Forests fuel fish growth in freshwater deltas

Aquatic ecosystems are fuelled by biogeochemical inputs from surrounding lands and within-lake primary production. Disturbances that change these inputs may affect how aquatic ecosystems function and deliver services vital to humans. Here we test, using a forest cover gradient across eight separate catchments, whether disturbances that remove terrestrial biomass lower organic matter inputs into freshwater lakes, thereby reducing food web productivity. We focus on deltas formed at the stream-lake interface where terrestrial-derived particulate material is deposited. We find that organic matter export increases from more forested catchments, enhancing bacterial biomass. This transfers energy upwards through communities of heavier zooplankton, leading to a fourfold increase in weights of planktivorous young-of-the-year fish. At least 34% of fish biomass is supported by terrestrial primary production, increasing to 66% with greater forest cover. Habitat tracers confirm fish were closely associated with individual catchments, demonstrating that watershed protection and restoration increase biomass in critical life-stages of fish.

[1]  Hari Seshan,et al.  Phytoplankton, not allochthonous carbon, sustains herbivorous zooplankton production , 2009, Proceedings of the National Academy of Sciences.

[2]  John M. Gunn,et al.  Restoration and Recovery of an Industrial Region , 1995 .

[3]  J. Neff,et al.  Dissolved Organic Carbon in Alaskan Boreal Forest: Sources, Chemical Characteristics, and Biodegradability , 2007, Ecosystems.

[4]  S. Carpenter,et al.  Carbon and water cycling in lake‐rich landscapes: Landscape connections, lake hydrology, and biogeochemistry , 2007 .

[5]  P. Sale,et al.  Application of otolith analyses to investigate broad size distributions of young yellow perch in temperate lakes , 2001 .

[6]  James H. Brown,et al.  A general model for ontogenetic growth , 2001, Nature.

[7]  J. Cole,et al.  BACTERIAL GROWTH EFFICIENCY IN NATURAL AQUATIC SYSTEMS , 1998 .

[8]  C. Solomon,et al.  Subsidy or Subtraction: How Do Terrestrial Inputs Influence Consumer Production in Lakes? , 2012 .

[9]  A. Andersson,et al.  Impacts of elevated terrestrial nutrient loads and temperature on pelagic food‐web efficiency and fish production , 2013, Global change biology.

[10]  Don Monteith,et al.  Alternative explanations for rising dissolved organic carbon export from organic soils , 2006 .

[11]  M. Huss,et al.  Bottom–up carbon subsidies and top–down predation pressure interact to affect aquatic food web structure , 2011 .

[12]  M. I C H A E,et al.  The role of highly unsaturated fatty acids in aquatic foodweb processes , 1997 .

[13]  Jeffrey N. Houser,et al.  Water color affects the stratification, surface temperature, heat content, and mean epilimnetic irradiance of small lakes , 2006 .

[14]  K. Vrede.  Nutrient and Temperature Limitation of Bacterioplankton Growth in Temperate Lakes , 2005, Microbial Ecology.

[15]  L. Tranvik,et al.  Terrestrial subsidies to lake food webs: an experimental approach , 2012, Oecologia.

[16]  Michael L. Pace,et al.  A SPATIALLY EXPLICIT WATERSHED-SCALE ANALYSIS OF DISSOLVED ORGANIC CARBON IN ADIRONDACK LAKES , 2004 .

[17]  Robert C. Wolpert,et al.  A Review of the , 1985 .

[18]  J. Hibbeln,et al.  Healthy intakes of n-3 and n-6 fatty acids: estimations considering worldwide diversity. , 2006, The American journal of clinical nutrition.

[19]  J. Gunn,et al.  Effects of colonizing predators on yellow perch (Perca flavescens) populations in lakes recovering from acidification and metal stress , 2007 .

[20]  Andrew Gelman,et al.  Bayesian Measures of Explained Variance and Pooling in Multilevel (Hierarchical) Models , 2006, Technometrics.

[21]  M. Appelberg.  Swedish standard methods for sampling freshwater fish with multi-mesh gillnets : stratified random sampling with Nordic multi-mesh gillnets provide reliable whole-lake estimates of the relative abundance and biomass of freshwater temperate lakes , 2000 .

[22]  Paul Hazlett,et al.  Logging impacts on the biogeochemistry of boreal forest soils and nutrient export to aquatic systems: A review , 2008 .

[23]  J. Post,et al.  Size-Selective Mortality in Young-of-the-Year Yellow Perch (Perca flavescens): Evidence from Otolith Microstructure , 1987 .

[24]  Donald A. Jackson,et al.  A Comparison of von Bertalanffy and Polynomial Functions in Modelling Fish Growth Data , 1992 .

[25]  O. Berglund,et al.  Essential fatty acids and phosphorus in seston from lakes with contrasting terrestrial dissolved organic carbon content , 2007 .

[26]  A. Paterson,et al.  Long-term changes in phytoplankton composition in seven Canadian Shield lakes in response to multiple anthropogenic stressors , 2008 .

[27]  D. Post,et al.  Size matters: comparing stable isotope ratios of tissue plugs and whole organisms , 2010 .

[28]  R. Spencer,et al.  Fluorescence spectroscopy opens new windows into dissolved organic matter dynamics in freshwater ecosystems: A review , 2010 .

[29]  M. C. Whiteside,et al.  Factors affecting the early life history of yellow perch,Perca flavescens , 2004, Environmental Biology of Fishes.

[30]  M. Xenopoulos,et al.  Unraveling the role of land use and microbial activity in shaping dissolved organic matter characteristics in stream ecosystems , 2010 .

[31]  Roger Jones,et al.  Seasonal changes in the importance of the source of organic matter to the diet of zooplankton in Loch Ness, as indicated by stable isotope analysis , 2001 .

[32]  D. W. Coble.  Dependence of Total Annual Growth in Yellow Perch on Temperature , 1966 .

[33]  S. Ludsin,et al.  Otolith microchemistry as a stock identification tool for freshwater fishes: testing its limits in Lake Erie , 2010 .

[34]  J. Richardson,et al.  Organic matter inputs into headwater streams of southwestern British Columbia as a function of riparian reserves and time since harvesting , 2010 .

[35]  D. Robson,et al.  Effect of Zooplankton Abundance and Body Size on Growth of Age-0 Yellow Perch (Perca flavescens) in Oneida Lake, New York, 1975–86 , 1989 .

[36]  Brett M. Johnson,et al.  Elemental signatures in otoliths of hatchery rainbow trout (Oncorhynchus mykiss): distinctiveness and utility for detecting origins and movement , 2009 .

[37]  R. P. Silliman.  Comparison between Gompertz and von Bertalanffy Curves for Expressing Growth in Weight of Fishes , 1969 .

[38]  N. Yan,et al.  Littoral Microcrustacean (Cladocera and Copepoda) Indicators of Acidification in Canadian Shield Lakes , 2003, Ambio.

[39]  A. Hodge,et al.  Plant and mycorrhizal regulation of rhizodeposition. , 2004, The New phytologist.

[40]  A. Finstad,et al.  Unimodal response of fish yield to dissolved organic carbon. , 2014, Ecology letters.

[41]  M. Pace,et al.  The influence of environmental water on the hydrogen stable isotope ratio in aquatic consumers , 2009, Oecologia.

[42]  D. Bureau,et al.  Modelling growth and body composition in fish nutrition: where have we been and where are we going? , 2010 .

[43]  M. T. Arts,et al.  Health and condition in fish: the influence of lipids on membrane competency and immune response , 2009 .

[44]  H. Ducklow,et al.  Bacterioplankton: A Sink for Carbon in a Coastal Marine Plankton Community , 1986, Science.

[45]  M. T. Arts,et al.  Seston composition and the potential for Daphnia growth , 1999, Aquatic Ecology.

[46]  Yoram J. Kaufman,et al.  Atmospheric correction against algorithm for NOAA-AVHRR products: theory and application , 1992, IEEE Trans. Geosci. Remote. Sens..

[47]  B. Henderson.  Factors affecting growth and recruitment of yellow perch, Perca flavescens Mitchill, in South Bay, Lake Huron , 1985 .

[48]  M. Jansson,et al.  Control of zooplankton dependence on allochthonous organic carbon in humic and clear‐water lakes in northern Sweden , 2003 .

[49]  R. Wetzel.  Limnology: Lake and River Ecosystems , 1975 .

[50]  J. Klug.  Positive and negative effects of allochthonous dissolved organic matter and inorganic nutrients on phytoplankton growth , 2002 .

[51]  B. McGlynn,et al.  Variable flushing mechanisms and landscape structure control stream DOC export during snowmelt in a set of nested catchments , 2010 .

[52]  Erkki Tomppo,et al.  A report to the food and agriculture organization of the united nations (FAO) in support of sampling study for National Forestry Resources Monitoring and Assessment (NAFORMA) in Tanzania , 2010 .

[53]  David M. Lodge,et al.  Regional comparisons of watershed determinants of dissolved organic carbon in temperate lakes from the Upper Great Lakes region and selected regions globally , 2003 .

[54]  S. Carpenter,et al.  Whole-lake carbon-13 additions reveal terrestrial support of aquatic food webs , 2004, Nature.

[55]  C. Guéguen,et al.  Distinguishing dissolved organic matter at its origin: size and optical properties of leaf-litter leachates. , 2013, Chemosphere.

[56]  P. Kortelainen,et al.  Carbon pools and fluxes in a chain of five boreal lakes: A dry and wet year comparison , 2011 .

[57]  Chris T. Darimont,et al.  Quantifying Inter- and Intra-Population Niche Variability Using Hierarchical Bayesian Stable Isotope Mixing Models , 2009, PloS one.

[58]  Martyn Plummer,et al.  JAGS: A program for analysis of Bayesian graphical models using Gibbs sampling , 2003 .

[59]  B. Cobb,et al.  An Experimental Approach , 1957 .

[60]  S. Carpenter,et al.  Strong evidence for terrestrial support of zooplankton in small lakes based on stable isotopes of carbon, nitrogen, and hydrogen , 2011, Proceedings of the National Academy of Sciences.

[61]  Stelios Katsanevakis,et al.  Modelling fish growth: multi‐model inference as a better alternative to a priori using von Bertalanffy equation , 2008 .

[62]  M. H. Olson,et al.  Changes in yellow perch (Perca flavescens) growth associated with the establishment of a walleye (Stizostedion vitreum) population in Canadarago Lake, New York (USA) , 2001 .

[63]  L. Zelles,et al.  Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review , 1999, Biology and Fertility of Soils.

[64]  Yves T. Prairie,et al.  EFFECT OF CATCHMENT SIZE ON PHOSPHORUS EXPORT , 1986 .

[65]  S. Carpenter,et al.  Carbon sources supporting fish growth in a north temperate lake , 2008, Aquatic Sciences.

[66]  A. Vähätalo,et al.  Photochemically produced bioavailable nitrogen from biologically recalcitrant dissolved organic matter stimulates production of a nitrogen‐limited microbial food web in the Baltic Sea , 2007 .

[67]  A. J. Mansueti.  Early Development of the Yellow Perch, Perca flavescens' , 1964 .

[68]  David M. Lodge,et al.  From Greenland to green lakes : Cultural eutrophication and the loss of benthic pathways in lakes , 2003 .

[69]  D. Rosauer,et al.  Development of yellow perch (Perca flavescens) broodstocks: Initial characterization of growth and quality traits following grow-out of different stocks , 2011 .

[70]  M. Pace,et al.  Dissolved organic carbon and nutrients as regulators of lake ecosystems: Resurrection of a more integrated paradigm , 1999 .

[71]  Monica G. Turner,et al.  DISSOLVED ORGANIC CARBON AS AN INDICATOR OF THE SCALE OF WATERSHED INFLUENCE ON LAKES AND RIVERS , 1999 .

[72]  E. R. Cohen.  An Introduction to Error Analysis: The Study of Uncertainties in Physical Measurements , 1998 .

[73]  Bradley P. Carlin,et al.  Bayesian measures of model complexity and fit , 2002 .

[74]  P. Legendre,et al.  Inferring Processes from Spatial Patterns: The Role of Directional and Non–Directional Forces in Shaping Fish Larvae Distribution in a Freshwater Lake System , 2012, PloS one.

[75]  M. PatersonAndrew,et al.  Water quality changes in south-central Ontario lakes and the role of local factors in regulating lake response to regional stressors , 2011 .

[76]  G. Asner,et al.  Dissolved Organic Carbon in Terrestrial Ecosystems: Synthesis and a Model , 2001, Ecosystems.

[77]  J. Post,et al.  Variability in first-year growth of yellow perch (Perca flavescens) : predictions from a simple model, observations, and an experiment , 1994 .

[78]  R. Carignan,et al.  Influence of catchment topography on water chemistry in southeastern Québec Shield lakes , 1997 .

[79]  Susan E. Trumbore,et al.  Precambrian Shield Wetlands: Hydrologic Control of the Sources and Export of Dissolved Organic Matter , 1998 .

[80]  J. G. Bell,et al.  Effects of purified diets containing different combinations of arachidonic and docosahexaenoic acid on survival, growth and fatty acid composition of juvenile turbot (Scophthalmus maximus) , 1994 .

[81]  L. Tranvik,et al.  Terrestrial carbon and intraspecific size-variation shape lake ecosystems. , 2007, Trends in ecology & evolution.

[82]  P. Dillon,et al.  Dissolved organic and inorganic carbon mass balances in central Ontario lakes , 1997 .

[83]  T. Francis,et al.  Shoreline urbanization reduces terrestrial insect subsidies to fishes in North American lakes. , 2009 .

[84]  I. Holopainen,et al.  Piscivory and Recruitment: Mechanisms Structuring Prey Populations in Small Lakes , 1992 .

[85]  M. T. Arts,et al.  Lipids in aquatic ecosystems , 2009 .

[86]  L. Rudstam,et al.  Gape limitation and prey selection in larval yellow perch (Perca flavescens), freshwater drum (Aplodinotus grunniens), and black crappie (Pomoxis nigromaculatus) , 1991 .

[87]  A. Fisk,et al.  Seasonal patterns in fatty acids of Calanus hyperboreus (Copepoda, Calanoida) from Cumberland Sound, Baffin Island, Nunavut , 2012, Marine Biology.

[88]  C. Tucker,et al.  Satellite remote sensing of primary production , 1986 .

[89]  H. Laudon,et al.  Terrestrial organic matter support of lake food webs: Evidence from lake metabolism and stable hydrogen isotopes of consumers , 2012 .

[90]  E. Moksness.  Otolith microstructure examination and analysis , 1993, Reviews in Fish Biology and Fisheries.

[91]  Jan Köhler,et al.  Lake responses to reduced nutrient loading - an analysis of contemporary long-term data from 35 case studies , 2005 .

[92]  S. Campana,et al.  Otoliths, increments, and elements: keys to a comprehensive understanding of fish populations? , 2001 .

[93]  D. G. George,et al.  The effect of climate on long-term changes in the crustacean zooplankton biomass of Lake Windermere, UK , 1985, Nature.

[94]  R. Hesslein,et al.  Predicting export of dissolved organic carbon from forested catchments in glaciated landscapes with shallow soils , 2008 .

[95]  J. Gunn,et al.  Terrestrial organic matter as subsidies that aid in the recovery of macroinvertebrates in industrially damaged lakes. , 2011, Ecological applications : a publication of the Ecological Society of America.

[96]  Stuart E. Bunn,et al.  CARBON FROM PERIPHYTON SUPPORTS FISH BIOMASS IN WATERHOLES OF A WET–DRY TROPICAL RIVER , 2013 .

[97]  J. Grey,et al.  An assessment, using stable isotopes, of the importance of allochthonous organic carbon sources to the pelagic food web in Loch Ness , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[98]  J. Post,et al.  Ontogenetic Changes in the Distribution of Larval and Juvenile Yellow Perch (Perca flavescens): A Response to Prey or Predators? , 1988 .

[99]  M. Vanderklift,et al.  Sources of variation in consumer-diet δ15N enrichment: a meta-analysis , 2003, Oecologia.

[100]  J. Pickova,et al.  Fatty acid composition of consumers in boreal lakes – variation across species, space and time , 2012 .

[101]  G. Arhonditsis,et al.  Mass Flux Calculations Show Strong Allochthonous Support of Freshwater Zooplankton Production Is Unlikely , 2012, PloS one.

[102]  S. Watmough,et al.  Drought-induced release of metals from peatlands in watersheds recovering from historical metal and sulphur deposition , 2013, Biogeochemistry.

[103]  S. Golladay.  Suspended Particulate Organic Matter Concentration and Export in Streams , 1997, Journal of the North American Benthological Society.

[104]  J. Cotner,et al.  Interactive effect of temperature and resources on carbon cycling by freshwater bacterioplankton communities , 2007 .

[105]  D. Burns.  What do hydrologists mean when they use the term flushing? , 2005 .

[106]  M. Jansson,et al.  Whole‐lake mineralization of allochthonous and autochthonous organic carbon in a large humic lake (örträsket, N. Sweden) , 2001 .

[107]  K. Dąbrowski,et al.  Nutrition and feeding of yellow perch (Perca flavescens) , 1996 .

[108]  P. Leavitt,et al.  Direct and interactive effects of allochthonous dissolved organic matter, inorganic nutrients, and ultraviolet radiation on an alpine littoral food web , 1998 .

[109]  D. O. Hessen,et al.  Climate change predicted to cause severe increase of organic carbon in lakes , 2011 .

[110]  M. Jansson,et al.  Poor direct exploitation of terrestrial particulate organic material from peat layers by Daphnia galeata , 2012 .

[111]  D. Isermann,et al.  Emergence of larval yellow perch, Perca flavescens, in South Dakota lakes: potential implications for recruitment , 2008 .

[112]  A. Ballantyne,et al.  The importance of dietary phosphorus and highly unsaturated fatty acids for sockeye (Oncorhynchus nerka) growth in Lake Washington — a bioenergetics approach , 2003 .

[113]  S. Carpenter,et al.  Terrestrial, benthic, and pelagic resource use in lakes: results from a three-isotope Bayesian mixing model. , 2011, Ecology.

[114]  Bill Shipley,et al.  Cause and Correlation in Biology: A User''s Guide to Path Analysis , 2016 .

[115]  C. Bernard,et al.  On the use of the FluoroProbe®, a phytoplankton quantification method based on fluorescence excitation spectra for large-scale surveys of lakes and reservoirs. , 2012, Water research.

[116]  D. Tocher.  Metabolism and Functions of Lipids and Fatty Acids in Teleost Fish , 2003 .

[117]  S. Carpenter,et al.  Differential support of lake food webs by three types of terrestrial organic carbon. , 2006, Ecology letters.

[118]  S. Carpenter,et al.  Resources supporting the food web of a naturally productive lake , 2012 .

[119]  G. Allan,et al.  Essential fatty acids in the diet of silver perch (Bidyanus bidyanus): effect of linolenic and linoleic acid on growth and survival , 2004 .

[120]  P. Carlsson,et al.  Nitrogen bound to humic matter of terrestrial origin - a nitrogen pool for coastal phytoplankton? , 1993 .

[121]  C. Walters,et al.  The von Bertalanffy growth function, bioenergetics, and the consumption rates of fish , 2001 .

[122]  J. G. Bell,et al.  Recent developments in the essential fatty acid nutrition of fish , 1999 .

[123]  Per Ask,et al.  Light limitation of nutrient-poor lake ecosystems , 2009, Nature.

[124]  D. Schindler,et al.  Comprehensive conservation planning to protect biodiversity and ecosystem services in Canadian boreal regions under a warming climate and increasing exploitation , 2010 .

[125]  Cynthia M. Jones,et al.  Relationships between Water, Otolith, and Scale Chemistries of Westslope Cutthroat Trout from the Coeur d'Alene River, Idaho: The Potential Application of Hard-Part Chemistry to Describe Movements in Freshwater , 2003 .

[126]  P. Dillon,et al.  Stable isotope variability of meso‐zooplankton along a gradient of dissolved organic carbon , 2009 .

[127]  G. Arhonditsis,et al.  The effects of seston lipids on zooplankton fatty acid composition in Lake Washington, Washington, USA. , 2010, Ecology.

[128]  B. Jezierska,et al.  The effects of heavy metals on embryonic development of fish (a review) , 2009, Fish Physiology and Biochemistry.

[129]  Eric J Ward,et al.  Habitat structure determines resource use by zooplankton in temperate lakes. , 2011, Ecology letters.

[130]  Ji‐Hyung Park,et al.  Controls on the dynamics of dissolved organic matter in soils: a review. , 2000 .

[131]  J. Post,et al.  Size-Dependent Overwinter Mortality of Young-of-the-Year Yellow Perch (Perca flavescens): Laboratory, In Situ Enclosure, and Field Experiments , 1989 .

[132]  C. Williamson,et al.  Environmental Constraints on Spawning Depth of Yellow Perch: The Roles of Low Temperature and High Solar Ultraviolet Radiation , 2004 .

[133]  M. T. Arts,et al.  Essential fatty acids in the planktonic food web and their ecological role for higher trophic levels , 2004 .

[134]  G. Ahlgren,et al.  Fatty Acid Ratios in Freshwater Fish, Zooplankton and Zoobenthos – Are There Specific Optima? , 2009 .

[135]  N. Pettorelli,et al.  Using the satellite-derived NDVI to assess ecological responses to environmental change. , 2005, Trends in ecology & evolution.

[136]  P. Dillon,et al.  Effect of landscape form on export of dissolved organic carbon, iron, and phosphorus from forested stream catchments , 1997 .

[137]  M. Power,et al.  Age-0 Yellow Perch Growth and Its Relationship to Temperature , 1999 .

[138]  Jonathan J. Cole,et al.  Patterns and regulation of dissolved organic carbon: An analysis of 7,500 widely distributed lakes , 2007 .

[139]  B. Hungate,et al.  Measuring terrestrial subsidies to aquatic food webs using stable isotopes of hydrogen. , 2007, Ecology.

[140]  M. Vanni,et al.  Terrestrial support of detritivorous fish populations decreases with watershed size , 2011 .