Diet of bottlenose dolphins, Tursiops truncatus, in southern Brazil.

SC/57/SM09
Diet of bottlenose dolphins, Tursiops truncatus, in southern Brazil.
Mehsen, M.1, Secchi, E. R.1, Fruet, P1. and Di Tullio, J.1
1
Marine Mammals Laboratory, Museu Oceanográfico “Prof. Eliézer C. Rios”,
Fundação Universidade Federal do Rio Grande, Cx. Postal 379, Rio Grande, RS, Brazil, 96200-970
ABSTRACT
Stomach contents of 11 bottlenose dolphins (Tursiops truncatus) stranded in southern coast of
Rio Grande do Sul State (31°13’S 52°08’W - 32°38’S- 52°08’W) Brazil, were analysed.
Individuals were found from november 2002 to march 2005, mostly during summer. The diet
was composed of 10 species of teleosts belonging to five families. Only one beak of coastal
squid (family Loliginidae) was found. According to frequency of occurrence the white
croacker, Micropogonias furnieri, is the most frequent species (71.43%) in the diet, followed
by cutless fish, Trichiurus lepturus (57.14%). No marked temporal changes on the diet of
bottlenose dolphins was found between this and Pinedo’s (1982) studies.
Key words: diet, Tursiops truncatus, cetaceans, southern Brazil
INTRODUCTION
In Rio Grande do Sul, southern Brazil, a small resident population of bottlenose dolphins
inhabits the Patos Lagoon estuary (32º06’S / 052º02’W) and adjacent coastal waters (Castello
and Pinedo, 1977; Möller et al., 1994; Dalla Rosa, 1999). Beach surveys along the coast have
been carried out since 1976 to investigate the mortality of cetaceans and pinnnipeds. Until
recently, coastal fisheries were thought to be a minor cause of bottlenose dolphins mortality in
the area. However, a recent investigation showed a marked increase in the number of
bottlenose dolphins washed ashore with evidence of interactions with fishing operations
(Fruet et al., 2005 – SC/57/SM8). There are evidences (genetic and distributional) that most
dolphins washed ashore belong to the Patos Lagoon population.
Despite almost 30 years of surveys to record and recover [especially small cetaceans and
pinnipeds] carcasses in the region yet very little is known about the feeding habits of
bottlenose dolphins (e.g. Pinedo, 1982). According to Pinedo (1982), bottlenose dolphins in
this area prey mostly upon teleost fishes and the white croacker, Micropogonias furnieri, was
the most frequent species found in the stomach of stranded animals.
1
SC/57/SM09
Diet provides information about dolphin distribution and potential overlap with fisheries
which might help understand the reasons for the recent observed increase in mortality. The
purpose of this study is to examine the diet of bottlenose dolphins washed ashore in recent
years and compare with the results obtained by Pinedo (1982).
MATERIAL AND METHODS
Beach surveys using a four-wheel drive truck to record and/or collect marine mammals
carcasses were conducted along a streatch of 355 km on coast of Rio Grande do Sul (31o21’S
- 33o44’S), southern Brazil. Stomachs of stranded bottlenose dolphins were collected from
november 2002 to march 2005.
Stomachs were removed after tying the digestive tract at the end of the esophagus and the
beginning of the intestineto avoid losing the contents, and frozen for posterior analysis. The
contents were washed with running water through 600 and 200 !m mesh sieves. Undigested
fish was measured and their sagittal otoliths were removed. Otoliths and other hard parts were
sorted and retrieved by hand, air dried and stored in vials.
The number of fish was estimated by counting the right otoliths. Fish species were identified
using an otolith reference collection. Relative prey importance was determined by the
frequency of occurrence (FO%) and numerical abundance (N%). FO% is the percentage of
stomach contents in which a prey taxon occurred and N% is the percentage of each prey taxon
from a tally of occurrences from all prey taxa found.
RESULTS
Stomachs from 11 bottlenose dolphins found washed between 2002-2005 were analysed
(Table 1). Nine dolphins were found in summer (December-March) and two in spring
(September-November). Four dolphins were found with empty stomachs. A 152cm long male
was probably still nursing though no milk was detected in its stomach. A total of 154 fish
belonging to ten species of five families were found. Most of the species found are demersal
and all occur in coastal or estuarine habitats. Many otoliths (n=109) were very digested or
broken and could not be identified. Individual diet diversity varied from one to six prey items.
Only one beak of coastal squid (family Loliginidae) was found.
2
SC/57/SM09
Table 1. Prey items of Tursiops truncatus from the southern coast of Rio Grande do Sul State, Brazil. D = demersal; P = pelagic.
27/11/2002
Body length
(cm)
270
17/03/2003
11/1/2004
25/10/2004
249
355
194
F?
M?
F**
20/12/2004
243
M*
11/1/2005
247
M*
13/1/2005
13/1/2005
13/1/2005
323
152
288
F**
M**
M**
27/1/2005
3/3/2005
276
272
M*
F *
Date
Sex
Prey species
F?
M. platanus (P)
M. ancylodon (D)
M. furnieri (D)
T. lepturus (P)
P. brasiliensis (D)
C. guatucupa (D)
Empty
M. furnieri (D)
C. guatucupa (D)
T. lepturus (P)
U. brasiliensis(D)
P. porosissimus (D)
squid
Stellifer sp. (D)
M. furnieri (D)
P. brasiliensis (D)
M. litoralis (D)
T. lepturus (P)
Stellifer sp. (D)
M. furnieri (D)
Empty
Stellifer sp. (D)
T. lepturus (P)
M. ancylodon (D)
P. brasiliensis (D)
M. furnieri (D)
Empty
Empty
Family
n
Mugilidae
Sciaenidae
Sciaenidae
Trichiuridae
Sciaenidae
Sciaenidae
1
1
7
4
7
1
Sciaenidae
Sciaenidae
Trichiuridae
Phycidae
Batrachoididae
Loliginidae
Sciaenidae
Sciaenidae
Sciaenidae
Sciaenidae
Trichiuridae
Sciaenidae
Sciaenidae
27
22
2
7
18
1
1
6
3
1
31
1
1
Sciaenidae
Trichiuridae
Sciaenidae
Sciaenidae
Sciaenidae
10
3
1
3
1
*Evidence of interaction with fisheries **No evidence of interaction with fisheries ? interaction with fisheries unknown
White croacker, Micropogonias furnieri, and the cutless fish, Trichiurus lepturus, were the
most frequent prey species occurring in 71.43% and 57.14% of the stomachs, respectively
(Table 2). In this study as well as in Pinedo’s (1982), the white croacker was the prey species
with the highest frequency of occurrence in stomachs of bottlenose dolphins in the area. This
prey occurred in 83.3% (Pinedo, 1982) and 71.4% in this study. Both studies analysed only
stomachs of bottlenose dolphins found in spring and summer. Although the diet composition
remains almost the same after more than 20 years (Table 3; Figure 1), the white croaker
seemed much more important in the past. In recent years, bottlenose dolphins seem to be
preying more intesively in a wider variety of preys (Figure 1).
3
SC/57/SM09
Table 2. Numerical frequency (N%) and frequency of occurrence (FO%) of prey in the stomachs of bottlenose dolphins washed ashore
on the southern coast of Rio Grande do Sul State, Brazil. (only for the stomachs with prey items (n=7)).
Numerical percentage
Food items
Common name
Fish
Micropogonias furnieri
Trichiurus lepturus
Paralonchurus brasiliensis
Stellifer sp.
Occurrence
N
N%
FO
FO%
154
99.35%
7
100%
white croacker
42
27.10%
5
71.43%
cutless fish
40
25.81%
4
57.14%
drum
13
8.39%
3
42.86%
little croacker
7
4.52%
3
42.86%
Cynoscion guatucupa.
striped weakfish
23
14.84%
2
28.57%
Macrodon ancylodon
king weakfish
2
1.29%
2
28.57%
stargazer
18
11.61%
1
14.29%
Brazilian codling
7
4.52%
1
14.29%
mullet
1
0.65%
1
14.29%
kingcroacker
1
0.65%
1
14.29%
1
0.65%
1
14.29%
1
0.65%
1
14.29%
155
100%
Porichthys porosissimus
Urophycis brasiliensis
Mugil platanus
Menticirrhus littoralis
Cephalopod
Loligo sp.
squid
Table 3. Comparative table of numerical percentage (N%) and frequency of occurrence (FO%) of prey items of bottlenose
dolphins analysed in this study and in Pinedo (1982)
Pinedo
(1982)
Present
study
Pinedo
(1982)
Present
study
Food items
N%
N%
FO%
FO%
Fishes
100%
99,35%
100%
100,00%
Micropogonias furnieri
76.56%
27.10%
83.33%
71.43%
Trichiurus lepturus
8.33%
25.81%
25.00%
57.14%
Paralonchurus brasiliensis
2.08%
8.39%
25.00%
42.86%
-
4.52%
-
42.86%
Cynoscion guatucupa .
3.65%
14.84%
16.66%
28.57%
Macrodon ancylodon
1.04%
1.29%
0.083%
28.57%
-
11.61%
-
14.29%
Urophycis brasiliensis
1.56%
4.52%
16.66%
14.29%
Mugil platanus
3.65%
0.65%
25.00%
14.29%
-
0.65%
-
14.29%
Umbrina canosai
0.52%
-
0.083%
-
Odontesthes bonairensis
1.56%
-
16.66%
-
Stellifer sp.
Porichthys porosissimus
Menticirrhus littoralis
Pogonias cromis
0.52%
-
0.083%
Lycengraulis grossidens
0.52%
-
0.083%
-
Ariidae
0.52%
-
0.083%
-
-
0.65%
-
14.29%
-
0.65%
-
14.29%
Cephalopod
Loligo sp.
100.00%
4
SC/57/SM09
Figure 1. Comparative frequency of occurrence of bottenose dolphin prey species between this (2002-2005) and Pinedo’ s 1982 studies
(1976-1980).
DISCUSSION
The analysis of the diet indicated that T. truncatus from southern Rio Grande do Sul can be
considered ichthyophagous, preying mostly upon demersal species. This pattern is similar to
those of other coastal bottlenose dolphin populations found elsewhere in Brazil (e.g.
southeastern Brazil - Di Beneditto et al., 2001) and worldwide (e.g. Florida – Barros, 1993;
Barros and Wells, 1998) and sciaenid fishes seem to be an important component of the
species diet (e.g. Barros and Wells, 1998). The bottlenose dolphin population from southern
Rio Grande do Sul appears to be an opportunistic predator feeding upon the most abundant
species. In this study as well as in Pinedo’s (1982), the white croacker was the prey species
with the highest frequency of occurrence in stomachs of bottlenose dolphins. The Patos
lagoon estuary and adjacent coastal waters are important nursing areas for M. furnieri
(Castello, 1986; Pereira, 1994). Nevertheless, the white croaker seemed much more important
in the past. In recent years, bottlenose dolphins seem to be preying more intesively in a wider
variety of preys. This might be related to the decline of white croacker stocks. M. furnieri has
been heavily exploited by gillnet and trawl fisheries for more than three decades (Reis 1992;
Haimovici 1998) and a drastic decrease in the density of juveniles in coastal waters has been
observed (Ruffino and Castello 1992) suggesting that the species became less available to top
predators. In the same area, temporal changes in the diet of franciscana have also been
5
SC/57/SM09
attributed to overfishing (Bassoi and Secchi, 2000; Secchi et al., 2003). Historical catch
records have demonstrated a local decline in yearly landings of M. furnieri and Macrodon
ancylodon (Haimovici 1998). This is consistent with a reduction in the occurrence of these
two species in the franciscana's diet between early 1980s and late 1990s (Bassoi and Secchi,
2000). In turn, predators need to change their diet preying upon less exploited species (e.g.
cutless fish, Trichiurus lepturus). Cutless fish had only little importance in the diet of
franciscana in the past and is now the second most important prey for the species in this
region (Bassoi and Secchi, 2000; Secchi et al., 2003). Similar trend has been observed for
bottlenose dolphins. Frequency of occurrence of cutless fish observed in this study is more
than twice as high as the observed in Pinedo’s (1982) study. This fish species has never been
targeted by commercial fishery in southern Brazil and is an abundant species in the trawlling
catches (Haimovici et al. 1996), especially during warm months as it is associated with
thermal fronts (Martins and Haimovici, in press). Unfortunately, no stomach contents are
available for other seasons to see if occurrence of cutless fish decreases in colder months.
Two stomachs out of 11 stomachs were empty. Both animals with empty stomachs showed
evidence of being incidentally killed in fisheries (i.e. both presented net marks on their
bodies). Although empty stomachs might be a consequence of entanglement (i.e. the animals
might have regurgitated after being trapped), it might be yet another evidence of less food
available. No empty stomachs were found by Pinedo (1982). Although larger sample size is
needed to test the relationship between temporal changes in the diet of bottleneose dolphins
and trends in fish stock abundance using robust statistical analyses, the preliminary data
presented here suggest that changes in bottlenose dolphin diet might parallel reduced
availability of certain prey species due to their over-exploitation as observed in franciscana
(Bassoi and Secchi, 2000; Secchi et al., 2003).
ACKNOWLEDGMENTS
We are indebted to Mônica Muelbert, Silvina Botta and Emanuel Ferreira (LMM-FURG), Lilia Fidelix (LMMMOFURG) for helping to collect data on stranded bottlenose dolphins along Rio Grande do Sul. We would like
to thank Fundo Nacional do Meio Ambiente (FNMA), Superintendência do Porto de Rio Grande (SUPRG) and
Museu Oceanográfico/Fundação Universidade Federal do Rio Grande (MO-FURG) for financial or logistical
support to this project. Otoliths were identified with an assistance of Dr. Manoel Haimovicci (Laboratory of
Demersal fish and Cephalopods - FURG).
REFERENCES
Barros, N. B. (1993). Feeding ecology and foraging strategies of bottlenose dolphin on central east coast of
Florida. PhD Thesis, University of Miami. pp. 328.
Barros, N. B. and Wells, R.S. (1998). Prey and feeding patterns of resident bottlenose dolphins (Tursiops
truncatus) in Sarasota Bay, Florida. Journal off Mammalogy 79(3): 1045-1059.
6
SC/57/SM09
Bassoi, M. and Secchi, E. (2000). Temporal variation in the diet of franciscana Pontoporia blainvillei (Cetacea,
Pontoporiidae) as a consequence of fish stocks depletion off southern Brazil. IV Workshop para a
Coordenação da Pesquisa e Conservação da Franciscana, Pontoporia blainvillei, no Atlântico Sul
Ocidental, Technical Paper No. 9.
Castello, H. P and Pinedo, M. C. (1977). Botos na Lagoa dos Patos. Natureza em Revista 12: 46-49.
Castello, J.P. (l986). Distribución, crecimiento y maduración sexual de la corvina juvenil Micropogonias
furnieri en el estuario de la Lagoa dos Patos, Brasil. Physis, 44 (106): 21-36.
Dalla Rosa, L. (1999). Estimativa do tamanho da população de botos, Tursiops truncatus, do estuário da Lagoa
dos Patos, RS, a partir da foto-identificação de indivíduos com marcas naturais e da aplicação de modelos de
marcação-recaptura. Master Dissertation, Fundação Universidade Federal do Rio Grande, Rio Grande.
(Unpublished).
Di Beneditto, A.P.M., Ramos, R.M.A, Siciliano, S., Santos, R.A., Bastos, G. and Fagundes-Neto, E. (2001).
Stomach contents of delphinids from Rio de Janeiro, Southeastern Brazil. Aquatic Mammals 27.1: 24-28
Fruet, P. F., Silva, K. G; Secchi E. R; Menezes, R. B; Di Tullio, J. C; Monteiro, D. S; Mehsen , M; and Estima S.
C. (2005). Temporal trend in the bycatch of botllenose dolphins, Tursiops truncatus, from a small resident
population in southern Brazil. Paper SC/57/SM8 presented to IWC meeting. Ulsan, South Korea, May/June,
2005.
Haimovici, M. (1998). Present state and perspectives for the southern Brazil shelf demersal fisheries. Fishery
Management and Ecology, 5, 277-289.
Haimovici, M. (2000). Recursos pesqueiros demersais da região sul - subsídios para o levantamento do estado
da
arte
dos
recursos
vivos
marinhos
do
Brasil
Programa
REVIZEE
http://www.mma.gov.br/port/sqa/projeto/revizee/doc/textos/dermesai.pdf
Haimovici, M., Vasconcellos, M.C., Kalikoski, D.C and Castello, J.P. (2004). Diagnóstico da pesca no Rio
Grande do Sul. Projeto milênio. 24 pp. (Unpublished).
Martins, A. S. and Haimovici, M. (in press) Distribution, abundance and biological interactions of the cutlassfish
Trichiurus lepturus in the southern Brazil subtropical convergence ecosystem. Fisheries Research. Res.
Möller, L. M., P.C. Simões-Lopes, E.R. Secchi and A. N. Zerbini (1994). Uso de fotoidentificação no estudo do
deslocamento de botos, Tursiops truncatus (Cetacea, Delphinidae) na costa sul do Brasil. Actas da 6a.
Reuniao de Especialistas em Mamiferos Aquaticos da America do Sul. Florianópolis, Brasil: 5 - 8.
Pereira, L.E. (1994). Variação diurna e sazonal dos peixes na barra do estuário da Lagoa dos Patos, RS, Brasil.
Atlântica 16: 5-22.
Pinedo, M. C. (1982) Análise dos conteúdos estomacais de Pontoporia blanvillei (Gervais e D’Orbigny, 1844) e
Tursiops gephyreus (Lahille, 1908) (Cetácea, Platanistidae e Delphinidae) na zona estuarial e costeira de Rio
Grande, RS, Brasil. Tese de mestrado. FURG. 95pp.
Pinedo, M. C. and Rosas, F. C. W. (1989). Novas ocorrências de Pseudorca crassidens (Cetacea, Delphinidae)
para o Atlântico Sul Ocidental, com observações sobre medidas cranianas e alimentação. Atlântica. 11: 7783.
Reis, E.G. (1992). An assessment of the exploitation of the white croaker Micropogonias furnieri (Pisces,
Sciaenidae) by the artisanal and industrial fisheries in coastal waters of southern Brazil. Ph.D. Thesis.
University of East Anglia, Norwich.
Ruffino, M. L. and Castello, J. P. (1992). Alterações na fauna acompanhante da pesca do camarão barba-ruça
(Artemesia longinaris) nas imediações da barra de Rio Grande, RS. Nerítica, 7, 43-55.
Secchi, E.R., Ott, P.H. and Danilewicz, D.S. (2003). Effects of fishing by-catch and conservation status of the
franciscana dolphin, Pontoporia blainvillei. Pages 174-191 in Gales, N., Hindell, M. and Kirkwood, R.
(Eds) Marine Mammals: Fisheries, Tourism and Management Issues. CSIRO Publishing. Collingwood.
Australia.
7