SPECIAL FEATURE

Kurt D. Fausch

Crossing boundaries: Shigeru Nakano’s enduring legacy for ecology

Received: 22 April 2017 / Accepted: 30 September 2017 / Published online: 9 November 2017� The Author(s) 2017. This article is an open access publication

Abstract Shigeru Nakano was a Japanese ecologistwhose work crossed boundaries among subdisciplines inecology, between aquatic and terrestrial habitats, andbetween different languages and cultures. He publishedhis first paper in 1985 while still an undergraduate, andis well known for his early research on the individualbehavior of stream salmonids in dominance hierarchies.Shortly after completing his Master’s degree in 1987 hebegan collaborating with many graduate students andother scientists, including those from the US, and ex-panded his research to include factors controlling streamsalmonid distribution and abundance across spatialscales ranging from local to landscape levels. In 1995 hemoved to a research station in southwestern Hokkaidoand began new collaborative research on interactionsbetween forest and stream food webs. Nakano pioneeredlarge-scale field experiments using greenhouses to severthe reciprocal fluxes of invertebrate prey between streamand riparian food webs. The strong direct and indirecteffects of isolating these food webs from each other onorganisms ranging from stream algae to fish, riparianspiders, and bats have revealed new linkages and ex-plained phenomena that were previously unexplained.When combined with similar results from other investi-gators, they have created a paradigm shift in ecology.Shigeru Nakano was lost at sea in Baja California onMarch 27, 2000 at the age of 37, but key papers from his15-year career set new standards for rigor, detail, andsynthesis. They continue to be highly cited and inspirenew research, and to foster new collaborations amongJapanese and western scientists.

Keywords Dominance hierarchies Æ Riverscapes ÆReciprocal food-web subsidies Æ Stream ecology ÆSalmonids

Introduction

Some scientists create with their work a watershed di-vide, a tipping point in time when much of the researchand progress that comes afterwards in that field isstrongly influenced by their unique contributions. Inecology, Giorgii Gause’s integration of mathematicalmodels of population growth with laboratory experi-ments to test competition between two species of uni-cellular organisms is one such example (Gause 1934).Raymond Lindeman’s quantitative synthesis of physio-logical and community ecology based on his data ontrophic levels in a lake food web is another such intel-lectual watershed divide (Lindeman 1942), and providedthe genesis for ecosystem ecology (McIntosh 1985). In-deed, many previously unexplained and sometimesunrelated observations suddenly may be explained by anew theory or model, leading to a ‘‘paradigm shift’’(Kuhn 1962) that sets a new baseline for future work.

In many ways, Shigeru Nakano was this sort of sci-entist, whose work helped catalyze a shift by ecologists,especially stream ecologists, toward new and moreproductive research and synthesis. His early studies onthe behavior and ecology of fish in Japanese streamslater expanded to include entire food webs linked acrossstreams and their riparian forests. To develop this syn-thesis, Nakano combined what he learned from studyingindividual components of the stream food web, such asfish and invertebrates, with observations and inferencesabout the ecology of riparian animals like spiders andbirds and bats. Working across the boundaries of taxaand subdisciplines in ecology, he first imagined and thenorganized and carried out pioneering large-scale exper-iments that severed the linkages between streams andtheir riparian forests and measured the drastic responsesin both habitats. Despite his tragic death with four other

Electronic supplementary material The online version of this article(doi:10.1007/s11284-017-1513-9) contains supplementary material,which is available to authorized users.

K. D. Fausch (&)Department of Fish, Wildlife, and Conservation Biology andGraduate Degree Program in Ecology, Colorado State University,Fort Collins, CO 80523, USAE-mail: kurt.fausch@colostate.eduTel.: +1 970 219 2716

Ecol Res (2018) 33: 119–133DOI 10.1007/s11284-017-1513-9

accomplished ecologists in March 2000 (Fausch 2000),the importance of Nakano’s collaborations and contri-butions has grown steadily since. His publications con-tinue to be widely read and cited, and inspire theresearch of others. Moreover, Nakano’s early work onthe individual behavior of stream salmonids, and hislater collaborations to understand their habitats andinterrelationships across local-to-riverscape spatialscales, were also groundbreaking research that hadstrong effects on these subdisciplines of ecology.

In this paper, I address Nakano’s enduring legacy forecology, nearly two decades after we lost him as a sci-entist, colleague, and friend. I first describe his back-ground, both personal and academic, which provided atemplate for both his interests and his drive to pursuethem as a scientist. Next I select key papers from each ofthree main groups in which his work can be categorized,summarize these findings, and show examples of howthese ideas crossed boundaries and set a new standardfor others who followed. Finally, I offer thoughts onwhy Shigeru Nakano’s legacy has endured, and is likelyto continue to inspire ecologists to cross new boundarieswell into the future.

Personal and academic background

Shigeru Nakano grew up in the small town of Kamioka,in the Hida Mountains of Gifu Prefecture in centralJapan, a region of beautiful streams and rivers tumblingthrough steep mountain valleys. Headwater streamsthere are inhabited by iwana, the form of whitespottedcharr (Salvelinus leucomaenis) recognized from this re-gion, and yamame, the river resident form of masu sal-mon (Oncorhynchus masou masou), which are foundfrom the middle reaches downstream (see Kawanabe1989 for common names of salmonids in Japan). Hisfamily often went camping along local rivers andstreams during summer, and Nakano was usually in thewater either fishing or snorkeling (Fig. 1). His motherand aunt ran a banquet restaurant in their home, and thechef told Shigeru stories about traveling deep into themountains to fish for charr, which captivated his interest(see Fausch 2015, Chapter 2). He pleaded with his par-ents to let him attend a private high school in Tokyo sohe could have a better chance to enter a good university,and they let him go. During his first year of high school,Shigeru read an article in a nature magazine written byTetsuo Furukawa, then a graduate student at KyotoUniversity, about studying the microhabitat use andinteractive segregation of whitespotted charr and masusalmon by making observations underwater whilesnorkeling (Furukawa 1978). This sparked Shigeru’simagination about becoming a scientist and using thismethod to study stream salmonids himself one day.

After high school Shigeru Nakano entered theDepartment of Fisheries at Mie University, located onthe Kii Peninsula in south central Japan. There he met

classmate Yukinori Tokuda, who had read the samearticle by Furukawa (1978) while in high school, andthey became best friends. During their second year theybegan traveling to small streams in the mountainsnearby to fish, and bought wetsuits so they could snorkelin the cold water to watch fish for fun. By their thirdyear they were helping Dr. Makoto Nagoshi, a professorat Mie University, with his research on the populationecology of amago, the fluvial redspotted masu salmon(O. masou ishikawai) found in southern Japan, whichinhabits Hirakura Stream on the Mie University Forest.As fourth-year students they also sampled fish by an-gling to conduct stomach analysis and snorkeled tomeasure the depths and velocities at their stream posi-tions (focal points), and these studies resulted in Naka-no’s first publications (Nakano and Nagoshi 1985;Nagoshi et al. 1988).

When Nakano graduated with his undergraduatedegree in Fisheries in March 1985, Nagoshi invited himto pursue a Master’s degree, which he started immedi-ately. Shigeru remembered the article that he and To-kuda had read in high school, and approached Dr.Furukawa-Tanaka (his married name) to learn moreabout his methods of measuring focal points and indi-vidual behavior of stream salmonids by snorkeling(Furukawa-Tanaka 1985, 1988, 1989). Nakano usedthese methods in his research on amago in HirakuraStream, which began in spring 1985 (Nakano 1994). Inaddition, he was invited to study cichlid fishes in Lake

Fig. 1 Shigeru Nakano with a rainbow trout he caught in theTakahara River near his home in Kamioka, Gifu Prefecture, Japan,in August 1987 (image by Y. Tokuda)

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Tanganyika in August and September 1985, as part of aproject led by Dr. Hiroya Kawanabe of Kyoto Univer-sity and Nagoshi. There he was exposed to detailedmethods of underwater observation and recording fishbehavior used by other scientists (e.g., Hori 1983;Kuwamura 1986). Unfortunately, Shigeru contractedmalaria during the expedition, which severely limited thetime available for research. He managed to completeunderwater observations on brood defense by a speciesof cichlid and published a paper from it (Nakano andNagoshi 1990), but the experience confirmed that hisreal interest lay in studying salmonids in mountainstreams.

After finishing his Master’s degree in 1987 (Nakano1987), Shigeru found a temporary position with theTakahara River Cooperative Fishery Union in Kamio-ka, where Yukinori Tokuda had secured a permanentposition, and they often worked together. For example,they conducted some of the first surveys of fish distri-butions throughout headwater streams of the region.After a year, Nakano landed a permanent job as abiologist in a small museum near Kamioka. Thesepositions afforded him a familiar environment in whichto continue pursuing his passion for underwater re-search. Overall, the studies Nakano undertook duringthe summers of 1985 through 1987 while conducting hisMaster’s degree and soon after while working nearKamioka were the first to attract the attention of otherecologists. And, the chance to attend a symposium oncharrs and masu salmon in Hokkaido in 1988 proved tobe a turning point in both his life and mine.

Contributions in three subdisciplines of ecology

Even though Shigeru Nakano’s scientific career waslimited to an approximately 15-year period from his firstpaper in 1985 until his death in 2000, he and his col-laborators were amazingly productive scientists, pub-lishing 111 journal articles and book chapters from theresearch they conducted, 94 in refereed journals, and 86in English (see Electronic Supplementary Material). Ofthese, 41 have been cited in other published papers atleast 41 times each (the h-index; based on GoogleScholar accessed 23 August 2017), and 76 have beencited at least 10 times (the i-10 index). Overall, paperspublished by Nakano either alone or with collaboratorshave been cited about 400 times per year or more everyyear since 2007, and more than 6300 times in total, anastounding number based on a 15-year career. This isespecially impressive for any scientist whose first lan-guage was not English.

Research by Shigeru Nakano alone and with hiscollaborators can be broadly categorized into threegroups: (a) his early work on individual behavior ofstream salmonids in dominance hierarches, (b) researchon the ecology of salmonids at population to landscapescales, and (c) research on stream and forest food webs,

and linkages across the terrestrial-aquatic boundary. Healso conducted additional studies on various otherorganisms and topics in aquatic and terrestrial ecology(e.g., Hino et al. 2002; Taniguchi et al. 2003). Each ofthese categories includes papers that have been cited atleast 100 times, which I arbitrarily consider to be the keypapers from this body of research. Although most ofNakano’s work is considered to fall within the realm ofstream ecology, what made it unique was that it crossedmany boundaries to employ new methods, span acrossdifferent habitats and taxa, and bridge across ecologicalsubdisciplines. Therefore, my goal here is to consider thekey papers in each of the three categories above, anddiscuss why they are unique in crossing these boundariesand thereby setting new standards. In each case I alsoreview a few subsequent papers that used Nakano’swork as a foundation on which to build additional newcontributions in those fields, forming an enduring legacyfor his work.

Individual behavior in stream salmonid dominancehierarchies

During Shigeru Nakano’s research for his Master’s de-gree and the summer afterwards (1985–1987), he con-ducted three highly detailed studies of the individualbehavior of salmon and charr and the mechanisms cre-ating their dominance hierarchies in mountain streamsof central and southern Japan (Fig. 2). Two were carriedout in Hirakura Stream (Nakano 1994, 1995b) whereNakano had worked with Dr. Makoto Nagoshi onamago, the fluvial redspotted masu salmon. The thirdconsidered interspecific dominance hierarchies of ya-mame (resident masu salmon) and iwana (whitespottedcharr) in a stream near Kamioka (Nakano 1995a). Thesestudies were my first introduction to Nakano’s work,and ultimately led to our work together.

Studies of individual behavior of salmonids that livein streams have a long history (Newman 1956; Kalleberg1958), but most had been conducted in artificial streamchannels which have the potential to induce artificialbehaviors. A few early studies in the western UnitedStates were conducted by making observations fromstream banks or platforms (Jenkins 1969) or bysnorkeling (Edmundson et al. 1968; Everest and Chap-man 1972; Griffith 1972). In turn, these led to theoriesand tests of the mechanisms by which salmonids selectforaging position in streams (Chapman 1966; Fausch1984; see Fausch 2014 and Piccolo et al. 2014 for re-views) and early field and laboratory experiments testinghow different species compete for these resources (e.g.,Fausch and White 1981, 1986).

However, underwater observations of stream fishhave a longer history in Japan than North America,owing to the pioneering research of Dr. HiroyaKawanabe on ayu (Plecoglossus altivelis) starting in 1955(e.g., Kawanabe et al. 1956; Kawanabe 1970; see Fauschand Nakano 1998 for a review). Moreover, this research

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began in the Laboratory of Animal Ecology at KyotoUniversity where investigators were already studying theindividual behavior and social systems of primates (Ja-panese macaques; Macaca fuscata) in the mountainsnearby. As a result, research on fish populations in Ja-pan, whether salmonids in streams or cichlids in AfricanRift lakes, began by considering fish as individuals withunique properties and behaviors, rather than as popu-lations of similar individuals as was often assumed inwestern science (Fausch and Nakano 1998). In turn,these individual properties can have effects that influencehow populations of individuals and communities ofinteracting species function. For example, Kawanabe(1969) found that the production of ayu depended on ashift in territorial behavior of individuals that wasinfluenced by density. Nakano and Nagoshi (1990) andKohda (1991) reported that territorial defense amongcichlid fishes in Lake Tanganyika was differentdepending on the function. Feeding territories were de-fended against species with similar foraging habits,whereas breeding territories were defended againstconspecifics, or potential predators of broods of smallfish.

Studies of individual behavior among fishes contin-ued in the Laboratory of Animal Ecology, whichKawanabe directed (e.g., Katano 1985, 1991), but Na-kano was particularly attracted to those by TetsuoFurukawa-Tanaka (Furukawa-Tanaka 1985, 1988,1989). As described above, his early magazine article(Furukawa 1978) had inspired Shigeru to pursue his ownstudies on focal points of stream salmonids in domi-nance hierarchies. In turn, Furukawa-Tanaka had beeninspired by an early paper I wrote developing a theory toexplain such positions (Fausch 1984) and subsequentlyinvited me to Japan to present a paper at the Interna-

tional Symposium on Charrs and Masu Salmon inSapporo in 1988 (Noakes 1989), perhaps with someurging from Nakano (see Nakano 1989).

Shigeru Nakano drew inspiration from this previouswork on fish behavior in North America, Europe, andJapan to create his unique research. His three studiesshowed clearly that stream salmonids like the redspottedmasu salmon and whitespotted charr whose behavior hemeasured in pools of mountain streams in Japan arearranged in linear dominance hierarchies (Nakano 1994,1995a, 1995b). The ranks of individuals in intraspecifichierarchies of the salmon are apparently determined bytheir size, and were often perfectly correlated with theirweight or length. In the most detailed analysis, Nakano(1995b) reported that the summer intraspecific domi-nance hierarchies of salmon were quite stable, withdominant fish holding positions near the head of thepool and closer to the water surface, where they fedmore frequently and on larger prey, and grew faster. Incontrast, subordinate fish had more agonistic encoun-ters, often were forced to flee from attacks, shiftedpositions often, had larger foraging ranges but lowerforaging rates, grew slower, and more often emigratedfrom pools than dominant fish (Nakano 1994). How-ever, in his study of both species in an interspecificdominance hierarchy, Nakano (1995a) found that sal-mon dominated charr, so that only charr more thanabout 40% greater in mass than salmon were clearlydominant. Moreover, salmon grew faster than charrduring summer, causing some individual salmon tosurpass some charr in rank.

What made these studies unique? After all, earlierinvestigators had described linear dominance hierarchiesbased on observations in the field (Jenkins 1969) andlaboratory (Fausch 1984). A primary reason is that

Fig. 2 Shigeru Nakano snorkeling in Shimosaya, Ibaraki Prefecture, Japan, in summer 1988 (image by Y. Tokuda)

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Shigeru Nakano crossed boundaries to adapt and de-velop new methods for observing and mapping positionsand habitat of stream salmonids underwater in naturalstreams (see Fausch 2015, Chapter 2). Moreover, hecollected so much data, and on so many different detailsof individual behavior, that no one could argue with hisconclusions. For example, during the three studies herecorded 856, 2191, and 2835 aggressive encountersfrom which he constructed the dominance hierarchies,and for one study he snorkeled to collect data in onepool during an amazing 41 consecutive days (Nakano1995a). He also collected highly detailed data on fishforaging in another study (Nakano 1995b), as well asmeasuring the diet and growth of individual fish, whichallowed him to relate dominance for stream positionswith the prey fish ate and their growth, a measure offitness. Most importantly, all of this work was doneunder entirely natural conditions in the field, allowinghim to confirm and extend findings previously reportedonly from the laboratory (e.g., Chapman and Bjornn1969; Fausch 1984). Finally, the highly detailed habitatmaps he created from measurements of depth, velocity,and substrate in grid cells often only 10 cm in eachdimension, coupled with simple and elegant analysesand succinct writing, ensured that his papers providedthe highest-quality data and synthesis to that date, andwill stand the test of time into the future. It is not sur-prising that along with a subsequent study of charrforaging (Nakano and Furukawa-Tanaka 1994), thesepapers were cited by one of the leading textbooks ofecology as among the best examples of intraspecific andinterspecific dominance hierarchies (Ricklefs and Miller2000).

As I have described and written about in more detailelsewhere, Shigeru Nakano showed me the results fromthese studies during our first meeting at the symposiumin Sapporo in October 1988 (see the RiverWebs docu-mentary film, http://www.riverwebs.org; Fausch 2015).His careful work and boundless enthusiasm impressedme so much that I later arranged to collaborate withhim, and we conducted four field studies in mountainstreams in Hokkaido, Japan, and Montana, USA, usingthe same methods of snorkeling in pools to measuredetailed microhabitat use and foraging behavior by na-tive charr and trout (e.g., Nakano et al. 1992, 1998). InHokkaido, we followed leads from his earlier collabo-ration with Furukawa-Tanaka (Nakano and Furukawa-Tanaka 1994) and a famous book by Ishigaki (1984)about the mechanisms causing shifts by oshorokoma orDolly Varden charr (Salvelinus malma) from defendingrelatively fixed positions and feeding on drifting inver-tebrates to ranging widely and picking benthic inverte-brates from the substrate (Fausch et al. 1997; Nakanoet al. 1999a). We used a combination of field experi-ments during one summer and underwater observationsacross four summers (Fig. 3) to demonstrate that thisflexible behavior allowed oshorokoma and amemasu (thecommon name for whitespotted charr in Hokkaido) topartition scarce food resources as drifting prey subsided

with declining stream flow through the summer in thesestreams. We proposed this as a key mechanism to ex-plain the coexistence of these two closely-related charr innarrow zones of sympatry in Hokkaido mountainstreams (Fausch et al. 1994; Taniguchi and Nakano2000), and in doing so crossed boundaries to link indi-vidual behavior with the community ecology of thisnative salmonid guild.

Nakano’s most detailed study (Nakano 1995b) isamong his four most highly cited papers, and catalyzedsubsequent research by others worldwide into themechanisms of salmonid foraging and behavior. Manyinvestigators cite his three papers (Nakano 1994, 1995a,1995b) as standard references to describe the first prin-ciples of stream salmonid microhabitat use (e.g., Gowan2007; Harvey and Railsback 2014), and have used thisfoundation to expand our understanding of how andwhy these fishes move to select positions both within andamong pools across reaches. For example, Gowan andFausch (2002) reported that energetically-favorableforaging positions declined throughout summer in aColorado, USA mountain stream as flows and driftingprey declined, and that dominant trout moved withinand among pools, or focused their foraging on terrestrialprey inputs at specific locations within pools, to meettheir energetic needs. Akbaripasand et al. (2014) foundthat subordinate galaxiids in New Zealand streams, andthose fish that grew more slowly, were more likely tomove among pools than dominant fish. These and otherrecent studies (e.g., Urabe et al. 2010; Wall et al. 2016)have also crossed boundaries to link individual behaviorin dominance hierarchies and the energetic tradeoffs atfocal points to population dynamics across entire streamreaches.

Other investigators report that behavioral experienceand genetic factors have strong effects on how domi-nance hierarchies in stream salmonids are structured.For example, White and Gowan (2013) found thatjuvenile brook trout (Salvelinus fontinalis) in laboratorystreams were able to discern their relative rank indominance hierarchies in part by observing the outcomeof interactions among pairs of other fish, a phenomenoncalled transitive inference. This proved most successfulwhen the subjects had interacted directly with one of thepair (see also Hotta et al. 2015 for a test with a cichlidfish). Such social learning allows fish to avoid contestsand injury, thereby increasing fitness, and additionalresearch showed that brook trout in natural streamscould learn to forage on novel prey from conspecifics(White and Gowan 2014). Hughes et al. (2016) reportedthat two life history forms of brown trout (Salmo trutta)from a Scottish loch showed clear differences in domi-nance, even when matched for size and reared in acommon environment, indicating that some combina-tion of genetic makeup or maternal effects accounted forthe differences.

Although it has been more than 20 years since Shi-geru Nakano published his seminal papers on domi-nance hierarchies in stream salmonids, and more than

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30 years since he conducted the research, to date I haveyet to see more comprehensive field studies on this as-pect of the behavioral ecology of these fishes than thosehe conducted. New imaging systems and software areproviding more accurate measurements of fish positions(Vivancos and Closs 2015; Neuswanger et al. 2016), butNakano’s papers are still the standard for defining theprinciples of how salmonid behavior creates the domi-nance hierarchies that are ubiquitous in natural streams.

Ecology of salmonids across local to landscape scales

By the early 1990s, it was becoming evident to animalecologists in general, and those studying salmonids instreams in particular, that predicting the distributionand abundance of fish and other animals depended onthe spatial and temporal scale at which their popula-tions, habitat, and other interacting biota were measured(Wiens 1986, 1989; Fausch et al. 1988; Bozek and Rahel1991). Stream habitat is inherently hierarchical, withclimate, geology, and geomorphology of catchmentssetting the broad-scale template of physical features inwhich the habitat at reach, channel-unit, and micro-habitat scales develops (Frissell et al. 1986; Fausch et al.2002b). In turn, fish evolve in response to this physicaltemplate, and develop life histories, species interactions,population dynamics, and individual behaviors thatinteract across all these scales (Baxter 2002). As a result,relationships between, for example, salmonid densityand habitat characteristics like pool volume are unlikelyto be constant across species or biomes or spatial scales,owing to other interacting factors (Fausch et al. 1988;Inoue et al. 1997; Inoue and Nakano 1998).

Five of the most highly cited papers reporting re-search on which Shigeru Nakano collaborated addressthe ecology of salmonids across spatial scales fromchannel units to entire drainage basins, and across levelsof ecological organization from individuals to commu-nities (Fausch et al. 1994; Inoue et al. 1997; Inoue andNakano 1998; Taniguchi and Nakano 2000; Fauschet al. 2001). In 1989, Shigeru earned a position as anAssistant Professor at the Nakagawa ExperimentalForest of Hokkaido University in northern Hokkaido(see Fausch 2000 for a chronology of his career). Aftergaining funding for our first collaborative field studies in1991 and 1992, Nakano and I conducted research withPh.D. student Satoshi Kitano in a small mountainstream in Hokkaido, part of which was focused onmeasuring what factors accounted for the distribution ofthe native salmonid guild in that catchment and othersacross Hokkaido. We found that temperature was astrong predictor of the largely non-overlapping bound-ary between Dolly Varden charr distributed upstreamand whitespotted charr found downstream in catch-ments across Hokkaido Island, and that the altitude ofthis boundary changed predictably across the islandowing to regional climate driven by ocean currents(Fausch et al. 1994; see Ishigaki 1984 for a previousdescription of the pattern with altitude). However,within the single catchment we studied in detail, charrdistributions differed between the mainstem and tribu-tary, apparently owing to stream discharge and flooddisturbance that affected habitat and populations at thereach scale.

We also conducted detailed research at the scale ofindividual pools along the narrow zone of sympatry, andfound that distribution of the two species apparently

Fig. 3 Shigeru Nakano, Satoshi Kitano, and Kurt Fausch (left to right) on the last day of their first summer of research in PoroshiriStream, Hidaka Mountains, Hokkaido, July 1991

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depended on interspecific competition, which also wasultimately modified by temperature. Long-term labora-tory experiments by Ph.D. student Yoshinori Taniguchiand Shigeru Nakano testing competition between thespecies at cold and warm temperatures subsequentlyshowed that the downstream limit of Dolly Varden charrwas apparently set by the temperature at which they lostcontests for stream positions to whitespotted charr, butthe upstream limit of whitespotted charr was most likelyset by the physiological intolerance of that species tocold temperature, rather than by strong effects of com-petition from Dolly Varden (Taniguchi and Nakano2000). The two species are likely to coexist in the narrowzones of sympatry where they both have positive sur-vival rates (Fausch 2015), and Dolly Varden probablypersist in these places in part because of their ability toshift foraging modes during late summer when prey re-sources are low (Fausch et al. 1997; Nakano et al.1999a). Overall, this set of field and laboratory studiescrossed new boundaries to link the zoogeography of thissalmonid guild with their ecology, physiology, andbehavior, and provides data invaluable for conservingtheir populations in an era marked by warming tem-peratures and a more variable disturbance regime.

The role of large wood that falls into streams increating habitat for stream salmonids also emerged as amajor focus of research during this period (e.g., Naka-mura and Swanson 1993; Richmond and Fausch 1995),but here too the effects are likely to vary across spatialscale. In the early 1990s, graduate student Mikio Inoueand Shigeru Nakano embarked on research across anextensive set of study reaches (n = 36–48 reaches) totest how large wood and its effects in streams differed innorthern Hokkaido compared to other regions, and howmasu salmon responded. They reported that the rela-tively small diameter and short length of the willow(Salix spp.) and alder (Alnus hirsuta) pieces that fell intothe streams they studied had little effect on channelmorphology and pool spacing at the reach scale, but didcreate overhead cover, visual isolation, and velocity re-fuges within individual channel units (pools, runs, andriffles; Inoue and Nakano 1998). Salmon density waslow in reaches adjacent to grasslands, owing to unsuit-ably high water temperatures (Inoue et al. 1997), but inforest reaches it was positively correlated with thephysical structure created by the large wood at bothreach and channel-unit scales (although with variouscontingencies). Overall, they concluded that the role oflarge wood in these streams, and the response of masusalmon to it, depended strongly on the geomorphictemplate, past land uses, and the spatial scale at which itwas measured. Additional research revealed manyimportant relationships between fish and habitat at evenfiner scales within pools (Inoue and Nakano 1999; Inoueand Nunokawa 2002), and at broader scales betweenforest conditions or forestry practices and salmon andcharr populations in streams throughout Japan (Inoueand Nakamura 2004; Inoue et al. 2013).

Nonnative salmonids have strong effects on nativespecies worldwide, and these also vary across scales.Rainbow trout (O. mykiss), originally native only to thePacific coast drainages north of Hokkaido and in west-ern North America (Behnke 2002), were introduced toHokkaido Island and began actively invading in the1980s, but were not invading in Honshu Island, Japandespite large numbers having been stocked there formore than 100 years (Fausch et al. 2001). I became in-trigued by what caused this difference. Working from ahypothesis about differences in flooding regimes acrossthe two islands and among other regions around theworld where rainbow trout were native or had beenintroduced, I collaborated with Taniguchi and Nakanoand several other investigators to assemble and analyzedata on these environmental variables. We found thatrainbow trout invasion success was high in regionswhere the seasonal flooding regime matched that in theirnative range, or where the probability of flooding waslow during the period of trout fry emergence, as inHokkaido (Fausch et al. 2001). In contrast, invasionsuccess was low in regions like Honshu and Coloradowhere floods during fry emergence wash fry away andreduce their survival and growth. Additional research byInoue and Taniguchi and their students in streams ofsouthwest Hokkaido showed that rainbow trout aremore likely to invade and establish reproducing popu-lations in catchments where discharge is stable, such asin spring-fed streams draining volcanic topography,than in streams with higher flow fluctuations (Inoueet al. 2009).

Determining the spatial scales at which salmonidpopulations and communities are related to physical andbiotic features is an active area of research. These pub-lications coauthored by Shigeru Nakano crossedboundaries to assess relationships of salmonids tohabitat and native and nonnative salmonids across awide range of scales, and thereby played an importantrole in fostering new ideas. Although originally coun-terintuitive, salmonids are often found to be morestrongly related to physical features that emerge atriverscape scales than to factors measured at local scales(e.g., Fausch et al. 2002b; Isaak et al. 2007; Flitcroftet al. 2012; Falke et al. 2013). Ongoing research in thisarena, including advances in methods for measuring andmodeling habitats across the entire spatial hierarchy(Peterson et al. 2013; Fullerton et al. 2015), will continueto yield insights and improve management of salmonidsin riverscapes.

Linkages between terrestrial and aquatic ecosystemsin forested streams

In April 1995, Shigeru Nakano moved to the Tomako-mai Experimental Forest of Hokkaido University insouthwestern Hokkaido, and began a new program ofstudy on the relationships between streams and forests.Conservation of biodiversity had become an important

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topic in Japan, as in many countries, and Nakano beganto think creatively about why forests are important tostreams and their biota, and how the streams he studiedalso might be important to the surrounding landscapeand its biological diversity. This latter question rancounter to most of the theory in stream ecology, whichheld that streams are primarily recipients of nutrientsand materials like leaves and wood from the adjacentforests and grasslands (e.g., Minshall 1967; Fisher andLikens 1973; Wallace et al. 1997). This new researchfocus was to become Nakano’s most enduring legacy forecology, and the source of nine of his most cited publi-cations (Nakano et al. 1999b, 1999c; Kawaguchi andNakano 2001; Nakano and Murakami 2001; Murakamiand Nakano 2002; Iwata et al. 2003; Kato et al. 2003;Kawaguchi et al. 2003; Fukui et al. 2006).

Nakano had also become intrigued with manipulativeexperiments in ecology, after participating in the fieldexperiments that I planned and we conducted during1991 and 1992 on foraging mode shifts by charr inHokkaido (Fausch et al. 1997), and those he planned oninterspecific interactions among native and nonnativesalmonids in Montana (Nakano et al. 1998). I recallwhen visiting him in northern Hokkaido during summer1994 that he asked me about experimental designs andthe statistics used to analyze them, which he then beganstudying on his own. Moreover, his former graduatestudents and collaborators from that era (Mikio Inoue,Yoichi Kawaguchi, Naotoshi Kuhara, Yo Miyake,Hirokazu Urabe) reported that while driving through anagricultural landscape during 1993 or 1994 Nakanorealized that the streams he studied could fit inside astandard greenhouse (Fig. 4), and that he could use

them to experimentally cut off inputs of terrestrialinvertebrates to streams.

These ideas led to the first three studies of theimportance of inputs of terrestrial invertebrates tostream fish, and the cascading top-down effects theyproduce in stream food webs (Nakano et al. 1999b,1999c; Kawaguchi and Nakano 2001). For this trio ofstudies, Nakano and his colleagues combined observa-tional and experimental approaches, a particularlyeffective strategy in any ecological research. They cros-sed both methodological boundaries, by being the firstto enclose a stream with a greenhouse to sever its con-nections with the riparian forest, and disciplinaryboundaries by moving beyond a focus on salmonidfishes and their invertebrate prey to food-web interac-tions that extended to streambed algae. First, in March1995, Kawaguchi and Nakano began a year-long sam-pling program of the inputs of terrestrial invertebrates,biomass of benthic invertebrates, biomass of driftingprey of both types, and prey in fish diets. They sampledeach component at frequent intervals in stream reachesadjacent to forest versus grassland riparian zones alongHoronai Stream, which traverses the TomakomaiExperimental Forest. For a month from late July to lateAugust that year, Nakano and six graduate students andcollaborators sampled these same characteristics inten-sively (e.g., inputs of terrestrial invertebrates were sam-pled every day, and every 4 h for 6 days), focusing ondiet selectivity by rainbow trout. In addition, in Juneand July 1995, Nakano and several graduate studentserected greenhouses covered with plastic sheeting overfour 50-m fenced reaches of the stream, and comparedthe effects of excluding terrestrial invertebrates and

Fig. 4 Shigeru Nakano describing the greenhouse frame used for experiments to cut off flows of invertebrates to and from HoronaiStream, July 1999 (image by M. Murakami)

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adding Dolly Varden charr on stream food webs in afactorial design including controls.

The results of these studies were striking. Salmonidbiomass in the forested reach was two to three times thatin the grassland reach, and this matched the annual in-puts of terrestrial invertebrates, which were nearly twiceas high in the forested reach (Kawaguchi and Nakano2001). Rainbow trout were highly selective for terrestrialinvertebrates, which were larger than larvae and adultsof aquatic insects, and drifted during periods when thetrout fed most (Nakano et al. 1999b). Cutting off inputsof terrestrial prey with the greenhouses forced DollyVarden to shift to foraging on benthos, which Nakanoknew from our earlier work is a shift at which they areadept (Fausch et al. 1997; Nakano et al. 1999a). Thisintense predation reduced herbivore benthos to about athird the biomass in control reaches (with no greenhouseor charr), which released streambed algae from grazingand caused an increase in algal biomass of about 60% ina trophic cascade (Nakano et al. 1999c). The amazingresults of this large-scale manipulation drew immediateattention from stream ecologists, including those whohad conducted similar research in northern California(Sabo and Power 2002a, 2002b). On reading the paper,my colleague LeRoy Poff changed the lecture on streamfood webs that he was about to present in his course onStream Ecology to include Nakano’s study (Fausch2015).

Observations during the first greenhouse experiment,and of Horonai Stream in general, also led Nakano torealize that insects emerging from the stream could beimportant to riparian predators like birds, bats, andspiders. Each morning Nakano drove along the stream,which ran close to the forest road from his home to hisoffice, and he often observed birds foraging there in allseasons. His former graduate students related that hehad also discovered a short paper in a regional journalfrom the midwestern US which reported the importanceof insects emerging from a prairie stream in Kansas tograssland birds, and the concentration of bird foragingnear the stream during periods of peak emergence inearly summer (Gray 1993; M. Inoue, Y. Kawaguchi, N.Kuhara, personal communication). In addition, duringthe experiment in 1995, insects emerging from the streamcollected rapidly underneath the greenhouse cover,requiring Nakano and his colleagues to first attempt tocapture them with sticky traps and then to simply cut awindow in each end to allow them to escape (Nakanoet al. 1999c; M. Murakami, personal communication).To explore these ideas, he began collaborating withPh.D. student Masashi Murakami, who had done re-search on forest birds, their foraging on terrestrial in-sects that damage riparian trees and shrubs, and thepotential for indirect effects among these food-webmembers (Murakami 1998, 1999; see also Murakamiand Nakano 2000).

Based on these observations, Nakano and Murakamideveloped the idea that ‘‘reciprocal’’ subsidies fromstream to forest could also be important to riparian

predators during different seasons, and conducted an-other trio of comparative and experimental studies totest it. During a 14-month period from May 1997 toJune 1998 they measured fluxes of invertebrates in bothdirections, and use of these prey resources by birds andfish. Then during summer 1999 Nakano and his col-leagues constructed a 1.2-km fine-meshed greenhouseover Horonai Stream, and installed it again in 2000.They measured spider abundance next to the greenhouseand in 600-m control reaches upstream and downstream(separated by a 100-m buffer), and bat foraging usingultrasonic detectors adjacent to the treatment reach andin a 1.2-km control reach downstream.

Here again, the results were striking. In the compar-ative study, Nakano and Murakami (2001) found that,on average, 26% of the annual energy budgets of 10forest birds came from adult aquatic insects emergingfrom the stream, based on > 13,400 observations ofbird foraging, with the highest proportions occurringduring winter and early spring when terrestrial inverte-brates were scarce. Conversely, an average of 44% of theannual energy budgets for the five stream fishes wasderived from terrestrial invertebrates that fell into thestream, based on > 1400 stomach samples flushed fromfish, with the highest proportions during summer andfall after most adult aquatic insects had emerged anddrifting aquatic invertebrates were primarily small lifestages (instars). Mary Power (2001) reported that thisintensive year-round study was the best demonstrationin any ecosystem of the seasonal shifts of cross-habitatresources subsidies, and that this complementarity ofresource pulses across the habitat boundary maintainedhigher densities, and possibly diversities, of both birdsand fishes than would otherwise be supported.

Results from the two experiments with the longgreenhouse were equally remarkable. Spiders that weavehorizontal orb webs to catch emerging insects (FamilyTetragnathidae) were reduced by about 60–80% duringMay through July in the riparian zone adjacent to thegreenhouse that excluded emerging aquatic insects onwhich they rely, whereas two other spider guilds thatforage on terrestrial arthropods were not reduced (Katoet al. 2003). In a similar fashion, during May whenaquatic insect emergence was highest, foraging by batswas 97% lower adjacent to the greenhouse than in thecontrol reach, even though there was no difference inforaging in the two reaches the next year when only thegreenhouse frame was left standing (Fukui et al. 2006).These results matched those of Sabo and Power (2002a,2002b) who found that riparian lizard abundance andgrowth were much lower where emerging insects wereexcluded from the riparian zone of the Eel River innorthern California, USA compared to controls (seeBaxter et al. 2005 for a review).

Nakano and his students and collaborators continuedto conduct experiments on these reciprocal subsidies andtheir effects on biodiversity and food web functionsusing fine-meshed greenhouses to cover Horonai Stream(Fig. 5), and mesh covers over riparian shrubs, eventu-

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ally completing a total of five major experiments andeight studies, before and after Nakano’s death (Nakanoet al. 1999c; Murakami and Nakano 2002; Kato et al.2003; Kawaguchi et al. 2003; Baxter et al. 2004, 2007;Fukui et al. 2006; Nakano et al. unpublished). Theseshowed, for example, that emerging aquatic insects hadpositive indirect effects on riparian shrubs during springby drawing birds into the riparian zone. These birds notonly fed on the emerging insects but also gleaned ter-restrial invertebrates from shrubs that normally damagetheir leaves (Murakami and Nakano 2002). In turn,cutting off the input of terrestrial invertebrates intostreams using greenhouses, which provides about half ofthe annual prey biomass and annual energy budget forstream fish (Kawaguchi and Nakano 2001; Nakano andMurakami 2001), either caused half the fish biomass toemigrate (Kawaguchi et al. 2003) or, if fish were en-closed, it reduced their growth markedly (Baxter et al.2007) and caused them to crop the benthos drastically(Baxter et al. 2004; see Fausch et al. 2010 for a review).In turn, the reduced benthos resulted in markedly re-duced insect emergence, a predictable decline in tetrag-nathid spider abundance, and a trophic cascade that

increased biomass of streambed algae (Baxter et al.2004). These different forms of indirect effects, depend-ing on whether predators are enclosed or free to move,fostered new ecological theory and modeling to incor-porate these important elements of complexity in realfood webs (Takimoto et al. 2002, 2009). This feedbackwhereby empirical research does not simply respond bytesting ecological theory, but indeed directs its devel-opment, is exactly the boundary that Gary Polis (1991)had proposed needed to be crossed. Likewise, the desirefor a more dynamic interaction between theory andempiricism was arguably one of the motivations thatdrew Nakano, Polis, and Mary Power together duringNakano’s fateful visit to California and Mexico inMarch 2000 (C. Baxter, personal communication).

These innovative studies first pioneered by ShigeruNakano and Mary Power and their colleagues, and thegrueling field and laboratory work accomplished bythem and their many collaborators, resulted in a para-digm shift (sensu Kuhn 1962) in the study of streams,their riparian habitats, and the diverse plants and ani-mals that occupy them. These investigators crossedmany boundaries by employing new methods, spanningacross adjacent habitats and different taxa, and mostimportantly, helping build a strong bridge between thedisciplines of food web and landscape ecology (see Poliset al. 2004). This research spawned a host of additionalmanipulative experiments excluding or adding preysubsidies for either aquatic or riparian predators (e.g.,Paetzold et al. 2006; Marczak and Richardson 2007;Eros et al. 2012; Sato et al. 2016). Additional researchthat Nakano participated in or inspired has addressedthe spatial and temporal heterogeneity of invertebratesubsidies and how it influences the distribution ofpredators like birds and spiders at different spatial scales(Iwata et al. 2003, 2010; Iwata 2007; Uesugi and Mur-akami 2007), and new research has revealed how spatialsubsidies of invertebrates stabilize resource fluxes inspatially and thermally heterogeneous river-tributarynetworks (Uno and Power 2015; Uno 2016). Recentmeta-analyses have shown that fish predation reducesadult aquatic insects that emerge to feed terrestrialpredators by about 40% (Wesner 2016), and that eventhough the flux of terrestrial prey to streams is nearly anorder of magnitude higher than aquatic prey to riparianzones, the contribution of aquatic prey to terrestrialpredators is apparently much higher than of terrestrialprey to aquatic predators (Bartels et al. 2012).

Another set of studies has crossed disciplinaryboundaries by applying these concepts to the conserva-tion biology of managed ecosystems. These investigatorshave assessed how the effects of human land uses such ascattle grazing (Saunders and Fausch 2007, 2012), log-ging (Inoue et al. 2013), and mining (Kraus et al. 2016),as well as the introduction and invasion of species likenonnative trout (Baxter et al. 2004, 2007; Benjamin et al.2011, 2013; Lepori et al. 2012) and global climate change(Larsen et al. 2016), can all have strong effects on theprocesses that produce or shape the flux of invertebrate

Fig. 5 Nakano’s greenhouse used by Colden Baxter and colleaguesto conduct experiments in summer 2002 on the combined effects ofnonnative trout and cutting off flows of invertebrates betweenHoronai Stream and its riparian forest (image by C. Baxter)

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prey across the stream-riparian boundary. For example,Benjamin et al. (2013) reported that nonnative brooktrout reduced the emergence of adult aquatic insects by55% compared to native cutthroat trout (O. clarkii), andprojected that this was sufficient to eliminate emerginginsects from the diets of two-thirds of riparian birds thatdepend, in part, on this food source. Kraus et al. (2016)reported that trout in streams polluted by heavy metalsfrom mining increased their reliance on terrestrialinvertebrate prey as in situ aquatic prey were lost owingto the metal pollution.

Conclusion: an enduring legacy for ecology

It is clear from this brief review of only the most highlycited papers published by Shigeru Nakano and his col-leagues that this body of research has created anenduring legacy for ecology. His early work on thebehavioral ecology of stream salmonids set a new stan-dard for detail and rigor in natural settings, and hasinspired others to conduct additional studies aimed atsimilarly detailed questions for salmonids and otherdrift-feeding stream fish in diverse locations worldwide.Likewise, his collaborative research on salmonids acrossspatial scales has inspired other Japanese and western

scientists alike to seek this kind of synthesis in othersystems.

And for ecology in general, his innovative manipula-tions of linkages between stream and riparian food websset new standards for holism and rigor in food webecology, expanding our horizons to the landscape scalebut with close attention to resolving the details of phe-nology, diet, and behavior of the species involved (Power2001; Fausch et al. 2002a). Indeed, I can offer no bettertribute than a recent personal communication fromMary Power, whose own work independently sought toanswer many similar questions about river-watershedexchanges. She wrote ‘‘Shigeru Nakano’s legacy is verystrong still today. He inspired a huge number of ecolo-gists, and especially young Japanese ecologists, to doexperimental work and to think at landscape scales aboutterrestrial-river interactions. He was an extraordinaryfigure in world ecology, and his tragic early loss has notdiminished his strong legacy, thanks to devoted friendsand colleagues and the many students he inspired.’’

One of Shigeru Nakano’s most indelible contribu-tions is the many graduate students and postdoctoralscientists he mentored, his own and those of other aca-demic colleagues. During his 15-year career those withwhom he published papers number more than 30, andmany of these have become accomplished professors and

Fig. 6 Faculty and graduate students assembled at TomakomaiExperimental Forest on June 15, 2003, many of whom wereconducting studies inspired by the research of Shigeru Nakano.From left to right: Back row – Kurt Fausch, Masashi Murakami,Colden Baxter, Masataka Miura, Toshihide Hirao, Koh Hasega-

wa, Kenta Tanaka, Yoshinori Taniguchi, Scott Laeser, DaisukeKishi, Tsutomu Hiura. Middle row (right of center): Mikio Inoue,Hiroshi Miyata, Hiromitsu Kamauchi, Dai Fukui, Taro Tosuji.Front row (kneeling): Maiko Hotta, Emiko Kubota, EriNabeshima, Michiko Matsuda, Fumie Okabe, Akane Uesugi

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research scientists in their own right. Each carriesunforgettable memories about their years in the ‘‘Na-kano school’’ and all that Shigeru taught them aboutresearch and life, and each has passed those lessons onto their own students and colleagues. Finally, perhaps anunappreciated aspect of Shigeru Nakano’s legacy is theongoing interaction and collaboration he inspiredamong those of us who followed the clues he left andconducted additional research that honors his work(e.g., see RiverWebs documentary film; Fausch 2015).These experiences have forged new friendships andconnections that span the globe (Fig. 6) and continue tofoster reciprocal collaborations and new research andsynthesis among Japanese researchers and western sci-entists that are advancing ecological research worldwide(e.g., Dunham et al. 2008; Fausch et al. 2010; Richard-son and Sato 2015; Sato et al. 2016).

Acknowledgements This manuscript is based on an invited keynotepresentation for a special session at the 2017 Ecological Society ofJapan annual meeting honoring Shigeru Nakano’s legacy, orga-nized by Jotaru Urabe, Yoshinori Taniguchi, and Itsuro Koizumi. Ithank the organizers for inviting me, Yoshinori Taniguchi forresearching information on many aspects of Nakano’s early career,Masashi Murakami for providing current references on food websand reciprocal subsidies, and Mary Power for her thoughts onNakano’s legacy. Taniguchi, Murakami, Mikio Inoue, TomoyaIwata, Colden Baxter, and an anonymous reviewer offered con-structive comments that helped improve the manuscript.

Open Access This article is distributed under the terms of theCreative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricteduse, distribution, and reproduction in any medium, provided yougive appropriate credit to the original author(s) and the source,provide a link to the Creative Commons license, and indicate ifchanges were made.

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