Lake Trout Ecosystems in a Changing Environment - Chapter 8 doc

chapter eightDissolved organic carbon as a controlling variable in lake trout and other Boreal Shield lakes David W.. Gunn Ontario Ministry of Natural Resources, Laurentian University

chapter eight

Dissolved organic carbon as a

controlling variable in lake trout

and other Boreal Shield lakes

David W Schindler

Department of Biological Sciences, University of Alberta

John M Gunn

Ontario Ministry of Natural Resources, Laurentian University

Contents

Introduction

The effect of DOC on the physical properties of lakes

The effect of DOC on the chemical properties of lakes

The effect of DOC on biological properties of lakes

Human activities that affect DOC

Local influences

Acid rain

Climate warming

Recommendations

Acknowledgments

References

Introduction

Lake trout lakes on the Boreal Shield are usually relatively clear (Martin and Olver, 1976; Johnson et al., 1977; Marshall and Ryan, 1987) Seventy percent have Secchi depths greater than 4 m (Figure 8.1) Transparency in Shield lakes is usually largely determined by the concentration of dissolved organic matter (usually called DOC, or dissolved organic car-bon, for it is usually quantified by measuring its carbon content) (Schindler, 1971;

Figure 8.2), much of which originates from decomposing vegetation in wetlands and forest soils Fulvic and tannic acids are important components of DOC, imparting a yellowish-brown color to the lakes and streams (Schindler, 1998) However, most lake trout lakes

contain enough DOC to have important effects on optical, chemical, physical, and biolog-ical properties (Schindler et al., 1997) For example, over 80% of lake trout lakes have DOC concentrations >3 mg L-1 (Figure 8.2), a range where DOC attenuates enough light to reduce photosynthesis and block UV radiation The most colored lake trout lakes tend to

be small, with areas of a few hundred hectares or less Without DOC, these Shield lakes would have Secchi depths exceeding 30 m (Figure 8.3), as are observed in the lakes on the orthoquartzite ridges of the LaCloche Mountains, along the northern shore of Lake Huron (Gunn et al., 2001)

Not all DOC is highly colored Some is also produced by algae and other plants within

the lake Such DOC is termed autochthonous, meaning produced within The highly colored DOC that originates from the watershed is termed allochthonous, meaning produced

out-side the lake In general, the larger a lake’s catchment, the higher the proportion of the basin that is covered by wetlands, and the wetter the climate, the darker the lake’s color

Figure 8.1 Secchi depth (m) in lake trout lakes of eastern North America From data compiled for text edited by Gunn, Steedman, and Ryder (2003)

Figure 8.2 DOC concentrations (mg/L) in lake trout lakes of eastern North America From data compiled for text edited by Gunn, Steedman, and Ryder (2003)

0

10

20

30

40

50

60

70

80

90

Secchi Depth (m)

32%

55%

73%

n = 2103

0 10 20 30 40 50 60 70 80 90 100

DOC (mg/L)

n = 2052

18 %

66 % 91%

will be (Engstrom, 1987; Rasmussen et al., 1989; Urban et al., 1989; Meili, 1992; Curtis and Schindler, 1997) However, colored allochthonous DOC can be bleached by exposure to

UV radiation near the surface of lakes The degree of bleaching depends on the pH (Donahue et al., 1998) and on how long the DOC is present in a lake, which in turn is related to how rapidly a lake is flushed with water Thus, there is a tendency for lakes with faster rates of water flushing to be darker in color

DOC can influence the food and habitat of lake trout and other Shield lake biota in a number of very subtle ways, for it is a pivotal variable that affects many important physical, chemical, and biological properties of lakes Below are some of its more important effects

The effect of DOC on the physical properties of lakes

The dark color of allochthonous DOC makes it an excellent attenuator (absorber) of light

As water containing DOC absorbs solar radiation, light energy is transformed to heat As

a result, the epilimnion of a high-DOC lake tends to be warmer than that of a clear lake

of the same size, subjected to the same climatic regime (Salonen et al., 1984; Perez-Fuen-tetaja et al., 1999)

Reduced penetration of light in highly colored lakes also causes the thermocline depth

to be shallower than in clear lakes of equivalent size This is particularly true of small lakes (Snucins and Gunn, 2000; Xenopoulos and Schindler, 2001), and the large majority

of lake trout lakes are indeed quite small, with about 75% of them less than 500 ha (Figure 8.4) For lakes greater than about 500 ha in area, the effect of wind on the lake’s surface becomes of overriding importance in determining thermocline depth (Fee et al., 1996;

Figure 8.5)

Because of its effect on water temperature and thermal stratification, DOC concentra-tion can control the summer habitat available to lake trout Small, high-DOC lakes have higher proportions of their volumes below the thermocline, where water is cold enough

to attract lake trout in summer It has recently been recognized that DOC data can be used

to predict lake trout habitat directly (Dillon et al., 2003)

It was discovered recently that DOC is also an excellent attenuator of UV radiation, serving as a sort of “sunscreen” to protect aquatic organisms (Scully and Lean, 1994; Figure 8.6) As we discuss below, climate change, increasing UV from stratospheric ozone deple-tion, and acid rain can potentially affect summer habitat via their effects on DOC

Figure 8.3 The relationship between DOC and Secchi depth in lakes of the LaCloche Mountain Lakes From Gunn et al (2001)

0 5 10 15 20 25 30 35

DOC (mg/L)

Figure 8.4 Size frequency (ha) of lake trout lakes in eastern North America From data compiled for text edited by Gunn, Steedman, and Ryder (2003)

Figure 8.5 The relationship between light transmission and mixing depth (e) in large and small lakes of northwestern Ontario Lakes <500 ha have their thermocline depth largely determined by color; larger lakes have their thermoclines determined by fetch because the fetch-determined ther-mocline is too deep for light penetration to have a significant effect From Fee et al (1996)

0 10 20 30 40 50 60 70 80 90

Surface Area (ha)

36 %

56 %

78 %

n = 2709

% Transmission, m-1

The effect of DOC on the chemical properties of lakes

Many papers have been written on the chemical properties of DOC Here, we discuss only those of relevance to lake trout and other biota of Boreal lakes

DOC includes many substances, of varying chemical structure Some molecules are small, in a size range ideal for uptake by organisms However, colored allochthonous DOC

is composed mostly of humic and fulvic acids and other large, charged molecules, which tend to combine with other charged chemicals, including trace metals, nutrients, and organic contaminants, to form stable colloids DOC prevents these chemicals from partic-ipating in biological and chemical reactions as if they were in truly dissolved form but also retards further coagulation, inhibiting their removal to the sediments (Weilenmann

et al., 1989)

DOC will combine with toxic trace metals, rendering most of them less toxic than if they were in dissolved ionic form Mercury, lead, aluminum, chromium, and copper are among metals with a high affinity for DOC (Kerndorf and Schnitzer, 1980) There is a strong correlation between DOC concentration in water and mercury concentration in fish, perhaps because wetlands tend to be the most important source of both in the catchments

of lakes (Urban et al., 1989; McMurty et al., 1989; St Louis et al., 1996) For example, lake catchments containing wetlands in the Experimental Lakes Area yield 26- to 79-fold more methyl mercury than catchments without wetlands (St Louis et al., 1994) As will be discussed later, DOC can greatly affect the toxicity of aluminum in lakes subjected to acid precipitation (Driscoll et al., 1995)

In some cases, DOC has complex effects on trace metal concentrations, biogeochemical cycles, and toxicity For example, although wetlands supply both DOC and mercury, DOC also inhibits the methylation of mercury in lakes (Miskimmin et al., 1992)

If wetlands are flooded, as occurs when reservoirs are constructed on the Shield, DOC and methyl mercury (MeHg) concentrations increase dramatically The latter is the result

of increased activity by methanogenic bacteria (Kelly et al., 1997) As a result, concentra-tions of mercury in fish increase dramatically, frequently to levels that pose a hazard to humans or other species that rely on fish for food (Hecky et al., 1992; Rosenberg et al., 1995; Bodaly et al., 1998; Bodaly et al., Chapter 9, this volume)

DOC may be important in controlling the transformation of MeHg to elemental mer-cury in surface waters Exposure of MeHg to UV and short-wavelength visible radiation

Figure 8.6 The effect of DOC on the attenuation of UV light From Schindler et al (1996)

DOC mg 1-1

accelerates this reaction, so that declining DOC may accelerate the process The conversion

of MeHg to elemental mercury is an important natural pathway for mercury to reach the atmosphere (Sellers et al., 1996; Amyot et al., 1997)

In well-oxygenated surface waters almost all of the iron will be bound to DOC complexes, with little remaining in dissolved ionic forms These complexes render much

of the iron unavailable to phytoplankton (Sakamoto, 1971) and also slow the removal of iron from solution (Curtis, 1993) In turn, iron–DOC complexes bind both trace metals and nutrients Phosphorus bound to iron–DOC complexes is less available for immediate biological uptake than ionic phosphate (Jackson and Schindler, 1975)

The attenuation of solar radiation by DOC also affects the formation of transient secondary thermoclines within the epilimnion, which can last for hours or days, depending

on wind conditions (Xenopoulos and Schindler, 2001) The frequency of formation of secondary thermoclines ranges from 30% to nearly 100% of summer days, with a higher incidence in lakes with higher DOC and smaller surface area (Xenopoulos and Schindler, 2001) Such thermoclines can isolate nonmotile species in near-surface layers that are less than a meter deep, causing them to be exposed to high levels of UV radiation High exposures in near-surface layers can affect the growth and physiological state of algae and bacteria (Xenopoulos et al., 2000)

The effect of DOC on biological properties of lakes

The depth to which photosynthesis can occur is also a function of DOC, which strongly attenuates all wavelengths of solar radiation Dark lakes are usually less productive than clear lakes with similar nutrient loadings Carpenter et al (1998) found that increasing DOC from 5 to 17 mg C per liter was equivalent to reducing inputs of phosphorus 10-fold, from 5 to 0.5 mg per m2 per day They believe that the main effect on primary production of DOC is by shading However, complexation of phosphorus and iron by DOC may also be involved

DOC contains energy potentially available to organisms, which may partly compen-sate for DOC’s negative effects on photosynthesis Bacteria, heterotrophic algae and pro-tozoa are among the organisms that rely on DOC as an energy source In turn, these supplement algal production, which supplies food for small zooplankton, which feed the large zooplankton and planktivorous fishes that are typically important in the diets of lake trout and other piscivorous fish Although this has not been studied in detail in lake trout lakes, it is doubtful whether the positive effects of DOC on the microbial food chain

to zooplankton would be sufficient to offset the negative effect of DOC on phytoplankton production, as discussed earlier

The DOC that enters lakes can be quite old In particular, DOC entering from ground-water can be quite recalcitrant, with some of it decades old (Schiff et al., 1997) However, once DOC is discharged into lakes, a variety of physical, chemical, and biological prop-erties combine to transform molecules that have resisted decomposition in the terrestrial environment UV radiation can cleave large, refractory DOC molecules into small mole-cules such as fatty acids and other substances that are directly usable by microorganisms (Wetzel et al., 1995) Allochthonous DOC tends to be rich in carbon but deficient in phosphorus, and if lake water contains phosphorus from other sources, DOC is more efficiently degraded (Schindler et al., 1992) As DOC is mineralized, CO2 concentrations reach supersaturation, so that it is released to the atmosphere (Dillon and Molot, 1997) It

is difficult to unravel the combinations and sequences of physical, chemical, and biological activity that decomposes DOC, and it is probably unrealistic to view any of the processes

in isolation

DOC can also play a role in buffering against acidification because it contains organic anions (A−) The amount of A− is a predictable function of DOC and pH for most surface waters (Oliver et al., 1983), for carboxyl groups (COOH) are the main functional groups, varying little between regions (Jones et al., 1986) In colored lakes, DOC can contribute substantially to the ability to neutralize incoming strong acids (Lazerte and Dillon, 1984)

In the process of degradation by UV radiation, DOC can release several toxic chemi-cals, including hydrogen peroxide, carbon monoxide, hydroxyl radichemi-cals, and superoxides (Keiber et al., 1990; Mopper and Zhou, 1990; Cooper et al., 1994; Shao et al., 1994) Although concentrations are small, hydrogen peroxide may be present at concentrations that are toxic to microorganisms (Xenopoulos, 1997; Xenopoulos and Bird, 1997)

Attenuation of light by DOC can also potentially affect the makeup of food chains at higher levels by affecting the nutritional value of food It is known that the zooplankton

tend to be dominated by Daphnia, in lakes where seston (algae and detritus) has low ratios

of C:P, whereas copepods tend to predominate at higher C:P ratios (Sterner et al., 1998) Higher C:P ratios in seston tend to be produced in lakes with higher penetration of light, i.e., lakes with low DOC (Hassett et al., 1997)

DOC can also directly affect trophic interactions via its effect on transparency to visible light Sight-dependent predators are probably favored in clear lakes (O’Brien, 1987; Clark and Levy, 1988) Increased UV can cause subtle and poorly understood changes in rela-tionships between invertebrate and fish species (Williamson, 1995) High light levels will

also increase the C:P ratio of phytoplankton, lowering its nutritional value for Daphnia

and other large grazing cladocerans (Sterner et al., 1998; Elser et al., 1998) Altered light regimes are also likely to affect the vertical migration of zooplankton (Dodson, 1990) Below, we give examples of how human activities are directly and indirectly affecting DOC, potentially changing important community interactions of several types

Human activities that affect DOC

A number of different activities affect DOC, changing physical, chemical, and biological processes that are important to lake trout Some of these are local, but others are regional

or global in their influence, so that there is little that we can do directly to control them (Schindler, 1998)

Local influences

Although data are scarce, several types of local influences, including logging, road build-ing, and other disruptions to the catchments of lakes can affect the inputs of DOC In general, any activity that increases the contact between water and wetland soils, such as clearcutting, wildfire, or drainage interruptions, will increase the concentrations of DOC

in runoff (Carignan et al., 2000) Similarly, raising the level of lakes even slightly can cause increased DOC if wetlands are flooded, as outlined later for reservoir construction

Acid rain

Among regional insults, acid rain is a potent modifier of DOC In general, lakes and streams become clearer and contain less DOC as the pH decreases below pH 5 (Schindler

et al., 1996b; Yan et al., 1996) Flocculation and precipitation with aluminum (Weilenmann

et al., 1989; Driscoll et al., 1995) and increased photolytic degradation (Molot and Dillon, 1996) appear to be mechanisms that remove DOC in acidifying lakes Lakes can lose 90%

or more of their natural DOC concentrations, with subsequent deepening of thermoclines and euphotic zones (Schindler et al., 1996a) Increased penetration of solar energy into the

hypolimnion of a small lake could also warm it (Yan and Miller, 1984), potentially making

it become too warm for lake trout (Gunn, 2001)

Loss of DOC poses several threats Most notably, its disappearance increases the exposure of littoral and shallow water organisms to higher UV radiation Approximately 20% of the lakes in Ontario that have been surveyed by the Ontario Ministry of Environ-ment (Neary et al., 1990) have natural DOC concentrations <3 mg/L, where even slight decreases in DOC will cause rapid increases in UV penetration because of the negative exponential nature of the relationship (Scully and Lean, 1994; Schindler et al., 1996b;

Figure 8.6) A similar proportion of lake trout lakes have low DOC and are vulnerable to increasing UV if DOC decreases significantly (Figure 8.3)

Thermocline deepening and hypolimnetic heating occur in acid lakes as the result of declining DOC (Schindler et al., 1996a; Snucins and Gunn, 2000) Both will reduce summer habitat for lake trout and other cold stenotherms As the result of clearer waters, there may be several other subtle changes to food chain relationships, as discussed above

Climate warming

Climate warming and/or drought will also cause increased transparency of lakes because less allochthonous DOC is delivered to the lakes from their catchments (Schindler et al., 1996a, 1997; Gunn et al., 2001), and there is increased in-lake removal and bleaching as the result of longer residence times (Dillon and Molot, 1997; Schindler et al., 1997) The effects are similar to those mentioned above for acid lakes At least in the early stages of climate change, effects are smaller than those caused by acidification (Schindler et al., 1996a,b) In general, climate and hydrology affect DOC in two ways First, inputs of colored allochthonous DOC decline in direct proportion to streamflow decreases The latter can result from less precipitation, increased evaporation at warmer temperatures, or a combi-nation of the two (Schindler et al., 1996b) Second, as for acidification, DOC bleaching and removal in lakes increase as water and, hence, DOC residence times increase (Dillon and Molot, 1997; Schindler et al., 1997)

Exacerbating the effects of acid rain and climate warming on UV is the depletion of stratospheric ozone in the northern hemisphere The three act in concert to affect the UV exposure of aquatic organisms, leading Gorham (1996) to declare that lakes are under a

“three-pronged attack” (Figure 8.7)

In summary, DOC can have many important effects on lake trout habitat by altering physical, chemical, and biological properties Maintaining the long-term integrity of lake trout habitat will require the management of activities in the catchments of lakes that affect DOC inputs to lakes Climate change and acid rain also affect fish habitats by changing DOC concentrations in addition to their well-known direct effects

Recommendations

At the local level, it is important to maintain DOC concentrations within the natural range expected for a given lake To do this, greater care is needed when planning clearcuts, roads, dams, and other human activities

Other influences on DOC are beyond local control Strong national and international policies are needed to control emissions of acidifying substances, greenhouse gases, and stratospheric ozone, which alone and in combination can degrade the habitat required by lake trout and their prey Such changes are particularly likely in small lakes, where even small declines in habitat can threaten fragile populations

Additional research and monitoring are needed in several areas because the wide-spread importance of DOC was not recognized until recently First, until recently, DOC

was not easy to analyze, particularly when <3 mg/L It was also not widely recognized

as important This has changed, and long-term records for DOC will be important in assessing changes to habitats, UV exposures, and euphotic zones Secondly, there are few data to show the impacts of landscape or drainage modification on DOC concentrations

in lakes Such changes are now easy to monitor, and DOC is clearly an important variable

to measure in assessing the impacts of local activity

Third, few studies have traced the effect of energy transfer from DOC to fisheries via heterotrophic bacteria and protozoans Modern stable isotope methods make this possible, and such studies are critical to linking how changes in DOC concentration might affect the energy flow to fisheries in lake trout lakes Finally, now that DOC has been shown to moderate the effects of climate warming, acid precipitation, stratospheric ozone depletion, and mercury cycling, its importance in linking these insults to aquatic effects needs to be explicitly studied

Acknowledgments

We thank Dick Ryder, Norm Yan, and Rob Steedman for providing review comments Data for the extensive survey of 2700 lake trout lakes were kindly provided by government agencies in Ontario, Quebec, Minnesota, New York, Michigan, and Wisconsin Michael Malette assisted with data management and preparation of graphics

Figure 8.7 A diagram showing how the “three-pronged attack” by stratospheric ozone depletion, climate warming, and acid rain on the aquatic UV environment is mediated by DOC From Schindler (1999)

Hypothesized Interactions of Stratospheric Ozone Depletion, Acid Rain, Climate Warning and Mercury Biogeochemistry

Stratospheric ozone

Acid lakes

Climate warming

Increased UV radiation

Lower DOC

Warmer water, deeper thermoclines

Increased water transparency

Increased mercury methylation, decreased demethylation Increased

underwater

mercury

Greater conversion

of methyl mercury

to Hgo

Increased release to atmosphere

Increased mercury deposition

Amyot, M., Mierle, G., Lean, D.R.S., and McQueen, D.J., 1997, Effects of solar radiation on the

formation of dissolved gaseous mercury in temperate lakes, Geochimica et Cosmochimica Acta

61: 975–987

Bodaly, R.A (Drew), St Louis, V.L., Paterson, M.J., Fudge, R.J.P., Hall, B.D., Rosenberg, D.M., and Rudd, J.W.M., 1998, Bioaccumulation of mercury in the aquatic food chain in newly flooded

areas, In Mercury and Its Effects on Environment and Biology, edited by H Segel and A Sigel,

Marcel Dekker, New York, pp 259–287

Carignan, R., D’Arcy, P., and Lamontagne, S., 2000, Comparative impacts of fire and forest harvesting

on water quality in boreal shield lakes, Canadian Journal of Fisheries and Aquatic Sciences,

57(Suppl 2): 105–117

Carpenter, S.R., Cole, J.J., Kitchell, J.F., and Pace, M.L., 1998, Impact of dissolved organic carbon, phosphorus, and grazing on phytoplankton biomass and production in experimental lakes,

Limnology and Oceanography 43: 73–80.

Clark, C.W and Levy, D.A., 1988, Diel vertical migrations by juvenile sockeye salmon and the

antipredation window, American Naturalist 131: 271–290.

Cooper, W.J., Chihwen, S., Lean, D.R.S., Gordon, A.S., and Scully, F.E., Jr., 1994, Factors affecting the distribution of H2O2 in surface waters, In Environmental Chemistry of Lakes and Rivers, edited

by L.A Baker, American Chemical Society, Washington, D.C., pp 391–422

Curtis, P.J., 1993, Effect of dissolved organic carbon on 59Fe scavenging, Limnology and Oceanography

38: 1554–1561

Curtis, P.J and Schindler, D.W., 1997, Hydrologic control of dissolved organic matter in low-order

Precambrian Shield lakes, Northwestern Ontario, Biogeochemistry 36: 125–138.

Dillon, P.J., Clark, B.J., and Molot, L.A., 2003, Predicting optimal habitat boundaries for lake trout

(Salvelinus namaycush Walbaum) in Canadian Shield lakes, Canadian Journal of Fisheries and

Aquatic Sciences (in press).

Dillon, P.J and Molot, L.A., 1997, Dissolved organic and inorganic carbon mass balances in central

Ontario lakes, Biogeochemistry 36: 29–42.

Dodson, S.I., 1990, Predicting diel vertical migration of zooplankton, Limnology and Oceanography

35: 1195–1200

Donahue, W.F., Schindler, D.W., Page, S.J., and Stainton, M.P., 1998, Acid-induced changes in DOC

quality in an experimental whole-lake manipulation, Environmental Science and Technolgy 32:

2954–2960

Driscoll, C.T., Blette, V., Yan, C., Schofield, C.L., Munson, R., and Holsapple, J., 1995, The role of dissolved organic carbon in the chemistry and bioavailability of mercury in remote

Adiron-dack lakes, Water, Air, and Soil Pollution 80: 499–508.

Elser, J.J., Chrzanowski, T.H., Sterner, R.W., and Mills, K.H., 1998, Stoichiometric constraints on

food-web dynamics: a whole-lake experiment on the Canadian Shield, Ecosystems 1: 120–136.

Engstrom, D.R., 1987, Influence of vegetation and hydrology on the humus budgets of Labrador

lakes, Canadian Journal of Fisheries and Aquatic Sciences 4: 1306–1314.

Fee, E.J., Hecky, R.E., Kasian, S.E.M., and Cruikshank, D.R., 1996, Effects of lake size, water clarity,

and climatic variability on mixing depths in Canadian Shield lakes, Limnology and

Oceanog-raphy 41: 912–920.

Gorham, E., 1996, Lakes under a three-pronged attack, Nature 381: 109–110.

Gunn, J.M., 2001, Impact of the 1998 El Nino event on a lake charr, Salvelinus namaycush, population

recovering from acidification, Environmental Biology of Fishes 41: 1–9.

Gunn, J.M., Snucins, E., Yan, N.D., and Arts, M.T., 2001, Use of water clarity to monitor the effects

of climate change and other stressors on oligotrophic lakes, Environmental Monitoring and

Assessment 67: 69–88.

Gunn, J.M., Steedman, R.J., and Ryder, R.A (Eds.), 2004, Boreal Shield Watersheds: Lake Trout Ecosystems

in a Changing Environment Lewis Publishers, Boca Raton.

Hassett, R.P., Cardinale, B., Stabler, L.B., and Elser, J.J., 1997, Ecological stoichiometry of N and P in pelagic ecosystems: comparisons of lakes and oceans with emphasis on

zooplankton–phy-toplankton interactions, Limnology and Oceanography 41: 648–662.