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Note / Nota Milmann Et Al.: Diet of Bottlenose Dolphinbjoce in Southern Brazil

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Note / Nota Milmann Et Al.: Diet of Bottlenose Dolphinbjoce in Southern Brazil Note / Nota Milmann et al.: Diet of bottlenose dolphinBJOCE in southern Brazil Feeding ecology of the common bottlenose dolphin, Tursiops truncatus, in southern Brazil: analyzing its prey and the potential overlap with fisheries Lucas Milmann1,2,3*, Daniel Danilewicz1,4, Rodrigo Machado1,5, Roberta Aguiar dos Santos6,7, Paulo Henrique Ott1,2 1 Grupo de Estudos de Mamíferos Aquáticos do Rio Grande do Sul (GEMARS). (Rua Machado de Assis, 1456 - Bairro Sulbrasileiro, Osório, RS, CEP: 95520-000) 2 Universidade Estadual do Rio Grande do Sul (UERGS). (Rua Machado de Assis, 1456 - Sulbrasileiro, Osório, RS, CEP: 95520-000) 3 Programa de Pós-graduação em Zoologia, Universidade Estadual de Santa Cruz (UESC). (Campus Soane Nazaré de Andrade - Rod. Jorge Amado, km 16 - Salobrinho, Ilhéus, BA, CEP: 45662-900) 4 Instituto Aqualie. (Av. Dr. Paulo Japiassu Coelho, 714 - Sala 206 - Juiz de Fora, MG, CEP: 36033-310) 5 Universidade Federal do Rio Grande do Sul, Programa de Pós-Graduação em Biologia Animal. (Av. Bento Gonçalves, 9500, Bloco IV, Prédio 43435, Sala 219, Porto Alegre, RS, CEP: 91501-970) 6 Instituto Chico Mendes de Conservação da Biodiversidade. (Estr. Hisaichi Takebayashi, 8600, Atibaia, SP, CEP: 12952-011) 7 Centro Nacional de Pesquisa e Conservação da Biodiversidade Marinha do Sudeste e Sul (CEPSUL). (Av. Ministro Victor Konder, 374 - Centro, Itajaí, SC, CEP: 88301-700) *Corresponding author: [email protected] The common bottlenose dolphin (henceforth and habitat degradation (VAN BRESSEM et al., 2007, referred to as the bottlenose dolphin), Tursiops truncatus 2015; FRUET et al., 2012). As a result, this population (Montagu 1821), is of worldwide distribution in tropical is currently classified as vulnerable (VU) at the regional and temperate regions in both coastal and oceanic waters level (RIO GRANDE DO SUL, 2014). (WELLS; SCOTT, 2009). In the Southwestern Atlantic Since knowledge of diet is fundamental to Ocean (SWA), the species occurs from the northern understanding habitat preferences, trophic interactions Brazilian coast (SICILIANO et al., 2008) to Tierra del and potential competition between marine mammals Fuego, Argentina (GOODALL et al., 2011). and fisheries for available marine food resources (e.g., Despite the wide distribution of the species in the SWA, KASCHNER; PAULY, 2005; BOYD, 2010; DUNSHEA information on the bottlenose dolphin’s feeding habits in et al., 2013), new qualitative and quantitative data on this region is relatively sparse. Only a comparatively small bottlenose dolphin feeding ecology in southern Brazil are number of specimens thus far been analyzed in the few presented here. studies published to date, mainly in southeastern Brazil The stomach contents of 21 stranded bottlenose (DI BENEDITTO et al., 2001; GURJÃO et al., 2004; dolphins were collected by a marine mammal research SANTOS; HAIMOVICI, 2001, SANTOS et al., 2002; team (Grupo de Estudos de Mamíferos Aquáticos do MELO et al., 2010). Rio Grande do Sul - GEMARS) during systematic beach In the southern most areas of the Brazilian shore, surveys (mostly monthly) along the central-northern coast the bottlenose dolphin is commonly sighted very close of Rio Grande do Sul, southern Brazil, between November to the shore, usually within less than 0.5 nm of it, and 1991 and October 2008. The area surveyed covered about inside estuaries and river mouths (e.g. SIMÕES-LOPES, 250 km of exposed sandy beaches, from Torres (29o19´S, 1991; DI TULLIO et al., 2015). In some of these 49o43’W) to the Lagoa do Peixe National Park (31o15’S, estuaries, bottlenose dolphins cooperate with the artisanal 50o54’W). fishermen’s fishing activity, mainly during the mullet The animals were classified, in the field, by sex and (Mugil spp.) fishing season (e.g. SIMÕES-LOPES et al., standard body length. The stomach of each dolphin was 1998; ZAPPES et al., 2011; DAURA-JORGE et al., 2013). removed from its abominal cavity during the dissection This coastal bottlenose population dolphin is known to procedure, for further examination. Voucher skulls were be under threat in various ways, including gill net fishing collected for all specimens and deposited at GEMARS’s http://dx.doi.org/10.1590/S1679-87592016116406404 BRAZILIAN JOURNAL OF OCEANOGRAPHY, 64(4):415-422;2016 415 Milmann et al.: Diet of bottlenose dolphin in southern Brazil scientific collection. In the laboratory, the three stomach HAIMOVICI; PEREZ, 1991; CARVALHO-FILHO, 1999; chambers of each dolphin were examined and their contents HAIMOVICI; KLIPPEL, 2002). Demersal species were washed through 0.3 mm and 1.0 mm mesh sieves. The the prey associated with the bottom and pelagic species cephalopod beaks found were stored in 70% ethanol. were the ones using the whole water column, excepting Otoliths and fish bones were stored dry. Fish otoliths and the bottom. Species that were present in both depth zones cephalopod beaks were identified as far as possible to were classified as demersal-pelagic. the species level, using local reference collections (e.g. To investigate potential dietary changes over time, a CEPSUL/ICMBio, for cephalopod beaks) and identification non-parametric test (chi-squared) was used to compare the guides (e.g., MENEZES; FIGUEIREDO, 1980; WAESSLE contributions (% N and % FO) of the main prey species for et al., 2003; ROSSI-WONGTSCHOWSKI et al., 2014). two pooled periods (1991-2002, n = 11; 2003-2008, n = 10). The minimum number of ingested fish in each stomach Direct comparisons of the IRI of the most important prey was estimated by the greater number of either right or items were also made for these two periods. left otoliths. When the side could not be determined, the Of the 21 bottlenose dolphins analyzed, 13 were male, total amount of those structures was divided by two. For three were female and five were of undetermined sex. The the cephalopods, the higher number of either upper or total length of the measured specimens ranged from 205.5 lower beaks was considered for quantifying the amount to 346.0 cm (median = 276.0; SD = 45.6; n = 16). The of prey ingested. Measurements of the prey remains (i.e. majority of the bottlenose dolphins were found between otoliths and cephalopod beaks) were gathered using a November and April (spring and summer) (n = 14), while stereomicroscope with ocular micrometer and precision May to October (autumn and winter) accounted for only of 0.1 mm. The prey’s total length (mm) and biomass (g) seven individuals. were back calculated using the size of these structures A total of 1,493 ingested prey items, including (i.e. otoliths and cephalopod beaks) and published 1,479 otoliths and 14 cephalopod beaks, were found regression equations (SANTOS; HAIMOVICI, 1998; in the stomachs of the dolphins. Due to the high degree HAIMOVICI; VELASCO, 2000; WAESSLE et al., 2003). of digestion, it was not possible to identify 55 otoliths, Otoliths that were severely eroded were counted but not comprising 30 teleosts (Table 1). The prey items identified included to estimate prey length and mass. In these cases, numbered at least 804, including 793 (98.6%) bony fishes these measurements were averaged from data of intact and 11 cephalopods (1.4%) (Table 1). Regarding marine structures of the same species. The correlation between debris, only one small piece of nylon was found in the the size (i.e. total body length) of bottlenose dolphins and stomach contents of one dolphin. their prey was tested using Spearman rank correlation. The diversity of prey ingested represents a total The numerical frequency (%N) and frequency of of 15 fish species belonging to eight families (Table occurrence (%FO) were defined as the percentage of each 1). Cephalopods were represented by three species prey ingested and the number of stomachs containing a (Argonauta nodosa, Doryteuthis plei and D. sanpaulensis). given prey, respectively. The relative importance of each The most important family of fish found was Sciaenidae, prey in the diet of bottlenose dolphins was assessed using accounting for eight species. All the other families were the index of relative importance (IRI), expressed both in represented by one member only. The diversity of prey the traditional way (IRI = [%N + %Prey biomass] x [%FO]; items ingested by each dolphin varied from one to 12 PINKAS et al., 1971), as well as on a percentage basis species (x = 4.80; SD = 2.87) (Table 1). (%IRIi = 100 IRIi /ΣIRIi; CORTÉS, 1997). In calculating The most important teleosts, by %IRI, were: IRI values, the unidentified teleosts were excluded from Trichiurus lepturus, Paralonchurus brasiliensis and the analysis, since it was not possible to estimate their Mugil cf. liza. In addition, four species showed a relatively biomass. To reduce possible bias from differential rates high frequency of occurrence (%FO>25): Urophycis of digestion among species (e.g., BOWEN, 2000), indices brasiliensis, Menticirrhus littoralis, Cynoscion guatucupa were calculated separately for each major taxonomic and Macrodon atricauda, although they did not reach high group (i.e. fishes and cephalopods). %IRI values (%IRI<5) (Table 1). Indices were calculated for prey species, as well as Diet composition has not changed drastically over the for ecological groups. Ecological groups were defined years, since 13 out of 18 prey species were consumed in according to prey habits and vertical distribution (e.g. both periods (i.e. 1991-2002 and 2003-2008). No statistical 416 BRAZILIAN JOURNAL OF OCEANOGRAPHY, 64(4):415-422;2016 Milmann et al.: Diet of bottlenose dolphin in southern Brazil Table 1. Prey species found in the stomach content of common bottlenose dolphins (n = 21) from the central-northern coast of Rio Grande do Sul, southern Brazil, from 1991 to 2008. Key to abbreviations: EG =Ecological group, DP = Demersal-pelagic, D = Demersal, P = Pelagic, N = Number, %N = Numerical frequency, FO = Frequency of occurrence, %FO = Percentage frequency of occurrence, W = Biomass, %W = Percentage biomass, IRI = Index of Relative Importance.
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