Terrestrial-Aquatic Linkages: Understanding the Flow of Energy and Nutrients across Ecosystem Boundaries

Artwork by USFS

Adam Hansen, Justin Peterson, Jeremy Ellis, Ginny Sednek, and Ben Wilson
Department of Fish, Wildlife, and Conservation Biology Colorado State University Fort Collins, Colorado 80526
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Abstract. The importance of aquaticterrestrial linkages has been well established in a variety of ecosystems. Marine subsidies support high primary consumer production, which sustains dense supralittoral secondary consumers. Terrestrial invertebrate inputs play important roles in streams. Depending on the season, invertebrates falling into a stream can make up as much as 50% of the annual consumption in some fish species. Similarly, emerging aquatic insects can comprise up to 90% of a riparian predators diet. The timing of both aquatic and terrestrial emergence can be crucial for food web sustainability. Anadromous salmon act as a vector for the transport of marine derived nutrients inland. Finally, subsidies can promote sustainable populations in low productivity terrestrial systems, or even be transported by migratory birds thousands of miles to the detriment of various lakes, ponds, and rivers, if overabundant. Adjacent ecosystems rarely function independently of each other, even those that appear to have discrete boundaries (Barret et al. 2005). For example, terrestrial and aquatic habitats interact extensively, with each system being inherently linked by the cross-habitat transfer of energy or nutrients (Ince et al. 2007). This flux of organic matter or nutrients from a donor habitat to a recipient habitat is known as an ecological subsidy (Polis et al. 2004; Ince et al. 2007). These subsidies typically have high temporal and spatial variation, can enter recipient habitats at any trophic level, can have dramatic influences on food web dynamics (e.g., competition), and can be transported through the movement of organisms (Polis et al. 2004). The goal of this paper is to review the current state of knowledge about the specific mechanisms driving the flow of energy and nutrients between different aquatic and terrestrial systems. 2

Trophic interactions at the land-sea interface: importance of food web linkages By Adam G. Hansen The land-sea interface or coastal ecotone (e.g., estuaries) is a major ecosystem encompassing 8% of the earths surface along an estimated 594,000 km of shoreline (Polis and Hurd 1996; Polis et al. 2004). Carbon and nutrients flow extensively across this ecotone boundary (i.e., subsidies), forming a complex food web (Vernberg and Vernberg 2001; Polis et al. 2004). Coastal zones are sites of significant human degradation (Kappel 2005), and conservation requires scientists to understand trophic interactions between these ecosystems (Pasquaud et al. 2007). The goal of this paper is to describe the primary mechanisms through which marine and adjacent terrestrial habitats receive subsidies, and their importance. Marine subsidies enter terrestrial systems through shoreline drift of animal carrion and detrital algae, the import of carcasses, food scraps, reproductive byproducts, and waste products (e.g., guano) from ocean foraging seabirds (e.g., cormorants and gulls), sea turtles, and pinnipeds (e.g., sea lions), and from windblown sea foam and spray (Polis et al. 2004; Ellis et al. 2006).

Detrital algae. Photo by Joseph Dougherty.

For example, Polis and Hurd (1996) estimated the ocean to contribute 2,720 2,810 g dry massm-2yr-1 and 110 530 g dry massm-2yr-1 of shoreline plant detritus and animal carrion (e.g., seabirds, fish, and crabs) to small, unproductive (< 100 g dry massm-2yr-1), desert islands in the Gulf of California, respectively. These subsidies support high primary consumer production (e.g., detritivorous arthropods), which sustains dense populations of supralittoral, arthropodivorous consumers (e.g., spiders, scorpions, and lizards) on small islands (low perimeter/area ratio) and in coastal areas worldwide (Polis and Hurd 1996; Anderson and Polis 1998). Polis and Hurd (1995) describe how supralittoral spiders achieve densities six times greater than inland counterparts, and increase further (4 5 times) on islands with seabird colonies due to the addition of avian parasites and scavengers to the food web (Figure 1).

(Gulf of California) spider and scorpion tissue having significantly greater levels of marine-derived 13C and 15N. Marine subsidies are important for carnivorous mammals (Polis and Hurd 1996). For example, Rose and Polis (1998) measured coyote Canis latrans density to be 2.4 13.7 times greater along the Gulf of California coast than in adjacent inland habitats receiving no marine input. Carlton and Hodder (2003) describe how mammals (e.g., raccoons, minks, and black bears) have been observed, worldwide, intentionally entering intertidal communities to prey on exposed marine organisms (e.g., gastropod mollusks, crabs, and fish). These mammals ultimately act as vectors for the transport of marine-derived nutrients inland (Carlton and Hodder 2003). Conversely, coastal marine systems receive terrestrial subsidies (nutrients, particulate and dissolved organic carbon) indirectly from river discharge and directly from supralittoral vegetation (Polis et al. 2004). Terrestrially-derived carbon, nitrogen, and phosphorus, delivered by rivers, stimulate in situ phytoplankton and benthic microalgal production, both being important drivers of coastal marine food webs and fish production (Loneragan and Bunn 1999).

Figure 1. Food web of small, desert islands in the Gulf of California. Arrows denote carbon and nutrient flow from one ecosystem component to another. The horizontal dotted line represents the land-sea interface (from Polis and Hurd 1995).

Lastly, Anderson and Polis (1998) provide direct evidence (stable isotopes) for coastal consumers exhibiting greater marine-based diets than inland individuals, with coastal 3

Lower estuary of Columbia River. Photo by Jim Wark.

Loneragan and Bunn (1999) found there to be strong, positive relationships between commercial fisheries catch (prawns, mud crabs, and mullet) and summer discharge from the Logan River, southeast Queensland, Australia, strengthening the argument for conserving natural flow regimes. Dunton et al. (2006) describe how nutrient and terrestrial detritus accumulation from arctic river input (e.g., Mackenzie River) can comprise 54 69% of the total particulate carbon available to consumers, in lagoon-barrier island systems, along the Alaskan Beaufort Sea coast (Figure 2). Based on stable isotopes, arctic cod inhabiting these lagoon systems were found to derive 52 85% of their carbon from terrestrial sources (Dunton et al. 2006).

provided evidence for the juvenile salmon forming a trophic hierarchy, partitioning marine and terrestrial-derived resources. It was concluded that subsidies derived from supralittoral vegetation may allow coexistence in resource limited marine habitats (Romanuk and Levings 2005). Carbon and nutrient flow between the land and sea occurs in both directions. Input of material from sea to land increases primary consumer production, allowing secondary consumers to achieve densities that would otherwise be unattainable without such subsidies (Polis and Hurd 1996). Terrestrial-derived subsidies contribute large amounts of carbon and nutrients to the sea, making coastal marine systems the most productive ocean habitats (Polis et al. 2004). Each system is greatly influenced by the other, and conservation efforts must recognize that coastal marine and terrestrial habitats are integrated, not discrete biological communities. Terrestrial-aquatic linkages: terrestrial invertebrate inputs into stream systems By Justin Peterson Stream systems have been studied historically by examining the organisms and processes that are restricted to the stream. Terrestrial inputs supplement streams that have low autochthonous production (Vannote et al. 1980), and influence carbon pathways in the system (Rosenfield and Roff 1992). More recent developments show the importance of terrestrial inputs into streams in terms of food webs within and outside of the stream (Nakano et al. 1999), as well as research applications (Nakano and Murakami 2001; Saunders and Fausch 2007). Terrestrial stream inputs are crucial links that provide fish forage (Kawaguchi and Nakano 2001), and can control the distribution of fishes in the stream (Kawaguchi et al. 2003). The following discusses terrestrial inputs into stream 4

Figure 2. Major factors accounting for the high productivity and biomass of estuarine inhabitants in northern Alaskan coastal ecosystems (from Dunton et al. 2006).

Supralittoral vegetation is an important source of carbon (terrestrial insects and leaf litter) for coastal marine fish (Polis et al. 2004). Fish species richness and arthropod addition are both positively associated with supralittoral vegetation (Romanuk and Levings 2003; Romanuk and Levings 2006). Based on stable isotopes, Romanuk and Levings (2005) estimated juvenile Pacific salmon (Chinook, chum, and pink) to derive 5.5 39.7% of their carbon from supralittoral vegetation sources along the coast of British Columbia. Results

systems, highlighting the importance of the riparian area, as well as invertebrate inputs. Fish are dependent on terrestrial inputs in various settings, and the importance of terrestrial inputs into streams has been well established. Drifting and falling invertebrates make up a large portion of salmonid diets and may determine their distributions in a stream system (Kawaguchi and Nakano 2001). Overall, invertebrates made 51% of the total annual prey consumption in forested streams, and 35% of total annual prey consumption in a grassland reach (Romanisyn et al. 2007). Differences are also observed in terms of riparian type and terrestrial input in a variety of streams (table 1 from Baxter et al. 2005).

The highest inputs are observed in closed canopy rivers and can make up approximately 50% of salmonid diets in those stream sections (Kawaguchi et al. 2003; Baxter et al. 2005). Differences in invertebrate input as a result of differing riparian vegetation and cover were observed in several studies (Dineen et al. 2007; Romanisyn et al. 2007). Terrestrial invertebrate supply can be influenced by riparian type. Drifting terrestrial invertebrates were highest in open-canopy streams (Dineen et al. 2007), and falling invertebrates highest in forested closed canopy streams (Romanisyn et al. 2007). Carbon pathways are also linked to terrestrial inputs.

Table 1. The differences of stream order, riparian type, and terrestrial input in a variety of streams in the spring, summer, fall, and winter (from Baxter et al. 2005). Values for terrestrial invertebrate input represent mean dry mass (mg m-2 day-1). Starred values represent fields with no data.

Rosenfield and Roff (1992) examined the carbon pathways in forested and unforested stream systems using carbon isotopes that differ based on origin in a terrestrial setting or in the stream. Results showed fish derive higher amounts of carbon from terrestrial inputs in forested stream sections (Rosenfield and Roff 1992). Food web dynamics can also be dependent on terrestrial subsidies. Terrestrial invertebrate inputs can have cascading impacts for the entire ecosystem food web in a headwater stream (Nakano et al. 1999). When terrestrial inputs were blocked from the channel, certain fish species shifted to forage on aquatic invertebrates, and the reduced grazing from those invertebrates led to an increase in benthic periphyton. Maintaining overhanging riparian vegetation and banks is crucial for invertebrate input for foraging fish species (Nakano and Murakami 2001; Romanisyn et al. 2007). Nakano et al. (figure 1 1999) relates the importance of terrestrial invertebrates in a forest stream system showing darker bars for those species that rely on terrestrial inputs.

Knowing the importance of terrestrial inputs helps can help identify streams that might be negatively affected as a result of reduced terrestrial linkages. Land use practices can negatively affect potential terrestrial inputs by interfering or changing riparian vegetation structure (Edwards and Huryn 1996). Saunders and Fausch (2007) examined the consequences of removed riparian vegetation by cattle grazing and showed that prolonged grazing reduces riparian vegetation, invertebrate input, and trout biomass. Ungrazed areas inside exclosures had higher numbers of juvenile Oncorhynchus mykiss, and relate the importance of intact riparian vegetation (Bayley and Li 2007).

Barrier used by Nakano and Murakami 2001. Figure 1. Food web illustration of a forest stream showing allochthonous invertebrate subsidies (modified from Nakano and Murakami 2001). Bar thickness is indicative of annual resource budgets of each fish species from terrestrial prey.

Seasonality can affect the timing of invertebrate input into streams, and affects forage availability (Edwards and Huryn 1996; Nakano and Murakami 2001; Baxter et 6

al. 2005; Romanisyn et al. 2007). Seasonality is important for terrestrial insect inputs in the form of drift, or fall into the stream system. Terrestrial input is highest in the summer months, (table 1 from Baxter et al. 2005), and seasonal differences in invertebrate inputs can also be seen (figure 2 modified from Nakano and Murakami 2001).

Terrestrial inputs are a crucial link for food webs, and maintaining natural ecosystem processes in streams. Overhanging riparian vegetation also ensures invertebrate inputs. Depending on the fish assemblage, disruption of inputs will alter food webs, and may result in a trophic cascade. Interrupting the input can disrupt entire food webs, forcing fish to focus on aquatic prey, leading to shifts in stream production. Sources that disrupt riparian vegetation alter these inputs, and threaten natural stream ecosystem functions. Emerging Insects: Trophic Interactions of Terrestrial and Aquatic Systems By Jeremy Ellis Emergent insects are an important food source for riparian predators (Lynch et al. 2002). Characteristics of these insects make them susceptible to high predation at certain times of the year. In some instances emerging insects can make up to 90% of a predators diet (Kato et al. 2004). Emergent insects are an important subsidy to birds, lizard and spiders (Burdon and Harding 2008). This paper will show how emerging insects disperse and how predation of these insects is an important subsidy to terrestrial predators like birds, lizards and spiders. Emerging aquatic insects have life history traits that make them susceptible to predation all year or at certain times of the year. These insects spend most of their life underwater and emerge as adults to breed and lay eggs back into the water. Ephemeroptera (mayflies), Plecoptera (stoneflies) and Trichoptera (caddisflies) (EPT) usually emerge in May-June in temperate regions. Diptera (true-flies) mostly emerge in the warmer months. In tropical regions emergence can be year round (Baxter el al. 2005). Emerging insects can average about 10,000-20,000 insects per meter (m) per year. These insects disperse above and 7

Figure 2. The allochthonous prey consumption of a fish assemblage from a forested stream for a 12-month period (modified from Nakano and Masashi Murakami 2001).

Increased allochthonous prey reliance occurs in the spring, peaks during the summer, and declines to the lowest occurrence in the winter. Input timing is also important due to the reduced occurrence of aquatic invertebrate availability during the times of high terrestrial input (Nakano and Masashi Murakami 2001).

Pan trap. Photo by Carl Saunders.

around the stream in order to feed, rest, breed, and disperse eggs.

Adult mayfly Ephemeroptera. (Phil Myers).

Lateral dispersal for emerging insects is important to understand how predators will react to their dispersal. This dispersal is usually to feed or is a mechanism to colonize new habitats (Malmqvist 2002). Some species of stoneflies marked with stable isotope 15N flew up to 1 km from their natal stream. But most emerging insects are found within 11 m of the stream (Winterbourn et al. 2007). Using Malaise traps, Winterbourn el al. (2007) found that about 7% of Ephemeroptera and 43% of Trichoptera migrated away from the stream into the entire valley or the surrounding hillsides (Table 1).
Table 1. Abundance (%) of insects Ephemeroptera, Plecoptera and Trichoptera trapped in forest, valley and hillside. Forests are closest to streams and hillsides are farthest from streams (from Winterbourn et al. 2007).

Ephemeroptera Plecoptera Trichoptera Likewise Lynch et al (2002) found

Forest Valley Hillside 90.2 2 7.8 91.9 6.2 1.9 56.7 36.3 7

that emerging insect abundance decreases exponentially farther from the waters edge. But this study shows that about 50 insects per m per day were moving into the riparian zone 15 m from stream center. This movement is important to understand because 8

when the insects leave the relative safety of the water they encounter new predators in the riparian areas. Aquatic insects are very important to spiders because the insects can provide a bulk of a spiders diet. Spiders, both web-building and ground dwelling, have been shown to have a higher biomass near a stream edge, and web densities increase near a stream where aquatic insect biomass is high, and decrease with distance from the stream (Baxter et al. 2005, Burdon and Harding 2008, and Sanzone et al. 2002) (Figure 2). Likewise, when the number of emerging insects was experimentally decreased, spider density near the stream declined (Burdon and Harding 2008). Using stable isotopes to measure the amount of carbon from aquatic origin, Kato et al. (2004) found that in June, the peak of emergence, 13C was most depleted, similar to aquatic prey. When emergence declined in July, 13C in spiders became more similar to terrestrial prey. Prey in orb-webs was 50-90% aquatic insects in May-June in the same area (Kato et al. 2003). This information shows that spiders can be dependent on emergent insect subsidies and respond to the densities of emerging insects, comparable to birds. Iwata et al. (2003) showed that abundance of flycatchers and gleaners was positively correlated to aquatic insect abundance in the riparian area. This was also observed in a prairie stream by Gray (1993). Gray (1993) also observed that when the stream dried and there was no emergence during a drought in 1989 densities of flycatchers and gleaners was greatly reduced. When the stream was flowing there were 11 birds/ha, and when the stream was dry there was about 2 birds/ha. This could be due to multiple factors but lack of asubsidy from the stream is one of them. Flycatchers fed above the stream or within 5 m of the stream. Dry mass of flycatchers diets is 82% aquatic insects due to this behavior (Iwata et al.

2003). Gleaners also show this behavior and had 67% of their diets composed of aquatic insects (Iwata et al. 2003). For these birds, emerging aquatic insects are a large part of their diet making emergence a very important factor for their food web.

Overall emerging insects have a large effect on the surrounding system. They influence predator movement and cause shifts in feeding habits during emergence. These subsidies cannot be overlooked because so many species depend on them to survive. Emerging insects connect terrestrial and aquatic environments by moving energy from streams to land. The impact of anadromous salmon on aquatic and terrestrial ecosystems By Ginny Sednek Anadromous salmon and trout (Oncorhynchus spp. and Salmo spp.) transport large magnitudes of nutrients to aquatic and terrestrial habitats. Ninety-five percent of the biomass of ocean migrating salmon is marine derived nutrients, (MDN), including carbon, nitrogen, and phosphorous (Naiman et al. 2002). The organic subsidy brought to freshwater habitats positively impacts food webs (Schindler et al. 2003) and biological productivity (Figure 1). The nutrients salmon provide to aquatic ecosystems are beneficial to fish, aquatic invertebrates, salmon eggs, and riparian habitats. Migrating salmon have an immense value to adjacent terrestrial ecosystems; transferring energy to the land which sustains wildlife and forests. Over the past century, salmon returning to spawn in their native freshwater habitats has decreased to 6-7% of their historic abundance (Gresh et al. 2000). Conservation of salmon are important to consider for biological productivity because of the ecological cascade that follows. Here, I review the importance of anadromous salmon in freshwater aquatic and terrestrial ecosystems. The benefit of salmon extends across habitat boundaries. Terrestrial ecosystems increase fish survival (cover, shade, nutrients, etc.) and anadromous salmon return to the same forested areas to reproduce and deposit 9

Figure 2. Linear relationship between spider densities (no. webs*m3) and emerging insect biomass (g*m2 of stream) (From Burdon and Harding 2008).

Emergent insects provide a subsidy for riparian lizards as well as birds and spiders. Sabo and Power (2002) show that when the aquatic insect subsidy is experimentally blocked from lizards, the lizards growth is lower when compared to unblocked lizards. The aquatic insects had effects on lower trophic levels as well. When emergence occurs, lizards tend to shift from terrestrial prey to emerging aquatics. This reduces pressures on terrestrial insects for a short time (Sabo and Power 2002).

Western fence lizard Sceloporus occidentalis. (Jim Boone Photo).

Figure 1. The effects of anadromous salmon, containing marine derived nutrients (MDN), on biological productivity in aquatic and terrestrial ecosystems (From Cederholm et al. 1999).

rich nutrients (Cederholm et al. 1999). The energy salmon transfer to oligotrophic systems consists of carbon, nitrogen, and phosphorous, positively impacting the biological communities (Gende et al. 2002). This nutrient subsidy enters the trophic system directly (consumption of flesh, eggs) and indirectly (dissolved nutrients) (Naiman et al. 2002). Energy from salmon becomes a part of different trophic levels, starting in riverine habitats and proceeding to inland forests. Salmon play important roles in riverine ecosystems. When salmon return to their natal streams they spawn, die, and create an abundant source of nutrients for fish and aquatic invertebrates (Cederholm et al. 1999). Other salmonids and fish species gain

an ample supply of nutrients when salmon spawn, by consuming carcasses, eggs, and fry (Gende et al. 2004). Aquatic invertebrates are also attracted to the vast amount of organic matter. Winder et al. (2005) discovered that the lifecycle of certain caddisfly species in southwest Alaska coincided with salmon runs. These aquatic invertebrate larvae also become a food source for other fish and wildlife (Cederholm et al. 1999). The habitat that surrounds riverine systems, the riparian areas, also benefits by the energy subsidy. Ben-David et al. (1998) studied the effects of salmon carcasses fertilizing riparian vegetation in southeast Alaska; their findings show how flooding and predator activity moves nitrogen-rich nutrients into the riparian zone.

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Spawning salmon help the development of their eggs and fry, allowing their species to thrive. According to Schindler et al. (2003), when female salmon build redds (nests), the sediment composition is altered, increasing water and oxygen flow (benefits developing eggs), while removing fine sediments. Dead adult salmon also provide nutrients for salmon fry, increasing growth rates and survival (Cederholm et al. 1999). The nutrients adult salmon provide enter a feedback loop, helping the survival of its own species. Wildlife communities adjacent to salmon run systems are heavily dependent on the abundance and availability of salmon. The nutrients salmon provide help the survival and reproduction of a variety of wildlife (e.g., bears, eagles, mink, otters, deer; Willson and Halupka 1995). BenDavid (1997) found that the timing of reproduction in mink (Mustela vison) coincides with salmon spawning so that the female has adequate nutrients for lactation. Female bears with cubs alter feeding habits when salmon are abundant, avoiding salmon streams to reduce infanticide by other bears (Ben-David et al. 2004).

In fall, salmon carcasses are an essential part of mink diets, aiding preparation for winter (Ben-David et al. 1997). Helfield and Naiman (2006) describe how bears and salmon are mutually dependent. Bears benefit from salmon nutrients and fertilize riparian areas (i.e. dragging up carcasses, defecation) which in turn improves riparian habitat for juvenile salmon. Bears can kill 50% of the salmon in small streams, carrying most of the carcasses to the riparian forest, and leaving the remains which enhance wildlife and vegetation (Gende et al. 2004). Salmon are an important resource that move nutrients across habitat boundaries. Conservation of these fishes is imperative for biological communities that rely on salmon rich in MDN. Reduced numbers of salmon has created a nutrient deficit, affecting salmon dependent ecosystems (Gresh et al. 2000). Salmon need to be considered as keystone species because of the extensive effect on many organisms. Understanding the effects salmon have on aquatic and terrestrial communities will allow biologists conserve habitats across physical boundaries. Aquatic subsidies promote viable populations in low productive terrestrial systems By Ben Wilson Typically systems with large amounts of primary production can produce a large amount of available food, which in turn can support greater populations (Odum et al. 1984). Ecologists have long recognized that the dynamics of one system are closely linked to processes occurring in adjacent or even distant environments (Odum et al. 1971). Energy being transported across habitat boundaries from an aquatic area of high primary production to a terrestrial habitat of lower primary production is crucial for an organisms sustainability (Huxel and 11

Photo from Schindler et al. 2003.

McCann 1998). Here I will discuss the connection of various terrestrial organisms preferred habitats and the aquatic systems within those habitats. I will do this by focusing on terrestrial carnivore and omnivore behaviors in very low productive terrestrial habitats that are adjacent to highly productive aquatic habitats. Furthermore, I will also investigate negative subsidy interactions of overpopulated terrestrial organisms on adjacent aquatic systems. Rose and Polis (1998) found while studying desert coyotes (Canis latrans) that aquatic primary production plays a crucial role in the coyotes chosen terrestrial habitat. Primary production from coastal areas was found to be on average 33 times higher than primary production of nearby arid desert habitats. Coyotes also frequented the coastal regions 4.7 times more often.

Fig. 1. The food web shows the Baja California coyote at the center, receiving energy from terrestrial and marine subsidies. The width of the line indicates the percentage of input the coyote receive from each source. (From Rose and Polis 1998)

The scat from these coyotes contained 47.8% of its mass from aquatic subsidies (mostly protein rich animal carrion). Predatory habits of the coyote allows for the highly productive aquatic systems to transfer allochthonous energy to low primary production systems (Polis 2004). 12

Predators benefit directly from aquatic systems by feeding on coastline animal carrion. Do omnivores also capitalize on an increase in productivity? Stapp and Polis (2003) observed higher population densities of mice in the supra-littoral zone, and that capture rates declined the further from the coast the traps were set on islands with no predators. They also suggested that mice were poor conduits for transporting energy inland and spent most of their time close to the coastline. Predators might choose to spend a majority of their time near coastlines not only for aquatic subsidies but also because of an increase in prey populations due to available aquatic subsidies. Both large and small terrestrial organisms have similar chosen habitats not only because of their trophic relationship with each other but also because of the availability of aquatic subsidies. In return both predator and prey benefit from each others presence. The input of marine allochthonous energy is likely to occur around the worlds 594000 km of coastline (Polis and Hurd 1996) (Hammond 1990). Considering that much of the world coastlines actually receive one or two orders of magnitude more marine biomass than that of coastal site in Baja California where these studies took place (Polis and Hurd 1996) we can infer that healthy productive aquatic systems are a key component for the viability of the worlds terrestrial populations. Therefore, protecting marine and freshwater systems should be considered when protecting all terrestrial species. In recent decades lesser snow geese populations have skyrocketed (7% per year) largely because of more food availability via agriculture and a decrease in hunting pressure (Jefferies et al. 2002). The increase in population has proven to be detrimental to their nesting grounds. Instead of typical feeding on above ground forage, the geese are also destructively feeding on roots and

rhizomes. This has converted the Arctic flats into Arctic marshes which have difficulty sustaining secondary invertebrate production (Power et al. 2004). An indirect effect would be the degradation of water quality in nearby aquatic systems. Loss of vegetation would cause an increase in nutrients draining into local lakes, ponds, and rivers. Geese have also been found to directly affect aquatic systems by transporting subsides from other areas. Up to 40,000 geese each year spend their winter in the Bosque del Apache National Wildlife Refuge in central New Mexico. It was estimated that 45%-75% of annual nitrogen and phosphorous for the area came from geese translocation from agricultural fields (Post et al. 1998).

terrestrial environments that are adjacent to highly productive aquatic systems to sustain viable populations. However, if the terrestrial organisms population becomes too large then the aquatic system suffers through negative subsidy exchanges. Therefore terrestrial populations surrounding aquatic systems are sensitive to the dynamics of both terrestrial and aquatic systems. Conclusion Conservation and management requires scientists to understand the trophic interactions between aquatic and terrestrial systems. Marine environments, freshwater environments, and associated terrestrial habitats are directly intertwined by the flux of material. These subsidies can have dramatic influences on population dynamics and food web processes. The greatest impact from subsidies is observed when they flow from productive to unproductive systems. References

Fig. 2 Daily ratios of nitrogen:phosphorous excreted and loaded in the winter and spring of 1994-1995 by lesser snow geese in the Bosque del Apache National Wildlife Refuge in central New Mexico. The average annual nitrogen:phosphorous ratio is shown for comparison (From Stapp and Polis 1998).

Increase of nutrients in an aquatic system can promote blue-green algae blooms. The density of the algae blooms can be lethally toxic to fish and invertebrates and natural restoration is difficult. Degraded water quality paired with eutrophication increases the chance of contagious cholera and type C botulism outbreaks that can threaten the entire ecosystem (Power et al. 2004). In conclusion, terrestrial organisms take advantage of increased productivity flowing as subsides from aquatic systems. Predator and prey populations are also found to increase. This allows for low productive 13

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