Food Web Bioaccumulation of Organohalogenated Compounds in High Mountain Lakes

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Limnetica, 29 (2): x-xx (2011) Limnetica, 31 (1): 155-164 (2012). DOI: 10.23818/limn.31.14 c Asociacion´ Iberica´ de Limnolog´aı , Madrid. Spain. ISSN: 0213-8409

Food web bioaccumulation of organohalogenated compounds in high mountain lakes

Mireia Bartrons1,2,∗,JoanO.Grimalt3 and Jordi Catalan2

1 Center for Limnology, University of Wisconsin, Madison, 680 N. Park St. Madison, WI 53706, USA. 2 Limnology Unit (CSIC-UB). Centre for Advanced Studies of Blanes (CEAB-CSIC). Acces´ Cala St. Francesc, 14. 17300 - Blanes, Catalonia, Spain. 3 Department of Environmental Chemistry (IIQAB-CSIC). Jordi Girona, 18. 08034-Barcelona, Catalonia, Spain.

∗ Corresponding author: [email protected] 2 Received: 2/1/2012 Accepted: 30/1/2012

ABSTRACT Food web bioaccumulation of organohalogenated compounds in high mountain lakes Persistent organic pollutants (POPs) are toxic substances that are usually produced for use in agricultural, industrial, and domestic applications. Because of their long-range atmospheric transport capacity, POPs are distributed worldwide. The global distillation theory predicts that there will be a temperature-dependent partitioning of these low volatility compounds in the environment. Concentration patterns of POPs in agreement with the theory have been observed for different environmental compartments, such as lake sediments and mosses, and along altitudinal and latitudinal gradients. However, concentration patterns in lake ﬁsh do not exactly match the expected results, indicating that further investigation into the bioaccumulation processes in food webs is required. Here, we brieﬂy review the state of the question of POPs bioaccumulation in high mountain lake food webs and present some hypotheses concerning processes worthy of investigation.

Key words: Persistent organic pollutants, organochlorinated compounds, PBDEs, bioaccumulation, food webs, high mountain lakes, altitudinal gradient.

RESUMEN Bioacumulacion´ de compuestos organohalogenados en redes tro´ficas de lagos de alta montana˜ Los contaminantes organicos´ persistentes (POPs) son sustancias producidas para usos agr´ıcolas, urbanos o industriales que presentan un caracter´ toxico.´ Debido a la capacidad de transporte atmosferico´ a largo alcance, los POPs son distribucidos por todo el mundo. La teor´ıa de la Destilacion´ Global propone una distribucion´ de estos compuestos de baja volatilidad en el medio ambiente dependiente de la temperatura del aire. Se ha observado este fenomeno´ en distintos compartimentos ambientales situados a lo largo de gradientes de altitud o latitud, como por ejemplo en sedimentos de lagos o en musgos. Sin embargo, algunas de las pautas observadas en peces no responden a lo esperado y ponen de relieve la falta de un conocimiento suficiente sobre la transferencia de estos contaminantes en las redes tro´ficas. Aqu´ı se hace una breve revision´ del estado de la cuestion´ sobre la bioacumalacion´ de compuestos organicos´ persistentes en lagos de montana˜ y se sugieren algunas hipotesis´ sobre posibles procesos a investigar.

Palabras clave: Compuestos organicos´ persistentes, organoclorados, PBDEs, bioacumulacion,´ redes tro´ﬁcas, lagos de alta montana,˜ gradiente altitudinal. 156 Bartrons et al.

PERSISTENT ORGANIC POLLUTANTS with the publication of Rachel Carson’s Silent Spring (Carson, 1962). Through her book and Persistent organic pollutants (POPs) are gen- the accompanying media attention, the general erally halogen-substituted toxic hydrocarbon public first became aware of a downside to the molecules that have a cyclic or aromatic struc- proliferation of chemicals. ture (Fig. 1). They are semi-volatile, highly hy- The first global regulation to outlaw, limit the drophobic and degrade slowly under natural use of or curtail the inadvertent production of conditions. They are produced for agricultural, POPs was agreed in the Stockholm Convention urban, and industrial applications. Because of on Persistent Organic Pollutants in May 2001 and these characteristics, they can be atmospherically entered into force on May 2004. Twelve groups transported long distances and bioaccumulate in of substances, known as the dirty dozen, were organisms. Many POPs are distributed widely initially included. All of the compounds exhib- across the earth, including in regions where they ited prolonged environmental persistence, bioac- have never been used (Wania & Mackay, 1993; cumulation, high toxicity, and the potential for Simonich & Hites, 1995). Due to their toxicity, long-range environmental transport. they can pose a threat to humans and the environment. For instance, biomagnification exposes animals from the top food web positions to doses GLOBAL DISTILLATION THEORY which may cause endocrine disruption, altered neurological development, immune system mod- The atmosphere is the main route of dispersal of ulation, and cancer (Who, 2003). POPs far from centers of human population The use of POPs began with the growth of (Eisenreich & Strachan, 1992). Once in the envi- the organic chemical industry in the early 20th ronment, they cycle and partition between major century; dichlorodiphenyltrichloroethane (DDT) environmental compartments. Due to their semi- was the first POP synthesised in 1874. As the volatile character (vapour pressure between 10−4 use of halogenated, particularly chlorinated, or- and 10−11 atm at 25 ◦C), the compounds also par- ganic chemicals rose in agricultural and indus- tition between the atmospheric gas and aerosol trial sectors, so did concern about potential ad- phases (Duinker & Bouchertall, 1989; Aceves verse consequences to human health and the & Grimalt, 1993; Kaupp & McLachlan, 1999) environment. In 1962, a turning point occurred (Fig. 2). Association with atmospheric particles increases their removal rate from the atmosphere

Cl Cl Cl Cl Cl by dry and wet deposition processes, which ulti- Cl Cl mately limits the distance they travel from their Cl Cl Cl Cl sources. Thus, removal from the atmosphere oc- Cl Cl curs by dry deposition of particulate-bound pol- Cl Cl Cl Cl lutants, diffusive gas exchange between atmo- HCHs HCB DDT sphere and water surfaces, and scavenging by O rain (wet deposition) (Fig. 2). In addition, during atmospheric transport, POPs can undergo a number of processes that will determine their fate Brm Brm Cln Cln in the global environment, such as degradation, PCBs PBDEs deposition to soils, vegetation or water bodies, Figure 1. Chemical structure of hexachlorocyclohexanes revolatilisation, sedimentation, and bioaccumula- (HCHs), hexachlorobenzene (HCB), dichlorodiphenyltrichlo- tion (Fig. 2). The signiﬁcanceof each of these pro- roethane (DDT), polychlorobiphenyls (PCBs) and polychlo- cesses depends on the climatic conditions and the rodiphenyl ethers (PBDEs). Estructura de los hexaclorociclo- hexanos (HCHs), hexaclorobenceno (HCB), diclorodifeniltri- physico-chemical properties of each compound. cloroetano (DDT), bifenilos policlorados (PCBs) y polibromo- Cold regions retain POPs as a result of difenil eteres´ (PBDEs). temperature-dependent partitioning between gas, Organohalogen bioaccumulation in lake food webs 157

ATMOSPHERE Gas-Particle Partition

Gas Air -Soil or air- Photodegradation vegetation exchange Dry Deposition Wet Deposition

Air -Water exchange SOIL WATER Hydraulic transport

Bioaccumulation Dissolved phase SedimentationSedimentation-Diffusion

SEDIMENT

Figure 2. Main environmental processes occurring during long-range atmospheric transport of POPs. Adapted from Fernandez´ & Grimalt (2003). Principales procesos ambientales que ocurren en la atmosfera´ durante el transporte de los contaminantes organicos´ persistentes a larga distancia. Adaptado de Fernandez´ & Grimalt (2003). water and particles during long-range transport. al., 2001). The global distillation theory is based The whole process is known as the global distil- on the shift in phase distribution equilibrium of lation theory (Wania & Mackay, 1993; Wania & semi-volatile chemicals from the atmospheric gas Mackay, 1996). POPs have been found at signiﬁ- phase to the earth’s surface with decreasing tem- cant concentrations at high latitudes (Kidd et al., perature. As a consequence, the theory predicts 1998) and altitudes (Blais et al., 1998; Grimalt et a process of global fractionation in which or-

High latitudes Deposition > Evaporation

Mid-latitudes Seasonal cycling of deposition High mobility with and evaporation Global distillation fractionation according to global mobility

Long-range atmospheric transport

Low mobility Low latitudes Evaporation > Deposition

“Grasshopping”

Figure 3. POP migration processes. Global deposition processes become more pronounced than evaporation at high latitudes and lower temperatures. Adapted from Wania & Mackay (1996). Procesos de migracion´ de POP. Los procesos globales de deposicion´ son mas´ pronunciados que los de evaporacion´ en las latitudes altas y temperaturas bajas. Adaptado de Wania y Mackay (1996). 158 Bartrons et al. ganic compounds become latitudinally and alti- depuration of the unchanged compound (mainly tudinally fractionated, “condensing” at different via gill loss) is generally slower than the rate ambient temperatures according to their volatil- of uptake (mainly via gut uptake) for highly ity. Transport to colder regions can, at least in lipophilic compounds (Catalan et al., 2004), thus part, occur via repeated cycles of deposition and the concentration in the organism may become evaporation driven by seasonal, frontal, and di- higher than would be expected from a thermody- urnal changes in temperature; this is known as namic equilibrium after achieving a steady state grasshopping transport (Fig. 3). of the input and output fluxes of the pollutant. However, in mountains, which are charac- The bioaccumulation potential of organic terised by a gradient of temperature from low to chemicals is often compared to the octanol-water high altitudes, the preferential accumulation of partition coefficient (KOW). KOW is the ratio of organic pollutants is different from the one pro- the concentration of a chemical in octanol to its duced between low and high latitudes (Grimalt concentration in water at equilibrium at a spec- et al., 2001; Fernandez & Grimalt, 2003). Sub- ified temperature (Mackay, 1982). It indicates stances accumulating in mountains are approxi- the hydrophobicity of a chemical and how it mately two orders of magnitude less volatile than thermodynamically distributes between the aque- the substances that experience latitudinal cold ous and organic phases. In aquatic food webs, trapping. Wania & Westgate (2008) proposed that only hydrophobic, fat-soluble chemicals with this phenomenon is produced by differences in octanol-water partition coefficients greater than the efficiency of precipitation scavenging at var- 100 000 are bioaccumulated. In contrast, poorly ious elevations, which in turn is caused by the metabolised, moderately hydrophobic substances temperature dependence of organic vapour parti- with a KOW between 100 and 100 000 do not tioning into rain, snow, and aerosols. biomagnify in aquatic food webs. However, they can biomagnify in food webs containing air- breathing animals (including humans) to a high FOOD WEB BIOACCUMULATION OF degree because of their high octanol-air partition ORGANOHALOGEN COMPOUNDS coefficient (KOA) and a corresponding low rate of respiratory elimination to air. Bioaccumulation is a process in which the con- Various conceptual models have been used centration of a chemical in an organism in- over the years to describe the toxicokinetics of creases compared to the concentration in the organohalogen compounds. The simplest treat- environment over time. It can occur directly ment of uptake is to multiply the feeding rate by from exchange with the media (bioconcentra- the concentration of organohalogen compound in tion) or by feeding (biomagnification) (Thomann, food and by the efficiency of uptake of the or- 1981). Bioaccumulation eventually results from ganism. There are numerous examples of feeding the balance between uptake, via dietary inges- studies in the literature showing that the uptake tion and respiration, and loss, via growth dilu- efficiency of organohalogen compounds from the tion, respiration, metabolism, and faecal egestion diet is high, presumably because the efficiency of (Campfens & Mackay, 1997). lipid uptake is also high. This simple approach Most POPs and natural compounds that have a was accepted for many years until it was called tendency to biomagnify in food webs are neutral into question by a theory that proposed that ab- organic compounds that are highly substituted (or sorption is driven by diffusion of organohalo- substituted at critical positions in the molecule) gen compounds between the gut content and with chlorine or bromine. These properties make the organism (Gobas et al., 1993). Within this them lipophilic and not easily metabolised. Their theory, food absorption is expected to “mag- lipophilic nature ensures their efficient uptake nify” the chemical concentration in the food, from the diet and storage in fat depots, and the thus raising the diffusion between the gut content halogens prevent attack by enzymes. The flux of and the organism internal media. Organohalogen bioaccumulation in lake food webs 159

In birds and mammals, the fugacity gradient HIGH MOUNTAIN LAKES model of Gobas et al. (1993) does not fitpar- ticularly well with what is known about the Remote mountain regions are increasingly af- physiology of lipid absorption in these organ- fected by anthropogenic influences, despite be- isms. For instance, studies in kestrels (Falco ing situated above the tree line in areas that are sparverius) and ring doves (Streptopelia risoria) rarely disturbed by agriculture, forestry, and hu- showed that uptake of organohalogen compounds man settlement. Recent research indicates that occurs in the upper gut through the same mecha- even the most remote lakes in Europe contain nism by which lipids are absorbed (Drouillard & atmospherically transported pollutants, and evi- Norstrom, 2000). The process is driven by dif- dence is growing that climate change is begin- fusion of lipid-containing micelles through the ning to have a significant impact on them (Battar- epithelial wall of the upper gut. The mechanism bee, 2005). In particular, alpine lake ecosystems is very efficient and not highly dependent on are especially sensitive to external forcing be- KOW. Once absorbed, distribution of organohalo- cause their small catchments in relation to the gen compounds among the various lipid pools lake area make atmospheric loading more rele- in the body occurs relatively quickly. Circulating vant in their dynamics. This feature and their re- organohalogen compounds are excreted slowly moteness from areas of high human activity make into the lower gut via a fugacity gradient-driven alpine lakes excellent sentinels and recorders of process, which is highly dependent on the log past and present global changes (Catalan et al., KOW of the compound and metabolism. This phe- 2006). However, most previous studies focused nomenon likely applies to all birds and mammals, on a reduced number of organisms or on spe- but it is not clear whether it also applies to fish cific ecological compartments (e.g., phytoplank- and other ectothermic organisms, such as inverte- ton, zooplankton, fish, etc.). There is still insuffi- brates, where lower body temperatures may slow cient knowledge of high mountain lake food webs diffusion rates and decrease the bioavailability of and how they change with increasing altitude. high KOW organohalogen compounds. Because temperature is a determinant of the In summary, there is evidence that not all distribution of organochlorine compounds along organisms bioaccumulate organohalogen com- altitudinal profiles (Blais et al., 1998; Carrera pounds in the same way. The organisms’ size, et al., 2001; Grimalt et al., 2001; Ribes et al., age, lipid content, metabolic rate and biotrans- 2002), high mountain lakes are excellent settings formation capacity are some of the factors that to study the processes involved in the “global influence bioaccumulation rate the most. For distillation theory”. The transport of organohalo- example, the concentrations of lipophilic and gen compounds in mountains has been well doc- persistent organochlorines are orders of magni- umented. They have been found in snow (Blais tude higher in endotherms than in ectotherms et al., 1998; Carrera et al., 2001), sediment (Gri- as a result of the different energy requirements, malt et al., 2001), mosses (Grimalt et al., 2004), bioaccumulation procedures (as described pre- amphipods (Blais, 2003) and fish ...(Grimalt et viously), and biotransformation abilities (Hop al., 2001; Vives et al., 2004; Demers et al., 2007; et al., 2002). Furthermore, the bioaccumulation Gallego et al., 2007), and the concentration of or- of organohalogen compounds is less understood ganichlorine (OC) and polybromodiphenyl ether in organisms of lower trophic levels. For in- (PBDE) compounds increased with elevation. stance, the biotransformation capacity of different organisms, the importance of their feeding habits and behaviour, and the influence BIOACCUMULATION OF OCs AND PBDEs of environmental variables such as tempera- IN HIGH MOUNTAIN LAKE FOOD WEBS ture on the biomagnification of organohalogen compounds by aquatic macroinvertebrates The distribution patterns of persistent organic is not well resolved at present. pollutants along mountain altitudinal profiles 160 Bartrons et al. are in agreement with the prediction of a explain the patterns. Alternately, the existence of temperature-dependent partitioning of low this variability without major differences in food volatile compounds by the global distillation the- web composition among lakes suggests that δ15N ory (Wania & Mackay, 1993; Wania & Mackay, values are suitable for monitoring and evaluating 1996). However, in several studies on mountain the increase in nitrogen deposition as a compo- lake fish (Vives et al., 2004; Demers et al., 2007; nent of global change. Gallego et al., 2007), the altitudinal patterns found do not fully agree with the POPs theo- Trophic position as a bioaccumulation factor retical phase-change enthalpies. In some cases (Vives et al., 2004), the pseudo-enthalpies are How important is trophic position in determin- two-fold higher than those found for sediments. ing the amount of OCs in an organism com- Therefore, investigating the food web bioac- pare to other factors? Does the importance of cumulation of halogenated compounds in high trophic position change according to the char- mountain lakes could provide new clues about acteristics of the compound (e.g., KOW)? Does the mechanisms involved in bioaccumulation temperature have any other additional effect be- processes and their temperature dependence. yond its role in setting the initial concentrations in water? How do trophic factors compare with Food web trophic structure other traditional factors, such as lipid content? Lipid content is a key factor introducing variation Determining the food web structure is a neces- among individuals of the same species, but is it sary first step to understand the bioaccumula- still relevant when comparing small organisms of tion of POPs in food webs. Therefore, stable iso- different trophic levels? topes from organic C and N in the main food Do all types of organohalogen compounds be- web organisms should be analysed. Bartrons et have similarly in food webs? For instance, PB- al. (2010) showed that variability in 15Nwas DEs are less biologically recalcitrant than the high in the initial sources of food web nitro- correspondent PCBs because they have a struc- gen (dissolved ammonium and nitrate). Nitro- ture similar to that of secondary metabolites gen deposition in remote areas has increased, but from marine and terrestrial plants and animals the effect on ecosystems is still poorly under- (Kicklighter et al., 2004; Teuten et al., 2005). stood. Differences in dissolved inorganic nitro- Perhaps PBDE and other organic pollutants are gen (DIN) between lakes cannot be understood biotransformed in food webs more than was without considering catchment characteristics. In commonly assumed. The evolutionary trophic mountains, catchment features (e.g., thermal con- history of each group could modulate the abil- ditions and land cover features) vary consider- ity of each organism to handle the pollutants. Or- ably with elevation. According to Bartrons et al. ganisms that experience frequent allelochemical (2010), lakes with a greater snow-type influence interactions might as a result be better adapted will most likely register changes in N deposition to biotransform PBDEs than those without such and pollution sources better, whereas lakes with a situation throughout their evolutionary history higher soil-type influence may reflect the long- (e.g., clades of secondary consumers). term effects of vegetation and soil dynamics. Due to this high isotopic variation in the initial ni- Metamorphosis and metabolism trogen sources and the in-lake habitat variability, we can expect large variation in the δ13Cand The occurrence of different metabolic states dur- δ15N values within (i.e., littoral/bottom) and be- ing the metamorphosis of aquatic insects (e.g., tween (i.e., montane/alpine) lake food webs. The pupa vs. larva) is also an important factor in nature and availability of the N sources for pri- the bioaccumulation of OCs and PBDEs in food mary producers and the omnivory in these olig- webs. For instance, weight loss by pupae during otrophic systems could turn out to be crucial to metamorphosis resulting from protein carbon ox- Organohalogen bioaccumulation in lake food webs 161 idation and lack of feeding produced increased ductivity is higher. In particular, thicker biofilms pollutant concentrations during metamorphosis develop, which increases the probability of find- (Bartrons et al., 2007). ing anaerobic microenvironments. Recently, we Metabolism should also be considered in the found that these sites are extremely important for context of the concentration changes of POPs in the microbial degradation of PBDEs (Bartrons et food web organisms from lakes located along al., 2011), which is enhanced in anaerobic envi- altitudinal gradients. PCBs are good candidates ronments (Gerecke et al., 2005; He et al., 2006; for investigating the metabolic aspects of bioac- Vonderheide et al., 2006). As a consequence of cumulation. The concentrations of PCBs found the change in the availability of these anaero- in the first trophic positions along the altitudi- bic microsites, a strong gradient in the concen- nal gradient should follow a similar trend to that tration of PBDEs in rock, sand and fine sediment found in sediments, with concentration increas- biofilms was found throughout the altitudinal ing with altitude. However, if metabolism is con- gradient. These results suggest that in addition trolling the bioaccumulation throughout the food to the global distillation effect, enhancement or web and temperature is controlling metabolism, depletion of biodegradation may be relevant for the rate of pollutant increase (slope) with al- the assessment of the global distribution of these titude should be lower the higher the trophic compounds at a planetary scale. position of a species. This is because ectothermic organisms have lower energetic requirements with decreasing temperature and consequently CONCLUSION have lower food intake and respiration. If this is the case, it implies that the food web does Food web bioaccumulation of persistent organic not have any direct influence on the altitudi- pollutants in mountain lakes is a consequence of nal amplification of organohalogen compounds multiple factors: the intrinsic features of the or- found in fish (Grimalt et al., 2001; Vives et ganisms, such as their developmental stage or al., 2004; Demers et al., 2007; Gallego et al., their metabolic activity in relation to their trophic 2007). Physiological and behavioural studies are position; the external factors related to lake al- needed to understand the observed altitudinal titude, which in turn affect the metabolic ac- trends of organohalogen compounds in fish. For tivity of the organisms; and the behaviour of instance, recent findings suggested that fish have POPs in the environment (Wania & Mackay, different capacities to biotransform PCBs de- 1993; Wania & Mackay, 1996). Both the pres- pending on the water temperature (Buckman et ence of POPs in these remote systems, located al., 2007). A better understanding of organohalo- far away from their emission sites, and the tem- gen compound transmission from brown trout fe- perature variation associated with the altitudi- males to their eggs and the bioaccumulation in nal gradient, which can be used to simulate cli- the succeeding developmental stages (fry, juve- mate change scenarios, are important aspects nile and adult fish) would be useful to clarify of the global change occurring on earth. Thus, the temperature dependence of bioaccumulation high-mountain lake food webs are suitable for of organohalogen compounds by fish. monitoring the effects of global change, especially those related to the toxification of na- The challenge of microenvironments ture by persistent organic pollutants. The loca- tion of high-mountain lakes far from centres of A lot of biological activity in mountain lakes human population, their position along large al- occurs microbiologically at microsites. The fea- titudinal gradients without other major changes tures of the environment in these sites may sig- in the main lake characteristics, the simplicity of nificantly different from that in the main water their food webs and, overall, their sensitivity to column. At lower altitudes with higher temper- external forcing, make them excellent sentinels atures and prolonged growing seasons lake pro- and recorders of present and past global changes. 162 Bartrons et al.

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