Structure of intestinal helminth communities of the striped dolphin, Stenella coeruleoalba, in the western Mediterranean: a long-term analysis
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1
University of Valencia, Cavanilles Institute of Biodiversity and Evolutionary Biology, Spain
Over the last decades, the western Mediterranean population of striped dolphins, Stenella coeruleoalba, has suffered significant environmental impacts. Firstly, the population suffered two epizootic events in 1990 and 2007 caused by the Dolphin Morbillivirus, or DMV (Raga et al. 2008). The first die-off was particularly severe and could have killed several thousands of individuals (Aguilar and Raga 1993). Secondly, there is correlational evidence that overfishing of a putative key prey species, the sardine, Sardina pilchardus, might have caused a significant dietary shift of dolphins towards demersal prey, particularly hake, Merluccius merluccius (Gómez-Campos et al. 2011). A hake-dominated diet could provide lower energy content resulting in long-term problems for the energetic balance of dolphins (Gómez-Campos et al. 2011).
Trophically-transmitted helminths are considered suitable tags to explore spatial and temporal changes, not only of their hosts’ populations, but also of local trophic webs (Marcogliese 2005). Striped dolphins harbour a depauperate intestinal community of trophically-transmitted helminths. However, it is composed of cestodes and acanthocephalans that presumably use several intermediate and paratenic (transport) hosts in their life cycles (Mateu et al. 2014), thus having the potential to trace changes in the food web. In this study we investigated how the dietary shift, and the viral outbreaks that striped dolphins have suffered over the last decades could have impacted its intestinal helminth fauna.
The intestine of 202 striped dolphins that were stranded along the coast of east Spain in the period 1990-2015 was analyzed for helminths. Two subsamples were initially considered, i.e., ‘epizootic’ (dolphins killed by the DMV; n= 73 for 1990 and n= 16 for 2007) and ‘non-epizootic’ (dolphins dead from other causes; n= 113). Differences of helminth community structure between both subsamples were examined with one-way PERMANOVA (Anderson et al. 2008). Years were arranged into five groups, namely 1 (1990), 2 (1991-1998), 3 (1999-2006), 4 (2007) and 5 (2008-2015). A full model including host length, sex, season, and year group was analyzed with PERMANCOVA. Temporal trends for abundance of helminth species were explored with LOESS functions with 95% confidence intervals being generated with 1000 bootstrapped LOESS regression curves (Efron 2005). To investigate the identity of Bolbosoma vasculosum we compared genetic distances and applied phylogenetic analyses on partial sequences of 18S, 28S and COI from 2 individuals and those from other species of Bolbosoma.
Four calves (body length < 100 cm) were uninfected and excluded from further analyses. A total of 6 helminth species were found, including the cestodes Tetrabothrius forsteri (frequency of occurrence: 95.5%, mean abundance in infected dolphins (SD) [range]: 47.3 (73.4) [1-518]), Trigonocotyle lintoni (6.0%, 2.8 (2.0) [1-6]) and Strobilocephalus triangularis (15.2%, 13.3 (19.0) [1-81]), and immature acanthocephalans of the genus Bolbosoma, i.e. B. vasculosum (16.7%, 2.4 (1.8) [1-7]), B. capitatum (a single individual) and B. balaenae (single individuals in two dolphins). Bolbosoma vasculosum was closely related to B. capitatum, raising the possibility that both taxa are conespecific. There were no significant differences in the helminth community structure of ‘epizootic’ vs. ‘non-epizootic’ dolphins. The PERMANCOVA model selected ‘year group’ as the only significant predictor. Dolphins from group 1 differed from the others by the moderate occurrence of B. vasculosum (43.8%), which only further appeared in a single dolphin from group 2. Apart from this, LOESS models detected no apparent temporal trends in infection levels of other helminths.
Results suggest that the helminth fauna of striped dolphins were not specifically affected by DMV symptoms, which include a fasting period prior to death. Also, helminth community structure was surprisingly stable over the years, except for the high prevalence of B. vasculosum in 1990. This observation is puzzling. Striped dolphins act as non-hosts for B. vasculosum but it is unclear what the definitive (cetacean) hosts are (Mateu et al. 2014). The effect of temporal inertia on infection levels in paratenic (fish) hosts rules out that the parasite was only available for striped dolphins in 1990. Perhaps the dietary shift of dolphins minimized later contacts with B. vasculosum, but the change of infection was too sudden. Further research on the life cycle of this parasite species is necessary to shed light on this issue.
Acknowledgements
This study was supported by projects CGL/2012/39545 (Ministry of Economy and Competitiveness, Spain), and PROMETEO II/2015/018 (Generalitat Valenciana, Spain).
References
Aguilar A and Raga JA. (1993). The striped dolphin epizootic in the Mediterranean Sea. Ambio 22: 524-528.
Anderson MJ, Gorley RN and Clarke KR. (2008). PERMANOVA þ for PRIMER: guide to software and statistical methods. 214 pp. Plymouth, PRIMER-E Ltd.
Efron B. (2005). Bayesians, frequentists, and scientists. Journal of the American Statistical Association 100: 1–5.
Gómez-Campos, E., Borrell, A., Cardona, L., Forcada, J. and Aguilar, A. (2011) Overfishing of small pelagic fishes increases trophic overlap between immature and mature striped dolphins in the Mediterranean Sea. Plos One 6: e24554.
Marcogliese DJ. (2005). Parasites of the superorganism: are they indicators of ecosystem health? International Journal for Parasitology 35:705-16.
Mateu P, Raga JA, Fernández M and Aznar FJ. (2014). Intestinal helminth fauna of striped dolphins (Stenella coeruleoalba) in the western Mediterranean: No effects of host body length, age and sex. Marine Mammal Science 30: 961–977.
Raga JA, Banyard A, Domingo M, Corteyn M, Van Bressem MF, Fernández M, Aznar FJ, Barrett T. (2008). Dolphin Morbillivirus epizootic resurgence, Mediterranean Sea. Emerging Infectious Diseases 14: 471–473.
Keywords:
Helminths,
Stenella coeruleoalba,
Long-term study,
Morbillivirus,
Dietary shift,
Cetaceans,
Bolbosoma,
Tetrabothrius,
Strobilocephalus,
Trigonocotyle,
Cestodes,
Acanthocephala
Conference:
IMMR | International Meeting on Marine Research 2016, Peniche, Portugal, 14 Jul - 15 Jul, 2016.
Presentation Type:
Poster presentation
Topic:
Biodiversity, Conservation and Coastal Management
Citation:
Aznar
FJ,
Sanz Tamarit
R,
Mateu Puncel
P,
Cervera Estevan
C,
Fraija Fernández
N,
Raga Esteve
J and
Fernández Martínez
M
(2016). Structure of intestinal helminth communities of the striped dolphin, Stenella coeruleoalba, in the western Mediterranean: a long-term analysis.
Front. Mar. Sci.
Conference Abstract:
IMMR | International Meeting on Marine Research 2016.
doi: 10.3389/conf.FMARS.2016.04.00084
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Received:
11 May 2016;
Published Online:
13 Jul 2016.
*
Correspondence:
Dr. Francisco J Aznar, University of Valencia, Cavanilles Institute of Biodiversity and Evolutionary Biology, Paterna, Valencia, 46980, Spain, francisco.aznar@uv.es