INTRODUCTION
The franciscana dolphin, Pontoporia blainvillei (Gervais & d'Orbigny, 1844), is a small coastal dolphin endemic to the south-western Atlantic Ocean. The species occurs from Itaúnas (18°25′S 30°42′W) in central Brazil to Golfo Nuevo (42°35′S 64°48′W) near Península Valdés, Argentina (Siciliano, Reference Siciliano1994; Crespo et al., Reference Crespo, Harris and González1998, Reference Crespo, Pedraza, Grandi, Dans and Garaffo2010).
Incidental captures in fishing gillnets and other fishing gear occur all along its geographical distribution (Corcuera, Reference Corcuera1994; Pinedo, Reference Pinedo1994a; Di Beneditto et al., Reference Di Beneditto, Ramos and Lima1998; Rosas et al., Reference Rosas, Monteiro Filho and de Oliveira2002; Cappozzo et al., Reference Cappozzo, Negri, Pérez, Albareda, Monzón and Corcuera2007; Franco Trecu et al., Reference Franco-Trecu, Costa, Abud, Dimitriadis, Laporta, Passadore and Szephegy2009; Prado et al., Reference Prado, Secchi and Kinas2013). Nowadays, it is estimated that more than 400 dolphins per year are incidentally caught in fishing gillnets in the Buenos Aires province (Bordino & Albareda, Reference Bordino and Albareda2004; Cappozzo et al., Reference Cappozzo, Negri, Pérez, Albareda, Monzón and Corcuera2007; Negri et al., Reference Negri, Denuncio, Panebianco and Cappozzo2012). Because of high by-catch levels, the species has been classified as ‘vulnerable’ by the International Union for the Conservation of Nature (IUCN) (Secchi, Reference Secchi2006; Reeves et al., Reference Reeves, Dalebout, Jefferson, Karkzmarski, Laidre, O'Corry-Crowe, Rojas-Bracho, Secchi, Slooten, Smith, Wang, Zerbini and Zhou2012).
In Argentina, the main published study on biological parameters of franciscana dolphins by-caught in artisanal fisheries (Corcuera et al., Reference Corcuera, Monzón, Crespo, Aguilar and Raga1994) is nearly 20 yr old. That study reported the sex-ratio, age and length distribution of by-caught franciscanas from Necochea and Claromecó (southern Buenos Aires province). It also made a preliminary comparison of reproductive parameters and physical maturity from a small Argentinian sample with those from Uruguay given by Kasuya & Brownell (Reference Kasuya and Brownell1979), but emphasized that further data were required before firm conclusions could be reached. At the moment, some reproductive aspects of the franciscana from southern Buenos Aires province have been revised by Panebianco et al. (Reference Panebianco, Negri and Cappozzo2012a). However, because these parameters were used to establish franciscana management areas (FMAs) within a phylogeographical framework (Secchi et al., Reference Secchi, Danilewicz and Ott2003a), updated parameter estimates may help improve conservation of the species. In addition, collection of biological data from by-caught dolphins can be useful to assess the effects of by-catch and to estimate vital rates (Secchi et al., Reference Secchi, Ott, Danilewicz, Gales, Hindell and Kirkwood2003b). New estimates of population parameters are also relevant, because some species suffering high levels of by-catch may show changes in growth rates (Caswell et al., Reference Caswell, Brault, Read and Smith1998), age distribution, proportion of mature individuals in the population and body fat conditions (Lockyer, Reference Lockyer1990; Pinedo, Reference Pinedo1994b; Murphy et al., Reference Murphy, Winship, Dabin, Jepson, Deaville, Reid, Spurrier, Rogan, López, González, Read, Addink, Silva, Ridoux, Learmonth, Pierce and Northridge2009).
The main goal of this paper is to estimate several biological parameters (age, body condition, sexual and physical maturity) of the franciscana dolphins by-caught in artisanal coastal fishery off southern Buenos Aires province in the first decade of the 21st Century.
MATERIALS AND METHODS
Study area and sampled data
Between 2003 and 2009 we collected 54 carcasses of franciscana dolphins incidentally entangled in the artisanal fishing nets along the southern coast of Buenos Aires province, Argentina, between the localities of Necochea (38°44′S 58°44′W) and Bahía Blanca (38°44′S 62°16′W) (Figure 1). Dolphins were accidentally caught in gillnets and shrimper gears all year round at 0.1–30.0 km offshore and 11–50 m depth. The sample survey took place during an incidental mortality estimation project carried out by the authors (Negri et al., Reference Negri, Denuncio, Panebianco and Cappozzo2012). A description of the fishing area, gear and effort can be found at Negri et al. (Reference Negri, Denuncio, Panebianco and Cappozzo2012).
Study area (shaded in grey), southern Buenos Aires, Argentina.
We worked in collaboration with the artisanal fishermen, who were asked not to discard the incidentally captured dolphins. Retrieved carcasses were kept in a freezer (−20°C) until necropsy was performed at the laboratory. During necropsies, standard information on sex, weight and body external measurements (following the method of Norris, Reference Norris1961) were recorded systematically by the authors. The protocol of the necropsies was carried out following the method of Winchell (Reference Winchell1982).
Age
The age of 51 individuals was estimated by counting of growth layer groups (GLGs) in histological sections of teeth following the protocol of Pinedo & Hohn (Reference Pinedo and Hohn2000) with ad hoc modifications (Negri, Reference Negri2010). The teeth were decalcified in the commercial acid mix RDO® and sectioned in a cryostat at −21°C. The 25 µm sections were stained with Mayer's haematoxylin and mounted in slides with glycerine.
Sex-ratio
The significance of differences in male and female sex-ratios was tested by a χ2 test, both within the whole sample and within categories of sexual and physical maturity.
Sexual maturity
Sexual maturity was estimated through histological procedures for 25 males and 21 females following the methods of Harrison et al. (Reference Harrison, Bryden, McBrearty and Brownnell1981) and Danilewicz (Reference Danilewicz2003) for females and Hohn et al. (Reference Hohn, Chiver and Barlow1985) and Danilewicz et al. (Reference Danilewicz, Claver, Pérez Carrera, Secchi and Fontoura2004) for males. During necropsy, the gonads were weighed to the nearest 0.1 g, measured to the nearest 0.01 cm and fixed in 10% formalin. The histological preparations followed standard protocols including inclusion of a 2–3 mm gonad block in Histoplast®, sectioning in 4–7 µm thick slides by microtome, staining with haematoxylin and eosin, and inspection by a compound microscope at magnifications from 40 to 1000×. Because histological preparations were not feasible for three males, sexual maturity was inferred for them from morphometric parameters (Danilewicz et al., Reference Danilewicz, Claver, Pérez Carrera, Secchi and Fontoura2004) as follows:
$$\eqalign{& \quad \hbox{Combined testes weight}\colon \ \hbox{CTW} = \hbox{rTW} + \hbox{lTW}\ \lpar \hbox{g}\rpar \cr & \hbox{Testicular maturity index}\colon \ \hbox{IM} = \hbox{CTW} / \hbox{CTL}\ \lpar \hbox{g}/\hbox{mm}\rpar }$$where: r/lTW = right/left testis weight (g); CTL = combined testis length = rTL + lTL (mm); r/lTL = right/left testis length (mm). Male dolphins were considered sexually mature for CTW ≥ 5.0 g and IM ≥ 0.08 g/mm (Danilewicz et al., Reference Danilewicz, Claver, Pérez Carrera, Secchi and Fontoura2004).
Because the symmetry in the external morphology of franciscana testes has been confirmed previously (Danilewicz et al., Reference Danilewicz, Claver, Pérez Carrera, Secchi and Fontoura2004), if one gonad was missing we assumed it had the same characteristics as the remaining one.
Physical maturity
Physical maturity was established according to the degree of fusion of epiphyses to the vertebral centra. After removal of flesh, carcasses were boiled to be skeletonized. Once clean, the vertebral column was set in order and we determined the degree of fusion of each epiphysis to its vertebral centrum thus: degree 1 = epiphyses completely unfused; degree 2 = epiphyses partially fused to the vertebral centrum; degree 3 = epiphyses fused to the vertebral centrum with visible line of fusion; degree 4 = epiphyses fused to the vertebral centrum without visible line of fusion. Dolphins were considered to be physically mature with 90% of the epiphyses fused to the vertebral centrum (degree 3 and/or 4) (Negri, Reference Negri2010).
Body condition
In order to establish the body condition of each specimen, three relative indices were used: Kn, fat index and liver index.
The relative index Kn measures the individual variations from the expected weight for length of an individual as indications of general ‘well-being’, and have been frequently studied under the general term ‘condition’ (Le Cren, Reference Le Cren1951). In this sense, body condition was calculated for each individual as follows:
$$\hbox{Kn} = \hbox{W}_{\rm o} / \hbox{W}_{\rm e}$$where Wo is the measured total wet weight of the animal (kg) and the We is the total weight estimated (kg) from a standard length–weight potential regression. The regression was calculated from 63 by-caught franciscana dolphins sampled by the authors in the same studied area (Negri, Reference Negri2010). Where the condition index was Kn ≥ 1, the individual was deemed healthy, while individuals with a condition index less than 1 were deemed underweight or unhealthy (Nilssen et al., Reference Nilssen, Haug, Grotnes and Potelov1997; Caon, Reference Caon1998; de Araujo, Reference de Araujo2005; Reyes-Küppers, Reference Reyes-Küppers2007, Panebianco et al., Reference Panebianco, Botte, Negri, Marcovecchio and Cappozzo2012b).
The fat index was determined from the contribution in percentage of the total weight of the fat in the blubber Wf (g), to the total body mass Wo (g):
$$\hbox{Fat index} = \hbox{W}_{\rm f}/\hbox{W}_{\rm o} \times 100.$$To analyse the fat index (Hanks, Reference Hanks, Fowler and Smith1981) the left blubber layer was removed from the carcasses from the area around the ears to the caudal peduncle, excluding the dorsal and pectoral fins, and weighed. Thus, the total blubber weight was double this measure, as it was considered that the blubber of the right and left sides of the dolphins was equal. For those specimens for which total blubber weight was not available (because of logistic issues or incomplete animals), it was estimated with the linear regression:
$$\eqalign{\hbox{Log}_{\rm BlubberWeight}&= \lpar \hbox{Log}_{\rm AxillaryGirth} - 0.741\rpar / 0.284\cr &\quad\ \lpar R^2=0.874\semicolon \; p \lt 0.001\rpar .}$$This regression was performed for both sexes combined as there were not significant gender differences (slope comparison t-test, P = 0.882). The variable ‘axillary girth’ is the girth with the greatest correlation with the total blubber weight of franciscana dolphins from the studied area (Negri, Reference Negri2010).
The liver index was calculated from the percentage contribution of the weight of the liver Wl (g) to the total body mass Wo (g):
$$\hbox{Liver index} = \hbox{W}_{\rm l} / \hbox{W}_{\rm o} \times 100.$$This index has been reported as a suitable body condition index for porpoises (Das et al., Reference Das, Siebert, Fontaine, Jauniaux, Holsbeek and Bouquegneau2004) and franciscanas (Foglia, Reference Foglia2008) as it is not linked to the age or length of the dolphins.
Each relative body condition index was compared between sexes and sexual maturity with the non-parametric Mann–Whitney U-test, as the sample groups did not follow a normal distribution. Moreover, our results were compared with the available results (mean ± standard deviation (SD)) presented for neighbouring areas (Kamiya & Yamasaki, Reference Kamiya and Yamasaki1974; Rodríguez et al., Reference Rodríguez, Rivero and Bastida2002) by t-test.
RESULTS
Age and length
The standard length for female franciscanas ranged from 78.70 to 160.50 cm (mean = 121.75 cm, SD = 21.20 cm, N = 22), and for males from 81.50 to 141.50 cm (mean = 117.33 cm, SD = 14.45 cm, N = 32).
The oldest individual in our sample was a 13 yr old male with a standard length of 141.5 cm and weight of 23.1 kg. The oldest females were two 8 yr old dolphins; one was 160.5 cm long and weighed 38.2 kg and the other, a pregnant individual, was 149.0 cm long and weighed 52.0 kg.
Sixty-nine per cent of the dolphins were juveniles less than 4 yr old, 41% of which were males (Figure 2). The age–frequency distribution was unimodal, with a peak at ages 1–3 yr for males and 1 yr for females (Figure 2).
Age–frequency distribution of the by-caught franciscana dolphins off southern Buenos Aires province in the period 2003–2009.
Sex-ratio
The sex-ratio, 32 males:22 females, did not differ from parity in the whole sample (χ2, P = 0.174).
Sexual maturity
A total of 74% of the dolphins examined in this study were immature. Males and females contributed equally to that fraction (χ2, P = 0.739). Throughout the surveyed period, three pregnant females were registered. They were captured between November and February and had a standard length of 142.0–150.0 cm, weighed 26.85–52.00 and were 4–8 yr old. An 8 yr old lactating female was also recorded with large amounts of milk in its mammary glands. This individual was 160.5 cm long and weighed 38.2 kg.
The seasonal frequency of mature and immature individuals showed that the proportion of dolphins of different sexual maturity stages was equal (67% of immature) in summer, autumn and winter, but a higher frequency of immature animals (86%) was registered during the spring (September–November, Figure 3). However, the low sample size of mature animals precluded testing significant differences.
Absolute frequency of the by-caught franciscana dolphins per season, sex (F, females; M, males) and sexual maturity.
The age, standard length and weight of sexually mature and immature dolphins are presented in Table 1.
Age (N = 46), standard length (TL) (N = 49) and weight (N = 48) of the sexually mature (M) and immature (I) franciscana dolphins by-caught in artisanal fisheries off southern Buenos Aires province.
N, sample size; SD, standard deviation.
Physical maturity
A total of 85% of the entangled franciscana dolphins were physically immature according to the analyses of the vertebral epiphyses. The proportion of physically immature males and females was not statistically different (50% males, 35% females, χ2, P = 0.238).
The age, standard length and weight of physically mature and immature dolphins are presented in Table 2.
Age (N = 51) and standard length (TL, N = 54) of the physically mature (M) and immature (I) franciscana dolphins by-caught in artisanal fisheries off southern Buenos Aires province.
N, sample size; SD, standard deviation.
Body condition
No statistical differences between sexes for the allometric coefficient b of the weight–length (W-TL) curve were found (slope comparison t-test, P = 0.381). Therefore, sexes were pooled in computing the following W-TL relationship:
$$\hbox{W}_{\rm e} \lpar \hbox{kg}\rpar = 0.0009 \times \hbox{TL} \lpar \hbox{cm}\rpar ^{2.1184}\semicolon \; R^2=0.827\ \lpar \hbox{Figure}\ 4\rpar$$The relative body condition index, Kn, of the sampled dolphins oscillated between 0.78 and 1.44. The fat index ranged from 7.37% to 49.01%, the lowest value was registered by a sexually mature male and the highest by an immature female. The relative liver index fluctuated between 0.97% and 4.64%. A comparison of the three indexes by sex and sexual maturity (Table 3) did not reveal significant differences; Mann–Whitney U-tests: Kn p F-M = 0.071, P I-M = 0.564; fat index P F-M = 0.115, p I-M = 0.090; liver index P F-M = 0.424, P I-M = 0.271 (F-M: females–males; I-M: immature–mature).
Standard length–weight (TL–W) relationship of franciscana dolphins off southern Buenos Aires.
Relative body condition indices: Kn (N = 52), Fat index (%) (N = 51) and Liver index (%) (N = 50) of franciscana dolphins by-caught in artisanal fisheries off southern Buenos Aires province. Comparisons of the three indices by sex and sexual maturity did not reveal significant differences (Mann–Whitney U-tests, P > 0.05).
N, sample size; mean (SD, standard deviation).
Contrasting with neighbouring areas, the values of Kn presented here were not significantly different (t-test, P = 0.084) from those obtained by Rodríguez et al. (Reference Rodríguez, Rivero and Bastida2002) for the entangled franciscanas of northern Buenos Aires province (1.028 ±0.120; N = 41). A significant difference was found in the fat index mean value of the franciscanas off the northern coast of Buenos Aires (Rodríguez et al., Reference Rodríguez, Rivero and Bastida2002), where values were higher (mean = 37.1, SD = 5.87, N = 10) than those reported here in this study (t-test, P = 0.001). Finally, the mean liver index reported here did not differ from the mean value of the northern coast of the province (t-test, P = 0.787). Moreover, comparisons made by sex with a small sample size of Uruguayan franciscanas also did not show differences between the studies in the liver index (females: 2.54 ±0.30, t-test, P = 0.665; males: 2.67 ±0.30, t-test, P = 0.558, Kamiya & Yamasaki, Reference Kamiya and Yamasaki1974).
DISCUSSION
Understanding the age distribution of incidentally killed animals is key to the evaluation of impacts of artisanal fisheries on incidental mortality of franciscana dolphins Pontoporia blainvillei (Crespo et al., Reference Crespo, Pedraza, Dans, Koen Alonso, Reyes, García, Coscarella and Schiavini1997; Secchi & Fletcher, Reference Secchi and Fletcher2004). This information, if subject to careful treatment to reduce bias, may also be useful in the estimation of approximate survival rates (Secchi & Fletcher, Reference Secchi and Fletcher2004) and valuable for species risk assessments.
An assessment of the age distribution of the by-catch can also be relevant to understanding which age-classes are more vulnerable. Previous studies have shown that juveniles appear to be most susceptible to fishing nets throughout the whole range of the species. For example, 62% of the franciscana dolphins captured in Uruguay and in southern Brazil (Pinedo & Hohn, Reference Pinedo and Hohn2000) were estimated to be less than 4 yr old. This is consistent with findings for the Buenos Aires province, where 64% of the entangled franciscanas along the southern coast (Corcuera et al., Reference Corcuera, Monzón, Crespo, Aguilar and Raga1994) and 67.5% of those measured along the northern coast (Denuncio, Reference Denuncio2012) were younger than 4 yr. Similarly, in the sample studied in this paper, over 60% of the entangled individuals were under 4 yr.
Some authors (e.g. Perrin et al., Reference Perrin, Donovan and Barlow1994; Danilewicz et al., Reference Danilewicz, Claver, Pérez Carrera, Secchi and Fontoura2004) have postulated that the higher proportion of young animals entangled in by-catch may be a consequence of behaviour as compared to older (mature) individuals. The lack of familiarity of young dolphins with fishing nets could lead to behaviours tied to curiosity that could make these individuals more prone to entanglement. However, it is not empirically known whether this applies to franciscanas. Furthermore, because population age distributions remain unknown, it is not possible to assess the reasons for juvenile-biased incidental catches.
More than 70% of the individuals captured in the study area from 1988–1992 (Corcuera, Reference Corcuera1996) and 2003–2009 (this study) were sexually immature. In contrast, only 13% of the specimens entangled were sexually mature females. Even though immature animals were present in all seasons, small sample sizes in winter and autumn preclude robust conclusions with regard to seasonal variation in the proportion of mature and immature animals in the by-catch. The higher proportion of sexually immature individuals during spring coincides with the breeding season of the species in Argentinean waters, and is in line with observations of other authors (Bordino et al., Reference Bordino, Thompson and Iñiguez1999; Faillá et al., Reference Failla, Seijas, Espósito and Iñíguez2012; Denuncio et al., Reference Denuncio, Bastida, Danilewicz, Moron, Rodriguez Heredia and Rodríguez2013). The fact that more immature dolphins were captured during spring could be influenced by seasonal differences in artisanal fishing effort, since the number of fishing days and vessels usually increases during the spring and summer (Cappozzo et al., Reference Cappozzo, Negri, Pérez, Albareda, Monzón and Corcuera2007; Negri et al., Reference Negri, Denuncio, Panebianco and Cappozzo2012), possibly leading to higher by-catch. On the other hand, it has been shown that there is age and sex segregation in some bays along the Argentinean coast, with juveniles found in shallower waters. It has also been shown that a seasonal distribution pattern may occur, with inshore movements during spring and summer (Bordino et al., Reference Bordino, Thompson and Iñiguez1999; Bordino & Albareda, Reference Bordino and Albareda2004). Unfortunately, it is not yet known if the same patterns occur in open-ocean habitats like the one studied here, but a combination of these hypotheses (differences in fishing effort and use of habitat) might explain higher frequencies of immature individuals entangled during the spring.
A greater proportion of sexually immature franciscanas found in the by-catch at the southern end of their range suggests that the impact of the fisheries is not as important as it would be if more mature animals were present (Caughley, Reference Caughley1977; Caswell, Reference Caswell2001). A risk assessment conducted with a species of relatively similar life history (Hector's dolphins, Cephalorhynchus hectori; Slooten et al., Reference Slooten, Fletcher and Taylor2000) concluded that high levels of mortality of sexually mature animals increases extinction risk. Gearin et al. (Reference Gearin, Melin, De Long, Kajimura and Johnson1994), in assessing interactions between the harbour porpoise, Phocoena phocoena, and the salmon fisheries of Washington, USA, noted that 63% of the by-catch involved immature individuals. The authors also suggested that, in the short-term, this may result in a lower impact on populations than by-catch of mature individuals. However, they highlighted the potential future detrimental impacts on recruitment, especially in species with low reproductive rates and relatively short life spans that limit reproductive flexibility, particularly with respect to a denso-dependent response to high levels of mortality.
The maximum age for Pontoporia blainvillei was recorded for the area of Uruguay, a female of 21 yr (Pinedo & Hohn, Reference Pinedo and Hohn2000). The oldest reported male was 17 yr old in Rio Grande de Sul, Brazil (Botta et al., Reference Botta, Muelbert, Secchi, Danilewicz, Negri, Cappozzo and Hohn2010). In the sample from southern Buenos Aires studied in this work, the oldest individual was a male of 13 yr. Considering the age of sexual maturity and the reproductive rate of the species, the average franciscana may have between five and ten offspring (Danilewicz, Reference Danilewicz2003) during a lifetime. Therefore, the species reproductive flexibility might be limited under population impacts caused by incidental mortality in gillnets.
The ages determined for mature males and females of the studied sample in southern Buenos Aires, would seem to coincide with the age estimates of attainment of sexual maturity (ASM) estimated by the species in the region. Most sexually mature dolphins had ages higher than or equal to these estimates (ASMfemales = 4.3–4.5 yr, Corcuera, Reference Corcuera1996; ASMmales = 2.92–3.54 yr, Panebianco et al., Reference Panebianco, Negri and Cappozzo2012a).
As physical maturity of these dolphins occurs a few years after sexual maturity (Corcuera, Reference Corcuera1996; Botta, Reference Botta2005), a higher percentage of physically immature individuals was expected to be accidentally captured. 83% of the entanglements observed in this study corresponded to specimens that had not reached 90% of vertebral epiphyses fusion to the vertebral centra, that is, they were physically immature.
Even though incidental mortality appears to be biased towards young individuals, there does not seem to be a deviation with regards to sex-ratio as the proportion of females and males sampled in this study is not statistically different from parity. This is consistent with studies of other cetacean species that also suffer from incidental catch in gillnets (e.g. bottlenose dolphins Tursiops truncatus (Cockcroft, Reference Cockcroft1992), and Chilean dolphin Cephalorhynchus eutropia (Dawson, Reference Dawson1991)) and indicates that both sexes are equally vulnerable to by-catch. Differences found in the sex-ratio of franciscana dolphins captured in fishing nets appear to be explained by other factors. For example, between 1988 and 1990 Corcuera et al. (Reference Corcuera, Monzón, Crespo, Aguilar and Raga1994) observed a male-bias in franciscana catches in southern Buenos Aires province. However, these authors speculated that this was likely linked to the difficulty of handling the larger-sized females which may, therefore, have been discarded by fishermen. So comparisons of sex-ratios might take into account this potential bias in behaviour as well as potential changes of species habitat use, as discussed above.
Regarding the franciscana's body condition, Palomares et al. (Reference Palomares, Sorongon, Hunter, Pauly, Palomares and Pauly2008) found that values of b (allometric coefficient of W vs TL) ranged between 2.31 and 3.97 for 53 species of marine mammals. The estimated b of franciscana dolphins in this study (b = 2.118 ±0.124) is close to that range and is comparable to those reported for northern Buenos Aires (b = 2.22; Rodríguez et al., Reference Rodríguez, Rivero and Bastida2002) and for Rio Grande do Sul, Brazil (b = 2.07; Botta et al., Reference Botta, Muelbert and Secchi2006). Results presented showed that the mean relative index Kn is nearly 1. Therefore, it is likely that the body condition of the entangled franciscanas does not suggest any type of nutritional disorder. In addition, consistent with the findings for the southern coast (this study), Rodríguez et al. (Reference Rodríguez, Rivero and Bastida2002) did not observe differences in Kn between sexes and between immature and sexually mature by-caught individuals.
In cetaceans, the blubber layer constitutes the main source of energy reserves (Aguilar & Borrell, Reference Aguilar and Borrell1990). As postulated by Hanks (Reference Hanks, Fowler and Smith1981), the fat index can be considered a variation of energy reserves in the form of fat and an index of physiological condition of the animal and its relationship with the environment. Sexually mature individuals tend to have lower values of total body fat relative to body weight because they consume some of their energy reserves during breeding (Caon et al., Reference Caon, Fialho and Danilewicz2007). On the other hand, immature dolphins, expend much of their energy reserves to grow and maintain their body temperature because of their low surface area/volume ratios (Lockyer, Reference Lockyer1995; Denuncio, Reference Denuncio2012). Unlike the finding of Caon et al. (Reference Caon, Fialho and Danilewicz2007) for franciscana dolphins from southern Brazil, there were no significant differences in the fat index between sexes and sexual maturity stages from this study. This might be a consequence of the small number of sexually mature dolphins analysed. Also, the disparity found with northern Buenos Aires might be a consequence of many factors: the low number of by-caught dolphins analysed in the northern area, differences in the biological characteristics (age and length) of franciscanas, the diet of dolphins or the environmental conditions of each area (southern vs northern coast) or a combination of these factors.
Finally, as was stated before, the liver index might also be considered a nutritional indicator. In mammals and birds, fasting results in a significant reduction of body and liver mass (Krämer et al., Reference Krämer, Markwitan, Menne and Pallauf1993, Debacker et al., Reference Debacker, Jauniaux, Coignoul and Bouquegneau2000, Reference Debacker, Rutten, Jauniaux, Daemers and Bouquegneau2001). Taking into account the absence of differences in this index between areas and its stability in the ontogeny of the species, the values reported here might reflect not only a similar nutritional status but also the actual liver to total body mass ratio of healthy franciscanas.
Despite the fact that histopathological analyses were not performed on the franciscana sampled, the body condition indices studied indicate that gillnetting is not related to any sickness or deficiency in the physical condition of the dolphins in terms of physiology and nutrition. This is important, because captured dolphins may be considered a representative sample of a healthy population. Therefore, a study of the biology and ecology of franciscanas based on entangled dolphins would not lead to biased results.
In contrast, as postulated by Lockyer (Reference Lockyer1995) stranded animals may include a high proportion of sick and those in poor body condition, whilst by-catch animals may be healthier. In this sense, Das et al. (Reference Das, Siebert, Fontaine, Jauniaux, Holsbeek and Bouquegneau2004) reported that the body condition of stranded harbour porpoises was poor compared to that of by-catch individuals, as reflected by blubber thickness and hepatic to total body mass ratio. Moreover, despite a small sample size, Negri (Reference Negri2010) found statistically lower Kn and fat index values for stranded franciscanas compared to by-caught ones. Our results might be used as baseline data to better establish the post-mortem and the health conditions of stranded animals.
In conclusion, results reported here are important in the assessment of the impact of artisanal fisheries on the population of franciscana dolphins in the southernmost area of its distribution. This is particularly relevant because of the relative scarcity of information on biological parameters of franciscanas on the coast of Argentina. Moreover, the data presented may provide a basis to assess potential temporal changes in population parameters, thus improving management of franciscanas in this area.
ACKNOWLEDGEMENTS
This study would not have been possible without the unconditional collaboration of the artisanal fishing communities of southern Buenos Aires, and we are indebted to all of them. Many people collaborated with the fieldwork and we wish to thank: M. Negri, F. Pérez, R. Gutiérrez, D. del Castillo, V. Di Martino, A. Mandiola, G. Giardino, M. Dassis, P. Polizzi and L. Fainburg. We also want to thank the park rangers and personnel of the protected areas of the region: M. Sotelo, M.V. Massola and A. Areco; and the technicians of the Estación Hidrobiológica de Puerto Quequén: K. Arias and L. Nogueira. D. Molina Schiller, S. Botta and M.A. Raduán were of great help with age determination. We are very grateful to P. Penchaszadeh, P. Faillace and R. Bernabeu who helped us with their facilities. Thanks to J. Marigo and D. Danilewicz who read an earlier version of the manuscript. In addition, we are grateful to K. Guillozet for her help with the English language and to the referees of the manuscript for their helpful corrections and suggestions.
FINANCIAL SUPPORT
This work was carried out with the financial support of the University of Valencia, Yaqu Pacha, Fundación de Historia Natural Félix de Azara, Cetacean Society International and Society for Marine Mammalogy. This research project was part of M.F.N.'s PhD thesis for which the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) from Argentina granted her a postgraduate fellowship.
