BULLETIN OF MARINE SCIENCE, 71(2): 753–770, 2002
CEPHALOPODS IN THE TROPHIC RELATIONS OFF SOUTHERN BRAZIL
Roberta Aguiar dos Santos and Manuel Haimovici
ABSTRACT Trophic relations of cephalopods in southern Brazil were investigated from predation on cephalopods by 71 species of potential predators, including two squids, 47 fishes, seven seabirds and 15 marine mammals from shelf, upper slope and oceanic adjacent waters. In all, 27 families and 41 species of cephalopods were identified from stomach contents. The number of families ranged from six, in the diet of shelf predators, to 27 families in those from upper slope and adjacent oceanic waters. The most frequent cepha- lopod prey on the shelf was Loligo sanpaulensis, particularly important in the diet of Franciscana dolphin Pontoporia blainvillei, occurring also in the diet of the penguin Spheniscus magellanicus, the fur seals Arctocephalus australis, A. gazella, A. tropicalis, and several benthic and demersal fishes. Ommastrephidae, mainly Illex argentinus and Ornithoteuthis antillarum, was the most frequent family in the diet of predators from upper slope and adjacent oceanic waters. Illex argentinus was an important prey for the wreckfish Polyprion americanus, the bigeye tuna Thunnus obesus, the swordfish Xiphias gladius and some marine mammals, especially in their winter and spring northward re- productive migration. Ornithoteuthis antillarum was frequent in the diet of the skipjack tuna Katsuwonus pelamis, the albacore Thunnus alalunga, the yellowfin tuna T. albacares, the Atlantic sailfish Istiophorus albicans and the white marlin Tetrapturus albidus. Am- moniacal squids, such as Ancistrocheirus lesueurii, Histioteuthis spp, Chiroteuthis veranii and Octopoteuthis sp, were mainly found in stomach contents of the blue shark, Prionace glauca, the pygmy sperm whale Kogia breviceps, the dwarf sperm whale K. sima, the long-finned pilot whale, Globicephala melas and oceanic seabirds. The relative impor- tance, based on frequency of occurrence, of cephalopods as food resources seems to be higher in the food chains of the upper slope and adjacent oceanic waters, when compared to the continental shelf.
Cephalopods play an important role in the trophic relations of marine ecosystems. Many of them are active and efficient predators of a great variety of animals and also are prey of several marine species, mainly for those from oceanic waters, where the availability of food resources is lower than more productive regions, as continental shelves (Clarke, 1987, 1996a; Amaratunga, 1983). The cephalopods occupy several trophic levels and are considered to be mainly intermediaries in the energetic flux between the primary and secondary consumers and the predators of third and fourth level of the food webs. Due to their fast growth, the trophic interactions of muscular squids may be very complex, act- ing as predators, prey or competitor of some species of abundant fishes (Amaratunga, 1983; Angelescu and Prenski, 1987; Dawe and Brodziak, 1998). In the marine ecosystems, the cephalopods generally occupy the role of subdominant predators and their importance in the food webs can be assessed from their relative im- portance in the diet of potential predators (Clarke, 1987). Among their predators are a large number of fishes, seabirds and marine mammals, many of them of commercial importance. For some large predators as sperm whales, pilot whales and zifids, cephalo- pods are the main source of food (Clarke, 1986a, 1996b). Tunas, billfishes and some
753 754 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 2, 2002 pelagic sharks depends heavily on cephalopods (Smale, 1996), as well as several species of oceanic seabirds, as albatrosses and petrels (Croxall and Prince, 1996). Many cephalopods, especially those inhabiting continental slopes and oceanic waters are difficult to catch with the fishing gears used in these environments. The stomach content analysis of the dominant predators, many of them target of commercial fishing, are the main source of data to assess the abundance and distribution of cephalopods. The identification of cephalopods in the stomach contents is difficult because these inverte- brates are fleshy, easily digested, and with few structures that resist digestion. Usually beaks (or mandibles), eye lens, parts of gladius, sucker rings and hooks are the only remains found in the stomach contents. Among these hard structures, the chitinous beaks are the most useful for cephalopod identification due to their resistance to digestion and characteristic shape and pigmentation (Clarke, 1986b). In this paper, the presence of cephalopods in the diet of fishes and cephalopods from commercial landings, cruise surveys and stranded or incidentally caught seabirds and marine mammals was analyzed to investigate their relative importance in the trophic relations of southern Brazilian shelf and adjacent oceanic waters.
THE STUDY AREA
The shelf and slope along southern Brazil are located in the western boundary of the Subtropical Convergence. Between late autumn and early spring, the shelf is dominated by cold waters of the coastal branch of the Malvinas (Falklands) Current, flowing north- ward, and the discharge of La Plata River and Patos Lagoon. From late spring to early autumn, warm coastal waters under the influence of the southward flowing Brazil Cur- rent are dominant (Castello et al., 1997; Garcia, 1997). The shelf waters productivity can be considered moderate to high, with the mean annual particulate primary production rates around 160 g C m−2 yr−1 (Odebrecht and Garcia, 1997). Upwelling processes of Subtropical Waters are common on the shelf in spring and summer, due to the strong influence of NE winds. This region sustains a multispecific demersal trawl fishery that, between 1990 and 1994, yielded in mean 50,000 t yr−1, of which several species of the family Sciaenidae represented over 70% (Haimovici et al., 1997). The shelf cephalopod fauna of southern Brazil is relatively well known (Palacio, 1977; Juanicó, 1979; Haimovici and Perez, 1991). The continental slope and oceanic adjacent waters are strongly influenced by the olig- otrophic waters of Brazil Current. Especially in winter and spring, productivity may be increased along the shelf break associated to upwelling of the Subtropical Water due to frontal vortices of cyclonic circulation formed by the Brazil and Malvinas (Falklands) Currents (Castello et al., 1997; Garcia, 1997). The demersal fishery over the upper slope is undertaken mainly by bottom longliners for wreckfish (Polyprion americanus) that, in the early 90s, yielded around 2000 t yr−1 (Peres and Haimovici, 1998). In the outer shelf and upper slope, the skipjack tuna (Katsuwonus pelamis) is fished with live bait and yielded ca 3200 t yr−1 (1990–1994). Tunas, billfishes and pelagic sharks are fished by Brazilian longliners over the slope and oceanic adjacent waters (ca 3400 t yr−1 in 1990– 1994) (Haimovici et al., 1997). The cephalopod fauna of these environments is less known than the one of the shelf (Perez and Haimovici, 1993). SANTOS AND HAIMOVICI: CEPHALOPODS IN THE TROPHIC RELATIONS OFF BRAZIL 755
MATERIAL AND METHODS
The presence of cephalopods was investigated in the diet of 71 nektonic potential predators of southern Brazil (26°S–34°S), including seven species of seabirds and 15 of marine mammals found stranded along beaches or incidentally caught in the gillnet coastal fishery, 36 species of pelagic and demersal fishes and two squids caught along the shelf (<200 m) and upper slope (200–500 m) and 11 species of oceanic pelagic fishes caught with surface longliners in oceanic waters adjacent to the upper slope (>500 m) (Fig. 1). Most of data were obtained from stomachs collected between 1980 and 1998 and examined by the authors (Haimovici et al., 1989; Teixeira and Haimovici, 1989; Haimovici and Krug, 1992; Capitoli and Haimovici, 1993; Santos and Haimovici, 1997; 1998; in press; Santos, 1999). Part of the data were obtained from published papers, thesis and unpublished reports by other authors (Clarke et al., 1980; Lessa, 1982; Pinedo, 1982; Pinedo and Barros, 1983; Juras and Yamaguti, 1985; Queiroz, 1986; Pinedo, 1987; Rosas, 1989; Schwingel, 1991; Vaske, 1994; Vaske and Rincón, 1998). The cephalopods were retrieved in various stages of digestion, ranging from whole individuals, in few stomach contents, to the presence of only beaks, as most cases. To estimate the size compo- sition of the cephalopods found in the diet of predators, regression equations which relate mantle length (ML-mm) and total weight (TW-g) with the beak size were used (Clarke, 1986b; Santos, 1999). The rostral lengths of upper (URL) and lower (LRL) beaks of squids and sepiolids and hood lengths of upper (UHL) and lower (LHL) beaks of octopuses were measured in tenths of millime- ters, following Clarke (1986b). The numbers of squids per stomach were estimated from undi- gested specimens and upper or lower beaks, whichever were the most numerous. The relative importance of the cephalopods in the diet of their different predators was not easy to assess from the available data. For a considerable number of the predator species, particularly among marine mammals, birds and large pelagic fishes, the total number of stomach contents was known but not the number of weight of the other type of prey. Thus we were not able to estimate the importance of cephalopods in the diet in mass and the only information available for all the preda- tors examined by the authors and most of the consulted papers was the number of stomachs with each cephalopod species (Nc) in relation to the total number of stomachs with food (Nt). This quantity was referred as ‘frequency of occurrence’ (FO = Nc/Nt × 100) and used as a measure of relative importance. The scientific names of cephalopods followed Sweeney and Roper (1998), fishes Eschmeyer (1998), seabirds Vooren and Fernandes (1989) and marine mammals Rice (1998). Inferences on the diet of predators from stomach content analysis have inherent limitations. Oceanic seabirds could have fed on dead squids, mainly when referred to ammoniacal ones, that float when die, as well as these animals could eat remains of cephalopods taken out of cetacean regurgitation or fishery discards (Clarke et al., 1981; Lipinski and Jackson, 1989; Croxall and Prince, 1994). Seabirds, large pelagic fishes and marine mammals can have eaten their preys far from where they were caught or found stranded and the diet of unhealthy animals can differ of healthy ones. These limitations were taken into account as far as possible in the interpretation of the results.
RESULTS
Twenty seven families and at least 41 species of cephalopods (Table 1, Fig. 1) were identified in the stomach contents of the 71 species of predators investigated (Table 2). The species of cephalopods eaten by shelf fishes and Loligo sanpaulensis are listed in Figure 2, those preyed upon by upper slope and oceanic adjacent waters fishes and Illex 756 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 2, 2002
Table 1. Taxonomic list of cephalopod species found in the diet of several predators of southern Brazil.
Class Cephalopoda Family Histioteuthidae Subclass Coleoidea Histioteuthis sp. Orbigny, 1841 Seuperorder Decabrachia Family Neoteuthida Order Spirulida Alluroteuthis antarctica Odhner, 1923 Feamily Spirulidae Family Brachioteuthida Spirula spirula (Linnaeus, 1758) Brachioteuthis sp. Verrill, 1881 Oerder Sepiolida Family Ommastrephida Family Sepiolidae Illex argentinus (Castellanos, 1960) Semirossia tenera (Verrill, 1880) Todarodes filippovae Adam, 1975 Heteroteuthis dispar (üR ppell, 1844 ) Ommastrephes bartramii (Lesueur, 1821) Order Teuthida Ornithoteuthis antillarum Adam, 1957 Suborder Myopsina Hyaloteuthis pelagica (Bosc, 1802) Feamily Loliginidae Family Thysanoteuthida Loligo plei Blainville, 1823 Thysanoteuthis rhombus Troschel, 1857 Loligo sanpaulensis Berakoniecki, 1984 Family Chiroteuthida Suborder Oegopsina Chiroteuthis veranii (éF russac, 1835 ) Feamily Lycoteuthidae Family Mastigoteuthida Lycoteuthis lorigera (Steenstrup, 1875) Mastigoteuthis sp. Verrill, 1881 Feamily Enoploteuthidae Family Cranchiida Enoploteuthis sap. Orbigny, 1844 Superorder Octobrachi Abralia veranyi (Rüp)pel l,a1844 Order Octopodid Abralia redfieldi Vaoss, 1955 Suborder Incirrin Abraliopsis sep. Joubin, 1896 Family Bolitaenida Family Ancistrocheiridae Japetella diaphana Hoyle, 1885 Ancistrocheirus lesueurii (eOrbigny, 1842) Family Octopodida Family Pyroteuthidae Octopus vulgaris Cuvier, 1797 Pteryogioteuthis giardi Fischer, 1896 Octopus tehuelchus Orbigny, 1834
argentinus are in Figure 3 and those found in the stomach contents of different seabirds and marine mammals in Figure 4. Loliginid squids were the main cephalopods preyed on the shelf and among them L. sanpaulensis was by far the most important (Figs. 2,3,4). Small and large squids were found (Fig. 5), and were very frequent in the diet of Pontoporia blainvillei and relatively important for Spheniscus magellanicus, Arctocephalus australis, A. gazella and A. tropicalis. It occurred with FO over 5% in the stomach contents of benthic and demersal fishes as Mustelus canis, Astroscopus sexpinosus, Percophis brasilianus, Helicolenus dactylopterus lahillei, Paralichthys isosceles, P. patagonicus and Merluccius hubbsi. With a lower frequency (FO < 5%) in the diet of several pelagic and demersal shelf fishes, as Pomatomus saltatrix, Trichiurus lepturus, Cynoscion guatucupa, Macrodon ancylodon and Pagrus pagrus. L. sanpaulensis occurred also in the diet of predators from upper slope and oceanic waters. The other loliginid found was Loligo plei, in the diet of some shelf and upper slope predators, but with very lower frequency (Figs. 2,3,4). Ommastrephid squids were important in the diet of upper slope and oceanic adjacent water predators. I. argentinus was found in the diet of many marine mammals and pelagic and demersal fishes, being frequent in the stomach contents of Thunnus obesus, Xiphias gladius, Polyprion americanus, Globicephala melas and K. breviceps. Although small individuals (< 100 mm ML) had been found, most of its predators fed on mature or maturing individuals (> 200 mm ML) (Fig. 5). Other frequent ommastrephids were Ornithoteuthis antillarum, the most frequent cephalopod in the diet of Katsuwonus pelamis, SANTOS AND HAIMOVICI: CEPHALOPODS IN THE TROPHIC RELATIONS OFF BRAZIL 757
od distributions based on
Figure 1. Diagrammatic summary of predation on cephalopods in southern Brazil. Full lines indicate frequent predation (cephalop Packard, 1972; Nesis, 1987). 758 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 2, 2002
,
d
)
n
c
i
a
g
s
a
c
l
e
r
t
e
r
u
a
o
e
p
o
d
P
d
S
d
n
a
n
a
l
a
7
s
r
9
e
9
1
h
m
c
,
e
6
1 11
1 4 71 11
31 2 9 6 1 0 3
31 0 0
9
51
0
34
.
a
t
l
d
o
i
31
81
31 11
21 21 31 52 11 21
4 31
11
31
(
,
a
m
o
wf
13
fa
t
o
t
t
a
e
t
Se
i
i
b
c
i
a
v
h
o
,
)
m
c
i
l
i
a
a
a
n
u
i
s
a
H
c
n
g
r
0
0
e
n
n
e
c
0
0
8 0 3
2
6
0
0
i
a
m
o
59
13
7 4 22
11
9
7
0
d
m
, ,
,
,
,
o
n
<
n
r
80 25
32
4
18
d
a
f
m
a
14
(
ld
<
e
n
o
a
l
ch
i
Ms
e
z
a
p
r
o
l
B
s
,
n
f
r
l
e
e
a
a a a a a
a a
a a
a a
a
a
a
a
h
h
t
s
s s s s s
s s
s s
s s
s
s
s
s
s
a
i
i
i
i
i
i
r
r r r r r
r r
r r
r r
r
r
r
r
u
t
(
e
e e e e e
e e
e e
e e
e
e
e
e
i
g
g
g
g
g
g
o
a
a
a
a
a
a
s
b
n
l
l
l
l
l
l
m
m m m m m
m m
m m
m m
m
m
m
m
a
o
e
e
e
e
e
e
e
e e e e e
e e
e e
e e
e
e
e
e
n
i
i
Hl
p-1
p2
p-2
p-5
p
p-9
d-3
d-61 d0 d-6 d-3 d-4
d-3 d5
d-1 d9
d6 d-4
d9
d-4
d
d8
g
)
e
d
R
o
i
.
r
s
e
d
p
o
p
4
p
p
o
9
o
o
l
l
l
9
a
s
s
i
i
i
i
1
h
,
,
o
n
n
n
n
i
−
p
f
f
a
a
a
a
l
l l l l
l l
l l
l l
l
l
l
l
e
p
p p
g
0
e
e
e
e
e
e e e e
e e
e e
e e
e
e
e
e
c
e
o
o
o
9
c
c
c
c
h
h h h h
l h h
h l h
h h l h
h
h
h
9
Rt
oc
oc
oc
oc
sl
sl sl sl sl sl
sl sl sc
sc sl sl
sl sl
sl
sl
sl
sl
n
1
o
(
s
n
g
o
i
n
t
i
a
d
d
n
e
a
r
l
p
d
l
e
d
r
h
a
n
i
e
s
h
o
r
i
h
c
s
n
f
n
f
e
i
i
r
s
r
h
n
i
f
f
z
n
e
e
s
i
d
f
r
-
h
i
i
h
a
f
g
e
e
h
s
e
a
f
g
h
-
s
m
i
i
g
s
s
i
n
k
h
r
b
k
n
o
f
r
p
g
i
m
d
f
a
a
s
o
l
o
m
e
f
a
b
l
a
o
k
k
n
k
i
a
r
u
i
n
t
l
c
h
o
e
o
k
a
g
r
f
t
a
a
o
n
s
a
u
c
a
d
l
e
s
a
o
e
k
y
t
e
e
e
s
w
y
s
l
m
o
h
a
d
n
l
n
t
l
n
n
n
r
r
w
n
n
r
a
g
s
h
l
c
i
i
i
k
e
a
a
a
o
e
e
t
e
e
n
r
i
t
t
t
c
o
o
s
i
i
h
i
e
c
c
l
i
t
u
d
i
l
b
t
d
d
w
o
i
n
n
n
f
m
d
a
i
o
n
f
o
e
n
e
n
m
m
t
k
j
o
a
n
n
e
e
e
p
t
t
z
h
n
r
a
o
g
p
n
r
c i
m
p
o
u
u
g
g
g
o
l
a
i
i
m
m
c
a
i
o
m
h
a
n
a
l
d
r
r
r
t
h
r
o
r
o
o
e
i
l
i
o
o
n
h
a
t k
c
m h
l
l
e
Ae
Af
Af
Ac
Jf
ff
ff
h
Bf
kf
be wf
pc
rf
Cn
cc
cf
af
ce
sf se
se
sf sc
n
t
a
e
d
a
m
h
d
t
i
n
a
e
a
h
l
.
t
l
i
d
d
s
e
h
o
r
t
a
o
o
a
l
f
t
c
a
i
s
s
h
d
d
u
t
u
s
i
e
r
i
n
s
n
u
r
i
r
e
s
t
u
w
s
t
i
a
p
e
s
s
a
a
e
n
s
e
i
y
p
i
s
s
s
s
u
l
r
o
s
p
o
n
i
e
n
n
o
r s
i
n
e
h
a
n
u
n
a
l
r
i
u
e
d
h
g
s
i
t
e
u u
c
c
m
a
n
t
s
y
s
i
)
c
c
i
u
r
o
S
s
n
t
e
a
p
a
p
i
c
f
a
l
a
b
u
b
8
u
l
o
t
s
f
o
i
l
e
c
o
x
s
t
p
a
y
y
r
t
D
l
b
h
9
a
s
m
e
h
i
e
s
o
b
s
e
a
s
u
c
a
i
c
n
i
o
n
l
c
i
u
u
c
9
g
m
a
o
s
h
p
O
d
u
t
c
n
n
u
i
t
u
g
o
a
n
n
a
h
n
1
a
s
s
i
r
i
s
i
P
s
s
e
s
s
a
g
j
n
d
t
s
p
a
a
i
p
y
y
a
,
r
g
s
b
s
u
p
u
u
o
i
c
n
u
o
n
f
O
n
h
h
y
r
L
s
a
u
n
n
n
s
u
t
s
n
p
n
t
t
c
e
g
e
n
o
i
a
x
e
i
r
i
o
L
s
i
p
o
e
o
o
.
r
o
t
l
o
h
h
g
e o
a
s
c
i
i
o
o
h
S
u
v
r
d
l
2
r
c
r
c
c
o
A
a
u
s
c
p
l
m
c
h
c
r
w
h
i
i
e
t
o
s
o
o
E
r
o
s
e
a
s
s
a
e
y
l
l
u
u
o
p
o
u
e
a
H
p
r
b
c
t
o
c
l
g
r
u
g
r
x r
o
o
l
y
a
a
i
e
s
H
m
i
x
c
s
d
r
o
r
P
r
u
l
l
t
i
g
c
n
r
r
r
g
l
o
n
n
b
t
i
m
e
e
S
e
a
i
u
t
e
u
a
a
a
a
s
E
l
n
v
o
y
o
y
a
a
a
a
o
r
I
u
l
s
s
A
N
I
L
E M
I M
E H M
M I
T
K
P
P
P
H
Pe
n
F
C
C
C
C G
C SANTOS AND HAIMOVICI: CEPHALOPODS IN THE TROPHIC RELATIONS OFF BRAZIL 759
c
r
t
u
a
;
;
o
o
d
1
1
S
h
c
61 0
9
6
1
51
1 4 32 4
4 11
0
51
1
51
1 0 0 2 9 2 6 51
1
a
t
o
i
1
21
11
11
9 21 71
11
5
11 11 87 12 41 71 61
41
;
,
m
o
>1
;
9
wf
17
fa
o
2
15
t
86
Se
l
a
a
u
i
s
c
n
g
r
0
0 0
0
0
n
n
e
3
0
2
6 6 8
0 0
0
0
7 0 5 4 2 8
8
i
a
0
0
5
48 90 93
50 53
0
0
0 54 5 40 6 1
68
d
m
,
,
,
,
,
,
, , ,
n
< <
n
20
10
34
19
18
10
14 96 13
a
m
a
ld
<
<
<
e
o
ch
Ms
a a
a
a
a a a
a
a
a a
a
a a a a a
s s
s
s
s
s s s
s
s
s
s
s s s s s
a
i
i
i i
i
i i i
i
r r
r
r
r
r r r
r
r
r
r
r r r r r
t
e e
e
e
e
e e e
e
e
e
e
e e e e e
i
g
g
g g
g
g g g
g
a
a
a a
a
a a a
a
b
l
l
l l
l
l l l
l
m m
m
m
m
m m m
m
m
m
m
m m m m m
a
e
e
e e
e
e e e
e
e e
e
e
e
e e e
e
e
e
e
e e e e e
Hl
p1
p9
p p
p-2
p5 p0 p5
p4
d-6 d6
d
d-4
d-6
d0 d-4 d8
d-81
d
d-0
d
d-9 d1 d9 d6 d8
p
o
l
s
i i
i i
i
i
,
o
n n
n
n n
n
i
f
a a
a
a a
a
l l l
l
l l l l
l
l l
l
l l l l l
p
p
p
g
e e
e
e e
e
e e e
e
e e e e
e
e e
e
e e e e e
e
o
o
o
c c
c
c c
c
l
h h h
h
h h h h
l
h
h h
h
h h h h h l
Rt
oc oc
oc
oc oc
oc
sl
sl sl sc
sl
sl sl sc sl
sl
sl
sl sl
sl
sl sc sl sl sl sl
k
r
r
a
n
e
h
h
k
a
r
s
d
r
s
d
k
i
e
n
a
m
r
f
a
l
k
r
u
a
h
g
p
e
e
a
l
a
i
a
s
o
h
n
h
g
n
t
e
o
l
i
h
t
s
i
m
r
n
r
l
u
f
t
d
s
n
a
a
t
u
n
e
i
a
c
l
d
a
a
a
i
d
k
k
l
n
f
g
n
d
k
i
c
r
r
e
o
n
r
h
k
b
n
e
e
a
a
c
h
i
r
a
a
e
c
s
a
h
u
i
g t
n
o
n
n
n
n
m
f
s
i
c
a
t
r
e
a
r
h
h
k
i
i
i
l
-
n a h
a
n o
o
f
s
r
t
t
m
e
s
s
i
i
i
f
h
a
a
s
s
e
n
m
o
d
e
l
l
o
i
n
n
s
w
r
e
r
k
m
s
h
i
i
l
l
h
a
e
g
f
w
m
y
c
r
e
e
e
e
s
o
e
t
c
a
z
z
b
e
e
i
g
t
t
a
e
e
k e
e
f
l
t
i
a
l
m
g
g
e
t a
a
l
l
l
m
u
g
g
t
a
a u
u
u
u
u
g
d
r
r
r
n
h
b
r
r
o
a
e
l
l
o l a
i
u
h
n
n
l
u
k
k q
e
o
a
Af
Af
yc
we
Pf Bf bf
lf
Bf rf bf
pe bc hc
bc rf
wc
Cn
cf
af
af
ac
ce
ge
sf
sf sf
s
s
u
i
c
u
e
i
s
s
i
t
s
i
m
n
r
u
d
n
u
i
x
s
.
s
i
o
i
r
a
s
n
s
n
i
n
s
a
d
e
s
s
r
u
a
i
g
s
l
a
p
a
u
l
e
a t
t
i
u
e
a
e
h
u
a
n
e
i
a i
i a
c
n
a
t
d
u
s
m
r
a
a
i
r
l
t l
t
i
u
c
n
a
k
g
i
s
t
t
a
t
s
a i
i
n
i
u
s
g
o
t
a
u
r
a
a
l
r
a
n
e
e
i
n
b
c
i
s s
s
c
l
e
t
n
r
o
c
i
n
u
e
h
c
l
r
i
p
a
o
g
t
b
n
u
n
d
o a
a
u
e
u
t
p
s
o
a
b
r
o
s
i
c
l
a
a
h
r
r
g
m
i
n
c
e
u
u
n
a
g
s
e a
p
s
e
p
a
b
l
l
l
b c
b
u
r
c
w
s
a
a
a
o
s
y
p
n
a
l b
l
s
u
p
a
i
i
g
s
e
g
a
o
u
c
u s
j
h
s
a o
a
u
s
s s
s
C
l
n
s
s
g
g
n
t
y
t
r
i i
i
i
u
i
i
u
e
m
r
.
u u
a
a
a
r
s s
s
a
o
h
h
c c
a
u r
h
r
r
r
h
a
t t
c
i
t
e
t
o
2
c
n
n
n
o
u u
u
n y y
r
e
e
b
u
p
u
r
t
n
i
o o
a
i
i
i
t
i
h
b
t
t
p i
n n
n
h h
l
t
t
t
o
r
o
o
h
r
e p
a
a
c
n n
n
i
p
p
a h
l
n n
n
p p
a
i
y
a
a
a
c
m
n
c
y
l
b
d
o o
o
r
c
i
l
r
m
r
b
r
u u
u
o o
i i
i
h
u
u
u
t
o y
m
m
a
i
e
h
m r r
a o
a e o
o
r r
r
r
h h r
h
e r
c c
p
q
y q
q
y
R
T P
P P P
P
P P
P
Pe
S S
S
S
S S
S
S
T T T
T
T T
U U U 760 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 2, 2002
c
1
1
1
1
;
;
;
;
r
t
1
8
1
1
u
a
o
o
d
S
h
c
a
1
2
11
41 31
2
11
5
1
(
a
t
;
o
i
21
11
2
;
;
11
m
o
5
;
6
wf
fa
o
18
1
59
t
1
Se
11
l
a
a
u
i
s
c
n
g
r
n
n
e
0
i
a
68
d
m
n
n
a
m
a
ld
e
o
ch
Ms
t
o
n
r
e
b
d
e
a
t
i
m
t
a
u
g
i
c
n
a
b
i
l
a
d
)
e
a
n
i
p1
Hl
(
i i
i
0
n n
n
8
a a
a
9
e e
e
1
c c
c
,
7
2
.
o o
o
l
i i
i
8
8
i
9
a
, ,
,
9
9
n n
n
n
8
e e
e
t
1
1
a a
a
a
9
e
p
p p p
p
p
e e
e
,
,
e
1
o
o o o
c c
o o
c
o
o
e
c
l
l l l
l l
,
d
d
o o
o
k
s
s
s s s
s s
o
i
i i
i i i
i
i i
i
i
r
e
e
a
, ,
,
a
,
, , ,
, ,
,
o
n
n n
n n n
n
n n
n
n
n
n
s
l
e e
e
i
f
f f f
f f
f
i
i
a
a a
a a
a a
a a
a
a
o
l
l
l l l
l l l
l
p p
p
g
P
P
C
e
e e
e e
e e
e e
e
e
e
e
e e e
e e e
e
R
e
o o
o
c
c c
c c
c c
c c
c
c
0
1
2
h
h
h h h
l l
h h h
l
h
9
Rt
oc
o31 o81
o11 o3
o7 o4
o31
o2 o11
o31
s0
s6
s) s31 s41
s41 s21
s10 s21 s7
s12
s2
1
1
1
s
s
o
r
t
l
n
a
3
a
o
s
b
8
e
9
e
i
l
l
s
l
l
s
9
9
a
a
o
l
a
1
1
e
e
r
s
r
a
a
n
h
l
t
s
y
,
,
e
s
i
e
u
e
t
a
l
a
s
n
n
f
s
t
o
l
w
u
s
i
a
o
e
o
h
b
r
r
r
a
n
l
r
r
g
l
t
h
t
r
h
o
e
i
n
n
c
r
a
n
e
a
a
e
w
a
t
n
a
s
o
p
i
a
a
u
n
h
a
t
s
6
l
l
h
w
a
h
i
e
f
b
m
c
c
h
i
a
p
d
B
8
l
m
o
d
l
r
i
i
p
p
l
R
m
e
p
p
w
w
2
e
r
r
c
9
a
a
e
e
r
d
w
u
u
l
l
a
r
o
m
d
i
l
l
8
e
e
1
r
c
f
f
d
n
r
t
e
r
a
t
o
a
d
w
n
n
d
i
g
e
9
e
a
n
,
e
c
e
p
h
a
h
e
n
e
a
d
o
m
m
c
c
s
n
l
1
n
n
a
z
r
e
s
i
i
s
p
r
n
l
a
c
i
n
h
n
a
o
o
t
t
a
i
,
w
o
o
i
s
h
s
r
A
A
r
l
s
e
s
b
'
o
t
r
f
n
a
c
c
s
y
n
l
i
d
i
k
m
e -
r
e
i
k
s
f
r
r
n
m
d
e
-
e
e
c
e
h
h
f
s
x
e
m
t
d k
r
s
h
m
r
t
l
a
a
t
a
t
m
e
n
u
t
a
g
s
n
r
g
t
a
a
e
t
t
c
n
a
i
n
m
o
s
h
u
b
u
g
t
m
a
a
a
u
e
c
e
l
a
a
n
n
n
Q
a
V
L
P
o
g
r
r
o
u
o
l
y
o
w
r
r
o
w
o
p
a
i
o
Ac
Ac
fc
7
5ó8
6
Mf
wc bc
lc
mc
lc
Fc pc
Ff
bc
Cn
cc
de
oc
gc
8
sc
Se
Sc
sc Se
sc
s
5
s
s
H
i
s
8
u
s
u
l
S
i
i
9
l
c
s
l
i
a
a a
M
i
s
r
t
L
1
e
a
l
e
a
c
i
n
l
r
l
n
h
a
,
.
r
i
d
h
s
l
A
e
i
t e
o
i
r
e
a
p
i
t
d
p
p
s
l
s
a
s z
s
o
b
d
v
l
u
o
l
e
a
e
o
M
S
o
l
i
u
s
u a
n
e
s
e
g
e
n
r
n
t
c
u
n
s
1
h
a
s
s
i
n
a g t
a
A
a
i
p
u
g
s
i
s
a
a
o
n
M
9
l
s
l
e
m
p
e
a
l
i
n
s
R
n
c i
r
a
i
u
s s s
c
a
9
l
m
u
t
a
e
c
i
i
i
e
A
o
v
c
r
c
a
a
1
u u u
n
f
a
x
b
s
p
c
a
n
y
4
p
h
m
l
d
l l l
f
l
e
c
e
S
a
i
a
,
sn
e
m
u
e
c
b
Y
l
9
o
p
M
l
g
a
a a a
r
u
a
a
v
p
a
s
r
v
r
l
a
l
9
D
e
m
i
a
t
s
s
i
h h h
g
p
e
C
d
a
a
h
d
u
a
e
s
a
o
1
m
r
g
g
c
E
r
r
u
e
l
e
e
n
p p p
R
i
p
r
c
.
s
r
g
d
u
t
s
s
r
,
n
f
o
I
n
s
a
b s
n
s
s
e e e
d d
e
i
e
r
N
2
p
e
i
o
e
n
o
i
u
u
o
i
p
t
u
I
t
c c c
e e
c
a
s
B
a
a
k
o
b
w
u
n
h
i
n
n
a a
e d
n
i
o
m
e
i
a
i
n
a
o o o
s
i
i
i i
e
t
R
h
e
l
s
m m
o
i
e
t t t
r
p
a
b
u
r
h
s
m f
f
a
d
c
l
g g
r
A
o
l f
f
n
y
g
b
c
c c c
u
o o
x
r
e
h
o
a
p
e
A
i
i i
e
V
S
J
l
o o
t
r
i
r r r
e
a
h
u u
u
o
h s
a
r
E
u
p
X
A A A
D D
M
D
L
T
P
F P
P
K K
P
P P
4
2
Pe
S
M
3
S
G
T
O
O
1 SANTOS AND HAIMOVICI: CEPHALOPODS IN THE TROPHIC RELATIONS OFF BRAZIL 761
Figure 2. Cephalopods preyed upon by Loligo sanpaulensis and pelagic and demersal fishes caught on the southern Brazilian shelf. (Circles indicate the presence in the diet; black circles indicate a frequency of occurrence (FO) over 10%). 762 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 2, 2002
Figure 3. Cephalopods preyed upon by Illex argentinus and pelagic and demersal fishes caught on upper slope and oceanic adjacent waters of southern Brazil. (Circles indicate the presence in the diet; black circles indicate a frequency of occurrence (FO) over 10%). SANTOS AND HAIMOVICI: CEPHALOPODS IN THE TROPHIC RELATIONS OFF BRAZIL 763
Figure 4. Cephalopods preyed upon by seabirds and marine mammals found dead in beaches or incidentally caught by coastal gillnet fishery of southern Brazil. (Circles indicate the presence in the diet; black circles indicate the main species in the diet). 764 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 2, 2002
Figure 5. Mantle length distribution of Loligo sanpaulensis, Illex argentinus and Ornithoteuthis antillarum in the stomach contents of some of their main predators. (FO: frequency of occurrence; ni: number of squids measured and n: number of predators with each species of squid).
Thunnus alalunga, T. albacares, Istiophorus albicans and Tetrapturus albidus, generally with small sizes (Fig. 5) and Ommastrephes bartramii frequent in the diet of Thunnus obesus, X. gladius and marine mammals, such as Orcinus orca and Kogia breviceps (Figs. 2,3,4). Todarodes filippovae and Hyaloteuthis pelagica, were far less frequent, found in the diet of marine mammals and pelagic and demersal fishes from upper slope and of oceanic adjacent waters. Other relatively frequent oceanic muscular squids were Lycoteuthis lorigera and Abralia spp, mainly in the diet of T. alalunga, T. obesus, Isurus oxyrinchus, Sphyrna lewini, Globicephala melas and K. breviceps (Figs. 2,3,4). Ammoniacal squids occurred with relatively frequency in the diet of upper slope and oceanic predators. The more frequent species were Ancistrocheirus lesueurii, Octopoteuthis sp, Histioteuthis spp and Chiroteuthis veranii, mainly in the diet of Prionace glauca, Kogia sima, K. breviceps, G. melas and oceanic seabirds (Figs. 3,4). With very low frequencies were observed other oceanic squids such as Enoploteuthis sp, Abraliopsis sp, Moroteuthis robsoni, Pholidoteuthis boschmai, as well as cranchiids and onychoteuthids not identified to specific level (Figs. 3,4). The presence of the benthic octopuses Eledone gaucha, E. massyae, Octopus tehuelchus and Octopus vulgaris was observed with low frequency in the diet of demersal fishes and SANTOS AND HAIMOVICI: CEPHALOPODS IN THE TROPHIC RELATIONS OFF BRAZIL 765
marine mammals of shelf and upper slope, although the presence of a small O. vulgaris (ML < 20 mm) was recorded in a stomach content of T. alalunga (Figs. 2–4). The pelagic octopus Argonauta nodosa was found mainly in the diet of species of shelf and upper slope, being frequent, sometimes in large number of very small individuals, in stomach contents of Spheniscus magellanicus and, to a lesser degree, in Katsuwonus pelamis (Figs. 2–4). Other pelagic octopuses, as Tremoctopus violaceus and Ocythoe tuberculata, were found in the stomach contents of large pelagic fishes and marine mam- mals of upper slope and oceanic adjacent waters. With small frequency occurred Japetella diaphana, Haliphron atlanticus and the bathypelagic vampyromorphid Vampyroteuthis infernalis (Figs. 3,4). Sepiolids were infrequent, Semirossia tenera was found mainly in stomach contents of shelf and upper slope predators, and Heteroteuthis dispar in predators from upper slope and oceanic adjacent waters (Figs. 2–4). The sizes of cephalopod prey were mostly small, with ML under 100 mm. The larger were Ommastrephes bartramii, I. argentinus, Thysanoteuthis rhombus, Ancistrocheirus lesueurii, Pholidoteuthis boschmai and Octopoteuthis sp, reaching ML over 250 mm, preyed upon mainly by P. americanus, T. alalunga, T. albacares, T. obesus, Xiphias gladius and by marine mammals from upper slope and of oceanic adjacent waters. The presence of remains of a buccal mass and arms remains of an Architeuthis sp, with estimated mantle length of 1012 mm and total weight of 92 Kg, was observed in the stomach content of a blue shark.
DISCUSSION
Six families and seven species of cephalopods were recorded in the diet of the shelf predators. Haimovici and Perez (1991) recorded the same number of families and one more species, in the review of the coastal cephalopod fauna of southern Brazil. The simi- larity in the numbers of shelf species recorded from predator’s diet and surveys shows that a fairly precise list of cephalopods can be obtained analysing stomach contents. In the upper slope and oceanic adjacent waters, 27 families were registered in the diet of predators, far more than the 12 families formerly recorded from bottom trawl surveys in the area (Perez and Haimovici, 1993). Furthermore, the higher number of taxa in the stomach contents compared with the survey from the slope and oceanic waters, confirms the utility of dietary studies to survey the cephalopod fauna composition. The low number of cephalopod taxa in the southern Brazilian shelf can be attributed to the low diversity of substrates, mostly soft bottoms, and to the influence of cold waters (<15°C) during part of the year that prevent the occurrence of tropical cephalopods. The higher diversity in upper slope and oceanic adjacent warm waters is reflected in the large number of widely distributed species of epi, meso and bathypelagic cephalopods in the Southwestern Atlantic (Nesis, 1999). The assessment of the importance of cephalopods in the food webs is made more diffi- cult because we lack estimates of abundance of the predators and also ignore the amount of energy represented by the cephalopods in their diets. A first approximation can be obtained assuming that landings represent the relative abundance of the fishes and the frequency of occurrence of cephalopods in the stomach contents are an index of their relative importance in the diets of their predators. 766 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 2, 2002
Following this approach, according to commercial landings reported by Haimovici et al. (1997), we estimated that the shelf fishes that preyed more heavily on cephalopods were of little importance in the catches, less than 1000 t yr−1. Those that fed occasion- ally on them (FO < 5%) yielded around 15,000 t yr−1, less than a third of the demersal trawl fishery landings. In contrast tunas, billfishes and wreckfish, which feed intensely on cephalopods (FO 10% – 80%), yielded over 5000 t yr−1 to Brazilian fishers, besides the catches by foreign longliners. Comparing this numbers we concluded that cephalo- pods have a larger relative importance in the upper slope and oceanic adjacent waters than in shelf waters. On the shelf Loligo sanpaulensis occurs year round and is the most abundant cephalo- pod (Haimovici and Andriguetto, 1986). The only estimates of its abundance are around 3000 t in the early 80s by Andriguetto and Haimovici (1991). It is part of the incidental catch of bottom trawlers, but no specific fishery is developed for it in southern Brazil. This squid seems to occupy an intermediary level in the energy transference, feeding in midwater and being a prey of both pelagic and benthic fishes (Santos and Haimovici, 1998). One of the species that fed more heavily on L. sanpaulensis was the Franciscana dolphin, that also feed on this species in all its distribution range, from coastal waters of Argentina to Rio de Janeiro (Brownell, 1975; Pinedo, 1982; Santos and Haimovici, 2001). Other seasonally important predators were juvenile Magellanic penguins that arrive in southern Brazilian coast from Patagonia, in some years, in large numbers (Vooren, 1997). All other cephalopod species were far less frequent and Loligo plei, octopuses and sepiolids were rare in bottom trawl survey catches and absent in commercial landings (Haimovici and Andriguetto, 1986). On the upper slope and oceanic adjacent waters two ommastrephids seems to be the most important links in the trophic relations: I. argentinus and O. antillarum. The first performs diel vertical migrations (Moiseev, 1991) and was found to be an important prey for large pelagic fishes, as the swordfish and bigeye tuna, that have the ability to prey in midwater up to 600 m (Carey and Robison 1981; Colette and Nauen 1983; Holland et al., 1990). It was also a prey for the near bottom dwelling wreckfish and the school shark, emphasising its role in the transference of energy between the pelagic and demersal envi- ronment (Santos and Haimovici, 2000). Tunas, billfishes and the swordfish, migrate from the tropics to southern Brazil from May to October, when the influence of cold waters of Malvinas (Falklands) Current is stronger in the region (Weidner and Arocha, 1999). Their permanence in the region is probably associated to the northward reproductive migration of adults and subadults I. argentinus from Uruguayan and northern Argentinean waters that occurs in the same time of the year (Santos and Haimovici, 2000). The other important ommastrephid was the smaller-sized and more epipelagic O. antillarum. Its major occurrence in the diet of the smaller tunas T. alalunga and T. albacares and billfishes, can be explained by the association of these predators with more superfi- cial waters and also because its small size. Juveniles O. antillarum (ml < 50 mm) were fairly frequent and mid water trawls in the EEZ of southern Brazil (REVIZEE Program– Avaliação do Potencial Sustentável dos Recursos Vivos na Zona Econômica Exclusiva do Brasil, unpubl. data). The neutrally buoyant and slow swimming ammoniacal squids were found in the diet of diverse predators from upper slope and oceanic adjacent waters, being more frequent in the stomach contents of blue shark, Prionace glauca, a slower swimmer with a broad SANTOS AND HAIMOVICI: CEPHALOPODS IN THE TROPHIC RELATIONS OFF BRAZIL 767 trophic range, and some marine mammals, as Kogia sima, K. breviceps and G. melas, teuthophagous species adapted to feed in deeper waters (Clarke, 1986a). From the analysis of the stomach contents of potential predators off southern Brazil, it was concluded that the cephalopod fauna is far more diverse and has a higher relative importance in the offshore food webs when compared to the neritic environment. The loliginid L. sanpaulensis was the dominant cephalopod on the shelf, whilst two ommastrephids dominated more oceanic waters, one of them I. argentinus, that may have some fishery potential, was important in the food web of the slope and the other, O. antillarum, appears as an important component of the pelagial food webs of oceanic adjacent waters.
LITERATURE CITED
Amaratunga, T. 1983. The role of cephalopods in the marine ecosystem. Advances in assessment of world cephalopod resources. FAO Fish. Tech. Pap. 231: 379–415. Andriguetto, J. M. and M. Haimovici. 1991. Abundance and distribution of Loligo sanpaulensis Brakoniecki, 1984 (Cephalopoda: Loliginidade) in southern Brazil. Sci. Mar. 55(4): 611–618. Angelescu, V. and L. B. Prenski. 1987. Ecologia trófica de la merluza común del mar argentino (Merluccidae, Merluccius hubbsi). Parte 2. Dinámica de la alimentación analizada sobre la base de las condiciones ambientales, la estructura y las evaluaciones de los efectivos en su área de distribución. Serie Contribuciones INIDEP No. 561. 205 p. Brownell, Jr., R.L. 1975. Feeding ecology of the Franciscana dolphin, Pontoporia blainvillei, in Uruguayan waters. J. Fish. Res. Bd. Can. 32: 1073–1078. Capitoli, R. R. and M. Haimovici. 1993. Dieta alimenticia del besugo Pagrus pagrus en el extremo sur de Brasil. Frente Marítimo 14: 81–86. Carey, F. G. and B. H. Robison. 1981. Daily patterns in the activities of swordfish, Xiphias gladius, observed by acoustic telemetry. Fish. Bull. 79(2): 277–292. Castello, J. P., M. Haimovici, C. Odebrecht and C. M. Vooren. 1997. Relationships and function of coastal and marine environments: the continental shelf and slope. Pages 171–178 in U. Seeliger, C. Odebrecht and J. P. Castello, eds. Subtropical convergence environments: the coast and sea in the Southwestern Atlantic. Springer, Berlin. Clarke, M.R. 1986a. Cephalopods in the diet of odontocetes. Pages 281–321 in M. M. Bryden and R. Harrison, eds. Research in dolphins. Claredon Press, Oxford. ______, ed. 1986b. The handbook for the identification of cephalopod beaks. Claredon Press, Oxford. 273 p. ______. 1987. Cephalopod biomass-estimation from predation. Pages 221-–238 in P. R. Boyle, ed. Cephalopod life cycles, vol. 2. Academic Press, London. ______, ed. 1996a. The role of cephalopods in the world’s oceans. Phil. Trans. Roy. Soc. London 351: 979–1112. ______. 1996b. Cephalopods as prey. III. Cetaceans. Pages 1053–1065–in M. R. Clarke, ed. The role of cephalopods in the world’s oceans. Phil. Trans. Roy Soc. London 351. ______, N. MacLeod, H. P. Castello and M. C. Pinedo. 1980. Cephalopod remains from stomach of the sperm whale stranded at Rio Grande do Sul in Brazil. Mar. Biol. 59(4): 235– 239. ______, J. P. Croxall and P. A. Prince. 1981. Cephalopod remains in regurgitations of the wandering albatross Diomedea exulans L. at South Georgia. British Antarc. Surv. Bull. 54: 9– 21. Colette, B. and C. E. Nauen. 1983. Scombrids of the world (2). FAO species catalogue. 135 p. Croxall, J. P. and P.A. Prince. 1994. Dead or alive, night or day: how albatrosses catch squid? Antarctic Sci. 6(2): 155–162. 768 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 2, 2002
______and ______. 1996. Cephalopods as prey. III. Seabirds. Pages 1023–1044 in M. R. Clarke, ed. The role of cephalopods in the world’s oceans. Phil. Trans. Roy. Soc. London 351. Dawe, E. G. and J. K. T. Brodziak. 1998. Trophic relationships, ecosystem variability and recruit- ment. Pages 125–156, Chapt. 7 in E. G. Dawe, P. G. Rodhouse and R. K. O’Dor, eds. Squid recruitment and dynamics: The genus Illex the model, the commercial Illex species and influ- ences on variability. FAO Fish. Tech. Pap., 376. Eschmeyer, W. N., ed. 1998. Catalog of fishes. Spec. Publ/ No.1 of the Center for Biodiversity Research and Information. California Academy of Sciences. San Francisco. Volumes 1–3. 2905 p. Garcia, C. A. E. 1997. Physical oceanography. Pages 94–96 in U. Seeliger, C. Odebrecht and J.†P. Castello, eds. Subtropical convergence environments: the coast and sea in the Southwestern Atlantic. Springer, Berlin. Haimovici, M. and J. M. Andriguetto. 1986. Cefalópodes costeiros capturados na pesca de arrasto do litoral sul do Brasil. Arqu. Biol. Tec. Paran· 29 (3): 473–495. ______and L. C. Krug. 1992. Alimentação e reprodução da anchova Pomatomus saltatrix no litoral sul do Brasil. Revta. brasil. Biol. 52(3): 503–513. ______and J. A. A. Perez. 1991. Coastal cephalopod fauna of southern Brazil. Bull. Mar. Sci. 49(1–2): 221–230. ______, R. L. Teixeira and M. C. de Arruda. 1989. Alimentação da castanha Umbrina canosai (Pisces: Scianidae) no sul do Brasil. Revta. brasil. Biol. 49(2): 511–522. ______, J. P. Castello and C. M. Vooren. 1997. Fisheries. Pages 181–196 in U. Seeliger, C. Odebrecht and J. P. Castello, eds. Subtropical convergence environments: the coast and sea in the Southwestern Atlantic. Springer, Berlin. Holland, K. N., R. W. Brill and R. K. Chang. 1990. Horizontal and vertical movements of yellowfin and bigeye tuna associated with fish aggregating devices. Fish. Bull., U.S. 88: 493–507. Juanicó, M. 1979. Contribuição ao estudo da biologia de cefalópodes Loliginidae do Atlântico Sul Ocidental, entre o Rio de Janeiro e Mar del Plata. Doctoral thesis Instituto, Oceanográfico da Univ. São Paulo, São Paulo, SP. 102 p. Juras, A. A. and N. Yamaguti. 1985. Food and feeding habits of king weakfish Macrodon ancylodon caught in the southern coast of Brazil (Lat. 29°–32°S). Bol. Inst. Oceanográfico 33(2): 149– 157. Lessa, R. 1982. Biologie et dinamique des populations de Rhinobatus horkelii du plateau continen- tal du Rio Grande do Sul (Brásil). Doctoral Thesis, Univ. Bretagne Occidentale, France. 238 p. Lipinski, M. R. and S. Jackson. 1989. Surface-feeding on cephalopods by procellariiform seabirds in the southern Benguela region, South Africa. J. Zool. Lond. 218: 549–563. Moiseev, S. I. 1991. Observation of the vertical distribution and behaviour of nektonic squids using manned submersibles. Bull. Mar. Sci. 49: 446–456. Nesis, K. N. 1987. Cephalopods of the world, squids, cuttlefishes, octopuses and allies. T.F.H. Publications, Neptune City. 351 p. ______. 1999. Cephalopoda. Pages 707–795 in D. Boltovskoy, ed. South Atlantic zooplankton. Backhuys Publishers, Leiden. Odebrecht, C. and V. M. T. Garcia. 1997. Phytoplankton. Pages 109–110 in U. Seeliger, C. Odebrecht and J.P. Castello, eds. Subtropical convergence environments: the coast and sea in the South- western Atlantic. Springer, Berlin. Packard, A. 1972. Cephalopods and fish: the limits of convergence. Biol. Rev. 47: 241–307 Palacio, F. J. 1977. The study of coastal cephalopods from Brazil with reference to Brazilian zooge- ography. Doctoral Dissertation, Univ. Miami, Miami. 311 p. Peres, M. B. and M. Haimovici. 1998. A pesca dirigida ao cherne poveiro, Polyprion americanus (Polyprionidae, Teleostei) no sul do Brasil. Atlântica (20): 141–161. Perez, J. A. A. and M. Haimovici. 1993. Cefalópodes do talude continental do sul do Brasil. Atlântica 15: 49–72. SANTOS AND HAIMOVICI: CEPHALOPODS IN THE TROPHIC RELATIONS OFF BRAZIL 769
Pinedo, M. C. 1982. Análise dos conteúdos estomacais de Pontoporia blainvillei (Gervais & D’Orbigny, 1844) e Tursiops gephyreus (Lahlile, 1908) (Cetacea, Platanistidae e Delphinidae) na zona estuarial e costeira de Rio Grande, RS, Brasil. Master Thesis, Fundação Univ. Rio Grande, Rio Grande, RS. 95 p. ______. 1987. First record of the dwarf sperm whale from Southwest Atlantic with reference to osteology, food habits and reproduction. Sci. Rep. Whales Res. Inst. 38: 71–186. ______and N. Barros. 1983. Análise dos conteúdos estomacais do leão marinho Otaria flavescens e do lobo marinho Arctocephalus australis na costa do Rio Grande do Sul, Brasil. Resumos do VIII Simpósio Latinoamericano sobre Oceanografia Biológica, 28 de novembro a 02 de dezembro de1983. Montevideo, Uruguay. 25 p. Queiroz, E. L. 1986. Estudo comparativo da alimentação de Sympterigia acuta Garman, 1877 e S. bonapartei Muller e Henle, 1841 (Pisces, Rajiformes) com relação à distribuição, abundância, morfologia e reprodução, nas águas litorâneas do Rio Grande do Sul, Brasil. Master Thesis, Fundação Univ. Rio Grande, Rio Grande, RS. 326 p. Rice, D. W. 1998. Marine mammals of the world. Systematics and distribution. Spec. Publ. No. 4. The society for marine mammalogy. Lawrence, Kansas. 231 p. Rosas, F. C. 1989. Aspectos da dinâmica populacional e interaçõs com a pesca do leão-marinho do Sul, Otaria flavescens (Shaw, 1800) (Pinnipedia, Otariidae), no litoral sul do Rio Grande do Sul, Brasil. Master Thesis, Fundação Univ. Rio Grande, Rio Grande, RS. 88 p. Santos, R. A. 1999. Cefalópodes nas relações tróficas do sul do Brasil. Doctoral thesis, Fundação Univ. Rio Grande, Rio Grande, RS. 222 p. ______and M. Haimovici. 1997. Food and feeding of the short -finned squid Illex argentinus (Cephalopoda: Ommastrephidae) off southern Brazil. Fish. Res. 33: 139–147. ______and ______. 1998. Trophic relationships of the long-finned squid Loligo sanpaulensis on the southern Brazilian shelf. S. Afr. J. Mar. Sci., 20: 81–91 ______and ______. 2000. The argentine short-finned squid Illex argentinus in the food webs of southern Brazil. Sarsia 85: 49–60. ______and ______. 2001. Cephalopods in the diet of marine mammals stranded or inci- dentally caught along southeastern and southern Brazil (21°S to 34°S). Fish. Res. 52: 99–112. Schwingel, P. R. 1991. Alimentação de Engraulis anchoita (Clupeiformes: Engraulidae) na plataforma continental do Rio Grande do Sul, Brasil. Master Thesis, Fundação Univ. Rio Grande, Rio Grande, RS. 98 p. Smale, M. J. 1996. Cephalopods as prey. IV. Fishes. Pages 1067–1082–in M. R. Clarke, ed. The role of cephalopods in the world’s oceans. Phil. Trans. Roy. Soc. Lond. 351. Sweeney, M. J. and C. F. E. Roper. 1998. Classification, type localities, and type repositories of recent Cephalopoda. Pages 561–599 in N. A. Voss, M. Vecchione, R. B. Toll and M. J. Sweeney, eds. Systematics and biogeography of Cephalopods, vol. II. Smithson. Contrib. Zool. No. 586. Teixeira, R. L. and M. Haimovici, 1989. Distribuição, reprodução e hábitos alimentares de Prionotus punctatus e P. nudigula (Pisces: Triglidae) no litoral do Rio Grande do Sul, Brasil. Atlântica 11(1): 13–45. Vaske, T., Jr. 1994. Alimentação da rêmora Remora osteochir Cuvier, 1829 e peixe-piloto Naucrates ductor Linnaeus, 1758, no sul do Brasil. Revta. brasil. Biol. 55(2): 315 -321. ______and G. Rincón. 1998. Conteúdo estomacal dos tubarões azul (Prionace glauca) e anequim (Isurus oxyrinchus) nas águas oceânicas no sul do Brasil. Revta. brasil. Biol. 58(3): 445–452. Vooren, C. M. 1997. Sea and shore birds. Pages 154–159 in U. Seeliger, C. Odebrecht and J. P. Castello, eds. Subtropical convergence environments. The coast and sea in the Southwestern Atlantic. Springer, Berlin. ______and A. C. Fernandes. 1989. Guia de albatrozes e petréis do sul do Brasil. Editora Sagra, Porto Alegre. 99 p. 770 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 2, 2002
Weidner, D. M. and F. Arocha. 1999. World swordfish fisheries. An analysis of swordfish fisheries, market trends and trade pattern. Past-present-future, vol. IV. Latin America. Part A. South America. Sec. 2. Atlantic. Segment B. Brazil. NOAA Tech. Memo. NMFS-F/SPO-35. 682 p.
ADDRESSES: (R.A.S., M.H.) Departamento de Oceanografia, Fundação Universidade do Rio Grande, Cx.P. 474, Rio Grande-RS, 96201-900, Brazil. E-mail: (R.A.S.)