Vrije Universiteit Brussel

Spatial stoichiometry: cross-ecosystem material flows and their impact on recipientecosystems and organismsSitters, Judith; Atkinson, Carla L.; Guelzow, Nils; Kelly, Patrick; Sullivan, Lauren L.

Published in:Oikos

DOI:10.1111/oik.02392

Publication date:2015

Document Version:Accepted author manuscript

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Citation for published version (APA):Sitters, J., Atkinson, C. L., Guelzow, N., Kelly, P., & Sullivan, L. L. (2015). Spatial stoichiometry: cross-ecosystem material flows and their impact on recipient ecosystems and organisms. Oikos, 124(7), 920-930.[124:7]. https://doi.org/10.1111/oik.02392

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Spatial stoichiometry: cross-ecosystem material fl ows and their impact on recipient ecosystems and organisms

Judith Sitters , Carla L. Atkinson , Nils Guelzow , Patrick Kelly and Lauren L. Sullivan

J. Sitters (judith.sitters@vub.ac.be), Dept of Ecology and Environmental Science, Ume å Univ., SE- 901 87 Ume å , Sweden. Present address: Plant Biology and Nature Management, Vrije Univ. Brussel, BE-1050 Brussels, Belgium. – C. L. Atkinson, Dept of Ecology and Evolutionary Biology, Cornell Univ., Ithaca, NY 14853, USA. Present address: Dept of Biological Sciences, Univ. of Alabama, Tuscaloosa, AL 35487, USA. – N. Guelzow, Dept of Geography and Environment, Mount Allison Univ., Sackville, New Brunswick, NB E4L 1E2, Canada. – P. Kelly, Dept of Biological Sciences, Univ. of Notre Dame, Notre Dame, IN 46556, USA. – L. L. Sullivan, Dept of Ecology, Evolution and Organismal Biology, Iowa State Univ., Ames, IA 50011-1020, USA. Present address: Dept of Ecology, Evolution and Behavior, Univ. of Minnesota, St. Paul, MN 55108, USA.

Cross-ecosystem material fl ows, in the form of inorganic nutrients, detritus and organisms, spatially connect ecosystems and impact food web dynamics. To date research on material fl ows has focused on the impact of the quantity of these fl ows and largely ignored their elemental composition, or quality. However, the ratios of elements like carbon, nitrogen and phosphorus can infl uence the impact material fl ows have on food web interactions through stoichiometric mismatches between resources and consumers. Th e type and movement of materials likely vary in their ability to change stoichiometric constraints within the recipient ecosystem and materials may undergo changes in their own stoichiometry during transport. In this literature review we evaluate the importance of cross-ecosystem material fl ows within the framework of ecological stoichiometry. We explore how movement in space and time impacts the stoichiometry of material fl ow, as these transfor-mations are essential to consider when assessing the ability of these fl ows to impact food web productivity and ecosystem functioning. Our review suggests that stoichiometry of cross-ecosystem material fl ows are highly dynamic and undergo changes during transport across the landscape or from human infl uence. Th ese material fl ows can impact recipient organ-isms if they change stoichiometry of the abiotic medium, or provide resources that have a diff erent stoichiometry to in situ resources. Th ey might also alter consumer excretion rates, in turn altering the availability of nutrients in the recipient ecosystem. Th ese alterations in stoichiometric constraints of recipient organisms can have cascading trophic eff ects and shape food web dynamics. We highlight signifi cant gaps in the literature and suggest new avenues for research that explore how cross-ecosystem material fl ows impact recipient ecosystems when considering diff erences in stoichiometric quality, their movement through the landscape and across ecosystem boundaries, and the nutritional constraints of the recipient organisms.

Ecosystems are spatially connected through the movement of materials, specifi cally inorganic nutrients, detritus and organisms, which cross ecosystem boundaries (Polis et al. 1997). Th is cross-ecosystem material fl ow drives food web dynamics in the recipient ecosystem (Polis et al. 1997, 2004, Loreau and Holt 2004). Th e majority of research involving these fl ows has focused on the response of recipient con-sumers and ecosystems as a function of fl ow quantity (Polis et al. 1997, 2004, Nakano and Murakami 2001); however, there is a growing body of literature that suggests the quality of fl ow to play a pivotal, but yet underappreciated role in spatial food web dynamics (Marcarelli et al. 2011, Bartels et al. 2012).

Resource quality can be determined by several factors (i.e. the structure of carbon molecules, specifi c amino acids, fatty acids or lipids; Lau et al. 2008, Brett et al. 2009), but is often expressed by the stoichiometric ratios of the ele-ments carbon (C) to nitrogen (N) and/or phosphorus (P).

Ecological stoichiometry provides an ideal framework for evaluating the impact of cross-ecosystem materials on recipient ecosystems and organisms, as it has been proposed as a unifying theory across multiple levels of biological organization because it provides predicted responses to resource elemental ratios (Sterner and Elser 2002, Allen and Gillooly 2009). Th e basis for ecological stoichiometry rests on the assumption that organism growth and reproduc-tion will be limited by the essential nutrient(s) available in the lowest quantity (Sterner and Elser 2002), and as such, mismatches between nutritional requirements and availabil-ity will regulate organism and food web productivity. Th ere-fore, the stoichiometric ratio of material fl ows may be an important determinant of the degree of recipient ecosystem response through either direct use of the material inputs by consumers, or indirectly, by altering the stoichiometry of resources within the recipient ecosystem (i.e. changing plant tissue stoichiometry; Urabe et al. 2002).

© 2015 Th e Authors. Oikos © 2015 Nordic Society Oikos Subject Editor: Martin Bezemer. Editor-in-Chief: Dustin Marshall. Accepted 30 March 2015

Oikos 000: 001–011, 2015 doi: 10.1111/oik.02392

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Although the stoichiometry of cross-ecosystem fl ows is important for recipient producers and consumers, it is also highly variable and dynamic in both space and time, rang-ing from constant or random inputs to pulsed, predictable events (Sabo and Power 2002, Marczak et al. 2007). Material fl ows cross ecosystem boundaries, which are gener-ally defi ned as locations where the rates or magnitudes of ecological transfers (e.g. energy and nutrient fl ows) change abruptly in relation to those within a patch (Wiens et al. 1985). Because boundaries diff er in their permeability to material fl ows, the movement of materials occur over vari-ous temporal and spatial scales, which may dramatically alter material composition (Wiens et al. 1985, Banks-Leite and Ewers 2009). Th erefore, the movement of material may directly infl uence its stoichiometry, as nutrients are transformed in transit or used and discarded while cross-ing boundaries (Schade et al. 2005). Furthermore, humans impact these cross-ecosystem material fl ows by altering resource availability through changes to global biogeochemi-cal cycles, and by altering movement through changes to habitat connectivity (Vitousek et al. 1997, Fahrig 2003). Hence, the stoichiometry of cross-ecosystem material fl ow likely changes with the mode of transport, the spatial and temporal scales under which it moves, and the boundaries it crosses. Th ese transformations can have signifi cant impacts on the net quality of resources within an ecosystem and may have stoichiometric implications for the response of producers and consumers in the recipient ecosystem.

We argue that the predictive ability of ecological stoichiometry as a concept for unifying resource nutrition and ecosystem functioning should be used for describing the dynamics of cross-ecosystem material fl ow and its impact on recipient ecosystems. However, there has yet to be a syn-thesis identifying how the stoichiometry of cross-ecosystem material fl ow is impacted by its mode of movement and the scale over which it moves, and how it in turn impacts the response of the recipient ecosystem. Th e objectives of this review are to: 1) explore how movement in space and time impacts the stoichiometry of cross-ecosystem material fl ow; 2) investigate how the stoichiometry of material fl ows infl u-ences organism responses in recipient ecosystems by altering stoichiometric constraints; 3) assess how human activities change the stoichiometry of material fl ows and stoichiomet-ric-related responses in recipient ecosystems; and 4) propose future research directions in order to encourage the explicit consideration of space and stoichiometry when studying the movement of material across the landscape.

Impacts of spatial and temporal scales on the stoichiometry of cross-ecosystem material fl ows

Cross-ecosystem material fl ows travel in the form of dissolved nutrients in an abiotic medium, detritus, or organisms, and have various modes and spatial scales of transport (see Table 1 for an overview of the most important cross-ecosystem material fl ows). Material fl ows either move by their own accord, as in organism fl ows, or are transported by abiotic means like wind and water. Th e farther material is moved, the more likely it is to cross one or more ecosys-tem boundaries. Th ese boundaries regulate material fl ows between ecosystems, and therefore may alter fl ow stoichio-

metric characteristics depending on their permeability, and how they aff ect the moving elements (Schade et al. 2001, 2005). For example, elemental nutrients are transported by wind, water or egestion/excretion by mobile organisms across a wide range of spatial scales, from micro-scale movements in the soil to trans-global organism migrations (Table 1, Fig. 1).

Th e spatial distance over which material fl ows are transported can alter the stoichiometry of these fl ows. Th e farther a fl ow moves, the more opportunities it has to inter-act with surrounding abiotic (e.g. geology, hydrology) and biotic features (e.g. organisms) that can alter fl ow stoichiom-etry. Diff erences in upward or downward groundwater move-ment may expose the moving water to either plant litter or deep soils, thus increasing N or P availability, respectively (Sardans and Pe ñ uelas 2014). Stream systems are an excel-lent example of cross-ecosystem material fl ows that change stoichiometry with movement. N tends to be transported over larger distances than P due to variation in the solubil-ity of these two elements (McDowell and Sharpley 2002, Petrone et al. 2007) (Table 1). As water moves over the land-scape, it also picks up nutrients from leaf litter in relative proportion to their solubility, infl uencing the stoichiometry of the water (Schreeg et al. 2013). Th ese nutrients are then cycled through biological components of stream systems. Th is downstream cycling is dependent on which nutrients are limiting within the system (Small et al. 2009), and the variation in macroinvertebrate biomass stoichiometries, stoichiometric requirements, and the fl exibility of their internal stoichiometries (Cross et al. 2003, Small et al. 2009). Hence, as water passes through serially linked ecosystems, substantial shifts in N:P ratios are observed (Schade et al. 2001).

When individual elements are transported in tissue biomass, as is the case in detritus and organisms, the spatial scale of their movement is coupled, but tissue nutri-ent content might change diff erentially, thus altering tissue stoichiometry with distance moved. Th ese changes may be regulated by decreases in lipid tissue from migration (Doucett et al. 1999), leading to net decreases in C and P content with distance moved (Elser et al. 1996). Addition-ally, processes like decomposition can alter detrital stoi-chiometry in space. Microbial activity on organic matter removes labile C fi rst, leaving the more recalcitrant forms of C and reducing the C:N ratio of detritus over time as it fl oats downstream (Manzoni et al. 2008). Th us, cross-ecosystem materials are likely to undergo changes in their stoichi-ometry during transport through either decomposition, consumption or other biogeochemical transformations (Schade et al. 2005), or when processed by diff erent organisms (Levi et al. 2013).

Th e stoichiometry and distance of material moved by mobile organisms, in the form of nutrients (i.e. urine) or detritus (i.e. faeces), is infl uenced by organism traits such as body size, dietary requirements, growth rate and homeostasis (Vanni 2002, Hall 2009). Together they determine the pro-portion of nutrients recycled through consumer excretion, and subsequently the stoichiometry of consumer-mediated material fl ow (Hessen et al. 2004, McIntyre et al. 2008, Allen and Gillooly 2009). Because organisms often track resource availability (Murray 1995, Clay et al. 2014) to

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Table 1. Spatial characteristics and elemental ratios of some important cross-ecosystem material fl ows.

Mode of transport

Movement distance

Type of material Example

Focal element

Measured fl ow stoichiometry

Wind hundreds of km 1 Detritus Pine pollen supplementation into aquatic systems

C, N C:N 17.7 2

Wind hundreds to thousands of km 3-5

Nutrients Atmospheric deposition of eroded dust N 5 , P 5 ,Fe 4,5 None mentioned

Water N: tens of cms-m 6-7 , P: tens of cms 8

Nutrients Soil nutrient diffusion N 6,7 , P 8 None mentioned

Water logs: no movement, sticks: cm-m,

leaves: cm-m, FPOM: m 9

Detritus Terrestrial litter fall into streams C, N C:N 20-750 10-12

Water tens of m 9,13 Detritus Dead aquatic and terrestrial invertebrates in streams

C, N C:N 4.4-5.6 14

Water tens of m 15,16 Organisms Drift of aquatic insects in streams C, N, P C:N 4.8-8.7 N:P 24.5-43.30 7-19

Water N: hundreds of m 20 , P: tens of m 21

Nutrients Overland fl ow of snowmelt, runoff, etc. N 20 , P 21 None mentioned

Water hundreds to thousands of m 22-24

Nutrients Ocean upwelling of nutrients N 22 , P 24 , Fe 23,25

None mentioned

Water thousands of m 16 Organisms Drift of zooplankton in freshwater streams

N, P N:P 13-19 26,27

Water N: hundreds of kms 28 Nutrients Riverine nutrient movement N 28 None mentionedWater hundreds to thousands of

kms 22-24,29 Detritus Movement of marine organic matter on

ocean currentsC, N, P C:N 11-20

N:P 25-139 30 Water hundreds to thousands of

kms 22-24,29 Nutrients Nutrient movement by oceanic currents N 30 , P 30 None mentioned

Organisms tens of m 31-33 Detritus On-shore sea turtle hatchling eggs and carcasses

N, P N:P 9.9 33

Organisms tens to hundreds of m 34-36 Organisms Aquatic insect emergence C, N, P C:N 5.8-6.2 N:P 23.6-16.7 37

Organisms tens to hundreds of m 38 Organisms Diel migration of marine zooplankton N, P N:P 26 26 Organisms tens to hundreds of kms 39 Detritus Spawning salmon carcasses C, N, P C:N 4.4

N:P 5.1 40 Organisms tens to hundreds of kms 39 Nutrients Spawning salmon excretion N 41-44 , P 41-44 None mentionedOrganisms tens to hundreds of kms 39 Organisms Salmon spawning upstream C, N, P C:N 9.0

N:P 5.6 40 Organisms tens to hundreds of kms 45,46 Nutrients Large herbivore excretion N 47-50 None mentionedOrganisms tens to hundreds of kms 45-46 Detritus Large herbivore dung C, N, P C:N 16-100

N:P 3.6-7.9 51 Organisms Foraging: tens of kms 52 ,

migrating: hundreds to thousands of kms 52,53

Detritus Goose egestion during seasonal migration and foraging

C, N, P C:N 8.8 N:P 11.1 54

Organisms hundreds to thousands of kms 55-57

Detritus Seabird egestion N, P N:P 6 58

Results from our literature review on the movement ability and measured stoichiometry of the most important and well-studied cross-ecosystem material fl ows. Material in the form of nutrients, detritus and organisms were considered and are categorized here fi rst by their mode of transport. These material fl ows can be moved through three different modes of transport: wind, water, or organisms. Movement distances represent the range of movement ability found in the literature. 1 Williams 2008, 2 Masclaux et al. 2013, 3 Prospero 1999, 4 Mahowald et al. 2009, 5 Shi et al. 2013, 6 Hajrasuliha et al. 1998, 7 Bai et al. 2012, 8 Chaiwanakupt and Robertson 1976, 9 Webster et al. 1999, 10 Stephens et al. 2013, 11 Cothran et al. 2014, 12 Junker and Cross 2014, 13 Minakawa and Gara 2005, 14 Sullivan et al. 2014, 15 Waters 1972, 16 Brittain and Eikeland 1988, 17 Cross et al. 2005, 18 Cross et al. 2007, 19 Veldboom and Haro 2011, 20 Petrone et al. 2007, 21 McDowell and Sharpley 2002, 22 Wolanski et al. 1988, 23 Coale et al. 1996, 24 Slomp and Van Cappellen 2007, 25 de Baar et al. 1995, 26 Sterner et al. 1992, 27 Elser and Hassett 1994, 28 Royer et al. 2004, 29 Falkowski et al. 1998, 30 Hopkinson et al. 1997, 31 Salmon and Lohmann 1989, 32 Salmon et al. 1995, 33 Bouchard and Bjorndal 2000, 34 M ü ller 1982, 35 Griffi th et al. 1998, 36 Muehlbauer et al. 2014, 37 Veldboom and Haro 2011, 38 Heywood 1996, 39 Kohler et al. 2012, 40 Jonsson and Jonsson 2003, 41 R ü egg et al. 2011, 42 Helfi eld and Naiman 2001, 43 Chaloner et al. 2004, 44 Tiegs et al. 2011, 45 Mob æ k et al. 2012, 46 Geremia et al. 2014, 47 Thomas et al. 1986, 48 Senft et al 1987, 49 Ruess and McNaughton 1988, 50 Van Uytvanck et al. 2010, 51 Sitters et al. 2014, 52 Kitchell et al. 1999, 53 Gauthier et al. 2005, 54 Liu et al. 2013, 55 Weimerskirch et al. 1997, 56 Ballance et al. 2006, 57 Wakefi eld et al. 2009, 58 Maron et al. 2006.

maintain stoichiometric requirements in their diet (e.g. optimal N:P or calcium (Ca):P; Nie et al. 2015), they often feed in one location and excrete/egest nutrients in another, providing ‘ new ’ and stoichiometrically unique nutrient sources (Hilderbrand et al. 1999, Vanni 2002). Th e large-scale migrations of anadromous (e.g. salmon) and iterop-arous fi sh (e.g. longnose suckers) are an important example

of material transport (Janetski et al. 2009, Childress and McIntyre 2015). Th ese fi sh species have diff erent move-ment and spawning strategies, therefore providing diff er-ent types of stoichiometrically distinct material in diff erent habitats along their migratory pathways. For example, eggs tend to have a lower N:P than excreta, which can sup-port P-limited systems where eggs are deposited along the

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Figure 1. A non-exhaustive overview of some important cross-ecosystem material fl ows and their spatial and stoichiometric characteristics (see Table 1 for actual values on distances and measured stoichiometries). Material fl ows travel a wide range of distances, from tens of centimeters to thousands of kilometers. In panel (A) material fl ows are grouped by their mode of transport (wind, water, mobile organisms). Detritus and organism fl ows also vary widely in their measured stoichiometric ratios, both C:N (B) and N:P (C). Nutrient fl ows are not depicted because stoichiometric data is rarely available in the literature.

migratory pathway. Carcasses also provide large infl uxes of N for terrestrial systems that can be N-limiting (Helfi eld and Naiman 2001).

Th e time it takes cross-ecosystem material fl ows to move among ecosystems can also have signifi cant implications for the stoichiometry of that fl ow as it moves through space. Temporal change in stoichiometry occurs largely through the same mechanisms described above; the longer a material fl ow takes to move among ecosystems, the more opportu-nities to interact with the surrounding geology or biology. As microbial processes and leaching of nutrients from sub-strates are subject to specifi c rates, the combination of these rates and the residence time of cross-ecosystem material will regulate the available nutrients in the abiotic medium (Hinkley et al. 2014). Similarly, diff erences in migraion distance for organisms will subject those organisms to dif-ferent rates of fat store usage and nutrient excretion that will change internal stoichiometry through time. As such, the impact of space and time are directly linked, and

play an important role in regulating the stoichiometry of cross-ecosystem material fl ows.

Stoichiometric impacts of cross-ecosystem material fl ows on recipient ecosystems and organisms

Change in stoichiometric constraints of recipient organisms Th e various forms of cross-ecosystem material fl ows enter recipient ecosystems at diff erent trophic levels and can change stoichiometry of the abiotic medium (either soil or water), subsequently impacting primary producers, or pro-vide resources to consumers that potentially have a diff erent stoichiometry compared to in situ resources. For example, inorganic nutrients entering an ecosystem alter the N:P stoichiometry of the abiotic medium. Primary producers assimilate nutrients from this abiotic medium and as they are often limited by N and/or P (Elser et al. 2007, Harpole et al. 2011), the fl ow of inorganic nutrients can either allevi-ate or exacerbate their elemental limitation. Th is in turn will

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Table 2. Summary of some existing studies demonstrating effects of cross-ecosystem material fl ows on recipient ecosystem stoichiometry and stoichiometric constraints of recipient organisms.

Example of material fl ow

Type of material

Change in ecosystem stoichiometry

Change in stoichiometric constraints of recipient organism

Seabirds subsidize terrestrial food webs with marine-derived nutrients from guano 1-4

Nutrients (N and P)

Decrease in soil N:P and C:N

Decrease in tree foliar C:N and C:P; change in plant species composition; increase in arthropod abundance and richness

Freshwater mussel fi ltration-feeding and consequential excretion of nutrients near the benthos 5,6

Nutrients (N and P)

Increase in water N:P near the mussel aggregations

Alleviation of system N-limitation (switches to co-limitation); increase in benthic algal biomass; changes in benthic algal species composition; incorporation of mussel N into food web

Migratory waterfowl subsidize freshwater food webs with terrestrial-derived nutrients from guano 7,8

Nutrients (N and P)

Decrease in reservoir water N:P

Change in algal nutrient limitation status from NP co-limitation to N-limitation and increase in growth

Arboreal ant excreta falls to the forest fl oor 9

Nutrients (N and P)

Increase in soil N:P Increase in decomposition rates below ant colonies; increase in abundance and biomass of detritivores and predators

Zooplankton move nutrients through excreta from the photic to aphotic zone via diel migrations 10

Nutrients (N and P)

Decreases in water N:P Increase in P-limitation of photic zone

Fruit bats transfer terrestrially derived nutrients into mangrove forests 11

Nutrients (N and P),

detritus

Decrease in soil C:N Decrease in foliar C:N and increase in N:P; increase in growth of mangrove trees

Pacifi c salmon subsidize freshwater food webs with marine-derived nutrients from excretion, their eggs, juveniles, and carcasses 12-14

Nutrients (N and P),

detritus

Increase in stream water N:P

Alleviation of nutrient limitation of benthic biofi lm and increase in productivity; increase in primary consumer abundance

Agricultural sediments enter freshwater reservoir 15

Nutrients (N and P),

detritus

Decrease in reservoir seston C:N:P ratios

Decrease in N:P excretion rates of detritivorous fi sh and increase in condition; increase in phyto-plankton growth due to change in excretion rates

Large ungulate carcasses supplement grasslands 16

Detritus Decrease in soil N:P The addition of decreased N:P increases annual forb, perennial forb and C 3 grass abundance and biomass

Terrestrial insect carcasses enter fresh water streams and ponds 17

Detritus Decrease in water N:P Bacteria and phytoplankton increase in biomass; secondary consumers increase in biomass

Pacifi c salmon migrating to freshwater are prey to brown bears 18-20

Organism None mentioned Increase in N:P excretion rates of bear; increase in terrestrial plant growth and decrease in foliar C:N due to change in excretion rates

1 Maron et al. 2006, 2 Jones 2010, 3 Havik et al. 2014, 4 Kolb et al. 2013, 5 Atkinson et al. 2013, 6 Atkinson et al. 2014, 7 Kitchell et al. 1999, 8 Olson et al. 2005, 9 Clay et al. 2013, 10 Hannides et al. 2009, 11 Reef et al. 2014, 12 Chaloner et al. 2004, 13 Tiegs et al. 2011, 14 R ü egg et al. 2011, 15 Pilati et al. 2009, 16 Towne 2000, 17 Nowlin et al. 2007, 18 Hilderbrand 1998, 19 Hilderbrand et al. 1999, 20 Helfi eld and Naiman 2001.

impact the productivity and foliar stoichiometry of primary producers, which can subsequently impact primary con-sumers feeding on them, as several studies have shown (Table 2). Additionally, the direct consumption of materials such as detritus or prey is often a tradeoff between availabil-ity and quality (Marcarelli et al. 2011). Th us, fl uxes of cross-ecosystem material can change the selection of resources by recipient consumers, especially if they are better able to alleviate stoichiometric constraints of consumers than in situ resources. For example, fi sh selected for ‘ high quality ’ terres-trial invertebrates that fell into streams over aquatic macroin-vertebrates that were of lower quality in proportions greater than would be predicted based on food quantity alone and thereby this material fl ow disproportionately aff ected food

web and ecosystem processes (e.g. fi sh production, trophic cascades) (Marcarelli et al. 2011).

However, cross-ecosystem material fl ows of detritus or prey organisms are not always of better quality (i.e. lower C:N stoichiometry) than in situ resources. Detritivores oftentimes show a large stoichiometric imbalance between their own low C:N ratio requirement and the higher C:N ratio in their food (Cross et al. 2003), and hence it is debated as to whether inputs of detritus can adequately support biomass production in organisms that do not have a wide range of stoichiometric tolerance (Brett et al. 2009, Kelly et al. 2014). Many detritivores have, however, adapted to deal with these stoichiometric constraints through selec-tive feeding, excretion of excess C, and higher tissue C:N

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organism-mediated nutrient fl uxes increasing primary and secondary production in aquatic ecosystems, and nutrients translocated from migrating birds or bats stimulating primary and secondary production in terrestrial and aquatic ecosystems by reducing C:nutrient ratios of basal resources (Table 2). However, shifts in resource stoichiometry can also negatively aff ect trophic interactions, for example, through shifts in producer species composition that negatively impact primary consumer biomass (e.g. higher inputs of N and P causing cyanobacteria blooms; Ghadouani et al. 2003), thereby disrupting energy transfer from primary producers to higher-level consumers. Th ese potential indirect eff ects can have far-reaching implications for food web structure (Carpenter et al. 1985). Little research has been done on the stoichiometric aspect of the eff ects of cross-ecosystem mate-rial fl ows on trophic interactions in the recipient ecosystem, although this is a topic worth exploring. For example, micro-cosm experiments have shown that diff erent supply ratios of C:P across connected patches create niches that allow for coexistence (Code ç o and Grover 2001). Additionally, theoretical investigations have illustrated that the ability of a cross-ecosystem fl ow to alter trophic interactions and impact food web dynamics is determined by its quality in terms of C:nutrient ratios and at which trophic level it enters the food web (Huxel et al. 2002, Leroux and Loreau 2008).

Human alteration to stoichiometry of cross-ecosystem material fl ow and responses in recipient ecosystems

Humans modify the environment and are dramatically infl u-encing cross-ecosystem material fl ows and their movement on a global scale (Vitousek et al. 1997, Rockstr ö m et al. 2009) through alterations to biogeochemical cycles and landscape connectivity. Since the mid 1800s, increased fossil fuel combustion and intensifi cation of agriculture have dra-matically altered biogeochemical pools and fl uxes of global C, N and P (Vitousek et al. 1997, Falkowski et al. 2000, Galloway et al. 2004, Bouwman et al. 2009). Agricultural activities promote N and P redistribution across the globe, as large amounts of these nutrients are in surplus on post-harvest croplands (Carpenter et al. 1998). Anthropogenic atmospheric deposition is also changing stoichiometrically, with larger N:P deposited yearly (Pe ñ uelas et al. 2013). Th is increase in the relative supply rate of N compared to P results in the increase of C:P and N:P ratios of soils and waters (Pe ñ uelas et al. 2013), leading to P-limitation in several European and North American lakes (Elser et al. 2009). In contrast, growing use of P as fertilizer can decrease N:P ratios in coastal waters and local aquatic ecosystems by runoff from agricultural land (Singer and Battin 2007, Pilati et al. 2009, Sardans et al. 2012). Th ese alterations in the stoi-chiometry of the recipient ecosystem has drastic implications for recipient organisms; increased environmental N:P ratios generally increase the N:P ratio of aquatic and terrestrial plants aff ecting their metabolism and growth rates, which in turn changes competitiveness between plants and can reduce biodiversity (Pe ñ uelas et al. 2013). Th e increased limitation of P in ecosystems across the globe can have large conse-quences for ecosystem functioning by reducing the capacity of terrestrial ecosystems to fi x C from human-induced CO 2

ratios than non-detritivores (Moe et al. 2005, Boersma and Elser 2006). Despite the physiological challenges associated with detrital resources, the sheer quantity of detrital inputs is important for supporting consumer biomass, leading to increases in macroinvertebrate biodiversity, abundance, organism survival and development, and overall ecosystem function (Wallace et al. 1999, Rowe and Richardson 2001, Rubbo et al. 2006, Nowlin et al. 2007). We argue that one of the main benefi ts from cross-ecosystem detrital fl ows is likely the addition of materials for both food and habitat, while the nutritional value actually comes from pre-treatment of the material by decomposers such as microbes, which break down the recalcitrant carbon to easier assimilated forms (Wallace et al. 1999, France 2011, Davis et al. 2011).

Cross-ecosystem material fl ows in the form of prey organisms have the ability to support secondary consumers (i.e. predators) and are often critical for their growth and reproduction, especially, during periods of low productivity in their native ecosystem (Nakano and Murakami 2001). However, because secondary consumers tend to have simi-lar biomass stoichiometries to their prey – the diff erence in C:N:P between a predator and a prey is signifi cantly less than the diff erence at the detritus – primary consumer level (Cross et al. 2003) – it is unlikely that secondary consumers are stoichiometrically constrained by their in situ resources. Rather, the overall quantity of the material fl ow relative to in situ resources is a more important factor in explaining increases in consumer productivity (Marczak et al. 2007). However, there are indications that nutrient limitation of secondary consumers might be more common than previ-ously assumed as the stoichiometry of certain prey subsidies can be highly variable (Cross et al. 2003) and nutritional limitation has been shown to travel up the food chain (Boersma et al. 2008).

Changes in nutrient excretion rates through consumption of cross-ecosystem material An important indirect stoichiometric-related eff ect on recipient ecosystems is the alteration of consumer N and P excretion rates if inputs of material diff er in stoichiometry from in situ resources, which in turn alter the availability of nutrients in the recipient ecosystem (Schindler and Eby 1997, Balseiro and Albari ñ o 2006). For example, terrestrial material has been observed to increase P excretion by fi sh and aquatic material to increase N excretion by brown bears (Table 2). Because of an organism ’ s impact on ecosystem stoichiometry through nutrient recycling, ecosystem nutrient limitation status may be temporally and spatially dynamic and dependent on the specifi c types of organisms present (Elser et al. 1988, Atkinson et al. 2013). Th ese considerations are necessary when trying to predict how specifi c cross-ecosystem material fl ows may indirectly – through organism-mediated nutrient cycling – alter the stoichiometry of the recipient ecosystems and infl uence trophic interactions.

Stoichiometric changes in trophic interactions Alleviation of stoichiometric constraints of producers and/or consumers through changes in the quality of resources by cross-ecosystem material fl ows can have cascad-ing trophic eff ects and shape food web dynamics (Boersma et al. 2008). Examples include anthropogenic-induced and

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fl ows plays a pivotal role in regulating ecosystem productiv-ity and shaping trophic interactions. We also revealed gaps in the literature and therefore highlight several avenues of future research including: 1) a focus on measuring the inter-active eff ects of material fl ow quantity and quality through controlled experiments; 2) incorporation of the metaeco-system framework to study spatial feedback eff ects of cross-ecosystem fl ows and their stoichiometry; and 3) an increase in quantifi cation of the stoichiometry of material fl ow and how it changes over time and space in order to parameter-ize spatial models of resource supply. Data from these areas will allow us to generate hypotheses about the stoichiometric implications of cross-ecosystem material fl ows.

Separating the quantity and quality of cross-ecosystem material fl ows Variation in both quantity (Wallace et al. 1997, Meyer et al. 2000, Cottingham and Narayan 2013) and quality (Sch ä dler et al. 2005, Kraus and Vonesh 2012) of materials moving into ecosystems have been shown to increase productivity in recipient habitats. However, although studies are rare, the simultaneous consideration of both aspects of material fl ow show that fl ow quality drives the productivity response (Lennon and Pfaff 2005, Marcarelli et al. 2011). We suggest future studies use controlled experimental methods that account for a gradient of both quantity and quality of material fl ow to determine how these factors interact to infl u-ence food web structure. Measuring individual, population or community level trait responses to these two controlled factors would also tease out general patterns of how recipient organisms respond to material fl uxes. Th is data would help to discern general patterns in response to cross-ecosystem material fl ows that cannot be gleaned from changes in com-munity composition alone (McGill et al. 2006, Litchman and Klausmeier 2008).

Use of the metaecosystem framework to study reciprocal fl ows and their stoichiometry Much of the research on cross-ecosystem material fl ows has focused on unidirectional fl ow, even though ecosystems are spatially connected by reciprocal fl uxes aff ecting nutrient and food web dynamics in both donor and recipient eco-systems (Nakano and Murakami 2001, Baxter et al. 2005, Iwata 2007). Th ese reciprocal fl ows often have dissimilar stoichiometries, for example, nutrient-rich material in the form of organisms fl ows from aquatic to terrestrial ecosys-tems, whereas nutrient-poor material in the form of leaf litter dominates the reciprocal fl ow (Bartels et al. 2012). We suggest new research focus on how the stoichiometries of these reciprocal material fl ows impact both donor and recipi-ent ecosystems. Incorporation of the recent metaecosystem theory would be ideal, as it considers the transfer of nutrients, energy and traits across patch boundaries and its eff ects on ecosystem properties such as stability (Gounand et al. 2014) and species coexistence (Gravel et al. 2010). Th is framework has mainly been tested theoretically (but see Legrand et al. 2012) and provides numerous opportunities to improve our understanding of spatial ecosystem dynamics. Th e meta-ecosystem framework currently does not consider the stoichi-ometry of materials as they cross habitat boundaries, which we show here is necessary to understand how reciprocal fl ows

emissions due to a decrease in vegetation productivity and by reducing crop yields in managed ecosystems in developing regions (Pe ñ uelas et al. 2013).

In addition to the direct impact on the stoichiometric landscape through anthropogenic nutrient fl ows at various spatial scales, humans can change the magnitude of ‘ natural ’ cross-ecosystem material fl ows, which in turn have indirect stoichiometric implications. Th ese alterations in fl ow size may also happen at a variety of scales and at diff erent trophic levels. Examples include deforestation that reduces terrestrial leaf litter inputs into streams (Bojsen and Jacobsen 2003), both increases and decreases in migratory bird nesting habi-tats (Fox et al. 2005), and invasive or stocked fi sh species reducing insect emergence to riparian ecosystems (Baxter et al. 2004). Although many human-induced changes to cross-ecosystem material fl ows are due to direct environmen-tal/land-use changes (e.g. deforestation) or human activities (e.g. hunting of migratory snow geese; B é chet et al. 2003), others are indirect consequences of human impacts on the landscape. Together with alterations in fl ow size, the dis-tance material is transported is often dramatically altered by human modifi cations to the landscape. For example, global connectivity through road and shipping networks can increase movement of novel materials (Forman and Alexan-der 1998, Kareiva et al. 2007, Seebens et al. 2013), while land conversion can both minimize material movement through fragmentation (Fahrig 2003, Gilbert-Norton et al. 2010, Hodgson et al. 2011), but also maximize movement when large tracts of new habitat are formed. For example, the conversion of increasing amounts of land from deeply-rooted perennials to shallowly-rooted annuals allows inor-ganic nutrients – in the form of N and P fertilizers used to increase crop yield – to be subsequently transported longer distances through increased soil compaction, soil erosion, and tile drainage (Zhou et al. 2010). Th ese anthropogeni-cally derived nutrients travel through the Mississippi River watershed, deposit in the Gulf of Mexico, and subsidize primary producers creating large hypoxic zones (Dodds 2006). On the other hand, damming of streams for fl ood and erosion can decrease the distance detrital and organ-ism materials can move by stopping the fl ow of water and decreasing connectivity of fi sh habitat (Ligon et al. 1995). Th ese alterations in material movement can have complex interactions with the stoichiometric landscape and resource availability, which can signifi cantly impact the productivity of the recipient food webs.

Future research directions for merging ecological stoichiometry and cross-ecosystem material fl ows in a spatial context

Our ability to synthesize the importance of the stoichiometry of cross-ecosystem material fl ows depends on the type and quality of data available. Th e stoichiometry of material mov-ing across ecosystem boundaries is dynamic, with specifi c ratios of nutrients being altered by movement distance in space and time, and by the infl uence of humans on the land-scape. From the existing literature on the implications of the stoichiometry of material fl ow on producer and consumer productivity, as well as research on resource stoichiometry in general, we hypothesize that the stoichiometry of material

EV-8

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alter ecosystem and community dynamics in heterogeneous environments.

Quantitative spatial models of cross-ecosystem material fl ows We suggest a promising direction of future research on the stoichiometry of cross-ecosystem material fl ows be based on quantitative spatial modelling that considers both local and regional fl uxes to better understand how nutrients, their ratios and their movements provide resources for organ-isms at diff erent scales. Th ese models should include how movement of material across the landscape infl uences fl ow stoichiometry. Th rough this review, we found a paucity of such data. We encourage direct measures of fl ow stoichiom-etry, including: tissue stoichiometry of detritus or organ-isms, and the stoichiometric ratio of nutrients excreted by mobile organisms, at multiple points along a fl ow ’ s pathway, in order to determine quantitatively how energy, nutrients and material move within and across ecosystems. Th ese mea-sures would allow for an empirical assessment of how vary-ing stoichiometries of cross-ecosystem material fl ows may be eliciting ecosystem level responses (e.g. altered net primary productivity, decomposition) in space.

Acknowledgements – Th is paper was a product of the workshop ‘ Woodstoich 2014 ’ . Financial support was provided by the Charles Perkins Center at the Univ. of Sydney and the US National Science Foundation (award DEB-1347502). We thank R. Sterner, D. Raubenheimer, A. Cease, J. Hood and E. Sperfeld for the organi-zation of this excellent workshop. We especially thank J. Hood for his early and continued contributions, and J. Urabe and R. Sterner for their helpful reviews and guidance. Comments from P. Bartels, K. Capps, C. Meunier, M. Cherif, S. Sistla and M. Bezemer greatly improved the manuscript. Th e preparation and creation of this man-uscript was a strong collaborative eff ort and all authors contributed equally. Authors are ordered alphabetically after the fi rst.

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