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What can a multi tracer approach tell us about the ecology of two sympatric species of Globicephala genus?

Silvia S. Monteiro1, 2*, Florence Caurant3, Alfredo López1, 4, José Cedeira4, Marisa Ferreira2, 5, José V. Vingada2, 6, Catarina Eira1, 2 and Paula Méndez-Fernandez7
  • 1 Universidade de Aveiro, Departamento de Biologia & CESAM, Portugal
  • 2 Universidade de Minho, Sociedade Portuguesa de Vida Selvagem, Portugal
  • 3 UMR 7372 CNRS-ULR, Centre d’Études Biologiques de Chizé, France
  • 4 Coordinadora para o Estudio dos Mamíferos Mariños (CEMMA), Spain
  • 5 Universidade de Minho, Departamento de Biologia & CBMA, Portugal
  • 6 Universidade de Minho, Departamento de Biologia & CESAM, Portugal
  • 7 Oceanographic Institute of the University of São Paulo, Brazil

Recent legal frameworks (e.g. Marine Strategy Framework Directive) emphasize the importance of understanding the ecological status and impact of anthropogenic threats on marine populations. Biogeochemical tracers (e.g. stable isotopes, fatty acids, trace elements, persistent organic pollutants) have been increasingly used as efficient tools to obtain a multitude of information regarding habitat and feeding habits and contamination status of marine mammal populations, on different time-scales. In this study, a multi-tracer approach was used to infer information regarding the feeding ecology, contamination status and ecological segregation of two sympatric species of the Globicephala genus in the North-west of the Iberian Peninsula (NWIP): the anti-tropical long-finned pilot whale (LFPW, Globicephala melas) and the tropical short-finned pilot whale (SFPW, Globicephala macrorhynchus). Additionally, the potential influence of biological variables, such as length (as proxy of age) was also investigated in each species. To that purpose, stable isotopes (δ13C and δ15N) in skin and renal and hepatic concentrations of 14 trace elements were measured in 24 stranded individuals (13 SFPW from a mass stranding and 11 LFPW from individual strandings). Stable isotope analyses were performed with an elemental analyser coupled to an Isoprime (Micromass) continuous-flow isotope ratio mass spectrometer. The trace elements (i.e. Ag, As, Cd, Co, Cr, Cu, Fe, Mn, Ni, Pb, Se, V and Zn) were analysed with an Inductively Coupled Plasma Atomic Emission Spectrophotometer and an Inductively Coupled Plasma Mass Spectrometer, while total Hg was determined using an Advanced Mercury Analyser (Altec AMA 254). Regarding skin isotopic composition, the mean values of δ13C and δ15N in LFPW were -17.9±0.7 and 12.1±1.0‰ respectively, while in SFPW they were -17.5±0.3 and 11.9±0.3‰, respectively. A higher variation was observed in LFPW stable isotopes. Concerning trace element analyses, in both species, Fe showed the highest concentrations of essential elements, while hepatic Hg and renal Cd presented the highest concentrations within non-essential elements. Inter-specific comparison of biogeochemical tracers revealed that skin stable isotopes (δ13C and δ15N) showed no significant differences, while hepatic Ag, Cd, Co, Hg, Pb, Se concentrations and renal Ag, Cu, Hg and Se concentrations were significantly different between species. In particular, SFPW exhibited significantly higher concentrations of hepatic Cd, Co and Pb and Ag, Hg and Se in both tissues, against the higher renal Cu levels shown by LFPW. Inter-specific differences were further corroborated by discriminant analyses based on stables isotopes and non-essential trace elements (i.e. Hg, Cd, Ag, Pb), which revealed a good separation of the species, with more than 80% of individuals well classified in each species group. Considering the shorter time-scale represented by skin stable isotopes (i.e. 1–3 months, Abend and Smith 1995) compared with the trace elements (e.g. > 10 years for renal Cd, Stoeppler 1991), it seems that recent foraging habits or habitats of both SFPW and LFPW are similar, suggesting a weak ecological segregation of these species in the stranding area (NWIP). In contrast, the stronger inter-specific differences in trace elements burdens ultimately suggest a stronger ecological segregation between species at a longer-term scale. This long-term inter-specific differences found in some hepatic and renal trace elements (e.g. Cd, Hg) may be due to: 1) differences in feeding preferences or prey availability, 2) differences in habitat or geographical areas, which may lead to exposure to different gradients of trace elements concentrations and/or environmental conditions, 3) metabolic differences between species. Hence, the results of the present study suggest that when both SFPW and LFPW are present in NWIP, they show similar feeding patterns at least in a short time-scale. However, in a longer time-scale these species may exhibit different feeding preferences and may occupy different habitats in this same area (e.g. oceanic vs. neritic). Alternatively, outside the period when they are both in NWIP, SFPW and LFPW may occupy different geographic regions (e.g. tropical vs. temperate regions) where they are exposed to different gradients of non-essential trace elements and environmental conditions that may ultimately influence the long-term integration of some trace element. At last, the discrepancies observed in trace elements in Globicephala species may also result from specific metabolic characteristics specially related to absorption and/or elimination processes. Additionally, the present study provides crucial information about the contamination status of the Globicephala individuals stranded in NWIP and represents the first record of trace element concentrations of SFPW in this area of the Northeast Atlantic. The SFPW seem to be more at risk compared to LFWP considering the higher concentrations of non-essential trace element, especially mercury. In particular, 54% of the SFPW have shown mean hepatic mercury concentrations higher than the threshold proposed for liver damage in mammals (60 µg/g wet weight, Rawson et al. 1993).Analysis of the contamination status of SFPW, in combination with future analysis of the health status of these animals (e.g. histopathology, virology, bacteriology, POPs analysis, among others), may help clarify the reason for the occurrence of this mass stranding event. In the present study there was influence of animal length (as proxy of age) on the bioaccumulation of some trace elements concentrations in each species. Linear models revealed a significant influence of this variable in the hepatic concentrations of Hg, Se and renal concentrations of Fe, Mn for SFPW, whereas in LFPW, the animal length affected the hepatic concentrations of Co, Hg, Se and renal concentrations of Ag, Co and Hg. In all situations, except for hepatic Mn, trace element concentrations increased with animal length. A long-term exposure to non-essential trace elements associated to a long half-life of these contaminants in marine mammals may explain their higher bioaccumulation in older cetaceans (e.g. Gaskin et al. 1979, Aguilar et al. 1999). In turn, relationship between essential trace elements and animal length seem to be related to their involvement in the elimination of non-essential elements (e.g. Se) or to metabolic requirements (e.g. Mn, Fe). In conclusion, although the potential influence of sampling bias (e.g. social structure, strandings) cannot be completely discarded, the present study provides useful information regarding the habitat and feeding preferences, as well as contamination status and ecological segregation of species belonging to the Globicephala genus.

References

Abend AG, Smith TD (1995) Differences in ratios of stable isotopes of nitrogen in long-finned pilot whales (Globicephala melas) in the western and eastern North Atlantic. ICES J Mar Sci 52: 837−841.
Aguilar A, Borrell A, Pastor T (1999) Biological factors affecting variability of persistent pollutant levels in cetaceans [special issue]. J Cetac Res Manage 1:83–116.
Gaskin DE, Stonefield KI, Suda P, Frank R (1979) Changes in mercury levels in harbour porpoises from the bay of Fundy, Canada and adjacent waters during 1969- 1977. Arch Environ Contam Toxicol 8:33–62.
Rawson AL, Patton GW, Hofmann S, Pietra GG, Johns L (1993) Liver abnormalities associated with chronic mercury accumulation in stranded Atlantic bottlenose dolphins. Ecotoxicol Environ Saf 25: 41–47.
Stoeppler M (1991) Cadmium. In: Merian E, Clarson TW (eds). Metal and their compounds in the environment. VCH, New York, p 803–851.

Keywords: Stable isotopes, Trace Elements, feeding ecology, Ecological segregation, bioaccumulation, North-west of the Iberian Peninsula, Pilot whales

Conference: XIX Iberian Symposium on Marine Biology Studies, Porto, Portugal, 5 Sep - 9 Sep, 2016.

Presentation Type: Oral Presentation

Topic: 1. ECOLOGY, BIODIVERSITY AND VULNERABLE ECOSYSTEMS

Citation: Monteiro SS, Caurant F, López A, Cedeira J, Ferreira M, Vingada JV, Eira C and Méndez-Fernandez P (2016). What can a multi tracer approach tell us about the ecology of two sympatric species of Globicephala genus?. Front. Mar. Sci. Conference Abstract: XIX Iberian Symposium on Marine Biology Studies. doi: 10.3389/conf.FMARS.2016.05.00086

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Received: 27 Apr 2016; Published Online: 02 Sep 2016.

* Correspondence: PhD. Silvia S Monteiro, Universidade de Aveiro, Departamento de Biologia & CESAM, Aveiro, Aveiro, 3810-193 Aveiro, Portugal, silvia.sm.monteiro@gmail.com