RIVER RESEARCH AND APPLICATIONS
River. Res. Applic. (2009)
Published online in Wiley InterScience
(www.interscience.wiley.com) DOI: 10.1002/rra.1283
RESOURCE SUBSIDIES ACROSS THE LAND–FRESHWATER INTERFACE AND
RESPONSES IN RECIPIENT COMMUNITIES
JOHN S. RICHARDSON,a* YIXIN ZHANG b and LAURIE B. MARCZAK c
a
Department of Forest Sciences, University of British Columbia, Vancouver, V6T 1Z4, Canada
b
Department of Biology, Texas State University, San Marcos, TX 78666, USA
c
Department of Biology and Biochemistry, University of Houston, Houston, TX 77004, USA
ABSTRACT
Fluxes of resource subsidies, such as terrestrial leaf litter to streams and adult aquatic insects to riparian predators, are examples
of important links between adjacent ecosystems. The importance of these cross-ecosystem resource flows from donor systems to
recipient consumers is increasingly recognized. Streams, especially small streams with their high edge ratio with the terrestrial
system, provide excellent models for the study of subsidies and a large portion of this literature has been produced by aquatic
scientists. Field experiments manipulating flows between small streams and their riparian areas (e.g. leaf litter, terrestrial
invertebrates, and adult aquatic insects to riparian areas) have indicated that consumers in streams and riparian areas are highly
dependent upon such subsidies and the value of the subsidies are further modified by patterns of retention and pathways of use.
Experiments typically indicate rapid growth or demographic responses by consumers, indicating these populations are resource
limited or at levels of incipient population limitation, and can capitalize on short-term resource pulses. More press manipulations
are still necessary to determine the dynamical consequences of subsidies for recipient communities. The nature of the subsidy
(e.g. species of litter or invertebrates) and its timing are also important details that need further study. Finally, there are
opportunities to consider the evolution of life cycle timing (modelling), interception strategies by recipient populations and
short-term and long-term responses of communities. Copyright # 2009 John Wiley & Sons, Ltd.
key words: allochthonous; consumers; dynamics; ecosystems; energy flux; linkage; nutrients; streams
Received 16 October 2008; Revised 14 March 2009; Accepted 14 May 2009
INTRODUCTION
Early conceptions of ecosystems held that ecological systems were self-contained entities and their dynamics were
largely determined locally by processes internal to the system while external forces were relatively weak (Forbes,
1887). This concept of the relative boundedness of ecosystems has been a useful simplification in trying to
understand the controls on the dynamics of ecosystems (e.g. Levin and Paine, 1974). However, over the past half
century the demonstration of the importance of movements of organisms and energy across ecosystem ‘boundaries’
has changed the view of ecosystems to being considered as leaky and strongly influenced from beyond the local
system (e.g. Likens and Bormann, 1974; Polis et al., 1997; Levin, 2005; Holt, 2008). One of the key processes that
crosses ecosystem boundaries and links adjacent systems are resource subsidies.
What is a resource subsidy? These are flows of biologically fixed energy and nutrients from one ecosystem to
another, i.e. allochthonous resources produced outside of the recipient system. The consequences of these subsidies
for recipient consumers can be either as a direct nutritional resource, or reducing a consumer’s costs of foraging by
augmenting the local resource supply. The expected results of subsidies are increases in population productivity and
enhanced population growth. Here, we distinguish active foraging across ecosystem boundaries from those of
subsidies, thus mergansers or otters foraging for fish in rivers would not constitute a subsidized system in our use of
the term, i.e. subsidy flows must be donor-controlled (see below). In a donor-controlled system the recipient
*Correspondence to: John S. Richardson, Department of Forest Sciences, University of British Columbia, Vancouver, V6T 1Z4 Canada.
E-mail: [email protected]
Copyright # 2009 John Wiley & Sons, Ltd.
J. S. RICHARDSON, Y. ZHANG AND L. B. MARCZAK
consumer cannot influence the supply rate of resources directly, i.e. they are dependent on the resource supply, such
as the input of terrestrial leaf litter to streams. Resource subsidies have been known for decades, for example the
importance to consumers of leaf litter inputs to streams or to soils (e.g. Lloyd, 1921; Hynes, 1941). The synthetic
approach developed by Polis et al. (1997) allowed for the integration of these qualitatively different forms of donorcontrolled resource subsidies and facilitated progress on conceptually unifying these processes. There is
considerable variation in the rates of subsidy fluxes in terms of magnitude, duration, amplitude and quality, with a
spectrum of possible dynamical responses of consumers (Holt, 2008). The availability of theory linking these
processes has resulted in formulation of a range of testable hypotheses (e.g. Polis et al., 1997; Loreau and Holt,
2004).
Freshwater scientists have repeatedly demonstrated the utility of aquatic systems as model systems for studying
resource subsidies. Since organisms that are mostly aquatic have specializations that identify them as distinct from
terrestrial organisms, and vice versa, the distinction across these boundaries is relatively clear. It is from this
physically distinct boundary at the ocean-shore interface that Polis and Hurd (1995, 1996) developed their
empirical and theoretical work providing a modern synthesis of the importance of cross-ecosystem subsidies (Polis
et al., 2004). From Polis’ examples of marine wrack on fringes of oceanic desert islands, to Dissolved organic
carbon (DOC) inputs to freshwaters, leaf litter to streams, etc., aquatic systems in general, and streams in particular,
have been forefront in the development and testing of these ideas. Oceans and lakes, while bounded by shorelines,
are now known to be more heterotrophic than previously considered, i.e. their productivity is largely dependent on
externally produced organic carbon (Cole et al., 2006; Cole et al., 2007). DOC, much of it from the terrestrial
landscape, plays a central role in the functioning of lake ecosystems and support of aquatic food webs (Pace et al.,
2004). By studying whole-lake ecosystems, Carpenter et al. (2005) found that carbon cycles relating to dissolved
and particulate organic carbon, zooplankton and fishes are substantially subsidized by flows of terrestrial organic
carbon from surrounding watersheds. Even more so than in lakes, the strong linkages of streams to the terrestrial
realm through resource subsidies have contributed some of the best demonstrations of the importance of these
cross-ecosystem fluxes. Streams provide a useful model system because they are gravitational attractors for
material and so tend to passively accumulate resources from adjacent terrestrial systems (Leroux and Loreau, 2008)
and also because of their high ratio of edge with the surrounding terrestrial environment. This is particularly true for
small streams that have a high edge to area ratio; systems with this kind of geometry receive larger amounts of
allochthonous material and energy as inputs into the food web.
In this review we concentrate on examples of cross-ecosystem resource subsidies involving streams, and to some
extent lakes, and particularly on examples from the past decade (Figure 1). Previous reviews by Polis et al. (1997)
and Baxter et al. (2005) described additional examples of resource subsidies. Details of some of the consequences
for consumers of resource flows to and from streams are available and hence we emphasize those examples. There
can be little doubt that freshwater scientists have made important contributions to the development and testing of
the significance of the dynamics of cross-ecosystem resource subsidies.
HOW HAS AQUATIC SCIENCE CONTRIBUTED TO THE DEVELOPMENT
OF ECOLOGICAL CONCEPTS?
Freshwater science has been at the forefront of testing of the roles of resource subsidies in recipient communities.
Many of the best examples of resource subsidies come from the interface of aquatic-terrestrial systems, probably
because of the relatively clear physical boundaries between adjacent ecosystems. Organisms primarily living in
aquatic or terrestrial systems possess a suite of traits that are suited more to one system than another. However, there
are also many organisms capable of moving across the aquatic-terrestrial boundary as part of their foraging
behaviour or as a consequence of ontogenetic niche shifts of complex life cycles.
Decades of experimental and descriptive work have demonstrated that cross-ecosystem resource subsidies across
the diffusive interface between freshwater and terrestrial realms can have large consequences for consumerresource dynamics and the resulting population responses. These studies in freshwater have also contributed to our
understanding of some of the controlling processes on populations and their communities, the development of
spatially explicit models for communities and the theory of trophic cascades.
Copyright # 2009 John Wiley & Sons, Ltd.
River. Res. Applic. (2009)
DOI: 10.1002/rra
RESOURCE SUBSIDIES ACROSS THE LAND–FRESHWATER INTERFACE
Figure 1. A schematic illustration of some of the major flows of biologically fixed energy across the stream-terrestrial interface and along the
fluvial network. Widths of arrows do not imply magnitudes of fluxes
EXAMPLES OF CROSS-ECOSYSTEM RESOURCE SUBSIDIES INVOLVING FRESHWATERS
Leaf litter and other terrestrial inputs to aquatic ecosystems
One of the best studied of all cross-ecosystem subsidies is the input of organic matter (Figure 1), particularly leaf
litter, to streams (e.g. Hynes, 1941; Fisher and Likens, 1972; Richardson, 1991; Wallace et al., 1999; Webster et al.,
1999). Many taxa feed more-or-less exclusively on decaying leaf litter (including surface biofilms and leaf tissue) in
streams and lakes, a functional group referred to as detritivores or ‘shredders’. Amounts of 400–700 g ash-free dry
mass m 2 year 1 of leaf litter can fall into forested streams (Richardson et al., 2005). Detailed experimental work
over the past two decades has demonstrated through additions and interception of leaf litter inputs that consumer
populations are strongly limited by these resource subsidies (e.g. Richardson, 1991; Dobson and Hildrew, 1992;
Wallace et al., 1999). Populations of stream detritivores feeding on terrestrial litter have a large scope for rapid
increase as resource abundance increases, and respond quickly to depletion of litter standing stocks (Wallace et al.,
1999; Rowe and Richardson, 2001). Wallace et al. (1999) have demonstrated that in the absence of litter inputs, the
productivity of an entire stream system, including predators, declined dramatically.
Copyright # 2009 John Wiley & Sons, Ltd.
River. Res. Applic. (2009)
DOI: 10.1002/rra
J. S. RICHARDSON, Y. ZHANG AND L. B. MARCZAK
Dissolved organic carbon (DOC: organic matter <0.63 mm) enters streams from the direct leaching from
particulate organic matter in the stream or through groundwater inputs carrying leachates from the organic horizons
of soils. DOC includes a diverse array of compounds, and provides a source of energy for bacterial production in
biofilms (e.g. Battin et al., 2008) and even to some macroinvertebrates such as filter-feeding blackfly larvae
(Ciborowski et al., 1997). The relative contribution of terrestrially derived DOC to stream productivity is still not
known, but likely to be substantial (Battin et al., 2008). The contribution of terrestrially derived DOC to lakes has been
demonstrated to be a major support of productivity of some temperate lakes (Carpenter et al., 2005; Cole et al., 2006).
Wood inputs to streams are considered to be a major influence connecting riparian areas to streams, mostly in the
context of structure within stream channels. However, wood also provides an important food resource to many
benthic organisms that feed on wood, either feeding on biofilms (also called epixylon) or digesting wood itself with
the aid of microbial symbionts. Some wood-eating invertebrates appear to be limited, or mostly so, to that food
source, including Lara avara LeConte (Coleoptera: Elmidae), Lipsothrix spp. (Diptera: Tipulidae) and the
caddisfly Heteroplectron californicum McLachlan. Many other invertebrates consume wood, mostly for the
biofilms associated with it (Bondar et al., 2005; Eggert and Wallace, 2007). In one Oregon stream Dudley and
Anderson (1982) recorded 56 species of invertebrates contained some wood fragments in their digestive tracts.
There has not yet been an estimate of the contribution of wood as a biological energy source in streams, but it may
be a substantial contributor to the productivity of streams.
Deposition of pollen from conifer trees can also be a major allochthonous input of limiting nutrients to boreal
lake ecosystems in spring (Graham et al., 2006). A lake survey and a mesocosm experiment indicated that jack pine
(Pinus banksiana) pollen inputs subsidized littoral nutrient levels and promoted production in small boreal lakes by
stimulating algal growth and zooplankton abundance. Phytoplankton and herbivorous zooplankton biomass, as
well as periphyton biomass significantly increased with pollen amendments. Fruits and seeds in some aquatic
systems are known to drive population dynamics and life history timing of consumers, especially freshwater fish
(e.g. Correa et al., 2007), as well as extending the recruitment shadow of the contributing terrestrial plants. Pollen,
fruits and seeds are typically of substantially greater food quality than leaves rendering their inputs to aquatic
systems of potentially greater importance than might be suggested by the mass of these inputs alone.
Terrestrial invertebrate inputs to streams
Terrestrial invertebrates falling to the stream surface have been shown to contribute a large portion of the diets of
some fish (Wipfli, 1997; Kawaguchi and Nakano, 2001; Romero et al., 2005; Chan et al., 2007), influencing the
distribution of fish populations (Kawaguchi et al., 2003), and leading to cascading trophic interactions in stream
ecosystems (Nakano et al., 1999). In some places nearly half the energy obtained by salmonids comes from
subsidies from the forest canopy (e.g. Wipfli, 1997). During some times of year, low flows (lack of a drift delivery
system) and early life stages of typical prey species (small and unavailable) combine to limit the growth of some
stream salmonids in the absence of terrestrial subsidies (Zhang and Richardson, 2007). Experimental augmentation
of prey to fish in natural streams has demonstrated the extent of this dependence on terrestrial sources when they are
available (e.g. Boss and Richardson, 2002; Baxter et al., 2004, 2007).
Flows from streams to terrestrial areas
The flux of adult aquatic insects emerging from streams provides a significant subsidy of energy and prey to
riparian web-building spiders (Jackson and Fisher, 1986; Williams et al., 1995; Henschel et al., 2001; Kato et al.,
2003; Marczak and Richardson, 2007; Burdon and Harding, 2008; Chan et al., 2009) and other riparian arthropods
(Paetzold et al., 2005; Paetzold and Tockner, 2005). In a temperate system, spiders were on average 1.75 times more
abundant where they had direct access to adult aquatic insects as prey compared to areas where these prey were
experimentally reduced (Marczak and Richardson, 2007). Disturbance can also interact with flows of subsidies. For
instance, Greenwood and McIntosh (2008) demonstrated that flood disturbances positively influenced aspects of
habitat quality of a riparian fishing spider—there was a higher proportion of habitat in the more disturbed rivers.
However, the abundance of aquatic prey was highest at stable rivers. Spider biomass peaked at the intermediate
levels of stability, suggesting the existence of a trade off between habitat quality and subsidy availability
(Greenwood and McIntosh, 2008).
Copyright # 2009 John Wiley & Sons, Ltd.
River. Res. Applic. (2009)
DOI: 10.1002/rra
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Other riparian-associated consumers also feed on adult aquatic insects (Sabo and Power, 2002 Richardson and
Danehy, 2007). Insectivorous bird abundance and distribution is influenced by adult aquatic insect fluxes in riparian
zones (Iwata et al., 2003; Iwata, 2007; Chan et al., 2008). Bats often forage along forest edges, especially in riparian
edges where they have access to emergent aquatic insects (Fukui et al., 2006). Along with birds, bats significantly
limit arthropod populations in tropical forests (Kalka et al., 2008; Williams-Guillén et al., 2008). Many dragonflies
likewise patrol stream-forest edges for insects.
In addition to adult aquatic insects flying from streams (or lentic systems) to adjacent terrestrial systems, there
are other flows. For instance, algae can be washed up onto riparian areas during high flows and provide a resource to
herbivorous species, such as grasshoppers (Bastow et al., 2002). Fine, organic sediments may also be washed onto
floodplains providing critical habitats for germination of many plants (Rood et al., 2003).
The benefit of resource subsidies to consumers depends as much on ‘packaging’ as on the constituent nutrients.
Salmon carcasses provide marine-derived subsidies to streams (Wipfli et al., 1998; Zhang et al., 2003), but also to
riparian areas and beyond (Gende et al., 2002). Note that we include this as a subsidy as these fish come from
marine environments (donor-control), even though their consumers may actively cross the stream-terrestrial
margin. These carcasses are eaten by a variety of consumers precisely because they are a complete source of protein
and fat (Wipfli et al., 1998). Bears, birds and a host of other consumers drag salmon carcasses out of streams, or
defecate away from streams, delivering a subsidy of nutrients and energy to terrestrial systems (e.g. Helfield and
Naiman, 2001). The various nutrients that are donated by reproducing salmon may enter food webs in their
dissolved form, but probably not until after they are passed through an initial recipient consumer. Whether or not
nutrients are actually limiting to these forest soils is another question, but evidence indicates that in some instances
plants show higher growth rates when their soils receive inputs of salmon than when they do not (Helfield and
Naiman, 2006). Such nutrients are also important to bottom-up processes by enhancing productivity of basal
resources including primary production and biofilms (Wipfli et al., 1998).
Flows from upstream to downstream, or from downstream to upstream
There are many resources that flow along the fluvial network in an upstream or downstream direction. The most
obvious example of an upstream-directed flow would be spawning salmon (as above) returning from the oceans and
delivering large amounts of nutrients and energy to streams (e.g. Bilby et al., 1996). Marine-derived nutrient fluxes
can be crucial resources for sustaining productivity and influencing biodiversity of the recipient ecosystems by
enhancing trophic pathways in oligotrophic freshwaters (Rand et al., 1992; Wipfli et al., 1998; Zhang et al., 2003).
These sorts of upstream (and downstream) flows can also be found for other spawning fishes, eels, palaemonid
prawns and other crustaceans.
Flows of resources downstream are more common. Fine particles of organic matter are produced by the activities
of many organisms, often by breaking particles down or concentrating them during their feeding, referred to as a
processing chain (Heard and Richardson, 1995). Malmqvist et al. (2001) demonstrated enormous masses of fine
particles in streams generated as faeces by filter-feeding organisms that are subsequently transported downstream
to other consumers. Some of this organic material (all particle sizes) reaches estuaries and can subsidise local
productivity there (Sakamaki and Richardson, 2008).
Small streams are numerous across the landscape, and are often underappreciated and frequently unmapped
(Gomi et al., 2002; Richardson and Danehy, 2007). However, small streams may contribute large masses of organic
matter and invertebrates to downstream reaches where they could be available to consumers, such as salmonid
fishes (Wipfli and Gregovich, 2002). These subsidies may be crucial to downstream consumers and potentially
provide a large portion of the energy that fuels food-webs of larger streams (Wipfli et al., 2007).
Lake outlets
Lakes and streams differ strongly in the types of organisms and the relative importance of particular kinds of
processes, and this results in a clear demarcation between these systems. High densities of filter feeding animals are
found in streams at the outflows of lakes, putatively because of the high concentrations of high quality food in
seston delivered in the outflow (Richardson, 1984; Richardson and Mackay, 1991). In this sense the planktonic
organisms from picoplankton to ‘net’ plankton sizes contribute a subsidy to receiving streams, as these organisms
Copyright # 2009 John Wiley & Sons, Ltd.
River. Res. Applic. (2009)
DOI: 10.1002/rra
J. S. RICHARDSON, Y. ZHANG AND L. B. MARCZAK
are not generally abundant in running waters unless water residence time is long. This particular interface has been
described many times, but still awaits critical tests of how much the resource subsidy, as opposed to the uniqueness
of the physical processes, is responsible for the characteristic community found at outflows of lakes.
Benthic-pelagic coupling in lentic systems
Another example that fits here, but stretches the idea of ‘across ecosystem boundaries’ is the importance of
benthic–pelagic coupling in lakes. There is a large literature regarding the reciprocal flows of materials and
organisms between the benthos and pelagic zones of lentic systems, which we will not attempt to summarize.
Linkages at the community level
Knight et al. (2005) demonstrated that the presence of predacious fish in aquatic systems could lead to a trophic
cascade in adjacent riparian ecosystems by suppressing the numbers of adult dragonflies. The numbers of dragonfly
larvae can be suppressed directly through fish predation or indirectly through behavioural modifications resulting in
fewer dragonfly adults. Such fish predation on dragonfly larvae indirectly facilitates terrestrial vegetation
reproduction, because insect pollinators were released from the predation pressure of dragonfly adults. Hence, the
numbers of pollinators were higher in riparian zones of fish-bearing ponds, where plants received more pollinator
visits than plants near fish-free ponds (Knight et al., 2005). Similarly, Ngai and Srivastava (2006) demonstrated that
aquatic communities in epiphytic bromeliads containing damselflies had lower rates of emergence of adults of
detritivorous insects (chironomids, tipulids, scirtids). As a consequence of a difference in communities the type and
rates of subsidies to the terrestrial environment constrained by the presence or absence of predators in the aquatic
system. These examples indicate that strong biotic interactions between species can reverberate across ecosystem
boundaries through consumer flows.
DO ECOSYSTEM BOUNDARIES REGULATE THE TRANSFER OF RESOURCE SUBSIDIES?
Natural ecosystems are patchy mosaics of different habitats, which are defined by their boundaries (Addicott et al.,
1987). These boundaries are complex and multidimensional (Cadenasso et al., 2003), are functions of ecosystem
size, and are often affected by isolation and habitat destruction. Fluxes of materials and nutrients move across
ecosystem boundaries through multiple mechanisms, including gravity, diffusion, deposition and drift
transportation, surface-ground water exchange, wind and animal movement. Terrestrial invertebrate prey inputs
to streams differed in deciduous and coniferous forest (Romero et al., 2005) as do the quantity and quality of leaf
material and consequent responses by aquatic invertebrates (Richardson et al., 2004). Although there is evidence
that the physical and biological structure of edges and permeability of boundaries can affect cross-system transfer
rates of resource subsidies, we lack general principles (Cadenasso and Pickett, 2001; Cadenasso et al., 2003;
Marczak et al., 2007a). Are pulsed subsidy inputs from different matrix habitats less efficiently used than the same
amount of constant addition of allochthonous resources (Marczak and Richardson, 2008)? Are coupled systems
more productive than two decoupled systems? What are the consequences of resource pulses on local resources in
streams? There are few empirical studies to answer these questions. However, using experimental stream channels,
Zhang et al. (2003) found that deposition of salmon carcasses temporarily decoupled the consumer-detrital
resource relation as salmon carcasses attracted invertebrate detritivores (larval caddisflies) away from leaf litter
processing. However, when the carcasses vanished from the stream habitat, those large detritivores switched back
to leaf litter, accelerating litter processing. Thus, in the long-term the resource subsidy pulse enhanced local
resource consumption.
NEW DIRECTIONS
Coupling ecosystem dynamics through complex life cycles and behaviour
Earlier we noted in our definition of subsidies that their flux must be donor-controlled, and that active foraging
across ecosystem boundaries was outside of our definition. In the case where a consumer has direct access to
Copyright # 2009 John Wiley & Sons, Ltd.
River. Res. Applic. (2009)
DOI: 10.1002/rra
RESOURCE SUBSIDIES ACROSS THE LAND–FRESHWATER INTERFACE
resources in another ecosystem, the resources are not donor-controlled and there is active sequestration of resources,
and therefore they are not subsidies. This direct, active linking of foodwebs can be considered a form of biological
pump. For instance, a very large number of riparian species feed directly on aquatic organisms. Species such as
piscivorous birds (e.g. loons, mergansers, osprey, etc.) and benthivorous species (e.g. dippers, water shrews,
harlequin ducks, etc.) directly link foodwebs of adjacent ecosystems (e.g. Feck and Hall, 2004). We are not aware of
many examples of aquatic organisms foraging actively out of the water, but archer fish, some crayfish and some
limnephilid caddisflies that forage on stream banks at night, might be examples of these. Therefore, in the case of
cross-ecosystem foraging behaviours these consumers are not equivalent to recipients dependent on resource
subsidies because many of the former species are obligates on resources in the other ecosystem and have no resources
in their own ‘ecosystem’ (e.g. piscivorous birds). The distinction between these two mechanisms, i.e. subsidies versus
active foraging across boundaries, may need refining if there are different consequences for recipient populations.
A number of consumers place themselves spatially within habitats to be the first recipients of certain flows, a
strategy that has been called trophic interception (Marczak et al., 2007a). One can think of species such as water
striders, gerrids and notonectids at the water–air interface as primed to pre-emptively capture prey as they intersect
the ecosystem boundary. The evolution of guilds of consumers poised to exploit resource subsidies suggests that
competition for access to resource subsidies occurs. Recipient populations farther down the resource chain may be
dependent on these opportunistic consumers of subsidies to either promote or limit the movement of the subsidy
further into the recipient ecosystem. We still have relatively few empirical studies of the relation between timing,
magnitude, duration and quality of resource subsidies and the scope for consumers to take advantage (growth,
reproduction, survival rate) of potentially short-lived resource pulses (Takimoto et al., 2002; Holt, 2008; Marczak
and Richardson, 2008). The consequent dynamics of consumer populations and guilds is even less studied.
The question of the consequences of subsidy flows for recipient populations and the communities within which
they exist provides much room for new study. There are many scaling issues with respect to press experiments of
duration shorter than a single generation time of most consumers. Among the best examples of a press experiment
of subsidies to flowing waters is Wallace et al.’s (1999) long-term study of consumer populations and ecosystem
processes following the experimental cessation of the inputs of leaf litter to a small stream. More press
manipulations of subsidy resource flows for time and spatial scales appropriate to questions about population and
community consequences are needed to test theory as it is developed.
Dynamical consequences
The most obvious direction, as outlined above, is to provide studies where the dynamical consequences of
particular kinds and rates of flows can be demonstrated for recipient systems. Although consumer-resource
dynamic theory has been developed for donor-controlled systems (Polis et al., 1997; Holt, 2008), there has been
limited experimental work rigorously applied to consumers associated with aquatic ecosystems. Well-controlled
experiments modulating the rates of cross-ecosystem fluxes (magnitude, pulse duration, etc.) are necessary to test
these models and examine the dynamical outcomes for consumers and their local prey.
Pulses of resource subsidies across ecosystem boundaries may be stabilising or destabilising of consumer
population dynamics, and this depends in part on the scaling of the duration and magnitudes of the subsidy relative
to the life cycle of the consumers, which can cause plastic community responses (e.g. Holt, 2008). Whether or not
subsidies are stabilising may also depend on what other in situ resources are available to consumers. Some species
have substitutable resources, such as biofilms consumed by detritivores (Ledger and Hildrew, 2001), which may
support them through periods when subsidy resources are scarce. Whether allochthonous inputs of energy would
stabilize food webs and influence species diversity in the recipient systems remains unclear.
Many consumers have complex life cycles whereby they inhabit different ecosystems during different
ontogenetic stages, e.g. many aquatic-breeding amphibians and most aquatic insects. These organisms themselves
provide subsidies across ecosystem boundaries, as the examples above illustrate. However, the dynamics of these
populations affect community dynamics in both (or more) ecosystems they inhabit (e.g. Schreiber and Rudolf,
2008). To date there has been very little empirical work dealing with the propagation of population dynamical
signals into adjacent ecosystems (e.g. Knight et al., 2005), although theoretical work has begun to consider this
(e.g. Loreau and Holt, 2004; Holt, 2008).
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These are donor-controlled systems, but do recipient populations demonstrate adjustments of life cycle
phenology to capitalize on these resource flows? Is there enough phenotypic plasticity to take advantage of shortterm pulses when available (Marczak and Richardson, 2008)? It appears that there is a tremendous scope for taking
advantage of resource pulses when they are available, in terms of growth rates, survival and reproduction. Whether
life cycle timing has evolved to optimize use of subsidies depends on the reliability of timing and magnitude of
flows, and the relative contributions of subsidies compared to local resources, a topic that may be amenable to modelling.
Are there costs to the donor system? Subsidy export to a recipient system suggests a loss to donor systems
(Loreau et al., 2003; Marczak, 2007). Such loss may not directly influence community dynamics in the source
habitat. However, the across boundary feedback from the recipient habitat may indirectly affect community
dynamics in the donor habitat (Loreau et al., 2003). Reciprocal, but temporally offset, flows of resources have been
illustrated, although these are probably special cases (Nakano and Murakami, 2001; Takimoto et al., 2009), and not
a necessary condition to be considered subsidies. These coupled systems are linked in ways that indicate the
dynamics of each are not independent, a theme frequently found in the literature.
Is food web stability influenced by nutrient and energetic resource subsidy? Huxel and McCann (1998) modelled
a tritrophic food chain model (a detrital-consumer-predator chain) with different input levels of allochthonous
energetic resources. They found that food web stability in recipient ecosystems tend to be increased at low to
moderate levels of allochthonous resource inputs. Increasing preference for the resource subsidy can stabilize first
and later destabilize the original food chain. At high levels of allochthonous resource inputs, the food chain tends to
be decoupled by weakening trophic cascades to trophic trickles (McCann et al., 1998) so that the food web could be
destabilized by losing one or all species. These theoretical modelling results need to be examined in real food webs
in the field.
Are subsidies ubiquitous? Probably yes, but their relative importance may vary among different systems, and life
cycle evolution of recipient consumers may result in these resource flows being more critically important to some
than others. This is not true only for low-productivity recipient systems (Marczak et al., 2007b), although it is
certainly easier to measure there. Donor system productivity certainly influences the quantity of subsidy that is
available to be transported between systems and the magnitude of the interaction between adjacent habitats. For
example, intraguild predation by aquatic vertebrate predators (fish) on invertebrate predators with terrestrial adult
stages (such as dragonflies or damselflies) may indirectly increase terrestrial to aquatic subsidies by releasing
terrestrial invertebrates from predation (Knight et al., 2005). There is potential for greater amounts of terrestrial
invertebrates to fall on the surface of streams, or for enhanced terrestrial plant production (when pollinators are
released from predation) to be redirected to streams, eventually enhancing secondary production within aquatic
habitats. Thus, there can be indirect interactions that reciprocally couple dynamics across habitats.
There are large qualitative differences in the types of resource subsidies. Those studying the roles of leaf litter
inputs to aquatic systems know that leaf quality, in terms of chemistry and structure, strongly influence breakdown
rates and support of consumer growth. Similarly, other resources vary as well and distinctions within categories of
resource subsidies may be worthwhile. For instance, the type of terrestrial insects falling to a stream (e.g. adult
beetles versus Lepidoptera larvae) may matter to a fish or other consumer, and might affect growth rates.
Are there potential negative effects of nutrient and energy fluxes (i.e. not subsidies in their consequences) on the
recipient ecosystem? That may depend on the source of organic components and their concentration in a subsidy.
Allochthonous leaves fallen into water bodies make a significant contribution to DOC (Meyer et al., 1998). Leaf
litter can contribute 30% of total DOC in streams (Kamara and Pflugmacher, 2008). Some leachate chemicals from
leaf litter may influence aquatic biota through exerting chemical stress, such as imposing oxidative stress (Steinberg
et al., 2006). As the major component of DOC, dissolved humic substances (DHS) may have direct and/or indirect
impact on aquatic organisms by affecting biochemical and biogeochemical pathway (Timofeyev et al., 2004). DHS
can have positive effect on freshwater ecosystems by supplying carbon (energy) to fuel the heterotrophic
components (Steinberg et al., 2006). On the other hand, DHS can bind to a variety of organic compounds and form
complexes with some metals, which reduces DHS’s bioavailability (Kamara and Pflugmacher, 2008). The
ecological consequences of DHS on freshwater food webs and ecosystem processes remain in need of further
experimental investigation.
Another topic in which river science has done well is in extending the ideas of resource subsidies to a landscape
and regional heterogeneity context, and more specifically to stream networks (Gomi et al., 2002; Grant et al., 2007).
Copyright # 2009 John Wiley & Sons, Ltd.
River. Res. Applic. (2009)
DOI: 10.1002/rra
RESOURCE SUBSIDIES ACROSS THE LAND–FRESHWATER INTERFACE
The quantitative contributions of flows from headwaters to downstream, and the spatial scaling of those flows, have
been estimated for some streams (Wipfli and Gregovich, 2002). The consequences for downstream consumers are
predicted to be large, but the direct evaluation of this for consumer population dynamics remains a challenge
(Wipfli et al., 2007). It is clear that spatial flows of materials and organisms can affect the functioning of local
ecosystems. Physical mass-balance constraints interacting with biological demographic constraints may play an
important role in the regulation of ecosystem functioning (Loreau and Holt, 2004).
There is no doubt that freshwater science has made a large contribution to the development of ideas related to the
rates and consequences of cross-ecosystem resource subsidies in spatial ecology. There are many questions still to
address, and aquatic scientists have systems and methods that are amenable to testing of these ideas from local to
regional scales. Challenges such as identifying the consequences of the timing and magnitude of subsidies on
population and community dynamics and the evolutionary response of life history timing relative to subsidy timing
and rates in freshwater systems should keep aquatic scientists occupied for decades to come.
ACKNOWLEDGEMENTS
The authors appreciate the invitation by Alexander (Sandy) Milner and Klement Tockner to participate in this
special session at the 2008 meeting of the North American Benthological Society. The authors are grateful for the
helpful comments of the reviewers. They thank Eric Leinberger for preparation of the figure. Their apologies to all
those authors that have contributed to this topic and that they did not have space to cite. They are grateful for the
support of their research through the Forest Sciences Program (BC).
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