Global Change Biology (2016) 22, 164–179, doi: 10.1111/gcb.12967

RESEARCH REVIEW

Impact of nitrogen deposition on forest and lake food webs in nitrogen-limited environments
C H E Z 1 and A N T O N I A L I E S S 1
R I C L . M E U N I E R 1 * , M I C H A E L J . G U N D A L E 2 , I R E N E S . S AN C ED 1 Department of Ecology and Environmental Sciences, Umea˚ University, 901 87 Umea˚, Sweden, 2Department of Forest Ecology and Management, Swedish University of Agricultural Sciences, Ume a 901 83, Sweden

Abstract Increased reactive nitrogen (Nr) deposition has raised the amount of N available to organisms and has greatly altered the transfer of energy through food webs, with major consequences for trophic dynamics. The aim of this review was to: (i) clarify the direct and indirect effects of Nr deposition on forest and lake food webs in N-limited biomes, (ii) compare and contrast how aquatic and terrestrial systems respond to increased Nr deposition, and (iii) identify how the nutrient pathways within and between ecosystems change in response to Nr deposition. We present that Nr deposition releases primary producers from N limitation in both forest and lake ecosystems and raises plants’ N content which in turn benefits herbivores with high N requirements. Such trophic effects are coupled with a general decrease in biodiversity caused by different N-use efficiencies; slow-growing species with low rates of N turnover are replaced by fast-growing species with high rates of N turnover. In contrast, Nr deposition diminishes below-ground production in forests, due to a range of mechanisms that reduce microbial biomass, and decreases lake benthic productivity by switching herbivore growth from N to phosphorus (P) limitation, and by intensifying P limitation of benthic fish. The flow of nutrients between ecosystems is expected to change with increasing Nr deposition. Due to higher litter production and more intense precipitation, more terrestrial matter will enter lakes. This will benefit bacteria and will in turn boost the microbial food web. Additionally, Nr deposition promotes emergent insects, which subsidize the terrestrial food web as prey for insectivores or by dying and decomposing on land. So far, most studies have examined Nr-deposition effects on the food web base, whereas our review highlights that changes at the base of food webs substantially impact higher trophic levels and therefore food web structure and functioning. Keywords: arctic, boreal, bottom-up, ecological stoichiometry, food quality, nutrient cycle, top-down, trophic interaction Received 15 December 2014; revised version received 26 March 2015 and accepted 29 April 2015

Introduction The use of agricultural fertilizers and fossil fuels has risen dramatically over the past 150 years (Galloway & Cowling, 2002), and today, reactive nitrogen (Nr) is produced at rates of about 10 times higher than a century ago (Steffen et al., 2004). This in turn has amplified atmospheric Nr concentrations and has increased atmospheric Nr-deposition rates (Holland et al., 2005; Galloway et al., 2008). Globally, it has been calculated that in 1860, 34 Tg N yr 1 was emitted and then deposited to the Earth’s surface. This value increased to 100 Tg N yr 1 in 1995, and it is projected that 200 Tg N yr 1 will deposit in 2050 (Galloway et al., *Present address: Alfred Wegener Institute, Ostkaje 1118, 27498, Helgoland, Germany Correspondence: C
edric L. Meunier, Department of Ecology and Environmental Sciences, Umea˚ University, 901 87 Umea˚, Sweden, tel. +49 4725 819 3361, fax +49 4725 819 3369, e-mail: [email protected]

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2004). In less impacted northern lakes and forests, N deposition is generally around 0.5 kg N ha 1 yr 1 or less (Dentener et al., 2006). However, there are now large regions of the world, including boreal forests and lakes, where average Nr-deposition rates exceed 10 kg N ha 1 yr 1 (Galloway et al., 2004). Therefore, the amount of N available to plants and animals has tremendously increased (Bobbink et al., 2010), disturbing the global N cycle, and making anthropogenic Nr deposition a key global change factor (Steffen et al., 2004). Deposition of Nr is likely to have its biggest impacts in ecosystems where Nr-deposition rates are substantially elevated by anthropogenic activities, and where net primary production is inherently N limited. As such, boreal and temperate forests are both N limited, and portions of these biomes also receive significant inputs of anthropogenically derived N, which has led them to be the focus of many Nr-deposition studies (Tamm, 1991; Schlesinger, 2009). Moreover, the increasing Nr-deposition gradient from arctic to temperate systems has caused southern lakes to shift towards © 2015 John Wiley & Sons Ltd

N - D E P O S I T I O N I M P A C T S O N N - L I M I T E D E N V I R O N M E N T S 165 phosphorus (P) limitation, while many lakes in the arctic remain N limited (Bergstr€ om & Jansson, 2006). This nutrient-limitation gradient has provided an opportunity to study the impact of Nr deposition on northern-boreal and arctic N-limited lakes. Understanding how food web structure is and will be affected by Nr deposition is an important step to predicting how terrestrial and aquatic ecosystems will respond to this key global change factor. Forests in boreal and temperate regions often exhibit a low degree of soil N availability, and thus, N is often the primary growth-limiting nutrient (Tamm, 1991). The effect of Nr deposition on temperate and boreal forest growth has been studied for over 30 years (e.g. Andersson et al., 1980), and it is well known that Nr deposition often directly enhances forest productivity. Numerous studies have described the impact of forest N enrichment on primary producers, whereas far fewer studies addressed whether Nr deposition alters trophic interactions among plants, herbivores, and predators (Tylianakis et al., 2008). Studies on freshwater ecosystem responses to Nr deposition have emerged during the last decade. These studies have investigated how Nr deposition affects nutrient limitation of lake primary producers and have shown that Nr deposition alleviates phytoplankton and periphyton N limitation and intensifies P limitation (Bergstr€ om et al., 2005; Bergstr€ om & Jansson, 2006; Elser et al., 2009a; Liess et al., 2009), which may change nutrient cycling and community structure of whole lake food webs. At the interface between aquatic and terrestrial ecosystems, dynamic exchange of nutrients (e.g. al-

lochthonous transfers) takes place, and Nr deposition is expected to increase nutrient fluxes in both directions. In this review, we outline the potential effects of Nr deposition on food web interactions (i) in N-limited temperate and boreal forests, (ii) in temperate, boreal, and arctic lakes, and (iii) at the interface between lakes and forests.

Nitrogen-deposition effects on forest food webs

Primary production In forest ecosystems, increasing Nr deposition influences the structure and functioning of food webs. Nitrogen is the element generally limiting primary production in most northern temperate and boreal forests (Tamm, 1991; Vitousek & Howarth, 1991). Deposition of Nr therefore has a direct fertilizing effect, which has been shown to increase carbon (C) uptake by vascular plants, and in particular trees, in the range of 15–60 kg of C per kilogram of N deposited (Fig. 1, I; H€ ogberg et al., 2006; Pregitzer et al., 2008; Thomas et al., 2010; De Vries et al., 2014; Gundale et al., 2014). Not only Nr deposition but also rising temperatures and CO2 levels are expected to influence primary production. Although the effects of these abiotic changes are synergistic, Nr deposition has been suggested as a main driver of increased net primary production (Churkina et al., 2009). Nitrogen deposition is also frequently associated with changes in the composition of the understory flora (Fig. 2a, Diekmann & Falkengren-Grerup, 2002). Results from field experiments and large-scale

Fig. 1 Simplified conceptual model of Nr-deposition effects on forest food webs. © 2015 John Wiley & Sons Ltd, Global Change Biology, 22, 164–179

166 C . L . M E U N I E R et al. (a1)

(a2)

(b1)

(b2)

(c1)

(c2)

Fig. 2 Boreal N-limited spruce forest divided in control (a1) and N-fertilization (average of 90 kg N ha 1 yr 1, (a2) plots. Thirty years of N fertilization resulted in higher tree growth (Ryan, 2013), lower understory cover, and altered understory species composition from a bilberry–blueberry to a fern dominated community (personal observations). The decrease in understory cover is mainly caused by high N-addition levels, which strongly increased tree growth and closed the canopy, hence shading the understory. Fertilization also decreased the fungal biomass, abundant in the control plots (b1) and very low in the fertilized plots (b2, Majdi et al., 2001). Consequently, the relative abundance of fungivore (c1) and bacterivore (c2) nematodes was switched in favour of the latter (C.L. Meunier, unpublished data). Fungal feeding nematodes are characterized by a piercing stylet, which is used to puncture the cell wall of fungi and to suck out the internal contents. Bacterial feeding nematodes have specialized ornate lip structures that distinguish them from other nematodes. Forest and soil pictures credit: N.I. Maaroufi, Swedish University of Agricultural Sciences, Department of Forest Ecology and Management. Nematodes mouth parts pictures credit: H.H.B. van Megen, Wageningen University, Department Nematology.

monitoring studies show that plant community composition changes can occur with even low N-addition doses (5–10 kg N ha 1 yr 1; Bobbink et al., 2010) and that vegetation recovery, once N inputs have stopped, is slow (Nordin et al., 2005; Bobbink et al., 2010). Changes in competitive relationships between understory species are of primary importance for vegetation changes (Kellner & Redbo-Torstensson, 1995; Bobbink et al., 1998). Tall-growing species with high growth rates are generally favoured by high Nr deposition at the expense of smaller species with conservative growth strategies (Diekmann & Falkengren-Grerup, 2002). Physiological plant features such as nutrient requirements also alter interspecific competition, giving a competitive advantage to nitrophilic species (Price & Morgan, 2007). While forest understory communities often exhibit rapid changes in response to N enrichment (e.g. Gundale et al., 2014), species turnover among canopy trees is often very slow, with a majority of research focused on tree physiological responses (e.g. changes in tissue production, chemistry, or within tree

C allocation H€ ogberg & Read, 2006; Pregitzer et al., 2008; Gundale et al., 2014). Both physiological and community-level responses to N availability result in changes in plant tissue quality. Nitrogen deposition has been shown to increase understory foliar N concentration by up to 22% for herbs and ferns and by 8% for deciduous tree seedlings (Hurd et al., 1998), and tree foliar N concentration by 22% for conifers and 13% for deciduous trees (Throop & Lerdau, 2004). Throop & Lerdau (2004) showed that Nr deposition can change leaf N composition, by increasing free amino acid concentrations. Other studies reported that N additions can result in higher foliar protein content and altered protein profiles (Pietila et al., 1991; Rao et al., 1993). Besides increasing foliar N concentration, Nr deposition can considerably change other foliar nutrient concentrations, such as base cations (Katzensteiner et al., 1992; Duquesnay et al., 2000). Reactive N deposition can also cause qualitative changes in plant C chemistry by impacting the biosynthesis of secondary metabolites. Forest plants often con© 2015 John Wiley & Sons Ltd, Global Change Biology, 22, 164–179

N - D E P O S I T I O N I M P A C T S O N N - L I M I T E D E N V I R O N M E N T S 167 tain a relatively large pool of nonstructural C compounds, which serve to defend plants against herbivores, in addition to other functions (for review, see Stamp, 2003). Several hypotheses, including the C: nutrient balance and the growth-differentiation balance hypotheses (Stamp, 2003), have been developed to describe how nutrient availability influences whether C is allocated to growth or defence. The C:nutrient balance hypothesis describes changes occurring at a plastic level (i.e. the same species can produce more or fewer defence compounds) and through modification in community composition (i.e. well-defended/slow-growing species are replaced by poorly defended/fast-growing species). The growth-differentiation balance hypothesis states that as growth and defence processes compete for available nutrients (Wadleigh et al., 1946; Veihmeyer & Hendrickson, 1961; Mooney & Chu, 1974), there are trade-offs between allocating nutrients towards growth or defence mechanisms (Lorio, 1986). Overall, these two hypotheses predict that increasing Nr-deposition rates lead to decreased allocation to C-based defence metabolites (Herms & Mattson, 1992; Jones & Hartley, 1999). Consistent with those predictions, a meta-analysis identified that species adapted to resource-rich environments grow inherently faster and invest less in constitutive defences than species adapted to less productive habitats (Endara & Coley, 2011).

Above-ground primary consumers Changes in plant quality are known to strongly impact the growth and reproduction rates of herbivores and parasites (Mattson, 1980; Scriber & Slansky, 1981; Slansky & Rodriguez, 1987; White, 1993). Elevated foliar N concentration has been identified as a mechanism promoting fungal infection (Strengbom et al., 2002), and many plant pathogens are increasing in incidence and

range (Parmesan, 2006; Tylianakis et al., 2008). An experiment tested the effects of N fertilization on the expansion of epiphytic algae and on the infection rate of mosses by a fungal parasite (Limpens et al., 2003). Both fungal infection and algal expansion were stimulated by N additions. The effects of Nr deposition on plant quality, described in the previous paragraphs, also have strong implications for herbivore performance. Although very little is known about Nr-deposition effects on the performance of large mammalian herbivores (Table 1), a number of studies have tested the consequences of Nr deposition for insect herbivores. A review by Throop & Lerdau (2004) showed that changes in plant tissue chemistry (higher foliar N and amino acid contents and lower defensive chemicals) caused by atmospheric Nr deposition generally have positive effects on insect performance. They hypothesized that Nr deposition may benefit insect herbivores by increasing plant biomass and the availability of newly flushed leaves, which have relatively high N content and low toughness. Overall, Nr deposition has a positive effect on insect herbivore populations, increasing by up to 30% the individual performance and population growth rates (Fig. 1, II; Throop & Lerdau, 2004). In addition to increasing the total insect herbivore density or population growth rate, Nr deposition can also influence insect community composition through a variety of mechanisms. First, feeding groups or individual species may respond differently to changes in plant nutritional quality resulting in changes in insect species relative abundances (Awmack & Leather, 2002), which has been shown in a variety of N-addition studies. For instance, studies by Eatough Jones (2004), Eatough Jones et al. (2011, 2008) in temperate forest environments showed that N enrichment caused the diversity of insect herbivores associated with ferns and pines to

Table 1 Summary of unknown Nr-deposition effects on different food web parameters, predicted direction and strength of such effects, and suggestion of studies that would fill these knowledge gaps

Food web

Parameter

Above-ground

Large herbivores biomass 2nd consumer biomass Faunal diversity 1st consumer biomass 2nd consumer biomass Zooplankton community structure Fish P limitation Phyto- and zooplankton diversity Benthic herbivores P limitation Benthic herbivores diversity

Below-ground Pelagic

Benthic

Predicted direction and strength + +

++ ++ ++

© 2015 John Wiley & Sons Ltd, Global Change Biology, 22, 164–179

Study type Multivariate statistics on existing datasets Long-term fertilization experiment (predatory insects) Multivariate statistics on existing datasets Long-term fertilization experiments Long-term fertilization experiments Survey of lakes subject to different N inputs Measurement of alkaline phosphatase activity Survey of lakes subject to different N inputs Measurement of alkaline phosphatase activity Survey of lakes subject to different N inputs

N - D E P O S I T I O N I M P A C T S O N N - L I M I T E D E N V I R O N M E N T S 167 tain a relatively large pool of nonstructural C compounds, which serve to defend plants against herbivores, in addition to other functions (for review, see Stamp, 2003). Several hypotheses, including the C: nutrient balance and the growth-differentiation balance hypotheses (Stamp, 2003), have been developed to describe how nutrient availability influences whether C is allocated to growth or defence. The C:nutrient balance hypothesis describes changes occurring at a plastic level (i.e. the same species can produce more or fewer defence compounds) and through modification in community composition (i.e. well-defended/slow-growing species are replaced by poorly defended/fast-growing species). The growth-differentiation balance hypothesis states that as growth and defence processes compete for available nutrients (Wadleigh et al., 1946; Veihmeyer & Hendrickson, 1961; Mooney & Chu, 1974), there are trade-offs between allocating nutrients towards growth or defence mechanisms (Lorio, 1986). Overall, these two hypotheses predict that increasing Nr-deposition rates lead to decreased allocation to C-based defence metabolites (Herms & Mattson, 1992; Jones & Hartley, 1999). Consistent with those predictions, a meta-analysis identified that species adapted to resource-rich environments grow inherently faster and invest less in constitutive defences than species adapted to less productive habitats (Endara & Coley, 2011).

Above-ground primary consumers Changes in plant quality are known to strongly impact the growth and reproduction rates of herbivores and parasites (Mattson, 1980; Scriber & Slansky, 1981; Slansky & Rodriguez, 1987; White, 1993). Elevated foliar N concentration has been identified as a mechanism promoting fungal infection (Strengbom et al., 2002), and many plant pathogens are increasing in incidence and

range (Parmesan, 2006; Tylianakis et al., 2008). An experiment tested the effects of N fertilization on the expansion of epiphytic algae and on the infection rate of mosses by a fungal parasite (Limpens et al., 2003). Both fungal infection and algal expansion were stimulated by N additions. The effects of Nr deposition on plant quality, described in the previous paragraphs, also have strong implications for herbivore performance. Although very little is known about Nr-deposition effects on the performance of large mammalian herbivores (Table 1), a number of studies have tested the consequences of Nr deposition for insect herbivores. A review by Throop & Lerdau (2004) showed that changes in plant tissue chemistry (higher foliar N and amino acid contents and lower defensive chemicals) caused by atmospheric Nr deposition generally have positive effects on insect performance. They hypothesized that Nr deposition may benefit insect herbivores by increasing plant biomass and the availability of newly flushed leaves, which have relatively high N content and low toughness. Overall, Nr deposition has a positive effect on insect herbivore populations, increasing by up to 30% the individual performance and population growth rates (Fig. 1, II; Throop & Lerdau, 2004). In addition to increasing the total insect herbivore density or population growth rate, Nr deposition can also influence insect community composition through a variety of mechanisms. First, feeding groups or individual species may respond differently to changes in plant nutritional quality resulting in changes in insect species relative abundances (Awmack & Leather, 2002), which has been shown in a variety of N-addition studies. For instance, studies by Eatough Jones (2004), Eatough Jones et al. (2011, 2008) in temperate forest environments showed that N enrichment caused the diversity of insect herbivores associated with ferns and pines to

Table 1 Summary of unknown Nr-deposition effects on different food web parameters, predicted direction and strength of such effects, and suggestion of studies that would fill these knowledge gaps

Food web

Parameter

Above-ground

Large herbivores biomass 2nd consumer biomass Faunal diversity 1st consumer biomass 2nd consumer biomass Zooplankton community structure Fish P limitation Phyto- and zooplankton diversity Benthic herbivores P limitation Benthic herbivores diversity

Below-ground Pelagic

Benthic

Predicted direction and strength + +

++ ++ ++

© 2015 John Wiley & Sons Ltd, Global Change Biology, 22, 164–179

Study type Multivariate statistics on existing datasets Long-term fertilization experiment (predatory insects) Multivariate statistics on existing datasets Long-term fertilization experiments Long-term fertilization experiments Survey of lakes subject to different N inputs Measurement of alkaline phosphatase activity Survey of lakes subject to different N inputs Measurement of alkaline phosphatase activity Survey of lakes subject to different N inputs

N - D E P O S I T I O N I M P A C T S O N N - L I M I T E D E N V I R O N M E N T S 169 differences in foliar N content among vascular plant species, highlighting the importance of shifts in plant species composition in driving changes in quality of litter inputs. Overall, increasing Nr deposition will increase the quality of litter entering the soil food web (i.e. reduce leaf-litter C:N ratios, Berg & Meentemeyer, 2002; Callesen et al., 2007). Soil organisms derive their energy almost exclusively from either living or dead plants. Mycorrhizal fungi derive their C directly from living plants and in return provide plants with soil resources, such as N (H€ ogberg & Read, 2006). In contrast, saprotrophic organisms derive their energy from dead plant material. Thus, the flow of C from living plants and plant detritus to soil organisms controls the activity and biomass of bacteria and fungi, and subsequently soil food web interactions. There is abundant evidence that N enrichment significantly affects the activity of the rhizosphere and of mycorrhizal root symbionts in particular (Treseder, 2004). For example, an N-supply gradient study identified that mycorrhizal fungi declined drastically in response to N enrichment (Fig. 1, V; H€ ogberg et al., 2003). Janssens et al. (2010) recently discussed the range of effects that high Nr deposition has on mycorrhizal fungi. Declines in the production of fruiting bodies by mycorrhizal fungi, the relative proportion of mycorrhizae to total microbial biomass, mycorrhizal diversity, mycorrhizal infection rates and survival, and arbuscular mycorrhizal biomass, hyphal length and storage structures have all been reported in response to N addition. This range of impact reflects lower dependence of trees on mycorrhizal symbionts under high Nr deposition, which triggers the reduction in below-ground C allocation (Janssens et al., 2010). While an enhancement in the quality of litter input (i.e. such as reduced C:N or lignin:N ratios) in response to Nr deposition might be expected to increase microbial consumer growth, biomass, and activity, several meta-analysis studies have shown that the opposite is usually the case (Janssens et al., 2010; Lu et al., 2011). In an analysis of 82 published field studies, Treseder (2004) showed that heterotrophic soil respiration declines by 15% on average under N fertilization. Numerous mechanisms have been provided to explain this reduction in soil microbial biomass, including reduced below-ground C allocation by plants to mycorrhizal fungi, direct inhibition of enzymes involved in lignin degradation, decrease in pH, and decrease in C availability (Treseder, 2008; Janssens et al., 2010). Fine roots and mycorrhizal hyphae release considerable amounts of labile C, which serves as an energy source for saprotrophic organisms. The stimulation of saprotrophic fungi and bacteria by root and mycorrhizal © 2015 John Wiley & Sons Ltd, Global Change Biology, 22, 164–179

exudates is referred to as the priming effect and can exert a significant control over organic matter decomposition (Kuzyakov et al., 2000). By supplying less substrate to decomposers, the N-induced reduction in below-ground C allocation by trees can thus be expected to hinder the decomposition of soil organic matter (Janssens et al., 2010). Additionally, Nr deposition can reduce decomposition of organic matter because nitrate and ammonium ions can toxify osmotic potentials in soil solution, therefore directly inhibiting microbial growth (Broadbent, 1965). Nitrogen saturation can also decrease soil pH, causing magnesium and calcium to leach and aluminium to accumulate (Vitousek et al., 1997). Consequently, it has been suggested that microbes may experience magnesium or calcium limitation, but could also suffer from aluminium toxicity (Treseder, 2008). Finally, excess N can inhibit ligninase production, limiting lignin degradation. More labile soil C substrates such as cellulose are often surrounded by a matrix of lignin; thus, impaired lignin degradation can have consequences for the microbial communities access to C (Malherbe & Cloete, 2002).

Secondary soil consumers Soil food webs are based on the energy transfer through two primary consumers, bacteria, and fungi (Wardle, 2002). The relative importance of the two energy channels shifts in response to changes in leaflitter chemistry. The bacterial energy channel consists of bacterial feeding protozoa, rotifers, nematodes, and a few micro-arthropods. The fungal energy channel is composed of fungal consumers such as micro-arthropods, and fungal feeding nematodes. Soil saprophytic bacteria are able to achieve extremely high growth rates and exploit labile C substrates more quickly than saprophytic fungi (Curl & Truelove, 1986). In contrast, fungi are able to degrade more recalcitrant organic matter than bacteria due to their production of specific extracellular enzymes, and their ability to overcome microsite resource limitation via hyphal transport. Fungi and their consumers occupy air-filled pore spaces and water films and possess longer generation times. The rates at which nutrients are processed within each channel differ as well, owing to differences in the recalcitrance of the materials that bacteria and fungi utilize and the different rates of biomass turnover within each channel (i.e. bacterial channels exhibit higher biomass turnover rates; Moore et al., 2003). A majority of evidence to date suggests that N enrichment can cause the relative importance of the bacterial energy channel to increase (Fig. 1, VI), and the fungal energy

170 C . L . M E U N I E R et al. channel to decrease in response to N enrichment (Wardle, 2002; H€ ogberg et al., 2003; Moore et al., 2003), and to overall decrease the total microbial biomass (Treseder, 2008). A significant reduction in microbial biomass in response to increased Nr deposition should induce resource limitation for higher trophic levels, thus decreasing their biomass (Fig. 1, VII) and, further, shift the composition of specialist consumers, such that fungal feeders are negatively affected by a decline in fungal biomass and bacterial feeders are positively affected by increases in bacterial biomass. Collembola, mites, and some specific nematode groups with fungal piercing mouthparts are known to feed primarily on fungi, while protozoans and nematodes with bacterial feeding mouthparts primarily consume bacteria (Bezemer et al., 2010). Consequently, changes in the abundance of bacteria and fungi impact fungivore and bacterivore populations in opposite ways. This was demonstrated in a study by Xu et al. (2009) in a subalpine N-limited forest subjected for 12 years to artificially increased Nr deposition, which caused total collembola densities to decrease. The authors attributed this response to a reduction in fungal biomass. In a similar study performed in a temperate forest, Sun et al. (2013) observed a decline in fungivore nematodes, while bacterivore nematodes biomass increased in response to N enrichment (Fig. 2c). Similar results have been demonstrated in other N fertilization experiments in boreal forest environments (Sohlenius & Wasilewska, 1984). Despite the clear responses of some specialized consumer groups, other soil animals are notoriously flexible in

their diet, and thus difficult to assign to a specific trophic level (Table 1; Scheu, 2002). However, the available evidence suggests that Nr deposition can also affect higher trophic levels within the soil food web.

Nitrogen-deposition effects on lake food webs The consequences of increased Nr deposition for lake food webs have received considerably less attention than for forests (but see Bergstr€ om et al., 2005; Bergstr€ om & Jansson, 2006; Liess et al., 2009). Nitrogen may enter surface waters either by direct atmospheric deposition or through surface run-off in the form of ammonium and nitrate. Ammonium is generally rapidly transformed or assimilated in upper layers of the water column; thus, nitrate dominates the dissolved inorganic N pool in lakes (Hessen, 2013). Nitrate can represent more than 50% of the total atmospheric Nr deposition, and nitrate leaching from land to water increases with increasing atmospheric Nr deposition (Hessen, 2013). Despite potential N retention in lake catchments, dissolved inorganic N concentrations in boreal lakes are highly correlated with Nr-deposition rates (Fig. 3, I; Bergstr€ om & Jansson, 2006), which suggests a strong potential effect on aquatic organisms.

Pelagic food webs Phytoplankton production depends on the interplay between nutrients and light availability (e.g. Philips et al., 1997). In oligotrophic clear-water lakes, where light is not limiting and where atmospheric Nr deposi-

Fig. 3 Simplified conceptual model of Nr-deposition effects on lake food webs. © 2015 John Wiley & Sons Ltd, Global Change Biology, 22, 164–179

N - D E P O S I T I O N I M P A C T S O N N - L I M I T E D E N V I R O N M E N T S 169 differences in foliar N content among vascular plant species, highlighting the importance of shifts in plant species composition in driving changes in quality of litter inputs. Overall, increasing Nr deposition will increase the quality of litter entering the soil food web (i.e. reduce leaf-litter C:N ratios, Berg & Meentemeyer, 2002; Callesen et al., 2007). Soil organisms derive their energy almost exclusively from either living or dead plants. Mycorrhizal fungi derive their C directly from living plants and in return provide plants with soil resources, such as N (H€ ogberg & Read, 2006). In contrast, saprotrophic organisms derive their energy from dead plant material. Thus, the flow of C from living plants and plant detritus to soil organisms controls the activity and biomass of bacteria and fungi, and subsequently soil food web interactions. There is abundant evidence that N enrichment significantly affects the activity of the rhizosphere and of mycorrhizal root symbionts in particular (Treseder, 2004). For example, an N-supply gradient study identified that mycorrhizal fungi declined drastically in response to N enrichment (Fig. 1, V; H€ ogberg et al., 2003). Janssens et al. (2010) recently discussed the range of effects that high Nr deposition has on mycorrhizal fungi. Declines in the production of fruiting bodies by mycorrhizal fungi, the relative proportion of mycorrhizae to total microbial biomass, mycorrhizal diversity, mycorrhizal infection rates and survival, and arbuscular mycorrhizal biomass, hyphal length and storage structures have all been reported in response to N addition. This range of impact reflects lower dependence of trees on mycorrhizal symbionts under high Nr deposition, which triggers the reduction in below-ground C allocation (Janssens et al., 2010). While an enhancement in the quality of litter input (i.e. such as reduced C:N or lignin:N ratios) in response to Nr deposition might be expected to increase microbial consumer growth, biomass, and activity, several meta-analysis studies have shown that the opposite is usually the case (Janssens et al., 2010; Lu et al., 2011). In an analysis of 82 published field studies, Treseder (2004) showed that heterotrophic soil respiration declines by 15% on average under N fertilization. Numerous mechanisms have been provided to explain this reduction in soil microbial biomass, including reduced below-ground C allocation by plants to mycorrhizal fungi, direct inhibition of enzymes involved in lignin degradation, decrease in pH, and decrease in C availability (Treseder, 2008; Janssens et al., 2010). Fine roots and mycorrhizal hyphae release considerable amounts of labile C, which serves as an energy source for saprotrophic organisms. The stimulation of saprotrophic fungi and bacteria by root and mycorrhizal © 2015 John Wiley & Sons Ltd, Global Change Biology, 22, 164–179

exudates is referred to as the priming effect and can exert a significant control over organic matter decomposition (Kuzyakov et al., 2000). By supplying less substrate to decomposers, the N-induced reduction in below-ground C allocation by trees can thus be expected to hinder the decomposition of soil organic matter (Janssens et al., 2010). Additionally, Nr deposition can reduce decomposition of organic matter because nitrate and ammonium ions can toxify osmotic potentials in soil solution, therefore directly inhibiting microbial growth (Broadbent, 1965). Nitrogen saturation can also decrease soil pH, causing magnesium and calcium to leach and aluminium to accumulate (Vitousek et al., 1997). Consequently, it has been suggested that microbes may experience magnesium or calcium limitation, but could also suffer from aluminium toxicity (Treseder, 2008). Finally, excess N can inhibit ligninase production, limiting lignin degradation. More labile soil C substrates such as cellulose are often surrounded by a matrix of lignin; thus, impaired lignin degradation can have consequences for the microbial communities access to C (Malherbe & Cloete, 2002).

Secondary soil consumers Soil food webs are based on the energy transfer through two primary consumers, bacteria, and fungi (Wardle, 2002). The relative importance of the two energy channels shifts in response to changes in leaflitter chemistry. The bacterial energy channel consists of bacterial feeding protozoa, rotifers, nematodes, and a few micro-arthropods. The fungal energy channel is composed of fungal consumers such as micro-arthropods, and fungal feeding nematodes. Soil saprophytic bacteria are able to achieve extremely high growth rates and exploit labile C substrates more quickly than saprophytic fungi (Curl & Truelove, 1986). In contrast, fungi are able to degrade more recalcitrant organic matter than bacteria due to their production of specific extracellular enzymes, and their ability to overcome microsite resource limitation via hyphal transport. Fungi and their consumers occupy air-filled pore spaces and water films and possess longer generation times. The rates at which nutrients are processed within each channel differ as well, owing to differences in the recalcitrance of the materials that bacteria and fungi utilize and the different rates of biomass turnover within each channel (i.e. bacterial channels exhibit higher biomass turnover rates; Moore et al., 2003). A majority of evidence to date suggests that N enrichment can cause the relative importance of the bacterial energy channel to increase (Fig. 1, VI), and the fungal energy

172 C . L . M E U N I E R et al. hypothesis could be tested by measuring the activity of alkaline phosphatase, an enzyme that is over expressed in P-limited animals (Elser et al., 2010), in fish inhabiting lakes over an Nr-deposition gradient (Table 1).

Benthic food webs Whole lake benthic primary production is primarily controlled by the availability of light and not by nutrients (Vadeboncoeur et al., 2008). In most lakes, the main benthic substrate is nutrient-rich sediment on which algae and bacteria grow, creating a microbial mat which limits the release of nutrients from the sediments into the water column (Hansson, 1990). Low nutrient availability and abundant light of arctic clear-water lakes create an ideal environment for benthic algae. In these clear-water lakes, where nutrient availability limits phytoplankton growth, benthic algal production dominates whole lake productivity. In nutrient-poor, boreal humic lakes, where light penetration is low, both benthic production and pelagic production are low (Ask et al., 2009; Karlsson et al., 2009). Under conditions of increased Nr deposition and increased N run-off into lakes, pelagic primary production in these oligotrophic clear-water and humic lakes will quickly switch from N to P limitation without affecting light availability or nutrient limitation of benthic algae (M. Jansson, personnel communication). However, P release rates from sediments will likely increase with increasing water temperatures, generally leading to higher P cycling rates (Chen et al., 2014; North et al., 2014). This may in turn intensify N limitation of benthic algae and even change nutrient cycling of both benthic and pelagic ecosystems. We conclude that algae and bacteria growing on lake sediments will not be affected by increased Nr deposition alone, neither directly via nutrient subsidies, nor indirectly via changes in light attenuation. Many boreal and arctic lakes also contain a stony littoral zone that constitutes a very productive habitat where epilithic periphyton is the base of the benthic food chain. In these shallow, stony habitats, both nutrients and light limit benthic algal production (Hillebrand et al., 2002; Liess & Kahlert, 2007). In addition, this epilithic periphyton is subjected to strong top-down control by grazing invertebrates and fish (Shurin et al., 2002). Besides ingesting periphyton biomass, benthic grazers affect periphyton indirectly by disrupting the periphyton matrix, by changing algal community composition, and by differentially recycling nutrients (Rosemond, 1993; Feminella & Hawkins, 1995; Steinman, 1996; Liess & Hillebrand, 2004; Liess &

Kahlert, 2009). In shallow littoral zones, where light is not limiting, nutrient recycling by grazers is an important source of nutrients for epilithic algae (Liess & Hillebrand, 2004). In particular, under low water column N availability, epilithic algal productivity and nutrient content is dependent on ammonium excreted by grazers (Liess & Hillebrand, 2004; Liess & Haglund, 2007), which is excreted even if N limits grazer growth (Liess et al., 2013). A field survey of lakes along a Ndeposition gradient in Sweden has shown that increasing Nr deposition is correlated to higher N availability for shallow epilithic algae, as indicated by increasing epilithic periphyton N:P ratios (Liess et al., 2009). Increased Nr deposition should therefore lead to a decoupling of the tight dependency of epilithic algae on grazer-mediated N cycling in N-limited systems (Hillebrand et al., 2004), whereas it should intensify the importance of grazer-mediated P cycling. Benthic grazer growth is usually assumed to be P limited (Frost & Elser, 2002; Stelzer & Lamberti, 2002; Fink & Elert, 2006). However, many Swedish boreal studies have indicated N limitation of grazer growth rather than P limitation (Hillebrand et al., 2004; Liess & Hillebrand, 2005; Liess & Kahlert, 2009), with N limitation of grazer growth becoming more severe towards higher latitude low Nr deposition lakes as periphyton N:P ratios decrease (Fig. 3, VI; as indicated by Liess et al., 2009). We therefore assume that increased Nr deposition will switch grazer growth in low Nr-deposition regions from N limitation to P limitation and increase the strength of P limitation of benthic grazer growth in moderate to high Nr-deposition regions (Table 1). Further, increased Nr-deposition rates in regions where grazer growth is N limited may enable Nrich grazers, such as gastropods, to increase in abundance (Liess & Hillebrand, 2005). Similar to zooplankton community shifts discussed above, increasing Nr deposition could lead to benthic grazer community shifts away from N-poor grazers, such as trichopterans and isopods (Liess & Hillebrand, 2005), towards N-rich gastropods. We conclude that increased Nr deposition could shift zoobenthic communities from high P grazers towards high N grazers. This in turn could lead to intensified P limitation of benthic littoral feeding fish (Fig. 3, VII), which are often already P limited in their growth (Vrede et al., 2011).

Nitrogen-deposition effects on forest–lake food web interactions Cross system nutrient subsidies are of great ecological importance in linking ecosystems. These ecosystem external nutrient subsidies are called allochthonous subsidies and can go in both directions, from water to © 2015 John Wiley & Sons Ltd, Global Change Biology, 22, 164–179

N - D E P O S I T I O N I M P A C T S O N N - L I M I T E D E N V I R O N M E N T S 173 land (aquatic subsidies) and from land to water (terrestrial subsidies, Baxter et al., 2005; Richardson et al., 2010). Aquatic subsidies need to overcome gravity and consist of animals such as emergent aquatic insects and fish (Nakano & Murakami, 2001; Baxter et al., 2005; Bartels et al., 2012). Terrestrial subsidies are principally controlled by physical drivers such as gravity (runoff) and wind. Freshwater ecosystems therefore receive terrestrial subsidies in dissolved and particulate forms (Bartels et al., 2012). As the nutritional quality of terrestrial and aquatic subsidies differs widely (i.e. aquatic subsidies are nutrient rich; Cross et al., 2005; whereas terrestrial subsidies are C rich and nutrient poor; Richardson et al., 2010), we expect that changes in subsidy fluxes will have very different effects on aquatic and terrestrial systems.

Impacts of terrestrial subsidies on lake food webs The flow of terrestrial C-rich matter into lakes is likely to increase in the future (Fig. 5, I). This is due to higher terrestrial plant-litter production caused by increasing Nr deposition (Hyv€ onen et al., 2007; Bardgett & Wardle, 2010), coupled with future increased and more intense precipitation, as predicted by climate change scenarios (Christensen et al., 2007). Lake pelagic food webs consist of two energy pathways, the autotrophic, phytoplankton-based energy pathway, and the heterotrophic bacteria-based energy pathway. Because terrestrial organic matter is C rich, increased terrestrial inputs will disproportionately increase bacterial production and therefore enhance the dominance of the heterotrophic energy pathway (Fig. 5,

II). While some argue that little of this bacterial C is transferred to higher trophic levels (Cole et al., 2006), other studies indicate that 50% or more of metazoan and fish biomass can consists of terrestrial C mobilized by bacteria (Karlsson et al., 2012). However, bacteria lack sterols and essential fatty acids, and they are generally considered to be poor-quality food (Fig. 5, III; Brett & M€ uller-Navarra, 1997). Consequently, it has been demonstrated that Daphnia are unable to survive on bacteria alone (Martin-Creuzburg et al., 2011). Higher bacterial biomass instead mainly benefits phagotrophic flagellates and ciliates, which in turn are consumed by mesozooplankton (Lef
ebure et al., 2013). This additional link in the food chain implies that the major energy pathway to zooplankton is via bacteria and microzooplankton instead of via phytoplankton. Consequently, the energy losses from the base to the top of the food web will be higher and will overall decrease trophic transfer efficiency (Jansson et al., 2000). Terrestrial particulate organic C can also subsidize lake food webs and has been shown to contribute between 33 and 73% of the C incorporated into zooplankton and between 20 and 50% of the C incorporated into fish in nonfertilized boreal lakes (Cole et al., 2006). However, terrestrial particulate organic C consumption by zooplankton varies between species and is not necessarily needed for building up large shares of terrigenous C in metazoan biomass (Berggren et al., 2010). Recent studies also pointed out that terrestrial particulate matter (t-PM), which is part of the zooplankton diet, is not a qualitatively sufficient food source for zooplankton (Wenzel et al., 2012), as zooplankton performance decreases with an increasing

Fig. 5 Simplified conceptual model of Nr-deposition effects on forest–lake food web interactions. © 2015 John Wiley & Sons Ltd, Global Change Biology, 22, 164–179

174 C . L . M E U N I E R et al. proportion of diet t-PM (Fig. 5, IV; Taipale et al., 2013). Increased inflow of t-PM to boreal and arctic lakes also leads to increased light attenuation in the water column. According to the light:nutrient hypothesis, low light levels should enhance phytoplankton food quality for zooplankton (Urabe & Sterner, 1996). However, the positive effects of light attenuation on phytoplankton C:nutrient stoichiometry tend to be outweighed by the negative effects of increased light attenuation on overall phytoplankton productivity. Further, high t-PM inputs negatively affect zooplankton performance in boreal clear-water systems by shifting algal composition towards less edible taxa (Fig. 5, V; Faithfull et al., 2011). For benthic systems, the effects of terrestrial C on the productivity and nutrient composition of basal producers are mainly mediated via light attenuation rather than via terrestrial C subsidies (Liess et al., 2015). Coloured terrestrial organic matter limits benthic primary production, which in turn affects production and biomass of higher trophic levels (such as fish), especially in unproductive high latitude lakes (Fig. 5, V; Karlsson et al., 2009).

Impacts of aquatic subsidies on terrestrial food webs Until recently, few studies have focused on the flux of nutrients from water to land. However, emergent aquatic insects and emergent amphibian larvae can transport substantial amounts of nutrients from water to land and be of considerable importance to a wide range of terrestrial predators (for review see Baxter et al., 2005). Almost all amphibians and large numbers of insect taxa, such as caddisflies, stoneflies, mayflies, mosquitoes, and chironomids, have aquatic larval stages, which constitute an important part of the zoobenthos. Zoobenthos exert strong top-down control on benthic primary producers and incorporate a large proportion of benthic nutrients into their biomass. With emergence, the adults transport these nutrients to the terrestrial environment, which can account for up to 140 mg C m 2 yr 1, 35 mg N m 2 yr 1, and 4 mg P m 2 yr 1 (calculated with data from Liess & Hillebrand, 2005; Fukui et al., 2006). Increases in Nr deposition raise benthic algal food quality for zoobenthos (see above Nr-deposition effects on lake food webs). Both insect larvae and amphibian larvae have higher growth and survival rates when feeding on higher quality food (Frost & Elser, 2002; Liess et al., 2013). A long-term monitoring program of a northern US lake found that increased N and P eutrophication lead to a quadrupling of chironomid densities from 1930 to 1961. Chironomids became the second most abundant zoobenthos group in the most polluted lake section (Carr & Hiltunen, 1965; Chadwick &

Huryn, 2005). After 1961, chironomid densities declined again due to improving water quality (Doherty et al., 1999). Observations from this and other studies (e.g. Townsend et al., 2003; Sanford et al., 2005) suggest that chironomid and mosquito larvae will benefit from increasing Nr deposition (Fig. 5, VI). Chironomids and mosquitoes are important prey for fish, birds, and terrestrial invertebrates. Thus, an increase in their biomass may have a positive subsidizing effect on terrestrial ecosystems (Fig. 5, VII; Richardson et al., 2010). However, these increases in Dipteran groups may come at the expense of eutrophication-sensitive insects species, for example caddisflies and mayflies (Fig. 5, VIII; Fig. 4c, d; e.g. Carr & Hiltunen, 1965). Bird species that preferentially feed on these larger insects may be negatively affected by this community shift (Fig. 5, IX). As an example, the Red-backed Shrike Lanius collurio and whinchats Saxicola sp. are two bird species that have considerably declined over the last decades due to the decrease in large insects (Van Nieuwenhuyse et al., 1999; Britschgi et al., 2006). We conclude that Nr deposition may have indirect negative effects on insectivorous birds by favouring aquatic larvae of smaller over larger emergent insects. Adult insects eventually die, and a portion of their population biomass subsidizes the terrestrial food web either as prey for birds or by entering the decomposition food chain. Here, insect carcasses can lead to a substantial increase in terrestrial arthropod biomass (Hoekman et al., 2011). Conversely, experimental reduction in aquatic insect flux depresses the density of spiders, providing direct evidence that the temporal dynamics of aquatic insect flux determines the distributional patterns of riparian spiders (Kato et al., 2003). As insect densities are expected to increase with increasing Nr deposition, we expect more insect carcasses to subsidize the decomposer food web (Fig. 5, X), although these effects are likely minor relative to the direct impact of Nr deposition on terrestrial environments.

Implications Changes in food web structure resulting from Nr deposition will in turn impact the functioning and stability of lake and forest food webs. It is well established that there exists a strong positive connection between the number of species per trophic level and the stability of an ecosystem (Hooper et al., 2005). Moreover, some species play a particular key role in communities, and the loss of such keystone species is known to dramatically affect ecosystem stability (Schulze & Mooney, 1994). Predicted biodiversity loss associated with Nr deposition makes it critical to understand how species © 2015 John Wiley & Sons Ltd, Global Change Biology, 22, 164–179

N - D E P O S I T I O N I M P A C T S O N N - L I M I T E D E N V I R O N M E N T S 175 loss influences ecosystem stability and function (McCann, 2000). Recent studies showed that chronic Nr deposition is a threat to the biodiversity of both plants and herbivores in N-limited forests. A long-term monitoring from 28 forest sites from northern Fennoscandia to southern Italy found that the cover of plant species which prefer nutrient-poor soils decreased proportionally with increasing Nr deposition (Dirnb€ ock et al., 2014). Further, a review of the impacts of Nr deposition on forest plant biodiversity concluded that Nr deposition and the resulting N excess reduces species diversity (Xiankai et al., 2008). In addition, a meta-analysis by Hillebrand et al. (2007) showed that fertilization significantly reduced the number of producer species in terrestrial systems by 18%. Two hypotheses have been proposed to explain changes of above-ground forest biodiversity (Grover, 1997; Xiankai et al., 2008; Elser et al., 2009b). Firstly, due to different N-use efficiencies, slow-growing species with low rate of N turnover are replaced by fast-growing species with high rate of N turnover with increasing Nr deposition, ultimately leading to a biodiversity decrease. Secondly, the N homogeneity hypothesis predicts biodiversity loss in ecosystems experiencing elevated Nr deposition. This hypothesis is based on the decrease in spatial heterogeneity that is typically high in forest soils under N-limited conditions (Gilliam, 2006). Consequently, certain primary consumers such as butterflies and ants decrease in abundance because they depend on nutrient-poor habitats and are sensitive to N-induced € stimulation of plant growth (Ockinger et al., 2006; Wallisdevries & Van Swaay, 2006; Pihlgren et al., 2010). Further, studies showed that the diversity of a large range of soil organisms, from fungi to collembola, is significantly lower in high Nr-deposition than in low Nr-deposition sites (Boxman et al., 1998; Xiankai et al., 2008). It has long been recognized that Nr deposition negatively affects fungal diversity. A study by Arnolds (1988) showed that forests subjected to high Nr deposition experienced a 10% diversity loss over the previous decade. Further, ectomycorrhizal fungal diversity has been shown to decline in response to short-term (60% for the rarest species to 10% for the most abundant species (Suding et al., 2005). Similar results linking N enrichment and biodiversity loss were obtained in aquatic systems (Rabalais, 2002), and both terrestrial and aquatic biodiversity loss are known to affect ecosystem properties such as productivity, decomposition rates, nutrient cycling, and resistance and resilience to perturbations (Loreau et al., 2001). A study by Sutton et al. (2014) showed that several years after the termination of N enrichment, food web recovery was not complete, probably due to a severe loss of diversity (Sutton et al., 2014). To better assess and understand Nr deposition impact on food webs, we suggest that future studies should focus on those species particularly sensitive to N enrichment, as such umbrella species can provide a simple way to monitor ecological communities.

176 C . L . M E U N I E R et al. Conclusions Increased Nr-deposition levels modify community structures and productivity of temperate, boreal, and arctic forest and lake ecosystems. In northern regions, where primary and secondary production is N-limited, forest above-ground and lake pelagic production is enhanced, with higher primary producer growth. Similar mechanisms lead to structural changes in forest and lake food webs. Increasing primary producers’ N content with increasing Nr deposition shifts producer nutrient composition towards higher tissue N:P and lower tissue C:N ratios. Herbivores feeding on these primary producers generally benefit from this change in resource quality, especially consumers with high N content and demand such as herbivorous insects, copepod zooplankton, and benthic gastropods. However, these primary consumer community shifts, from large to small insects, from cladocerans to copepods, and from trichopterans to chironomids and gastropods, may have a negative effect on a number of secondary consumers, such as birds and fish. Further, Nr deposition diminishes below-ground production in forests, due to a range of mechanisms that reduce microbial biomass, and decreases lake benthic productivity by switching herbivore growth from N to P limitation, and by strengthening P limitation of benthic fish. Predicted enhanced Nr deposition over the next 100 years will also have a detrimental impact on the biodiversity of N-limited forests and lakes and therefore impact on food web structure and threaten the stability and functioning of these ecosystems.

Acknowledgements We thank Micael Jonsson, Karolina Stenroth, Anne Deininger,  G€ oran Agren, Kristin Palmqvist, Carolyn Faithfull, and Mats Jansson for helpful input. C.L.M. was financed by the Young Researchers Award from Ume a University to A.L. M.J.G.’s contribution to the review was supported by TC4F and FORMAS. A.L. was financed by the FORMAS funded Lake Ecosystem Response to Environmental Change (LEREC) project.

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