0.006). Martialia hyadesi was consumed more by grey-headed albatrosses (19 190 tonnes) than by black-browed albatrosses (6559 tonnes) as well as K. longimana (11 779 tonnes for grey-headed albatrosses and 5649 tonnes for black-browed albatrosses). Moroteuthis knipovitchi was consumed more by black-browed albatrosses (1479 tonnes) than by grey-headed albatrosses (1218 tonnes). Gonatus antarcticus was consumed more by grey-headed albatrosses (729 tonnes) than by black-browed albatrosses (328 tonnes). Discussion The reparameterised model results show that there were marked interannual variations in cephalopod consumption by both albatross species. These variations are important for understanding the underlying processes of predator–prey interactions, particularly the cephalopod ecology (Xavier and Croxall 2007). As there are no Antarctic squid fisheries, these interannual variations are caused by natural variability within the squid populations not from the effects of exploitation of the stocks. Moreover, for Martialia hyadesi, years of low consumption (and presumably low availability) had significant repercussions for albatross breeding performance; both grey-headed and black-browed albatrosses had very low breeding success in 1998 (1.4% and 1.6% of breeding success, respectively) and 2000 (16.8% and 24.0%) in comparison with the other years (1996: 52.4% and 40.7%; 1997: 63.3% and 33.1% and 1999: 45.4% and 41.2%) (Xavier et al. 2003a). As albatrosses are limited to feeding in the top 15 m of the ocean (Prince et al. 1994a), it is likely that they only take a relatively small proportion of the total cephalopods present (Rodhouse 1998). Despite this, the diets of albatrosses seem to be a very good indicator of the availability (and potentially abundance) of M. hyadesi around South Georgia waters (Xavier et al. 2003a). Generally, black-browed albatrosses tend to forage more in Antarctic waters (feeding mostly on krill, fish, and, to a lesser extent, squid) whereas grey-headed albatrosses forage further north, in theAntarctic Polar Frontal Zone (APFZ) waters, feeding mostly on M. hyadesi (Xavier et al. 2003a). When environmental changes occur in their foraging areas, food availability is affected. For example, when looking at air and water predators in 2000, M. hyadesi was almost absent in the diets of black-browed albatrosses, grey-headed albatrosses and Patagonian toothfish

J. C. Xavier et al.

Dissostichus eleginoides (one lower beak out of 178) (Xavier et al. 2002); D. eleginoides is a predator that feeds occasionally on M. hyadesi (only M. hyadesi beaks have been found in previous studies of the diet of D. eleginoides around South Georgia; P. Rodhouse, personal communication), which forages at the bottom and in bentho-pelagic waters. Also, as 2000 was oceanographically abnormal around South Georgia (Xavier et al. 2003c), it is likely that changes in availability/abundance and distributional patterns of prey, including squid like M. hyadesi, could have been attributed to oceanographic changes (Xavier et al. 2006), including the El Niño Southern Oscillation (ENSO) (Xavier et al. 2003a). Indeed, in certain years when both albatross species experienced poor breeding success, such as in 1998 (but not in 2000), there was a large ENSO event (Xavier et al. 2003a). Overall, changes in oceanographic conditions in 2000 caused low availability of M. hyadesi in the diet of D. eleginoides and in the diet of albatrosses. Predators of Martialia hyadesi, Kondakovia longimana, Moroteuthis knipovitchi and Gonatus antarcticus In order to understand the role of cephalopods in the Southern Ocean food web, it is imperative to assess their importance in the diet of predators. M. hyadesi, K. longimana, M. knipovitchi and G. antarcticus are known to be consumed by a wide range of predators, including whales, seals, penguins, albatrosses, petrels and fish in the south Atlantic sector of the Antarctic Ocean (Table 4). Martialia hyadesi is the most important cephalopod by estimated mass in the diet of king penguins (Aptenodytes patagonicus), macaroni penguins (Eudyptes chrysolophus), greyheaded and black-browed albatrosses (in most years) (Xavier et al. 2003a); K. longimana in the diet of elephant seals (Mirounga leonina), Antarctic fur seals (Arctocephalus gazella), Ross seals (Omatophoca rossii), emperor penguins (Aptenodytes forsteri), grey-headed and black-browed albatrosses (in some years), southern bottlenose whales (Hyperoodon planifrons), wandering albatrosses and patagonian toothfish. Moroteuthis knipovitchi was reported to be important, in terms of mass, in the diet of black-browed albatrosses in 1999. Gonatus antarcticus occurs in great numbers in the diet of rockhopper penguins (Eudyptes chrysocome), gentoo penguins (Pygoscelis papua) and magellanic penguins (Spheniscus magellanicus) breeding in the Falkland Islands (Table 4). Owing to the occurrence of these squid species in such a wide range of predator diets, the present study reinforces the need for a prior assessment of the potential impacts of a future commercial squid fishery in the Southern Ocean. Implications of the new data for proposed precautionary measures for a squid fishery around South Georgia Within the species with commercial interest, M. hyadesi has been the species that attracted more attention. Current precautionary measures for any new fishery for M. hyadesi in the Scotia Sea involves setting an annual TAC (total allowable catch) of no more than 10% (25 000 tonnes) of the most conservative estimate of predator consumption of this squid (Rodhouse 1997). However, such a measure may be unnecessarily cautious in years of high availability of M. hyadesi and, conversely, insufficient to prevent adverse effects in years of low availability to natural predators.



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Table 4. Predators of Antarctic squid with commercial potential for commercial exploitation from the south Atlantic waters The % by number and % mass are given for the cephalopod component of each predator diet in parenthesis

Whales Hyperoodon planifrons Globicephala malaena Physeter catodon Seals Mirounga leonina Arctocephalus gazella Arctocephalus tropicalis Leptonychotes weddelli Omatophoca rossii Hydrurga leptonyx Penguins Aptenodytes forsteri Aptenodytes patagonicus Eudyptes chrysolophus Eudyptes chrysocome Pygoscelis papua Spheniscus magellanicus Albatrosses Thallassarche chrysostoma Thallassarche melanophrys Diomedea exulans Phoebetria palpebrata Petrels Procellaria aequinoctialis Macronectes halli Macronectes giganteus Fish Lampris immaculatus Dissostichus eleginoides

Martialia hyadesi

Kondakovia longimana


Gonatus antarcticus

(0.8; 3)1

(2.5; 58.5)1

(0.5; 1.1)1

(16.7; 17.8)22

(21.7; 4)22

(8.7; 11)1 (0.8; 0.4)1 (3.1; 0.2)22

(13.4; 24)11 , (2.3; 2.7)12 (?; ∼50)14

(11.3; 31.2)11 , (1; 3.5)12

(6.3; 3.6)11 , (4; 3.5)12

(1.8; 1)15 (31.1; 48.5)23

(