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Terrestrial Support of Aquatic Food Webs

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Presentation by Dr. Jonathan J. Cole, Cary Institute of Ecosystem Studies

Starting in its earliest development, limnology has tended to view lakes as rather isolated from their terrestrial watersheds. This view of lakes as microcosms (Forbes 1887) proved useful in some ways, but it failed to help explain phenomena such as eutrophication which is driven by the external input of nutrients. While the study of limiting nutrients has fully embraced the watershed for decades, the study of C cycling in lakes has maintained a somewhat microcosm viewpoint. This is a viewpoint in which organic C is envisioned as being formed almost entirely by photosynthesis within the system (autochthonous sources); exogenous sources are largely ignored, downplayed, or assumed to be refractory. A number of disparate research threads in recent decades have completely overturned this view.

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Terrestrial Support of Aquatic Food Webs

  1. 1. THANKS! • To the National Science Foundation- OPUS program- Ecosystem Studies • To the Cary Institute of Ecosystem Studies • To my colleagues for working with me. • To my colleagues for putting up with me. • To Inter-Research for the ECI Award
  2. 2. Terrestrial support of Aquatic Food Webs • This talk summarizes two chapters from a recent book: • Cole, J.J. 2013. “Freshwater ecosystems and the carbon cycle”. In: Kinne O (ed) Excellence in ecology. Book 18. International Ecology Institute, Oldendorf/Luhe 146 pp. • The honor and obligation for writing the book came from winning the Excellence in Ecology Prize from Inter-Research. • The financial support needed to complete the book came from the National Science Foundation OPUS Program from Ecosystem Studies and from the Cary Institute of Ecosystem Studies. • The book is available at http://www.int-res.com/book- series/excellence-in-ecology-books/ee18/
  3. 3. Terrestrial support of lake food webs (and some lake- like rivers: A review How much of the biomass of these fish came from aquatic versus terrestrial photosynthesis?
  4. 4. Outline • Refine the question • Review (briefly) the extant literature and the weight of scientific opinion on the terrestrial fraction in lakes (and lake like rivers) for: – Fishes – Benthic invertebrates – zooplankton – DOC and POC • Present a few summary patterns that have emerged • Suggest some ideas for research needs
  5. 5. Refining the Questions we are and are not asking • What fraction of a consumer’s biomass (or a detrital compartment) is derived ultimately from terrestrial versus aquatic photosynthesis? • How much new growth of consumers in supported by terrestrial organic matter? • Does terrestrial organic matter subsidize (e.g. enhance) the growth of aquatic consumers? • It may be the case that terrestrial organic matter contributes to the biomass of aquatic consumers and at the same times inhibits their growth. That is, terrestrial organic matter, while not great food, is sometimes the food that is available (Marcarelli et al. 2010; Jones et al. 2012; Kelly et al. 2014)
  6. 6. Fishes • 18 published Studies from 1982 to 2012 • Many involve multiple lakes, multiple spp. • Details in Cole (2013 ECI Book). • Methods – Diet studies 3 – Diet plus stable isotopes 3 – Stable isotopes (13C and/or 15N) 9 – Stable isotopes (2H and/or 13C,15N) 2 – Organic biomarkers 1 • Range is 0 to 100% terrestrial • 10 studies (56%) find >20% terrestrial support for at least one taxon. Some much more. Several studies qualitative only.
  7. 7. Amazon at flood stage- trees are covered to near crowns Tambaqui- eats terrestrial nuts from trees – has specialized teeth Colossoma macropomum Some fishes are terrestrial specialists
  8. 8. The Tambaqui is also eat by people
  9. 9. Francis and Schindler (2009); Oncorynchus spp. Diet study. Pacific NW lakes – intensive study Pacific NW survey Literature N. America
  10. 10. Proportionterrestrialingizzardshad Babler et al. 2011. Gizzard shad. d2H study. 11 lakes or reservoirs in Ohio.
  11. 11. Benthic Invertebrates • 13 published studies from 1980 to 2014. • Many involve multiple lakes, multiple spp. • Details in Cole (2013) Book. (excepting Berggren et al. 2014). • Methods – Diet studies 0 – Stable isotopes (13C and/or 15N) 8 – Stable isotopes (2H and/or 13C,15N) 4 – Organic biomarkers plus isotopes 1 • Range is 0 to 100% terrestrial among taxa and system • ALL studies (100%) find >20% terrestrial support for at least one taxon.
  12. 12. Larson et al. 2011. Crayfish (Pacifastacus leniusculus). Lakes in the Pacific NW. Literature data (filled circles); new data (open circle). 13C gradient study.
  13. 13. Karube et al. 2010. Lake Biwa (littoral) 13C study. Snail (Semisculcopira spp.) and bivalve (Unio douglasiae biwae)
  14. 14. Zooplankton • 27 published studies from 1993 to 2014. • Many involve multiple lakes, multiple spp. • Details in Cole (2013) Book. (excepting Berggren et al. Ecol, IN PRES). • Methods – Stable isotopes (13C and/or 15N) 12 – Stable isotopes (2H and/or 13C,15N) 6 – Ambient 14C 1 – 13C additions (whole lake or mesocosm) 4 – Organic biomarkers 1 – Organic biomarkers plus isotopes 1 – Model or mass balance 2 • Range is 0 to 80% terrestrial among taxa and system • 22 studies (81%) find >20% terrestrial support for at least one taxon.
  15. 15. Phyto. SAV FlAV Phyto. SAV FlAV Ancient. Terrestrial Modern Terrestrial. Zoo. Ancient. Terrestrial Modern Terrestrial. Zoo. -400 -300 -200 -100 0 100 -35 -30 -25 -20 -400 -300 -200 -100 0 100 -250 -200 -150 -100 d13C (o/oo) dD (o/oo) D14C(o/oo) Caraco et al. 2010; Hudson River Hudson River; 14C and stable isotopes Mixing model suggest cladocerans ~ 35% terrestrial; copepods ~25%
  16. 16. Caraco et al. 2010 (same study). Small particles are the most 14C depleted. Cladocerans (Bosmina) are “older” than copepods. The old particles cannot be auotochthonous – must be imported from the watershed.
  17. 17. Wilkinson et al. 2013. d2H gradient study for 39 lakes (Chaoborus spp) and 15 lakes cladocerans and copepods. Both dietary water and terrestrial veg pull values away from phytoplankton. Terrestrial vegetation
  18. 18. - Wilkinson et al. 2013 (same study). Bayesian mixing model including uncertainty for: End member estimates; Dietary water correction; Analytical error cladocerans copepods Small, high DOC ,low pH For lakes that had deep chl. maxima- model could be run with metalimnetic phytoplankton also. No difference in the resulting terrestrial fraction.
  19. 19. DOC, POC gradient study with 13C. 13 lakes in Sweden. Data from J. Karlsson (several papers). 13C gradient study. Simple mixing model: POC 80% to 95% terrestrial on average DOC >90% terrestrial on average.
  20. 20. δ2H of Water δ2HofPOMorDOM Wilkinson et al. 2013, GCB. d2HGradient study 39 lakes chosen to range from oligotrophic to highly eutrophic. POM DOM DOM basically entirely terrestrial. POM ranges from <10% to >90% terrestrial. Get same results using d13C .
  21. 21. Rank FractionPOMTerrestrial Wilkinson et al. 2013 same study Small. High DOC, low pH Eutrophic or large
  22. 22. t-POC detrital algal POC Low DOC lake. mestotrophic large; 15 m deep; DOC 3 mg/L; chl-a 10 g/L DOC T = 75%; POC High DOC lake. oligotrophic small; 5 m deep; DOC 10 mg/L; chl-a 1 g/L DOC T = 99%; POC detrital algal POC t-POC live phytoplankton algal DOC DOC (75% terrestrial) DOC (99% terrestrial) How much OC in a lake is of terrestrial origin? Look at two extremes. 1) Small, humic lake. Autochthonous OC (detrital + living) is small, <0.8% of total OC. 2) Large, mesotrophic lake, autochthonous OC is 25% of total. SEDIMENTS?? Total OC 52 g C m-2 Total OC 64 g C m-2
  23. 23. What about deep autochthonous sources? • Some primary production occurs in the metalimnion. • It may be different isotopically from that produced in surface waters. Usually more depleted in 13C and 2H. • This potential additional source can be a confounding factor in mixing models if it is a significant food source to zooplankton.
  24. 24. Two direct experiments to test the importance of metalimnetic primary production to zooplankton • Armengol et al (2012) added 15N-ammonium to the metalimnion of a small lake in Spain. Seston near the metalimnion was highly labeled with 15N. • Zooplankton collected either during the day or night were NOT labeled with the added 15N. • Wilkinson et al. (2014) labeled a 2-m thick layer of the metalimnion in small lake with 13C as DIC. • The DIC of that layer was highly enriched in a 2-m thick layer that occupied the entire layer of the metalimnion. • Zooplankton collected during the day or night in epilimnetic waters were not labeled with the added 13C.
  25. 25. N‰ 20 40 60 80 100 120 Depth(meters) zooplankton day zooplankton night seston 0 5 10 15 20 25 Armengol et al. 2012. 15N addition to chl maximum in a small lake. Phytoplankton took up the 15N at the metalimnion but zooplankton did not become labeled. “day” and “night” refer to the times zooplankton were collected. Zooplankton were not significantly consuming phytoplankton from the metalimnion.
  26. 26. Conclusions • Most authors who have looked for terrestrial support of aquatic consumers have found evidence for it. • Much of the POM and most of the DOM standing stocks is of terrestrial origin. • Evidence for terrestrial support of some fishes is inarguable. • For the stable isotope studies, (benthic inverts and zooplankton) the data is consistent with terrestrial support in many cases but this does not constitute proof. • A few studies, those over gradients, and or with multiple approaches are very convincing. • Terrestrial support: highest in small, humic lakes; lowest in large or eutrophic lake.
  27. 27. Research Suggestions. • Sediments- data is very sparse, methods not yet ideal. • Very little data on bacteria. Emma Kritzberg (several papers 2004-2006; Martin Berggren Ecol. IN PRESS); Leigh McCalister (for a river). • Reconcile C budgets with isotopic evidence of origin of carbon pools. • More studies over convincing and useful gradients (lake size, eutrophication, shoreline development etc). • Studies that use multiple methods are the most convincing.
  28. 28. For a 13C addition to a metalimnion: • Grace Wilkinson et al. “Results of a whole lake metalimnetic 13C addition to test habitat specific resource use by zooplankton” • Monday, Abstract. Session #:026 • Paper In Press in L&O. • The most important resource for zooplankton was terrestrial organic matter (56-73%) regardless of habitat. • …in lakes like Peter Lake, metalimnetic autochthonous resources are of minor importance to zooplankton…

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