[en] Harbour porpoises are the most common small cetaceans in the North Sea and Dutch coastal waters. To study their trophic level and feeding location, stable carbon and nitrogen isotope ratios (d13C and d15N) were analysed in muscle and bone samples collected from 157 porpoises stranded along the Dutch coast (20062008). In addition, samples from 30 prey species were analysed. Prey samples showed high d15N values in species of higher trophic level. In addition, geographic differences in isotopic composition were found, with higher d15N and d13C values in prey from more southern, coastal and estuarine areas. Based on muscle d15N values, we found neonatal enrichment and that larger porpoises, in particular males, seem to feed on lower trophic level species, compared to smaller individuals. Also bone d15N values show that larger animals had fed on lower trophic levels in distant times. Porpoises from the Eastern Scheldt reveal distinct d13C values in muscle, but not in bone. This shows that these animals had foraged in the Eastern Scheldt for a longer time period but were not born there. Seasonal variation in bone d15N and d13C values revealed two distinct groups of porpoises along the Dutch coast, a winter group (mainly males) that migrated from neighbouring regions and a Dutch subpopulation in summer. These results furthered our insight about shifts in trophic level and feeding location of harbour porpoises from the southern North Sea over time.
Research center :
MARE - Centre Interfacultaire de Recherches en Océanologie - ULiège
Disciplines :
Aquatic sciences & oceanology
Author, co-author :
Jansen, Okka
Geert, Aarts
Das, Krishna ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Océanologie
Lepoint, Gilles ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Océanologie
Michel, Loïc ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Systématique et diversité animale
Reijnders, Peter
Language :
English
Title :
Feeding ecology of harbour porpoises: stable isotope analysis of carbon and nitrogen in muscle and bone
Aarefjord, H, Bjørge, AJ, Kinze, CC and Lindstedt, I. 1995. Diet of harbour porpoise (Phocoena phocoena) in Scandinavian waters. Report of the International Whaling Commission, 16: 211-22.
Ambrose, SH. 1990. Preparation and characterization of bone and tooth collagen for isotopic analysis. Journal of Archaeological Science, 17: 431-51.
Andersen, LW, Ruzzante, DE, Walton, M, Berggren, P, Bjørge, A and Lockyer, C. 2001. Conservation genetics of harbour porpoises, Phocoena phocoena, in eastern central North Atlantic. Conservation Genetics, 2: 309-24.
Barnes, C, Jennings, S and Barry, JT. 2009. Environmental correlates of large-scale spatial variation in the δ 13C of marine animals. Estuarine Coastal and Shelf Science, 81: 368-74.
Bond, AL and Diamond, AW. 2011. Recent bayesian stable-isotope models are highly sensitive to variation in discrimination factors. Ecological Applications, 21: 1017-23.
Börjesson, P, Berggren, P and Ganning, B. 2003. Diet of harbor porpoises in the Kattegat and Skagerrak seas: Accounting for individual variation and sample size. Marine Mammal Science, 19: 38-58.
Budge, SM, Iverson, SJ and Koopman, HN. 2006. Studying trophic ecology in marine ecosystems using fatty acids: A primer on analysis and interpretation. Marine Mammal Science, 22: 759-801.
Burnham, KP and Anderson, DR. 2002. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach, 2nd edition, 488 pagesNew York, NY: Springer Verlag.
Camphuysen, CJ. 2011. Recent trends and spatial patterns in nearshore sightings of harbour porpoises (Phocoena phocoena) in the Netherlands (Southern Bight, North Sea), 1990-2010. Lutra, 54: 37-44.
Camphuysen, CJ. 2004. The return of the harbour porpoise (Phocoena phocoena) in Dutch coastal waters. Lutra, 47: 113-22.
Camphuysen, CJ, Smeenk, C, Addink, M, Van Grouw, H and Jansen, OE. 2008. Cetaceans stranded in the Netherlands from 1998 to 2007. Lutra, 51: 87-122.
Caut, S, Angulo, E and Courchamp, F. 2009. Variation in discrimination factors (Δ 15N and Δ 13C): the effect of diet isotopic values and applications for diet reconstruction. Journal of Applied Ecology, 46: 443-53.
Chauvenet W. 1863. A Manual of Spherical and Practical Astronomy, Vol II. New York, NY: Dover. 566 pages.
Christensen, JT and Richardson, K. 2008. Stable isotope evidence of long-term changes in the North Sea food web structure. Marine Ecology Progress Series, 368: 1-8.
Clementz, MT and Koch, PL. 2001. Differentiating aquatic mammal habitat and foraging ecology with stable isotopes in tooth enamel. Oecologia, 129: 461-72.
Cullen, JT, Rosenthal, Y and Falkowski, PG. 2001. The effect of anthropogenic CO 2 on the carbon isotope composition of marine phytoplankton. Limnology and Oceanography, 46: 996-98.
Dalerum, F and Angerbjörn, A. 2005. Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes. Oecologia, 144: 647-58.
Das, K, Lepoint, G, Leroy, Y and Bouquegneau, JM. 2003. Marine mammals from the southern North Sea: feeding ecology data from δ 13C and δ 15N measurements. Marine Ecology Progress Series, 263: 287-98.
Das, K, Holsbeek, L, Browning, J, Siebert, U, Birkun, A and Bouquegneau, J-M. 2004a. Trace metal and stable isotope measurements (δ 13C and δ 15N) in the harbour porpoise Phocoena phocoena relicta from the Black Sea. Environmental Pollution, 131: 197-204.
Das, K, Siebert, U, Fontaine, M, Jauniaux, T, Holsbeek, L and Bouquegneau, JM. 2004b. Ecological and pathological factors related to trace metal concentrations in harbour porpoises Phocoena phocoena from the North Sea and adjacent areas. Marine Ecology Progress Series, 281: 283-95.
DeNiro, MJ and Epstein, S. 1978. Influence of diet on distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta, 42: 495-506.
DeNiro, MJ and Epstein, S. 1981. Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta, 45: 341-51.
Folch, J, Lees, M and Stanley, GHS. 1957. A simple method for the isolation and purification of total lipides from animal tissues. Journal of Biological Chemistry, 226: 497-509.
Gaskin, DE. 1984. The harbour porpoise Phocoena phocoena (L.): Regional populations, status, and information on direct and indirect catches. Report of the International Whaling Commission, 34: 569-86.
Gómez-Campos, E. 2011. Nitrogen and carbon stable isotopes do not reflect nutritional condition in the striped dolphin. Rapid Communication in Mass Spectronomy, 25: 1343-47.
Habran, S, Debier, C, Crocker, DE, Houser, DS, Lepoint, GBouquegneau, JM. 2010. Assessment of gestation, lactation and fasting on stable isotope ratios in northern elephant seals. Marine Mammal Science, 26: 880-95.
Hammond, PS, Berggren, P, Benke, H, Borchers, DL, Collet, AHeide-Jørgensen, MP. 2002. Abundance of harbour porpoise and other cetaceans in the North Sea and adjacent waters. Journal of Applied Ecology, 39: 361-76.
Hammond PS. 2006. Small Cetaceans in the European Atlantic and North Sea (SCANS-II). LIFE04NAT/GB/000245, Sea Mammal Research Unit, St Andrews. 54 pages.
Hedges, REM. 2003. On bone collagen-apatite-carbonate isotopic relationships. International Journal of Osteoarchaeology, 13: 66-79.
Hobson, KA. 1999. Tracing origins and migration of wildlife using stable isotopes: A review. Oecologia, 120: 314-26.
Hobson, KA and Clark, RG. 1992a. Assessing avian diets using stable isotopes 2: Factors influencing diet-tissue fractionation. The Condor, 94: 189-97.
Hobson, KA and Clark, RG. 1992b. Assessing avian diets using stable isotopes 1: Turnover of 13C in tissues. The Condor, 94: 181-88.
Hobson, KA, Schell, DM, Renouf, D and Noseworthy, E. 1996. Stable carbon and nitrogen isotopic fractionation between diet and tissues of captive seals: Implications for dietary reconstructions involving marine mammals. Canadian Journal of Fisheries and Aquatic Sciences, 53: 528-33.
Hyslop, EJ. 1980. Stomach contents analysis-A review of methods and their application. Journal of Fish Biology, 17: 411-29.
Iverson, SJ, Field, C, Bowen, WD and Blanchard, W. 2004. Quantitative fatty acid signature analysis: A new method of estimating predator diets. Ecological Monographs, 74: 11-235.
Jacob, U, Mintenbeck, K, Brey, T, Knust, R and Beyer, K. 2005. Stable isotope food web studies: A case for standardized sample treatment. Marine Ecology Progress Series, 287: 251-53.
Jenkins, SG, Partridge, ST, Stephenson, TR, Farley, SD and Robbins, CT. 2001. Nitrogen and carbon isotope fractionation between mothers, neonates, and nursing offspring. Oecologia, 126: 336-41.
Kastelein RA, Hardeman J, Boer H. 1997. Food consumption and body weight of harbour porpoises (Phocoena phocoena). Chapter 4 in: Read AJ, Wiepkema PR, Nachtigall PE The Biology of the Harbour Porpoise. Woerden: De Spil Publishers, p 217-33.
Knijn RJ, Boon TW, Heessen HJL, Hislop JRG. 1993. Atlas of North Sea Fishes based on bottom-trawl survey data for the years 1985-1987. ICES Cooperative Research Report 194. 268 pages.
Koch PL. 2007. Isotopic study of the biology of modern and fossil vertebrates. Chapter 5 in: Michener R, Lajtha K Stable Isotopes in Ecology and Environmental Science. Oxford: Blackwell Publishing, p 99-154.
Kuiken T. 1996. Diagnosis of bycatch in cetaceans: Proceedings of the second ECS workshop on cetacean pathology. Montpellier, France, 2 March 1994. European Cetacean Society Newsletter 26, Special Issue. 43 pages.
Kurle, CM and Worthy, GAJ. 2002. Stable nitrogen and carbon isotope ratios in multiple tissues of the northern fur seal Callorhinus ursinus: Implications for dietary and migratory reconstructions. Marine Ecology Progress Series, 236: 289-300.
Lesage, V, Hammill, MO and Kovacs, KM. 2001. Marine mammals and the community structure of the Estuary and Gulf of St Lawrence, Canada: Evidence from stable isotope analysis. Marine Ecology Progress Series, 210: 203-21.
Lidén, K, Takahashi, C and Nelson, DE. 1995. The effects of lipids in stable carbon isotope analysis and the effects of NaOH treatment on the composition of extracted bone collagen. Journal of Archaeological Science, 22: 321-26.
Lockyer, C. 2003. Harbour porpoises (Phocoena phocoena) in the North Atlantic: Biological parameters. NAMMCO Scientific Publication, 5: 71-90.
MacLeod, CD, Pierce, GJ and Santos, MB. 2007. Starvation and sandeel consumption in harbour porpoises in the Scottish North Sea. Biology Letters, 3: 535-36.
Michener RH, Kaufman L. 2007. Stable isotope ratios as tracers in marine food webs: An update. Chapter 9 in: Michener RH, Lajtha K Stable Isotopes in Ecology and Environmental Science. Boston, MA: Blackwell Publishing, p 238-82.
Moore, KM, Murray, ML and Schoeninger, MJ. 1989. Dietary reconstruction from bones treated with preservatives. Journal of Archaeological Science, 16: 437-46.
Newsome, SD, Clementz, MT and Koch, PL. 2010. Using stable isotope biogeochemistry to study marine mammal ecology. Marine Mammal Science, 26: 509-72.
Nienhuis, PH and Smaal, AC. 1994. The Oosterschelde estuary, a case study of a changing ecosystem: An introduction. Hydrobiologia, 282/283: 1-14.
O'Regan, HJ, Chenery, C, Lamb, AL, Stevens, RE, Rook, L and Elton, S. 2008. Modern macaque dietary heterogeneity assessed using stable isotope analysis of hair and bone. Journal of Human Evolution, 55: 617-26.
Phillips, DL and Eldridge, PM. 2006. Estimating the timing of diet shifts using stable isotopes. Oecologia, 147: 195-203.
Pierce GJ, Allcock L, Bruno I, Bustamante P, González A, Guerra A, et al. 2010. Cephalopod biology and fisheries in Europe. ICES Cooperative Research Report 303. 175 pages.
Pierce, GJ and Boyle, PR. 1991. A review of methods for diet analysis in piscivorous marine mammals. Oceanography and Marine Biology, 29: 409-86.
Post, DM. 2002. Using stable isotopes to estimate trophic position: Models, methods, and assumptions. Ecology, 83: 703-18.
R Development Core Team. 2009. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Computer program. www.R-project.org. (accessed in April 2012).
Recchia, CA and Read, AJ. 1989. Stomach contents of harbour porpoises, Phocoena phocoena (L.), from the Bay of Fundy. Canadian Journal of Zoology, 67: 2140-46.
Richards, MP, Mays, S and Fuller, BT. 2002. Stable carbon and nitrogen isotope values of bone and teeth reflect weaning age at the medieval Wharram Percy site, Yorkshire, UK. American Journal of Physical Anthropology, 119: 205-10.
Santos, MB and Pierce, GJ. 2003. The diet of harbour porpoise (Phocoena phocoena) in the northeast Atlantic. Oceanography and Marine Biology: an Annual Review, 41: 355-90.
Santos, MB, Pierce, GJ, Learmonth, JA, Reid, RJ, Ross, HMPatterson, IAP. 2004. Variability in the diet of harbor porpoises (Phocoena phocoena) in Scottish waters 1992-2003. Marine Mammal Science, 20: 1-27.
Sealy, J, Armstrong, R and Schrire, C. 1995. Beyond lifetime averages: Tracing life histories through isotopic analysis of different calcified tissues from archaeological human skeletons. Antiquity, 69: 290-300.
Smith, GJD and Gaskin, DE. 1983. An environmental index for habitat utilization by female harbour porpoises with calves near Deer Island, Bay of Fundy. Ophelia, 22: 1-13.
Smith, RJ and Read, AJ. 1992. Consumption of euphausiids by harbor porpoise (Phocoena phocoena) calves in the Bay of Fundy. Canadian Journal of Zoology, 70: 1629-32.
Sotiropoulos, MA, Tonn, WM and Wassenaar, LI. 2004. Effects of lipid extraction on stable carbon and nitrogen isotope analyses of fish tissues: Potential consequences for food web studies. Ecology of Freshwater Fish, 13: 155-60.
Teilmann, J and Dietz, R. 1998. Status of the harbour porpoise in Greenland. Polar Biology, 19: 211-20.
Thomsen, F, Laczny, M and Piper, W. 2006. A recovery of harbour porpoises (Phocoena phocoena) in the southern North Sea? A case study off Eastern Frisia, Germany. Helgoland Marine Research, 60: 189-95.
Tieszen, LL, Boutton, TW, Tesdahl, KG and Slade, NA. 1983. Fractionation and turnover of stable carbon isotopes in animal tissues: Implications for δ 13C analysis of diet. Oecologia, 57: 32-37.
Walton, MJ. 1997. Population structure of harbour porpoises Phocoena phocoena in the seas around the UK and adjacent waters. Proceedings of the Royal Society of London Series B Biological Sciences, 264: 89-94.
Witt, GB. 2001. Carbon isotope variability in the bone collagen of red kangaroos (Macropus rufus) is age dependent: Implications for palaeodietary studies. Journal of Archaeological Science, 28: 247-52.
Worthy, GAJ and Edwards, EF. 1990. Morphometric and biochemical factors affecting heat loss in a small temperate cetacean (Phocoena phocoena) and a small tropical cetacean (Stenella attenuata). Physiological Zoology, 63: 432-42.
Yurick, DB and Gaskin, DE. 1987. Morphometric and meristic comparisons of skulls of harbor porpoise Phocoena phocoena (L.) from the North Atlantic and North Pacific. Ophelia, 27: 53-75.
