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.

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. 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. 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. 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. 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. 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. 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. The Tambaqui is also eat by people

9. Francis and Schindler (2009); Oncorynchus spp. Diet study.
Pacific NW lakes – intensive study
Pacific NW survey
Literature N. America

10. Proportionterrestrialingizzardshad
Babler et al. 2011. Gizzard shad.
d2H study. 11 lakes or reservoirs
in Ohio.

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. Larson et al. 2011. Crayfish (Pacifastacus leniusculus). Lakes in
the Pacific NW. Literature data (filled circles); new data
(open circle). 13C gradient study.

13. Karube et al. 2010. Lake Biwa (littoral) 13C study. Snail
(Semisculcopira spp.) and bivalve (Unio douglasiae biwae)

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. 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. 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. 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. - 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. 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. 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. Rank
FractionPOMTerrestrial
Wilkinson et al. 2013 same study
Small. High
DOC, low pH
Eutrophic or
large

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. 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. 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. 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. 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. 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.

29. 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…