Vrije Universiteit Brussel
Spatial stoichiometry: cross-ecosystem material flows and their impact on recipient
ecosystems and organisms
Sitters, Judith; Atkinson, Carla L.; Guelzow, Nils; Kelly, Patrick; Sullivan, Lauren L.
Published in:
Oikos
Publication date:
2015
Document Version
Peer reviewed version
Link to publication
Citation for published version (APA):
Sitters, J., Atkinson, C. L., Guelzow, N., Kelly, P., & Sullivan, L. L. (2015). Spatial stoichiometry: crossecosystem material flows and their impact on recipient ecosystems and organisms. Oikos, 124(7), 920-930.
[124:7].
General rights
Copyright and moral rights for the publications made accessible in the public portal are retained by the authors and/or other copyright owners
and it is a condition of accessing publications that users recognise and abide by the legal requirements associated with these rights.
• Users may download and print one copy of any publication from the public portal for the purpose of private study or research.
• You may not further distribute the material or use it for any profit-making activity or commercial gain
• You may freely distribute the URL identifying the publication in the public portal
Take down policy
If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately
and investigate your claim.
Download date: 31. jul. 2017
Oikos 000: 001–011, 2015
doi: 10.1111/oik.02392
© 2015 The Authors. Oikos © 2015 Nordic Society Oikos
Subject Editor: Martin Bezemer. Editor-in-Chief: Dustin Marshall. Accepted 30 March 2015
Spatial stoichiometry: cross-ecosystem material flows and their
impact on recipient ecosystems and organisms
Judith Sitters, Carla L. Atkinson, Nils Guelzow, Patrick Kelly and Lauren L. Sullivan
J. Sitters ([email protected]), Dept of Ecology and Environmental Science, Umeå Univ., SE- 901 87 Umeå, 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 flows, in the form of inorganic nutrients, detritus and organisms, spatially connect ecosystems
and impact food web dynamics. To date research on material flows has focused on the impact of the quantity of these flows
and largely ignored their elemental composition, or quality. However, the ratios of elements like carbon, nitrogen and
phosphorus can influence the impact material flows have on food web interactions through stoichiometric mismatches
between resources and consumers. The 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 flows within the framework of ecological
stoichiometry. We explore how movement in space and time impacts the stoichiometry of material flow, as these transformations are essential to consider when assessing the ability of these flows to impact food web productivity and ecosystem
functioning. Our review suggests that stoichiometry of cross-ecosystem material flows are highly dynamic and undergo
changes during transport across the landscape or from human influence. These material flows can impact recipient organisms if they change stoichiometry of the abiotic medium, or provide resources that have a different stoichiometry to in
situ resources. They might also alter consumer excretion rates, in turn altering the availability of nutrients in the recipient
ecosystem. These alterations in stoichiometric constraints of recipient organisms can have cascading trophic effects and
shape food web dynamics. We highlight significant gaps in the literature and suggest new avenues for research that explore
how cross-ecosystem material flows impact recipient ecosystems when considering differences 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, specifically inorganic nutrients, detritus and
organisms, which cross ecosystem boundaries (Polis et al.
1997). This cross-ecosystem material flow drives food web
dynamics in the recipient ecosystem (Polis et al. 1997, 2004,
Loreau and Holt 2004). The majority of research involving
these flows has focused on the response of recipient consumers and ecosystems as a function of flow quantity (Polis
et al. 1997, 2004, Nakano and Murakami 2001); however,
there is a growing body of literature that suggests the quality
of flow 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, specific amino acids,
fatty acids or lipids; Lau et al. 2008, Brett et al. 2009), but
is often expressed by the stoichiometric ratios of the elements 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). The basis for ecological stoichiometry
rests on the assumption that organism growth and reproduction 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 availability will regulate organism and food web productivity. Therefore, the stoichiometric ratio of material flows 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).
EV-1
Although the stoichiometry of cross-ecosystem flows is
important for recipient producers and consumers, it is also
highly variable and dynamic in both space and time, ranging from constant or random inputs to pulsed, predictable
events (Sabo and Power 2002, Marczak et al. 2007).
Material flows cross ecosystem boundaries, which are generally defined as locations where the rates or magnitudes of
ecological transfers (e.g. energy and nutrient flows) change
abruptly in relation to those within a patch (Wiens et al.
1985). Because boundaries differ in their permeability to
material flows, the movement of materials occur over various temporal and spatial scales, which may dramatically
alter material composition (Wiens et al. 1985, Banks-Leite
and Ewers 2009). Therefore, the movement of material
may directly influence its stoichiometry, as nutrients are
transformed in transit or used and discarded while crossing boundaries (Schade et al. 2005). Furthermore, humans
impact these cross-ecosystem material flows by altering
resource availability through changes to global biogeochemical cycles, and by altering movement through changes to
habitat connectivity (Vitousek et al. 1997, Fahrig 2003).
Hence, the stoichiometry of cross-ecosystem material flow
likely changes with the mode of transport, the spatial and
temporal scales under which it moves, and the boundaries it
crosses. These transformations can have significant 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 flow and its impact
on recipient ecosystems. However, there has yet to be a synthesis identifying how the stoichiometry of cross-ecosystem
material flow 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. The objectives of this
review are to: 1) explore how movement in space and time
impacts the stoichiometry of cross-ecosystem material flow;
2) investigate how the stoichiometry of material flows influences organism responses in recipient ecosystems by altering
stoichiometric constraints; 3) assess how human activities
change the stoichiometry of material flows and stoichiometric-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 flows
Cross-ecosystem material flows 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 flows). Material flows either move
by their own accord, as in organism flows, or are transported
by abiotic means like wind and water. The farther material
is moved, the more likely it is to cross one or more ecosystem boundaries. These boundaries regulate material flows
between ecosystems, and therefore may alter flow stoichioEV-2
metric characteristics depending on their permeability, and
how they affect 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).
The spatial distance over which material flows are
transported can alter the stoichiometry of these flows. The
farther a flow moves, the more opportunities it has to interact with surrounding abiotic (e.g. geology, hydrology) and
biotic features (e.g. organisms) that can alter flow stoichiometry. Differences in upward or downward groundwater movement may expose the moving water to either plant litter or
deep soils, thus increasing N or P availability, respectively
(Sardans and Peñuelas 2014). Stream systems are an excellent example of cross-ecosystem material flows that change
stoichiometry with movement. N tends to be transported
over larger distances than P due to variation in the solubility of these two elements (McDowell and Sharpley 2002,
Petrone et al. 2007) (Table 1). As water moves over the landscape, it also picks up nutrients from leaf litter in relative
proportion to their solubility, influencing the stoichiometry
of the water (Schreeg et al. 2013). These nutrients are then
cycled through biological components of stream systems.
This 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 flexibility 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 nutrient content might change differentially, thus altering tissue
stoichiometry with distance moved. These 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). Additionally, processes like decomposition can alter detrital stoichiometry in space. Microbial activity on organic matter
removes labile C first, leaving the more recalcitrant forms of
C and reducing the C:N ratio of detritus over time as it floats
downstream (Manzoni et al. 2008). Thus, cross-ecosystem
materials are likely to undergo changes in their stoichiometry during transport through either decomposition,
consumption or other biogeochemical transformations
(Schade et al. 2005), or when processed by different
organisms (Levi et al. 2013).
The stoichiometry and distance of material moved by
mobile organisms, in the form of nutrients (i.e. urine) or
detritus (i.e. faeces), is influenced by organism traits such as
body size, dietary requirements, growth rate and homeostasis
(Vanni 2002, Hall 2009). Together they determine the proportion of nutrients recycled through consumer excretion,
and subsequently the stoichiometry of consumer-mediated
material flow (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
Table 1. Spatial characteristics and elemental ratios of some important cross-ecosystem material flows.
Mode of
transport
Movement
distance
Type of
material
Wind
hundreds of km1
Detritus
Wind
Water
hundreds to thousands of
km3-5
N: tens of cms-m6-7, P: tens
of cms8
logs: no movement, sticks:
cm-m,
leaves: cm-m,
FPOM: m9
tens of m9,13
Water
tens of m15,16
Water
N: hundreds of m20, P: tens
of m21
hundreds to thousands of
m22-24
thousands of m16
Water
Water
Water
Water
Water
Water
Focal
element
Measured flow
stoichiometry
C, N
C:N 17.72
Nutrients
Pine pollen supplementation into aquatic
systems
Atmospheric deposition of eroded dust
N5, P5,Fe4,5
None mentioned
Nutrients
Soil nutrient diffusion
N6,7, P8
None mentioned
Detritus
Terrestrial litter fall into streams
C, N
C:N 20-75010-12
Detritus
C, N
C:N 4.4-5.614
Organisms
Dead aquatic and terrestrial invertebrates
in streams
Drift of aquatic insects in streams
C, N, P
Nutrients
Overland flow of snowmelt, runoff, etc.
N20, P21
C:N 4.8-8.7
N:P 24.5-43.307-19
None mentioned
Nutrients
Ocean upwelling of nutrients
Organisms
Drift of zooplankton in freshwater
streams
Riverine nutrient movement
Movement of marine organic matter on
ocean currents
Nutrient movement by oceanic currents
N22, P24,
Fe23,25
N, P
Nutrients
Detritus
Organisms
N: hundreds of kms28
hundreds to thousands of
kms22-24,29
hundreds to thousands of
kms22-24,29
tens of m31-33
Organisms
tens to hundreds of m34-36
Organisms
Organisms
Water
Nutrients
N28
C, N, P
None mentioned
N:P 13-1926,27
N30, P30
None mentioned
C:N 11-20
N:P 25-13930
None mentioned
N, P
N:P 9.933
Organisms
On-shore sea turtle hatchling eggs and
carcasses
Aquatic insect emergence
C, N, P
tens to hundreds of m38
tens to hundreds of kms39
Organisms
Detritus
Diel migration of marine zooplankton
Spawning salmon carcasses
N, P
C, N, P
Organisms
Organisms
tens to hundreds of kms39
tens to hundreds of kms39
Nutrients
Organisms
Spawning salmon excretion
Salmon spawning upstream
N41-44, P41-44
C, N, P
Organisms
Organisms
tens to hundreds of kms45,46
tens to hundreds of kms45-46
Nutrients
Detritus
Large herbivore excretion
Large herbivore dung
N47-50
C, N, P
Organisms
Foraging: tens of kms52,
migrating: hundreds to
thousands of kms52,53
hundreds to thousands of
kms55-57
Detritus
Goose egestion during seasonal migration
and foraging
C, N, P
C:N 5.8-6.2
N:P 23.6-16.737
N:P 2626
C:N 4.4
N:P 5.140
None mentioned
C:N 9.0
N:P 5.640
None mentioned
C:N 16-100
N:P 3.6-7.951
C:N 8.8
N:P 11.154
Detritus
Seabird egestion
N, P
Organisms
Detritus
Example
N:P 658
Results from our literature review on the movement ability and measured stoichiometry of the most important and well-studied crossecosystem material flows. Material in the form of nutrients, detritus and organisms were considered and are categorized here first by their
mode of transport. These material flows 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.
1Williams 2008, 2Masclaux et al. 2013, 3Prospero 1999, 4Mahowald et al. 2009, 5Shi et al. 2013, 6Hajrasuliha et al. 1998, 7Bai et al.
2012, 8Chaiwanakupt and Robertson 1976, 9Webster et al. 1999, 10Stephens et al. 2013, 11Cothran et al. 2014, 12Junker and Cross 2014,
13Minakawa and Gara 2005, 14Sullivan et al. 2014, 15Waters 1972, 16Brittain and Eikeland 1988, 17Cross et al. 2005, 18Cross et al. 2007,
19Veldboom and Haro 2011, 20Petrone et al. 2007, 21McDowell and Sharpley 2002, 22Wolanski et al. 1988, 23Coale et al. 1996, 24Slomp and
Van Cappellen 2007, 25de Baar et al. 1995, 26Sterner et al. 1992, 27Elser and Hassett 1994, 28Royer et al. 2004, 29Falkowski et al. 1998,
30Hopkinson et al. 1997, 31Salmon and Lohmann 1989, 32Salmon et al. 1995, 33Bouchard and Bjorndal 2000, 34Müller 1982, 35Griffith et al.
1998, 36Muehlbauer et al. 2014, 37Veldboom and Haro 2011, 38Heywood 1996, 39Kohler et al. 2012, 40Jonsson and Jonsson 2003, 41Rüegg
et al. 2011, 42Helfield and Naiman 2001, 43Chaloner et al. 2004, 44Tiegs et al. 2011, 45 Mobæk et al. 2012, 46Geremia et al. 2014, 47Thomas
et al. 1986, 48Senft et al 1987, 49Ruess and McNaughton 1988, 50Van Uytvanck et al. 2010, 51Sitters et al. 2014, 52Kitchell et al. 1999,
53Gauthier et al. 2005, 54Liu et al. 2013, 55Weimerskirch et al. 1997, 56Ballance et al. 2006, 57Wakefield et al. 2009, 58Maron 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). The largescale migrations of anadromous (e.g. salmon) and iteroparous fish (e.g. longnose suckers) are an important example
of material transport (Janetski et al. 2009, Childress and
McIntyre 2015). These fish species have different movement and spawning strategies, therefore providing different types of stoichiometrically distinct material in different
habitats along their migratory pathways. For example, eggs
tend to have a lower N:P than excreta, which can support P-limited systems where eggs are deposited along the
EV-3
Figure 1. A non-exhaustive overview of some important cross-ecosystem material flows and their spatial and stoichiometric characteristics
(see Table 1 for actual values on distances and measured stoichiometries). Material flows travel a wide range of distances, from tens of
centimeters to thousands of kilometers. In panel (A) material flows are grouped by their mode of transport (wind, water, mobile organisms).
Detritus and organism flows also vary widely in their measured stoichiometric ratios, both C:N (B) and N:P (C). Nutrient flows are not
depicted because stoichiometric data is rarely available in the literature.
migratory pathway. Carcasses also provide large influxes of
N for terrestrial systems that can be N-limiting (Helfield and
Naiman 2001).
The time it takes cross-ecosystem material flows to move
among ecosystems can also have significant implications for
the stoichiometry of that flow as it moves through space.
Temporal change in stoichiometry occurs largely through
the same mechanisms described above; the longer a material
flow takes to move among ecosystems, the more opportunities to interact with the surrounding geology or biology.
As microbial processes and leaching of nutrients from substrates are subject to specific 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, differences in migraion
distance for organisms will subject those organisms to different 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
EV-4
play an important role in regulating the stoichiometry of
cross-ecosystem material flows.
Stoichiometric impacts of cross-ecosystem material
flows on recipient ecosystems and organisms
Change in stoichiometric constraints of recipient organisms
The various forms of cross-ecosystem material flows enter
recipient ecosystems at different trophic levels and can
change stoichiometry of the abiotic medium (either soil or
water), subsequently impacting primary producers, or provide resources to consumers that potentially have a different
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 flow of inorganic nutrients can either alleviate or exacerbate their elemental limitation. This in turn will
impact the productivity and foliar stoichiometry of primary
producers, which can subsequently impact primary consumers 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 availability and quality (Marcarelli et al. 2011). Thus, fluxes of crossecosystem 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, fish selected for ‘high quality’ terrestrial invertebrates that fell into streams over aquatic macroinvertebrates that were of lower quality in proportions greater
than would be predicted based on food quantity alone and
thereby this material flow disproportionately affected food
web and ecosystem processes (e.g. fish production, trophic
cascades) (Marcarelli et al. 2011).
However, cross-ecosystem material flows 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 selective feeding, excretion of excess C, and higher tissue C:N
Table 2. Summary of some existing studies demonstrating effects of cross-ecosystem material flows on recipient ecosystem stoichiometry and
stoichiometric constraints of recipient organisms.
Example of
material flow
Type of
material
Change in ecosystem
stoichiometry
Change in stoichiometric constraints
of recipient organism
Seabirds subsidize terrestrial food webs
with marine-derived nutrients from
guano1-4
Nutrients
(N and P)
Decrease in soil N:P and
C:N
Freshwater mussel filtration-feeding
and consequential excretion of
nutrients near the benthos5,6
Nutrients
(N and P)
Increase in water N:P
near the mussel
aggregations
Migratory waterfowl subsidize
freshwater food webs with
terrestrial-derived nutrients from
guano7,8
Arboreal ant excreta falls to the forest
floor9
Nutrients
(N and P)
Decrease in reservoir
water N:P
Nutrients
(N and P)
Increase in soil N:P
Nutrients
(N and P)
Decreases in water N:P
Decrease in tree foliar C:N and
C:P; change in plant species
composition; increase in arthropod
abundance and richness
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
Change in algal nutrient limitation
status from NP co-limitation to
N-limitation and increase in
growth
Increase in decomposition rates
below ant colonies; increase in
abundance and biomass of
detritivores and predators
Increase in P-limitation of photic
zone
Nutrients
(N and P),
detritus
Nutrients
(N and P),
detritus
Decrease in soil C:N
Nutrients
(N and P),
detritus
Decrease in reservoir
seston C:N:P ratios
Large ungulate carcasses supplement
grasslands16
Detritus
Decrease in soil N:P
Terrestrial insect carcasses enter fresh
water streams and ponds17
Detritus
Decrease in water N:P
Pacific salmon migrating to freshwater
are prey to brown bears18-20
Organism
None mentioned
Zooplankton move nutrients through
excreta from the photic to aphotic
zone via diel migrations10
Fruit bats transfer terrestrially derived
nutrients into mangrove forests11
Pacific salmon subsidize freshwater
food webs with marine-derived
nutrients from excretion, their eggs,
juveniles, and carcasses12-14
Agricultural sediments enter freshwater
reservoir15
Increase in stream water
N:P
Decrease in foliar C:N and increase
in N:P; increase in growth of
mangrove trees
Alleviation of nutrient limitation of
benthic biofilm and increase in
productivity; increase in primary
consumer abundance
Decrease in N:P excretion rates
of detritivorous fish and increase
in condition; increase in phytoplankton growth due to change
in excretion rates
The addition of decreased N:P
increases annual forb, perennial
forb and C3 grass abundance and
biomass
Bacteria and phytoplankton increase
in biomass; secondary consumers
increase in biomass
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
1Maron
et al. 2006, 2Jones 2010, 3Havik et al. 2014, 4Kolb et al. 2013, 5Atkinson et al. 2013, 6Atkinson et al. 2014, 7Kitchell et al. 1999,
et al. 2005, 9Clay et al. 2013, 10Hannides et al. 2009, 11Reef et al. 2014, 12Chaloner et al. 2004, 13Tiegs et al. 2011, 14Rüegg et al.
2011, 15Pilati et al. 2009, 16Towne 2000, 17Nowlin et al. 2007, 18Hilderbrand 1998, 19Hilderbrand et al. 1999, 20Helfield and Naiman
2001.
8Olson
EV-5
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 benefits from cross-ecosystem detrital flows 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 flows 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 similar biomass stoichiometries to their prey – the difference in
C:N:P between a predator and a prey is significantly less
than the difference 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 flow 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 previously 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 effect on
recipient ecosystems is the alteration of consumer N and P
excretion rates if inputs of material differ in stoichiometry
from in situ resources, which in turn alter the availability
of nutrients in the recipient ecosystem (Schindler and Eby
1997, Balseiro and Albariño 2006). For example, terrestrial
material has been observed to increase P excretion by fish
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 specific types of organisms present
(Elser et al. 1988, Atkinson et al. 2013). These considerations
are necessary when trying to predict how specific crossecosystem material flows may indirectly – through organismmediated nutrient cycling – alter the stoichiometry of the
recipient ecosystems and influence 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 flows can have cascading trophic effects and shape food web dynamics (Boersma
et al. 2008). Examples include anthropogenic-induced and
EV-6
organism-mediated nutrient fluxes 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 affect 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. These potential indirect effects
can have far-reaching implications for food web structure
(Carpenter et al. 1985). Little research has been done on the
stoichiometric aspect of the effects of cross-ecosystem material flows on trophic interactions in the recipient ecosystem,
although this is a topic worth exploring. For example, microcosm experiments have shown that different supply ratios
of C:P across connected patches create niches that allow
for coexistence (Codeço and Grover 2001). Additionally,
theoretical investigations have illustrated that the ability of a
cross-ecosystem flow 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 flow and responses in
recipient ecosystems
Humans modify the environment and are dramatically influencing cross-ecosystem material flows and their movement
on a global scale (Vitousek et al. 1997, Rockström et al.
2009) through alterations to biogeochemical cycles and
landscape connectivity. Since the mid 1800s, increased fossil
fuel combustion and intensification of agriculture have dramatically altered biogeochemical pools and fluxes 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 postharvest croplands (Carpenter et al. 1998). Anthropogenic
atmospheric deposition is also changing stoichiometrically,
with larger N:P deposited yearly (Peñuelas et al. 2013).
This 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 (Peñuelas 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). These alterations in the stoichiometry 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 affecting their metabolism and growth rates, which in
turn changes competitiveness between plants and can reduce
biodiversity (Peñuelas et al. 2013). The increased limitation
of P in ecosystems across the globe can have large consequences for ecosystem functioning by reducing the capacity
of terrestrial ecosystems to fix C from human-induced CO2
emissions due to a decrease in vegetation productivity and by
reducing crop yields in managed ecosystems in developing
regions (Peñuelas et al. 2013).
In addition to the direct impact on the stoichiometric
landscape through anthropogenic nutrient flows at various
spatial scales, humans can change the magnitude of ‘natural’
cross-ecosystem material flows, which in turn have indirect
stoichiometric implications. These alterations in flow size
may also happen at a variety of scales and at different 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 habitats (Fox et al. 2005), and invasive or stocked fish species
reducing insect emergence to riparian ecosystems (Baxter
et al. 2004). Although many human-induced changes to
cross-ecosystem material flows are due to direct environmental/land-use changes (e.g. deforestation) or human activities
(e.g. hunting of migratory snow geese; Béchet et al. 2003),
others are indirect consequences of human impacts on the
landscape. Together with alterations in flow size, the distance material is transported is often dramatically altered
by human modifications to the landscape. For example,
global connectivity through road and shipping networks can
increase movement of novel materials (Forman and Alexander 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 deeplyrooted perennials to shallowly-rooted annuals allows inorganic 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). These anthropogenically 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 flood
and erosion can decrease the distance detrital and organism materials can move by stopping the flow of water and
decreasing connectivity of fish habitat (Ligon et al. 1995).
These alterations in material movement can have complex
interactions with the stoichiometric landscape and resource
availability, which can significantly impact the productivity
of the recipient food webs.
Future research directions for merging ecological
stoichiometry and cross-ecosystem material flows in
a spatial context
Our ability to synthesize the importance of the stoichiometry
of cross-ecosystem material flows depends on the type and
quality of data available. The stoichiometry of material moving across ecosystem boundaries is dynamic, with specific
ratios of nutrients being altered by movement distance in
space and time, and by the influence of humans on the landscape. From the existing literature on the implications of the
stoichiometry of material flow on producer and consumer
productivity, as well as research on resource stoichiometry
in general, we hypothesize that the stoichiometry of material
flows plays a pivotal role in regulating ecosystem productivity 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 interactive effects of material flow quantity and quality through
controlled experiments; 2) incorporation of the metaecosystem framework to study spatial feedback effects of crossecosystem flows and their stoichiometry; and 3) an increase
in quantification of the stoichiometry of material flow and
how it changes over time and space in order to parameterize spatial models of resource supply. Data from these areas
will allow us to generate hypotheses about the stoichiometric
implications of cross-ecosystem material flows.
Separating the quantity and quality of cross-ecosystem
material flows
Variation in both quantity (Wallace et al. 1997, Meyer et al.
2000, Cottingham and Narayan 2013) and quality (Schädler
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
flow show that flow 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 flow to determine how these factors interact to influence 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 fluxes. This data would help
to discern general patterns in response to cross-ecosystem
material flows that cannot be gleaned from changes in community composition alone (McGill et al. 2006, Litchman
and Klausmeier 2008).
Use of the metaecosystem framework to study reciprocal
flows and their stoichiometry
Much of the research on cross-ecosystem material flows has
focused on unidirectional flow, even though ecosystems are
spatially connected by reciprocal fluxes affecting nutrient
and food web dynamics in both donor and recipient ecosystems (Nakano and Murakami 2001, Baxter et al. 2005,
Iwata 2007). These reciprocal flows often have dissimilar
stoichiometries, for example, nutrient-rich material in the
form of organisms flows from aquatic to terrestrial ecosystems, whereas nutrient-poor material in the form of leaf
litter dominates the reciprocal flow (Bartels et al. 2012).
We suggest new research focus on how the stoichiometries of
these reciprocal material flows impact both donor and recipient 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 effects on
ecosystem properties such as stability (Gounand et al. 2014)
and species coexistence (Gravel et al. 2010). This framework
has mainly been tested theoretically (but see Legrand et al.
2012) and provides numerous opportunities to improve our
understanding of spatial ecosystem dynamics. The metaecosystem framework currently does not consider the stoichiometry of materials as they cross habitat boundaries, which
we show here is necessary to understand how reciprocal flows
EV-7
alter ecosystem and community dynamics in heterogeneous
environments.
Quantitative spatial models of cross-ecosystem material
flows
We suggest a promising direction of future research on the
stoichiometry of cross-ecosystem material flows be based
on quantitative spatial modelling that considers both local
and regional fluxes to better understand how nutrients, their
ratios and their movements provide resources for organisms at different scales. These models should include how
movement of material across the landscape influences flow
stoichiometry. Through this review, we found a paucity of
such data. We encourage direct measures of flow stoichiometry, including: tissue stoichiometry of detritus or organisms, and the stoichiometric ratio of nutrients excreted by
mobile organisms, at multiple points along a flow’s pathway,
in order to determine quantitatively how energy, nutrients
and material move within and across ecosystems. These measures would allow for an empirical assessment of how varying stoichiometries of cross-ecosystem material flows may be
eliciting ecosystem level responses (e.g. altered net primary
productivity, decomposition) in space.
Acknowledgements – This 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 organization 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. The preparation and creation of this manuscript was a strong collaborative effort and all authors contributed
equally. Authors are ordered alphabetically after the first.
References
Allen, A. P. and Gillooly, J. F. 2009. Towards an integration of ecological stoichiometry and the metabolic theory of ecology to
better understand nutrient cycling. – Ecol. Lett. 12: 369–384.
Atkinson, C. L. et al. 2013. Aggregated filter-feeding consumers
alter nutrient limitation : consequences for ecosystem and
community dynamics. – Ecology 94: 1359–1369.
Atkinson, C. L. et al. 2014. Tracing consumer-derived nitrogen in
riverine food webs. – Ecosystems 17: 485–496.
Bai, J. et al. 2012. Spatial and seasonal distribution of nitrogen in
marsh soils of a typical floodplain wetland in northeast China.
– Environ. Monitoring Assessment 184: 1253–1263.
Ballance, L. T. et al. 2006. Oceanographic influences on seabirds
and cetaceans of the eastern tropical Pacific: a review. – Progr.
Oceanogr. 69: 360–390.
Balseiro, E. and Albariño, R. 2006. detritivore C – N mismatch in
the leaf litter – shredder relationship of an Andean Patagonian
stream detritivore. – J. N. Am. Benthol. Soc. 25: 607–615.
Banks-Leite, C. and Ewers, R. M. 2009. Ecosystem boundaries.
– Wiley.
Bartels, P. et al. 2012. Reciprocal subsidies between freshwater and
terrestrial ecosystems structure consumer–resource dynamics.
– Ecology 93: 1173–1182.
Baxter, C. et al. 2004. Fish invasion restructures stream and forest
food web by interrupting reciprocal prey subsidies. – Ecology
85: 2656–2663.
EV-8
Baxter, C. V et al. 2005. Tangled webs: reciprocal flows of
invertebrate prey link streams and riparian zones. – Freshwater
Biol. 50: 201–220.
Béchet, A. et al. 2003. Spring hunting changes the regional
movements of migrating greater snow geese. – J. Appl. Ecol.
40: 553–564.
Boersma, M. and Elser, J. J. 2006. Too much of a good thing:
on stoichiometrically balanced diets and maximal growth.
– Ecology 87: 1325–1330.
Boersma, M. et al. 2008. Nutritional limitation travels up the food
chain. – Int. Rev. Hydrobiol. 93: 479–488.
Bojsen, B. and Jacobsen, D. 2003. Effects of deforestation on
macroinvertebrate diversity and assemblage structure in
Ecuadorian Amazon streams. – Arch. Hydrobiol. 158:
317–342.
Bouchard, S. S. and Bjorndal, K. A. 2000. Sea turtles as biological
transporters of nutrients and energy from marine to terrestrial
ecosystems. – Ecology 81: 2305–2313.
Bouwman, A. F. et al. 2009. Human alteration of the global
nitrogen and phosphorus soil balances for the period
1970–2050. – Global Biogeochem. Cycles 23: 1–16.
Brett, M. T. et al. 2009. Phytoplankton, not allochthonous carbon,
sustains herbivorous zooplankton production. – Proc. Natl
Acad. Sci. USA 106: 21197–21201.
Brittain, J. E. and Eikeland, T. J. 1988. Invertebrate drift – a review.
– Hydrobiologia 166: 77–93.
Carpenter, S. R. et al. 1985. Trophic interactions and lake productivity. – Bioscience 35: 634–639.
Carpenter, S. R. et al. 1998. Nonpoint pollution of surface
waters with phosphorus and nitrogen. – Ecol. Appl. 8:
559–568.
Chaiwanakupt, P. and Robertson, W. 1976. Leaching of phosphate
and selected cations from sandy soils as affected by lime.
– Agron. J. 68: 507–511.
Chaloner, D. T. et al. 2004. Variation in responses to spawning
Pacific salmon among three south-eastern Alaska streams.
– Freshwater Biol. 49: 587–599.
Childress, E. S. and McIntyre, P. B. 2015. Multiple nutrient
subsidy pathways from a spawning migration of iteroparous
fish. – Freshwater Biol. 60: 490–499.
Clay, N. A. et al. 2013. Manna from heaven: refuse from an
arboreal ant links aboveground and belowground processes in
a lowland tropical forest. – Ecosphere 4(11):141.
Clay, N. a. et al. 2014. Short-term sodium inputs attract microbidetritivores and their predators. – Soil Biol. Biochem. 75:
248–253.
Coale, K. H. et al. 1996. Control of community growth and export
production by upwelled iron in the equatorial Pacific Ocean.
– Nature 379: 621–624.
Codeço, C. T. and Grover, J. P. 2001. Competition along a spatial
gradient of resource supply: a microbial experimental model.
– Am. Nat. 157: 300–315.
Cothran, R. D. et al. 2014. Leaves and litterbugs: how litter
quality affects amphipod life-history and sexually selected
traits. – Freshwater Sci. 33: 812–819.
Cottingham, K. L. and Narayan, L. 2013. Subsidy quantity and
recipient community structure mediate plankton responses to
autumn leaf drop. – Ecosphere 4(7):89.
Cross, W. F. et al. 2003. Consumer-resource stoichiometry in
detritus-based streams. – Ecol. Lett. 6: 721–732.
Cross, W. F. et al. 2005. Ecological stoichiometry in freshwater
benthic systems: recent progress and perspectives. – Freshwater
Biol. 50: 1895–1912.
Cross, W. F. et al. 2007. Nutrient enrichment reduces constraints
on material flows in a detritus-based food web. – Ecology 88:
2563–2575.
Davis, J. M. et al. 2011. Increasing donor ecosystem productivity
decreases terrestrial consumer reliance on a stream resource
subsidy. – Oecologia 167: 821–834.
de Baar, H. J. et al. 1995. Importance of iron for plankton blooms
and carbon dioxide drawdown in the Southern Ocean.
– Nature 373: 412–415.
Dodds, W. K. 2006. Nutrients and the ‘dead zone’: The link
between nutrient ratios and dissolved oxygen in the northern
Gulf of Mexico. – Front. Ecol. Environ. 4: 211–217.
Doucett, R. R. et al. 1999. Effects of the spawning migration on
the nutritional status of anadromous Atlantic salmon (Salmo
salar): insights from stable-isotope analysis. – Can. J. Fish.
Aquat. Sci. 56: 2172–2180.
Elser, J. J. and Hassett, R. P. 1994. A stoichiometric analysis of
the zooplankton–phytoplankton interaction in marine and
freshwater ecosystems. – Nature 370: 211–213.
Elser, J. J. et al. 1988. Zooplankton-mediated transitions between
N- and P-limited algal growth. – Limnol. Oceanogr. 33:
1–14.
Elser, J. J. et al. 1996. Organism size, life history, and N:P stoichiometry. – Bioscience 46: 674–684.
Elser, J. J. et al. 2007. Global analysis of nitrogen and phosphorus
limitation of primary producers in freshwater, marine and terrestrial ecosystems. – Ecol. Lett. 10: 1135–1142.
Elser, J. J. et al. 2009. Shifts in lake N:P stoichiometry and
nutrient limitation driven by atmospheric nitrogen deposition.
– Science 326: 835–837.
Fahrig, L. 2003. Effects of habitat fragmentation on biodiversity.
– Annu. Rev. Ecol. Evol. Syst. 34: 487–515.
Falkowski, P. G. et al. 1998. Biogeochemical controls and feedbacks
on ocean primary production. – Science 281: 200–206
Falkowski, P. et al. 2000. The global carbon cycle: a test of our
knowledge of earth as a system. – Science 290: 291–296.
Forman, R. T. T. and Alexander, L. E. 1998. Roads and their major
ecological effects. – Annu. Rev. Ecol. Syst. 29: 207–231.
Fox, A. D. et al. 2005. Effects of agricultural change on abundance,
fitness components and distribution of two arctic-nesting
goose populations. – Global Change Biol. 11: 881–893.
France, R. L. 2011. Leaves as ‘crackers’, biofilm as ‘peanut butter’:
exploratory use of stable isotopes as evidence for microbial
pathways in detrital food webs. – Oceanol. Hydrobiol. Stud.
40: 110–115.
Galloway, J. N. et al. 2004. Nitrogen cycles: past, present and
future. – Biogeochemistry 70: 153–226.
Gauthier, G. et al. 2005. Interactions between land use, habitat
use, and population increase in greater snow geese: what are
the consequences for natural wetlands? – Global Change Biol.
11: 856–868.
Geremia, C. et al. 2014. Integrating population-and individuallevel information in a movement model of Yellowstone bison.
– Ecol. Appl. 24: 346–362.
Ghadouani, A. et al. 2003. Effects of experimentally induced
cyanobacterial blooms on crustacean zooplankton communities. – Freshwater Biol. 48: 363–381.
Gilbert-Norton, L. et al. 2010. A meta-analytic review of corridor
effectiveness. – Conserv. Biol. 24: 660–668.
Gounand, I. et al. 2014. The paradox of enrichment in metaecosystems. – Am. Nat. 184: 752–763.
Gravel, D. et al. 2010. Patch dynamics, persistence and species
coexistence in metaecosystems. – Am. Nat. 176: 289–302.
Griffith, M. B. et al. 1998. Lateral dispersal of adult aquatic insects
(Plecoptera, Trichoptera) following emergence from headwater
streams in forested Appalachian catchments. – Ann. Entomol.
Soc. Am. 91: 195–201.
Hajrasuliha, S. et al. 1998. Fate of 15N fertilizer applied to
trickle-irrigated grapevines. – Am. J. Enology Viticulture 49:
191–198.
Hall, S. R. 2009. Stoichiometrically explicit food webs: feedbacks
between resource supply, elemental constraints and species
diversity. – Annu. Rev. Ecol. Evol. Syst. 40: 503–528.
Hannides, C. C. S. et al. 2009. Export stoichiometry and migrantmediated flux of phosphorus in the North Pacific Subtropical
Gyre. – Deep-Sea Res. I Oceanogr. Res. Papers 56: 73–88.
Harpole, W. S. et al. 2011. Nutrient co-limitation of primary
producer communities. – Ecol. Lett. 14: 852–862.
Havik, G. et al. 2014. Seabird nutrient subsidies benefit nonnitrogen fixing trees and alter species composition in South
American coastal dry forests. – PloS ONE 9: e86381.
Helfield, J. M. and Naiman, R. J. 2001. Effects of salmon-derived
nitrogen on riparian forest growth and implications for stream
productivity. – Ecology 82: 2403–2409.
Hessen, D. O. et al. 2004. Carbon, sequestration in ecosystems:
the role of stoichiometry. – Ecology 85: 1179–1192.
Heywood, K. J. 1996. Diel vertical migration of zooplankton in
the northeast Atlantic. – J. Plankton Res. 18: 163–184.
Hilderbrand, G. 1998. Studies of the nutritional ecology of
coastal brown bears. – PhD thesis, Washington State Univ.,
Pullman.
Hilderbrand, G. V. et al. 1999. Role of brown bears (Ursus arctos)
in the flow of marine nitrogen into a terrestrial ecosystem.
– Oecologia 121: 546–550.
Hinkley, E. S. et al. 2014. Nitrogen retention and transport differ
by hillslope aspect at the rain-snow transition of the Colorado
Front Range. – J. Geophys. Res. Biosci. 119: 1281–1296.
Hodgson, J. A. et al. 2011. Habitat area, quality and connectivity:
striking the balance for efficient conservation. – J. Appl. Ecol.
48: 148–152.
Hopkinson, C. S. et al. 1997. Stoichiometry of dissolved organic
matter dynamics on the continental shelf of the northeastern
USA. – Continental Shelf Res. 17: 473–489.
Huxel, G. R. et al. 2002. Effects of partitioning allochthonous and
autochthonous resources on food web stability. – Ecol. Res.
17: 419–432.
Iwata, T. 2007. Linking stream habitats and spider distribution:
spatial variations in trophic transfer across a forest – stream
boundary. – Ecol. Res. 22: 619–628.
Janetski, D. J. et al. 2009. Pacific salmon effects on stream ecosystems: a quantitative synthesis. – Oecologia 159: 583–595.
Jones, H. P. 2010. Prognosis for ecosystem recovery following
rodent eradication and seabird restoration in an island archipelago. – Ecol. Appl. 20: 1204–1216.
Jonsson, B. and Jonsson, N. 2003. Migratory Atlantic salmon
as vectors for the transfer of energy and nutrients between
freshwater and marine environments. – Freshwater Biol. 48:
21–27.
Junker, J. R. and Cross, W. F. 2014. Seasonality in the trophic
basis of a temperate stream invertebrate assemblage: importance of temperature and food quality. – Limnol. Oceanogr
59: 507–518.
Kareiva, P. et al. 2007. Domesticated nature: shaping landscape and
ecosystems for human welfare. – Science 316: 1866–1869.
Kelly, P. T. et al. 2014. Terrestrial carbon is a resource, but not a
subsidy, for lake zooplankton. – Ecology 95: 1236–1242.
Kitchell, J. F. et al. 1999. Nutrient cycling at the landscape scale:
the role of diel foraging migrations by geese at the Bosque del
Apache National Wildlife Refuge, New Mexico. – Limnol.
Oceanogr. 44: 828–836.
Kohler, A. E. et al. 2012. Nutrient enrichment with salmon carcass
analogs in the Columbia River Basin, USA: a stream food web
analysis. – Trans. Am. Fish. Soc. 141: 802–824.
Kolb, G. S. et al. 2013. Ecological stoichiometry and density
responses of plant–arthropod communities on cormorant
nesting islands. – PloS ONE 8: e61772.
Kraus, J. M. and Vonesh, J. R. 2012. Fluxes of terrestrial and
aquatic carbon by emergent mosquitoes: a test of controls and
implications for cross-ecosystem linkages. – Oecologia 170:
1111–1122.
EV-9
Lau, D. C. P. et al. 2008. Experimental dietary manipulations
for determining the relative importance of allochthonous
and autochthonous food resources in tropical streams.
– Freshwater. Biol. 53: 139–147.
Legrand, D. et al. 2012. The Metatron: an experimental system to
study dispersal and metaecosystems for terrestrial organisms.
– Nat. Meth. 9: 828–33.
Lennon, J. T. and Pfaff, L. E. 2005. Source and supply of terrestrial
organic matter affects aquatic microbial metabolism. – Aquat.
Microb. Ecol. 39: 107–119.
Leroux, S. J. and Loreau, M. 2008. Subsidy hypothesis and
strength of trophic cascades across ecosystems. – Ecol. Lett.
11: 1147–1156.
Levi, P. S. et al. 2013. Biogeochemical transformation of a nutrient
subsidy: salmon, streams and nitrification. – Biogeochemistry
113: 643–655.
Ligon, F. K. et al. 1995. Downstream ecological effects of dams.
– Bioscience 45: 183–192.
Litchman, E. and Klausmeier, C. A. 2008. Trait-based community
ecology of phytoplankton. – Annu. Rev. Ecol. Evol. Syst. 39:
615–639.
Liu, Y. et al. 2013. Nutrient release characteristics from droppings
of grass-foraging waterfowl (Anser brachyrhynchus) roosting in
aquatic habitats. – Ecohydrology 7: 1216–1222.
Loreau, M. and Holt, R. D. 2004. Spatial flows and the regulation
of ecosystems. – Am. Nat. 163: 606–615.
Mahowald, N. M. et al. 2009. Atmospheric iron deposition: global
distribution, variability and human perturbations. – Annu.
Rev. Mar. Sci. 1: 245–278.
Manzoni, S. et al. 2008. The global stoichiometry of litter nitrogen
mineralization. – Science 321: 684–687.
Marcarelli, A. et al. 2011. Quantity and quality: unifying food web
and ecosystem perspectives on the role of resource subsidies in
freshwaters. – Ecology 92: 1215–1225.
Marczak, L. B. et al. 2007. Meta-analysis: trophic level, habitat and
productivity shape the food web effects of resource subsidies.
– Ecology 88: 140–148.
Maron, J. L. et al. 2006. An introduced predator alters Aleutian
Island plant communities by thwarting nutrient subsidies.
– Ecol. Monogr. 76: 3–24.
Masclaux, H. et al. 2013. How pollen organic matter enters
freshwater food webs. – Limnol. Oceanogr. 58: 1185–1195.
McDowell, R. and Sharpley, A. 2002. Phosphorus transport in
overland flow in response to position of manure application.
– J. Environ. Qual. 31: 217–227.
McGill, B. J. et al. 2006. Rebuilding community ecology from
functional traits. – Trends Ecol. Evol. 21: 178–185.
McIntyre, P. B. et al. 2008. Fish distributions and nutrient cycling
in streams: can fish create biogeochemical hotspots? – Ecology
89: 2335–2346.
Meyer, J. L. et al. 2000. Terrestrial litter inputs as determinants of
food quality of organic matter in a forest stream. – Int. Verein.
Theor. Angew. Limnol. Verhandl. 27: 1346–1350.
Minakawa, N. and Gara, R. I. 2005. Spatial and temporal
distribution of coho salmon carcasses in a stream in the Pacific
Northwest, USA. – Hydrobiologia 539: 163–166.
Mobæk, R. et al. 2012. Experimental evidence of density dependent activity pattern of a large herbivore in an alpine ecosystem.
– Oikos 121: 1364–1369.
Moe, S. et al. 2005. Recent advances in ecological stoichiometry:
insights for population and community ecology. – Oikos 109:
29–39.
Muehlbauer, J. D. et al. 2014. How wide is a stream? Spatial extent
of the potential “stream signature” in terrestrial food webs
using meta-analysis. – Ecology 95: 44–55.
Müller, K. 1982. The colonization cycle of freshwater insects.
– Oecologia 52: 202–207.
EV-10
Murray, M. G. 1995. Specific nutrient requirements and migration
of wildebeest. – In: Sinclair, A. R. E. and Arcese, P. (eds),
Serengeti II: dynamics, management and conversation of an
ecosystem. Univ. of Chicago Press, pp. 673.
Nakano, S. and Murakami, M. 2001. Reciprocal subsidies: dynamic
interdependence between terrestrial and aquatic food webs.
– Proc. Natl Acad. Sci. USA 98: 166–170.
Nie, Y. et al. 2015. Obligate herbivory in an ancestrally carnivorous
lineage: the giant panda and bamboo from the perspective of
nutritional geometry. – Funct. Ecol. 29: 256–34.
Nowlin, W. H. et al. 2007. Allochthonous subsidy of periodical
cicadas affects the dynamics and stability of pond communities. – Ecology 88: 2174–2186.
Olson, M. H. et al. 2005. Impact of migratory snow geese on
nitrogen and phosphorus dynamics in a freshwater reservoir.
– Freshwater Biol. 50: 882–890.
Peñuelas, J. et al. 2013. Human-induced nitrogen–phosphorus
imbalances alter natural and managed ecosystems across the
globe. – Nat. Commun. doi: 10.1038/ncomms3934.
Petrone, K. et al. 2007. Hydrologic and biotic control of
nitrogen export during snowmelt: a combined conservative
and reactive tracer approach. – Water Resour. Res. 43:
1–13.
Pilati, A. et al. 2009. Effects of agricultural subsidies of nutrients
and detritus on fish and plankton of shallow-reservoir ecosystems. – Ecol. Appl. 19: 942–960.
Polis, G. A. et al. 1997. Toward an integration of landscape and
food web ecology: the dynamics of spatially subsidized food
webs. – Annu. Rev. Ecol. Syst. 28: 289–316.
Polis, G. A. et al. 2004. Food webs at the landscape level. – Univ.
of Chicago Press.
Prospero, J. M. 1999. Long-range transport of mineral dust in the
global atmosphere: impact of African dust on the environment
of the southeastern United States. – Proc. Natl Acad. Sci. USA
96: 3396–3403.
Reef, R. et al. 2014. Mammalian herbivores in Australia transport
nutrients from terrestrial to marine ecosystems via mangroves.
– J. Trop. Ecol. 30: 179–188.
Rockström, J. et al. 2009. A safe operating space for humanity.
– Nature 461: 472–475.
Rowe, L. and Richardson, J. S. 2001. Community responses to
experimental food depletion: resource tracking by stream
invertebrates. – Oecologia 129: 473–480.
Royer, D. L. et al. 2004. CO2 as a primary driver of Phanerozoic
climate. – GSA Today 14: 4–10.
Rubbo, M. J. et al. 2006. Terrestrial subsidies of organic carbon
support net ecosystem production in temporary forest ponds:
evidence from an ecosystem experiment. – Ecosystems 9:
1170–1176.
Rüegg, J. et al. 2011. Salmon subsidies alleviate nutrient limitation
of benthic biofilms in southeast Alaska streams. – Can. J. Fish.
Aquat. Sci. 68: 277–287.
Ruess, R. and McNaughton, S. 1988. Ammonia volatilization and
the effects of large grazing mammals on nutrient loss from East
African grasslands. – Oecologia 77: 382–386.
Sabo, J. L. and Power, M. E. 2002. Numerical response of lizards
to aquatic insects and short-term consequences for terrestrial
prey. – Ecology 83: 3023–3036.
Salmon, M. and Lohmann, K. J. 1989. Orientation cues used by
hatchling loggerhead sea turtles (Caretta caretta L.) during
their offshore migration. – Ethology 83: 215–228.
Salmon, M. et al. 1995. Behavior of loggerhead sea turtles on an
urban beach. I. Correlates of nest placement. – J. Herpetol.
29: 560–567.
Sardans, J. and Peñuelas, J. 2014. Hydraulic redistribution by
plants and nutrient stoichiometry: shifts under global change.
– Ecohydrology 7: 1–20.
Sardans, J. et al. 2012. The C:N:P stoichiometry of organisms
and ecosystems in a changing world: a review and perspectives.
– Perspect. Plant Ecol. Evol. Syst. 14: 33–47.
Schade, A. J. D. et al. 2001. The influence of a riparian shrub on
nitrogen cycling in a Sonoran desert stream. – Ecology 82:
3363–3376.
Schade, J. D. et al. 2005. A conceptual framework for ecosystem
stoichiometry: balancing resource supply and demand. – Oikos
109: 40–51.
Schädler, M. et al. 2005. Food web properties in aquatic microcosms with litter mixtures are predictable from component
species. – Arch. Hydrobiol. 163: 211–223.
Schindler, D. E. and Eby, L. A. 1997. Stoichiometry of fishes and
their prey: implications for nutrient recycling. – Ecology 78:
1816–1831.
Schreeg, L. A. et al. 2013. Nutrient-specific solubility patterns of
leaf litter across 41 lowland tropical woody species. – Ecology
94: 94–105.
Seebens, H. et al. 2013. The risk of marine bioinvasion caused by
global shipping. – Ecol. Lett. 16: 782–790.
Senft, R. et al. 1987. Nitrogen and energy budgets of free-roaming
cattle. – J. Range Manage. 40: 421–424.
Shi, J. H. et al. 2013. Concentration, solubility and deposition
flux of atmospheric particulate nutrients over the Yellow Sea.
– Deep Sea Res. II: Topical Stud. Oceanogr. 97: 43–50.
Singer, G. a and Battin, T. J. 2007. Anthropogenic subsidies alter
stream consumer–resource stoichiometry, biodiversity, and
food chains. – Ecol. Appl. 17: 376–389.
Sitters, J. et al. 2014. Interactions between C: N: P stoichiometry
and soil macrofauna control dung decomposition of savanna
herbivores. – Funct. Ecol. 28: 776–786.
Slomp, C. and Van Cappelen, P. 2007. The global marine phosphorus cycle: sensitivity to oceanic circulation. – Biogeosciences 4: 155–171.
Small, G. E. et al. 2009. Can consumer stoichiometric regulation
control nutrient spiraling in streams? – J. N. Am. Benthol.
Soc. 28: 747–765.
Stephens, J. P. et al. 2013. Anthropogenic changes to leaf litter
input affect the fitness of a larval amphibian. – Freshwater Biol.
58: 1631–1646.
Sterner, R. W. and Elser, J. J. 2002. Ecological stoichiometry:
the biology of elements from molecules to the biosphere.
– Princeton Univ. Press.
Sterner, R. W. et al. 1992. Stoichiometric relationships among
producers, consumers and nutrient cycling in pelagic ecosystems. – Biogeochemistry 17: 49–67.
Sullivan, M. L. et al. 2014. Carbon and nitrogen ratios of aquatic
and terrestrial prey for freshwater fishes. – J. Freshwater Ecol.
29: 259–266.
Thomas, R. et al. 1986. Fate of sheep urine-N applied to an upland
grass sward. – Plant Soil 91: 425–427.
Tiegs, S. D. et al. 2011. Ecological effects of live salmon exceed
those of carcasses during an annual spawning migration.
– Ecosystems 14: 598–614.
Towne, E. G. 2000. Prairie vegetation and soil nutrient responses
to ungulate carcasses. – Oecologia 122: 232–239.
Urabe, J. et al. 2002. Reduced light increases herbivore production
due to stoichiometric effects of light/nutrient balance.
– Ecology 83: 619–627.
Van Uytvanck, J. et al. 2010. Nitrogen depletion and redistribution
by free-ranging cattle in the restoration process of mosaic landscapes: the role of foraging strategy and habitat proportion.
– Restor. Ecol. 18: 205–216.
Vanni, M. J. 2002. Nutrient cycling by animals in freshwater
ecosystems. – Annu. Rev. Ecol. Syst. 33: 341–370.
Veldboom, J. A. and Haro, R. J. 2011. Stoichiometric relationship
between suspension-feeding caddisfly (Trichoptera: Brachycentridae) and seston. – Hydrobiologia 675: 129–141.
Vitousek, P. M. et al. 1997. Human alteration of the global
nitrogen cycle: sources and consequences. – Ecol. Appl. 7:
737–750.
Wakefield, E. D. et al. 2009. Quantifying habitat use and preferences of pelagic seabirds using individual movement data: a
review. – Mar. Ecol. Progr. Ser. 391: 165–182.
Wallace, J. et al. 1997. Multiple trophic levels of a forest stream
linked to terrestrial litter inputs. – Science 277: 102–104.
Wallace, J. B. et al. 1999. Effects of resource limitation on a
detrital-based ecosystem. – Ecol. Monogr. 69: 409–442.
Waters, T. F. 1972. The drift of stream insects. – Annu. Rev.
Entomol. 17: 253–272.
Webster, J. R. et al. 1999. What happens to allochthonous material
that falls into streams? A synthesis of new and published information from Coweeta. – Freshwater Biol. 41: 687–705.
Weimerskirch, H. et al. 1997. Alternative foraging strategies
and resource allocation by male and female wandering
albatrosses. – Ecology 78: 2051–2063.
Wiens, J. A. et al. 1985. Boundary dynamics: a conceptual
framework for studying landscape ecosystems. – Oikos 45:
421–427.
Williams, C. G. 2008. Aerobiology of Pinus taeda pollen clouds.
– Can. J. For. Res. 38: 2177–2188.
Wolanski, E. et al. 1988. Tidal jets, nutrient upwelling and
their influence on the productivity of the alga Halimeda in the
Ribbon Reefs, Great Barrier Reef. – Estuarine Coastal Shelf
Sci. 26: 169–201.
Zhou, X. et al. 2010. Perennial filter strips reduce nitrate levels
in soil and shallow groundwater after grassland-to-cropland
conversion. – J. Environ. Qual. 39: 2006–2015.
EV-11