Herbivore Impacts on Carbon Cycling in Boreal Forests
2020; Elsevier BV; Volume: 35; Issue: 11 Linguagem: Inglês
10.1016/j.tree.2020.07.009
ISSN1872-8383
AutoresShawn Leroux, Yolanda F. Wiersma, Eric Vander Wal,
Tópico(s)Bioenergy crop production and management
ResumoLarge animals can directly and indirectly impact elemental cycling, but these animals are often overlooked as agents in biogeochemical cycling.Human activities have led to the gain or loss of large animals in many biomes, with repercussions on carbon (C) stocks and flows at local and regional extents.The impacts of large animals on C cycling may be particularly important in boreal forests.We argue for a greater focus on large herbivore zoogeochemical impacts in boreal forests to understand spatiotemporal variability in boreal C stocks and flows.The approach we outline can be applied to study animal effects on C cycling in other forest and nonforest ecosystems. Large herbivores can have substantial effects on carbon (C) cycling, yet these animals are often overlooked in C budgets. Zoogeochemical effects may be particularly important in boreal forests, where diverse human activities are facilitating the expansion of large herbivore populations. Here, we argue that considering trophic dynamics is necessary to understand spatiotemporal variability in boreal forest C budgets. We propose a research agenda to scale local studies to landscape extents to measure the zoogeochemical impacts of large herbivores on boreal forest C cycling. Distributed networks of exclosure experiments, empirical studies across gradients in large herbivore abundance, multiscale models using herbivore distribution data, and remote sensing paired with empirical data will provide comprehensive accounting of C source–sink dynamics in boreal forests. Large herbivores can have substantial effects on carbon (C) cycling, yet these animals are often overlooked in C budgets. Zoogeochemical effects may be particularly important in boreal forests, where diverse human activities are facilitating the expansion of large herbivore populations. Here, we argue that considering trophic dynamics is necessary to understand spatiotemporal variability in boreal forest C budgets. We propose a research agenda to scale local studies to landscape extents to measure the zoogeochemical impacts of large herbivores on boreal forest C cycling. Distributed networks of exclosure experiments, empirical studies across gradients in large herbivore abundance, multiscale models using herbivore distribution data, and remote sensing paired with empirical data will provide comprehensive accounting of C source–sink dynamics in boreal forests. Arguments that animals make important contributions to biogeochemical cycles were advanced decades ago [1.Huntley M. et al.Top predators in the Southern ocean: a major leak in the biological carbon pump.Science. 1991; 253: 64-66Crossref PubMed Scopus (82) Google Scholar,2.Jones C.G. Lawton J.H. Linking Species & Ecosystems. Chapman & Hall, 1995Crossref Google Scholar], yet current continental or global C cycle models do not generally include animals (but see [3.Dangal S.R.S. et al.Integrating herbivore population dynamics into a global land biosphere model: plugging animals into the earth system.J. Adv. Model. Earth Syst. 2017; 9: 2920-2945Crossref Scopus (11) Google Scholar]). The omission of animals from such models implies they are not, to a large extent, important components of C cycling [4.Kurz W.A. et al.Mountain pine beetle and forest carbon feedback to climate change.Nature. 2008; 452: 987-990Crossref PubMed Scopus (1253) Google Scholar,5.Schmitz O.J. et al.Animals and the zoogeochemistry of the carbon cycle.Science. 2018; 362eaar3213Crossref PubMed Scopus (63) Google Scholar]. One key reason for this omission may be because most studies of animal effects on elemental cycling are done at local extents (reviewed in [6.Forbes E.S. et al.Synthesizing the effects of large, wild herbivore exclusion on ecosystem function.Funct. Ecol. 2019; 33: 1597-1610Crossref Scopus (24) Google Scholar]). However, the emerging field of zoogeochemistry (see Glossary) points to the potential role of large, mobile animals in C cycling and provides methods to study animal–ecosystem feedbacks at larger extents (reviewed in [5.Schmitz O.J. et al.Animals and the zoogeochemistry of the carbon cycle.Science. 2018; 362eaar3213Crossref PubMed Scopus (63) Google Scholar,7.Schmitz O.J. et al.Animating the carbon cycle.Ecosystems. 2013; 17: 344-359Crossref Scopus (109) Google Scholar]). Here, we argue that large animals, particularly mobile herbivores, are critical for C cycling in forest ecosystems because these animals have the potential to regulate spatial patterns in vegetation, C uptake, and soil C retention [5.Schmitz O.J. et al.Animals and the zoogeochemistry of the carbon cycle.Science. 2018; 362eaar3213Crossref PubMed Scopus (63) Google Scholar]. Forests sequester and cycle large amounts of C. Yet, there are still many uncertainties associated with quantifying C storage in terrestrial systems [8.IPCC IPCC Guidelines for National Greenhouse Gas Inventories. IPCC, 2006Google Scholar,9.Erb K.-H. et al.Unexpectedly large impact of forest management and grazing on global vegetation biomass.Nature. 2018; 553: 73-76Crossref PubMed Scopus (174) Google Scholar]. The boreal forest is the largest forested biome on Earth, encompassing one third of forested regions on the globe and is largely thought to be a C sink [10.Bradshaw C.J.A. et al.Urgent preservation of boreal carbon stocks and biodiversity.Trends Ecol. Evol. 2009; 24: 541-548Abstract Full Text Full Text PDF PubMed Scopus (121) Google Scholar,11.Gauthier S. et al.Boreal forest health and global change.Science. 2015; 349: 819-822Crossref PubMed Scopus (407) Google Scholar]. However, this perspective has mostly ignored the role of animals in C storage and flux. While many populations of large mammals may be declining in some biomes [12.Bar-On Y.M. et al.The biomass distribution on Earth.Proc. Natl. Acad. Sci. U. S. A. 2018; 115: 6506-6511Crossref PubMed Scopus (654) Google Scholar], in boreal forests, many ungulate herbivore populations are increasing [13.Côté S.D. et al.Structuring effects of deer in boreal forest ecosystems.Adv. Ecol. 2014; 2014: 1-10Crossref Google Scholar]. Specifically, humans are creating conditions where large herbivores can thrive, by removing top predators [14.Estes J.A. et al.Trophic downgrading of planet earth.Science. 2011; 333: 301-306Crossref PubMed Scopus (2215) Google Scholar], transforming old-growth forests to earlier successional stages via harvesting of trees [15.Nuttle T. et al.Historic disturbance regimes promote tree diversity only under low browsing regimes in eastern deciduous forest.Ecol. Monogr. 2013; 83: 3-17Crossref Scopus (86) Google Scholar], expanding agricultural fields [16.Hobson K.A. et al.Large-scale conversion of forest to agriculture in the boreal plains of Saskatchewan.Conserv. Biol. 2002; 16: 1530-1541Crossref Scopus (69) Google Scholar], and introducing species into novel environments [17.Gosse J. et al.Degradation of boreal forests by non-native herbivores in Newfoundland’s national parks: recommendations for ecosystem restoration.Nat. Areas J. 2011; 31: 331-339Crossref Scopus (28) Google Scholar]. These human practices, which are increasing during the Anthropocene, will potentially alter the zoogeochemistry of boreal forests. A greater focus on large herbivore zoogeochemical effects in boreal forests is necessary to understand spatiotemporal variability in boreal C stocks and flows. Herbivores can affect aboveground and belowground boreal forest ecosystem C cycling via a suite of direct and indirect mechanisms (Figure 1; [13.Côté S.D. et al.Structuring effects of deer in boreal forest ecosystems.Adv. Ecol. 2014; 2014: 1-10Crossref Google Scholar,18.Bardgett R.D. Wardle D.A. Aboveground-Belowground Linkages: Biotic Interactions, Ecosystem Processes, and Global Change. Oxford University Press, 2010Google Scholar]). Direct effects include selectively foraging on palatable species [17.Gosse J. et al.Degradation of boreal forests by non-native herbivores in Newfoundland’s national parks: recommendations for ecosystem restoration.Nat. Areas J. 2011; 31: 331-339Crossref Scopus (28) Google Scholar], deposition of excreta and urine [19.Pastor J. et al.Moose browsing and soil fertility in the boreal forests of Isle Royale national park.Ecology. 1993; 74: 467-480Crossref Scopus (379) Google Scholar], carcasses [20.Bump J.K. et al.Wolves modulate soil nutrient heterogeneity and foliar nitrogen by configuring the distribution of ungulate carcasses.Ecology. 2009; 90: 3159-3167Crossref PubMed Scopus (83) Google Scholar], and trampling [21.Howison R.A. et al.Biotically driven vegetation mosaics in grazing ecosystems: the battle between bioturbation and biocompaction.Ecol. Monogr. 2017; 87: 363-378Crossref Scopus (17) Google Scholar]. By selectively feeding on high quality (i.e., low C:nitrogen; C:N) plants, large herbivores can change aboveground plant community composition. For example, in boreal forests, ungulates selectively feed on the foliage of deciduous shrubs and trees [e.g., white birch (Betula papyrifera)] in the summer, with a switch to a diet of buds and foliage of coniferous trees [e.g., balsam fir (Abies balsamea)] in the winter [22.Ellis N.M. Leroux S.J. Moose directly slow plant regeneration but have limited indirect effects on soil stoichiometry and litter decomposition rates in disturbed maritime boreal forests.Funct. Ecol. 2017; 31: 790-801Crossref Scopus (19) Google Scholar,23.Bump J.K. et al.Nutrient release from moose bioturbation in aquatic ecosystems.Oikos. 2017; 126: 389-397Crossref Scopus (11) Google Scholar]. Exclosure experiments in North America [19.Pastor J. et al.Moose browsing and soil fertility in the boreal forests of Isle Royale national park.Ecology. 1993; 74: 467-480Crossref Scopus (379) Google Scholar,22.Ellis N.M. Leroux S.J. Moose directly slow plant regeneration but have limited indirect effects on soil stoichiometry and litter decomposition rates in disturbed maritime boreal forests.Funct. Ecol. 2017; 31: 790-801Crossref Scopus (19) Google Scholar,24.McLaren B. et al.Broadleaf competition interferes with balsam fir regeneration following experimental removal of moose.For. Ecol. Manag. 2009; 257: 1395-1404Crossref Scopus (23) Google Scholar] and Fennoscandinavia [25.Danell K. et al.Moose browsing on Scots pine along a gradient of plant productivity.Ecology. 1991; 72: 1624-1633Crossref Scopus (75) Google Scholar,26.Speed J.D.M. et al.General and specific responses of understory vegetation to cervid herbivory across a range of boreal forests.Oikos. 2014; 123: 1270-1280Crossref Scopus (17) Google Scholar] have shown that selective feeding by moose (Alces alces) can lead to a reduced height of palatable species and, in the long-term, a switch in vegetation community structure to a grass (Poa sp.) and unpalatable shrub-dominated understory and an open spruce (Picea sp.) canopy. Likewise, the direct deposition of excreta, urine, and carcasses [19.Pastor J. et al.Moose browsing and soil fertility in the boreal forests of Isle Royale national park.Ecology. 1993; 74: 467-480Crossref Scopus (379) Google Scholar,20.Bump J.K. et al.Wolves modulate soil nutrient heterogeneity and foliar nitrogen by configuring the distribution of ungulate carcasses.Ecology. 2009; 90: 3159-3167Crossref PubMed Scopus (83) Google Scholar], as well as trampling [21.Howison R.A. et al.Biotically driven vegetation mosaics in grazing ecosystems: the battle between bioturbation and biocompaction.Ecol. Monogr. 2017; 87: 363-378Crossref Scopus (17) Google Scholar], by large herbivores can influence local nutrient storage and plant growth, creating spatial heterogeneity in soil fertility at regional extents [27.Pastor J. et al.Spatial patterns in the moose-forest-soil ecosystem of Isle Royale, Michigan, USA.Ecol. Appl. 1998; 8: 411-424Google Scholar,28.Pastor, J. et al. Spatial heterogeneities, carrying capacity, and feedbacks in animal-landscape interactions. J. Mammal. 78, 1040–1052Google Scholar]. These diverse effects of large herbivores can lead to boreal landscapes, where large herbivores decrease regeneration in some local forest patches but increase regeneration in other local forest patches. The spatial heterogeneity in large herbivore effects that may explain the many cascading, indirect effects of herbivores that link C cycling in green and brown food webs is still an active field of research. By selectively feeding on palatable forage species, large herbivores alter the character of litterfall inputs to soils with indirect effects on soil communities ([18.Bardgett R.D. Wardle D.A. Aboveground-Belowground Linkages: Biotic Interactions, Ecosystem Processes, and Global Change. Oxford University Press, 2010Google Scholar,19.Pastor J. et al.Moose browsing and soil fertility in the boreal forests of Isle Royale national park.Ecology. 1993; 74: 467-480Crossref Scopus (379) Google Scholar], but see [22.Ellis N.M. Leroux S.J. Moose directly slow plant regeneration but have limited indirect effects on soil stoichiometry and litter decomposition rates in disturbed maritime boreal forests.Funct. Ecol. 2017; 31: 790-801Crossref Scopus (19) Google Scholar,29.Kolstad A.L. et al.Cervid exclusion alters boreal forest properties with little cascading impacts on soils.Ecosystems. 2018; 21: 1027-1041Crossref Scopus (14) Google Scholar]). Trampling by large herbivores can lead to soil compaction, resulting in higher soil bulk density, less soil oxygen, and subsequent reductions in microbial activity and nitrogen (N) mineralization potential [21.Howison R.A. et al.Biotically driven vegetation mosaics in grazing ecosystems: the battle between bioturbation and biocompaction.Ecol. Monogr. 2017; 87: 363-378Crossref Scopus (17) Google Scholar]. Recent theory also demonstrates that omnivorous microbes in the brown web may be a key determinant of herbivore impacts on terrestrial ecosystem functioning and that aboveground herbivore impacts may be greatest in sites with low fertility (i.e., low soil N), such as the boreal forest [30.Buchkowski R.W. et al.Microbial and animal nutrient limitation change the distribution of nitrogen within coupled green and brown food chains.Ecology. 2019; 100e02674Crossref PubMed Scopus (7) Google Scholar]. In boreal forests, natural disturbances, such as insect outbreaks, can create canopy gaps and beneficial conditions for establishing fast-growing palatable deciduous species and recruitment of coniferous trees to the canopy [15.Nuttle T. et al.Historic disturbance regimes promote tree diversity only under low browsing regimes in eastern deciduous forest.Ecol. Monogr. 2013; 83: 3-17Crossref Scopus (86) Google Scholar]. However, these very conditions also provide ample forage for large herbivores, such as moose. Recent research demonstrated that invertebrate herbivores [e.g., mountain pine beetle (Dendroctonus ponderosae) [4.Kurz W.A. et al.Mountain pine beetle and forest carbon feedback to climate change.Nature. 2008; 452: 987-990Crossref PubMed Scopus (1253) Google Scholar]] and invasive earthworms [31.Cameron E.K. et al.Modelling interacting effects of invasive earthworms and wildfire on forest floor carbon storage in the boreal forest.Soil Biol. Biochem. 2015; 88: 189-196Crossref Scopus (11) Google Scholar] can shift large regions of boreal forest from being a C sink to a C source during outbreak years. We surmise that large herbivore impacts will be greatest when mediated by natural and human disturbances [15.Nuttle T. et al.Historic disturbance regimes promote tree diversity only under low browsing regimes in eastern deciduous forest.Ecol. Monogr. 2013; 83: 3-17Crossref Scopus (86) Google Scholar,32.MacSween J. et al.Cross-ecosystem effects of a large terrestrial herbivore on stream ecosystem functioning.Oikos. 2019; 128: 135-145Crossref Scopus (4) Google Scholar] and that such impacts can lead to failed natural forest regeneration and alternative ecosystem states (Figure 2 and Box 1; [13.Côté S.D. et al.Structuring effects of deer in boreal forest ecosystems.Adv. Ecol. 2014; 2014: 1-10Crossref Google Scholar,17.Gosse J. et al.Degradation of boreal forests by non-native herbivores in Newfoundland’s national parks: recommendations for ecosystem restoration.Nat. Areas J. 2011; 31: 331-339Crossref Scopus (28) Google Scholar,19.Pastor J. et al.Moose browsing and soil fertility in the boreal forests of Isle Royale national park.Ecology. 1993; 74: 467-480Crossref Scopus (379) Google Scholar]).Box 1Dynamics of Spruce Budworm and Moose in Eastern North American Boreal ForestsThrough natural, accidental, and intentional introductions, the mammalian fauna on the island of Newfoundland, Canada has undergone a change over the past ~150 years; shifting from a carnivore-dominated system with 13 species, to a herbivore-dominated one with 26 species [64.Strong J.S. Leroux S.J. Impact of non-native terrestrial mammals on the structure of the terrestrial mammal food web of Newfoundland, Canada.PLoS ONE. 2014; 9e106264Crossref PubMed Scopus (16) Google Scholar]. The most notable is the moose, introduced in 1904 [64.Strong J.S. Leroux S.J. Impact of non-native terrestrial mammals on the structure of the terrestrial mammal food web of Newfoundland, Canada.PLoS ONE. 2014; 9e106264Crossref PubMed Scopus (16) Google Scholar], and the population of which has since reached higher abundances (7 moose/km2) than is typical [65.McLaren B.E. et al.Effects of overabundant moose on the Newfoundland landscape.Alces. 2004; 40: 45-59Google Scholar].Moose populations have fluctuated since then [65.McLaren B.E. et al.Effects of overabundant moose on the Newfoundland landscape.Alces. 2004; 40: 45-59Google Scholar], and an overlay with spruce budworm outbreaks [66.Arsenault, A. et al. Unravelling the past to manage Newfoundland’s forests for the future. Forest. Chr. 92, 487–502Google Scholar] suggests that moose population increases (black arrows in Figure I) can follow 1–4 years after budworm outbreaks (gray arrows in Figure I). A hypothesis underlying this pattern is that budworm create open canopies and a flush of new, palatable growth that promotes moose population growth. Other disturbances (fire or forest harvest), can also create similar flushes of new growth, which can occur at different spatial extents and vary temporally in their frequency, duration, and periodicity. On the island of Newfoundland, natural fires are rare, but the forest harvest industry was very active during the 1980s–1990s and has since declined substantially. Both natural and human-caused disturbances create heterogeneous patterns across the landscape. Consequently, we expect the dynamics of disturbance–moose interactions to vary spatially, with negative impacts on C cycling in some forest patches and positive impacts on C cycling in other forest patches.Moose impacts on plant communities have been understood through long-term exclosures, which have been installed across the island, mostly in areas affected by budworm outbreak [22.Ellis N.M. Leroux S.J. Moose directly slow plant regeneration but have limited indirect effects on soil stoichiometry and litter decomposition rates in disturbed maritime boreal forests.Funct. Ecol. 2017; 31: 790-801Crossref Scopus (19) Google Scholar,24.McLaren B. et al.Broadleaf competition interferes with balsam fir regeneration following experimental removal of moose.For. Ecol. Manag. 2009; 257: 1395-1404Crossref Scopus (23) Google Scholar]. These have revealed that forest responses to moose herbivory are most prominent in areas with intense budworm outbreak and occur over both the short- and long-term. Responses of preferred deciduous species are particularly acute. Red maple (Acer rubrum) densities were three times higher inside exclosures only 3 years after their establishment [17.Gosse J. et al.Degradation of boreal forests by non-native herbivores in Newfoundland’s national parks: recommendations for ecosystem restoration.Nat. Areas J. 2011; 31: 331-339Crossref Scopus (28) Google Scholar], and growth rates of white birch were reduced when exposed to moose browsing. Where high moose densities have overlapped with areas affected by intense budworm outbreak, the effect of moose browse on young saplings has created alternate ecosystems dominated by grasses and woody, unpalatable shrubs, which are structurally different from predisturbance forests [17.Gosse J. et al.Degradation of boreal forests by non-native herbivores in Newfoundland’s national parks: recommendations for ecosystem restoration.Nat. Areas J. 2011; 31: 331-339Crossref Scopus (28) Google Scholar,65.McLaren B.E. et al.Effects of overabundant moose on the Newfoundland landscape.Alces. 2004; 40: 45-59Google Scholar]. Over the long-term, these changes in plant community affect forest carbon stocks bound in trees, litter, and soils. Failure of palatable trees to recruit into the population has impacts for stored C in mature tree tissue. Leaf litter in browsed control plots had lower quantities of C, N, and phosphorus relative to exclosures 16–19 years after exclosure establishment [22.Ellis N.M. Leroux S.J. Moose directly slow plant regeneration but have limited indirect effects on soil stoichiometry and litter decomposition rates in disturbed maritime boreal forests.Funct. Ecol. 2017; 31: 790-801Crossref Scopus (19) Google Scholar]. These findings are similar to systems from other parts of the world that have high herbivore densities [6.Forbes E.S. et al.Synthesizing the effects of large, wild herbivore exclusion on ecosystem function.Funct. Ecol. 2019; 33: 1597-1610Crossref Scopus (24) Google Scholar]. Long-term monitoring for the duration of at least one life cycle of palatable tree species (~30 years for a tree to reach adult in this part of the world) across a landscape is necessary to better understand the impacts of budworm–moose interaction on spatiotemporal patterns in total forest C stocks as well as soil and litter C, N, and phosphorus.Figure IHerbivore Dynamics on the Island of Newfoundland from 1945 to 1991.Show full captionLeft axis: millions of hectares defoliated by spruce budworm (open circles). Right axis: moose population (black squares). Gray arrows indicate the first peaks of spruce budworm outbreak, occurring on ~20–25 year cycles. Black arrows indicate increases in moose population within 5 years of a budworm outbreak. Data from [65.McLaren B.E. et al.Effects of overabundant moose on the Newfoundland landscape.Alces. 2004; 40: 45-59Google Scholar] (right axis) and [66.Arsenault, A. et al. Unravelling the past to manage Newfoundland’s forests for the future. Forest. Chr. 92, 487–502Google Scholar] (left axis).View Large Image Figure ViewerDownload Hi-res image Download (PPT) Through natural, accidental, and intentional introductions, the mammalian fauna on the island of Newfoundland, Canada has undergone a change over the past ~150 years; shifting from a carnivore-dominated system with 13 species, to a herbivore-dominated one with 26 species [64.Strong J.S. Leroux S.J. Impact of non-native terrestrial mammals on the structure of the terrestrial mammal food web of Newfoundland, Canada.PLoS ONE. 2014; 9e106264Crossref PubMed Scopus (16) Google Scholar]. The most notable is the moose, introduced in 1904 [64.Strong J.S. Leroux S.J. Impact of non-native terrestrial mammals on the structure of the terrestrial mammal food web of Newfoundland, Canada.PLoS ONE. 2014; 9e106264Crossref PubMed Scopus (16) Google Scholar], and the population of which has since reached higher abundances (7 moose/km2) than is typical [65.McLaren B.E. et al.Effects of overabundant moose on the Newfoundland landscape.Alces. 2004; 40: 45-59Google Scholar]. Moose populations have fluctuated since then [65.McLaren B.E. et al.Effects of overabundant moose on the Newfoundland landscape.Alces. 2004; 40: 45-59Google Scholar], and an overlay with spruce budworm outbreaks [66.Arsenault, A. et al. Unravelling the past to manage Newfoundland’s forests for the future. Forest. Chr. 92, 487–502Google Scholar] suggests that moose population increases (black arrows in Figure I) can follow 1–4 years after budworm outbreaks (gray arrows in Figure I). A hypothesis underlying this pattern is that budworm create open canopies and a flush of new, palatable growth that promotes moose population growth. Other disturbances (fire or forest harvest), can also create similar flushes of new growth, which can occur at different spatial extents and vary temporally in their frequency, duration, and periodicity. On the island of Newfoundland, natural fires are rare, but the forest harvest industry was very active during the 1980s–1990s and has since declined substantially. Both natural and human-caused disturbances create heterogeneous patterns across the landscape. Consequently, we expect the dynamics of disturbance–moose interactions to vary spatially, with negative impacts on C cycling in some forest patches and positive impacts on C cycling in other forest patches. Moose impacts on plant communities have been understood through long-term exclosures, which have been installed across the island, mostly in areas affected by budworm outbreak [22.Ellis N.M. Leroux S.J. Moose directly slow plant regeneration but have limited indirect effects on soil stoichiometry and litter decomposition rates in disturbed maritime boreal forests.Funct. Ecol. 2017; 31: 790-801Crossref Scopus (19) Google Scholar,24.McLaren B. et al.Broadleaf competition interferes with balsam fir regeneration following experimental removal of moose.For. Ecol. Manag. 2009; 257: 1395-1404Crossref Scopus (23) Google Scholar]. These have revealed that forest responses to moose herbivory are most prominent in areas with intense budworm outbreak and occur over both the short- and long-term. Responses of preferred deciduous species are particularly acute. Red maple (Acer rubrum) densities were three times higher inside exclosures only 3 years after their establishment [17.Gosse J. et al.Degradation of boreal forests by non-native herbivores in Newfoundland’s national parks: recommendations for ecosystem restoration.Nat. Areas J. 2011; 31: 331-339Crossref Scopus (28) Google Scholar], and growth rates of white birch were reduced when exposed to moose browsing. Where high moose densities have overlapped with areas affected by intense budworm outbreak, the effect of moose browse on young saplings has created alternate ecosystems dominated by grasses and woody, unpalatable shrubs, which are structurally different from predisturbance forests [17.Gosse J. et al.Degradation of boreal forests by non-native herbivores in Newfoundland’s national parks: recommendations for ecosystem restoration.Nat. Areas J. 2011; 31: 331-339Crossref Scopus (28) Google Scholar,65.McLaren B.E. et al.Effects of overabundant moose on the Newfoundland landscape.Alces. 2004; 40: 45-59Google Scholar]. Over the long-term, these changes in plant community affect forest carbon stocks bound in trees, litter, and soils. Failure of palatable trees to recruit into the population has impacts for stored C in mature tree tissue. Leaf litter in browsed control plots had lower quantities of C, N, and phosphorus relative to exclosures 16–19 years after exclosure establishment [22.Ellis N.M. Leroux S.J. Moose directly slow plant regeneration but have limited indirect effects on soil stoichiometry and litter decomposition rates in disturbed maritime boreal forests.Funct. Ecol. 2017; 31: 790-801Crossref Scopus (19) Google Scholar]. These findings are similar to systems from other parts of the world that have high herbivore densities [6.Forbes E.S. et al.Synthesizing the effects of large, wild herbivore exclusion on ecosystem function.Funct. Ecol. 2019; 33: 1597-1610Crossref Scopus (24) Google Scholar]. Long-term monitoring for the duration of at least one life cycle of palatable tree species (~30 years for a tree to reach adult in this part of the world) across a landscape is necessary to better understand the impacts of budworm–moose interaction on spatiotemporal patterns in total forest C stocks as well as soil and litter C, N, and phosphorus. While some studies of herbivore effects on terrestrial ecosystems measure components of the C cycle (reviewed in [6.Forbes E.S. et al.Synthesizing the effects of large, wild herbivore exclusion on ecosystem function.Funct. Ecol. 2019; 33: 1597-1610Crossref Scopus (24) Google Scholar,33.Tanentzap A.J. Coomes D.A. Carbon storage in terrestrial ecosystems: do browsing and grazing herbivores matter?.Biol. Rev. 2012; 87: 72-94Crossref PubMed Scopus (122) Google Scholar]), most research on animal effects on ecosystems focuses on other components of coupled green and brown food webs, such as plant richness, composition, and structure. Similarly, large herbivores are highly mobile, spanning multiple components of boreal forest landscapes; yet most research on large herbivore effects on forests comes from experiments reporting patterns measured at local extents [5.Schmitz O.J. et al.Animals and the zoogeochemistry of the carbon cycle.Science. 2018; 362eaar3213Crossref PubMed Scopus (63) Google Scholar,34.Bernes C. et al.Manipulating ungulate herbivory in temperate and boreal forests: effects on vegetation and invertebrates. A systematic review.Environ. Evid. 2018; 713Crossref Scopus (38) Google Scholar]. We argue that a shift to (i) tracking components of C storage and flux; and (ii) scaling up studies to landscape extents has the potential to inform understanding of the role of large herbivores on boreal forest C dynamics. The net exchange of CO2 between the atmosphere and boreal forest [i.e., net ecosystem production (NEP)] is a result of the balance of two processes; net primary production (NPP) and heterotrophic respiration (HR; NE
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