Reciprocal Flows of Invertebrate Prey Link Streams and Riparian Zones

Freshwater Biology (2005) 50, 201–220 doi:10.1111/j.1365-2427.2004.01328.x

INVITED REVIEW Tangled webs: reciprocal ﬂows of invertebrate prey link streams and riparian zones

COLDEN V. BAXTER, KURT D. FAUSCH AND W. CARL SAUNDERS Department of Fishery and Wildlife Biology and Graduate Degree Program in Ecology, Colorado State University, Fort Collins, CO, U.S.A.

SUMMARY 1. Streams and their adjacent riparian zones are closely linked by reciprocal flows of invertebrate prey. We review characteristics of these prey subsidies and their strong direct and indirect effects on consumers and recipient food webs. 2. Fluxes of terrestrial invertebrates to streams can provide up to half the annual energy budget for drift-feeding fishes such as salmonids, despite the fact that input occurs principally in summer. Inputs appear highest from closed-canopy riparian zones with deciduous vegetation and vary markedly with invertebrate phenology and weather. Two field experiments that manipulated this prey subsidy showed that it affected both foraging and local abundance of stream fishes. 3. Emergence of adult insects from streams can constitute a substantial export of benthic production to riparian consumers such as birds, bats, lizards, and spiders, and contributes 25–100% of the energy or carbon to such species. Emergence typically peaks in early summer in the temperate zone, but also provides a low-level flux from autumn to spring in ice-free streams. This flux varies with in-stream productivity, and declines exponentially with distance from the stream edge. Some predators aggregate near streams and forage on these prey during periods of peak emergence, whereas others rely on the lower subsidy from autumn through spring when terrestrial prey are scarce. Several field experiments that manipulated this subsidy showed that it affected the short-term behaviour, growth, and abundance of terrestrial consumers. 4. Reciprocal prey subsidies also have important indirect effects on both stream and riparian food webs. Theory predicts that allochthonous prey should increase density of subsidised predators, thereby increasing predation on in situ prey and causing a negative indirect effect via apparent competition. However, short-term experiments have produced either positive or negative indirect effects. These contrasting results may be due to characteristics of the subsidies and individual consumers, but could also result from differences in experimental designs. 5. New study approaches are needed to better determine the direct and indirect effects of reciprocal prey subsidies. Experiments coupled with comparative research will be required to measure their effects on individual consumer fitness and population demographics. Future work should investigate whether reciprocal prey fluxes stabilise linked stream–riparian ecosystems, explore how landscape context affects the magnitude and importance of subsidies, and determine how impacts of human disturbance can propagate between streams and riparian zones via these trophic linkages. Study of these

Correspondence: Colden V. Baxter, Stream Ecology Center, Department of Biological Sciences, Idaho State University, Pocatello, ID 83209, U.S.A. E-mail: [email protected]

2005 Blackwell Publishing Ltd 201 202 C.V. Baxter et al.

reciprocal connections is helping to define a more holistic perspective of catchments, and has the potential to shape new directions for ecology in general.

Keywords: allochthonous inputs, aquatic insects, emergence, food webs, resource subsidies, riparian ecology, stream ecology, terrestrial insects

ecosystem processes. This review begins by descri- Introduction bing characteristics of these prey subsidies, factors Streams and their adjacent riparian zones are ecosys- that affect their flux, and their direct effects on stream tems closely linked by flows of materials and the fish and riparian predators that consume them. We movements of organisms. Ecologists have long recog- then examine empirical and theoretical evidence for nised that these systems are strongly influenced by indirect effects of these allochthonous prey in stream the exchange of organic and inorganic materials like and riparian food webs. We describe how different nutrients, leaves, and woody debris (Likens & indirect effects may be produced by variation among Bormann, 1974; Hynes, 1975). However, recent re- study systems as well as characteristics of experimen- search has focused attention on two direct ‘prey tal designs. We conclude by discussing future subsidies’ (sensu Polis, Anderson & Holt, 1997), research that will be needed for a more complete terrestrial invertebrates that fall into streams and feed understanding of these reciprocal linkages and the fish and the reciprocal flow of adult aquatic insects critical roles they play in stream and riparian systems. that emerge and feed riparian consumers like birds and spiders (Fig. 1). Within both habitats, these Terrestrial invertebrates as prey subsidies for subsidies have effects at individual, population, com- stream fish munity, and ecosystem levels. Most studies to date have focused on the population-level consequences of Although inputs of terrestrial plant matter have been these prey fluxes, but recent work has begun to central to study and theory in stream ecology (Cum- explore their roles in food web dynamics and mins, 1974; Vannote et al., 1980; Wallace et al., 1997),

Fig. 1 A generalised diagram showing reciprocal ﬂows of invertebrate prey and inputs of plant material (dark arrows) that have direct and indirect effects in stream and riparian food webs.

2005 Blackwell Publishing Ltd, Freshwater Biology, 50, 201–220 Prey subsidies link stream and riparian food webs 203 this energy source only indirectly affects higher this prey flux to streams been measured directly. consumers such as fish. In contrast, terrestrial inver- Summer inputs have averaged as high as 111 indi- ) ) ) ) tebrates that fall into streams are a high quality food viduals m 2 day 1 and 223 mg m 2 day 1 (Cloe & source directly available to fish (Mason & MacDonald, Garman, 1996; Table 1). We found three studies that 1982). However, only recently has research focused on measured this flux year-round, yielding estimates of the spatial and temporal variation of these inputs, annual input ranging from 8.7 · 103 and ) ) their use by fish, and their effect on fish populations. 11 · 103 mg m 2 year 1 to small forested streams in Japan (Kawaguchi & Nakano, 2001) and Scotland ) ) (Bridcut, 2000), to as little as 624 mg m 2 year 1 to a Characteristics of terrestrial invertebrate inputs to pasture stream in New Zealand (Edwards & Huryn, streams 1995). Inputs of terrestrial invertebrates to headwater Accounts of terrestrial invertebrate prey in fish diets streams may potentially equal in situ production of are plentiful (e.g. Hunt, 1975), but only recently has benthic invertebrates (Mason & MacDonald, 1982;

Table 1 Flux of terrestrial invertebrates to various streams. For each location-vegetation-season combination, values represent mean ) ) dry mass (mg m 2 day 1).

Terrestrial invertebrate input Riparian Location vegetation Spring Summer Autumn Winter Reference

Headwater streams, Revillagigedo, Coniferous forest * 37.0 * * Wipﬂi, 1997 Alaska, U.S.A. Headwater streams, Coniferous forest * 83.3 * * Allan et al., 2003 Prince of Whales Island, Alaska, U.S.A. Second order streams, Deciduous forest 50.0 450.0 50.0 10.0 Cloe & Garman, 1996 James River drainage, Virginia, U.S.A.† Third order streams, Deciduous forest 78.0 145.0 20.0 4.0 Cloe & Garman, 1996 James River drainage, Virginia, U.S.A.† Sixth order streams, Deciduous forest 5.0 50.0 20.0 <1.0 Cloe & Garman, 1996 James River drainage, Virginia, U.S.A.† Horonai Stream (second order), Deciduous forest * 112.0 * * Nakano et al., 1999c Hokkaido, Japan (1995) Horonai Stream (second order), Mown grassland 8.7 29.9 17.4 0.20 Kawaguchi & Nakano, 2001 Hokkaido, Japan (1995–1996) Horonai Stream (second order), Deciduous forest 14.0 63.3 74.0 <1 Nakano & Murakami, 2001 Hokkaido, Japan (1997–1998) Horonai Stream (second order), Deciduous forest * 41.7 * * Baxter et al., unpublished Hokkaido, Japan (2002) River Arrow (7-m width), Deciduous forest * 107.0 * * Mason & MacDonald, 1982 Herfordshire, Whales Headwater streams, Deciduous forest 21.2 26.8 19.5 1.4 Bridcut, 2000 River Nethy drainage, Scotland†,‡ Headwater streams, Mooreland 5.5 30.0 9.4 1.2 Bridcut, 2000 River Nethy drainage, Scotland†,‡ Sutton Stream, Pasture 3.3 4.9 0.8 * Edwards & Huryn, 1995 Taieri River drainage, New Zealand Headwater streams, Pasture * 1.3 * * Edwards & Huryn, 1996 Taieri River drainage, New Zealand Headwater streams, Tussock grassland * 5.7 * * Edwards & Huryn, 1996 Taieri River drainage, New Zealand Headwater streams, Deciduous forest * 11.6 * * Edwards & Huryn, 1996 Taieri River drainage, New Zealand

*Terrestrial invertebrate input was not measured in these seasons. †Calculated for this paper from data contained in the original work. For Cloe & Garman (1996), summer input averaged ) ) 223 mg m 2 day 1 across stream sizes (see text). ‡Values include adult aquatic insects.

2005 Blackwell Publishing Ltd, Freshwater Biology, 50, 201–220 204 C.V. Baxter et al. Cloe & Garman, 1996; Wipfli, 1997), but this has never 1982). Indeed, studies have demonstrated higher been tested directly. Terrestrial invertebrates falling inputs to streams flowing through deciduous versus into temperate streams are often dominated by larvae conifer-dominated forest (Mason & MacDonald, 1982; and adults of the orders Hymenoptera, Diptera, Piccolo & Wipfli, 2002; Allan et al., 2003; Wipfli & Coleoptera, Lepidoptera, Homoptera, Orthoptera, Musslewhite, 2004), and greater flux to streams traver- Hemiptera and Arachnida, as well as Collembola, sing forest and natural grassland versus pasture Oligochaeta, and Gastropoda (e.g. Mason & MacDo- (Edwards & Huryn, 1995, 1996) or mown grassland nald, 1982; Cloe & Garman, 1996; Edwards & Huryn, (Kawaguchi & Nakano, 2001; Table 1). Moreover, the 1996; Wipfli, 1997; Young, Rader & Belish, 1997; highest inputs were measured at sites with relatively Bridcut, 2000). closed canopies of deciduous trees (Cloe & Garman, The flux of terrestrial invertebrates to streams is 1996; Nakano, Miyasaka & Kuhara, 1999c). Patch highly variable in time (Hunt, 1975). Seasonal vari- structure of streamside vegetation, combined with ation is pronounced, with the peak(s) occurring aerial and terrestrial dispersal of arthropods, abiotic during late spring, summer, or early autumn in factors such as wind, and downstream transport of temperate zones (Nelson, 1965; Mason & MacDonald, terrestrial invertebrates, might confound the role of 1982; Edwards & Huryn, 1995; Cloe & Garman, 1996; adjacent riparian vegetation in explaining inputs Bridcut, 2000; Kawaguchi & Nakano, 2001; Nakano & among stream reaches. However, Kawaguchi & Murakami, 2001). The magnitude and timing of inputs Nakano (2001) found that even small grassland reaches can also vary considerably among years. For example, (1.5–6 ha area) received lower inputs than adjacent peak input to Horonai Stream, a spring-fed stream densely forested ones. Hence, the spatial scale(s) at with deciduous riparian forest in Hokkaido, Japan, which riparian vegetation influences the flux of terrest- was measured during midsummer (July) in 1995 rial invertebrates to streams is unclear. (Kawaguchi & Nakano, 2001; Table 1), whereas it occurred in early autumn (September) in 1997 Consumption of terrestrial invertebrates and its (Nakano & Murakami, 2001). Moreover, although consequences for stream fish peak values were similar in these 2 years, they were nearly 50% lower during the cooler, wetter summers Consumption of terrestrial invertebrates by fish has of 2001 and 2002 (M. Murakami & K. Tatara, unpubl. been well documented, especially among salmonids data; C. Baxter, K. Fausch, and M. Murakami, unpubl. (Metzelaar, 1929; Allen, 1938; Hunt, 1975; Allan, 1981; data). With regard to diel variation, direct measure- Cada, Loar & Cox, 1987; Hubert & Rhodes, 1989; ments of flux are lacking, but measurements of drift Wipfli, 1997; Young et al., 1997; Dunham et al., 2000). composition over 24-h periods (Angradi & Griffith, These allochthonous prey are also frequently con- 1990; Edwards & Huryn, 1995; Rader, 1997; Young sumed by cyprinids (Starrett, 1950; Angermeier, 1982; et al., 1997; Nakano et al., 1999b) suggest that input of Garman, 1991), centrarchids (Cloe & Garman, 1996), terrestrial invertebrates is highest during afternoon galaxiids (Cadwallader, Eden & Hook, 1980; Main & and evening. Inputs also vary daily, because terrest- Lyon, 1988; Hicks, 1997; McIntosh, 2000), clupeids rial invertebrates are often produced, and contribute (Massman, 1963), and eels (Hicks, 1997), as well as to stream drift, during short periods because of their representatives of many tropical fish families (Kno¨p- phenology (Nelson, 1965; Mason & MacDonald, 1982). pel, 1970; Zaret & Rand, 1971; Goulding, 1980; Additionally, changes in air temperature and humid- Angermeier & Karr, 1983; Lowe-McConnell, 1987 ity affect invertebrate activity, which combined with and references therein; Winemiller, 1990). Aquatic wind, rain, and flow may affect their transport into consumers other than fish (including invertebrate streams (Hunt, 1975; Mason & MacDonald, 1982; predators; Townsend & Hildrew, 1979) may also prey Edwards & Huryn, 1995). on terrestrial invertebrates, but the extent is not The magnitude of terrestrial invertebrate flux to known. streams also varies spatially, and may be related to In systems where terrestrial invertebrate inputs are attributes of the riparian zone. Arthropod communities high, they can make up large proportions of the diet of on different riparian vegetation types differ in both fish during summer months (e.g. 50–86% in Garman, species richness and abundance (Mason & MacDonald, 1991; Wipfli, 1997; Nakano et al., 1999b) and as much

2005 Blackwell Publishing Ltd, Freshwater Biology, 50, 201–220 Prey subsidies link stream and riparian food webs 205 as 50% of their annual diet and energy budget Dolly Varden charr (Salvelinus malma Walbaum) to (Kawaguchi & Nakano, 2001; Nakano & Murakami, shift from foraging on drifting prey to picking 2001). Even in systems where terrestrial invertebrates invertebrates from the stream bottom (cf. Fausch, composed only 10–15% of the drift, they made up Nakano & Kitano, 1997; Nakano, Fausch & Kitano, more than a third of the diet (Hubert & Rhodes, 1989; 1999a). Using the same greenhouses, Kawaguchi, Young et al., 1997), indicating that stream fish often Nakano & Taniguchi (2003) showed that when prey selectively on terrestrial invertebrates in the terrestrial invertebrate input was experimentally stream drift (cf. Elliot, 1967; Furukawa-Tanaka, 1985; excluded from un-fenced 50-m reaches, fish biomass Main & Lyon, 1988; Garman, 1991). This may be decreased by nearly 50% because fish emigrated, because of their larger size, buoyancy, potentially apparently redistributing themselves in proportion to greater availability during daylight hours, and visibil- prey availability. These findings indicate that loss of ity against the light background of the sky. Their much terrestrial invertebrate prey can trigger both beha- greater mass, on average, than aquatic prey (Nakano vioural and numerical responses in fish populations. et al., 1999b), also makes them more valuable energet- In general, terrestrial invertebrates contribute sig- ically. Specialised behaviours for capturing terrestrial nificantly to the diets of many stream fish, particularly prey are known in some tropical fish. For example, in smaller systems with abundant deciduous riparian Rivulus hartii jumps out of the water to capture vegetation, and may account for higher density and terrestrial insects from overhanging vegetation diversity of fishes in such streams (Nakano & (Seghers, 1978), and archerfish (Toxotidae) spit water Murakami, 2001; Power, 2001). In temperate systems, to dislodge prey from tree branches (Allen, 1991). total fish production may be subsidised by terrestrial Fish consumption of terrestrial invertebrates gener- invertebrate prey inputs, in part because they occur ally appears to track prey availability. In temperate during summer and autumn when biomass of benthic streams, it is greatest between late spring and early stream invertebrates is declining (Nakano & Muraka- autumn, and may be insignificant during winter mi, 2001). For such streams, this subsidy may help (Allan, 1981; Bridcut & Giller, 1993; Cloe & Garman, explain ‘Allen’s paradox,’ which was based on Allen’s 1996; Nakano et al., 1999b; Kawaguchi & Nakano, (1951) observation that production of aquatic inverte- 2001). For example, in Horonai Stream in northern brates was insufficient to support fish production in Japan, terrestrial invertebrates in salmonid diets fell Horokiwi Stream, New Zealand. Nonetheless, no from >70% in summer to only 1% during winter published study has measured the contribution of (Kawaguchi & Nakano, 2001; Nakano & Murakami, terrestrial invertebrate prey to fish growth or repro- 2001). In tropical systems, fish consumption of duction, so it is unknown how much this subsidy terrestrial invertebrates differed between wet and contributes to fish abundance or production. Stable- dry seasons (Zaret & Rand, 1971; Angermeier & Karr, carbon-isotope analysis has been used to quantify the 1983) and may increase greatly on inundated flood- relative contribution of terrestrial energy sources to plains (Goulding, 1980; Lowe-McConnell, 1987). Diel stream fish (e.g. Doucett et al., 1996; Perry, Bradford & studies of fish foraging suggest that most consumption Grout, 2003), but most studies have focused on occurs during afternoon or evening, when terrestrial the indirect flow of plant carbon to fish through prey are believed to be most abundant (Angradi & aquatic invertebrate prey. Carbon isotope studies that Griffith, 1990; Young et al., 1997; Nakano et al., 1999b). also investigated fish diets have shown that terrestrial Because terrestrial invertebrate inputs peak during the invertebrates are an important component of the day and aquatic insects drift primarily at night (Rader, terrestrial carbon input to fish (Main & Lyon, 1988; 1997), diel sampling is necessary to accurately deter- Hicks, 1997), but efforts to quantify this contribution mine their relative contribution to fish diets. to fish populations have been limited. Only two experiments, in the same stream, have related subsidies of terrestrial invertebrate prey to Emerging aquatic insects as prey subsidies for behaviour and population demographics of fish. riparian consumers Nakano et al. (1999c) experimentally excluded terrestrial prey from 50-m fenced reaches of Horonai Stream Until recently, few studies have focused on the flux of using a plastic greenhouse cover. This caused native prey in the opposite direction, from streams to their

2005 Blackwell Publishing Ltd, Freshwater Biology, 50, 201–220 206 C.V. Baxter et al. riparian zones. In part, this has been because of the by late summer (Sweeney & Vannote, 1982; Sabo & assumption that material exchange in catchments is Power, 2002b), but can also provide a low level of prey dominated by flux from land to water (Power et al., flux to the riparian zone during autumn through early 2004). However, ecologists have discovered that spring (Jackson & Fisher, 1986; Nakano & Murakami, emergent adults of aquatic insects are as important 2001). Large pulses of emergence can be easily missed, to a wide range of riparian predators (Fig. 1) as so measuring total emergence requires frequent terrestrial invertebrates are to stream fish, and influ- sampling throughout the ice-free season (Judd, 1962; ence both their distribution and population biology. Harper, 1978; Nakano & Murakami, 2001). The flux of emergent insects also varies spatially, and may be related to characteristics of river and Characteristics of aquatic insect emergence riparian habitat, as well as insect behaviour. For To date, stream ecologists have focused primarily on example, Iwata (2003) reported that emergence from measuring abundance and timing of emergence of Horonai Stream was 4.5 times greater from pools than adult aquatic insects (Judd, 1962; Corbet, 1964; riffles, which he attributed to greater biomass of Harper, 1978), and material and energy flows through benthic detritivore larvae in pools. Power & Rainey the water surface (Teal, 1957; Webster & Patten, 1979), (2000) and Power et al. (2004) proposed that any rather than addressing consequences for populations habitat feature that retains or provides predation of riparian consumers. These fluxes can be large, refuge for aquatic insects, such as floating algal mats, ) ) averaging about 10 000–20 000 insects m 2 year 1 could enhance local emergence. Following emergence, ) ) (range: 700–156 000 individuals m 2 year 1 for 20 the number of adult insects penetrating riparian zones studies summarised in Jackson & Fisher, 1986), and typically declines exponentially with distance from ) ) about 2–7 · 103 mg m 2 year 1 dry mass (range: 500– the stream edge, and often reaches low levels within ) ) 23.1 · 103 mg m 2 year 1). Moreover, emergence can 10–25 m (Jackson & Resh, 1989; Power & Rainey, 2000; be a large proportion of annual benthic production, Henschel, Mahsberg & Stumpf, 2001; Lynch, Bunn & ranging from 4 to 57% for various taxa (e.g. Speir & Catterall, 2002; Iwata, Nakano & Murakami, 2003; Anderson, 1974), of which <1–66% of the adult insects Sanzone et al., 2003; Power et al., 2004). However, may return to the water (Gray, 1989; summarised in differences in adult behaviour among insect taxa (e.g. Jackson & Fisher, 1986). Based on a comprehensive swarming near the water surface versus aggregation study of benthic secondary production and emer- at upslope positions within or above the canopy) and gence from Sycamore Creek, a desert stream in their response to environmental conditions (e.g. forest Arizona, Jackson & Fisher (1986) found high annual or hill slope structure, weather) may mediate lateral ) ) production (121 · 103 mg m 2 year 1 dry mass) and flux of this subsidy into the catchment (Power & ) ) emergence (23 · 103 mg m 2 year 1), because of the Rainey, 2000; Power et al., 2004). We are aware of no warm water temperatures and rapid insect develop- investigation of this topic. ment. This resulted in a net export of 17% of benthic production to the riparian zone. Adult Diptera often Effects of emergent insects on terrestrial consumers make up 60–99% of emergent biomass (Judd, 1962; Jackson & Fisher, 1986; Gray, 1989), the rest being Adult aquatic insects emerging from streams provide primarily adult Ephemeroptera, Plecoptera, Trichop- prey for a host of riparian consumers, including bats tera, and Odonata. (Belwood & Fenton, 1976; Swift, Racey & Avery, 1985; Emergence of adult aquatic insects is highly vari- Barclay, 1991; de Jong & Ahleń, 1991; Sullivan et al., able in time (Corbet, 1964). In temperate zones, 1993; Power & Rainey, 2000), birds (Orians, 1966; emergence of individual taxa is usually seasonal and Swanson, Meyer & Serie, 1974; Davies, 1976; Custer & highly synchronous over a few days to a few months Pitelka, 1978; Busby & Sealy, 1979; Keast, 1990; Gray, (Sweeney & Vannote, 1982), whereas emergence can 1993; McIntosh, 2000), lizards (Sabo & Power, be relatively continuous in tropical regions where 2002a,b), salamanders (Burton, 1976), adult odonates temperatures are aseasonal (Corbet, 1964). Total (Higashi et al., 1979; Sukhacheva, 1996), beetles (Her- community emergence in temperate zone streams ing & Platcher, 1997; Paetzold, Schubert & Tockner, in typically peaks in early summer and declines sharply press), and spiders (Williams, Ambrose & Browning,

2005 Blackwell Publishing Ltd, Freshwater Biology, 50, 201–220 Prey subsidies link stream and riparian food webs 207 1995; Power & Rainey, 2000; Collier, Bury & Hibbs, derived 100% of their carbon, and free-living spiders 2002; Kato et al., 2003; Sanzone et al., 2003; Power gained 68% of theirs, from in-stream sources. In et al., 2004; Paetzold et al., in press). In addition, in- addition, after the stable isotope 15N was added to the stream production of both algae and invertebrates can stream for only 6 weeks, the web-weaving spider provide subsidies to terrestrial consumers that use guild had obtained 39% of their nitrogen from them directly, such as grasshoppers that forage on emerging aquatic insects and free-living spiders had stranded algae (Bastow et al., 2002) and dippers received 25% of theirs from the same source. Power & (Cinclus spp.; Price & Bock, 1983; Tyler & Ormerod, Rainey (2000) also reported that individuals of a sheet- 1994), ducks (Collier, 1991), and water shrews weaving spider (Linyphiidae) derived at least half of (Soricidae; Beneski & Stinson, 1987; Churchfield, their carbon from emergent insects, even when 1990) that eat significant amounts of aquatic insect located hundreds of meters from a northern California larvae. river. Although most studies have been conducted on Emergent aquatic insects have been reported to small streams, Paetzold et al., in press found that make up a substantial proportion of the diets of predatory beetles (Carabidae and Staphylinidae) and terrestrial consumers. In their comprehensive 14- free-living spiders (Lycosidae) aggregated along month study of Horonai Stream, Nakano & Murakami shorelines in a large river floodplain during periods (2001) reported that aquatic insects made up 26% of of increased emergence, and derived 48–100% of their the total annual energy budget for the entire bird carbon from aquatic sources. assemblage of 10 species found in a 200-m wide plot Concentrations of emergence can alter the beha- that included the riparian zone (n ¼ 7200 individual viour and demographics of mobile consumers, result- bird observations). Among individual bird taxa, ing in immigration and increased abundance during aquatic insects made up about 10–40% of the annual peak emergence periods. Summer migrant birds often energy for 4 year-round residents and five summer move into riparian zones during such periods (Davies, migrants, although the latter foraged heavily on 1976; Gray, 1993; Nakano & Murakami, 2001), result- emergent insects only during May and June of their ing in a shift of their populations away from uplands 4-month stay. Surprisingly, emergent insects made up (Murakami & Nakano, 2002). In a Kansas prairie the highest proportion of bird diets during the stream, Gray (1993) found that insect emergence was autumn through spring defoliation period (November higher from perennial downstream reaches bordered to May) when terrestrial prey were scarce, accounting by oak gallery forest than intermittent upstream for 50–90% of the monthly energy budget for the five reaches bordered by shrubs, and peaked rapidly after species residing in the forest during winter. In fact, flash floods as in desert streams (Fisher et al., 1982). In winter wren (Troglodytes troglodytes Linnaeus), the turn, bird abundance was strongly correlated with the single winter-only resident species, depended on flux of emerging insects, both spatially among reaches emergent insects for 98% of its diet, and was and temporally in concert with flow fluctuations, frequently seen foraging intensively for prey along resulting in concentration of both summer migrant stream banks and from the stream channel. Henschel and yearlong resident birds in riparian zones for et al. (2001) and Iwata et al. (2003) also made direct restricted periods (cf. Davies, 1976; Sweeney & observations of prey use by spiders and birds, Vannote, 1982). Similarly, distributions of some respectively, and found that aquatic prey made up species of bats are also influenced by spatio-temporal 54% of spider diets and 67–82% of bird diets along availability of insects emerging from rivers (de Jong & the lotic systems they studied. Ahleń, 1991; Power & Rainey, 2000; Power et al., Elemental composition of riparian arthropods 2004). Power et al. (2004) predicted that flying pred- based on stable isotope analysis also indicates their ators have greater potential for responding to prey reliance on emergent insects. In the riparian zones of subsidies than ground-based consumers because of two New Zealand streams, Collier et al. (2002) found their mobility. that both web-weaving and free-living spiders ob- Several investigators have reported that the distri- tained the majority of their carbon from aquatic bution and abundance of lizards and spiders also production. Likewise, Sanzone et al. (2003) found that track aquatic prey subsidies. Sabo & Power (2002a) web-weaving spiders along Sycamore Creek, Arizona used mesh barrier walls at the stream edge to reduce

2005 Blackwell Publishing Ltd, Freshwater Biology, 50, 201–220 208 C.V. Baxter et al. emergence to the riparian zone of the Eel River in production often exceeds allochthonous inputs (Min- northern California and found that lizard abundance shall, 1978) and the export of emergent insects may be averaged only about 60% of that in control plots essential to fuel terrestrial predators (Jackson & through the season, because of emigration. Similarly, Fisher, 1986; Power et al., 2004). Although consumers Kato et al. (2003) used a mesh-covered greenhouse to prey heavily on emergent insects during early sum- exclude emerging aquatic insects from the riparian mer, year-round resident taxa may rely almost zone of Horonai Stream. Their experimental manipu- entirely on the low level of emergence throughout lation reduced densities of mobile riparian-specialist winter from streams that remain ice-free (cf. Jackson & spiders that weave horizontal webs (Tetragnathidae) Fisher, 1986; Nakano & Murakami, 2001). Never- by more than half compared with control reaches, but theless, little is known about the role of aquatic insect not terrestrial-specialists that weave vertical webs emergence in winter, and study of the consequences (Araneidae) or less mobile sheet-weavers (Linyphii- of emergence for longer-term measures of fitness dae). Although sedentary consumers like sheet-weav- (i.e. growth and survival) of terrestrial consumers has ing spiders are unable to track emergent prey through just begun. movement, spatial or temporal variation in the subsidy may change growth rates and metabolic reserves, Indirect effects of invertebrate prey subsidies and thereby affect fitness (Power et al., 2004). in stream and riparian food webs In only one study has aquatic insect emergence been manipulated and growth of a riparian consumer Allochthonous inputs of invertebrate prey to stream been measured as an indicator of fitness. Sabo & and riparian habitats may also have significant Power (2002b) reduced emergence using the mesh indirect effects that propagate throughout recipient walls described earlier, but in this experiment also food webs (Fig. 1). Polis et al. (1997) argued that prevented immigration and emigration of lizards spatial subsidies of resources from donor habitats using enclosures. During early summer when emer- across ecotone boundaries (i.e. the land–water inter- gence was high, riparian lizards grew seven times face) could support high densities of consumers in faster in control enclosures that received the subsidy recipient habitats. Polis et al. (1997; Polis, 1999) compared with treatment ones where the flux of suggested these subsidised consumers could, in emergent aquatic insects was reduced by 55–65%.In turn, exert strong negative effects on in situ prey contrast, there was no difference in growth later in via a mechanism akin to apparent competition summer when emergence had declined to 20% of the (sensu Holt, 1977; Fig. 2a), potentially causing indi- early season levels. Moreover, lizard growth rates rect positive effects on their food resources via an were positively correlated with biomass of emergence ‘apparent’ trophic cascade. Polis & Strong (1996) among these and other plots throughout the catch- proposed that the way forward for understanding ment. The combined results of their complementary such subsidised food webs requires experimental experiments (Sabo & Power, 2002a,b) show that manipulation of flows from donor to recipient stream-derived prey can drive behavioural, numer- habitats at the boundary, and of key species, ical, and growth responses in terrestrial consumer followed by measurements of interaction webs (i.e. populations. population-level effects) to elucidate strong versus The general pattern emerging from these studies is weak links (cf. Paine, 1988, 1992; Strong, 1988; that adult aquatic insects attract predators to riparian Power et al., 1996). There have been relatively few zones along streams, especially during peak emer- such studies to date, but several have addressed gence in early summer, either temporarily via linkages at the stream–riparian interface. immigration as for birds, or for their entire life cycle via colonisation as for spiders and beetles. Thus, this Effects of terrestrial invertebrate inputs on stream food prey subsidy may help explain the higher density and webs diversity of consumers reported in riparian zones (Power & Rainey, 2000; Nakano & Murakami, The flux of terrestrial invertebrate prey may have 2001). In particular, in streams of arid ecosystems indirect effects on stream food webs, although this has like deserts and grassland steppes, autochthonous been investigated in only a single system. Nakano

2005 Blackwell Publishing Ltd, Freshwater Biology, 50, 201–220 Prey subsidies link stream and riparian food webs 209 shifted to benthic foraging. This shift reduced herbivorous benthic insects, thereby releasing periphyton from grazing and causing increased algal biomass in an archetypal trophic cascade (Fausch, Power & Murakami, 2002a). In contrast, in reaches with fish that were subsidised by natural inputs of terrestrial prey, biomass of benthic herbivores and algae were no different than in reaches from which fish were excluded altogether. As part of a later study on the same system, Baxter et al. (2004) also found that experimental reduction of terrestrial invertebrate inputs caused the same indirect effects in the stream food web. Interestingly, the results of the Nakano et al. (1999c) study contrasted with theoretical expecta- tions. Polis et al. (1997) predicted that subsidised consumers should exert increased predation pressure on in situ prey so that the net indirect effect of the subsidy on these prey would be negative (Fig. 2a). In contrast, Nakano et al. (1999c) found that the terrestrial prey subsidy buffered the effect of the fish predator on in situ benthic prey, because adding the fish had no effect on benthos when the subsidy was uninterrupted. Moreover, excluding the subsidy caused the fish to exert higher predation on the benthos. Thus, the subsidy had an indirect positive effect on in situ prey. Such positive indirect interactions between prey that share predators may frequently occur when predators exhibit strong switching behaviour (Abrams & Matsuda, 1996; Fig. 2b), as did the charr in the study by Nakano Fig. 2 Food web structures depicting alternate scenarios under et al. (1999c). Switching behaviour may be driven which an allochthonous prey subsidy has a negative (a) versus a positive (b) indirect effect on in situ prey of the recipient food both by prey characteristics and densities. For web. Open arrows indicate indirect effects and show the signs. example, terrestrial prey are highly vulnerable and Changes in size of circles and filled arrows represent the preferred by fish, whereas benthic prey can retreat numerical and functional responses by the predator, and the to interstitial refuges in the streambed and are less associated shifts in predator and prey abundance. Numerical response of a predator to an allochthonous prey subsidy may preferred, probably because they are much smaller. drive the indirect effect on in situ prey in a negative direction (a), However, characteristics of the terrestrial prey flux, whereas a predator functional response such as switching as well as the identities and behaviours of predators behaviour may drive the indirect effect in a positive direction and in situ prey will differ among systems. Any of (b). Note that in situ prey may have a similar indirect effect on allochthonous prey if they supply a reciprocal subsidy to the these factors might change the indirect effects of the donor habitat (see text), as indicated by the double-headed terrestrial subsidy (see below), but none have been arrows. investigated. et al. (1999c) reported strong direct and indirect effects Effects of emergent insects on riparian food webs of fish predation after experimentally excluding terrestrial prey from reaches of Horonai Stream using a Experiments and quantitative sampling have also greenhouse cover. As described earlier, when demonstrated indirect effects of emergent stream deprived of terrestrial prey, native Dolly Varden insects on riparian food webs. For example, Henschel

2005 Blackwell Publishing Ltd, Freshwater Biology, 50, 201–220 210 C.V. Baxter et al. et al. (2001) and Henschel (2004) showed that the flux recipient food webs may be evaluating the numerical of emerging adult aquatic insects to riparian plots, and functional responses of subsidised predators, and and the density of spiders that consumed these prey, their resultant indirect effects on in situ prey (Fig. 2; both decreased with distance from the edge of a large Murakami & Nakano, 2002; Sabo & Power, 2002a; Bavarian river. Moreover, in plots at the shore they Takimoto, 2002). A numerical response, whereby found that subsidised spiders exerted higher preda- predators immigrate to use a prey subsidy or increase tion pressure that reduced numbers of in situ herbi- by reproducing, could drive a negative indirect effect vorous insects, compared with plots farther from the on in situ prey (Fig. 2a), assuming a generalist pred- riverbank (30 and 60 m). In turn, this resulted in ator that eats both prey types. In contrast, predator reduced herbivory near shore on nettles (Urtica dioica functional responses to a subsidy, such as through Linnaeus), the dominant riparian plant. Spider prey switching or predator satiation, are likely to removal experiments at the sites close to and farther drive a positive indirect effect on in situ prey (Fig. 2b; from the riverbank caused terrestrial herbivores and Abrams & Matsuda, 1996). Which of these takes herbivory to increase at sites near shore, but had no primacy may govern the consequences of the subsidy effect at sites farther from shore. Thus, via the indirect for the entire recipient food web. In turn, Takimoto mechanism hypothesised by Polis et al. (1997, Fig. 2a), (2002) showed that the balance that is struck between Henschel et al. (2001) found that the aquatic prey these two opposing forces may be determined by the subsidy to riparian predators had a negative effect on rates of predator’s functional and numerical responses in situ terrestrial prey and subsequently reduced and the frequencies of the temporal variation of herbivory on a dominant riparian plant. allochthonous inputs. Similar indirect effects of emerging adult insects A second reason that may explain the divergent on riparian forest food webs can occur through bird findings regarding indirect effects of allochthonous predation. Murakami & Nakano (2002) showed that prey is the different experimental designs applied in insectivorous birds visited riparian forest plots more these studies (Table 2). For example, short-term frequently than upland plots in early summer, and removal or exclusion of a subsidised predator (e.g. consumed both adult aquatic insects emerging from Henschel et al., 2001; Murakami & Nakano, 2002) tests the stream and herbivorous insects that fed on the effect of predator density on in situ prey, but does riparian vegetation. A bird exclosure experiment so without assessing the possible influence of func- showed that bird predation depressed in situ insect tional responses by the predator. Consequently, such herbivores in the riparian forest more than in the an approach may increase the likelihood of inferring a upland forest. Thus, allochthonous prey input negative indirect effect of the prey subsidy on in situ modified the interaction between birds and herbi- prey (Fig. 2a; Table 2). In contrast, short-term mani- vorous insects in the riparian forest, thereby creat- pulation of the subsidy while enclosing predators at ing the potential for different food web structures in constant densities (e.g. Nakano et al., 1999c) allows riparian versus upland forest environments. Overall, expression of predator functional responses, but not a the negative indirect effect of allochthonous inputs numerical response, and thus may increase the like- on in situ prey measured in riparian food webs by lihood of concluding that the subsidy has positive Murakami & Nakano (2002) was similar to that effects on in situ prey (Fig. 2b; Table 2). reported by Henschel et al. (2001), but contrasted Combinations of short-term experimental designs with the positive indirect effect reported in stream can provide further insight regarding indirect effects food webs (Nakano et al., 1999c; Baxter et al., 2004). of subsidies. Sabo & Power (2002a,b) conducted complementary experiments, described earlier, in which predator presence (riparian lizards) and the Factors influencing the sign of indirect effects detected subsidy of emerging stream insects were both from experiments manipulated, and the indirect effects on in situ prey Short-term experiments have yielded divergent (ground-dwelling invertebrates) were measured. results regarding the indirect effects of allochthonous When lizards were enclosed, they observed a positive prey inputs in stream and riparian food webs. One indirect effect of the aquatic prey subsidy on in situ key to understanding the effects of prey subsidies on terrestrial prey, analogous to the results of Nakano

2005 Blackwell Publishing Ltd, Freshwater Biology, 50, 201–220 Prey subsidies link stream and riparian food webs 211 et al. (1999c, Fig. 2b; Table 2). In the second experiment, however, free-ranging lizards responded to the reduced prey subsidy by emigrating from plots, and the positive effect of the aquatic prey subsidy on in situ prey;

ferred effect of terrestrial prey was diminished. Sabo & Power (2002a) and Takimoto (2002) pointed out the need to under- in situ stand the balance between any numerical response versus functional responses of the predator to the prey subsidy. However, the numerical response Sabo &

predator and potential for functional and numerical response of predator over multiple generations Power (2002a) observed was the result of predators Long-term manipulation of subsidy or natural experiment Tests effect of subsidy on Jefferies, 2000 redistributing themselves according to prey availability, similar to that observed by Kato et al. (2003) for tetragnathid spiders and Kawaguchi et al. (2003) for stream ﬁsh. Such movements can create patchiness in

prey; the predator distribution over the short-term, so using

, 2003 this type of design may also decrease the likelihood of in situ

et al. detecting positive effects of allochthonous inputs on , 2003; in situ prey (Table 2). These observations highlight

et al. potential effects of study design on observed interactions, but also emphasise the need for better under- potential for functional and numerical response of predator, but the latter only via short-term movement predator and Kato Kawaguchi Short-term manipulation of subsidy (predator not enclosed) Tests effect of subsidy on Sabo & Power, 2002a; standing of predator perceptual capabilities and movements.

Promising directions for study Determining direct and indirect effects of invertebrate prey subsidies , 1999c; , 2004 Because of the potential for study design to affect et al. et al. prey, but not potential observed relationships (Fig. 2; Table 2), it is likely that a suite of different experiments, combined with predator functional response and in situ numerical response of predator Sabo & Power, 2002b; Baxter Short-term manipulation of subsidy (predator enclosed) Tests effect of subsidy on Nakano comparative research, must be applied to a given study system before the direct and indirect effects of allochthonous prey inputs can be fully understood. The experiments described above were designed to prey, detect stream or riparian predator behavioural and numerical responses to prey subsidies, and subse- , 2001; in situ quent shifts in recipient food webs, over relatively et al. short time frames (typically 2–8 wks in summer). Studies at such time scales may detect shifts in prey via a shared predator in the recipient food web, are shown. predator on but not potential functional response of predator Murakami & Nakano, 2002 predator foraging or changes in distribution in Treatment Short-term manipulation of predator (enclosed/exclosed) Negative Positive Negative or neutral Positive or negative response to prey availability, but encompass at most in situ one generation of these predators. Experiments in which resource subsidies are manipulated over long

prey time periods and larger spatial scales (e.g. Likens & Bormann, 1974; Wallace et al., 1997) are logistically Study designs to test the direct and indirect effects of allochthonous prey in food webs. The effects tested by each design, and the sign of the likely in in situ challenging, but may provide a clearer picture of indirect effects, as can opportunistic use of natural Table 2 allochthonous prey on Effects tested Tests effect of subsidised Attribute of experiment Sign of likely inferred effect of allochthonous prey on Examplesexperiments Henschel (e.g. Jefferies, 2000; Jefferies, Henry &

2005 Blackwell Publishing Ltd, Freshwater Biology, 50, 201–220 212 C.V. Baxter et al. Abraham, 2004; Table 2). Comparative studies can els. Baxter et al. (2004) showed that experimentally also help assess how short-term experimental results reducing terrestrial invertebrate inputs to Horonai ‘scale-up’ in both space and time. Moreover, theory Stream not only triggered a trophic cascade in the predicts additional indirect effects that we have not stream, but also reduced the reciprocal flux of emer- discussed, such as impacts on competitors of subsi- ging adult insects to the riparian forest. In this dised predators and effects at higher trophic levels manner, prey in one habitat may be affected by (Holt, 2004), and these also have not been empirically allochthonous prey from another, but may also supply investigated. a reciprocal subsidy to the adjacent habitat that could affect flux back to the first (Fig. 2). Thus, one allochthonous subsidy may influence the other, dri- Do reciprocal prey fluxes stabilise stream–riparian ving a feedback loop that amplifies connectivity systems through feedback loops? between the two food webs (Figs 1 & 2). Such More studies are needed that simultaneously address complex feedback may be common in real food webs the effects of reciprocal prey fluxes between streams (Polis & Strong, 1996), and awaits investigation. and forests. An important characteristic of the reciprocal prey subsidies described by Nakano & Muraka- Tangled food webs are set within the context of riverine mi (2001) was the seasonal asynchrony of in situ prey landscapes biomass and allochthonous prey supply. Previously, it was assumed that riparian forests served as the more A principal challenge for future research is to under- productive donors to less productive stream systems stand reciprocal invertebrate prey subsidies within on a year-round basis. However, Nakano & Muraka- the spatial context of entire catchments. By addressing mi (2001) showed that because peak periods of insect the effects of resource subsidies on recipient food production in the forest and stream are offset webs, researchers have taken an important step seasonally, the forest feeds the stream food web towards integrating landscape and food web ecology during summer, but the stream feeds the forest food (Polis et al., 1997), but more is needed. Stream and web from autumn to spring (Power, 2001). Such riparian ecologists have begun to develop more asymmetry may be typical for systems subject to continuous, holistic perspectives of riverine land- temperate climatic regimes, but the generality of this scapes (Fausch et al., 2002b; Tockner et al., 2002; seasonal pattern remains to be demonstrated. Wiens, 2002), and more studies are focusing on Theoretical and empirical studies are also needed to heterogeneity in river networks that sets the spatial investigate the consequences of reciprocal fluxes of context for variation in food web structure (Power & invertebrate prey for the stability of linked stream and Rainey, 2000; Power & Dietrich, 2002; Woodward & riparian food webs. Previous theoretical efforts have Hildrew, 2002; Huxel, Polis & Holt, 2004). However, focused on the consequences of resource fluxes from few studies to date have examined the roles of donor to recipient systems (Holt, 1985; Oksanen, 1990; invertebrate prey subsidies within this spatial context. Polis & Winemiller, 1996). Models have suggested that Reciprocal fluxes of invertebrate prey are likely to prey fluxes from one habitat to another can positively vary along the longitudinal gradient of river systems, or negatively affect stability of recipient food webs, partly because of changes in stream size and depending on characteristics of the prey flux, predator physiognomy of the stream–riparian interface. As responses (Huxel & McCann, 1998; Huxel, McCann & stream size increases, the ratio of ‘edge’ to ‘interior’ Polis, 2002; Takimoto, Iwata & Murakami, 2002), or (i.e. perimeter-to-area, P/A) decreases, resulting in the trophic level at which the subsidy enters (Holt, reduced allochthonous input per unit area (Vannote 2004). For example, Takimoto et al. (2002) showed that et al., 1980; Polis et al., 1997). This effect underlies a seasonality of the terrestrial prey flux from forest to major tenet of the River Continuum Concept (RCC; stream, coupled with switching behaviour of predat- Vannote et al., 1980), that the role of terrestrial detrital ory fish, could stabilise the Horonai Stream food web. inputs decreases with increasing stream size. Terrest- However, system behaviour might change if recipro- rial invertebrate fluxes may similarly decrease, but the cal subsidies are considered together for linked food only data available come from small streams. Cloe & webs, rather than in one-way, donor–recipient mod- Garman (1996) reported that inputs per unit area were

2005 Blackwell Publishing Ltd, Freshwater Biology, 50, 201–220 Prey subsidies link stream and riparian food webs 213 greater to second order than sixth order Virginia aerial predators to forage more effectively on piedmont streams (Table 1). The relationship prob- emerging insects. For example, bats may commute ably changes in larger rivers with intact floodplains long distances to hunt over wider channels because where complex shorelines, anastomosing channels, turbulence in headwaters interferes with their ultra- and flooded forests increase both the perimeter and sonic prey detection (Power et al., 2004). Iwata et al. surface area of the aquatic–terrestrial interface (Junk, (2003) showed that birds concentrated their foraging Bayley & Sparks, 1989; Ward et al., 2002). close to more sinuous stream reaches, in part because Stream size may affect the relative importance of of more open habitat for foraging, but also because terrestrial invertebrate prey to fish. For example, meandering channels had greater surface area and consumption of terrestrial prey by American shad hence more total insect emergence. (Alosa sapidissima Wilson) declined downstream in Superimposed on longitudinal patterns, the local two Virginia rivers (Massman, 1963). In contrast, Cloe heterogeneity of stream and riparian habitats are & Garman (1996) found that, although input of likely to cause variation in reciprocal invertebrate terrestrial invertebrates per unit area declined down- subsidies. Catchment geomorphology constrains the stream, their consumption by centrarchid fishes was spatial arrangement of tributary junctions and alluvial similar. In large systems with intact floodplains like floodplain segments (Frissell et al., 1986; Montgomery, the Amazon River, terrestrial insects are important to 1999), both of which represent ‘hotspots’ in riverine the diet of many fishes that forage in flooded forests landscapes (Stanford, 1998; Power & Dietrich, 2002; and grasslands (Goulding, 1980). Allochthonous prey Benda et al., 2004). Such habitats are discontinuities were also once important to fish in large temperate (Poole, 2002), where nutrient concentration and phys- rivers (Forbes, 1895; Bayley, 1991), but most have lost ical disturbance lead to increased sunlight and pro- connections with their floodplains (Petts, Moller & duction of algae and emergent insects (Hawkins, Roux, 1989; Dynesius & Nilsson, 1994; Sparks, 1995). Murphy & Anderson, 1982; Power & Dietrich, 2002), Stable isotope analyses of aquatic invertebrate con- and where abundant deciduous vegetation may also sumers and benthic-feeding fish have generally increase terrestrial invertebrate inputs. In addition, shown that the role of allochthonous carbon decreases Wipfli (Wipfli et al., 1999; Wipfli & Gregovich, 2002; with increasing stream size (Finlay, 2001 and refer- Wipfli & Musslewhite, 2004) has shown that the ences therein), but consumption of terrestrial inverte- effects of invertebrate prey subsidies relative to other brates by drift-feeding fish may be underappreciated resource subsidies (e.g. marine derived nutrients, as a path of carbon flux, even in larger river systems. plant detritus) may vary within networks, as well as Emergence and lateral fluxes of adult aquatic from one catchment to the next, but investigations of insects may also change predictably from headwaters this are just beginning. More studies are needed to to large rivers. Power & Rainey (2000) proposed that explicitly address how the magnitude and effects of rates of emergence should increase with stream size, reciprocal invertebrate subsidies change within river- as channels and valley walls widen and sunlit scapes, especially in larger river-floodplain systems. riverbeds support more macroalgal growth. They also predicted that lateral fluxes of prey should expand in Human disturbances can interrupt reciprocal subsidies lowland rivers with intact floodplains that produce many emergent insects, and where winds may advect Ultimately, we require a better understanding of how prey farther from the river channel. However, where human disturbances like habitat destruction and floodplain connectivity has been lost, emergence was species invasions affect reciprocal flows of inverteb- predicted to decline. rate prey and other resource subsidies between linked Predation on emergent insects may also change stream and riparian habitats. Ecologists have long with stream size. For example, Power et al. (2004) recognised that degrading riparian habitat can alter reported that a tetragnathid spider was denser and flows of resources like leaves, wood, and dissolved foraged for shorter periods along the more productive organic carbon to stream ecosystems (e.g. Likens & mainstem of the Eel River where emergence was Bormann, 1974), but the impacts of reducing terres- greater, compared with smaller tributaries where trial invertebrate flux to streams has been considered emergence was less. Wider rivers also may allow only recently. Converting riparian forest to grassland

2005 Blackwell Publishing Ltd, Freshwater Biology, 50, 201–220 214 C.V. Baxter et al. (Kawaguchi & Nakano, 2001), grazing riparian zones terrestrial invertebrates and, hence, inputs to the (Edwards & Huryn, 1996), or changing the species stream. Thus, human disturbances such as species composition of riparian vegetation (Mason & MacDo- invasions and habitat destruction can interrupt flows nald, 1982) can alter terrestrial invertebrate inputs, of invertebrate prey and other resources between thereby restructuring stream food webs (Nakano streams and riparian zones, causing effects that et al., 1999c; Baxter et al., 2004). However, riparian propagate across their boundaries. Changes in these disturbance can also affect many other factors like food web connections require further exploration, and light, temperature, and channel morphology, so their implications should be integrated into manage- research is needed to assess interactions between ment and restoration of streams and riparian zones. these and allochthonous inputs. The study of these reciprocal prey linkages is Degradation of stream habitat for aquatic insect helping to define a more holistic perspective of larvae could also alter the flux of emergence to riparian catchments, but also has the potential to shape new consumers. Channelisation and siltation reduce the directions for ecology in general – something stream surface area and quality of habitat for aquatic larvae, ecology has done in only modest ways in the past and hence, the biomass of emerging adult insects (Fisher, 1990). Indeed, theoretical and empirical work (cf. Iwata et al., 2003). Moreover, disturbances that on river–catchment connections (e.g. Power & Die- reduce terrestrial invertebrate inputs to streams may trich, 2002) can lead the way toward integrating ideas trigger food web effects in the stream that reduce flux from community, landscape and ecosystem ecology of emergent insects back to the riparian zone (Baxter that have long remained disparate. This integration is et al., 2004). Because streams and riparian zones are reflected in the evolution of new theoretical constructs coupled in their vulnerability to habitat degradation, such as ‘meta-ecosystems’ (Loreau, Mouquet & Holt, assessing the health of one requires attention to the 2003), which might be tested using spatial flows of other. For example, Golet et al. (2003) suggested that resources in catchments. Progress along these lines bats, whose density and diversity may depend on will be enhanced by further creative thinking and new emergent insects from streams, might be useful indi- interdisciplinary interactions, coupled with empirical cators of health for river–riparian ecosystems. efforts that are at once holistic in their scope and Like habitat destruction, invasions of non-native rigorous in the manner in which they are conducted. species can also alter reciprocal flows of invertebrate prey, with consequences for stream and riparian Acknowledgments consumers and food webs. Results of a large-scale field experiment by Baxter et al. (2004) showed that We thank G. Takimoto, M. Murakami, and T. Iwata invasion of non-native rainbow trout (Oncorhynchus for discussion of ideas and sharing their unpublished mykiss Walbaum) interrupted reciprocal prey fluxes in manuscript, and A. McIntosh, P. Bayley and K. the Horonai stream-forest ecosystem of northern Winemiller for suggesting references. G. Takimoto, Japan. They found that rainbow trout usurped ter- M. Murakami, W. Clements, J. Monroe, and two restrial invertebrate prey, causing native Dolly Var- anonymous reviewers provided comments that im- den to shift their foraging to herbivorous stream proved the manuscript. J. Monroe created the figure insects. This indirectly increased algal biomass, but artwork. In preparing this review, the authors were also decreased insect emergence and led to a 65% supported by funding from the U.S. National Science reduction in the density of tetragnathid spiders in the Foundation (DEB0108222) and the U.S. Department of riparian forest. Likewise, invasions in riparian zones Agriculture, Natural Resources Conservation Service, may have similar far-reaching effects. Invasive plants Wildlife Habitat Management Institute (Agreement 68– such as saltcedar (Tamarix remosissima Ledeb) or 7482–3-131; administered by W. Gilgert and K. Boyer). bamboo (Bambusa spp.) alter flux of plant detritus and organic matter processing in streams (O’Connor References et al., 2000; Kennedy & Hobbie, 2004) which could, in turn, alter emergence of adult insects whose larvae Abrams P.A. & Matsuda H. (1996) Positive indirect forage on detritus. Moreover, such changes in riparian effects between prey species that share predators. vegetation could alter the assemblage of herbivorous Ecology, 77, 610–616.

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