188
Integrated Environmental Assessment and Management — Volume 11, Number 2—pp. 188–194 Published 2014 SETAC
Why Care About Aquatic Insects: Uses, Benefits, and Services Glenn W. Suter II*y and Susan M. Cormiery yNational Center for Environmental Assessment, US Environmental Protection Agency, Cincinnati, Ohio
(Submitted 28 July 2014; Returned for Revision 12 September 2014; Accepted 1 November 2014)
Brief Communication
ABSTRACT Aquatic insects are common subjects of ecological research and environmental monitoring and assessment. However, their important role in protecting and restoring aquatic ecosystems is often challenged because their benefits and services to humans are not obvious to decision makers or the public. Insects are food for fish, amphibians, and wildlife. They are important contributors to energy and nutrient processing, including capturing nutrients and returning them to terrestrial ecosystems and purifying water. They provide recreation to fishermen and nature lovers and are cultural symbols. Monetary benefits to fishermen can be quantified, but most other benefits have been described qualitatively. Integr Environ Assess Manag 2015;11:188–194. Published 2014 SETAC. This article is a US Government work and, as such, is in the public domain in the USA. Keywords: Cost–benefit
Ecological economics
Ecosystem services
INTRODUCTION Researchers who study aquatic insects, and applied environmental scientists who include them in monitoring programs and assessments, know that they are important. However, researchers and assessors often find themselves explaining and justifying the use of these organisms to everyone from friends and family to research funders and environmental managers. In our own experience, a state official asked, “What is important about mayflies?” And, a remedial project manager asked, “Why should I care about bugs in the mud?” Assessors need to have ready responses to such questions. In addition, the laws and regulations of the United States and other nations sometimes require that the benefits to humans of environmental protection be documented and even quantified. Support for cost–benefit analysis Environmental goods and services are valued in analyses that balance the benefits of regulations against the costs to regulated parties. In the United States, such analyses are required by executive order for all economically significant federal regulatory actions. Assessment of risks to public welfare Ecosystem services generate benefits to the public that enhance welfare and may be considered by decision makers. For example, the US Clean Air Act (CAA) provides protection from “known or anticipated effects to public welfare” via secondary National Ambient Air Quality Standards. Support natural resource damage assessments Responsible parties may be required to compensate natural resource trustees for damages to natural resources. In the United States, assessment of damages to natural resources are required by the Superfund and Oil Pollution Acts. * Address correspondence to: [email protected] Published online 6 November 2014 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/ieam.1600
Macroinvertebrates
Mayfly
More commonly, clarifying the value of environmental protection or remediation is not required, but it enhances the decision-making process by clarifying the utilitarian benefits of environmental protection. For example, many ecological risk assessments evaluate effects to insects and other benthic invertebrates, but decision makers and stakeholders often do not understand that those organisms are food for fish and other vertebrates, much less that they contribute to human wellbeing through the processing of energy and nutrients. Enumeration of the services provided by aquatic insects and the benthic invertebrate community can strengthen the basis for a protective decision and enhance communication of the benefits of protection to the public. Our objective is to make the case that aquatic insects are valuable by listing benefits and providing evidence from the literature that those benefits can be significant. We use the Central Appalachian region of the United States as a case study to illustrate the application of those benefits, because this review was prompted by the development of a field-based method for deriving benchmarks for conductivity using data from this region (USEPA 2011). In Central Appalachia, mountaintop coal mining removes large volumes of overburden that is used to fill headwater valleys. The leachate from those fills consists primarily of Ca2þ, Mg2þ, HCO3, and SO42, which elevates conductivity and causes the loss of aquatic insects; among these are many species of mayflies and stoneflies. The mining industry has attacked the use of mayflies because they are too sensitive to water quality (Stokstad 2014). The information presented here is intended to support the use of aquatic insects in our work in Central Appalachia but also for assessments elsewhere in the world because the same functions and benefits are afforded to most streams by aquatic insects. However, ecological assessments are typically site- or region-specific, so the strategy illustrated here of using regional evidence when available supported by evidence from elsewhere when necessary is generally appropriate. Therefore, we present our case as a possible template for assessors working in other regions. Other studies have reviewed some benefits of invertebrates in general or insects in general, but not expressly the aquatic insects considered here (Kellert 1993; Losey and Vaughan 2006).
Benefits of Aquatic Insects—Integr Environ Assess Manag 11, 2015
This article emphasizes mayflies because they were important to our case and because they are among the more sensitive stream taxa to many contaminants (Clements et al. 2000; Cormier et al. 2013). However, other insect taxa are used when they provide better evidence of a benefit.
ECOSYSTEM SERVICES AND BENEFITS The services and associated benefits of stream insects fall into 3 categories: they serve as food for fish and other organisms, they perform ecosystem functions such as nutrient retention, and they are used by humans in environmental monitoring, recreation, education, and other activities. These services and benefits result from the life histories of these insects including, for most of them, aquatic immature stages and a flying reproductive stage. There is no market for aquatic insects or their services, but some of their benefits can be quantified in monetary terms. The only benefit that could be monetized in our case is the recreational value of the trout fishery that depends on insects. Further monetization would require environmental economic research. Stream insects are food The most easily recognized benefit of stream insects is as food for fish and other vertebrates that are valued by humans. For example, hundreds of species have been shown to consume mayflies (Grant 2001). With few exceptions, fish in streams depend on insects directly as food or as part of their food chain, and most freshwater game fish depend on insects in part of their life cycles. In our case, aquatic insects are the principle food for the game fish that occur in Appalachian streams (e.g., brook, rainbow, and brown trout). Trout in Appalachian streams appear to be food-limited, and although terrestrial insects make an important contribution, aquatic insects dominate their diets (Allan 1981; Cada et al. 1987; Richardson 1993; Sweka and Hartman 2008). In addition, the Appalachian coal region is a center of fish biodiversity, and the 7 threatened or endangered species of fish that occur in the region are insectivores (USEPA 2003). Stream insects are also food for amphibians. As larvae, stream salamanders consume insects, and adults may feed on stream or terrestrial insects (Burton 1976). Few studies of stream salamanders have more specific data, but the diet of the stream-dwelling larvae of the Pacific giant salamander is predominantly aquatic insects including 30% to 69% mayfly nymphs (Parker 1994). In a headwater Appalachian stream, salamander production was limited by the availability of prey (Wallace et al. 1997). The support provided by insects is particularly important in Appalachia, because approximately 10% of the global diversity of salamanders occurs in southern Appalachia (Green and Pauley 1987). Stream insects are food for birds. Bird watching is an important recreational activity, and the sight and sounds of birds are valued by most people. The Louisiana water thrush and spotted sandpiper feed on the aquatic insects in Appalachian streams. Other birds—such as dippers, harlequin ducks and pied-billed grebes—feed on aquatic insects in other aquatic habitats. Many other birds such as swallows, warblers, and flycatchers feed on the emergent phases of aquatic insects. In one temperate, deciduous forest, 25.6% of the annual energy budget of insectivorous birds came from emergent stream insects (Nakano and Murakami 2001). Birds consumed 57% to
189
87% of insects emerging from a prairie stream (Gray 1993). In the Sierra Nevada, California, mountain lakes where mayflies had not been extirpated by stocked trout supported 5.9 times more rosy finches (Epanchin et al. 2010). In addition, herons, loons, mergansers, and kingfishers benefit indirectly from aquatic insects when they feed on fish and amphibians. Bats feed on mass-emerging aquatic insects. A study of little brown bats found that they feed mainly on aquatic insects, particularly mayflies (Clare et al. 2011). One mayfly genus, Caenis, comprised approximately 32% of items in their diet during the maternity season. Semi-aquatic mammals that feed on aquatic insects include water shrews, raccoons, minks, and otters. The American water shrew (Sorex palustris), in particular, is associated with mountain streams and subsists primarily on aquatic insects and crustaceans. The subspecies S. palustris punctulatus is listed as threatened in Pennsylvania (Butchkoski 2010). This status has been attributed to the loss of macroinvertebrate prey from acid mine drainage (PADCNR 2013); whereas, the state of West Virginia states that water shrews are vulnerable to the loss of invertebrates resulting from poor water quality in general (WVDNR 2004). Stream insects perform ecosystem functions Aquatic insects perform various functions in streams that contribute to ecosystem services. Because water quality assessments are often concerned with preventing the loss of a proportion of the macroinvertebrate assemblage, it is important to consider the effects of lost biodiversity on ecosystem functions. In general, the loss of biodiversity reduces rates of ecosystem functions and resulting ecosystem structural attributes such as biomass (Hooper et al. 2005; Cardinale 2011). These functions are indirect ecosystem services. The associated direct services to humans, such as improved aesthetics, can be inferred based on knowledge of the relationships between the functions and attributes desired by humans. The ecosystem functions performed by stream invertebrates include nutrient retention, litter decomposition, cleaning rocks, stream recovery, and removal of algae and pathogenic microbes. Nutrient retention. Insects retain nutrients in their biomass that otherwise would be carried downstream (Newbold et al. 1982, 1983; Jackson and Resh 1989; Wallace and Webster 1996; Evans-White et al. 2005). In an Appalachian stream, macroinvertebrates contained 25% of the P (Newbold et al. 1983). When insects emerge, less than 20% and in some cases as little as 1% of insects return to the stream (Huryn and Wallace 2000). Therefore, N, P, and other nutrients are removed from streams and returned to terrestrial ecosystems. This affects at least 3 ecosystem services: 1) it increases the productivity of forests and other terrestrial ecosystems, increasing the many services of those ecosystems, 2) it improves the water quality in streams, enhancing native oligotrophic biota and improving the quality of recreation, and 3) it reduces downstream eutrophication (Figure 1). Overall, nutrient retention by insects increases forests, fish, and fisheries, and reduces the costs of water treatment from algae and algal toxins. Litter decomposition. The shredder and collector feeding guilds are important to leaf decomposition in streams (Short and Maslin 1977; Anderson and Sedell 1979; Wallace et al. 1982; Wallace and Webster 1996). Shredders reduce leaves to
190
Integr Environ Assess Manag 11, 2015—GW Suter II and SM Cormier
Figure 1. Conceptual model of some potential benefits of stream insects resulting from the ecosystem service, nutrient retention. Key: arrows indicate increases " or decreases # in ecosystem services or other attributes. Ovals indicate final ecosystem services (i.e., those that are directly beneficial).
particles that are consumed by collectors such as net-feeding caddisflies. Together, they increase fish habitat and improve aesthetics in small forest streams that would otherwise fill with slowly decomposing leaves. Without detritivorous insects, the gravel substrates of forest streams could fill with partially decomposed leaves, which would reduce habitat for salamanders, as well as fish eggs and larvae, and would decrease interstitial dissolved O2. Furthermore, anoxic stream beds create sulfurous odors and may reduce the quality of sources of drinking water. The vulnerability of leaf decomposition is illustrated by a study in Zn-contaminated Colorado headwater streams (Carlisle and Clements 2005). The most active shredder (Taenionema pallidum) was the most sensitive to Zn, so breakdown of leaves was greatly reduced in even low Zn streams relative to reference streams. Cleaning rocks. Scrapers remove periphyton from rocks, thereby reducing the amount of “scum” and, in some conditions, increasing the productivity of the remaining algae (Wallace and Webster 1996). For example, Yasuno et al. (1982) and Nakano et al. (1999) found that periphyton biomass greatly increased when stream insects were extirpated by a pesticide treatment or were depleted by increased fish predation. Insects can also cause desirable changes in periphyton composition such as reducing an overstory of filamentous blue-green algae while tending their diatom “lawns” (Hart 1985). Scrapers therefore improve the aesthetics of streams for recreationists and may decrease the likelihood of falling while wading. In highly productive
streams, scrapers may prevent periphyton from cementing the gravel and potentially reducing habitat for fish and salamanders. Participation in elemental cycles. In addition to retaining nutrients, stream insects participate in the transformation of nutrient elements through mineralization and assimilation and by influencing microbes that perform oxidation or reduction processes, such as nitrification or denitrification (Newbold et al. 1982; Mulholland et al. 1991). Nutrient cycling is essential to all the services performed by ecosystems. However, the roles of stream insects are not well characterized and are highly variable among streams (Evans-White et al. 2005). Stabilization of stream beds. Although beds of freshwater mussels are the most well-known stabilizers of stream bottoms, colonies of caddisflies also perform that function and are more common, especially in contaminated systems. In experimental stream channels colonized with net spinning caddisflies, 1% to 30% stronger currents were required to erode sediments than in those without caddisfly colonies (Cardinale et al. 2004). As a result, at velocities that scoured 87% of particles from control channels, 0% to 43% of particles were scoured in channels colonized by the caddisflies. This may be important because reduced sediment erosion and suspension stabilizes habitat for other benthic species and reduces the frequency with which organisms are scoured. Cardinale et al. (2004) estimate that the stabilizing effect of caddisflies could reduce the probability
Benefits of Aquatic Insects—Integr Environ Assess Manag 11, 2015
of bed scour in a given year by a mean of 17% (range, 7.4%– 29.8%). Presumably, reduced scour also decreases downstream suspended sediment levels thereby benefiting fish and humans (USEPA 2007). Stream recovery. Stream insects are essential for stream recovery. For example, the caddisfly Lepidostoma rapidly colonizes following disturbance, shredding large leaves and beginning the food web based on allochthonous inputs (Whiles et al. 1993). The biomass of these shredders belies their overall importance. Their high consumption rates process large particulate organic matter and their low assimilation efficiency produces abundant resources for the collectors and filterers (Grafius and Anderson 1980). Removal of algae and pathogenic microbes. Collectors remove algae and microbes from the water column and consume them. In addition, although there are no studies of collectors that focus on removal of human pathogens, it seems likely that they perform this function. This is a particular issue in Central Appalachia where some residences have inadequate sewage treatment. Different species are most effective at different flow velocities (Georgian and Wallace 1981) and at capturing different sized particles (Wallace and Merritt 1980) again illustrating the importance of diversity. Insects can clear water at remarkable levels. In a study of a headwater stream, fluorescently labeled bacteria were removed from the water column in less than 100 m, but only 7% of removal was performed by invertebrates of which 91% was by the filterfeeding blackfly, Simulium (Hall et al. 1996). However, scrapers and shredders, such as the mayfly Epeorus and the stonefly Tallaperla, respectively also ingested the bacteria, presumably from biofilms. In different circumstances, simuliid larvae removed approximately 60% of cellular algae from a lake outlet in less than a half kilometer of stream (Maciolek and Tunzi 1968). These rates are load and insect density dependent (Ladle et al. 1972; McCullough et al. 1979). Stream arthropods have direct human uses Some benefits of insects are not mediated by functions or by support for other species or biotic communities. Indicators. Stream insects, particularly mayflies, are indicators of water quality and are used for that purpose in the United States, Canada, the European Union, Australia, New Zealand, South Africa, and other countries (Cormier and Messer 2004). Most biological indices of water quality include the number or relative abundance of Ephemeroptera, Plecoptera, and Trichoptera (EPT) taxa (Davis and Simon 1995; Barbour et al. 1999). For example, the West Virginia Department of Environmental Protection performs bioassessments based on a macroinvertebrate index, the West Virginia Stream Condition Index (WVSCI), which contains percentage of families of EPT and EPT abundance. Macroinvertebrates are more suited to this purpose than fish or other stream biota because they are easily sampled, are very diverse, and have a wide range of sensitivities to various agents. Fishing. In addition to providing food for fish, insects are essential to some types of fishing. Fly fishermen rely on stream insects as models for their lures, and insect emergences are occasions for angler excursions. Many specific mayfly and stonefly hatches are renowned and can draw large numbers of
191
fly fishermen from substantial distances, resulting in additional tourism and equipment sales. Bait fishermen sometimes use insects as bait. With respect to the case example, mountain trout anglers spent $146 million in North Carolina in 2008 (Responsive Management 2009). All anglers spent $333 million in West Virginia in 2006 and 47% of those anglers were trout fishermen (USFWS 2006). Economic input from use by anglers of a mile of trout stream in West Virginia or Pennsylvania is estimated to range from $28,000 to $74,000 per annum (Hansen 2007; Hansen et al. 2008). The monetary benefits of restoring trout waters in Central Appalachia from acidic coal mine drainage ranged from $1.4 to $73.6 million per annum for the Cheat River, Northern Branch Potomac River, and the West Branch Susquehanna River watersheds (Williamson et al. 2007; Williamson et al. 2008; Hansen et al. 2008; Hansen et al. 2010; Collins et al. 2009). Creeking. Stream insects and organisms such as fish and salamanders that feed on them are an important component of this recreational activity of children and even the occasional adult. Creeking involves exploring a stream and picking up rocks to see what is on or under them. The equivalent activity in ponds and lakes typically involves a net and is called “critter dipping.” Some stream partnerships, schools, and other organizations have adapted this recreational activity for education. Education. Stream insects have been used for education in biology and ecology (Klein and Merritt 1994). The Izaak Walton League (1996), Council for Environmental Education (2003), and others (Gaskell and Gilbertson 2013) provide resources for education focused on aquatic insects. The Girl and the Boy Scouts of America offer merit badges and other forms of recognition for learning about stream ecology by creeking, and making and using a kick net to sample benthic invertebrates (e.g., PUD). Kits that use stream insects to teach ecology to children are available from the Stroud Water Research Center and the LaMotte Company, and simple systems have been developed for raising mayflies in the classroom (http://www.stroudcenter.org/lpn/ and http:// www.mayflyintheclassroom.org). Collecting and watching. Some individuals and organizations collect and study stream insects recreationally, particularly the Odonata (dragonflies and damselflies). Fanciers collect, catch, and release, or simply watch odonates, a pastime called oding or dragonflying (see the website Odes for Beginners or blogs of individual fanciers, such as Dragonfly Eye). Organizations include the Ohio Odonata Society and the Dragonfly Society of the Americas. Other orders, however, also have their fanciers (see the Amateur Entomologists’ Society, BugGuide, Troutnut, and Mayfly Central, which is for “general users and enthusiasts”). Photography. Photographing insects has become a hobby for some individuals. Examples include the BugShot events, websites devoted to insect photographs, and the numerous photographs contributed to Mayfly Central and Odonata Central. Literary images and metaphors. Mayflies have been used as a metaphor for the brevity of life. Numerous song lyrics and poems refer to mayflies and a haiku journal is titled Mayfly. A
192
Integr Environ Assess Manag 11, 2015—GW Suter II and SM Cormier
poem by former poet laureate of the United States, Billy Collins (2011) contains the lines: It doesn’t take much to remind me what a mayfly I am A play titled Time Flies by David Ives is about a pair of mayflies realizing they have a mere 24 hours to live. The lyrical use of mayflies is illustrated by a surprisingly poetic commercial video (http://www.youtube.com/watch?v ¼ 6 FyDSbc9XR0&feature ¼ player_embedded). The 2014 Sherlock Holmes television series, Sherlock, featured a villain, the Mayfly Man, who assumes an identity for 24 hours. Even judges and attorneys wax poetic in tax court memoranda of findings referring to short lived and questionable ventures as having mayfly-like lives from their hatching to their dispatching (US Tax Court 2013). Other stream insects have occurred in literature but not to the same extent. Commercial and organizational symbols. Mayflies have been used in the names of many companies, products, and events to convey lightness, delicacy, grace, or some other attribute. For example, Nike makes a line of lightweight Mayfly running shoes and Hewlett Packard produced a parallel processing server called the Mayfly. At least 5 breweries produce mayfly beers and there are several mayfly pubs, perhaps appealing to the ideas of lightness, clean water, or the brevity of life. There is a Mayfly Symphony Orchestra in Paris, Mayfly Records, multiple bands with mayfly in their names, and a Mayfly Free Festival in Oxford, UK. Other stream insects may have use as commercial symbols (e.g., there is a software company called Stonefly Inc. and a Stonefly Brewing Company), but only dragonflies rival the mayflies as commercial symbols. Art and design. Stream insects, particularly odonata, have provided motifs for artists and craftsmen. Examples include the often-copied Tiffany dragonfly lamps and many pieces of jewelry with dragonfly forms by Tiffany, Lalique, and others. Caddisfly cases formed from gold, pearls, or semiprecious stones are used to make jewelry or sculpture (e.g., http://www. wildscape.com/). The Tiszavirag (mayfly) Bridge on the Tisza River, Hungary, was designed to resemble a mayfly and a nearby sculpture merges mayfly and human forms. Potential physical or chemical value. Who can predict what chemicals, structures, or processes might be found in these species that will prove useful? For example, the silk produced by caddisflies is extremely strong, but unlike moth and spider silk, phosphorylation makes the proteins sticky when wet and its long fibers behave like collagen. A synthetic version of the silk is being considered for development as an underwater adhesive, for wound healing, and artificial human tendons and ligaments (Addison et al. 2013). Aesthetics. Stream insects, particularly the dragonflies, mayflies, and damselflies, are aesthetically appealing to many and add pleasure to recreational outings or everyday experiences. Mayfly images have attracted buyers of books (see the enthusiastic comments on Amazon.com for Mayflies by T. Fauceglia) and photographs (e.g., http://fineartamerica.com/ art/photographs/mayfly/all).
CONCLUSIONS The services and benefits of stream insects in Appalachia and aquatic insects in general can be organized in terms of their utilities to humans. They are food for fish and other organisms that people value, they contribute to ecosystem functions, and they provide direct benefits to people. For some purposes, such as cost–benefit analysis, it is necessary to provide monetary values such as the values of the trout fisheries that aquatic insects support. However, in our case it was unnecessary because the Clean Water Act does not base its mandates on economic considerations (USEPA 2011). Even when monetary values are required, it is important to supplement them by quantifying the functional services that insects perform and by describing the unquantifiable aesthetic, philosophical, and cultural benefits (Funtowicz and Ravetz 1994). As an example of using nonmonetary benefits, the importance of insects to the ecological processing of organic matter and nutrients can, with a little background information, be explained to decision makers and the public. Although the contributions of insects to these essential ecosystem processes have not yet been quantified or translated into economic terms, even without more research, they can be qualitatively related to the costs of eutrophication, the benefits of terrestrial fertilization, and other contributions of functioning ecosystems to human well-being. The roles of mayflies and other aquatic insects in recreation, art, literature, music, commerce, and other cultural activities have not, to our knowledge, been reviewed. However, we believe that they are potentially important to understanding the full benefits of protecting these organisms. How will the quality of life be affected if there are fewer mayflies, birds, salamanders, and bats to be seen? How can someone who has not seen a mayfly hatch understand how they provide a symbol of delicacy or a metaphor for the brevity of life? When considering and conveying the many roles of aquatic insects, it is important to note that the functional services of insects depend on a diverse assemblage and in some streams are performed by only one or a few taxa (e.g., Lepidostoma and Taenionema for the shredding of fresh leaves). Although there may be many taxa of aquatic insects in a stream, there may be little or no redundancy for critical functions (Carlisle and Clements 2005). Diversity also contributes to the value of insects to fishermen (e.g., more emergences mean more opportunities for dry fly fishing) and to the fish and wildlife that consume them (e.g., bats need emergences at critical life stages such as nursing). Hence, it is important to protect the members of the aquatic insect community and to realize that aquatic insect species are functionally unique and cannot be replaced with a similar species. These benefits of stream insects are not apparent to most people. Even typical ecologists are unaware of some of these ecosystem services. Hence, even without quantification, simply describing these benefits can open the eyes of assessors, decision makers, and stakeholders to the importance of preserving aquatic insects. Without the insects and other invertebrates, streams would be simply channels that support algae and other microbes. Acknowledgment—We thank Laurie Alexander, Hale Thurston, members of the USEPA’s Risk Assessment Forum and anonymous reviewers for their helpful comments. Disclaimer—The views expressed in the article are those of the authors and do not necessarily represent the views or policies of the US Environmental Protection Agency or the
Benefits of Aquatic Insects—Integr Environ Assess Manag 11, 2015
IEAM Editorial Board. The authors declare that this work received no support other than the salaries provided by their employer and they have no conflicts of interest. The views presented within this article are those of the authors alone and do not necessarily represent the policies of our respective organizations. The peer-review process for this article was managed by the Editorial Board without involvement of Board members GW Suter II and SM Cormier.
REFERENCES Addison JB, Ashton NN, Weber WS, Stewart RJ, Holland GP, Yarger JL. 2013. b-Sheet nanocrystalline domains formed from phosphorylated serine-rich motifs in caddisfly larval silk: A solid state NMR and XRD study. Biomacromolecules 14:1140–1148. Allan JD. 1981. Determinants of diet of brook trout (Salvelinus fontinalis) in a mountain stream. Can J Fish Aquat Sci 38:184–192. Anderson NH, Sedell JR. 1979. Detritus processing by macroinvertebrates in stream ecosystems. Ann Rev Entomol 24:351–377. Barbour MT, Gerritsen J, Snyder BD, Stribling JB. 1999. Rapid bioassessment protocols for use in streams and wadeable rivers: Periphyton, benthic macroinvertebrates and fish. Washington DC: USEPA. EPA-841-B-99-002. Burton TM. 1976. An analysis of the feeding ecology of the salamanders (Amphibia, Urodela) of the Hubbard Brook Experimental Forest, New Hampshire. J Herpetol 10:187–204. Butchkoski E. 2010. West Virginia water shrew, Sorex palustris punctulatus. Pittsburgh (PA): Pennsylvania Game Commission. [cited 2014 June 20]. Available from: http://www.naturalheritage.state.pa.us/factsheets/11437.pdf Cada GF, Loar JM, Sale MJ. 1987. Evidence for food limitation of rainbow and brown trout in Southern Appalachian soft-water streams. Trans Am Fish Soc 116:692–702. Cardinale BJ, Gelmann ER, Palmer MA. 2004. Net spinning caddisflies as stream ecosystem engineers: The influence of Hydropsyche on benthic substrate stability. Funct Ecol 18:381–387. Cardinale BJ. 2011. Biodiversity improves water quality through niche partitioning. Nature 472:86–89. Cardinale BJ, Srivastava DS, Duffy JE, Wright JP, Downing AL, Sankaran M, Jouseau C. 2006. The effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443:989–992. Carlisle DM, Clements WH. 2005. Leaf litter breakdown, microbial respiration and shredder production in metal-polluted streams. Freshw Biol 50:380– 390. Clare EL, Barber BR, Sweeney BW, Herbert PD, Fenton MB. 2011. Eating local: Influence of habitat on the diet of little brown bats (Myotis lucifugus). Mol Ecol 20:1772–1780. Clements WH, Carlisle DM, Lazorchak J, Johnson P. 2000. Heavy metals structure benthic communities in Colorado mountain streams. Ecol Appl 10:626–638. Collins A, Rosenberg RS, Fletcher JJ. 2009. Valuing restoration of acidic streams in the Appalachian Region, a stated choice method. In: Thurston HW, Heberling MT, Schrecongost A, editors. Environmental economics of watershed restoration. Boca Raton (FL): CRC. p 29–52. Collins B. 2011. Horoscopes for the dead: Poems. New York (NY): Random House. 128 p. Cormier SM, Messer JJ. 2004. Opportunities and challenges in surface water quality monitoring. In: Wiersma GB, editor. Environmental monitoring. Boca Raton (FL): CRC. p 217–238. Cormier SM, Suter GW, II, Zheng L, Pond GJ. 2013. Assessing causation of the extirpation of stream macroinvertebrates by a mixture of ions. Environ Toxicol Chem 32:277–287. Council for Environmental Education. 2003. Project WILD aquatic K–12 curriculum and activities guide. Houston (TX): Council for Environmental Education. Davis WS, Simon TP, editors. 1995. Biological assessment and criteria. Boca Raton (FL): CRC. 415 p. Epanchin PN, Knapp RA, Lawler SP. 2010. Nonnative trout impact an alpinenesting bird by altering aquatic-insect subsidies. Ecology 91:2406–2415. Evans-White MA, Stelzer RS, Lambert GA. 2005. Taxonomic and regional patterns of benthic macroinvertebrate elemental composition in streams. Freshw Biol 50:1786-1799.
193 Funtowicz SO, Ravetz JR. 1994. The worth of a songbird: Ecological economics as a post-normal science. Ecol Econ 10:197–207. Gaskell P, Gibson C. 2013. A teacher's introduction and reference to mayfly in the classroom. The Wild Trout Trust. [cited 2013 April 17]. Available from. http:// www.wildtrout.org/sites/default/files/projects/teache rs_introduction_to_ma yfly_in_the_classroom.pdf Georgian TJ Jr, Wallace JB. 1981. A model of seston capture by net-spinning caddisflies. Oikos 36:147–157. Grafius E, Anderson NH. 1980. Populations dynamics and role of two species of Lepidostoma (Trichoptera:Lepidostomatidae) in an Oregon coniferous forest stream. Ecology 60:808–816. Grant PM. 2001. Mayflies as food. In: Dominguez E, editor. Trends in research in ephemeroptera and plecoptera. New York (NY): Kluwer Academic. p 107– 124. Gray LJ. 1993. Emergence production and export of aquatic insects in riparian habitats in a tallgrass prairie. Am Midl Nat 129:288–300. Green NB, Pauley TK. 1987. Amphibians and reptiles in West Virginia. Pittsburgh (PA): Univ Pittsburgh. 241 p. Hall RO Jr, Peredney CL, Meyer JL. 1996. The effect of invertebrate consumption on bacterial transport in a mountain stream. Limnol Oceanogr 41:1180–1187. Hansen E. 2007. Protecting West Virginia trout streams. West Virginia Public Affairs Reporter 24:1–11. Hansen E, Collins A, Svetlik J, McClurg S, Shrecongost A, Stenger R, Schilz M, Boettner F. 2008. An economic benefit analysis for abandoned mine drainage remediation in the West Branch Susquehanna River watershed, Pennsylvania. Morgantown (WV): Downstream Strategies. Hansen E, Collins A, Zegre S, Hereford A. 2010. The benefit of acid mine drainage remediation on the North Branch Potomac River. Morgantown (WV). Downstream Strategies. Hart DD. 1985. Grazing insects mediate algal interactions in a stream benthic community. Oikos 44:40–46. Hooper DU, Chapin FS III, Ewel JJ, Hector A, Inchausti P, Lavorell S, Lawton JH, Lodge DM, Loreau M, Naeem S, et al. 2005. Effect of biodiversity on ecosystem functioning: A consensus of current knowledge. Ecol Monogr 75:3–35. Huryn AD, Wallace JB. 2000. Life history and production of stream insects. Ann Rev Entomol 45:83–110. Izaak Walton League. 1996. Hands on save our streams: Science projects guide for students. Granville (OH): McDonald and Woodward. 48 p. Jackson JK, Resh VH. 1989. Distribution and abundance of adult aquatic insects in the forest adjacent to a Northern California stream. Environ Entomol 18:278– 283. Kellert SR. 1993. Values and perceptions of invertebrates. Conserv Biol 7:845–855. Klein ES, Merritt E. 1994. Environmental education as a model for constructivist teaching. J Environ Educ 25:14-21. Ladle M, Bass JAB, Jenkins WR. 1972. Studies on production and food consumption by the larval Simuliidae of a chalk stream. Hydrobiologia 39:429–448. Losey JE, Vaughan M. 2006. The economic value of ecological services provided by insects. BioScience 56:311–323. Maciolek JA, Tunzi MG. 1968. Microseston dynamics in a simple Sierra Nevada lake-stream system. Ecology 49:60–75. McCullough DA, Minshall GW, Cushing CE. 1979. Bioenergetics of lotic filterfeeding insects Simulium spp. and Hydropsyche occidentalis and their function in controlling organic transport in streams. Ecology 60:585–596. Mulholland PJ, Steinman AD, Palumbo AV, Elwood JW, Kirschtel DB. 1991. Role of nutrient cycling and herbivory in regulating periphyton communities in laboratory streams. Ecology 72:966–982. Nakano S, Miyasaka H, Kuhara N. 1999. Terrestrial-aquatic linkages: Riparian arthropod inputs alter trophic cascades in a stream food web. Ecology 80:2435–2441. Nakano S, Murakami M. 2001. Reciprocal subsidies: Dynamic interdependence between terrestrial and aquatic food webs. Proc Natl Acad Sci USA 98:166– 170. Newbold JD, O'Neill RV, Elwood JW, Van Winkle W. 1982. Nutrient spiraling in streams: implications for nutrient limitation and invertebrate activity. Amer Nat 120:628–652. Newbold JD, Elwood JW, O'Neill RV, Sheldon AL. 1983. Phosphorus dynamics in a woodland stream ecosystem: A study of nutrient spiraling. Ecology 64:1249– 1263.
194
Integr Environ Assess Manag 11, 2015—GW Suter II and SM Cormier
[PADCNR] Pennsylvania Department of Conservation and Natural Resources. 2013. Endangered and threatened species in Pennsylvania, West Virginia Water Shrew Sorex palustris punctulatus. Pennsylvania Department of Conservation and Natural Resources. [cited 2013 April 17]. Available from: http://www.dcnr. state.pa.us/ Parker MS. 1994. Feeding ecology of stream-dwelling Pacific giant salamander larvae (Dicamptodon tenebrosus). Copeia 1994:705–718. [PUD] Public Utility District. Stream watchers badge, a project to educate and inform girls about water quality and to promote stewardship of our local streams. Public Utility District 1 of Kitsap County and Girls Scouts Totem Council. [cited 2014 June 20]. Available from: https://www.girlscoutsww.org/ Things-To-Do/discover- more/Documents/StreamWatchersBadge.pdf Responsive Management. 2009. The economic impact of mountain trout fishing in North Carolina. Harrisonburg (VA) Responsive Management. Richardson JS. 1993. Limits of productivity of streams: Evidence from studies of macroinvertebrates. Can Spec Publ Fish Aquat Sci 118:9-15. Short RA, Maslin PE. 1977. Processing of leaf litter by a stream detritivore: Effect on nutrient availability to collectors. Ecology 58:935–938. Stokstad E. 2014. The mountaintop witness. Science 343:592–595. Sweka JA, Hartman KJ. 2008. Contribution of terrestrial invertebrates to yearly brook trout consumption and growth. Trans Am Fish Soc 137:224– 235. [USEPA] US Environmental Protection Agency. 2003. Draft programmatic environmental impact statement on mountaintop mining/valley fills in Appalachia. Philadelphia (PA): USEPA, Region 3. [USEPA] US Environmental Protection Agency. 2007. Framework for developing suspended and bedded sediment (SABS) water quality criteria. Washington DC: USEPA. EPA/822-R-06-001. USEPA] US Environmental Protection Agency. 2011. A field-based aquatic life benchmark for Conductivity in Central Appalachian streams. Washington DC: National Center for Environmental Assessment. EPA/600/R-10/023A.
[USFWS] US Fish and Wildlife Service. 2006. National survey of fishing, hunting, and wildlife associated recreation—West Virginia. Washington DC: USFWS. FHW/06-WV. US Tax Court. 2013. T.C. Memo. 2013-49: 6611, Ltd., Ricardo Garcia, Tax Matters Partner, et al. V. Commissioner of Internal Revenue. Docket Nos. 13088-05, 13250-05, 13251-05. Filed February 14, 2013. Available from: http://www. ustaxcourt.gov/InOpHistoric/6611,Ltd.TCM.WPD.pdf Wallace JB, Eggert SL, Meyer JL, Webster JR. 1997. Multiple trophic levels of a forested stream linked to terrestrial litter inputs. Science 277:102–104. Wallace JB, Merritt RW. 1980. Filter-feeding ecology of aquatic insects. Ann Rev Entomol 25:103–132. Wallace JB, Webster JR. 1996. The role of macroinvertebrates in stream ecosystem function. Ann Rev Entomol 41:115–139. Wallace JB, Webster JR, Cuffney TF. 1982. Stream detritus dynamics: Regulation by invertebrate consumers. Oecologica 53:197–200. Whiles MR, Wallace JB, Chung K. 1993. The influence of Lepidostoma (Trichoptera: Lepidostomatidae) on recovery of leaf-litter processing in disturbed headwater streams. Am Midl Nat 130:356–363. Williamson JM, Thurston HW, Heberling MT. 2007. Valuing acid mine drainage remediation in West Virginia: Benefit transfer with preference calibration. Environ Econ Pol Stud 8:271–293. Williamson JM, Thurston HW, Heberling MT. 2008. Valuing acid mine drainage remediation in West Virginia: A hedonic modeling approach. Ann Region Sci 42:987–999. [WVDNR] West Virginia Department of Natural Resources. 2004. Wildlife diversity notebook: The northern water shrew. West Virginia Wildlife Magazine. Winter Issue. [cited 2014 June 20]. Available from: http://www.wvdnr.gov/wildlife/ magazine/archive/04Winter/wildlife_diversity_notebook.shtm Yasuno M, Fukushima S, Hasegawa, Shioyama F, Hatakeyama S. 1982. Changes in benthic fauna and flora after application of temephos to a stream on Mt. Tsukuba. Hydrobiologia 89:205–214.
Integrated Environmental Assessment and Management — Volume 11, Number 2—pp. 188–194 Published 2014 SETAC
Why Care About Aquatic Insects: Uses, Benefits, and Services Glenn W. Suter II*y and Susan M. Cormiery yNational Center for Environmental Assessment, US Environmental Protection Agency, Cincinnati, Ohio
(Submitted 28 July 2014; Returned for Revision 12 September 2014; Accepted 1 November 2014)
Brief Communication
ABSTRACT Aquatic insects are common subjects of ecological research and environmental monitoring and assessment. However, their important role in protecting and restoring aquatic ecosystems is often challenged because their benefits and services to humans are not obvious to decision makers or the public. Insects are food for fish, amphibians, and wildlife. They are important contributors to energy and nutrient processing, including capturing nutrients and returning them to terrestrial ecosystems and purifying water. They provide recreation to fishermen and nature lovers and are cultural symbols. Monetary benefits to fishermen can be quantified, but most other benefits have been described qualitatively. Integr Environ Assess Manag 2015;11:188–194. Published 2014 SETAC. This article is a US Government work and, as such, is in the public domain in the USA. Keywords: Cost–benefit
Ecological economics
Ecosystem services
INTRODUCTION Researchers who study aquatic insects, and applied environmental scientists who include them in monitoring programs and assessments, know that they are important. However, researchers and assessors often find themselves explaining and justifying the use of these organisms to everyone from friends and family to research funders and environmental managers. In our own experience, a state official asked, “What is important about mayflies?” And, a remedial project manager asked, “Why should I care about bugs in the mud?” Assessors need to have ready responses to such questions. In addition, the laws and regulations of the United States and other nations sometimes require that the benefits to humans of environmental protection be documented and even quantified. Support for cost–benefit analysis Environmental goods and services are valued in analyses that balance the benefits of regulations against the costs to regulated parties. In the United States, such analyses are required by executive order for all economically significant federal regulatory actions. Assessment of risks to public welfare Ecosystem services generate benefits to the public that enhance welfare and may be considered by decision makers. For example, the US Clean Air Act (CAA) provides protection from “known or anticipated effects to public welfare” via secondary National Ambient Air Quality Standards. Support natural resource damage assessments Responsible parties may be required to compensate natural resource trustees for damages to natural resources. In the United States, assessment of damages to natural resources are required by the Superfund and Oil Pollution Acts. * Address correspondence to: [email protected] Published online 6 November 2014 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/ieam.1600
Macroinvertebrates
Mayfly
More commonly, clarifying the value of environmental protection or remediation is not required, but it enhances the decision-making process by clarifying the utilitarian benefits of environmental protection. For example, many ecological risk assessments evaluate effects to insects and other benthic invertebrates, but decision makers and stakeholders often do not understand that those organisms are food for fish and other vertebrates, much less that they contribute to human wellbeing through the processing of energy and nutrients. Enumeration of the services provided by aquatic insects and the benthic invertebrate community can strengthen the basis for a protective decision and enhance communication of the benefits of protection to the public. Our objective is to make the case that aquatic insects are valuable by listing benefits and providing evidence from the literature that those benefits can be significant. We use the Central Appalachian region of the United States as a case study to illustrate the application of those benefits, because this review was prompted by the development of a field-based method for deriving benchmarks for conductivity using data from this region (USEPA 2011). In Central Appalachia, mountaintop coal mining removes large volumes of overburden that is used to fill headwater valleys. The leachate from those fills consists primarily of Ca2þ, Mg2þ, HCO3, and SO42, which elevates conductivity and causes the loss of aquatic insects; among these are many species of mayflies and stoneflies. The mining industry has attacked the use of mayflies because they are too sensitive to water quality (Stokstad 2014). The information presented here is intended to support the use of aquatic insects in our work in Central Appalachia but also for assessments elsewhere in the world because the same functions and benefits are afforded to most streams by aquatic insects. However, ecological assessments are typically site- or region-specific, so the strategy illustrated here of using regional evidence when available supported by evidence from elsewhere when necessary is generally appropriate. Therefore, we present our case as a possible template for assessors working in other regions. Other studies have reviewed some benefits of invertebrates in general or insects in general, but not expressly the aquatic insects considered here (Kellert 1993; Losey and Vaughan 2006).
Benefits of Aquatic Insects—Integr Environ Assess Manag 11, 2015
This article emphasizes mayflies because they were important to our case and because they are among the more sensitive stream taxa to many contaminants (Clements et al. 2000; Cormier et al. 2013). However, other insect taxa are used when they provide better evidence of a benefit.
ECOSYSTEM SERVICES AND BENEFITS The services and associated benefits of stream insects fall into 3 categories: they serve as food for fish and other organisms, they perform ecosystem functions such as nutrient retention, and they are used by humans in environmental monitoring, recreation, education, and other activities. These services and benefits result from the life histories of these insects including, for most of them, aquatic immature stages and a flying reproductive stage. There is no market for aquatic insects or their services, but some of their benefits can be quantified in monetary terms. The only benefit that could be monetized in our case is the recreational value of the trout fishery that depends on insects. Further monetization would require environmental economic research. Stream insects are food The most easily recognized benefit of stream insects is as food for fish and other vertebrates that are valued by humans. For example, hundreds of species have been shown to consume mayflies (Grant 2001). With few exceptions, fish in streams depend on insects directly as food or as part of their food chain, and most freshwater game fish depend on insects in part of their life cycles. In our case, aquatic insects are the principle food for the game fish that occur in Appalachian streams (e.g., brook, rainbow, and brown trout). Trout in Appalachian streams appear to be food-limited, and although terrestrial insects make an important contribution, aquatic insects dominate their diets (Allan 1981; Cada et al. 1987; Richardson 1993; Sweka and Hartman 2008). In addition, the Appalachian coal region is a center of fish biodiversity, and the 7 threatened or endangered species of fish that occur in the region are insectivores (USEPA 2003). Stream insects are also food for amphibians. As larvae, stream salamanders consume insects, and adults may feed on stream or terrestrial insects (Burton 1976). Few studies of stream salamanders have more specific data, but the diet of the stream-dwelling larvae of the Pacific giant salamander is predominantly aquatic insects including 30% to 69% mayfly nymphs (Parker 1994). In a headwater Appalachian stream, salamander production was limited by the availability of prey (Wallace et al. 1997). The support provided by insects is particularly important in Appalachia, because approximately 10% of the global diversity of salamanders occurs in southern Appalachia (Green and Pauley 1987). Stream insects are food for birds. Bird watching is an important recreational activity, and the sight and sounds of birds are valued by most people. The Louisiana water thrush and spotted sandpiper feed on the aquatic insects in Appalachian streams. Other birds—such as dippers, harlequin ducks and pied-billed grebes—feed on aquatic insects in other aquatic habitats. Many other birds such as swallows, warblers, and flycatchers feed on the emergent phases of aquatic insects. In one temperate, deciduous forest, 25.6% of the annual energy budget of insectivorous birds came from emergent stream insects (Nakano and Murakami 2001). Birds consumed 57% to
189
87% of insects emerging from a prairie stream (Gray 1993). In the Sierra Nevada, California, mountain lakes where mayflies had not been extirpated by stocked trout supported 5.9 times more rosy finches (Epanchin et al. 2010). In addition, herons, loons, mergansers, and kingfishers benefit indirectly from aquatic insects when they feed on fish and amphibians. Bats feed on mass-emerging aquatic insects. A study of little brown bats found that they feed mainly on aquatic insects, particularly mayflies (Clare et al. 2011). One mayfly genus, Caenis, comprised approximately 32% of items in their diet during the maternity season. Semi-aquatic mammals that feed on aquatic insects include water shrews, raccoons, minks, and otters. The American water shrew (Sorex palustris), in particular, is associated with mountain streams and subsists primarily on aquatic insects and crustaceans. The subspecies S. palustris punctulatus is listed as threatened in Pennsylvania (Butchkoski 2010). This status has been attributed to the loss of macroinvertebrate prey from acid mine drainage (PADCNR 2013); whereas, the state of West Virginia states that water shrews are vulnerable to the loss of invertebrates resulting from poor water quality in general (WVDNR 2004). Stream insects perform ecosystem functions Aquatic insects perform various functions in streams that contribute to ecosystem services. Because water quality assessments are often concerned with preventing the loss of a proportion of the macroinvertebrate assemblage, it is important to consider the effects of lost biodiversity on ecosystem functions. In general, the loss of biodiversity reduces rates of ecosystem functions and resulting ecosystem structural attributes such as biomass (Hooper et al. 2005; Cardinale 2011). These functions are indirect ecosystem services. The associated direct services to humans, such as improved aesthetics, can be inferred based on knowledge of the relationships between the functions and attributes desired by humans. The ecosystem functions performed by stream invertebrates include nutrient retention, litter decomposition, cleaning rocks, stream recovery, and removal of algae and pathogenic microbes. Nutrient retention. Insects retain nutrients in their biomass that otherwise would be carried downstream (Newbold et al. 1982, 1983; Jackson and Resh 1989; Wallace and Webster 1996; Evans-White et al. 2005). In an Appalachian stream, macroinvertebrates contained 25% of the P (Newbold et al. 1983). When insects emerge, less than 20% and in some cases as little as 1% of insects return to the stream (Huryn and Wallace 2000). Therefore, N, P, and other nutrients are removed from streams and returned to terrestrial ecosystems. This affects at least 3 ecosystem services: 1) it increases the productivity of forests and other terrestrial ecosystems, increasing the many services of those ecosystems, 2) it improves the water quality in streams, enhancing native oligotrophic biota and improving the quality of recreation, and 3) it reduces downstream eutrophication (Figure 1). Overall, nutrient retention by insects increases forests, fish, and fisheries, and reduces the costs of water treatment from algae and algal toxins. Litter decomposition. The shredder and collector feeding guilds are important to leaf decomposition in streams (Short and Maslin 1977; Anderson and Sedell 1979; Wallace et al. 1982; Wallace and Webster 1996). Shredders reduce leaves to
190
Integr Environ Assess Manag 11, 2015—GW Suter II and SM Cormier
Figure 1. Conceptual model of some potential benefits of stream insects resulting from the ecosystem service, nutrient retention. Key: arrows indicate increases " or decreases # in ecosystem services or other attributes. Ovals indicate final ecosystem services (i.e., those that are directly beneficial).
particles that are consumed by collectors such as net-feeding caddisflies. Together, they increase fish habitat and improve aesthetics in small forest streams that would otherwise fill with slowly decomposing leaves. Without detritivorous insects, the gravel substrates of forest streams could fill with partially decomposed leaves, which would reduce habitat for salamanders, as well as fish eggs and larvae, and would decrease interstitial dissolved O2. Furthermore, anoxic stream beds create sulfurous odors and may reduce the quality of sources of drinking water. The vulnerability of leaf decomposition is illustrated by a study in Zn-contaminated Colorado headwater streams (Carlisle and Clements 2005). The most active shredder (Taenionema pallidum) was the most sensitive to Zn, so breakdown of leaves was greatly reduced in even low Zn streams relative to reference streams. Cleaning rocks. Scrapers remove periphyton from rocks, thereby reducing the amount of “scum” and, in some conditions, increasing the productivity of the remaining algae (Wallace and Webster 1996). For example, Yasuno et al. (1982) and Nakano et al. (1999) found that periphyton biomass greatly increased when stream insects were extirpated by a pesticide treatment or were depleted by increased fish predation. Insects can also cause desirable changes in periphyton composition such as reducing an overstory of filamentous blue-green algae while tending their diatom “lawns” (Hart 1985). Scrapers therefore improve the aesthetics of streams for recreationists and may decrease the likelihood of falling while wading. In highly productive
streams, scrapers may prevent periphyton from cementing the gravel and potentially reducing habitat for fish and salamanders. Participation in elemental cycles. In addition to retaining nutrients, stream insects participate in the transformation of nutrient elements through mineralization and assimilation and by influencing microbes that perform oxidation or reduction processes, such as nitrification or denitrification (Newbold et al. 1982; Mulholland et al. 1991). Nutrient cycling is essential to all the services performed by ecosystems. However, the roles of stream insects are not well characterized and are highly variable among streams (Evans-White et al. 2005). Stabilization of stream beds. Although beds of freshwater mussels are the most well-known stabilizers of stream bottoms, colonies of caddisflies also perform that function and are more common, especially in contaminated systems. In experimental stream channels colonized with net spinning caddisflies, 1% to 30% stronger currents were required to erode sediments than in those without caddisfly colonies (Cardinale et al. 2004). As a result, at velocities that scoured 87% of particles from control channels, 0% to 43% of particles were scoured in channels colonized by the caddisflies. This may be important because reduced sediment erosion and suspension stabilizes habitat for other benthic species and reduces the frequency with which organisms are scoured. Cardinale et al. (2004) estimate that the stabilizing effect of caddisflies could reduce the probability
Benefits of Aquatic Insects—Integr Environ Assess Manag 11, 2015
of bed scour in a given year by a mean of 17% (range, 7.4%– 29.8%). Presumably, reduced scour also decreases downstream suspended sediment levels thereby benefiting fish and humans (USEPA 2007). Stream recovery. Stream insects are essential for stream recovery. For example, the caddisfly Lepidostoma rapidly colonizes following disturbance, shredding large leaves and beginning the food web based on allochthonous inputs (Whiles et al. 1993). The biomass of these shredders belies their overall importance. Their high consumption rates process large particulate organic matter and their low assimilation efficiency produces abundant resources for the collectors and filterers (Grafius and Anderson 1980). Removal of algae and pathogenic microbes. Collectors remove algae and microbes from the water column and consume them. In addition, although there are no studies of collectors that focus on removal of human pathogens, it seems likely that they perform this function. This is a particular issue in Central Appalachia where some residences have inadequate sewage treatment. Different species are most effective at different flow velocities (Georgian and Wallace 1981) and at capturing different sized particles (Wallace and Merritt 1980) again illustrating the importance of diversity. Insects can clear water at remarkable levels. In a study of a headwater stream, fluorescently labeled bacteria were removed from the water column in less than 100 m, but only 7% of removal was performed by invertebrates of which 91% was by the filterfeeding blackfly, Simulium (Hall et al. 1996). However, scrapers and shredders, such as the mayfly Epeorus and the stonefly Tallaperla, respectively also ingested the bacteria, presumably from biofilms. In different circumstances, simuliid larvae removed approximately 60% of cellular algae from a lake outlet in less than a half kilometer of stream (Maciolek and Tunzi 1968). These rates are load and insect density dependent (Ladle et al. 1972; McCullough et al. 1979). Stream arthropods have direct human uses Some benefits of insects are not mediated by functions or by support for other species or biotic communities. Indicators. Stream insects, particularly mayflies, are indicators of water quality and are used for that purpose in the United States, Canada, the European Union, Australia, New Zealand, South Africa, and other countries (Cormier and Messer 2004). Most biological indices of water quality include the number or relative abundance of Ephemeroptera, Plecoptera, and Trichoptera (EPT) taxa (Davis and Simon 1995; Barbour et al. 1999). For example, the West Virginia Department of Environmental Protection performs bioassessments based on a macroinvertebrate index, the West Virginia Stream Condition Index (WVSCI), which contains percentage of families of EPT and EPT abundance. Macroinvertebrates are more suited to this purpose than fish or other stream biota because they are easily sampled, are very diverse, and have a wide range of sensitivities to various agents. Fishing. In addition to providing food for fish, insects are essential to some types of fishing. Fly fishermen rely on stream insects as models for their lures, and insect emergences are occasions for angler excursions. Many specific mayfly and stonefly hatches are renowned and can draw large numbers of
191
fly fishermen from substantial distances, resulting in additional tourism and equipment sales. Bait fishermen sometimes use insects as bait. With respect to the case example, mountain trout anglers spent $146 million in North Carolina in 2008 (Responsive Management 2009). All anglers spent $333 million in West Virginia in 2006 and 47% of those anglers were trout fishermen (USFWS 2006). Economic input from use by anglers of a mile of trout stream in West Virginia or Pennsylvania is estimated to range from $28,000 to $74,000 per annum (Hansen 2007; Hansen et al. 2008). The monetary benefits of restoring trout waters in Central Appalachia from acidic coal mine drainage ranged from $1.4 to $73.6 million per annum for the Cheat River, Northern Branch Potomac River, and the West Branch Susquehanna River watersheds (Williamson et al. 2007; Williamson et al. 2008; Hansen et al. 2008; Hansen et al. 2010; Collins et al. 2009). Creeking. Stream insects and organisms such as fish and salamanders that feed on them are an important component of this recreational activity of children and even the occasional adult. Creeking involves exploring a stream and picking up rocks to see what is on or under them. The equivalent activity in ponds and lakes typically involves a net and is called “critter dipping.” Some stream partnerships, schools, and other organizations have adapted this recreational activity for education. Education. Stream insects have been used for education in biology and ecology (Klein and Merritt 1994). The Izaak Walton League (1996), Council for Environmental Education (2003), and others (Gaskell and Gilbertson 2013) provide resources for education focused on aquatic insects. The Girl and the Boy Scouts of America offer merit badges and other forms of recognition for learning about stream ecology by creeking, and making and using a kick net to sample benthic invertebrates (e.g., PUD). Kits that use stream insects to teach ecology to children are available from the Stroud Water Research Center and the LaMotte Company, and simple systems have been developed for raising mayflies in the classroom (http://www.stroudcenter.org/lpn/ and http:// www.mayflyintheclassroom.org). Collecting and watching. Some individuals and organizations collect and study stream insects recreationally, particularly the Odonata (dragonflies and damselflies). Fanciers collect, catch, and release, or simply watch odonates, a pastime called oding or dragonflying (see the website Odes for Beginners or blogs of individual fanciers, such as Dragonfly Eye). Organizations include the Ohio Odonata Society and the Dragonfly Society of the Americas. Other orders, however, also have their fanciers (see the Amateur Entomologists’ Society, BugGuide, Troutnut, and Mayfly Central, which is for “general users and enthusiasts”). Photography. Photographing insects has become a hobby for some individuals. Examples include the BugShot events, websites devoted to insect photographs, and the numerous photographs contributed to Mayfly Central and Odonata Central. Literary images and metaphors. Mayflies have been used as a metaphor for the brevity of life. Numerous song lyrics and poems refer to mayflies and a haiku journal is titled Mayfly. A
192
Integr Environ Assess Manag 11, 2015—GW Suter II and SM Cormier
poem by former poet laureate of the United States, Billy Collins (2011) contains the lines: It doesn’t take much to remind me what a mayfly I am A play titled Time Flies by David Ives is about a pair of mayflies realizing they have a mere 24 hours to live. The lyrical use of mayflies is illustrated by a surprisingly poetic commercial video (http://www.youtube.com/watch?v ¼ 6 FyDSbc9XR0&feature ¼ player_embedded). The 2014 Sherlock Holmes television series, Sherlock, featured a villain, the Mayfly Man, who assumes an identity for 24 hours. Even judges and attorneys wax poetic in tax court memoranda of findings referring to short lived and questionable ventures as having mayfly-like lives from their hatching to their dispatching (US Tax Court 2013). Other stream insects have occurred in literature but not to the same extent. Commercial and organizational symbols. Mayflies have been used in the names of many companies, products, and events to convey lightness, delicacy, grace, or some other attribute. For example, Nike makes a line of lightweight Mayfly running shoes and Hewlett Packard produced a parallel processing server called the Mayfly. At least 5 breweries produce mayfly beers and there are several mayfly pubs, perhaps appealing to the ideas of lightness, clean water, or the brevity of life. There is a Mayfly Symphony Orchestra in Paris, Mayfly Records, multiple bands with mayfly in their names, and a Mayfly Free Festival in Oxford, UK. Other stream insects may have use as commercial symbols (e.g., there is a software company called Stonefly Inc. and a Stonefly Brewing Company), but only dragonflies rival the mayflies as commercial symbols. Art and design. Stream insects, particularly odonata, have provided motifs for artists and craftsmen. Examples include the often-copied Tiffany dragonfly lamps and many pieces of jewelry with dragonfly forms by Tiffany, Lalique, and others. Caddisfly cases formed from gold, pearls, or semiprecious stones are used to make jewelry or sculpture (e.g., http://www. wildscape.com/). The Tiszavirag (mayfly) Bridge on the Tisza River, Hungary, was designed to resemble a mayfly and a nearby sculpture merges mayfly and human forms. Potential physical or chemical value. Who can predict what chemicals, structures, or processes might be found in these species that will prove useful? For example, the silk produced by caddisflies is extremely strong, but unlike moth and spider silk, phosphorylation makes the proteins sticky when wet and its long fibers behave like collagen. A synthetic version of the silk is being considered for development as an underwater adhesive, for wound healing, and artificial human tendons and ligaments (Addison et al. 2013). Aesthetics. Stream insects, particularly the dragonflies, mayflies, and damselflies, are aesthetically appealing to many and add pleasure to recreational outings or everyday experiences. Mayfly images have attracted buyers of books (see the enthusiastic comments on Amazon.com for Mayflies by T. Fauceglia) and photographs (e.g., http://fineartamerica.com/ art/photographs/mayfly/all).
CONCLUSIONS The services and benefits of stream insects in Appalachia and aquatic insects in general can be organized in terms of their utilities to humans. They are food for fish and other organisms that people value, they contribute to ecosystem functions, and they provide direct benefits to people. For some purposes, such as cost–benefit analysis, it is necessary to provide monetary values such as the values of the trout fisheries that aquatic insects support. However, in our case it was unnecessary because the Clean Water Act does not base its mandates on economic considerations (USEPA 2011). Even when monetary values are required, it is important to supplement them by quantifying the functional services that insects perform and by describing the unquantifiable aesthetic, philosophical, and cultural benefits (Funtowicz and Ravetz 1994). As an example of using nonmonetary benefits, the importance of insects to the ecological processing of organic matter and nutrients can, with a little background information, be explained to decision makers and the public. Although the contributions of insects to these essential ecosystem processes have not yet been quantified or translated into economic terms, even without more research, they can be qualitatively related to the costs of eutrophication, the benefits of terrestrial fertilization, and other contributions of functioning ecosystems to human well-being. The roles of mayflies and other aquatic insects in recreation, art, literature, music, commerce, and other cultural activities have not, to our knowledge, been reviewed. However, we believe that they are potentially important to understanding the full benefits of protecting these organisms. How will the quality of life be affected if there are fewer mayflies, birds, salamanders, and bats to be seen? How can someone who has not seen a mayfly hatch understand how they provide a symbol of delicacy or a metaphor for the brevity of life? When considering and conveying the many roles of aquatic insects, it is important to note that the functional services of insects depend on a diverse assemblage and in some streams are performed by only one or a few taxa (e.g., Lepidostoma and Taenionema for the shredding of fresh leaves). Although there may be many taxa of aquatic insects in a stream, there may be little or no redundancy for critical functions (Carlisle and Clements 2005). Diversity also contributes to the value of insects to fishermen (e.g., more emergences mean more opportunities for dry fly fishing) and to the fish and wildlife that consume them (e.g., bats need emergences at critical life stages such as nursing). Hence, it is important to protect the members of the aquatic insect community and to realize that aquatic insect species are functionally unique and cannot be replaced with a similar species. These benefits of stream insects are not apparent to most people. Even typical ecologists are unaware of some of these ecosystem services. Hence, even without quantification, simply describing these benefits can open the eyes of assessors, decision makers, and stakeholders to the importance of preserving aquatic insects. Without the insects and other invertebrates, streams would be simply channels that support algae and other microbes. Acknowledgment—We thank Laurie Alexander, Hale Thurston, members of the USEPA’s Risk Assessment Forum and anonymous reviewers for their helpful comments. Disclaimer—The views expressed in the article are those of the authors and do not necessarily represent the views or policies of the US Environmental Protection Agency or the
Benefits of Aquatic Insects—Integr Environ Assess Manag 11, 2015
IEAM Editorial Board. The authors declare that this work received no support other than the salaries provided by their employer and they have no conflicts of interest. The views presented within this article are those of the authors alone and do not necessarily represent the policies of our respective organizations. The peer-review process for this article was managed by the Editorial Board without involvement of Board members GW Suter II and SM Cormier.
REFERENCES Addison JB, Ashton NN, Weber WS, Stewart RJ, Holland GP, Yarger JL. 2013. b-Sheet nanocrystalline domains formed from phosphorylated serine-rich motifs in caddisfly larval silk: A solid state NMR and XRD study. Biomacromolecules 14:1140–1148. Allan JD. 1981. Determinants of diet of brook trout (Salvelinus fontinalis) in a mountain stream. Can J Fish Aquat Sci 38:184–192. Anderson NH, Sedell JR. 1979. Detritus processing by macroinvertebrates in stream ecosystems. Ann Rev Entomol 24:351–377. Barbour MT, Gerritsen J, Snyder BD, Stribling JB. 1999. Rapid bioassessment protocols for use in streams and wadeable rivers: Periphyton, benthic macroinvertebrates and fish. Washington DC: USEPA. EPA-841-B-99-002. Burton TM. 1976. An analysis of the feeding ecology of the salamanders (Amphibia, Urodela) of the Hubbard Brook Experimental Forest, New Hampshire. J Herpetol 10:187–204. Butchkoski E. 2010. West Virginia water shrew, Sorex palustris punctulatus. Pittsburgh (PA): Pennsylvania Game Commission. [cited 2014 June 20]. Available from: http://www.naturalheritage.state.pa.us/factsheets/11437.pdf Cada GF, Loar JM, Sale MJ. 1987. Evidence for food limitation of rainbow and brown trout in Southern Appalachian soft-water streams. Trans Am Fish Soc 116:692–702. Cardinale BJ, Gelmann ER, Palmer MA. 2004. Net spinning caddisflies as stream ecosystem engineers: The influence of Hydropsyche on benthic substrate stability. Funct Ecol 18:381–387. Cardinale BJ. 2011. Biodiversity improves water quality through niche partitioning. Nature 472:86–89. Cardinale BJ, Srivastava DS, Duffy JE, Wright JP, Downing AL, Sankaran M, Jouseau C. 2006. The effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443:989–992. Carlisle DM, Clements WH. 2005. Leaf litter breakdown, microbial respiration and shredder production in metal-polluted streams. Freshw Biol 50:380– 390. Clare EL, Barber BR, Sweeney BW, Herbert PD, Fenton MB. 2011. Eating local: Influence of habitat on the diet of little brown bats (Myotis lucifugus). Mol Ecol 20:1772–1780. Clements WH, Carlisle DM, Lazorchak J, Johnson P. 2000. Heavy metals structure benthic communities in Colorado mountain streams. Ecol Appl 10:626–638. Collins A, Rosenberg RS, Fletcher JJ. 2009. Valuing restoration of acidic streams in the Appalachian Region, a stated choice method. In: Thurston HW, Heberling MT, Schrecongost A, editors. Environmental economics of watershed restoration. Boca Raton (FL): CRC. p 29–52. Collins B. 2011. Horoscopes for the dead: Poems. New York (NY): Random House. 128 p. Cormier SM, Messer JJ. 2004. Opportunities and challenges in surface water quality monitoring. In: Wiersma GB, editor. Environmental monitoring. Boca Raton (FL): CRC. p 217–238. Cormier SM, Suter GW, II, Zheng L, Pond GJ. 2013. Assessing causation of the extirpation of stream macroinvertebrates by a mixture of ions. Environ Toxicol Chem 32:277–287. Council for Environmental Education. 2003. Project WILD aquatic K–12 curriculum and activities guide. Houston (TX): Council for Environmental Education. Davis WS, Simon TP, editors. 1995. Biological assessment and criteria. Boca Raton (FL): CRC. 415 p. Epanchin PN, Knapp RA, Lawler SP. 2010. Nonnative trout impact an alpinenesting bird by altering aquatic-insect subsidies. Ecology 91:2406–2415. Evans-White MA, Stelzer RS, Lambert GA. 2005. Taxonomic and regional patterns of benthic macroinvertebrate elemental composition in streams. Freshw Biol 50:1786-1799.
193 Funtowicz SO, Ravetz JR. 1994. The worth of a songbird: Ecological economics as a post-normal science. Ecol Econ 10:197–207. Gaskell P, Gibson C. 2013. A teacher's introduction and reference to mayfly in the classroom. The Wild Trout Trust. [cited 2013 April 17]. Available from. http:// www.wildtrout.org/sites/default/files/projects/teache rs_introduction_to_ma yfly_in_the_classroom.pdf Georgian TJ Jr, Wallace JB. 1981. A model of seston capture by net-spinning caddisflies. Oikos 36:147–157. Grafius E, Anderson NH. 1980. Populations dynamics and role of two species of Lepidostoma (Trichoptera:Lepidostomatidae) in an Oregon coniferous forest stream. Ecology 60:808–816. Grant PM. 2001. Mayflies as food. In: Dominguez E, editor. Trends in research in ephemeroptera and plecoptera. New York (NY): Kluwer Academic. p 107– 124. Gray LJ. 1993. Emergence production and export of aquatic insects in riparian habitats in a tallgrass prairie. Am Midl Nat 129:288–300. Green NB, Pauley TK. 1987. Amphibians and reptiles in West Virginia. Pittsburgh (PA): Univ Pittsburgh. 241 p. Hall RO Jr, Peredney CL, Meyer JL. 1996. The effect of invertebrate consumption on bacterial transport in a mountain stream. Limnol Oceanogr 41:1180–1187. Hansen E. 2007. Protecting West Virginia trout streams. West Virginia Public Affairs Reporter 24:1–11. Hansen E, Collins A, Svetlik J, McClurg S, Shrecongost A, Stenger R, Schilz M, Boettner F. 2008. An economic benefit analysis for abandoned mine drainage remediation in the West Branch Susquehanna River watershed, Pennsylvania. Morgantown (WV): Downstream Strategies. Hansen E, Collins A, Zegre S, Hereford A. 2010. The benefit of acid mine drainage remediation on the North Branch Potomac River. Morgantown (WV). Downstream Strategies. Hart DD. 1985. Grazing insects mediate algal interactions in a stream benthic community. Oikos 44:40–46. Hooper DU, Chapin FS III, Ewel JJ, Hector A, Inchausti P, Lavorell S, Lawton JH, Lodge DM, Loreau M, Naeem S, et al. 2005. Effect of biodiversity on ecosystem functioning: A consensus of current knowledge. Ecol Monogr 75:3–35. Huryn AD, Wallace JB. 2000. Life history and production of stream insects. Ann Rev Entomol 45:83–110. Izaak Walton League. 1996. Hands on save our streams: Science projects guide for students. Granville (OH): McDonald and Woodward. 48 p. Jackson JK, Resh VH. 1989. Distribution and abundance of adult aquatic insects in the forest adjacent to a Northern California stream. Environ Entomol 18:278– 283. Kellert SR. 1993. Values and perceptions of invertebrates. Conserv Biol 7:845–855. Klein ES, Merritt E. 1994. Environmental education as a model for constructivist teaching. J Environ Educ 25:14-21. Ladle M, Bass JAB, Jenkins WR. 1972. Studies on production and food consumption by the larval Simuliidae of a chalk stream. Hydrobiologia 39:429–448. Losey JE, Vaughan M. 2006. The economic value of ecological services provided by insects. BioScience 56:311–323. Maciolek JA, Tunzi MG. 1968. Microseston dynamics in a simple Sierra Nevada lake-stream system. Ecology 49:60–75. McCullough DA, Minshall GW, Cushing CE. 1979. Bioenergetics of lotic filterfeeding insects Simulium spp. and Hydropsyche occidentalis and their function in controlling organic transport in streams. Ecology 60:585–596. Mulholland PJ, Steinman AD, Palumbo AV, Elwood JW, Kirschtel DB. 1991. Role of nutrient cycling and herbivory in regulating periphyton communities in laboratory streams. Ecology 72:966–982. Nakano S, Miyasaka H, Kuhara N. 1999. Terrestrial-aquatic linkages: Riparian arthropod inputs alter trophic cascades in a stream food web. Ecology 80:2435–2441. Nakano S, Murakami M. 2001. Reciprocal subsidies: Dynamic interdependence between terrestrial and aquatic food webs. Proc Natl Acad Sci USA 98:166– 170. Newbold JD, O'Neill RV, Elwood JW, Van Winkle W. 1982. Nutrient spiraling in streams: implications for nutrient limitation and invertebrate activity. Amer Nat 120:628–652. Newbold JD, Elwood JW, O'Neill RV, Sheldon AL. 1983. Phosphorus dynamics in a woodland stream ecosystem: A study of nutrient spiraling. Ecology 64:1249– 1263.
194
Integr Environ Assess Manag 11, 2015—GW Suter II and SM Cormier
[PADCNR] Pennsylvania Department of Conservation and Natural Resources. 2013. Endangered and threatened species in Pennsylvania, West Virginia Water Shrew Sorex palustris punctulatus. Pennsylvania Department of Conservation and Natural Resources. [cited 2013 April 17]. Available from: http://www.dcnr. state.pa.us/ Parker MS. 1994. Feeding ecology of stream-dwelling Pacific giant salamander larvae (Dicamptodon tenebrosus). Copeia 1994:705–718. [PUD] Public Utility District. Stream watchers badge, a project to educate and inform girls about water quality and to promote stewardship of our local streams. Public Utility District 1 of Kitsap County and Girls Scouts Totem Council. [cited 2014 June 20]. Available from: https://www.girlscoutsww.org/ Things-To-Do/discover- more/Documents/StreamWatchersBadge.pdf Responsive Management. 2009. The economic impact of mountain trout fishing in North Carolina. Harrisonburg (VA) Responsive Management. Richardson JS. 1993. Limits of productivity of streams: Evidence from studies of macroinvertebrates. Can Spec Publ Fish Aquat Sci 118:9-15. Short RA, Maslin PE. 1977. Processing of leaf litter by a stream detritivore: Effect on nutrient availability to collectors. Ecology 58:935–938. Stokstad E. 2014. The mountaintop witness. Science 343:592–595. Sweka JA, Hartman KJ. 2008. Contribution of terrestrial invertebrates to yearly brook trout consumption and growth. Trans Am Fish Soc 137:224– 235. [USEPA] US Environmental Protection Agency. 2003. Draft programmatic environmental impact statement on mountaintop mining/valley fills in Appalachia. Philadelphia (PA): USEPA, Region 3. [USEPA] US Environmental Protection Agency. 2007. Framework for developing suspended and bedded sediment (SABS) water quality criteria. Washington DC: USEPA. EPA/822-R-06-001. USEPA] US Environmental Protection Agency. 2011. A field-based aquatic life benchmark for Conductivity in Central Appalachian streams. Washington DC: National Center for Environmental Assessment. EPA/600/R-10/023A.
[USFWS] US Fish and Wildlife Service. 2006. National survey of fishing, hunting, and wildlife associated recreation—West Virginia. Washington DC: USFWS. FHW/06-WV. US Tax Court. 2013. T.C. Memo. 2013-49: 6611, Ltd., Ricardo Garcia, Tax Matters Partner, et al. V. Commissioner of Internal Revenue. Docket Nos. 13088-05, 13250-05, 13251-05. Filed February 14, 2013. Available from: http://www. ustaxcourt.gov/InOpHistoric/6611,Ltd.TCM.WPD.pdf Wallace JB, Eggert SL, Meyer JL, Webster JR. 1997. Multiple trophic levels of a forested stream linked to terrestrial litter inputs. Science 277:102–104. Wallace JB, Merritt RW. 1980. Filter-feeding ecology of aquatic insects. Ann Rev Entomol 25:103–132. Wallace JB, Webster JR. 1996. The role of macroinvertebrates in stream ecosystem function. Ann Rev Entomol 41:115–139. Wallace JB, Webster JR, Cuffney TF. 1982. Stream detritus dynamics: Regulation by invertebrate consumers. Oecologica 53:197–200. Whiles MR, Wallace JB, Chung K. 1993. The influence of Lepidostoma (Trichoptera: Lepidostomatidae) on recovery of leaf-litter processing in disturbed headwater streams. Am Midl Nat 130:356–363. Williamson JM, Thurston HW, Heberling MT. 2007. Valuing acid mine drainage remediation in West Virginia: Benefit transfer with preference calibration. Environ Econ Pol Stud 8:271–293. Williamson JM, Thurston HW, Heberling MT. 2008. Valuing acid mine drainage remediation in West Virginia: A hedonic modeling approach. Ann Region Sci 42:987–999. [WVDNR] West Virginia Department of Natural Resources. 2004. Wildlife diversity notebook: The northern water shrew. West Virginia Wildlife Magazine. Winter Issue. [cited 2014 June 20]. Available from: http://www.wvdnr.gov/wildlife/ magazine/archive/04Winter/wildlife_diversity_notebook.shtm Yasuno M, Fukushima S, Hasegawa, Shioyama F, Hatakeyama S. 1982. Changes in benthic fauna and flora after application of temephos to a stream on Mt. Tsukuba. Hydrobiologia 89:205–214.
