ICES Journal of Marine Science, 62: 116e122 (2005) doi:10.1016/j.icesjms.2004.09.004
Short communication Food and feeding ecology of juvenile albacore, Thunnus alalunga, off the Bay of Biscay: a case study C. Pusineri, Y. Vasseur, S. Hassani, L. Meynier, J. Spitz, and V. Ridoux Pusineri, C., Vasseur, Y., Hassani, S., Meynier, L., Spitz, J., and Ridoux, V. 2005. Food and feeding ecology of juvenile albacore, Thunnus alalunga, off the Bay of Biscay: a case study. e ICES Journal of Marine Science, 62: 116e122. Although immature albacore tuna, Thunnus alalunga, are of economic and social importance in the Bay of Biscay, little is known about their diet and feeding ecology there. For this study, the diet of 78 albacore caught in the French driftnet fishery during summer 1993 is analysed. Fish dominated the diet in terms of relative abundance (86%N), and reconstituted mass (60%M), the most important being Maurolicus muelleri (79%N, 23%M), Scomberesox saurus (2%N, 30%M), and Arctozenus risso (4%N, 4%M). Crustaceans were also important in the diet (12%N, 2%M), but given their small size, it is questionable whether they were primary or secondary prey. Foraging on cephalopods seemingly took place only occasionally: they represented 2%N and 39%M of the total diet, but were absent from the fresh fraction of stomach contents. Prey sizes ranged from 6 to 228 mm. Juvenile albacore consume either epipelagic prey by day, or vertically migrating mesopelagic species that reach the surface layer by night. Ó 2004 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved.
Keywords: albacore, Bay of Biscay, diet, feeding ecology, Northeast Atlantic, Thunnus alalunga. Received 11 June 2004; accepted 9 September 2004. C. Pusineri, Y. Vasseur, and V. Ridoux: Laboratoire de Biologie et Environnements Marins, FRE 2727, Universite´ de La Rochelle (ULR), 17000 La Rochelle, France. S. Hassani: Laboratoire d’Etude des Mammife`re Marins, Oce´anopolis, 29200 Brest, France. L. Meynier, and J. Spitz: Centre de Recherche sur les Mammife`res Marins (CRMM), Universite´ de La Rochelle, 17000 La Rochelle, France. Correspondence to V. Ridoux: tel: C33 05 46 44 99 10; fax: C33 05 46 44 99 45; e-mail:
[email protected].
Introduction Albacore (Thunnus alalunga) are oceanic in tropical and subtropical waters, and limited in their distribution in a coastward direction by continental slopes. In the Atlantic, three stocks are commonly recognized by ICCAT (2003; the International Commission for the Conservation of Atlantic Tunas): the northern and southern stocks, separated by latitude 5(N, and the Mediterranean stock. In the North Atlantic, adults are found mainly in tropical waters, and reproduce in the Sargasso Sea (Bard, 1981). They are 90e130 cm long and live for about 10 years. They have been reported to forage from epi- to upper mesopelagic waters, down to depths of 500 m (Saito et al., 1970; Grandperrin and Legrand, 1971; Bertrand et al., 2002). 1054-3139/$30.00
Immature fish 1e5 years old range from 40 to 90 cm long. They are supposed to be physiologically constrained to the upper 100 m of the water column and a temperature range of 15e20(C (Aloncle and Delaporte, 1973). Consequently, when sea surface temperature increases in summer, immature albacore migrate north to areas off the European coasts (Bard, 1981). There, from the beginning of June until the end of September, they are the target of major North Atlantic albacore fisheries (ICCAT, 2003): the Spanish and Portuguese trolling and live bait boat fisheries (10 905 t caught in 2002), and the French and Irish pelagic trawl fisheries (5390 t caught in 2002). Hence, the species is of particular economic and social importance in the area. However, quite surprisingly, few detailed and recent studies are currently available on the ecology of immature albacore
Ó 2004 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved.
Feeding ecology of juvenile albacore off the Bay of Biscay
117
Figure 1. Sampling locations off the Bay of Biscay.
off the coast of Europe. The purpose of the present study is both to analyse quantitatively the diet of these fish and to interpret the diet in terms of feeding ecology.
Material and methods During summer 1993, the stomach contents of 78 albacore were sampled as part of a study on the impact of the albacore driftnet fishery on small cetaceans (Goujon et al., 1993). The fish were caught off the Bay of Biscay between 10 and 25(W and 40 and 50(N (Figure 1). Albacore were caught at night in driftnets 2.5 km long and 20 m high. They ranged in size from 53 to 93 cm, corresponding to two dominant age classes: 50% were 2 years old (58e67 cm) and 44% 3 years old (68e80 cm; Bard, 1981). Sample analysis was aimed at describing the diet in terms of prey occurrence, relative abundance, reconstituted mass, and size distribution. The defrosted stomach contents were washed through a sieve of 0.2-mm mesh size, the diagnostic parts and fresh prey recovered and identified to the lowest taxonomic level using published guides
(Lagarde`re, 1971; Clarke, 1986; Ha¨rko¨nen, 1986) and our own reference collection. To minimize overestimation of prey resistant to digestion (e.g. cephalopod beaks: Bigg and Fawcett, 1985), each prey item was scored on a scale specific to the main prey type ( fish, cephalopods, crustaceans), according to their state of decomposition. This allowed us to determine, in addition to the classic total diet, a ‘‘fresh fraction’’ that better represents the composition of the ingested prey, irrespective of prey speciesspecific digestion rates (Pusineri et al., 2003). Diagnostic hard parts such as beaks, otoliths, and carapaces were measured with a digital vernier calliper (G0.02 mm), following standards (Clarke, 1986; Ha¨rko¨nen, 1986). A random subsample of up to 30 diagnostic hard parts per prey species per stomach sample was measured. Individual prey body length and mass were then calculated using relationships either in the literature (Perez-Ganderas, 1983; Clarke, 1986; Ha¨rko¨nen, 1986), or that were determined with measurements performed on specimens in our reference collection (CRMM, unpublished data). The occurrence of a given prey taxon was the number of stomachs in which the taxon was observed, and relative
118
Table 1. Diet composition of albacore (lengths are standard length for fish, mantle length for cephalopods, and total length without rostrum for crustaceans). Total composition (N Z 4 571, M Z 7 783.7 g) Composition by number
Total fish Cranchiidae Teuthowenia megalops Onychoteuthidae Ancistroteuthis lichtensteini Octopoteuthidae Octopoteuthis sp. Gonatidae Gonatus steenstrupi Total cephalopods Euphausiidae Meganyctyphanes norvegica Hyperiidae Themisto gaudichaudi Total crustaceans
%N
95% CI
10.0 52.0 4.0
0.8 4.0 0.0
48.0
Mass ( g) Mean G s.d.
Composition by mass
Mean G s.d.
Range
n
% Occurrence
%N
%M reconstituted
0.2e1.9 2.3e7.2 0e0.1
109 G 59 94 G 36 136 G 31
16e224 14e204 104e169
67 173 4
3.6 G 5.5 1.5 G 1.6 3.5 G 2.0
!0.1e18.6 !0.1e12.8 1.5e5.73
3.0 4.1 0.1
0e9.3 1.8e7.5 0.0e0.3
11.9 59.5 4.8
1.5 7.4 0.1
9.1 11.8 0.3
2.1
1.2e3.9
177 G 23
119e221
129
21.2 G 4.9
11.4e32.2
29.9
16.2e45.1
28.6
2.0
45.3
2.0
!0.1
0e0.1
25 G 0
25e25
1
0.7 G 0.0
e
!0.1
0.0
2.0
!0.1
!0.1
46.0
78.5
62.7e90.5
38 G 8
12e62
506
0.4 G 0.2
!0.1e1.6
22.6
12.7e35.6
52.4
64.5
29.1
92.2
85.5
80.4
75.5
95.6
4.0
!0.1
0e0.1
12.0
0.2
0e0.4
58 G 34
2.0
0.4
0e1.7
4G1
20.0
2.0
0.5e3.3
29.4
2.1
4.0
7.3
0e19.6
32 G 1
30e33
11
0.3 G 0.04
18.0
5.1
0.8e14
13 G 3
7e18
30
!0.1
17.6
12.4
Range
%M reconstituted
95% CI
59.7
129 G 0
57 G 21
129e129
1
24.4 G 0.0
24.4e24.4
0.3
0.0e11.0
0.0
0.0
0.0
24e128
7
8.5 G 9.8
1.1e30.2
0.8
0.1e1.8
0.0
0.0
0.0
3e8
19
9.9 G 2.5
6.2e18.5
2.7
0.0e10.4
0.0
0.0
0.0
9e108
68
39.5 G 27.6
3.8e129.6
35.0
14.3e51.7
0.0
0.0
0.0
0.0
0.0
0.0
38.8
0.2e0.3
1.3
0.0e4.5
4.8
14.4
3.9
!0.1e0.1
0.2
0.0e0.4
21.4
10.1
0.5
17.6
24.5
4.4
1.5
C. Pusineri et al.
Paralepididae Paralepididae sp. Arctozenus risso Macroparalepis affinis Scomberesocidae Scomberesox saurus Myctophidae Benthosema glaciale Sternoptychidae Maurolicus muelleri
% Occurrence
Length (mm)
Fresh fraction (N Z 2 319, M Z 1 943.8 g)
50 45 40 35 30 25 20 15 10 5 0
%N
220-230
200-210
180-190
160-170
140-150
120-130
100-110
80-90
60-70
40-50
20-30
%M
0-10
Frequency (%)
Feeding ecology of juvenile albacore off the Bay of Biscay
Length class
Figure 2. Overall prey body length distribution in %N and %M of Northeast Atlantic albacore (length classes refer to standard length for fish, total length for cephalopods, and total length without rostrum for crustaceans).
abundance was denoted by the number of items of the same taxon found in the sample set. The reconstituted biomass of a taxon was the product of the number of individuals in each stomach and the subsample average reconstituted body mass, summed throughout the sample set. Each of these indices was calculated separately for the total content and the fresh fractions. Standard deviations for the compositions by number (%N) and mass (%M) were generated by bootstrapping (Reynolds and Aebischer, 1991). The bootstrapping routine was written using the R software (Ihaka and Gentleman, 1996). Random samples were drawn with replacement, and the procedure was repeated 300 times.
Results The analyses were based on the 51 non-empty stomachs. In all, 4571 prey items were identified (Table 1), among which were 3906 fish, belonging to six species and four families, 96 cephalopods, corresponding to four species and four families, and 569 crustaceans, which belonged to two species and two families. The stomach contents analysed weighed 34 G 47 g on average, and the mean reconstituted prey biomass was 142 G 155 g per tuna. Albacore diet was mainly fish, 86%N and 60%M of the total diet, but 76%N and 96%M of the fresh fraction (Table 1). Maurolicus muelleri, Scomberesox saurus, and Arcozenus risso were the most significant fish prey by number (79%, 2%, and 4%, respectively) and mass (23%, 30%, and 4%, respectively). Cephalopods, exclusively observed in digested states, accounted for 2% by number and 39% by mass of the total diet, but were totally absent from the fresh fraction. Gonatus steenstrupi was the most important in terms of occurrence (20%), abundance (2%), and reconstituted mass (35%). Crustaceans, some euphausiids and hyperiids, comprised 12%N and 2%M of the total diet, and as much as 25%N and 4%M of the fresh fraction.
119
However, given their small size, it is questionable whether they were primary or secondary prey. Albacore fed on prey items 6e228 mm long (Figure 2). Within this overall prey size range, prey in the 30e50-mm size class were most abundant (75%N), whereas the size classes that contributed most to the composition by mass were 30e50 mm (19%M) and 120e170 mm (35%M). Confidence intervals (95% CI) around average %N and %M were calculated by bootstrapping, and are given for every prey taxon (Table 1). For the three main species, the width of this 95% CI was generally 11e19% around estimated %N and %M. This analysis confirms that M. muelleri is the dominant prey species by number, because its 95% CI does not overlap with any other prey species, and that M. muelleri, S. saurus, and G. steenstrupi are of similar importance in reconstituted mass in the total diet, because their 95% CIs largely overlap, even if the last is absent from the fresh fraction.
Discussion Assessment of the study The study was limited in time and space as a result of the characteristics of the commercial fishery: sampling took place at night from June to September 1993. As all albacore were caught in driftnets set at night, the quantities of prey preferentially caught nocturnally are likely to be overestimated. Sample size was smaller than usual in most studies of commercial fish species, but similar to standards in studies of other top predators. Moreover, uncertainty around average %N and %M, assessed by calculating 95% CIs from resampled data sets, was always lower than G19%. Finally, although we dealt with the problem of prey-specific digestion rates by considering separately the total diet composition and the composition of the fresh fraction, to date there is insufficient published experimental background on prey-specific transit and digestion times in tuna confidently to infer real diet from stomach content analysis. This issue is general to all dietary studies based on analysis of stomach contents of top predators (Jobling and Breiby, 1986; Pierce and Boyle, 1991; Santos et al., 2001). Despite these different sources of limitation, which are general to most studies of the diet of top marine predators, and because few detailed studies are currently available on the ecology of the immature albacore, the present work is deemed to provide additional qualitative and quantitative dietary data for a species of major commercial importance in the area.
Comparison with other studies For immature albacore in the Northeast Atlantic, only two quantitative works (Aloncle and Delaporte, 1973; Ortiz de Zarate, 1987) are available (Table 2). The Aloncle and Delaporte survey was more extensive in time and space than the present work, and therefore resulted in more prey
C. Pusineri et al.
120
Table 2. Comparison with other albacore diet studies. Quoted families were either found in this study, or one of the main taxa were found in at least one other paper. The letter P indicates prey observed, but not quantified. Diversity is the number of species identified for the corresponding taxon. An asterisk denotes a value outside the 95% CI calculated in the study. Aloncle and Delaporte, 1973; Bay of Biscay and Azores; 1968e1971
This study; Bay of Biscay; 1993; n Z 78 Taxon
Ortiz de Zarate, 1987; Bay of Biscay; 1986; n Z 97
Clemens and Iselin, 1962 ; Northeastern Pacific; 1955e1961
% Occurrence
%N
%M
% Occurrence
% Occurrence
%N
%M
Total fish Engraulidae Sternoptychidae Myctophidae Paralepididae Scomberesocidae Gadidae Carangidae Trichiuridae Scombridae Callionymidae Stromateidae Scorpaenidae Other fish
95.9 0 46.0 2.0 55.1 48.0 0 0 0 0 0 0 0 0
85.5 0 78.5 !0.1 4.8 2.1 0 0 0 0 0 0 0 0
63.9 0 20.3 !0.1 6.4 37.2 0 0 0 0 0 0 0 0
PPP 0 11.0 0 20.9 16.2 0 P 0 P 0 0 0 P
86.0 9.0 12.0 0 1.0 26.0 12.0 43.0 8.0 1 2.0 0 0 P
86.2 5.0 0.8* 0 !0.1* 12.0* 2.0 42.0 1.0 !0.1 P 0 0 5.0
38.7 2.0 1.9* 0 !0.1* 0.6* 4.6 28.0 1.0 0 !0.1 0 0 1.0
47.3 8.3 0.7* 0.5* 1.1* 1.2 0 3.5 0 !0.1 0 0.5 4.5 27.0
Total cephalopods Cranchiidae Onychoteuthidae Octopoteuthidae Gonatidae Loliginidae Sepiolidae
30.6 4.0 12.0 2.0 20.0 0 0
2.1 !0.1 0.2 0.4 2.0 0 0
34.8 0.3 0.7 2.4 31.4 0 0
P
6.0 0 0 0 0 P P
0.7 0 0 0 0* P P
0.2 0 0 0 0* P P
9.9 PP 0 0 0* 0 0
Total crustaceans Euphausiidae Hyperiidae
18.4 4.0 18.0
12.4 7.3 5.1
1.3 1.2 0.1
PP 26.1 23.5
67.0 32.0 54.0
11.5 6.2 5.3
57.1 25.7* 31.4*
42.8 36.7* 0
14.0
1.6
4.0
0.1
Other (tunicates, larvae, cnidarians, etc) Diversity Fish Cephalopods Crustaceans
6 4 2
11 P 4
species being identified. They found cephalopods essentially as highly digested remains (i.e. loose beaks), and did not consider that group further in their analysis. Likewise in the present work, cephalopods appeared as digested remains, and were absent from the fresh fraction. Among the other prey categories, the dominant fish and crustacean taxa were the same in both studies: paralepidids, the scomberesocid Scomberesox saurus, the sternoptychid Maurolicus muelleri, the euphausiid Meganyctyphanes norvegica, and hyperiids. The survey of Ortiz de Zarate (1987) took place in oceanic waters and over the continental shelf. She reported several typically neritic prey taxa: loliginids, sepiolids, callionymids, engraulids, gadoids, scombrids, and carangids. Apart from that, her
9 P 2
%N
44 O2 10
results were similar to ours in terms of diversity, proportions of fish, crustaceans and cephalopods, and composition of oceanic prey taxa ( paralepidids, Scomberesox saurus, Maurolicus muelleri). Although the diet of albacore in the Pacific (Clemens and Iselin, 1962) is very different from their diet observed in the Bay of Biscay, there are some similarities: cephalopods are of secondary importance, and all taxonomic families identified in the Bay of Biscay were also found in the Pacific.
Feeding ecology Considering that a fish of medium size is totally digested by a tuna in !24 h (Aloncle and Delaporte, 1973; transit time
Feeding ecology of juvenile albacore off the Bay of Biscay
22
23
24
1
Day 2
Night
21
3
Hyperiidae
M.norvegica
Paralepididae
S.saurus
M.muelleri
G.steenstrupi
A.lichtensteini
Fresh prey
Intermediate 2
Intermediate 1
Accumulated prey (cephalopod beaks and fish otoliths)
Driftnet active
4
20
Digestion state
121
19
5
18
6 7
17 8
16
Prey Cephalopods M. muelleri Paralepididae
15
9 14
13
12
11
10
Crustaceans S. saurus
Figure 3. Hypothetical foraging rhythm of albacore off the Bay of Biscay, as suggested from the digestion states of prey in the stomachs. The histograms show the digestion states of the prey, and the circular chart the hypothetical daily pattern of prey ingestion for each category.
assessed from the examination of stomach contents), and that the stomach contents reflect foraging activity before the tuna were caught in driftnets (set at about 21:00 and hauled at about 05:00), the digested condition of the prey (Figure 3) suggest a possible daily pattern in albacore food composition. Paralepidids are medium-sized fish, and were found mostly as accumulated items in the stomachs, suggesting that they were caught during the day. M. muelleri is a very small mesopelagic and vertically migrating fish, and is likely to be fully digested within just a few hours. It was found as accumulated material, suggesting that it was probably consumed during the evening and early night. S. saurus is a fairly large, by albacore prey standards, epipelagic fish, which was found in various stages of digestion, suggesting that it was preyed upon by the albacore both day and night. Crustaceans are vertically migrating mesopelagic macroplankters that are likely to be digested within just a few hours; they were always found as fresh remains, indicating that they were certainly eaten at night. Cephalopods were found either as fully digested beaks and partially digested specimens (beaks in buccal mass) of medium-sized, mesopelagic, vertically migrating species. Beaks resist digestion by top predators for long periods (Bigg and Fawcett, 1985). Hence, we suggest that the digested beaks corresponded to cephalopods caught prior to the day of sampling, whereas beaks still in the buccal mass corresponded to specimens taken by the albacore early in the evening when the mesopelagic fauna migrates towards the surface. To summarize, juvenile albacore seem to be active feeders, consuming mainly epipelagic prey such as paralepidids and S. saurus by day, and vertically migrating mesopelagic fish, such as M. muelleri, or cephalopods such as G. steenstrupi, in the evening. At night, foraging activity is likely reduced, and the species probably feeds on smaller organisms, still from the vertically migrating mesopelagic fauna: Themisto gaudichaudi and M. norvegica. The
catchability of the vertically migrating mesopelagic fauna by surface predators is not well understood. However, it seems that such fauna would tend to form large, dense shoals at depth during the day, move up to the surface fairly synchronously, still forming dense patches at dawn and early night, but would disperse in the surface layer at night as they themselves forage actively. According to this general scheme, such a resource would be out of reach of immature albacore by day, be more catchable at dawn and early night, and would be energetically less profitable at night.
Acknowledgements The work formed part of a large research programme on the role and the dietary preferences of small cetaceans and other pelagic top predators in the Bay of Biscay and adjacent Atlantic. Funding was provided by the national research project Chantier Golfe de Gascogne, Programme National d’Environnement Coˆtier. The identification of prey reference specimens was checked by Jean-Paul Lagarde`re (CREMA, L’Houmeau, France), Jean-Claude Que´ro (Muse´um d’Histoire Naturelle, La Rochelle, France), Yves Cherel (CNRS, Chize´, France), and Begon˜a Santos Vasquez (University of Aberdeen, Aberdeen, UK). Franc¸ois-Xavier Bard provided us with helpful comments at an early stage of the manuscript. Mrs Vignard improved the English. All offered their time and competence, and are gratefully acknowledged.
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