(SpringerBriefs in Biology) Noboru Okuda, Katsutoshi Watanabe, Kayoko Fukumori, Shin-ichi Nakano, Takefumi Nakazawa (auth.) - Biodiversity in Aquatic Systems and Environments_ Lake Biwa-Springer Japan.pdf

SPRINGER BRIEFS IN BIOLOGY
Noboru Okuda · Katsutoshi Watanabe
Kayoko Fukumori · Shin-ichi Nakano
Takefumi Nakazawa
Biodiversity
in Aquatic
Systems and
Environments
Lake Biwa
123
SpringerBriefs in Biology
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Noboru Okuda • Katsutoshi Watanabe
Kayoko Fukumori • Shin-ichi Nakano
Takefumi Nakazawa
Biodiversity in Aquatic
Systems and Environments
Lake Biwa
Noboru Okuda Katsutoshi Watanabe
Center for Ecological Research Department of Zoology
Kyoto University Graduate School of Science
Otsu, Japan Kyoto University
Kyoto, Japan
Kayoko Fukumori
Section of Integrative Biology Shin-ichi Nakano
The University of Texas at Austin Center for Ecological Research
Austin, TX, USA Kyoto University
Otsu, Japan
Takefumi Nakazawa
Department of Life Sciences
The College of Biosciences
and Biotechnology
National Cheng Kung University
Tainan, Taiwan
ISSN 2192-2179 ISSN 2192-2187 (electronic)

ISBN 978-4-431-54149-3 ISBN 978-4-431-54150-9 (eBook)
DOI 10.1007/978-4-431-54150-9
Springer Tokyo Heidelberg New York Dordrecht London
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Foreword
While the twentieth century was the century when researchers tried to discover “the
general basic principles of organisms,” the twenty-first century is expected to be the
century when researchers try to understand “the evolution and diversity of organ-
isms” on the basis of such general principles of organisms by integrating various
disciplines such as morphology, physiology, and ecology.
The chief difficulty in studying “the evolution and diversity of organisms” lies in
the fact that we have to consider factors at various levels ranging from the genome
to the ecosystem. As taking various factors into account may cause a loss of focus,
traditional studies have been restricted to analyzing only one individual level or fac-
tor. However, unfortunately, the current research and education system based on
such a compartmentalized approach is inadequate for incisively studying “the evo-
lution and diversity of organisms.”
In order to solve these problems, we should strongly emphasize the necessity for
joint studies and integration of the education programs between micro-level biology
(genomic science, evolutionary developmental biology, genetic science, cell biol-
ogy, neurobiology, molecular physiology, and molecular evolutionary studies) and
macro-level biology (primatology, anthropology, ethology, environmental biology,
evolutionary taxonomy, and so on) to young biologists. We launched a new educa-
tion program in Kyoto University, called “Global COE program for Evolution and
Biodiversity Research” to promote such integrative studies at various levels, and
have succeeded in initiating novel currents of study of biodiversity that led rather
than followed those in the rest of the world. To this aim, we decided to publish six
books in “SpringerBriefs in Biology” which we hope will stimulate interest in such
novel approaches on the evolution and diversity of organisms in the world and
among young biologists.
This book covers a broad range of aquatic biology from molecular biology,
through ecology, to paleobiology in Lake Biwa, a fascinating ancient lake that is
also famed as a biodiversity hotspot. It will be a useful resource not only for
researchers and technicians but also for graduate students who want to learn aquatic
science. Naturalists and nature lovers can enjoy here a virtual tour of the world of
biodiversity in this ancient lake. That biodiversity ranges over vast differences of
v
vi Foreword
scale: We describe the latest molecular genetics techniques that have revealed a
relationship between the lake’s microbial diversity and its ecosystem functioning.
We also describe the evolutionary history of the lake’s biodiversity, especially fish
diversity, as well as laboratory experiments that revealed that diversity of fish feed-
ing morphology affects the body size of plankton communities and consequently
the overall ecosystem properties.
Unfortunately, Lake Biwa is also known as a tragic lake which has suffered from
a variety of human disturbances, such as eutrophication, habitat destruction, exotic
species introduction, and global warming, and that is now threatened by biodiver-
sity loss and ecosystem deterioration. This book thus will appeal to conservationists
and policy makers who are interested in biodiversity conservation and ecosystem
management. As well, it will provide an opportunity for all readers to think deeply
about the need to conserve the earth’s biodiversity.
Kiyokazu Agata
Professor, Department of Biophysics, Kyoto University
Project Leader of Kyoto University Global COE program
“Evolution and Biodiversity”
Preface
Two decades have passed since the Earth Summit, at which the Convention on
Biological Diversity (CBD) came into force to encourage the conservation of bio-
logical diversity on the earth and the fair and equitable sharing of benefits arising
from the sustainable use of its components. At present, the loss of biological diver-
sity has progressed at an accelerating rate and is particularly severe in freshwater
ecosystems, in which environmental alterations have been extreme due to drastic
changes in land-use patterns. For most of us, it is intuitively understandable why
fishery resources should be conserved, because they provide humankind with ben-
efits such as food sources, i.e., a provisioning service from aquatic ecosystems.
However, it is not so easy to answer the question of why fish diversity is necessary
for human well-being. We also have little knowledge on how diversity of other
aquatic biota, especially of microbes, affects ecosystem properties such as organic
production, water purification, and nutrient cycling. Or rather, we human beings
have no inherent sense to discern the invisible nature of diversity in a microscopic
world. For aquatic biologists, therefore, it is a great challenge to perceive the entity
of biological diversity in aquatic ecosystems, trace its evolutionary history, and dis-
cover the ecological consequences of its evolutionary diversification, toward the
integration of biodiversity sciences.
Here we introduce the latest topics of ecological and evolutionary research on
aquatic biological diversity from bacteria to fishes, with special reference to the case
of Lake Biwa. Lake Biwa, in western Japan, is an ancient lake with a geological
history of four million years, making it the third oldest lake in the world. It is called
a biodiversity hotspot, where 1,769 aquatic species including 61 endemics are
recorded, providing a rare opportunity to study the evolutionary diversification of
aquatic biota and its ecological consequences. In this book, we first narrate the evo-
lutionary history of biological diversity, especially of fish diversity in this lake,
focusing on its paleogeography and molecular phylogeny (Chap. 1 by Katsutoshi
Watanabe). The reader will learn how physical features of the lake have promoted
evolutionary diversification of feeding functions in fishes.
vii
viii Preface
Functional diversification of fishes, which play important ecological roles as

keystone predators of lake ecosystems, can sometimes be a major driver for altering
an entire lake community through their top-down trophic cascading effects (Chap. 2
by Noboru Okuda and Kayoko Fukumori). We demonstrate that predator functional
diversity has the potential for altering species composition, size structure, and tro-
phic relations of an entire biological community, which in turn affects ecosystem
functioning such as energy flows and nutrient cycling.
In lakes, the leading actors in ecosystem functioning, such as production and
mineralization of organic matter, are microbes, which are often regarded as ecosys-
tem engineers altering aquatic environments because of their overwhelming domi-
nance in number and mass. A few decades ago, the diversity of aquatic microbes in
nature remained unexplored because a large portion of bacteria never grow under
cultivation to be isolated for taxonomic identification. However, the recent explo-
sion of advances in molecular techniques has vigorously encouraged microbiolo-
gists to characterize genetic and functional diversity of in situ microbial communities
(Chap. 3 by Shin-ichi Nakano).
While respecting the blessings of invaluable biological diversity in lake ecosys-
tems, we have to warn that modern human activities have brought a crisis of biodi-
versity loss in lakes worldwide, which will result in deterioration of ecosystem
functioning and thus of ecosystem services. In the face of such human disturbances,
ecosystem alterations are often catastrophic, a phenomenon known as ecological
regime shift. To understand how human-mediated environmental changes can
induce regime shifts in lake ecosystems and to evaluate how their biological diver-
sity, especially intraspecific phenotypic diversity, affects ecosystem resilience, i.e.,
dampening the incidence and intensity of regime shifts, a promising approach is
construction of theoretical models, which is considered a kind of thought experi-
ment to test probable future scenarios (Chap. 4 by Takefumi Nakazawa).
Again, we stress that Lake Biwa can be an ideal model system in which to prac-
tice biodiversity conservation with the promotion of ecological and evolutionary
understanding of biological diversity in lake ecosystems. This opportunity exists
because Lake Biwa has experienced a variety of serious environmental problems
that are shared by many other lakes worldwide, and also because the lake currently
shows symptoms of recovery from the biodiversity loss and ecosystem deteriora-
tion, recognized only by our persistent efforts in biodiversity research. Through this
book, the reader will learn how the evolutionary diversification of aquatic organ-
isms interplays with the ecology of their populations and communities, and vice
versa, and why we should conserve biological diversity at different levels of bio-
logical organization from genes to ecosystems.
Otsu, Japan Noboru Okuda

Contents
1 Origin and Diversification of Freshwater Fishes in Lake Biwa .............. 1

1.1 Introduction: Lake Biwa and Its Fish Fauna ........................................ 1
1.2 A Brief Review on the Origins and Evolution
of Freshwater Fishes ............................................................................ 8
1.3 Molecular Phylogenetic Approaches ................................................... 10
1.3.1 Origin of Endemic Lineages .................................................... 10
1.3.2 Population Establishment by Endemic
and Non-endemic Species........................................................ 14
1.4 Conclusions and Perspectives .............................................................. 15
References ..................................................................................................... 17
2 Predator Diversity Changes the World: From Gene to Ecosystem ........ 21
2.1 Why is Biodiversity Important? ........................................................... 21
2.2 Biodiversity at Three Levels ................................................................ 22
2.3 What is Phenotypic Polymorphism? .................................................... 22
2.4 Phenotypic Polymorphism in Aquatic Ecosystems ............................. 23
2.4.1 Trophic Polymorphism and Adaptive Divergence ................... 23
2.4.2 Ecological Speciation and Species Pair ................................... 25
2.4.3 The Ancient Lake Biwa as an Evolutionary Hot Spot ............. 26
2.4.4 Life History Polymorphism ..................................................... 27
2.4.5 Rapid Evolution of Trophic Polymorphism ............................. 28
2.4.6 Genetic Mechanisms of Trophic Polymorphism ..................... 30
2.5 Niche Construction .............................................................................. 31
2.6 Predator Diversity and Ecosystem Functioning................................... 33
2.6.1 Mesocosm Experiments ........................................................... 35
2.6.2 Food Web Properties as a Universal Measure ......................... 37
2.7 Eco-Evolutionary Feedbacks ............................................................... 40
2.7.1 Feedback Loops ....................................................................... 41
2.7.2 Community Genomic Dynamics ............................................. 43
2.8 Why is Predator Diversity Important? ................................................. 44
References ..................................................................................................... 45
ix
x Contents
3 Biodiversity Researches on Microbial Loop in Aquatic Systems............ 51

3.1 Introduction.......................................................................................... 51
3.2 Towards More Complicated Microbial Food Web............................... 52
3.3 Detection of Microorganisms Using Molecular
Biological Techniques.......................................................................... 54
3.3.1 Biodiversity of Bacteria ........................................................... 54
3.3.2 Biodiversity of Protists ............................................................ 56
3.4 Recent Development in Studies on Food Chain
Between Bacteria and Protists ............................................................. 57
3.5 Predation on Protists ............................................................................ 59
3.6 Biodiversity Researches on Microbial Loop in Lake Biwa ................. 59
3.7 Concluding Remarks ........................................................................... 61
References ..................................................................................................... 62
4 A Dynamic Resilience Perspective Toward Integrated Ecosystem
Management: Biodiversity, Landscape, and Climate .............................. 69
4.1 Introduction.......................................................................................... 69
4.2 Regime Shift and Resilience as Key Concepts
in Ecosystem Management .................................................................. 70
4.3 Regime Shifts Mediated by Ontogenetic Niche Shifts ........................ 72
4.4 Effects of Ecological Contexts on the Occurrence
of Regime Shifts Mediated by Ontogenetic Niche Shifts .................... 75
4.4.1 Food-Web Topology ................................................................ 76
4.4.2 Spatial Configuration ............................................................... 78
4.4.3 Seasonality ............................................................................... 81
4.4.4 Other Factors............................................................................ 83
4.5 Toward Integrated Ecosystem Management ........................................ 85
4.5.1 From Static to Dynamic Resilience Perspectives .................... 85
4.5.2 Implications for Lake Ecosystem Management....................... 86
References ..................................................................................................... 88
Chapter 1
Origin and Diversification of Freshwater
Fishes in Lake Biwa
Abstract Lake Biwa is the largest and oldest lake in Japan. It harbors more than a
thousand animal and plant species, including 67 indigenous freshwater fish species/
subspecies with 16 endemic or semi-endemic forms. Paleogeographical and paleonto-
logical studies have revealed that the location and environment of the lake have
changed during its history of more than four million years. The current Lake Biwa,
with its unique environments, was established 0.4 million years ago. Endemic fishes
in Lake Biwa are traditionally divided into old “relict species” and new “species that
evolved in the lake,” the latter being assumed to have evolved through ecological
adaptations to the present lake environment. However, recent molecular phylogenetic/
population genetic analyses have revealed that many of the “species that evolved in
the lake” have origins that are older than the present Lake Biwa, while other species
likely evolved in the present environment through ecological adaptation. On the other
hand, many fish populations that inhabit Lake Biwa, irrespective of their origin, show
similar patterns involving recent population expansions that occurred several tens of
thousands of years ago. Extensive community level analyses of “lacustrine syn-
dromes” that are found in Lake Biwa are necessary based on morphology, physiology,
phylogenetics, population genetics, and also new “omics” approaches.
Keywords Adaptation • Ancient lake • Divergence time • Ecological speciation •

Endemic species • Fossil records • Mitochondrial DNA (mtDNA) • Phylogeny •
Phylogeography
1.1 Introduction: Lake Biwa and Its Fish Fauna
Lake Biwa, located in central Honshu Island, Japan (35°20′N, 136°10′E, 84.4 m
above sea level), is a representative ancient lake in East Asia. It is the largest lake in
Japan in terms of surface area (670.3 km2) and volume (27.5 km3), and is also the
oldest lake in Japan, with its origin dating back to four million years ago (Mya)
N. Okuda et al., Biodiversity in Aquatic Systems and Environments: 1

Lake Biwa, SpringerBriefs in Biology, DOI 10.1007/978-4-431-54150-9_1,
2 1 Origin and Diversification of Freshwater Fishes in Lake Biwa
Fig. 1.1 Changes in the position of Paleo-Lake Biwa. (1) Lake Ohyamada (>3.2 Mya), (2) Lake
Ayama (3.0–2.7 Mya), (3) Lake Koka (2.7–2.5 Mya), (4) Lake Gamo (2.5–1.8 Mya), (5) Lake
Katata (1.0–0.4 Mya), (6) “present” Lake Biwa (<0.4 Mya). Drawn mainly based on Kawabe
(1994). The names and ages of the paleo-lakes follow the Research Group for Natural History of
Lake Biwa (1994)
(Yokoyama 1984; Kawabe 1994). Like other ancient lakes, Lake Biwa harbors
many species (>1,000), including diverse endemic animal and plant taxa (~60 spe-
cies/subspecies; Nishino 2003; Nishino and Hamabata 2005). Thus, it has been rec-
ognized as a central research area for studying the biodiversity and speciation of
freshwater organisms in Japan (Kawanabe 1996; Rossiter 2000).
Lake Biwa is primarily divided into southern and northern basins. The southern
basin is small (52.5 km2; 7.8 % of total lake area) and shallow (average depth, 4 m;
maximum depth, <7 m). In contrast, the northern basin has a large (617.8 km2;
92.2 %), deep (average depth, 43 m; maximum depth, 103.6 m) pelagic zone and
heterogeneous bottom features, which characterize the unique environment of the
lake. However, these characteristic features of Lake Biwa formed over the last 0.3–
0.4 million years (Myr), which encompasses the last one-tenth of the lake’s long
history (Fig. 1.1; Yokoyama 1984; Meyers et al. 1993; Kawabe 1994). Lake Biwa
was born as a shallow subtropical lake about 4–6 Mya and was located southeast of
1.1 Introduction: Lake Biwa and Its Fish Fauna 3
Fig. 1.2 Nested structure of the freshwater fish fauna of Japan, as represented by a parsimony
analysis of endemicity (PAE). (a) The regional division of the main islands of Japan based on the
major watersheds and straits. (b) Strict consensus area cladogram and (c) nested structure of
endemic areas calculated by PAE using distribution data for Japanese freshwater fishes. Each verti-
cal bar on a branch in (b) represents an “apomorphic” (=endemic) fish form with consistency
index = 1.0, according to the DELTRAN reconstruction. Solid and dashed surrounding area(s) in
(c) indicate endemic areas defined by one and more than one endemic fish form, respectively.
Modified from Watanabe (2012)
its present position (the Ueno Basin, Mie Prefecture) (Kawabe 1994; Yokoyama
1984). After experiencing drastic geological changes (e.g., Yokoyama 1968, 1984),
the lake reformed about 1 Mya in the location of the current southern basin; the
transition was followed by the formation of the northern basin (<0.4 Mya).
The unique fish fauna of Lake Biwa has been repeatedly emphasized (e.g., Tanaka
1908; Annandale 1922; Tomoda 1978, 1991; Takahashi 1989; Yuma et al. 1998). The
Kinki region, including the freshwater system of Lake Biwa and the Yodo River (the
only outflow of the lake), is recognized as one of the cores of endemism of Japanese
freshwater fish fauna (Fig. 1.2; Watanabe 2012). Among the 312 freshwater fish forms
(species/subspecies) found in the Japanese and Ryukyu Archipelagos that were listed
in Kawanabe et al. (2001), 85 forms (including recently divided species) are found in
Lake Biwa and its inlets. Among the latter, 67 forms are likely indigenous and 16
forms are endemic or semi-endemic to Lake Biwa (Table 1.1).
4
Table 1.1 Fishes in Lake Biwa and its tributaries

Endemic/
Scientific name Standard name semi-endemic Extinct Native Domestic alien Foreign alien
Pteromyzontidae (2; 0)
1 Lethenteron reissneri Sunayatsume (Southern sp.) x
2 Lethenteron sp. N Sunayatsume (Northern sp.) x
Anguillidae (1; 0)
3 Anguilla japonica Unagi x x
Osmeridae (1; 0)
1
4 Hypomesus nipponensis Wakasagi x

5 Plecoglossus altivelis Ayu x
Salmonidae (4; 1)
6 Oncorhynchus masou subsp. Biwamasu x x
7 Oncorhynchus masou ishikawae Amago x x
8 Oncorhynchus masou masou Yamame x x
9 Salvelinus leucomaenis Iwana x x
10 Oncorhynchus mykiss Nijimasu x
Cyprinidae (36; 8)
11 Nipponocypris temminckii Kawamutsu x
12 Nipponocypris sieboldii Numamutsu x
13 Zacco platypus Oikawa x
14 Opsariichthys uncirostris Hasu x x
15 Hemigrammocypris rasborella Kawabatamoroko x
16 Tribolodon hakonensis Ugui x
17 Rhynchocypris lagowskii Aburahaya
18 Rhynchocypris oxycephalus Takahaya x
19 Ctenopharyngodon idellus Sougyo x
20 Mylopharyngodon piceus Aouo x
21 Ischikauia steenackeri Wataka x x
Origin and Diversification of Freshwater Fishes in Lake Biwa
22 Hypophthalmichthys molitrix Hakuren x

23 Gnathopogon caerulescens Honmoroko x x
1.1
24 Gnathopogon elongatus Tamoroko x x?

25 Pungtungia herzi Mugitsuku x
26 Pseudorasbora parva Motsugo x x
27 Sarcocheilichthys biwaensis Aburahigai x x
28 Sarcocheilichthys variegatus Biwahigai x x
microoculus
29 Pseudogobio esocinus Kamatsuka x
30 Abbottina rivularis Tsuchifuki x? x?
31 Biwia zezera Zezera x
32 Biwia yodoensis Yodozezera x
33 Squalidus chankaensis biwae Sugomoroko x x
34 Squalidus chankaensis tsuchigae Kouraimoroko x
35 Squalidus japonicus japonicus Dememoroko x
36 Squalidus gracilis gracilis Itomoroko x
37 Hemibarbus barbus Nigoi x
Introduction: Lake Biwa and Its Fish Fauna
38 Hemibarbus labeo Korainigoi x

39 Hemibarbus longirostris Zunaganigoi x
40 Cyprinus carpio (native type) Koi (wild type) x
41 Cyprinus carpio (introduced) Koi x
42 Carassius auratus grandoculis Nigorobuna x x
43 Carassius cuvieri Gengorobuna x x
44 Carassius auratus langsdorfii Ginbuna x
45 Tanakia lanceolata Yaritanago x
46 Tanakia limbata Aburabote x
47 Rhodeus ocellatus ocellatus Tairikubaratanago x
48 Rhodeus ocellatus kurumeus Nipponbaratanago x x
49 Acheilognathus rhombeus Kanehira x
50 Acheilognathus longipinnis Itasenpara x x
(continued)
5
6
Table 1.1 (continued)

Endemic/
Scientific name Standard name semi-endemic Extinct Native Domestic alien Foreign alien
51 Acheilognathus cyanostigma Ichimonjitanago x
52 Acheilognathus tabira tabira Shirohiretabira x
Botiidae (1; 0)
53 Parabotia curta Ayumodoki x? x
Cobitidae (5; 2)
54 Misgurnus anguillicaudatus Dojo x
1
55 Paramisgurnus dabryanus Karadojo x

56 Cobitis minamorii oumiensis Biwakogatasujishimadojo x x
57 Cobitis magnostriata Oogatasujishimadojo x x
58 Cobitis biwae Shimadojo x
59 Niwaella delicata Ajimedojo x
Balitoridae (2; 0)
60 Lefua echigonia Hotokedojo x
61 Lefua sp. Nagarehotokedojo x
Bagridae (1; 0)
62 Pseudobagrus nudiceps Gigi x
Amblycipitidae (1; 0)
63 Liobagrus reini Akaza x
Siluridae (3; 2)
64 Silurus lithophilus Iwatokonamazu x x
65 Silurus biwaensis Biwakooonamazu x x
66 Silurus asotus Namazu x
Adrianichthyidae (1; 0)
67 Oryzias latipes Medaka S x
Origin and Diversification of Freshwater Fishes in Lake Biwa
68 Gambusia affinis Kadayashi x

1.1
Gasterosteidae (1; 0)
69 Gasterosteus microcephalus Hariyo x
Channidae (0; 0)
70 Channa argus Kamuruchi x
Sinipercidae (0; 0)
71 Coreoperca kawamebari Oyanirami x
Centrarchidae (0; 0)
72 Micropterus salmoides Largemouth bass x
73 Micropterus dolomieu Smallmouth bass x
74 Lepomis macrochirus Blue gill x
Cichlidae (0; 0)
75 Oreochromis niloticus Nile tilapia x
76 Tilapia zillii Redbelly tilapia x
Introduction: Lake Biwa and Its Fish Fauna
Odontobutiidae (1; 0)
77 Odontobutis obscura Donko x
Gobiidae (5; 2)
78 Rhinogobius kurodai Touyoshinobori x
79 Rhinogobius flumineus Kawayoshinobori x
80 Rhinogobius sp. BW Biwayoshinobori x x
81 Gymnogobius urotaenia Ukigori x
82 Gymnogobius isaza Isaza x x
83 Tridentiger brevispinis Numachichibu x
Cottidae (2; 1)
84 Cottus pollux Kajika (Large-egg form) x
85 Cottus reinii Utsusemikajika (Lake-form) x x
16 2 + 1? 66 + 1? 7 + 2? 15
In parentheses after family names, number of native forms (species/subspecies) and that endemic to Lake Biwa
Updated in September 2013
7
At least for the primary freshwater fishes, all of the species in Lake Biwa are
categorized into the “warm-temperature group,” which is defined physiologically
and biogeographically. Therefore, they are considered to consist of East Asian tem-
perate faunal components. Some landlocked or freshwater forms of diadromous
fishes from the “cool temperature group” also occur in and around Lake Biwa (e.g.,
a lamprey, Lethenteron sp. “Northern forms,” some salmonids from Salvelinus and
Oncorhynchus).
The fishes that occur in Lake Biwa use several types of habitats in and around the
lake (Miura 1966; Tokui and Kawanabe 1984; Yuma et al. 1998; Fujita et al. 2008).
Some use different habitats during different life-history stages and seasons. The
species of Lake Biwa have been categorized into eight life-history types based on
their main habitats and migration patterns (Hosoya 2005). Among the available
habitats, the rocky bottom area and the pelagic zone of Lake Biwa are unique in
Japanese fresh waters. Also, vast areas of sandy bottom provide unique habitats for
some benthic/benthopelagic fishes (e.g., Pseudogobio esocinus and Biwia zezera).
Lagoons, or shallow satellite lakes (called “Naiko”), around Lake Biwa were origi-
nally very important habitats for many species, especially for reproduction and as
nursery areas (Fujita et al. 2008). However, due to recent reclamation, the total area
of these satellite lakes has decreased to about 10 % of the original area (32.4 km2 in
~1925, 4.25 km2 in 1995; Nishino 2005).
The number of endemic species (~60 animals and plants, including a dozen fish
forms) is not very large when compared to levels of endemism in other ancient lakes
throughout the world (e.g., >600 species in Lake Tanganyika; ~1,000 species in
Lake Baikal; Martens 1997). The ratio of endemic forms in Lake Biwa is <10 %
(24 % for fish) (Table 1.1). The taxonomic composition of the freshwater fish
assemblage in Lake Biwa does not differ greatly from that of rivers in western
Japan. There is no prominent taxonomic group in terms of endemism, as found in
the African Great Lakes with cichlids or in Lake Baikal with sculpins. Therefore,
endemism in Lake Biwa cannot be characterized as “species flocks” (e.g.,
Greenwood 1984). Instead, the assemblage of Lake Biwa consists of several sets of
one or a few endemic and non-endemic forms from various taxonomic groups; in a
manner of speaking, it is like a “salad bowl.”
1.2 A Brief Review on the Origins and Evolution

of Freshwater Fishes
Several authors have discussed the origins of the endemic fish fauna of Lake Biwa.
Fossil records are the only direct evidence of past faunal characteristics and their
historical changes. Since Kodera and Nakamura (1976) discovered pharyngeal teeth
of Cyprinus, fragmented fossil remains such as the pharyngeal teeth of cyprinids,
crania and spines of siluriforms, and a jaw of a channid have been reported from
Paleo-Lake Biwa (=the “Kobiwako” Group) (see below). Mollusk and diatom
1.2 A Brief Review on the Origins and Evolution of Freshwater Fishes 9
fossils have also provided important keys for understanding changes (succession/
alternation) in the aquatic biota of Paleo-Lake Biwa (Research Group for Natural
History of Lake Biwa 1994).
Paleogeographical and paleontological data suggest that there was a large fresh-
water system that consisted of a series of rivers and lakes in western Japan in the
Pliocene (called the “second Setouchi river/lake system”). This system would have
harbored a rich basal freshwater fish fauna that was closely related to the continental
fauna. The initial stages of Paleo-Lake Biwa and its eastern neighbor, Paleo-Lake
Tokai, were located at the eastern end of the second Setouchi river/lake system. The
initial stage of Paleo-Lake Biwa (>3.2 Mya; “Lake Ohyamada”) was inferred to be a
subtropical shallow lake, from which cyprinids, including Cyprininae, Xenocyprininae,
Cultrinae, Gobioninae, Leuciscinae, and Acheilognathinae (Nakajima 1987), bagrid
and silurid catfishes (Kobayakawa 1994; Watanabe and Uyeno 1999), and a channid
(Tanimoto and Okuyama 2003), have been discovered. Cyprinins, especially Cyprinus
spp., were the dominant components of this paleofauna (called the “lake of carp”) and
xenocyprinins were also common, although the latter do not occur in present-day
Japan (Nakajima 1994).
According to a quantitative comparison of cyprinid pharyngeal teeth among the for-
mations of Paleo-Lake Biwa (Nakajima 1994), the paleo-ichthyofauna after Lake
Ohyamada became rather simple. Cyprinin genera, Cyprinus and Carassius, were con-
spicuously dominant in “Lake Ayama” (3.0–2.7 Mya), “Lake Koka (or Sayama)” (2.7–
2.5 Mya), and “Lake Gamo” (2.5–1.8 Mya) (called the “lake of crusian carp”).
Stratigraphical studies have suggested that large-scale standing waters disappeared after
Lake Gamo was lost in this region. Then, “Lake Katata” formed around the present
southern basin of Lake Biwa (1.0–0.4 Mya) (Fig. 1.1). It had a rich ichthyofauna includ-
ing cyprinid Cyprininae, Xenocyprininae, Cultrinae, Gobioninae, and Leuciscinae
(Nakajima 1994), and a bagrid catfish (Kobayakawa 1994). These fossil remains could
include those related to current endemic species in Lake Biwa and they are the first
recognized endemics in this paleolake (the cyprinin Carassius cuvieri and the cultrin
Ischikauia steenackeri; Nakajima 1994). Fossil pharyngeal teeth similar to those of the
specialized phytoplankton feeder C. cuvieri, which is endemic to Lake Biwa, exhibit
several levels of specialization (Kodera 1985). Nakajima (1994) suggested that those
ancestral forms would produce endemic species through ecological adaptations to the
environments of the succeeding “present Lake Biwa.”
As above, the fossil record has contributed to our understanding of major fea-
tures and succession in the ichthyofauna of Paleo-Lake Biwa that occurred over a
period of 4 Myr (Tomoda 1991; Nakajima 1994). However, low taxonomic resolu-
tion and possible bias in the sampling of fossils have prevented a detailed recon-
struction of the origins and formation of the endemic fauna of Lake Biwa.
Another approach to understanding the origins of endemism in Lake Biwa
involves comparisons of faunal and species traits (e.g., Ueno 1943; Kawanabe 1978,
1996; Tomoda 1978). Kawanabe (1978) divided the endemic forms into two catego-
ries: species that differentiated in situ and relic species. This division was probably
based on the geographical distributions of putative ancestral forms and their eco-
logical features. The former, “species that evolved in the lake,” were represented by
the gudgeon Gnathopogon caerulescens (from G. elongatus), Carassius cuvieri

(from C. auratus), Gymnogobius isaza (from G. urotaenia), and so on (Kawanabe
1978, 1996; the scientific names have been changed to match the recent literature).
Tomoda (1978) clearly dealt with the “ecological speciation” scenario (see
Rundle and Nosil 2005) for some fish groups such as Carassius carps and Silurus
catfishes in Lake Biwa, mainly by considering modifications in feeding habits/appa-
ratus, habitat types, and migration patterns in endemic species. Takahashi (1989)
focused on the Lake Biwa floating goby Gymnogobius isaza and examined the eco-
logical speciation process that followed the development of the present environment
of Lake Biwa. It would be reasonable to consider that ecological adaptation to the
present environment (large, deep pelagic zone/heterogeneous bottom features)
occurred after the development of these environmental conditions. Therefore, some
authors have concluded that the “species that evolved in Lake Biwa” originated dur-
ing the last 0.3–0.4 Myr (Nakajima 1987; Takahashi 1989). However, the derivation
of endemic lineages from closest extant lineages may or may not occur at the same
time as adaptive evolution (Nakajima 1994). A reliable phylogenetic framework is
required to test ecological speciation scenarios for the origins of endemic species,
as well as to reexamine the categorization of endemic species that was proposed by
Kawanabe (1978).
1.3 Molecular Phylogenetic Approaches
Recent experimental and theoretical developments in molecular genetics can allow

us to discuss historical dynamics in the evolutionary diversification of organisms
within a phylogenetic framework (see, e.g., Avise 2004). The origins of endemic
biodiversity in the world’s ancient lakes have been the focus of research using
molecular phylogenetic/population genetic approaches (e.g., Salzburger and Meyer
2004 for the African Great Lakes; Kontula et al. 2003 for Lake Baikal; also see
Cristescu et al. 2010). These studies have revealed evolutionary patterns and the
tempo of explosive adaptive radiations in ancient lakes. In contrast, until very
recently, only a few molecular studies have examined the biodiversity of Lake Biwa.
Here, I illustrate some examples of previous studies as well as ongoing research into
the origin and establishment of endemic species in Lake Biwa.
1.3.1 Origin of Endemic Lineages
As mentioned above, the traditional view of the origin of endemic “species that
evolved in Lake Biwa” is concerned with ecological adaptation after the develop-
ment of the present Lake Biwa environment, i.e., over the last 0.4 Myr. It is difficult
to determine when adaptive evolution occurred in a genetic sense (Barrett and
Schluter 2008). However, using molecular phylogenetic approaches, we can test the
1.3 Molecular Phylogenetic Approaches 11
hypothesis that endemic species evolved from putative ancestral species (extant sis-
ter lineages) after the development of the present Lake Biwa environment.
The Lake Biwa floating goby Gymnogobius isaza is a typical species that adapted
to the pelagic environment of Lake Biwa (Takahashi 1989). The goby completes its
whole life history within the lake; it lives in the pelagic zone and exhibits diel verti-
cal migrations, except during the reproductive season when it spawns in shallow
areas near the shore. Based on a phylogenetic analysis of Gymnogobius gobies
using mitochondrial DNA sequence data, Harada et al. (2002) rejected two previous
hypotheses, that G. isaza was derived from a presumed ancestor, G. urotaenia, that
lived around Lake Biwa; and that the former lineage originated after the develop-
ment of the present Lake Biwa. Instead, using molecular clocks for fishes, they
found that G. isaza was derived from the common ancestor of G. urotaenia and
G. petschiliensis (referred to as Gymnogobius sp. 1) in the Pliocene (>2 Mya). This
result was supported by subsequent studies (Sota et al. 2005; Tabata and Watanabe
2013) that dated the phylogenetic tree using geological calibration data (i.e., the
formation of the Tsushima Strait, which presumably divided the freshwater species
into continental and Japanese species).
Similarly, our mtDNA analysis, which used a relaxed molecular clock model
with geological constraints, provided evidence that the gudgeon Gnathopogon cae-
rulescens, a representative species that exhibits limnetic adaptation, was derived
from the closest monophyletic group within G. elongatus 1.7 Mya [0.5–3.5 Mya,
95 % highest posterior density region (HPD)] (Kakioka et al. 2013). The old
(>4 Myr) derivation of the Carassius cuvieri lineage from C. auratus was also
inferred based on a molecular clock (1.52 % pairwise distance/Myr) (Takada et al.
2010). Furthermore, according to our ongoing exhaustive phylogenetic analyses of
endemic fishes in Lake Biwa (R. Tabata et al., unpublished data), derivation of most
of the presumed “species that evolved in Lake Biwa” from their closest lineages is
estimated to date back to the early Pleistocene, the Pliocene, or even the Late
Miocene. These patterns do not agree with the hypothesis that the divergence of
endemic species occurred in the present Lake Biwa (<0.4 Mya) unless we firmly
assume that all of the direct ancestral forms of these endemic species have already
gone extinct during the last <0.4 Myr.
A few endemic species, however, are little differentiated from their extant sister
forms. Benthopelagic gudgeons Sarcocheilichthys are good examples of such spe-
cies. The gudgeons show conspicuous trophic polymorphism, especially in the head
part, and two species/subspecies are described from Lake Biwa; S. variegatus
microoculus (endemic subspecies), which has a short to long head, and S. biwaensis
(endemic species), which has a long head and a darker body color. No significant
differentiation is found between the two species in neutral genetic markers, mtDNA,
or microsatellites (Fig. 1.3; Komiya et al. 2011), and the level of differentiation
between Lake Biwa and neighboring populations is not large (Komiya et al. 2013).
Head shape and body color are likely adaptive traits because they obviously corre-
spond to habitat characteristics; S. v. microoculus with a short head and yellowish
body inhabits sandy bottom habitats, whereas S. v. microoculus and S. biwaensis
with longer heads and darker bodies inhabit rocky bottom habitats that are formed
Fig. 1.3 mtDNA haplotype group frequencies (a), statistical parsimony network of mtDNA (b),
and the result of a Bayesian genetic assignment analysis (K = 2) based on 14 microsatellites (c) for
Sarcocheilichthys fishes. Sb, S. biwaensis; others, S. variegatus microoculus. In both (a) and (b),
each clade is shown in the same color. No distinct genetic divergence between the species/local
samples was detected in mtDNA (b) or microsatellites (c). Modified from Komiya et al. (2011)
in restricted areas in the northern basin of Lake Biwa (Komiya et al. 2011). Hence,
their trophic traits and body colors probably evolved rapidly following the develop-
ment of the rocky shore environment in the present Lake Biwa, although it is pos-
sible that variation in those traits can be attributed to phenotypic plasticity. Another
endemic gudgeon subspecies Squalidus chankaensis biwae, which shows adapta-
tions to the pelagic zone, also seems to be a young endemic form (R. Kakioka et al.,
unpublished data). Further, Oohara and Okazaki (1996) suggested that the Biwa
salmon, Oncorhynchus masou rhodurus, originated in the present Lake Biwa
(~0.5 Mya) based on an mtDNA molecular clock of 2 % pairwise distance/Myr. Our
mtDNA analysis results, which were obtained using a relaxed molecular clock
model with geological constraints, roughly agrees with this inference (0.4–0.7 Myr
95 % HPD, R. Tabata et al., unpublished data).
1.3 Molecular Phylogenetic Approaches 13
Fig. 1.4 Bayesian phylogenetic tree of Biwia species based on mtDNA cytochrome b sequences
with the HKY + G model. The tree was dated using the random local clock model with two node
age constraints [C1 a lognormal prior distribution with mean = 1.25 Mya, log (SD) = 0.09, offset = 0
(2.5–97.5 % quantiles: 1.04–1.49); C2 a lognormal prior distribution with mean = 0.45 Mya, log
(SD) = 0.4, offset = 0 (2.5–97.5 % quantiles: 0.19–0.91)]. Numbers at nodes indicate Bayesian pos-
terior probabilities. Horizontal bars at nodes show credible intervals as 95 % HPD. Data from
Watanabe et al. (2010)
Although not treated as distinct taxonomic units, populations of some species in

Lake Biwa exhibit unique phenotypes. The benthic gobionins Biwia zezera and
Pseudogobio esocinus show similar trends in body shape modification (e.g., elon-
gated bodies) in Lake Biwa (Nakamura 1969; Kawanabe et al. 2001). The function
of this unique morphology is not obvious, but it may represent an adaptation to life
in standing water. According to the mtDNA phylogeny of B. zezera (Fig. 1.4; calcu-
lated from the data of Watanabe et al. (2010)), the Lake Biwa population includes
two clades, one of which forms a clade with haplotypes from the western neighbor-
ing “Sanyo” population. At a minimum, these two lineages advanced into Lake
Biwa. If it can be assumed that the Kyushu population was separated from the
Honshu populations by the formation of mountains in northern Kyushu (>0.4 Mya;
see Nakajima et al. 2006), invasions by B. zezera into Lake Biwa should have
occurred more recently (Fig. 1.4). The estimated times of the most recent common
ancestors of each Lake Biwa clade are 0.41 and 0.40 Myr. This suggests that the
time scale for adaptation to Lake Biwa was less than ~0.4 Myr, i.e., adaptation
occurred after the development of the present Lake Biwa. Pseudogobio esocinus
presents similar results (K. Tominaga et al., unpublished data). A unique landlocked
form of Ayu, Plecoglossus altivelis, in Lake Biwa is also estimated to have differen-
tiated after formation of the present Lake Biwa (0.1 Mya from Nei’s genetic dis-
tance for allozyme data; Nishida 1985).
In summary, molecular phylogenetic analyses are revealing that most of the
endemic lineages in Lake Biwa differentiated from extant related lineages long
before the development of the present Lake Biwa (<0.4 Mya). However, irrespective
of taxonomical treatment, adaptive phenotypes that are endemic to Lake Biwa can
be inferred to have evolved in the present Lake Biwa environment. Exhaustive phy-
logenetic analyses of Lake Biwa endemics will further alter our view of the pattern
and time scale of the origin of endemic lineages in the lake.
1.3.2 Population Establishment by Endemic

and Non-endemic Species
The divergence time for endemic lineages in Lake Biwa varies greatly among spe-
cies, as shown above. However, our ongoing comparative demographic analysis of
Lake Biwa populations has shown similar patterns among many species. A Bayesian
skyline plot analysis (Drummond et al. 2005), as well as traditional mismatch dis-
tribution analysis, has provided information regarding historical demographic
changes using molecular genetic data (Ho and Shapiro 2011). Many populations,
including both old and young endemic lineages of “species that evolved in Lake
Biwa” as well as “relict species,” show a pattern of recent population expansion that
occurred several tens of thousands of years ago (Fig. 1.5). This pattern has also been
observed for many non-endemic species (R. Tabata et al., unpublished data). This
means that the present populations in Lake Biwa colonized the lake in the late
Pleistocene, after the present lake environment developed, or they experienced
severe bottlenecks and subsequently became reestablished during that period.
Drastic climate changes in the Pleistocene are believed to have had large impacts
on freshwater fish populations. Rising sea levels in the interglacial period would
have reduced the habitats available to freshwater fishes, especially considering
island topography, and the cool and dry climate in the glacial period would also
have had negative impacts on populations that were adapted to a temperate monsoon
climate. Even in Lake Biwa, reductions in population size in the late Pleistocene
have been inferred for many species. However, the lake would have also functioned
as a “reservoir” for many species, which are represented by the “relict endemic
species” as well as other general species.
1.4 Conclusions and Perspectives 15
Fig. 1.5 Bayesian skyline

plots for three endemic
species in Lake Biwa. The
central bold line represents
the median value for the
relative effective population
size and the solid area
denotes the 95 % upper and
lower credible limits. Drawn
based on unpublished data
from R. Tabata et al.
1.4 Conclusions and Perspectives
Recent molecular phylogenetic and phylogeographic studies have questioned the tra-
ditional simple dichotomy of Lake Biwa endemics into old “relict species” that are no
longer found outside the lake and new “species that evolved in the lake” that exhibit
ecological adaptations to the present unique lake environments. For many species that
were thought to belong to the latter group, evidence now shows that they were derived
prior to ecological adaptations to the new lake environment. However, most of the
results of recent studies were based only on mtDNA sequence data, which might
result in biased estimations of phylogeny and divergence times. Further studies should
be conducted using plenty of information from the nuclear DNA genome.
During drastic climate changes in the late Pleistocene, the large water body of
Lake Biwa would have functioned as a reservoir for endemic and non-endemic spe-
cies. Under such conditions, both old and new lineages from various taxonomic
groups would have been facilitated to adapt ecologically to the unique lake environ-
ments, such as the pelagic zone and rocky bottom. They evolved similar sets of
phenotypic traits in parallel, which can be treated as “lacustrine syndromes” (e.g.,
pelagic plankton feeders, sustained swimmers, rocky bottom specialists). Such par-
allel adaptive evolution at the community level might have occurred repeatedly in
western Japan at several time points since the Pliocene. Unlike other typical cases
in the world’s ancient lakes, no remarkable species flocks are found in the present
Lake Biwa. However, the multiple colonizations and independent radiations inferred
in East African cichlids (e.g., Salzburger and Meyer 2004) are likely shared with the
situation in Lake Biwa. The geographical location and history may be attributable
to the less developed species flocks in Lake Biwa, which has never been glaciated
and has maintained some connections with river systems adjacent to the lake.
Considering possible unique aspects of the endemic community in Lake Biwa, par-
allel adaptive evolution should be examined throughout the fish assemblage based
on phylogeny, population genetics, ecology, and traditional morphological/physio-
logical comparisons.
Currently, several “omics” studies have also been initiated to examine lacustrine
adaptations in Lake Biwa (e.g., proteomics, QTL association mapping with RAD-
seq; Kakioka et al. 2013). These studies will contribute to identifying the genetic
basis of some aspects of adaptation. Furthermore, genome-level studies may pro-
vide a clue to answering “when” such adaptive evolution occurred (Barrett and
Schluter 2008). Were the previous inhabitants of Paleo-Lake Biwa able to adapt to
the present Lake Biwa more easily than newcomers due to their standing variation?
Interactions between adaptations and community structuring over multiple time
scales remain an open question. Such evolutionary interactions would have caused
feedback into ecosystem processes, which might have prompted further adaptation
and speciation in the lake. To learn more from Lake Biwa, we should concentrate on
reducing human impacts on the lake ecosystem, which currently suffers from eutro-
phication, destruction of the ecotone area, and destruction of endemic communities
through introductions of invasive alien species, such as sunfishes.
Acknowledgments I express my sincere thanks to Noboru Okuda for providing me the opportunity
to write this review. I also thank Takefumi Komiya, Ryoichi Tabata, Ryo Kakioka, Koji Tominaga,
and Shigefumi Kanao for providing information on the results of their studies, which will be pub-
lished in the near future and will enhance this incomplete review on the origin of Lake Biwa
endemics. Kohji Mabuchi provided constructive suggestions for improving the manuscript. This
study was supported in part by the Grants-in-Aid from the Ministry of Education, Culture, Sports,
Science and Technology, Japan (nos. 18570086, 21370035, and “Formation of a Strategic Base for
Biodiversity and Evolutionary Research: from Genome to Ecosystem” of the GCOE) and the WEC
Research Fund for Ecology and Civil Engineering (2009-6).
References 17
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Chapter 2
Predator Diversity Changes the World:
From Gene to Ecosystem
Abstract Trophic polymorphism, defined as the state in which two or more clearly
different feeding functional traits exist within the same population of a species, is
general in fishes. In aquatic ecosystems, the fishes often have strong impacts on prey
communities as keystone predators, so that phenotypic divergence of their feeding
traits can alter biotic and abiotic attributes of environments through changes in the
form of trophic interactions. The predator-induced environmental alterations may,
in turn, drive evolutionary changes in adaptive traits of themselves as well as of
other members in the communities. This process, in which ecology and evolution
reciprocally interplay over contemporary time-scales, is termed “eco-evolutionary
feedback.” In this chapter, we review how and when trophic polymorphism has been
generated in fish populations and then discuss what consequences it has in ecologi-
cal and evolutionary aspect. Special references are made to the case in the ancient
Lake Biwa, which has a geological history long enough for divergent fish popula-
tions to come to ecological speciation and thus provides a good opportunity to
understand how such an evolutionary process diversifies biological communities
and consequently ecosystem properties in lakes.
Keywords Biodiversity • Eco-evolutionary feedback • Ecological speciation •

Ecosystem functioning • Keystone predator • Mesocosm • Species pair • Trophic
polymorphism
2.1 Why is Biodiversity Important?
What is the ecological significance of conserving biological diversity within a spe-

cies? In the context of conservation biology, it could be argued that maintenance of
intraspecific phenotypic variation has the advantage of increasing population viabil-
ity because it provides the population with the adaptability to respond to changing
environments. However, such a traditional view has been replaced by recent

22 2 Predator Diversity Changes the World: From Gene to Ecosystem
ecological findings that the intraspecific diversity of a keystone species impacts

substantially on biological communities and their ecosystem functioning. In this
chapter, we first focus on phenotypic polymorphism in fishes as keystone predators
of aquatic ecosystems, referring to genetic mechanisms underlying their polymor-
phism. We also introduce some of the latest studies, which demonstrate that intra-
specific functional diversity of fish predators alters aquatic community structure and
ecosystem processes. Finally, we show that environments modified by a predator’s
functional diversity can serve as a driver for the evolutionary diversification of
aquatic biota through eco-evolutionary feedbacks.
2.2 Biodiversity at Three Levels
According to the Convention on Biological Diversity (CBD), biological diversity

includes diversity within species, between species and of ecosystems, being
viewed at different levels of biological organization from genes to ecosystems. In
terms of conservation biology, the maintenance of intraspecific diversity is of
ecological importance because a population with a variety of phenotypes, which
have the potential for adaptation against unpredictable environmental changes in
the future, such as global warming, habitat alteration and prevalence of emerging
pathogens, may be able to prevent extinction. Furthermore, recent developments
in community genetics have provided a new insight into the ecological and evo-
lutionary consequences of intraspecific diversity. In a population of terrestrial
plant, for example, cottonwood Populus, individual phenotypes can harbor dif-
ferent arthropod communities according to their anti-herbivore defense capacity,
which is based on genotypes (Whitham et al. 2006). The genotypic difference
among individuals further causes intraspecific variation in condensed tannin pro-
duction in leaves, which in turn affects litter decomposition processes attribut-
able to forest floor microbes. Since this finding, an increasing number of studies
have looked at the cascading effects of intraspecific biodiversity on community
structure and ecosystem processes, attracting much attention from both commu-
nity and evolutionary ecologists.
2.3 What is Phenotypic Polymorphism?
Phenotypic polymorphism, defined as the state in which two or more clearly differ-
ent phenotypic traits exist within the same population of a species, is a common
phenomenon found in a variety of taxonomic groups from prokaryotes to higher
vertebrates. The polymorphic phenotypes include behavioral, morphological, phys-
iological and life history traits (Gross 1996). In a narrower sense, phenotypic poly-
morphism is confined to discontinuous phenotypic variation within a Mendelian
population in which interbreeding individuals share a common gene pool. In a broad
2.4 Phenotypic Polymorphism in Aquatic Ecosystems 23
sense, however, it is applicable to the case in which intraspecific phenotypic varia-

tion results from secondary contact between multiple populations under different
selection regimes and/or undergoing different genetic drifts in different locations. In
addition, some studies have recently reported that the polymorphic state is attained
by phenotypic plasticity within a genetically monomorphic population (Agrawal
2001; Miner et al. 2005). To understand the evolution of phenotypic polymorphism,
it is essential to elucidate the origins of polymorphic phenotypes and the underlying
mechanisms for polymorphic expression. But yet, such a subject is at the state of the
art. In this chapter, when treating with cases in which there exists discontinuous
phenotypic variation within a given population at a given time, we regard all of them
as phenotypic polymorphism without referring to the processes and mechanisms for
generating it.
2.4 Phenotypic Polymorphism in Aquatic Ecosystems
In aquatic organisms, phenotypic polymorphism is often observed in traits related

to predator–prey interactions. Prey organisms often show a polymorphic pattern of
traits in relation to inedibility, termed anti-predator defensive traits. For example,
phytoplankton can avoid zooplankton predation by means of colony formation,
while zooplankton under high predation pressure express their sharp helmet and
extended tail spine, which functions to deter fish and invertebrate predation (Lass
and Spaak 2003). In contrast, fish predators show polymorphism in behavioral and
morphological traits associated with feeding habits, which is referred to as trophic
polymorphism (Smith and Skulason 1996). Intraspecific variation in feeding traits
leads to discrete variation in species trophic niche through functional differences in
prey size selectivity or prey species-specific foraging efficiency (Robinson 2000).
2.4.1 Trophic Polymorphism and Adaptive Divergence
In the East African Great Lakes, which have a long geological history spanning
hundreds of thousands to tens of millions of years, cichlid fishes are well known to
be a group showing adaptive radiation. In this group, it has been believed that a
small number of ancestral species evolved to the diversity of existing species
through specialization of their habitat and food resource utilization (Seehausen
2006). The ancestral species, which was the first to colonize these lakes, would have
intensified intraspecific competition for food resources and habitats in the process
of its population expansion under environments in which there existed few or no
predators and competitors. As an efficient way to reduce intraspecific competition,
the fish might have partitioned their resources to occupy alternative empty niches as
the population became saturated. Individual variation in plastic foraging behavior
may have been the first step of niche specialization (Bolnick et al. 2003). When the
foraging behavior is partly inherited in the progeny, behavioral specialization can

facilitate the subsequent physiological and morphological adaptations to specific
resource utilization (Sacotte and Magnan 2006). Such a phenotypic adaptation,
which enables each individual to utilize different resources more efficiently, will
favor disruptive selection within the population (Knudsen et al. 2010). If it is accom-
panied by reproductive isolation due to sexual selection, then the adaptive diver-
gence can lead to ecological speciation (Seehausen et al. 2008). Marked interspecific
diversity of trophic niches and morphology found in African cichlids may be an
evolutionary consequence of resource partitioning among individuals derived from
a colonized population (Bootsma et al. 1996; Genner et al. 1999).
There is excellent evidence supporting the evolutionary scenario of adaptive
radiation in cichlids, in which colonized populations of ancestral species partitioned
resources among individuals and subsequently diversified their morphology, lead-
ing to ecological speciation. In a Nicaraguan crater lake, which was formed by
volcanic activity less than 23,000 years ago, two cichlid species coexist and form a
monophyletic assemblage (Barluenga et al. 2006). One species, which is wide-
spread among adjacent lakes, lives in the littoral habitat and another endemic spe-
cies lives in the limnetic habitat of the deep crater lake. The two species also differ
greatly in their feeding habits and morphology, with the limnetic species possessing
a more slender body. Molecular data revealed that these two species were reproduc-
tively isolated less than 10,000 years ago, suggesting that morphological divergence
through habitat/food preference and subsequent reproductive isolation through
assortative mating led to sympatric speciation. This finding seems to reconfirm
assumptions of adaptive radiation of cichlids in African Great Lakes in which mor-
phologically diverse species have derived from a few ancestors. In the case of
Nicaraguan cichlids, colonization to newly created environments, where competi-
tors are originally absent, would have facilitated phenotypic divergence of trophic
morphology and the subsequent ecological speciation, which provides unique
opportunities to understand the evolutionary process of adaptive diversification
within a lake environment.
Although trophic polymorphism has been found in phylogenetically different
groups of fishes, some of its features are shared among them. One of the most
remarkable, in this respect, is that the evolutionary pattern of morphological diver-
gence associated with feeding specialization is similar across species. For example,
individuals with a deeper body, a shorter snout and a wider mouth feed on benthic
prey preferentially, while those with a slenderer body and an elongated snout fre-
quently feed on plankton in pelagic waters. In the former case, the wider mouth has
the advantage of readily consuming benthic prey on the lake bottom (Robinson
2000) and the deeper body allows the development of larger pharyngeal muscles,
which are advantageous in the crushing of the hard shells of benthic invertebrates,
such as gastropods and decapods (Wainwright et al. 1991; Osenberg et al. 2004). By
contrast, in the latter case, the slender body is suited to optimize swimming perfor-
mance, which would be required to extensively search for planktonic prey (Hendry
et al. 2011). In addition, these individuals have a greater gill raker number and nar-
rower gill raker spacing, which are both effective in the filtration of small particles
such as plankton (Robinson 2000). Such a morphological divergence is closely

associated with habitat-specific food resource distribution, characterized by typical
lake food webs, i.e., plankton prey derived from a pelagic food chain in the limnetic
habitat and benthos prey from a benthic food chain in the littoral habitat. For many
fish species with phenotypic polymorphism, even if there are interspecific varia-
tions, their morphological divergence is usually associated with two different tro-
phic niches, planktivory and benthivory.
2.4.2 Ecological Speciation and Species Pair
Trophic polymorphism has also been frequently observed in freshwater fish species
inhabiting postglacial lakes in northern temperate environments: e.g., salmonids,
sticklebacks and osmerids (Taylor 1999). The reason for this is associated with the
geological history of these lakes. In high latitudes of the Northern Hemisphere, the
land surface was extensively covered by ice during the last glaciation, which
extended from approximately 110,000 to 10,000 years ago. According to the most
predominant hypothesis, fish species that were the first to colonize in postglacial
lakes would have undergone morphological divergence in order to utilize unused
food resources in the absence of competitors. If that is true, the evolution of trophic
polymorphism in high latitudes must have occurred during the last 10,000 years.
This time scale is too short for the fish population to diverge into different biological
species with complete reproductive isolation (i.e., speciation) but it may be long
enough for the population to undergo adaptive divergence (Hendry et al. 2009).
The above situation reported for freshwater fishes in high latitudes is often
regarded as a species pair. A species pair is defined as a pair of populations that are
typically distinguished from each other by differences in ecology, behavior and/or
morphology, but are taxonomically classified as the same species because of their
incomplete reproductive isolation (Taylor 1999). However, sexual selection follow-
ing divergent natural selection will lead to the evolution of reproductive isolation
through assortative mating based on ecologically selected traits, which can be the
principal mechanism of ecological speciation (McKinnon and Rundle 2002). Recent
molecular studies also provide strong support for the hypothesis that adaptive diver-
gence contributing to reduction of gene flows will cause genetic incompatibility
responsible for reproductive isolation and promote ecological speciation between
members of a sympatric species pair (Rogers and Bernatchez 2007).
In traditional systematics based on morphological taxonomy, it does not matter
if the species pair accords with the entity of biological species. For freshwater fishes
whose local populations have experienced isolation and reorganization repeatedly
through geological events such as river and lake capture, it is not easy to define a
boundary for a biological species. Whether discrete variation in feeding traits found
in a focal taxa is regarded as intraspecific or interspecific variation relies on how a
researcher classifies a biological entity into “single species” or “different species”.
However, “species” is just an operational taxonomic unit and its definition is not an
important issue for understanding how a diversity of feeding functions has evolved
from an ancestral lineage. It is more important to recognize that polymorphic popu-
lations observed in nature can be arrayed somewhere along a continuum from pan-
mixia to complete reproductive isolation (Hendry 2009).
2.4.3 The Ancient Lake Biwa as an Evolutionary Hot Spot
The ancient Lake Biwa, which has a geological history longer than postglacial lakes
(tens of thousands years) and shorter than the oldest African Great Lakes (tens of
millions years), provides a good opportunity to observe how the process of ecologi-
cal speciation leads to species diversification. This lake was formed south far from
its current location ca. four million years ago (see Chap. 1). It is a tectonic lake, i.e.,
the lake formed as a result of tectonic movement, having gradually moved north-
wards. The lake deepened through faulting at the current location ca. 400 thousand
years ago and then has stood still there. At present, it shows a high biodiversity with
1,769 aquatic species recorded, including 61 endemics (Timoshkin et al. 2011).
Similar to other ancient lakes created by tectonic movements, Lake Biwa is charac-
terized by the development of deep pelagic habitats, which support many pelagic
fishes (Okuda et al. 2012). Recent molecular techniques have revealed that some
endemic fishes, which have adapted to pelagic environments, are derived from lit-
toral or fluvial ancestral species (see Chap. 1). Many of these pelagic species share
adaptive traits, such as a slender body and narrow gill raker spacing, which are
advantageous to inhabiting pelagic waters. Because such an evolutionary diver-
gence is found among phylogenetically distant groups, it is suggested that conver-
gent evolution of phenotypes adaptive to the pelagic habitats has occurred following
the appearance of newly created deep water environments in Lake Biwa.
Even if divergent evolution progressed over geological time scales in this lake,
reproductive isolation may remain incomplete. This is the case in sister species of a
minnow, Gnathopogon, living in Lake Biwa (Fig. 2.1). Gnathopogon elongatus elon-
gatus is a common freshwater fish inhabiting rivers and ponds in western Japan, while
G. caerulescens is endemic to Lake Biwa. In Lake Biwa, these two species coexist but
segregate their habitats: i.e., G. elongatus elongatus lives in littoral and fluvial habi-
tats, whereas G. caerulescens lives in limnetic habitats. The former is typical of ben-
thivores and the latter of planktivores. The planktivorous G. caerulescens has a slender
body and narrower gill raker spacing, which is advantageous to feeding on plankton
in pelagic waters. An advanced molecular technique, with a next generation sequencer,
elucidated the genetic basis of such a morphological adaptation (Kakioka 2013; also
see Sect. 2.4.6). Although there are remarkable morphological differences between
these coexisting fishes, their phylogenetic relationship is closer than that of allopatric
populations within the species G. elongatus elongates (Kakioka et al. 2013a; Fig. 2.1).
More interestingly, they are reproductively compatible to each other in captive condi-
tions and their hybrids sometimes occur in nature (Nakamura 1969; T. Kokita, unpub-
lished data), suggesting that discrete variation in their feeding morphology stands for
Feeding habits and morphology Molecular phylogeny

Planktivorous
Sympatric lacustine population G. Caerulescens
Sympatric lacustine population
(G. Caerulescens)
Allopatric lacustrine population G. elongatus elongatus Allopatric lacustrine population

(G. elongatus elongatus)
Sympatric lacustrine population
Allopatric fluvial population
Sympatric lacustrine population
Allopatric fluvial population

Benthivorous
Fig. 2.1 Feeding habits, morphology and molecular phylogeny of a genus Gnathopogon in Japan.
The phylogenetic tree was modified after Kakioka et al. (2013a)
trophic polymorphism within a species pair rather than interspecific variation between
sister species. This phenomena may also be true for sister species of some other fish
groups in Lake Biwa.
2.4.4 Life History Polymorphism
In freshwater fishes, another example of phenotypic polymorphism is often found in

life history traits. In many species of salmon and sticklebacks in which trophic poly-
morphism is well known, two different life history forms coexist within a popula-
tion, i.e., a diadromous form, which migrates between freshwater and marine
habitats, and a non-diadromous (or landlocked) form, which occurs in freshwater
environments throughout its entire life (Taylor 1999). In these polymorphic popula-
tions the non-diadromous form generally has a smaller body size at maturity and
more gill rakers or narrower gill raker spacing than those in the anadromous form
(Foote et al. 1999; McKinnon and Rundle 2002). For migratory threespine stickle-
backs with a marine origin, molecular phylogenetic evidence suggests that the
migration-related morphological traits (e.g., the pattern, number, and size of the
bony lateral plates) have evolved repeatedly in populations from different locations
(Colosimo et al. 2004).
An alewife Alosa pseudoharengus (Clupeidae) is one example where relationships

between life history, trophic morphology and feeding habits have been intensively
investigated (Palkovacs and Post 2008). In this species, anadromous fish migrate from
the ocean to freshwater lakes for breeding in spring. Their young-of-the-year (YOY)
fish spend several months in nursery lakes to preferentially prey upon large bodied
zooplankton before migrating to the ocean in autumn. However, if there are any physi-
cal barriers to their migration route, the migratory populations become landlocked,
completing their entire life in the nursery lakes. While migratory populations are
sometimes landlocked by natural barriers such as beaver dams and wind throws for
years to decades, some of them have been completely isolated by artificial barriers
such as man-made dams, resulting in the prevention of gene flows.
In alewives, non-migratory landlocked populations have smaller gape width
and narrower gill raker spacing than anadromous populations. In lakes with land-
locked alewives, zooplankton size is small all year round, as compared to lakes
with anadromous alewives, because of constant fish predation of large bodied
zooplankton. In a situation where intra- and/or inter-specific food competition is
intense and constant among planktivores coexisting in lakes, evolution might
favor the landlocked morph with the smaller gape width and narrower gill raker
spacing, which are more adept at foraging on small-bodied prey items. Estimations
based on molecular data suggest that such a divergent evolution occurred between
5000 and 270 years ago, during which time dams were built in this region
(Palkovacs et al. 2008).
For migratory fishes, geographic barriers temporarily isolate local populations
in terms of geological time scales, while their high mobility promotes the reorga-
nization of different populations under different selection regimes, creating
spatio-temporal heterogeneity in trait distribution within and/or among popula-
tions. As a consequence, a multimodal distribution of phenotypes may be observed
at a given time and space in relation to trophic morphology as well as life history
traits. This may explain why polymorphic phenomena, such as trophic polymor-
phism or a species pair, have often been reported for freshwater fishes with a
diadromous origin.
2.4.5 Rapid Evolution of Trophic Polymorphism
How rapidly can trophic polymorphism emerge within a population after coloni-
zation of a new environment? Human introductions of non-native species, which
have been considered a serious conservation issue worldwide, can provide unex-
pected opportunities to study the evolutionary process of trophic polymorphism.
The bluegill sunfish Lepomis macrochirus was introduced into Japan from the
United States in 1960 and, thereafter, rapidly spread throughout the country.
Surprisingly, all of the introduced fish are derived from only 18 individuals col-
lected from the Mississippi River at Guttenberg, Iowa, and genetic diversity is
very low in the respective introduced populations, probably due to a founder
effect arising from introduction of a small number of individuals with subsequent

genetic drift (Kawamura et al. 2006). In the original population there are two
feeding morphs. The littoral or benthic morph has an enlarged body depth and
long pectoral fins, indicating a feeding specialization towards benthic prey, while
the limnetic or pelagic morph has a slender body and short pectoral fins, which
give an advantage in searching for zooplankton in pelagic waters (Ehlinger 1990,
1991; Wilson 1998).
In Lake Biwa, there are records indicating that introduced bluegills mainly fed
on shrimp in the early phase of their colonization during the 1970s (Terashima
1980), suggesting that their founders were originally the littoral morph. More than
half a century after the colonization, however, Yonekura et al. (2002) found that the
introduced population showed specialization of feeding habits, i.e., individual food
preferences for zooplankton, zoobenthos or submerged plants, and that they indi-
vidually differed in morphology corresponding to their feeding specialization.
Their trophic morph-specific feeding habits were also consistent through the time,
as suggested by their stable isotopic signatures, which revealed that each of the
morphs occupied a different trophic niche (Uchii et al. 2007). Such a feeding spe-
cialization might have been promoted by food resource partitioning among intro-
duced bluegills because their habitats are confined to a narrow zone of shallow
waters in this deep lake. Yonekura et al. (2007b) demonstrated that the smaller gill
raker spacing characteristic of the pelagic morph increases foraging efficiency for
zooplankton prey, whereas the wider mouth characteristic of the benthic morph
increases foraging efficiency for zoobenthos prey. More interestingly, submerged
plant feeders have developed an intermediate morph between benthic and limnetic
morphs. Uchii (2007) revealed that bluegills in captive conditions could not com-
pensate for their growth by feeding on submerged plants exclusively, suggesting
that the submerged plant feeders found naturally adopt “the best of a bad situation”
strategy, because their intermediate morph is not specialized for either benthos or
plankton feeding.
The example of introduced bluegills implies that newly colonized populations
can achieve phenotypic divergence much faster than expected from the evolutionary
time required for a species pair, which is estimated as ten thousand years.
Unfortunately, it remains untested whether trophic polymorphism of introduced
bluegills is attributed to genetic divergence during their colonization, which gives
direct evidence for the rapid evolution. However, recent molecular data suggests the
possibility that polymorphic variation in feeding traits is under the control of phe-
notypic plasticity (see Sect. 2.4.6). Another excellent example of the rapid evolu-
tion, if not of trophic polymorphism, in fishes is the case of sockeye salmon, in
which introduced populations derived from a common ancestry colonized adjacent
river and lake habitats separately, resulting in phenotypic divergence. In these intro-
duced populations, Hendry et al. (2000) demonstrated that reproductive isolation
rapidly evolved between two divergent populations within fewer than 13 genera-
tions of their colonization. Therefore, it is possible for newly colonized populations
to evolve trophic polymorphism followed by assortative mating between the same
morphs on an ecological time-scale, sometimes even within decades.
2.4.6 Genetic Mechanisms of Trophic Polymorphism
Although it remains unknown how phenotypic polymorphism is maintained within

a population, there are two mechanisms for generating it. One is genetic variation,
with the other being phenotypic plasticity, defined as ontogenetic phenotypic
changes in response to changes in the environment. Some studies have reported that
trophic polymorphism in fishes has at least partly a genetic basis. For example,
Proulx and Magnan (2004) conducted common garden experiments with a lacus-
trine brook charr, in which both pelagic and littoral morphs coexisted. Young-of-
the-year (YOY) fish of each morph were transplanted to a tank, either simulating a
pelagic or a littoral habitat, and fed pelagic or benthic food respectively. Some vari-
ation in feeding morphology was accounted for by genetic effects, whereas some
was environmental. More interestingly, additional experiments, under which fish
habitats were alternated between each other during their growth, indicated that
some of the morphological traits were plastically changed to adjust to a new habitat,
suggesting the ecological significance of phenotypic plasticity during ontogenetic
habitat shifts. For many species showing trophic polymorphism, phenotypic plastic-
ity plays an important role in intraspecific phenotypic variation, as discussed later.
Recent advances in molecular techniques have stimulated studies to elucidate the
genetic mechanisms of phenotypic polymorphism in fishes: the techniques include
comparative genomics, genetic mapping, candidate gene approaches, transcrip-
tomics and so on (Ellegren and Sheldon 2008). Quantitative trait loci (QTL) analy-
sis, one of the linkage mapping, is a powerful approach for identifying genome
regions that contain genes responsible for variation in quantitative traits. Since the
QTL analysis requires intercross and backcross between different populations,
which have divergent phenotypic traits but are reproductively compatible to each
other, species pairs are considered a promising subject for this analysis. Threespine
sticklebacks are among the best understood species in fishes in relation to the
genetic basis on life history and trophic polymorphisms with the application of the
QTL (Peichel et al. 2001; Colosimo et al. 2004; Cresko et al. 2004; Shapiro et al.
2004; Kimmel et al. 2005). Although we have difficulty in applying this technique
to wild populations of non-model organisms because of the labor intensive and time
consuming work required to get their genomic resources, the development of high
throughput next generation sequencers will enable us to efficiently perform it with
wild fish populations (Baird et al. 2008; Kakioka et al. 2013b).
Because the QTL can only detect genome regions containing or linked to target
genes, positional cloning and nomination of candidate genes are required to find
causative genetic variants. Colosimo et al. (2005) is the first to identify a particular
gene involved in the expression of divergent phenotypes in wild fish populations. In
threespine sticklebacks, landlocked populations evolved from fully armored anad-
romous ancestors and experienced armor reduction repeatedly in different locations
(Barrett 2010). Colosimo et al. (2005) demonstrated that the ectodysplasin gene,
which is involved in proper development of a number of ectodermal derivatives and
dermal bones in mammals, was responsible for the armor reduction in landlocked
threespine sticklebacks by means of genetic mapping, sequencing and transgenic
2.5 Niche Construction 31
techniques. Surprisingly, the causative alleles were shared among widely separated
populations, suggesting a molecular genetic basis of the rapid parallel evolution of
phenotypes adaptive to freshwater habitats.
Transcriptome profiling is also a promising tool for unraveling complex molecular
genetic basis of phenotypic divergence between closely relatives by examining their
differential gene expression on the microarray. Using this technique, for example,
Derome and others demonstrated in polymorphic populations of lake whitefish
Coregonus clupeaformis that two sympatric morphs, a dwarf morph adaptive to lim-
netic habitats and a normal morph to benthic habitats, showed differential expression
of genes involved in energetic metabolism and regulation of muscle contraction, both
of which are associated with swimming activity, and that their differential gene expres-
sion was parallel among different lakes (Derome and Bernatchez 2006; Derome et al.
2006). This is reasonable when considering that the dwarf morphs are selected for
high swimming performance in the limnetic habitats. More interestingly, the expres-
sion of the same genes involved in modulating swimming activity were upregulated
for a sympatric congener Coregonus artedi, a specialist competitor for the limnetic
trophic niche, providing the molecular evidence of parallel phenotypic evolution.
While an increasing number of studies have reported evidence for the molecular
genetic basis of phenotypic polymorphism in fishes, they do not usually reject the pos-
sibility of its environmental determination, i.e., phenotypic plasticity. Many research-
ers have used common garden experiments to demonstrate that phenotypic plasticity
of feeding morphology is induced by diet and/or habitat manipulation in fish popula-
tions with polymorphic phenotypes (Hegrenes 2001; Andersson 2003; Andersson
et al. 2005; Olsson and Eklöv 2005). In introduced populations, which have been
recently colonized by a small number of individuals and, therefore, possess low
genetic variation, trophic polymorphism may be substantially controlled by pheno-
typic plasticity, as in the case of bluegills introduced into Japan (Yonekura et al.
2007a; also see Sect. 2.4.5). Although it is hypothesized that the phenotypic plasticity
can be controlled by epigenetics (i.e., heritable changes in gene expression or cellular
phenotype caused by mechanisms other than changes in the underlying DNA
sequence), its molecular mechanisms are poorly understood. In particular there is lit-
tle published information regarding which key genes are involved in phenotypic plas-
ticity of polymorphic traits and how they control developmental plasticity through a
gene regulatory network (Sibthorpe et al. 2006). Without understanding the molecular
mechanisms for phenotypic plasticity, difficulties remain in discriminating between
genetic and environmental effects on trophic polymorphism. Further advances in
molecular techniques and their application to wild fish populations are needed to elu-
cidate the genetic mechanisms underlying life history and trophic polymorphisms.
2.5 Niche Construction
A member of a biological community embedded within an ecosystem has a number

of effects on other individuals simply by utilizing the space and energy provided by
the ecosystem. These effects can sometimes alter ecosystem structure and
functioning through ecological interactions between individuals or between biotic

and abiotic components. In such an interaction network, species that have strong
impacts on community and ecosystem processes are termed “keystone species” or
“ecosystem engineers.” When “environment” is defined as “physical, chemical and
biological properties outside the organism under consideration,” phenotypes of the
keystone species can shape their environments. The environments altered by the
keystone species may, in turn, act as a driver for the evolution of both itself and
other members of the community. The process by which phenotypes expressed by a
given species shapes the adaptive landscape of phenotypic evolution for itself or
other species through alteration of biotic and abiotic attributes of their environments
is termed “niche construction” (Odling-Smee et al. 2003).1
In aquatic ecosystems, although there are a large number of examples of niche
construction by fish acting as keystone predators, two key mechanisms of trophic
cascade and nutrient transportation can be recognized (Fig. 2.2). Trophic cascade is
defined as a food web consequence in which predators have indirect effects on non-
prey organisms at trophic levels lower than those of their prey, through trophic inter-
actions within a food web (Carpenter et al. 1985). For example, in the presence of
planktivorous fish, large-bodied zooplankton are preferentially eliminated from the
plankton community through fish predation (Brooks and Dodson 1965). This preda-
tion effect can alter microbial communities including microalgae, bacteria and pro-
tozoa. Since large-bodied zooplankton such as Daphnia have higher grazing rates,
they depress growth of their microbial prey to a greater extent. Despite their micro-
scopic size, microalgae and bacteria have large impacts on ecosystem processes,
including production and decomposition rates, because of their large biomass and
high metabolic turnover. When the abundance of planktivorous fish increases,
microbial communities enhance their production and decomposition through alle-
viation of predation by large-bodied zooplankton, resulting in an alteration of
aquatic environments.
The mechanism of nutrient transportation is more effective in a situation where
predator fish move from productive to less productive habitats (Vanni 2002). For
example, when a large shoal of anadoromous fish migrate from the ocean to oligo-
trophic streams and lakes, or when benthic fish exhibit vertical feeding migration
from the lake bottom to surface waters in which nutrients are prone to be depleted,
a supply of nutrients is transported to the less productive habitat as their excreta or
their body mass themselves. The transported nutrients are quickly consumed by
microalgae and bacteria, increasing their production and decomposition rates. This
fish-driven nutrient transportation can have a substantial effect on material cycling
within an ecosystem.
In this way, fishes that are considered keystone predators of aquatic ecosystems
have the potential to drastically alter community structure and ecosystem processes
1
Post and Palkovacs (2009) recommended restricting the use of the term “niche construction” to
the process by which organisms shape environments in order to separate it from the process by
which biologically constructed environments shape selection regimes for the evolution of organis-
mal traits.
2.6 Predator Diversity and Ecosystem Functioning 33
a Trophic cascade b Nutrient transportation
Fish predator Fish predator
Predation (-)
Growth (+)
Top-down Nutrient
trophic cascade regeneration
Zooplankton prey (+) Zooplankton prey (+)
Predation (-)
Growth (+)
Microbes Microbes
Fig. 2.2 Ecological impacts of keystone fish predators on plankton communities through top-
down trophic cascade (a) and nutrient transportation (b). (+) and (−) indicate positive and negative
effects on prey or predator biomass, respectively
through trophic cascade and nutrient transportation. If mutation occurs on loci

involved in the expression of traits affecting trophic interactions and nutrient trans-
portation or if gene flows occur through outbreeding with such variants from differ-
ent populations, a new niche might be constructed within the naive population. In
the next section, we will introduce some empirical studies demonstrating that intra-
specific phenotypic variation in predator fish creates new environments in aquatic
ecosystems.
2.6 Predator Diversity and Ecosystem Functioning
It has been a great challenge for ecologists to answer the question of why biodiver-
sity is important for us. A plant ecologist David Tilman tried to answer this question
by elucidating relationships between biodiversity and ecosystem functioning (Kinzig
et al. 2001). He is the first to experimentally demonstrate that plant species diversity
positively correlates with their biomass as an index of primary productivity in ter-
restrial ecosystems. Considering that terrestrial plants provide a variety of ecosystem
services, (i.e., humankind benefits from a multitude of resources and processes sup-
plied by natural ecosystems, such as, supporting, provisioning, regulation and
cultural services; see Millennium Ecosystem Assessment 2005 for definition), it is

obvious that we profit from the conservation of plant species diversity, which results
in increased primary production. Inspired by his work, several theoretical models
have been proposed and subsequently an increasing number of empirical studies
have been conducted, for both animal and plant communities, to test the hypothesis
that biodiversity enhances ecosystem functioning (Waide et al. 1999).
What about the role of predators? Unfortunately, very few studies have examined
how the species diversity of predators affects community composition and ecosystem
processes (Straub and Snyder 2006; Schmitz 2009). There are various reasons why
studies on predator diversity effects are so limited. First, we have difficulty in experi-
mentally manipulating the species composition of predators, which have an extensive
home range associated with their high mobility. Secondly, it is not easy to theoreti-
cally predict how a combination of different predator species, which feed on prey at
different trophic levels and from different trophic pathways, will impact on an ecosys-
tem. Even if predator diversity effects are detected, we cannot easily interpret their
mechanisms using theoretical models. Furthermore, even when effects on community
composition and ecosystem processes can be quantified for each predator species, it is
impossible to conclude what traits actually lead to such community and ecosystem
consequences because the species are different from each other in traits other than
those related to feeding (Chalcraft and Resetarits Jr. 2003; Wesner 2012). However,
there is a measure to overcome such difficulties in demonstrating predator functional
diversity effects on community structure and ecosystem processes, which is, to
manipulate a diversity of trophic morphs or a species pair of fish predators.
As mentioned previously, trophic morphs are usually different only in trophic
and/or life history traits and, otherwise, share all other ecological characteristics. By
comparing different morphs or by manipulating a combination of these morphs
within a predator population, we can examine how phenotypic diversity of a focal
trait affects community and ecosystem properties. Based on this idea, Post et al.
(2008) tried to demonstrate that intraspecific phenotypic variation among predator
fish populations can alter prey community structure under natural conditions.
Post et al. (2008) focused on geographic variation in migration behavior and feed-
ing morphology among alewife populations from 19 lakes in Connecticut, USA. They
compared body size and biomass of zooplankton prey among lakes either with anad-
romous or landlocked alewives or entirely without alewives. As stated in Sect. 2.4.4,
since the anadromous alewives have larger gape width and gill raker spacing than the
landlocked alewives, the former preferentially feed on large-bodied zooplankton prey.
In the anadromous lakes, alewives were absent during the winter season, so that large-
bodied zooplankton dominated in the absence of strong zooplankton predators.
However, spring breeding migration by the anadromous alewives and the subsequent
recruitment of their YOY facilitated selective predation on large-bodied zooplankton,
seasonally eliminating larger individuals from the zooplankton communities. By con-
trast, in landlocked lakes in which alewives reside through the year, zooplankton com-
munities are always exposed to intense and indiscriminate predation by landlocked
YOY with smaller gape and gill raker spacing, perpetually skewing the zooplankton
community size towards a smaller distribution.
Intraspecific geographic variation over their life history and trophic polymor-
phisms of alewives can also alter lake environments through top-down trophic cas-
cades (Post et al. 2008). In the anadromous lakes, phytoplankton biomass increases
during the seasonal reduction in zooplankton body size and biomass, suggesting
that the anadromous YOY have positive, indirect effects on phytoplankton by
depressing the grazing intensity of large-bodied zooplankton. The work of Post
et al. (2008) is noteworthy as a milestone study demonstrating that intraspecific
variation in predator feeding functions affects ecosystem processes such as primary
productivity.
2.6.1 Mesocosm Experiments
Even though variations in prey community structure and ecosystem processes were
found between lakes with different feeding functions within a predator species, they
might be attributed to geographic variation in limno-physical and -chemical charac-
teristics or to the density of other planktivorous fish. In order to reveal the ecosys-
tem consequence of intraspecific predator functional diversity, experiments are
required in which environmental factors, with the exception of predator feeding
functions, are controlled. One promising approach is that of mesocosm
experiments.
Since Forbes (1887) proposed the idea of “The Lake as a Microcosm,” in which
lakes are considered as self-contained and circulating systems, the term “micro-
cosm” has often been used in microbiology to refer to microbial cultivation systems
containing essential components for their sustainable growth. Following experi-
mental attempts to simulate lake ecosystems containing macro organisms such as
zoobenthos and fish, the microcosms have been too small to ensure their sustain-
ability. In order to fulfill energy and space requirements for the macro organisms,
we have to provide them with a larger cultivation system. Such a self-contained
experimental system, which is larger than microbial cultivation systems but smaller
than natural ecosystems (i.e., on the meso-scale), is termed a “mesocosm.”
Mesocosm experiments enable us to manipulate a given factor by controlling all
other physical, chemical and biological environments and, thereby, to assess the
ecosystem effects of the focal factor (Fig. 2.3).
An interesting mesocosm experiment considering trophic polymorphism in ale-
wives was undertaken by Palkovacs and Post (2009) who constructed solid walled
polyethylene enclosures with 2 m diameter and 6 m depth in Rogers Lake,
Connecticut, USA. Plankton communities were exposed to different predation
regimes by introducing 15 YOY fish of either anadromous or landlocked alewives
into each enclosure in order to examine effects of predator feeding functions on prey
communities. Some enclosures were left unstocked (i.e., no fish) as a control.
Mesocosm experiments were conducted during the summer season when the YOY
fish cause top-down trophic cascades in natural zooplankton communities. Weekly
sampling of zooplankton communities from the enclosures was undertaken.
Fig. 2.3 Twelve 2,000 L mesocosms tanks set up in Center for Ecological Research, Kyoto
University. It is possible to automatically control water temperature, light intensity and L:D length.
They are useful for experiments to examine effects of fish predator manipulation on ecosystem
properties (see Sect. 2.6.2)
Experimental results were consistent with those reported for natural lakes, with
summer zooplankton body size and biomass significantly reduced only in systems
containing anadromous alewives. In addition, the presence of anadromous alewives
led to a marked reduction in species richness and the diversity index of zooplankton
communities. Palkovacs and Post (2009) were successful in demonstrating that intra-
specific variation in predator feeding functions alone could alter zooplankton size
distribution and species composition using these mesocosm experiments. This may
also support the previous conclusion that variation between lakes in primary produc-
tivity is due to differential trophic cascading effects caused by alewife morphs.
Similar results have been reported for another system exhibiting trophic poly-
morphism in fish predators. Harmon et al. (2009) conducted mesocosm experiments
with a species pair of threespine sticklebacks that underwent adaptive divergence to
benthic (i.e., benthivorous) and limnetic (i.e., planktivorous) morphs from a gener-
alist ancestor. To examine the effects of evolutionary diversification of the threes-
pine sticklebacks on ecosystem properties, they manipulated a combination of two
specialist morphs or one generalist ancestor in large tanks to artificially simulate
pond ecosystems including the plankton and benthos communities. They found
strong effects of predator functional diversification on prey community composition
and ecosystem processes such as primary productivity and water chemistry. One of
the more remarkable outcomes was that they could detect synergistic effects of the
predators’ adaptive diversification on the pond ecosystems as well as differential
effects of each morph, by comparing ecosystem consequences between simple and
diverse feeding functions. The results have ecological implications for the evolu-
tionary diversification of the sticklebacks because these morphs often coexist in
natural ponds and lakes.
Intraspecific phenotypic diversity effects of fish predators can also appear
through nutrient transportation. In guppies inhabiting streams in Trinidad, local
populations are often isolated by natural barriers such as waterfalls and are exposed
to different predation regimes from piscivorous fish. The high predation risk favors
the evolution of life history traits in guppies, including a younger age at maturity, a
smaller body size at maturity and higher reproductive rates. These life history traits
are also linked with metabolic rate, which determines physiological performance
such as respiration and excretion rate. The common garden experiments to manipu-
late fish from different populations showed that phenotypic diversification in gup-
pies results in the divergence of community structure (benthic algal and invertebrate
biomass) and ecosystem processes (gross primary productivity, leaf decomposition
rates and nutrient flux), which are altered through nutrient transportation driven by
intraspecific variation in the excretion rate of fish from different populations
(Palkovacs et al. 2009; Bassar et al. 2010).
2.6.2 Food Web Properties as a Universal Measure
In previous sections, we cited some examples in which intraspecific phenotypic

diversity in fish predators alters ecosystem properties. However, some ecosystem
properties are system-specific (e.g., species composition) and others are just a func-
tional trait of a specific guild (e.g., primary productivity by algae and decomposi-
tion rate by bacteria and fungi) rather than ecosystem functions performed by an
entire community. How then can we generalize from a variety of results from differ-
ent systems and what is a universal measure for ecosystem properties, which are
ubiquitous and intrinsic to all aquatic systems, thus allowing comparisons to be
made between systems? Here we focus on structural properties of food web as a
universal measure for the entire community.
A food web is a diagram to depict the overall energy flows through trophic inter-
actions within an entire community (Lindeman 1942). Since the Eltonian pyramid
(Elton 1927), a variety of ideas have been proposed to describe structural properties
of intricate food webs in nature. One of promising measures to characterize food
web properties is food chain length (FCL), defined as the number of trophic trans-
fers of energy from primary producers to a top predator, which has been easily
measured and comparable across ecosystems, with the recent development of isoto-
pic technique (Post 2002). In lake ecosystems, the FCL can be the best explained by
the lake size in volume (Post et al. 2000). However, it also varies temporally even
Fig. 2.4 Allometric

relationships between body
size and trophic level or
Trophic level
numerical abundance in
aquatic communities
Abundance
Body size
within a lake, as in the case of Lake Biwa (Okuda et al. 2012). The possible mecha-
nism to cause temporal variation in the FCL may be compositional and functional
changes in plankton and benthos prey communities, which can affect the number of
trophic links.
In aquatic food webs, there also exists a general rule in which larger organisms
eat smaller ones and becomes fewer in number, so that organisms increase their
trophic levels and decrease abundance with their body mass (Fig. 2.4; also see
Cohen et al. 2003). Based on the allometric relationship between body size and
biomass (body mass multiplied by the numerical abundance in each size class), size
distribution of entire community can be formulated as the size-biomass spectrum,
defined as the slope of body mass–biomass regression (de Eyto and Irvine 2007;
Jennings and Mackinson 2003). When the community size distribution skews
toward smaller-sized organisms, the size-biomass spectrum slope become steeper.
Jennings et al. (2002) also proposed a new method to predict predator–prey body-
mass ratios (PPMR) in food webs, using their nitrogen stable isotope ratio as a
proxy of trophic level. The PPMR can be calculated as the inverse of body size-
trophic level regression slope in Fig. 2.4. The PPMR is an important factor deter-
mining interaction strength between preys and predators and in turn the stability of
food webs (Emmerson and Raffaelli 2004).
To examine how evolutionary diversification of fish feeding traits alters food web
properties of prey communities, we conducted mesocosm experiments that simu-
lated conditions at Lake Biwa where ecological diversification occurred indepen-
dently in some phylogenetically distant fish groups during the last 400,000 years
a b
No fish (NO) Benthivores (B)
G. elongatus elongatus
G. elongatus elongatus
c d
Benthivore & planktivore (BP) Planktivores (P)
G. elongatus elongatus G. Caerulescens
G. Caerulescens G. Caerulescens
Fig. 2.5 An experimental design of predator manipulation. Each treatment corresponds to histori-
cal change in diversity of fish feeding functions in a lake. The lake has no fish in original condition
(a), an ancestral benthivorous fish colonizes the lake (b), and then the colonized population experi-
ences ecological speciation into benthivorous and planktivorous species (c). However, fish diver-
sity decreases if either of these two becomes extinct. The ancestral benthivorous species may go
extinct for some reason, e.g., destruction of coastal habitats under human disturbances (d)
after the development of deep pelagic habitats (see Sect. 2.4.3). We set up 12 meso-
cosm tanks in which abiotic environments (i.e., light intensity, L:D length, water
temperature and nutrient levels) were controlled and then a plankton community
and supplementary zoobenthos prey were provided (Fig. 2.3). We manipulated the
phenotypic diversity of feeding functions in fish predators, using a species pair of
Gnathopogon that had diverged into planktivorous G. caerulescens and benthivo-
rous G. elongatus elongatus but remained reproductively compatible to each other
(see Sect. 2.4.3). We conducted experiments with a full-factorial design for four
treatments: no fish (NO), benthivorous G. elongatus elongatus (B), and both plank-
tivorous G. caerulescens and benthivorous G. elongatus elongatus (PB), and plank-
tivorous G. caerulescens (P), assuming historical change in diversity of fish feeding
functions in a lake (Fig. 2.5).
We measured the size-biomass spectrum, FCL and PPMR of plankton prey com-
munities in the mesocosm tanks. It was predicted that planktivorous fish would
skew the plankton communities toward a smaller size distribution through a top-
down trophic cascading effect, under which a large zooplankton biomass would be
depressed and a smaller plankton biomass would be indirectly enlarged, resulting in
a steeper slope of size-biomass spectrum in the order of NO < B < PB < P. Contrary
to this prediction, the plankton size-biomass spectrum did not significantly differ
among these four treatments though the presence of fish predator increased the bio-
mass of phytoplankton (Fukumori et al. unpublished data). The benthivorous
G. elongatus elongatus feeds mainly on benthos but also less efficiently on plank-
ton, as is often the case in other benthivorous fishes. The mesocosm tanks with a
volume of 2,000 L might not be large enough to control predation of ben-
thivorous G . elongatus elongates on zooplankton.
However, we found significant differences in the FCL and PPMR among the
treatments. Under the presence of benthivorous fish, the plankton FCL, defined as
the highest trophic level observed for all samples of size-fractionated plankton com-
munities, increased and the PPMR of plankton communities decreased (Sakai
2013). Although underlying mechanisms for these results remain unclear, selective
predation of the two fishes on different species of large-sized zooplankton (e.g.,
cladocerans versus copepods) is likely to alter trophic relations within plankton
communities. More interestingly, we detected synergetic effects of predator feeding
functional diversity on both indices. Under the coexistence of fish with different
feeding functions, fish production, particularly for benthivorous fish, increased,
possibly due to reduced food resource competition between planktivorous and ben-
thivorous fish: the benthivore can exploit benthic food exclusively in the absence of
benthic competitors (Fukumori et al., unpublished data). Assuming that the nutrient
excretion rate scales with fish body mass (Torres and Vanni 2007; McIntyre et al.
2008), the benthivorous fish coexisting with the planktivorous fish might enhance
nutrient transportation from the benthic to the pelagic habitats, resulting in syner-
getic effects of top-down and bottom-up trophic cascades on the plankton food
webs. Our experiments demonstrate that predator phenotypic diversity can alter
food web properties of prey communities and thus the overall energy flows within
an ecosystem.
2.7 Eco-Evolutionary Feedbacks
There is no doubt that intraspecific phenotypic diversity of fish predators is an

important driver for altering prey community composition and thus ecosystem prop-
erties. However, we must also consider an overlooked point, which is that ecosys-
tem alteration, as a consequence of fish phenotypic diversification, creates new
aquatic environments, i.e., niche construction, which can shape the adaptive land-
scape for the evolution of predators themselves as well as prey species. Ecological
interactions between a keystone species and other community members drive evo-
lutionary changes in their adaptive traits through environmental alterations and, in
turn, the adaptive evolutionary changes shape the form of ecological interactions.
This process, in which ecology and evolution reciprocally interplay over contempo-
rary time-scales, is termed “eco-evolutionary feedback” (Post and Palkovacs 2009;
2.7 Eco-Evolutionary Feedbacks 41
Keystone predators
Evolutionary diversification
Gene Individual
Expression
Natural selection Impact

Population
&
Community
Characterization Action
Ecosystem
Environment
properties
Niche
construction
Fig. 2.6 A conceptual model for eco-evolutionary feedbacks. In aquatic ecosystems, fish preda-
tors often have evolved phenotypic polymorphism as a consequence of intraspecific resource par-
titioning in colonized populations or under newly created environments. When they alter ecosystem
properties through compositional changes of prey communities, a new niche is constructed, which
in turn molds fitness landscapes for themselves and other species, feeding back to metagenomic
changes in the whole community
Fig. 2.6). Although eco-evolutionary feedbacks are poorly understood, some studies
have provided evidence that such feedbacks do operate in natural conditions.
2.7.1 Feedback Loops
A good example of a widely studied system is that of alewife-zooplankton interac-

tions in lakes. In landlocked lakes, intense and constant predation by alewives elimi-
nates large-bodied zooplankton and skews the prey size toward a smaller distribution
throughout the year. This results in individuals with smaller gape width and gill
raker spacing being favored when foraging on smaller prey. Such a situation will
place the landlocked alewives under strong directional selection for feeding on
small-bodied zooplankton, driving the adaptive evolution of the landlocked morph
from an anadromous ancestor (Palkovacs and Post 2008). In addition, sporadic
occurrences of physical barriers to fish migration between freshwater and marine
habitats promotes the parallel evolution of landlocked morphs independently in dif-
ferent locations, resulting in spatio-temporal heterogeneity in the geographic distri-
bution of feeding traits within the species (Palkovacs et al. 2008).
It has been also suggested for Gnathopogon fishes that planktivorous morphs evolved
from the fluvial ancestors with benthivorous morph independently in some lakes where
there exist few fish competitors for zooplankton prey (Kakioka et al. 2013b). Among
these populations with the great geographic variation in geometric morphology, a popu-
lation endemic to Lake Biwa seems to have been most adapted for plankton feeding in
pelagic environments, with its longest evolutionary history (Kakioka 2013).
Geographic variation in keystone predator phenotypes also has the potential to
drive evolutionary divergence in their prey as well as to alter food web properties of
prey communities. Walsh and Post (2011) recently evaluated the link between pheno-
typic variation in predators and their prey species by rearing water fleas, Daphnia,
from lakes containing predatory alewives with different phenotypes under different
water temperature and resource conditions, and then comparing their life history traits
among these lakes. They found that Daphnia grew faster, matured earlier, and pro-
duced more offspring in lakes with anadromous alewives than in lakes with land-
locked or no alewives. Although life history theory predicts that increased predation
on large sized-zooplankton selects for maturity at smaller size, laboratory experiments
showed that Daphnia matured at a slightly larger size in anadromous lakes, in which
alewives have both a larger gape width and gill raker spacing to preferentially forage
larger prey (see Sect. 2.4.4). This result seems to be inconsistent with the theory. The
evolutionary response of Daphnia to divergent predation regimes can be best explained
as an adaptation to a colder environment and shorter growing season known as coun-
tergradient variation (sensu Conover et al. 2009). For Daphnia from the anadromous
lakes, the colder environment and shorter growing season results from the seasonal
migration and predation by anadromous alewives, which substantially extirpated
reproductive populations of Daphnia early in the summer. In this prey–predator sys-
tem, prey life history evolution is facilitated by seasonal occurrence of increased pre-
dation, associated with predator life history traits rather than predation intensity and
size-specific predation associated with predator feeding traits.
Walsh and Post (2012) also focused on how predator evolutionary divergence can
mold the evolution of phenotypic plasticity in prey life history traits. It is well known
that Daphnia alternate between sexual and asexual phases, producing parthenogenetic
eggs (i.e., fully developed eggs without fertilization) throughout most of the year and
sexual resting eggs during periods when environmental conditions deteriorate.
Increased occurrence of predators selects for prey individuals that pass through the
period of high predation as resting eggs. In lakes with landlocked alewives, Daphnia
are under intense year-round predation, whereas they experience temporal but predict-
able predation in the anadromous lakes into which alewives seasonally migrate from
marine habitats. According the theory, the temporal variation of alewife occurrence
should affect a response of Daphnia engaged in sexual reproduction. To test this pre-
diction, Daphnia from lakes with different alewife phenotypes were exposed to ale-
wife kairomones as an environmental cue for the presence of predators. They found
that, when exposed to the fish kairomones, Daphnia from the anadromous lakes
invested more in sexual reproduction than those from the landlocked or alewife free
lakes, suggesting a flexible life history trade-off in response to the predation risk. In
conclusion, the divergent evolution of predator phenotypes has evolutionary conse-
quences for phenotypic plasticity of prey life history traits.
2.7 Eco-Evolutionary Feedbacks 43
2.7.2 Community Genomic Dynamics
In lake ecosystems, eco-evolutionary feedback loops can also cascade from

Daphnia to microbes, such as bacteria, microalgae and protozoa, because
Daphnia has strong impacts on microbial communities through resource com-
petition and nutrient regeneration, due to its high grazing ability and excretion
rate (Carpenter et al. 1985; Carpenter et al. 1992). However, such cascading
effects have been hitherto evaluated only as the overall response of each tro-
phic guild (e.g., primary producer, primary consumer or decomposer) or func-
tional group (i.e., pico-, nano- or micro-plankton) rather than of each microbial
taxon. Microbial diversity, particularly of bacteria, is primarily important in
determining ecosystem functioning and, thus, ecosystem services for human-
kind, including the decomposition of organic matter, nutrient cycling and water
purification (Bell et al. 2005; Cardinale 2011). Prompt responses of bacterial
communities to changing environments are achieved by rapid evolution rates as
well as by species turnover (Fukami et al. 2007; Gravel et al. 2011). Decades
ago, the largest obstacle to disentangling the intricate relationships between
bacterial diversity and ecosystem functioning was the difficulty in character-
izing bacterial species composition in situ because most of them are unculti-
vable and thus cannot be isolated for species identification. However, recent
advances in molecular techniques and bioinformatics have developed metage-
nomics or ecogenomics to characterize a profile of community-level genetic
diversity in situ or comprehensively search for functional genes involved in
phenotypic expression (see Chap. 3). The advent of next generation sequencer
technologies has also accelerated ecological research as well as advancing our
understanding of the molecular phylogenetics of aquatic microbial communi-
ties (Kalyuzhnaya et al. 2008).
As discussed previously, plankton communities can be affected by pheno-
typic polymorphism in fish predators. Recent molecular studies on fish pheno-
typic polymorphism suggest that alleles at a small number of loci have large
effects on adaptively divergent traits (Colosimo et al. 2005), contrary to tradi-
tional views of quantitative genetics that consider polygenic variation in a large
number of loci to have additive small effects on phenotypes. If it is general in
fishes, such a gene with large effects may act as a “keystone gene” to influence
metagenomic dynamics of whole plankton communities and, consequently,
ecosystem properties. This is known to occur in terrestrial ecosystems where
genetic variation within a population of foundation plant species is inherited
through its phenotypic expression (e.g., concentration of chemical defense sub-
stances) to community and ecosystem phenotypes (e.g., species composition
and interactions, nutrient cycling, and decomposition rate) (Whitham et al.
2006). It will not be long before we can examine the nature of the eco-evolu-
tionary feedbacks as community genomic dynamics under water, through a
molecular-scope.
2.8 Why is Predator Diversity Important?
Traditionally, evolutionary biologists have searched for an answer to the questions

of how and when current biological communities diversified using fossil and molec-
ular records, which help to infer the past changes in morphology and DNA sequence.
However, ecologists have been more interested in what are the ecological implica-
tions for evolutionary diversification of current biological communities, often
assuming that species’ traits are static rather than variable. As demonstrated by an
increasing number of studies, we now perceive that organismal traits are evolving at
a faster rate than was previously assumed (Hairston et al. 2005), which leads to a
new idea that the evolution of the organismal traits dynamically interplays with the
ecology of populations, communities and ecosystems, and vice-versa (Post and
Palkovacs 2009). Biological diversity observed in nature can therefore be viewed
not only as a consequence of past evolutionary events but also as a product of on-
going evolution in existing communities. Diversity currently found within/among
keystone predator populations can have the potential to influence the future direc-
tion of diversity at three levels of biological organization, from genes to ecosystems,
through eco-evolutionary feedbacks.
At present, species extinction has progressed rapidly, with an accelerating rate,
due to anthropogenic disturbances ranging from local human activities to global
climate change. Biodiversity loss is particularly severe in freshwater ecosystems
(Secretariat of the Convention on Biological Diversity 2010). Although much atten-
tion has been paid to the conservation of species, specifically those that are endan-
gered, we also have to conserve the functional diversity of keystone species within/
among populations, which may not necessarily be endangered. The effects of preda-
tor functional diversity can sometimes extend to ecosystem functioning, such as
energy flows and nutrient cycling, from which we can enjoy a variety of ecosystem
services profitable for human well-being.
In this chapter, the ecological and evolutionary importance of functional diver-
sity of fish predators in the context of ecosystem management, as well as of tradi-
tional conservation biology, has been discussed. In order to deepen our understanding
of the processes and mechanisms for generating and maintaining biological diver-
sity, we have to further accumulate empirical data and establish a framework to
integrate the theory of eco-evolutionary feedbacks. This idea is expected to develop
a new paradigm for biological synthesis, linking from molecular biology to
macroecology.
Acknowledgements We thank Dr. T. Kokita for his comments on our manuscript. We also thank
R. Kakioka and Y. Sakai for providing their unpublished data. This manuscript was under the sup-
port of the Global COE Program (06) from the MEXT, Japan, and The Environment Research and
Technology Development Fund (D-1102 and S-9) of the Ministry of the Environment, Japan, and
the JSPS Grant-in Aid (No.20370009 and No.23657019).
References 45
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Chapter 3
Biodiversity Researches on Microbial
Loop in Aquatic Systems
Abstract The food linkage between heterotrophic bacteria and protists is so-called
“microbial loop,” functioning as important matter cycling in pelagic food webs.
Biomass of heterotrophic bacteria sometimes predominates total heterotrophic bio-
mass in lakes, and organic matter transfer started from heterotrophic bacteria has been
intensively studied by numerous researchers all over the world. The roles of plank-
tonic protists, such as heterotrophic nanoflagellates and ciliates, in microbial loop are
to consume bacteria that are too small to serve directly as major prey items for most
zooplankters, and to be themselves utilized by the zooplankton. There is a consensus
that food linkages between bacteria and protists are substantial in many lakes. In addi-
tion, bacterial loss due to viral lysis has also been paid great attention by many
researchers since the late 1990. The present review provides the overview on the trend
and future stage of microbial loop researches in freshwater systems, with special ref-
erence to culture-independent molecular techniques such as PCR cloning and sequenc-
ing, fluorescently in situ hybridization or denaturing gradient gel electrophoresis for
phylogenetic analyses on microbial communities. A review on ecology and biodiver-
sity researches on microbial loop in Lake Biwa is also provided.
Keywords Bacteria • Biodiversity • Ciliates • Culture-independent molecular tech-

niques • Lakes • Microbial food web • Microbial loop • Nanoflagellates • Protists
3.1 Introduction
In pelagic areas of lakes or oceans, matter cycling is mainly driven by planktonic food
web. It is well known that the herbivorous food web where phytoplankton are preyed
on zooplankton is one important matter cycling in pelagic ecosystems. By contrast,
the food linkage between heterotrophic bacteria and protists, so-called “microbial
loop,” has been known as another important matter cycling in pelagic food webs
(Fig. 3.1) (Azam et al. 1983). Phytoplankton release dissolved organic matter (DOM)

52 3 Biodiversity Researches on Microbial Loop in Aquatic Systems
as intermediate products of photosynthesis and/or as autolytic products (Riemann and

Søndergaard 1986). DOM thus released is utilized for growth of heterotrophic bacte-
ria, followed by protistan grazing on bacteria. Protists thereafter are consumed by
meso-zooplankton such as cladocerans and/or copepods. Biomass of heterotrophic
bacteria sometimes predominates total heterotrophic biomass in lakes (Kawabata and
Nakanishi 1996), and organic matter transfer started from heterotrophic bacteria has
been intensively studied by numerous researchers all over the world.
The roles of planktonic protists, such as heterotrophic nanoflagellates and cili-
ates, in microbial loop are to consume bacteria that are too small to serve directly as
major prey items for most zooplankters, and to be themselves utilized by the zoo-
plankton (Azam et al. 1983). There is a consensus that food linkages between bac-
teria and protists are substantial in many lakes (Nagata 1988; Bloem and Bar-Gilissen
1989; Sanders et al. 1989; Šimek et al. 1990, 1995; Šimek and Straskrabova 1992;
Nakano et al. 1998a, b). In addition, bacterial loss due to viral lysis has also been
paid attention by many researchers since the late 1990 (Suttle 2007).
The present review provides the overview on the trend and future stage of micro-
bial loop researches mainly in freshwater systems, together with some related
researches in marine systems, during the last decade. In addition, I review biodiversity
researches on microbial loop in Lake Biwa, together with a perspective on them.
3.2 Towards More Complicated Microbial Food Web
Bergh et al. (1989) reported density of virus in freshwaters (254 × 106 particles
mL−1) is higher than that of marine waters (up to 14.9 × 106 particles mL−1). Due to
stimulation by Bergh et al. (1989), aquatic microbial ecologists examined abun-
dance of bacteria infected by viruses (0.7–9 %, Weinbauer and Höfle 1998). Based
on the measurements of primary production, bacterial production, protistan bacte-
rivory, bacterial lysis by viruses, and production of viruses, Bratbak et al. (1992)
have concluded importance of DOM release by viral lysis of bacteria in carbon
cycle in a microbial loop, and they proposed “viral loop” which included the DOM
release in a basic microbial loop (Fig. 3.1). Wilhelm and Suttle (1999) pointed out
that viruses were also infectious to other planktonic organisms such as phytoplank-
ton, suggesting “viral shunt” which included DOM releases from viral lysis of bac-
teria, phytoplankton and their grazers.
Since virus infection is basically species specific, viral lysis of bacteria may
occur at population level. So, viruses may preferentially reduce the bacterial popu-
lation with active growth (“kill the winner” model, Thingstad 2000). The model
shows coexistence of bacterial populations by host-specific viruses that prevent the
best bacterial competitors from building up a high biomass (Thingstad 2000). Since
the late 1990s, some researchers have made comparison in loss of bacterial abun-
dance between protistan grazing and viral lysis, and the relative importance between
the two may be dependent on oxygen environment in a water column (Weinbauer
and Höfle 1998; Pradeep Ram et al. 2010). Some researchers have reported differ-
ence in the relative importance among bacterial phylogenies. In Rimov Reservoir,
3.2 Towards More Complicated Microbial Food Web 53
Fig. 3.1 (a) The original concept of “microbial loop” (Azam et al. 1983) and (b) microbial food
webs revised by using the literature so far published after Azam et al. (1983). In the panel B, food
webs within protists are shown. Mixotrophic protists are included in phytoplankton, but serve as
grazers depending on environmental conditions. The food chain from phytoplankton to zooplank-
ton via fungi is called as “Myco-loop” (Kagami et al. 2007). “Viral loop” (Bratbak et al. 1992) and
the food chain via microparticles (Kerner et al. 2003) are also shown
Czech Repblic, the most important loss process of β-proteobacteria was protistan
grazing (Šimek et al. 2007). In contrast, loss to grazing on Cytophaga bacteria was
not so high relative to that of β-proteobacteria, and this was more remarkable in the
presence of viruses (Šimek et al. 2007). Pradeep Ram and Sime-Ngando (2008)
have reported stimulation of virus infection to bacteria due to activation of bacterial
growth supported by nutrient regeneration by bacterial grazers.
Thus, since the incorporation of viruses into microbial loop, researchers have
been studying more complicated food web dynamics (Fig. 3.1). This is further
accelerated after the fusion of food web with nutrient cycling. However, the present
trend is important, because organisms in many lakes and ponds live under nitrogen
and/or phosphorus limitation.
In addition, the finding of abiotic particles produced by aggregation of DOM
under some chemical processes is also important for microbial loop researches
(Kerner et al. 2003). Some of those abiotic particles have the sizes similar to those
of planktonic bacteria, containing DNA, lipids, sugars and/or proteins those of
which make the C:N ratio of the particle as 4.1–6.8 (Kerner et al. 2003). Those
results strongly suggest that the particles are important food items for bacteria graz-
ers such as protists. More interestingly, production rate of the particle was similar to
that of bacterial production (Kerner et al. 2003). In future studies, we may have to
include organic matter transfer from the particles to bacterial grazers to figure out
more reliable food web dynamics and/or matter cycling in planktonic systems
(Fig. 3.1).
3.3 Detection of Microorganisms Using Molecular Biological

Techniques
3.3.1 Biodiversity of Bacteria
Culture-independent molecular techniques such as PCR cloning and sequencing,

fluorescently in situ hybridization (FISH) or Denaturing Gradient Gel Electrophoresis
(DGGE) are now commonly used for phylogenetic analyses on microbial communi-
ties (DeLong and Karl 2005). FISH, which demonstrated the predominant bacterial
clade SAR11 (α-proteobacteria) in oceans (Giovannoni and Stingl 2005), is one of
the most powerful techniques to detect particular microbial populations. In freshwa-
ter systems, phylogenetic analyses on bacterial community structure have been con-
ducted with several methods including clone library or FISH. There are 34
phylogenetic clusters of closely related sequences that are restricted to freshwater
and/or dominated by freshwater sequences (Zwart et al. 2002). Some dominant
clusters such as the ACK-M1 cluster (acI-A) of Actinobacteria, the LD12 cluster
(alfV) of Alphaproteobacteria, the Rhodoferax sp. BAL47 cluster (including the
R-BT065 cluster) (beta I), the Polynucleobacter necessarius cluster (beta II) of
Betaproteobacteria, and the SOL cluster (including the LD2 cluster) of Bacteroidetes
have so far been reported from freshwater systems (Zwart et al. 2003; Warnecke
et al. 2004, 2005; Schauer and Hahn 2005; Šimek et al. 2005; Hahn 2006; Newton
et al. 2011; Salcher et al. 2011; Hahn et al. 2012; Watanabe et al. 2012). Members
of the R-BT065 subgroup and the newly proposed genus Limnohabitans are
included in the Rhodoferax sp. BAL47 cluster (Šimek et al. 2001; Hahn et al. 2010a,
b; Kasalický et al. 2010).
Ecological roles of some of those dominant bacterial phylogenetic clusters have
already been elucidated. Abundance of Polynucleobacter necessarius ssp. asymbi-
oticus (PnecC) has positive correlation with concentration of lake humic substances,
suggesting importance of the bacteria as decomposers of the organic matter
(Jezberová et al. 2010). The bacteria in Limnohabitans cluster have high growth
rates, serving as important food sources for heterotrophic nanoflagellates (Horňák
et al. 2006; Šimek et al. 2006). For bacterial phylogenetic groups other than
3.3 Detection of Microorganisms Using Molecular Biological Techniques 55
Limnohabitans cluster bacteria, phosphorus availability may be more important

than grazing (Horňák et al. 2006).
Recently, pyrosequencing (next-generation sequencing) technique has been
remarkably applied to analyze microbial community structure, and those studies
have so far demonstrated enormous bacterial and/or archaeal species (Operational
Taxonomy Unit, OTU) diversity in marine environments (Sogin et al. 2006; Brazelton
et al. 2010). Those studies have revealed many undescribed taxa and lineages of
bacterial and/or archaeal species, and have indicated the presence of large numbers
of rare taxa among the relatively few abundant species that dominate these assem-
blages in any particular environment, so called “rare biosphere” (Sogin et al. 2006;
Brazelton et al. 2010). Those rare biosphere species have low abundance, suggesting
less mortality due to limited encounter with their grazers and/or specific viruses
(Sogin et al. 2006; Caron and Countway 2009). In addition, protistan grazers may not
consume those rare biosphere species so much because of their small cell size and/or
low growth rate (Pedrós-Alió 2006). Those rare biosphere species may serve as a
potentially inexhaustible genomic reservoir, which could explain how microbial
communities respond to subtle environmental changes (Sogin et al. 2006).
For bacterial community structure analyses in freshwater systems using pyrose-
quencers, not so many studies have so far been conducted. Those studies examined
bacterial community structure in biofilms developed in a drinking water distribution
system (Hong et al. 2010), bacterial community structure of Amazon River (Ghai
et al. 2011), difference in community structure of air-borne bacteria inoculated into
sterilized Swedish rock pool waters (Langenheder and Székely 2011), seasonal
changes in bacterial OTU composition in relation to some environmental events such
as phytoplankton blooms, wax and wane of zooplankton and nitrification in Lake
Erken, Sweden (Eiler et al. 2012) and bacterial OTU richness in fourteen Swedish
lakes with different lake area, catchment area and trophic status (Logue et al. 2012).
Eiler et al. (2012) successfully demonstrated the responses of bacterial community to
those biological changes, identifying ecological characteristics of some bacterial
phylogenetic groups. Logue et al. (2012) tried to elucidate the mechanisms that
underlie and maintain bacterial biodiversity and patterns in its spatial distribution in
fourteen nutrient-poor Swedish lakes. The authors found a positive correlation
between bacterial OTU richness and nutrient availability, but the relationships
between bacterial OTU richness and lake/catchment area were negative. Those new
studies are ecologically interesting, and more collection of bacterial community
structure in freshwater systems using next-generation sequencing will be needed.
Besides exploring genetic diversity of bacteria, we need to know ecophysiology
of each bacterial species. To do that, isolation and incubation of particular bacterial
species are necessary. It is well known that almost all bacterial species are non-
culturable, and some isolation and incubation techniques have been developed for
higher-throughput of bacterial cultures (Connon and Giovannoni 2002). This is also
the case for freshwater bacteria. Most of bacteria in 34 freshwater phylogenetic
clusters are non-culturable (Zwart et al. 2002), but some studies have developed
successful culture methods for some dominant freshwater bacterial clusters (Hahn
2003; Watanabe et al. 2009).
3.3.2 Biodiversity of Protists
Molecular biological techniques have also been largely introduced into protistan
biodiversity researches (Massana et al. 2006). Moon-van der Staay et al. (2001)
demonstrated high diversity of picoeukaryotes in the sequences of the 18S ribo-
somal RNA gene amplified from a picoplanktonic assemblage collected in the equa-
torial Pacific Ocean. The sequences of those picoeukaryotes were previously
unknown which might be assigned to some major marine phyla such as prasino-
phytes, haptophytes, dinoflagellates, stramenopiles, choanoflagellates and acanthar-
ians. Stramenopiles which include many of so-called flagellates are one of the most
commonly detected marine phyla (Massana et al. 2006). Most of flagellates do not
have distinct morphological characteristics which should be used for identification
for genus or species, and cells of some flagellate species are easily deformed by
addition of fixatives. So, some DNA probes to detect certain flagellate populations
by FISH method have been developed (Lim et al. 1999). Massana et al. (2009) used
two oligonucleotide probes prepared with 18S rRNA genes derived from chryso-
phyceae flagellates in Blanes Bay, Spain, and respectively detected two populations
with average 19 % and 3 % within the total flagellate community. In addition, some
of those flagellates ingested fluorescently labeled bacteria (Massana et al. 2009).
Countway et al. (2005, 2007) investigated protistan diversity by T-RFLP method
in the waters collected from the North Atlantic and North Pacific oceans, and found
that dominant OTUs of the protists from both oceans contributed only to Atlantic or
Pacific OTUs, and the OTUs detected in both the Atlantic and Pacific Ocean sam-
ples accounted only for 22 % of the total. Pyrosequencing technique has been also
introduced to examine protistan diversity, and Logares et al. (2012) have demon-
strated high diversity of marine stramenopile flagellates in European coastal waters
in relation to their geographical distribution and habitat condition.
The term “rare biosphere” is also valid for protistan diversity: the presence of
large numbers of rare taxa among the relatively few abundant species that dominate
these assemblages in any particular environment, so called “rare biosphere” (Caron
and Countway 2009). Countway et al. (2005) incubated a seawater sample collected
from the Western North Atlantic and found changes in overall eukaryotic diversity
predominated by protists and species composition expressed as phylotype diversity.
The eukaryotic diversity estimated with species richness showed minor changes.
However, changes in the dominant eukaryotic phylotypes were substantial, and this
was also the case for “rare biosphere” species. Those results again suggest that pro-
tistan species in “rare biosphere” serve as a potentially inexhaustible genomic res-
ervoir, which could explain how protistan communities respond to subtle
environmental changes (Caron and Countway 2009).
In freshwater systems, we already have plenty of information about ciliate diver-
sity (Beaver and Crisman 1982, Finlay et al. 1998 and literature therein, Foissner
1999 and literature therein). By contrast, the information about flagellate diversity
is still very limited (Auer and Arndt 2001). However, if we consider freshwater
protistan species in “rare biosphere,” we do not have any information so far. To
3.4 Recent Development in Studies on Food Chain Between Bacteria and Protists 57
detect “rare biosphere” microorganisms, we need to use some molecular biological

techniques. Studies with some molecular biological approaches are necessary to
have the information about freshwater protistan species in “rare biosphere.”
One of flagellate genera commonly detected in freshwaters is Spumella. Many of
previous studies have determined dominant flagellate genera using cell morphology,
and many small colorless chrysophytes have been identified as the genus Spumella
or Spumella-like (Sanders et al. 1989). Pfandl et al. (2009) investigated the molecu-
lar microdiversity for 13 Spumella-like flagellate strains isolated from two Austrian
freshwaters, followed by examination of their affiliation to different ecotypes with
distinct small subunit ribosomal ribonucleic acid (SSU rRNA) genotypes. The eco-
physiological tolerances of the flagellates to temperature or salinity were also exam-
ined. The authors have found that those strains consisted of different ecotypes and
genotypes, and molecular distance was correlated to temperature and salinity toler-
ances. Those results contradict the assumption that variations in SSU rRNA are due
to accumulation of neutral mutations. So, the authors have concluded that current
taxonomy of species on the Spumella-like flagellate strains is inappropriate at least
with respect to ecological or ecophysiological studies.
3.4 Recent Development in Studies on Food Chain Between

Bacteria and Protists
As we discussed earlier, molecular biological techniques have enabled us to have

detection of microbial genus/species level and analysis of microbial diversity. So,
the researchers of microbial loop have been paying attention to difference in vulner-
ability for grazing among bacterial phylogenetic groups. In marine studies so far
conducted, we have not yet found any particular bacterial phylogenetic groups vul-
nerable to grazing (Yokokawa and Nagata 2005; Massana et al. 2009). By contrast,
some bacterial phylogenetic groups in some freshwaters have been reported as vul-
nerable to grazing (Šimek et al. 2007).
The commonest method to determine grazing rate on bacteria by protists may be
the one which uses surrogate food particles such as fluorescently labeled bacteria
(Sherr et al. 1987; Nakano et al. 1998a, b) or beads (Ichinotuska et al. 2006;
Okamura et al. 2012). There are two great advantages of this method. The first is
that incubation times are short. The second is that we can observe protists which
ingest surrogate particles under an appropriate microscope, and this enables us to
identify which protists (species or genus) are bacterivores, and how much percent-
age of protists conduct bacterivory. Fluorescently labeled bacteria (FLB) are most
frequently used as surrogate particles (Sherr et al. 1987; Nakano et al. 1998a, b).
However, this method has some challenges (Landry 1994). The most serious point
is that protists select among a variety of particle types. Some protists ingest surro-
gate particles added, and the others do not show any response even if they are bac-
terivores. No general pattern of preference has been found for either heat-killed
bacteria or artificial latex beads (Sanders et al. 1989; Montagnes and Lessard 1999).
Some studies have demonstrated protistan prey preference for living over non-living
microorganisms (Landry et al. 1991; Montagnes and Lessard 1999; Massana et al.
2009). A stramenopile flagellate Spumella egested FLB ingested into its food vacu-
ole after a vacuole passage time of about three minutes, while the vacuole passage
time of unstained living bacteria exceeded twenty minutes. Massana et al. (2009)
prepared FLB using Brevundimonas diminuta and two FISH probes which respec-
tively detected two bacterial strains Nereida sp. and Dokdonia sp. FLB of
B. diminuta was heat-killed, while other two bacterial strains were also prepared as
alive. The authors used natural flagellate grazers in a water sample collected in
Blanes Bay, Spain, and two stramenopile flagellate groups, MAST-4 and MAST-1C,
were detected using two FISH probes. Using those stuffs, the authors made com-
parisons between grazing rates determined with the FLB and with the living bacte-
rial strains. For MAST-4 flagellates, their grazing rates determined with the living
bacterial strains were higher than those with the FLB, similar to the results in previ-
ous studies (Boenigk et al. 2001). By contrast, for MAST-1C flagellates, the grazing
rates determined with the FLB were higher than those with the alive bacteria. In
addition, MAST-1C flagellates did not ingest Dokdonia sp. The authors concluded
that small cell size of Dokdonia sp. made the bacteria inedible for MAST-1C flagel-
lates. Researchers of microbial ecology in freshwaters have so far examined bacte-
rial response to grazing. Pernthaler (2005) summarized phenotypic properties of
bacteria which may provide protection from protistan grazing: filamentation of cell
morphology, changes in cell surface potential, cell size reduction, changes in motil-
ity patterns, toxin production, cell-to-cell communication, and production of exo-
polymer wrapping cells inside. Among those, filamentous form of bacteria is mostly
known as protection by protistan grazing, and filamentous bacteria were often abun-
dant at high protozoan grazing pressure to resist grazing (Pernthaler 2005; Young
2006). Mysteriously, microbial ecology researchers in marine environments have
not paid great attention to bacterial response to grazing so far (Sherr and Sherr
2002). The information so far collected by freshwater researchers will be useful also
for marine researchers, though I do not know the reason for much less studies on
bacterial response to grazing in marine environments.
After 1990s, bacterivory by mixotrophic protists has also been paid great atten-
tion (Fig. 3.1b). Studies on mixotrophs’bacterivory have been conducted both in
freshwater and marine systems, and relative importance of bacterivory between
mixotroph and heterotrophs has been examined. Zubkov and Tarran (2008) made
comparisons of grazing rate on bacteria by plastidic and aplastidic protists in the
euphotic layer of the North Atlantic Ocean. The former was considered as mixotro-
phic and numerically dominant. The authors especially referred on plastidic protists
with small cell size (<2 μm). The latter was heterotrophic and less numerically
abundant relative to the former one. Specific ingestion rates (bacterial number
ingested one cell of protist per unit time) of plastidic protists were lower than those
of aplastidic protists. As a result, community ingestion rates (bacterial number
ingested by protists in one ml of water per unit time) of small plastidic protists were
at levels similar to those of aplastidic protists.
3.6 Biodiversity Researches on Microbial Loop in Lake Biwa 59
In freshwater systems, there are good researches on bacterivory by mixotrophic

protists (Kimura and Ishida 1985; Bird and Kalff 1986; Urabe et al. 2000; Jones
2000).Tittel et al. (2003) studied on ecology of mixotrophic flagellate, genus
Ochromonas, together with formation mechanism of deep subsurface chlorophyll a
maximum in an acidified lake whose food web structure was simple with poor flora
and fauna. Ochromonas could kept its high abundance and grazing activity by
organic matter production of its photosynthesis even after consuming bacteria and
small algae to low levels, and the flagellate had further grazing activity on those
food items. Abundance of metazoan predators decreased due to the decrease in
abundance of small algae which was food resource also for the predators. So, it is
likely that Ochromonas takes advantage for bacterivory over heterotrophic protists
under less predation pressure by metazoans. In addition, the formation of deep sub-
surface chlorophyll a maximum was elucidated as accumulation of phytoplankton
which escaped from Ochromonas grazing conducted in epilimnion.
Studies on relative importance of bacterivory between mixotroph and hetero-
trophs after 2000 thus have revealed high grazing pressure on bacteria by mixotro-
phic protists. Further, high grazing activity of those mixotrophs occasionally have
trophic cascade to phytoplankton and zooplankton. So, the ecological importance of
those mixotrophs may be more significant that we evaluated before (Fig. 3.1b).
3.5 Predation on Protists
In freshwaters, studies about predation on flagellates by ciliates, rotifers, cladocer-

ans and copepods (Burns and Schallenberg 2001; Nakano et al. 2001; Yoshida et al.
2001a, b) (Fig. 3.1b) and about predation on ciliates by rotifers, cladocerans and
copepods (Hansen 2000; Adrian et al. 2001; Burns and Schallenberg 2001; Nakano
et al. 2001) are available. However, we still have only limited information about
predation on protists (Sherr and Sherr 2002) even at the present, though this may be
important transfers of organic matter within a food web (Fig. 3.1). This is also the
case for marine waters.
The reason for less availability of studies about predation on protists may be due
to fragility of protistan cells and/or to researchers’ interest in bacteria which are
relatively easy materials for applying molecular biological techniques.
3.6 Biodiversity Researches on Microbial Loop in Lake Biwa
There is a large accumulation of scientific information about Lake Biwa (Kawanabe

and Maehata 2012). In the pelagic area of the lake, planktonic food web is important
matter cycling. We already have excellent publications on long term changes in
abundance and species composition of phytoplankton (Hsieh et al. 2010; Tsujimura
and Ichise 2012) and zooplankton (Miura and Cai 1990; Tsugeki et al. 2003;
Kawabata 2012). Plenty of ecological researches on phytoplankton (Nakanishi et al.

1992a; Tezuka and Nakano 1993; Miyajima et al. 1994, 1995; Nakano et al. 1996)
and zooplankton (Kawabata 1987a, b, 1989, 1991, 1993, 1995) are also available.
Food web dynamics in the herbivorous food chain is also well documented
(Nakanishi et al. 1992b; Kawabata and Nakanishi 1996).
In the present review, I would like to introduce research development on micro-
bial loop in Lake Biwa.
A driving power of microbial loop is DOM supply from phytoplankton primary
production, and there are some studies on bacterial utilization of DOM released by
phytoplankton in Lake Biwa (Tanaka et al. 1974, 1975; Ohara et al. 1993). Tanaka
et al. (1974, 1975) found that phytoplankton in Lake Biwa released glycolate as a
major component of released photosynthetic products, and that glycolate-utilizing
bacteria dominated when the glycolate excretion rate of the phytoplankton was
high. Ohara et al. (1993) reported that dominant phytoplankton species partly deter-
mined the dominant bacterial populations in the lake, through release of DOM.
From the point of view of biodiversity researches on microbial loop, those three
studies may be pioneer studies in Lake Biwa.
Food chain interactions, together with matter cycling within a food chain, have
been intensively studied on microbial loop in freshwater and marine systems. A pio-
neer and representative work on microbial loop in Lake Biwa is Nagata (1988), and
his work was followed by some functional studies such as nutrient regeneration
through microbial loop (Nakano 1994) and top-down/bottom-up control on bacterial
abundance (Gurung and Urabe 1999; Gurung et al. 2000). Those three studies paid
special attention to phosphorus cycling through microbial loop, because Lake Biwa is
a severely P limited lake. For biodiversity in microbial loop in Lake Biwa, there are
some studies by Nagata and his colleagues. Nishimura et al. (2005) examined three
types of ecology among bacteria with very high nucleic acid contents, bacteria with
high nucleic acid contents, and bacteria with low nucleic acid contents, suggesting
that P limitation exerts relatively severe constraints on the growth of bacterial groups
with higher nucleic acid contents, which allows bacteria with low nucleic acid con-
tents to be competitive and become an important component of the microbial loop.
Using FISH, Nishimura and Nagata (2007) also found dominance by α-proteobacteria
in the epilimnion of Lake Biwa. Since many previous studies have reported that a
dominant phylogenetic group in lakes is β-proteobacteria (Glöckner et al. 1999),
Nishimura and Nagata (2007) provide unique information about bacterial diversity in
Lake Biwa. Okazaki et al. (2013) also used FISH and found that a predominant bacte-
rial phylogenetic group in the oxygenated hypolimnion of Lake Biwa affiliated with
the CL500-11 cluster (phylum Chloroflexi) which may be a potentially important
component of the pelagic biogeochemical cycling in the lake.
We still have only limited information about ecological roles of viruses in micro-
bial loop in Lake Biwa (Honjo et al. 2007; Pradeep Ram et al. 2010). Pradeep Ram
et al. (2010) reported high bacterial loss to viral infection in the epilimnion and
moderate in the hypolimnion. This result to some extent contradicts to those of other
studies (Weinbauer and Höfle 1998; Bettarel et al. 2004; Colombet et al. 2006), and
we have to collect more information about loss of bacteria due to virus infection in
Lake Biwa.
3.7 Concluding Remarks 61
Our information about ecological roles of protists in microbial loop in Lake

Biwa is still limited, similar to the case of viruses. The only literature which reports
ciliate diversity in the lake is Yoshida et al. (2001b), and no information about flag-
ellate diversity of the lake is available. The information about grazing on bacteria by
heterotrophic/autotrophic flagellates in Lake Biwa is available (Nakano 1994;
Nakano et al. 1998b; Urabe et al. 2000), but this is not the case for ciliates. In addi-
tion, Yoshida et al. (2001a) is the only publication which reports predation on pro-
tists in Lake Biwa.
Lake Biwa may be the lake where microbial loop studies have been most inten-
sively conducted in Japan. However, even so, there are still many ecological and/or
biodiversity studies which should be conducted in future. Some molecular biologi-
cal techniques such as next-generation sequencing may provide us new and massive
information about microbial diversity in Lake Biwa. It is essential for us microbial
ecologists to use those techniques, because many microorganisms such as bacteria
or small protists have limited morphological characteristics for microscopic identi-
fication. To have more profound understanding on microbial ecology in the lake, we
need to relate biodiversity information derived from those molecular biological
techniques to ecological functions or processes.
3.7 Concluding Remarks
Some authors have so far revised the basic structure of “microbial loop” (Bratbak
et al. 1992; Caron and Finlay 1994; Kerner et al. 2003). Figure 3.1b shows a revised
version of microbial loop after inclusion of all the possible components, though I
have skipped to figure out numerous food linkages within protists. Protists have
several feeding modes such as filter, raptorial, diffusion and cytopharyngeal basket
feedings, and protists probably have web-like food chains. In addition, in freshwater
systems, there is another “loop” so-called “myco-loop” (Kagami et al. 2007). In
myco-loop, large inedible phytoplankton species are infected by fungi, nutrients
within these cells are consumed by parasitic fungi, and some of which in turn are
grazed by zooplankton (Kagami et al. 2007).
There are four advantages when we conduct studies on microbial ecology in
freshwater systems. The first, if we consider lakes, a lake environment is a closed
system. So, we have relatively clear border between a lake and another system.
Also, a lake system is more susceptible to changes in external environments than
marine system.
The second, we can conduct in situ experiments in many freshwater systems. In
those experiments, we have natural condition on experimental systems, taking
appropriate care of them. This is important for ecological researches. Cole et al.
(2006) followed organic matter transfer within a lake food web by daily addition of
bicarbonate labeled with stable isotope carbon. The organic matter supply to the
lake was dominated by terrestrial origin. However, only 2 % of the organic matter
supply reached to zooplankton via microbial loop. Elaborated and precise studies
such as Cole et al. (2006) may be feasible only in lake systems.
The third, lake systems are usually much smaller than marine systems. So, costs
needed for scientific researches in lakes should be smaller than those in marine
systems. In addition, many freshwater systems are easily accessible in terms of
geography and/or economy, and this makes frequent visit possible.
The forth, freshwater systems consist of lentic and lotic ones. In rivers or streams,
there are biofilms on solid surfaces. Biofilms provide unique ecosystems with high
microbial diversity and concentrated microbial biomass, consisted of microalgae,
fungi, bacteria and protists (Fukuda et al. 2004). Only limited studies have so far
been conducted for biofilms in lotic environments, and further studies are needed to
elucidate the unique systems.
Freshwater systems are susceptible to human activities, due to high accessibility
relative to other ecosystems. So, studies in freshwater systems are important to elu-
cidate complex interactions within ecosystems and to determine what can be done
for the better management of ecosystems for the sustainable existence of human
beings and other living organisms. We need to have up-to-date, modern, sophisti-
cated and well-organized research system for future human well-being.
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Chapter 4
A Dynamic Resilience Perspective Toward
Integrated Ecosystem Management:
Biodiversity, Landscape, and Climate
Abstract Ecosystems often show sudden and drastic shifts in their states following
relatively small environmental changes, yet the environmental restoration does not
necessarily easily recover the original state. The resilience theory has played a piv-
otal role in ecosystem management by providing a theoretical basis for such abrupt
and irreversible phase transitions (i.e., regime shifts). However, a major concern
remains that the existing theory considers ecosystem responses along only a single
disturbance axis (e.g., eutrophication), despite the fact that natural ecosystems are
subject to multiple anthropogenic disturbances. In this chapter, I introduce ontoge-
netic niche shifts (i.e., changes in resource use or predation vulnerability during
individual growth) as a possible common mechanism of regime shifts. Based on this
framework, I show how additional factors not accounted for the basic resilience
theory (e.g., species extinction and invasion, habitat loss and fragmentation, and
phenological shifts) may affect whether or where regime shifts occur along environ-
mental gradients. I conclude that these results taken together illustrate the impor-
tance of interdisciplinary research integrating biodiversity conservation, landscape
protection, and climate change adaptation for more effective management of lake
ecosystems.
Keywords Alternative stable states • Bistability • Ecosystem disturbance • Ecosystem

restoration • Food-web dynamics • Global change • Positive feedback • Warming
4.1 Introduction
We enjoy various benefits from lake ecosystems such as drinking water, fishery
resources, and opportunities for leisure, sport, and education (Postel and Carpenter
1997). These ecosystem services are a driving force for the development and main-
tenance of human society, as ancient people achieved highly advanced civilization

70 4 A Dynamic Resilience Perspective Toward Integrated Ecosystem Management…
around big rivers such as the Nile River and the Tigris–Euphrates basin. We exploit
the natural resources of lakes, especially large lakes, in which a large amount of
fresh water is available and diverse aquatic species, especially fish, coexist. However,
the human activities around these ecosystems inevitably cause various anthropo-
genic disturbances. In the last several decades, lake-ecosystem services have been
significantly degraded through anthropogenic disturbances such as eutrophication
(Smith et al. 2006; Smith and Schindler 2009), biodiversity degradation (Lovel
1997; Chapin et al. 2000; Sala et al. 2000), and landscape modification (Fahrig
2003; Cushman 2006; Collinge 2009). In addition, climate change creates a serious
global problem for ecosystem services (Lovejoy and Hannah 2005; Hannah 2010;
Kernan et al. 2010). These ecosystem disturbances may reduce water quality, fish-
ery catch, and the cultural value of lakes, thereby potentially preventing sustainable
development of human society.
This is true and important for Lake Biwa and people living around the lake as
well. Lake Biwa has been subject to various ecosystem disturbances during the lat-
ter half of the twentieth century such as eutrophication (Hsieh et al. 2010, 2011),
biological invasion (Nakai 1999), lakeshore development (Nakanish and Sekino
1996), and climate change (Hsieh et al. 2010, 2011). As a result, the ecosystem
services of Lake Biwa (in particular, water supply and fishery) have been seriously
degraded, which is essential for our life and culture (Kawanabe et al. 2012).
Establishing effective ecosystem management is therefore a pressing concern in
ecological research. In this chapter, I will present a novel and widely applicable
perspective for ecosystem management based on the resilience (regime shift) the-
ory, and consider the possibility that it could help improve the ecosystem manage-
ment of lakes including Lake Biwa.
4.2 R
egime Shift and Resilience as Key Concepts
in Ecosystem Management
Monitoring is a pivotal part of ecosystem management. We monitor ecosystems by

assuming that changes in ecosystem states reflect changes in environmental condi-
tions. As such, we expect that we can predict future ecosystem states and prevent
environmental disturbances from becoming serious. However, the relationships
between the ecosystem state and environmental condition are not necessarily linear
(see below). As a result, ecosystems often undergo sudden and rapid shifts follow-
ing relatively small environmental changes. Such abrupt state transitions are gener-
ally called regime shifts (Scheffer et al. 2001; Scheffer and Carpenter 2003; Folke
et al. 2004; Schröder et al. 2005). Understanding the dynamic nature of such eco-
systems is crucial for establishing more effective ecosystem management.
Ecological regime shift is defined as rapid and drastic reorganization of systems
(e.g., ecosystem and community), from one relatively stable state to another, in
response to relatively small environmental changes (Scheffer et al. 2001; Schröder
4.2 Regime Shift and Resilience as Key Concepts in Ecosystem Management 71
Ecosystem states
c3 c1 c2
Environmental conditions
Fig. 4.1 A conceptual diagram of regime shifts. The horizontal and vertical axes represent envi-
ronmental conditions and ecosystem states, respectively. Arrows indicate drastic shifts in ecosys-
tem state in response to small environmental changes. Regime shifts are possible when alternative
stable states exist over a range of environmental conditions, as indicated by shading. Solid and
dotted lines are stable and unstable equilibrium states, respectively
et al. 2005). Figure 4.1 provides a conceptual diagram of regime shift, in which
ecosystem (or community) states are indicated by a nonlinear (S-shaped) curve
plotted against an environmental condition. Along this curve, the solid parts repre-
sent stable ecosystem states, to which the ecosystem can converge. Suppose that the
initial ecosystem state (e.g., water quality) is “high” (i.e., upper solid line) at envi-
ronmental condition c1. Subsequently, the environmental condition changes from c1
to c2 (e.g., due to eutrophication). This environmental shift dramatically changes the
ecosystem state from “high” to “low” levels despite a small environmental altera-
tion. This is a regime shift. More importantly, the environmental thresholds for the
regime shifts from “higher” to “lower” states and from “lower” to “higher” states
may not be the same. This means that the ecosystem state cannot return to the
“high” level even if the environment recovers from c2 to c1 and a return to the “high”
level requires the much larger shift to c3 (which is called hysteresis). In fluctuating
environments, therefore, the occurrence of regime shifts makes it difficult to main-
tain present ecosystem states and to predict future community dynamics. In relation
to these concepts, the capacity of a system to absorb environmental disturbance and
to reorganize itself is called resilience (Gunderson 2000). Regime shits occur in
systems with low resilience. As such, regime shift and resilience are key concepts in
ecosystem management (Folke et al. 2004; Mayer and Rietkerk 2004).
Regime shifts can occur when alternative stable ecosystem or community states
exist over a range of environmental conditions due to positive feedback mechanisms (as
indicated by solid lines in the shading area of Fig. 4.1). Over the last decade, increasing
effort has been devoted to identifying the mechanisms of alternative stable states in
diverse ecosystems in terrestrial, marine, and freshwater environments (reviewed by
Scheffer et al. 2001; Scheffer and Carpenter 2003; Folke et al. 2004; Schröder et al.
2005). In lake ecosystems, for example, researchers have focused on regime shifts
between a macrophyte-dominated clear water phase and a phytoplankton-dominated
turbid water phase along a gradient nutrient loading (Scheffer 1998; Genkai-Kato and
Carpenter 2005). In this case, the positive feedback involves antagonistic interactions
between two producers (macrophytes and phytoplankton) as follows. When phyto-
plankton are dominant, they suppress submerged macrophytes by reducing the light
intensity that is available at the bottom. When macrophytes are dominant, they suppress
phytoplankton by inhibiting the resuspension of organic matter from lake sediments
into the water. This antagonistic relationship leads to the prediction that lake ecosys-
tems will converge to either a macrophyte-dominated or phytoplankton-dominated
state, depending on the initial conditions, and the sudden change in ecosystem state
from a clear to a turbid water phase can occur following eutrophication. In addition,
such regime shifts can result in an alteration of ecosystem functions such as lake pri-
mary productivity (Genkai-Kato et al. 2012). Many other types of alternative stable
states and regime shifts have also been identified in aquatic and terrestrial ecosystems.
Examples of these regimes shifts include shifts between the presence and absence of
piscivorous fish (Jansson et al. 2007; Persson et al. 2007), forest and savanna (Peterson
2002), social concern and indifference for ecosystem management (Suzuki and Iwasa
2009), and many others (see reviews by Scheffer et al. 2001; Scheffer and Carpenter
2003; Folke et al. 2004; Schröder et al. 2005).
4.3 Regime Shifts Mediated by Ontogenetic Niche Shifts
Here, I introduce a recently identified, but very important, mechanism of alternative

stable states. This mechanism is ontogenetic niche shift, that is, the changes in eco-
logical niches, such as resource use and predation vulnerability, during individual
growth. Virtually all multi-cellular organisms on the earth exhibit individual growth
between birth and death and most species experience ontogenetic niche shifts
(Wilbur 1980; Werner and Gilliam 1984). A well-known example of ontogenetic
niche shift is the metamorphosis of amphibians and insects whereby they change
their morphology drastically. However, ontogenetic niche shifts without clear mor-
phological changes are also common in nature (Werner and Gilliam 1984; Nakazawa
and Yamamura 2007; also see Sect. 4.4.2).
Importantly, ontogenetic niche shifts divide a species into distinct groups (e.g.,
stage and size) that allow individuals of the same species to occupy different eco-
logical niches within a community (Nakazawa et al. 2011; Miller and Rudolf 2011).
As a result, ontogenetic niche shifts play an important role in determining commu-
nity structure and dynamics (Nakano and Murakami 2001; Baxter et al. 2005;
Knight et al. 2005). In aquatic ecosystems, for example, the ontogenetic niche shifts
of fish from planktivory to benthivory connect pelagic and benthic trophic pathways
(Persson et al. 1996; Reñones et al. 2002; Xu et al. 2007; Briones et al. 2012), gen-
erally called pelagic-benthic coupling (Schindler and Scheuerell 2002). Several
theoretical studies have recently suggested that ontogenetic niche shifts may
4.3 Regime Shifts Mediated by Ontogenetic Niche Shifts 73
mediate the occurrence of regime shifts by generating alternative stable community

states along environmental gradients.
In one such study, Schreiber and Rudolf (2008) developed a simple one con-
sumer–two resource model that included consumer ontogenetic diet shift, as
follows:
dRJ / dt = rJ (1 R J / K J ) R J a J C J R J (4.1a)

dRA / dt = rA (1 R A / K A )R A a A C A R A (4.1b)

dCJ / dt = b A a A C A R A b J a J C J R J d J C J (4.1c)

dCA /dt = b J a J CJ R J d A CA (4.1d)

In the model, Rh (h = J or A) represents the density of a resource used by either
juveniles (J) or adults (A), and Ch is the density of the consumer at each stage. The
resources exhibit logistic growth and are reduced by either juvenile or adult con-
sumers (Eqs. 4.1a and 4.1b). Resource consumption at the adult stage promotes
reproduction and supports recruitment into the juvenile stage (Eq. 4.1c). Likewise,
resource consumption at the juvenile stage promotes maturation and supports
recruitment into the adult stage (Eq. 4.1d). The juveniles are lost by maturation and
natural mortality (Eq. 4.1c), whereas the adults are lost only by natural mortality
(Eq. 4.1d). The parameters are defined as follows: rh intrinsic growth rate, Kh carry-
ing capacity, ah resource consumption rate, bh energy conversion efficiency, and dh
death rate. Using this model, Schreiber and Rudolf (2008) illustrated how ontoge-
netic shifts can result in alternative stable community states and how the system can
undergo regime shifts in response to environmental changes (left panel of Fig. 4.2).
Regime shifts in this model result from the positive feedback caused by the apparent
competition-like interactions between the juvenile and adult resources. Suppose
that the resource that the juveniles use becomes more abundant, promoting matura-
tion. In this case, the resource used by the adults is affected negatively through
consumption by the increased density of adults. The decrease in the adult resource,
in turn, leads to a decrease in reproduction and an increase in the juvenile resource,
as the density of juveniles decreases. This results in positive feedback and the sys-
tem converges to either juvenile- or adult-dominated states, depending on the initial
conditions. In this system, therefore, a sudden and drastic shift in population stage-
structure and community structure can occur following changes in environmental
conditions such as resource carrying capacity or consumer death rate.
Guill (2009) also explored a one-consumer–two-resource model containing a
consumer’s ontogenetic niche diet shift. His model is conceptually similar to that of
Schreiber and Rudolf (2008). One major difference of his model is that it is based
on biomass dynamics while Schreiber and Rudolf (2008) based their model on the
dynamics of population abundance. As such, Guill (2009) assumed that if the
resource is not sufficiently available, the body mass of the consumer may decrease
or the consumer may cease to reproduce because of the associated metabolic costs.
Removing P Adding P
a predator a predator
CJ CA CJ CA CJ CA
RJ RA RJ RA RJ RA
Juvenile abundance CJ
10
8
6
4
2
0
0 20 40 60 80 100 0 20 40 60 80 100 0 20 40 60 80 100
Productivity at adult habitat KA
Fig. 4.2 Effects of food-web topology on the occurrence of regime shifts. The upper panels show
topologies of food webs where the juveniles and adults feed on different resources and the juve-
niles have (left) no predators, (center) a predator, and (right) an intermediate predator that is
attacked by a top predator. Arrows indicate inter-stage flow due to maturation or reproduction. The
lower panels show juvenile equilibrium densities along an environmental gradient (here, adult
habitat productivity) corresponding to the upper panels. The solid and dotted lines represent the
stable and unstable equilibrium densities, respectively. A regime shift can occur in the left and
right scenarios. Parameter values are: KJ = 7.5, rh = 1, ah = 0.1, bh = 0.5, and dh = 0.1 (h = J, A, P, or Q).
The model formulations and parameter definitions are given in the text
Using numerical simulations, Guill 2009 showed that this system could also result
in alternative stable community states. The model by Guill (2009) behaves similarly
to that by Schreiber and Rudolf (2008), despite their different assumptions. This
implies that the occurrence of regime shifts seems to be robust to the system in
which a species exhibit ontogenetic niche shifts.
Ontogenetic niche shifts occur not only through changes in resource use, but also
through changes in predation vulnerability. de Roos et al. (2008) explored a math-
ematical model describing the ontogenetic predator shifts of a prey species. In this
model, they assumed that the juvenile and adult prey share a common resource, but
are attacked by different predator species. Counterintuitively, their results showed
that one predator might not be able to persist unless the other predator is also pres-
ent, suggesting emergent facilitation between apparently antagonistic predators
feeding on conspecific prey of different sizes. This model prediction indicates that
ontogenetic predator shifts may generate alternative stable states between the coex-
istence and extinction of the two predators. de Roos et al. (2008) explained the
between-predator facilitation through asymmetric increases in the rate of prey mat-
uration and reproduction when predation relaxes competition among the prey for
their shared resource. Suppose that the predator of the juveniles becomes more
abundant (e.g., due to decreasing mortality). This suppresses the juvenile abun-
dance, but at moderate levels, it may promote the maturation rate of the surviving
4.4 Effects of Ecological Contexts on the Occurrence of Regime Shifts Mediated… 75
juveniles because of food-dependent individual growth. The increased maturation

rate may positively affect the predator of the adults (also see de Roos et al. 2007).
Similarly, moderate predation of the adults may promote reproduction among the
surviving individuals, thereby positively affecting the predator of the juveniles. de
Roos et al. (2008) further showed that the emergent facilitation between stage-
specific predators is also possible when a shared prey species has more than two
stages.
These theoretical models all assume that environmental conditions (e.g., resource
availability and mortality risk) at one life stage strongly affect the performance of
other stages via density-dependent effects; for example, higher maturation rates
intensify resource competition at the adult stage and reduce the per-capita reproduc-
tion rate. This implies that alternative stable states may not exist when maturation
or reproduction are density-independent (McCoy et al. 2009) or are governed by
other rules (de Roos et al. 2002; Takimoto 2003; Nakazawa and Yamamura 2007).
To test the key assumption, empirical studies have recently examined to what extent
stage-specific performance is density-dependent (Walter and Kiutchell 2001;
Ohlberger et al. 2012; also see reviews by Abrams 2009; Vincenzi et al. 2012). On
the other hand, direct tests of model predictions are rather difficult because they
require long-term data on community dynamics. Even so, the occurrence of regime
shifts mediated by ontogenetic niche shifts is expected to be widespread in nature
because ontogenetic niche shifts are ubiquitous among organisms (Wilbur 1980;
Werner and Gilliam 1984). Notably, Persson et al. (2007) have recently illustrated,
via whole-lake manipulations, that a reduction in the density of large prey individu-
als caused an increase in the abundance of small individuals, allowing their predator
(piscivores) to recover. They explained that the underlying mechanism would be the
prey’s ontogenetic shift in predation vulnerability. The results of Persson et al.
(2007) suggest that the presence and absence of the piscivores could be alternative
stable states in natural environments.
4.4 E
ffects of Ecological Contexts on the Occurrence
of Regime Shifts Mediated by Ontogenetic Niche Shifts
The occurrence of regime shifts that are mediated by ontogenetic niche shifts seems
to be intrinsic to the dynamics of size/stage-structured (i.e. almost all) ecological
communities. Although this has significant implications for ecosystem management
(see Sect. 4.2), many questions remain. In particular, it is important to determine
whether regime shifts always occur in size-structured communities, and if not,
under what conditions they occur. Ontogenetic niche shifts may not necessarily
generate alternative stable states in the presence of additional factors that diminish
or eliminate their effects. I explain below how the occurrence of regime shifts that
are mediated by ontogenetic niche shifts are altered in complex ecosystems. I focus
on three factors: (i) food-web topology, (ii) spatial configuration, and (iii)
seasonality. The reason that I focused on these factors is not only that real food webs
are much more complex than assumed in the simple models described above. At
present, both aquatic and terrestrial ecosystems are under various anthropogenic
disturbances such as biodiversity degradation due to species extinction and invasion
(Lovel 1997; Chapin et al. 2000; Sala et al. 2000), habitat loss and fragmentation
due to landscape modification (Fahrig 2003; Cushman 2006; Collinge 2009), and
phenological shifts due to climate change (Lovejoy and Hannah 2005; Hannah
2010; Kernan et al. 2010). Understanding the conditions that cause regime shifts in
various ecological contexts (i.e., species composition and their relationships in
space and time), will lead to a better understanding of how ecosystem resilience
varies with anthropogenic disturbance.
4.4.1 Food-Web Topology
In this section, I examine how regime shifts mediated by ontogenetic niche shifts
can be altered by changes in food-web topology. First, suppose that juveniles and
adults are both primary consumers feeding on different resources and only the juve-
niles are attacked by a predator species (Nakazawa 2011a). The dynamics of this
system are described as follows:
dRJ / dt = rJ (1 R J / K J )R J a J CJ R J (4.2a)

dRA / dt = rA (1 R A / K A )R A a A C A R A (4.2b)

dCJ / dt = b A a A C A R A b J a J C J R J d J C J a P C J P (4.2c)

dCA / dt = b J a J CJ R J d A CA (4.2d)

dP / dt = b P a P C J P d P P (4.2e)
In the model, the predator P increases by feeding on the juveniles and decreases due
to natural mortality (Eq. 4.2e). The parameters aP, bP, and dP are the attack rate, energy
conversion efficiency, and death rate. The other model variables and parameters are the
same as in the model by Schreiber and Rudolf (2008) (see above). This system has
only one stable equilibrium, where CJ* = dP/bPaP and CA* = KJbJaJdP(rJbPaP ‐ aJdP)/rJb-
P aP dA (center panel of Fig. 4.2). Given that alternative stable states can exist in the
2 2
absence of the predator (left panel of Fig. 4.2; see also Schreiber and Rudolf 2008),
this result indicates that stage-specific predation suppresses alternative stable states
and prevents regime shifts after environmental changes. This can be explained intui-
tively as follows: The introduced predator P relaxes resource competition among juve-
niles by controlling juvenile abundance. This breaks down the positive feedback
caused by the apparent competition-like interactions between the resources at the juve-
nile and adult stages.
When another species is added as a new top predator feeding on predator P, the
model is modified as follows:
dRJ / dt = rJ (1－R J / K J ) R J － a J CJ R J (4.3a)

dRA / dt = rA ( 1 －R A / K A ) − a A CA R A (4.3b)

dCJ / dt = b A a A C A R A － b J a J CJ R J － d J CJ － a P CJ P (4.3c)

dCA / dt = b J a J CJ R J － d A C A (4.3d)

dP / dt = b P a P CJ P － d P P － a Q PQ (4.3e)

dQ / dt = b Q a Q PQ − d Q Q (4.3f)

The variable Q represents the abundance of the newly added predator. The
parameters aQ, bQ, and dQ are the attack rate, energy conversion efficiency, and death
rate, respectively, of predator Q. This model predicts that the system recovers the
potential for alternative stable states (right panel of Fig. 4.2; see Nakazawa 2011a
for analysis). This is because the new top predator Q controls intermediate predator
P abundance and cancels the suppression of alternative stable states caused by pred-
ator P. The same qualitative result is obtained when the presence of predators is
manipulated at the adult stage or at both juvenile and adult stages (Nakazawa
2011a). This means that regime shifts can occur if either of the following two condi-
tions is satisfied for both juveniles and adults: they are top predators (left panel of
Fig. 4.2), or they are consumed by an intermediate predator that is attacked by a top
predator (right panel of Fig. 4.2). Notably, juvenile and adult trophic levels do not
affect the results (Nakazawa 2011a). Therefore, top-down regulation by predators
critically affects the potential for regime shifts. On the other hand, the bottom-up
effects of resource availability (e.g., stage-specific resource productivity and trophic
levels) alters the likelihood that a system will be in a particular alternative stable
state (i.e., the parameter space) when regime shifts are possible; however, bottom-
up effects do not affect whether regime shifts can occur (Nakazawa 2011a).
The potential for alternative stable states in systems wherein juveniles and adults
are generalist consumers can be explored by manipulating the number of alternative
resources that are available at each life-stage (Nakazawa 2011b). A one-consumer
n-resource system without predators is the simplest case, and can be modeled as:
dRJ , i / dt = rJ , i (1－ R J , i / K J , i )R J , i － a J , i CJ , i R J , i (4.4a)

dRA , i / dt = rA , i (1－ R A , i / K A , i ) R A , i － a A , i C A , i R A , i (4.4b)

( ) ( )
dCJ / dt = ∑ b A , i a A , i R A , i CA －∑ b J ,i a J , i R J , i C J － d J , i CJ , i

(4.4c)

( )
dCA / dt = ∑ b J , i a J , i R J , i CJ － d A , i CA , i

(4.4d)
In this model, i (i = 1 to nh) denotes the ith resource of the juveniles or adults and
nh (h = J or A) is the number of resources used by the juveniles or adults. Analysis
of the model showed that the relative balance of total resource availability is crucial
for the development of alternative stable states. This is probably because the relative
balance of maturation and reproduction flow allows for the development of the posi-
tive feedback that is caused by apparent competition-like interactions between the
juvenile and adult resources (see above). The same qualitative results are obtained
when the juveniles or adults utilize allochthonous subsidies from outside the system
(Nakazawa 2011b).
The results of the models in this section indicate that food-web topology is a
key determinant of the regime shift occurrence. Anthropogenic changes in species
composition, due to extinction and invasion, may cause or prevent regime shifts
by altering the resilience of ecosystems and communities to environmental pertur-
bations. For example, regime shifts may become more likely when a native top
predator goes extinct (from center to left panels of Fig. 4.2) or when a predator is
introduced and feeds on the native top predator (from center to right panels of
Fig. 4.2). While this is an oversimplification of real-life situations, it is sufficient
to illustrate the point.
4.4.2 Spatial Configuration
In the field of spatial ecology, researchers have increasingly recognized that spa-
tially distinct food webs are frequently connected by the movement of organisms
and that local food-web dynamics are tightly regulated by biotic and abiotic con-
ditions within distinct habitats. This idea has been considered from a variety of
perspectives, including meta-community (Holyoak et al. 2005), spatial subsidy
and cross-ecosystem linkage (Polis et al. 2004, food web theory (Rooney et al.
2006), and meta-ecosystem perspectives (Loreau et al. 2003). Even though onto-
genetic food-web coupling is fairly common in nature, ontogenetic niche shifts
have rarely been considered by spatial ecologists as a major factor coupling dis-
tinct food webs. As a well-known example, aquatic insect and amphibian meta-
morphosis couples aquatic and terrestrial food webs (Nakano and Murakami
2001; Baxter et al. 2005; Knight et al. 2005). In addition, the so-called breeding
migration that has been observed in a variety of animal taxa couples the spatially
distinct food webs that are in feeding and breeding grounds (see reviews in
Nakazawa and Yamamura 2007). Ontogenetic food-web coupling is widely
observed on a smaller scale within localized areas. For example, many fish species
switch from planktivory to benthivory as they grow, coupling the pelagic and lit-
toral food webs of aquatic ecosystems (Persson et al. 1996; Reñones et al. 2002;
Xu et al. 2007; Briones et al. 2012).
The development of alternative stable states in meta-community dynamics driven

by ontogenetic niche shifts can also be explored through modeling (Nakazawa
2011b). Suppose here that both juveniles and adults are primary consumers and they
have multiple stage-specific habitats, in which they exploit different resources. For
simplicity, assume that the habitat colonization processes are random and the juve-
niles and adults do not move among stage-specific habitats. The dynamics of this
system are described as follows:
dRJ , i / dt = rJ , i (1 －R J , i / K J , i)R J , i － a J , i CJ , i R J , i (4.5a)

dRA , i / dt = rA , i (1 − R A , i / K A , i )R A , i － a A , i C A , i R A , i (4.5b)

( )
dCJ , i / dt = (1 / n J ) ∑ b A , i a A , i C A , i R A , i － b J , i a J , i C J , i R J , i － d J , i CJ , i

(4.5c)

( )
dCA , i / dt = (1 / n A ) ∑ b J , i a J , i CJ , i R J , i d A , i CA , i

(4.5d)
In the model, i (i = 1 to nh) denotes the ith habitat of the juveniles or adults and nh
(h = J or A) is the number of habitats used by the juveniles or adults. Definitions of
the other variables and parameters are the same as in the models presented previ-
ously. The juveniles and adults are recruited into each stage-specific habitat at the
rate of (1/nh) ∑ (bh,iah,iCh,iRh,i) (i.e., the total reproduction or maturation production
divided by the stage-specific habitat number).
First, consider the simple situation in which parameter values are identical in all
juvenile or adult habitats (i.e., rh,i = rh, Kh,i = Kh, ah,i = ah, bh,i = bh and dh,i = dh). Under
these conditions, Rh,i* = Rh*and Ch,i* = Ch*, which allows rigorous mathematical
analysis (see Nakazawa 2011b for details). The model predicts that alternative sta-
ble states exist (i.e., regime shifts can occur) when the number of juvenile and adult
habitats are comparable. This condition is consistent with the argument outlined
above that the relative balance of the total resource availability in the juvenile and
adult habitats is essential for the development of alternative stable states. This also
suggest that if maturation rate surpasses reproduction rate (e.g., due to higher pro-
ductivity in juvenile habitats than in adult habitats), then an alternative stable state
could exist when there are fewer juvenile habitats than adult habitats. In reality, of
course, it is not easy to rigorously count the number of stage-specific habitats or to
fully characterize the habitat properties that determine maturation and reproduction
rates. Nevertheless, these results clearly indicate that spatial configuration such as
habitat area and connectivity critically affect the occurrence of regime shifts.
On the basis of these predictions, I emphasize that changes in spatial configura-
tion due to habitat loss or fragmentation may critically affect the occurrence of
regime shifts. Suppose that both juvenile and adult stages have two habitats in the
initial spatial configuration (i.e., nh = 2), alternative stable states exist over a certain
range of environmental conditions, and regime shifts can occur through changes in
adult habitat productivity (center panel of Fig. 4.3). However, regime shifts are pre-
vented when a juvenile habitat is lost (left panel of Fig. 4.3). This can be explained
CJ,2 CA,2
CJ,1 CA,1
RJ,2
RA,2
RJ,1
RA,1
Juvenile Adult
habitats habitats
Juvenile habitat loss Adult habitat loss
Juvenile abundance CJ*
10
8
6
4
2
0
0 20 40 60 80 100 0 20 40 60 80 100 0 20 40 60 80 100
Fig. 4.3 Effects of spatial configuration on the occurrence of regime shifts. The upper panels
show spatial structures where the juveniles and adults can have multiple (here two) habitats. In the
center panel, both stages have two habitats. In the left and right panels, only the juvenile and
adults, respectively, have two habitats, while the other stage has a single habitat. Arrows indicate
inter-stage flow due to maturation or reproduction. The lower panels show juvenile equilibrium
densities along an environmental gradient (here, adult habitat productivity) corresponding to the
upper panels. Stage-specific parameters are identical in the two juvenile or adult habitats. The
solid and dotted lines represent stable and unstable equilibrium densities, respectively. A regime
shift can occur in the center and right scenarios. Parameter values are: KJ,i = 7.5, rh,i = 1, ah,i = 0.1,
bh,i = 0.5, dh,i = 0.1, and nh = 1 or 2 (h = J or A and i = 1 or 2). The model formulations and parameter
definitions are given in the text
as follows. The existence of alternative stable states requires that the relative bal-
ance of total resource availability for juveniles and adults is maintained. Therefore,
if alternative stable states are to exist, adult habitats must have low productivity
when juvenile have fewer habitats than adults; however, the consumer population
cannot be supported under such poor conditions. In contrast, alternative stable states
exist for a much wider range of adult habitat productivity when an adult habitat is
lost (right panel of Fig. 4.3). This is because the relative balance of the total resource
availability at the juvenile and adult stages is more likely to be maintained when
adult habitat productivity is increased. This does not necessarily indicate that regime
shifts are very likely (right panel of Fig. 4.3), because the equilibrium state is
unlikely to reach the environmental threshold for regime shift. However, the devel-
opment of alternative stable states implies that significant population disturbances
(i.e., changes in juvenile-adult stage distribution) may cause a drastic shift of the
community state from one stable state to another, and subsequently, the system may
become unable to return to the initial community state.
When environmental conditions are heterogeneous in space, as when some habi-
tats are relatively productive while others are not, mathematical analysis is quite
difficult. However, preliminarily numerical simulations show that multiple (i.e.,

more than two) stable states can exist in spatially heterogeneous environments
(Nakazawa 2011b). Assume that both juveniles and adults have two habitats (i.e.,
nh = 2) and the productivities of the two juvenile habitats (i.e., KJ,1 and KJ,2) are dif-
ferent. Under these conditions, at least three alternative stable states are found for
some parameter settings (Nakazawa 2011b). One of these stable states is an adult-
dominated state, and the other two are juvenile-dominated states, in which juvenile
abundance is dominated by either of the two subpopulations. This result suggests
that understanding spatial community dynamics is much more difficult than we
have supposed and it may be impossible without sufficiently detailed information
regarding the initial spatial distribution of species. This idea is apparently consistent
with the notion of historical contingency of community assembly, which states that
equilibrium community structure is governed by initial conditions and stochastic
processes (Law 1999; Fukami 2004; but see Fukami and Nakajima 2011). The
model results also indicate that juvenile abundance can be higher in the less produc-
tive habitat than in the more productive habitat (Nakazawa 2011b). This pattern is
produced by a source-sink relationship among stage-specific habitats; that is, the
more productive juvenile habitat can support the juvenile subpopulation in the less
productive habitat through facilitation of maturation. The existence of multiple sta-
ble states suggests that mismatches between local environmental conditions and
local community structure are possible, that the source-sink relationships depend on
the initial conditions, and that these relationships may suddenly collapse (i.e.,
regime shifts occur) following environmental change. These predictions are still
preliminary but potentially quite important for ecosystem management in space.
Future work is needed to more fully elucidate how the regime shifts are influenced
by changes in spatial configuration and local environmental conditions.
4.4.3 Seasonality
Phenology, the timing of life-history events such as breeding and migration, is cru-
cial for population dynamics. The importance of phenology in population dynamics
is illustrated by the match/mismatch hypothesis. This hypothesis states that if the
most energy-expensive period of the consumer’s reproductive phenology is close to
the peak period of the resource availability, then recruitment of the consumer will
be high (Cushing 1990). This is becoming a key concept in seasonal community
dynamics (Nakazawa and Doi 2012). This idea can also be applied to a stage-
structured system. Assume that juveniles and adults are primary consumers and
they change their maturation or reproduction efficiencies seasonally, as follows:
dRJ / dt = rJ (1 R J / K J ) R J a J CJ R J (4.6a)

dRA / dt = rA (1 R A / K A )R A a A CA R A (4.6b)

dCJ / dt = p A ( t ) b A a A C A R A p J ( t ) b J a J C J R J d J C J (4.6c)

dCA / dt = p J ( t ) b J a J CJ R J d A CA (4.6d)

In the model, the time-varying function ph(t) (h = J or A) represents the phenol-
ogy of maturation or reproduction. Note that the phenology in the model indicates
seasonal variations in behavioral efficiency or activity that are governed by environ-
mental cues (e.g., temperature and precipitation), rather than by resource consump-
tion. The functional form of ph(t) is determined by empirical data or specific
assumptions. For simplicity, and as is common in the literature (Namba 1984;
Abrams 2004; Nakazawa and Doi 2012), I opt here for sinusoidal functions, ph(t) =
1 + uhsin{2π(t ‐ vh)/T}, where T, uh, and vh represent seasonal period, amplitude, and
peak timing of maturtion or reproduction, respectively.
Using the model, numerical simulations of long-term (i.e., over many seasonal
cycles) average community states were performed with initial population abun-
dances of Rh = 1 and Ch = 1. When the model is run along a gradient of adult habitat
productivity (KA) for differing degrees of phenological mismatch between matura-
tion and reproduction (i.e., vJ − vA), the results show that a regime shift-like transi-
tion occurs around KA = 15 when vJ − vA = 0 and that the severity or threshold of the
shift varied with changes in the maturation-reproduction phenological mismatch
(Fig. 4.4a). When the long-term average abundances of both juveniles and adults
along a gradient of maturation-reproduction phenological mismatches are evalu-
ated, the results show that juvenile and adult abundances are highly variable,
depending on maturation and reproduction phenology. Most notably, the stage dis-
tribution may suddenly and drastically shift when maturation–reproduction pheno-
logical mismatch changes (Fig. 4.4b). Detecting regime shifts in scenarios like this
is difficult because the system undergoes seasonal (i.e., ever-fluctuating) changes,
making equilibrium states impossible to evaluate. Nevertheless, the above results
clearly indicate that long-term community dynamics may change drastically with
match/mismatch of maturation and reproduction phenology.
Climate change has altered individual growth rates and, as a result, the timing of
ontogenetic niche shifts (Post et al. 2008; Seebens et al. 2009; Ozgul et al. 2010;
Yang and Rudolf 2010) and reproduction (Beebee 1995; Crick et al. 1997; Taylor
2007). Therefore, climate change-indued phenological shifts may also alter the
resilience of communities. However, it is still not clear how climate change advances
or delays species-specific and trait-specific phenology. This is because life-history
parameters are bioenergetically related to one another and climate change regulates
multiple life-history traits in complex ways (Ozgul et al. 2010). Accumulating phe-
nology data is necessary in order to better understand the occurrence of regime
shifts in seasonal community dynamics and to more accurately predict their
responses to climate change.
a b
10 vJ - vA = -2T/5
4
CJ CA
0 3
10 vJ - vA = -T/5
2
Population abundance
0 CJ
1
10 vJ - vA = 0
0 -150 -100 -50 0 50 100 150

10 vJ - vA = T/5 Phenological mismatch between
maturation and reproduction vJ-vA
0
10 vJ - vA = 2T/5
0
0 10 20 30 40 50 60
Fig. 4.4 Effects of seasonality on long-term average consumer abundance. Arrows roughly indi-
cate the threshold for regime shifts. In panel (a), the juvenile abundances are plotted along an
environmental gradient (here, adult habitat productivity) for different levels of maturation-
reproduction phenological mismatch (vJ – vA = − 2/5, −T/5, 0, T/5, and 2T/5 from upper to lower
panels, respectively). In panel (b), the gray and black lines represent the juvenile and adult abun-
dances, respectively, against maturation-reproduction phenological mismatch. Parameter values
are: KJ = 15, rh = 1, ah = 0.1, bh = 0.5, dh = 0.1, uh = 1, and T = 365 (h = J or A). In the panel (b), KA = 15.
For all simulations, the initial population abundances are: Rh = 1 and Ch = 1. The model formula-
tions and parameter definitions are given in the text
4.4.4 Other Factors
Finally I present two additional scenarios for model extension: (i) inter-stage resource
sharing and (ii) nonlinearity of trophic interactions. These scenarios are closely
related to food-web topology and spatial configuration. First, suppose that juveniles
and adults are able to utilize the major resource of the other stage. The stage-speci-
ficity of resource utilization is determined not only by stage-specific resource prefer-
ence but also by stage-dependent foraging ability. For example, adults (with possibly
high mobility) may be better able to search for resources in a large area, while juve-
niles may exploit resources in a localized area. In this case, the juveniles have to
share the resource with the adults, but not vice versa. A similar situation occurs
when an ontogenetic niche shift is triggered by growth in body size. For example,
adult fish can exploit not only benthic (i.e., large) but also planktonic (i.e., small)
prey while juvenile fish feed mainly on small planktonic prey because of gape-
limited predation (Persson et al. 1996; Reñones et al. 2002; Xu et al. 2007;
Briones et al. 2012). This example may be categorized as ontogenetic niche expan-
sion. I developed a one-consumer two-resource model with inter-stage resource shar-
ing as follows:
dRJ / dt = rJ (1 R J / K J )R J a J , J CJ R J a A , J CA R J (4.7a)

dRA / dt = rA (1 R A / K A )R A a J , A CJ R A a A , A CA R A (4.7b)

( ) ( )
dCJ / dt = b A , J a A , J R J + b A , A a A , A R A CA b J , J a J , J R J + b J , A a J , A R A CJ d J , i CJ , i

(4.7c)

( )
dCA / dt = b J , J a J , J R J + b J , A a J , A R A CJ d A , i CA , i

(4.7d)
where aJ,A and aA,J determine the rates at which juveniles or adults consume the
resource of the other stage. Analysis of the model shows that alternative stable
states are generally suppressed as these parameters increase in value (Nakazawa
2011b); that is, inter-stage resource sharing suppresses the occurrence of regime
shifts. This result can be explained as follows: If the adults exploit the juvenile
resource with high efficiency, thereby regulating the amount of the juvenile resource,
then it can interrupt the positive feedback caused by apparent competition-like
interactions between juvenile and adult resources.
The nonlinearity of trophic interactions is also crucial for understanding the
occurrence of regime shifts. Schreiber and Rudolf (2008) showed through numeri-
cal simulations that regime shifts are generally smoothed or prevented when the
juveniles or adults have a long handling time (i.e., Holling type-II functional
responses) in the simplest one-consumer-two resource system (model 1). Similar
patterns are observed when there is strong interference competition within stages
(Nakazawa 2011a). This is because low food-dependent maturation or reproduction
interrupts the positive feedback that is necessary for the development of alternative
stable states. Other species (e.g., predators) may also have nonlinear functional
responses that have significant effects on the occurrence of regime shifts. Suppose
that juveniles have a top predator with a nonlinear functional response. Nakazawa
(2011a) showed that, in contrast to systems with linear functional responses of pred-
ators (center panel of Fig. 4.2), alternative stable states can exist when the predator
exhibits strong interference competition. This is because interference competition
controls prey (i.e., the juveniles) in a density-dependent manner similar to the con-
trol exerted when a new top predator attacks the predator (right panel of Fig. 4.2).
On the other hand, regime shifts remain impossible when the predator has a Holling
type-II functional response (Nakazawa 2011a). These results suggest that the non-
linearity of trophic interactions may either cause or prevent the occurrence of regime
shifts, depending on the basic food-web configuration.
4.5 Toward Integrated Ecosystem Management 85
4.5 Toward Integrated Ecosystem Management
4.5.1 From Static to Dynamic Resilience Perspectives
The occurrence of regime shifts that are mediated by ontogenetic niche shifts can be
significantly altered by various factors, such as food-web topology, spatial configu-
ration, and seasonality. These results shed light on our understanding of regime
shifts in complex ecosystems. At the same time, they open new avenues for future
research and for establishing more effective ecosystem management based on resil-
ience theory. What is the most important is to more accurately evaluate ecological
contexts (i.e., species compositions and their relationships in space and time) to
understand the occurrence of regime shifts. This information will allow us to under-
stand long-term community dynamics and ecosystem responses to disturbances.
This idea is straightforward, but has not been established by empirical research on
regime shifts and ecosystem management. This is because ecosystem disturbances
(e.g., biodiversity degradation, landscape modification, and phenological shift) and
regime shift (or resilience) have conventionally been studied independently of one
another in ecosystem management research (Peterson et al. 1998; Awiti 2011). In
particular, the primary concern in the previous study of regime shifts has been the
determination of the point at which regime shifts occur along environmental gradi-
ents (e.g., nutrient loading) and how to predict them (Andersen et al. 2009). These
attempts implicitly assume that ecological contexts are invariant. The only excep-
tions, to my knowledge, are the work of Genkai-Kato and Carpenter (2005) and
Genkai-Kato (2007). These researchers studied how regime shifts in shallow eutro-
phic lakes would be altered by changes in the relative pelagic-to-littoral habitat area
and the associated presence of macrophytes or piscivores, respectively. Genkai-
Kato and Carpenter (2005) argued that the resilience is determined by lake size and
morphology, but their results can be used to suggest that resilience may be altered
by lakeshore development through decreases in macrophyte-dominated littoral area.
Genkai-Kato (2007) incorporated the effects of macrophytes and piscivores by
manipulating parameter values associated with zooplankton grazing rate or plankti-
vore death rate, although he did not explicitly describe their population dynamics.
Despite these studies, however, regime shifts in complex ecosystems remain poorly
understood. More detailed studies on regime shift and resilience should be taken
into account in future, and even past, studies of regime shift and resilience.
The resilience of ecosystems is determined by ecological contexts. This implies
that changes in ecological context due to anthropogenic disturbances may affect
whether or where regime shifts occur along environmental gradients. Recognizing
the importance of the novel concept, here I wish to propose “dynamic resilience
perspective,” in contrast to the conventional view that ecological resilience is
defined in constant ecological contexts (Gunderson 2000). This concept is quite
important in ecosystem management because of current various ecosystem distur-
bances. Acceleration of biodiversity loss and biological invasion are serious con-
cerns all over the world (Lovel 1997; Chapin et al. 2000; Sala et al. 2000). Apex
predatory species are especially vulnerable to extinction (Myers and Worm 2003;
Prugh et al. 2009), while invasive predators frequently occupy the top-predator
niche, exploiting the resident prey community (Eby et al. 2006). In addition, habitat
loss and fragmentation due to landscape modification (Fahrig 2003; Cushman 2006;
Collinge 2009) and phenological shifts due to climate change (Lovejoy and Hannah
2005; Hannah 2010; Kernan et al. 2010) are increasingly serious worldwide.
Theoretical predictions based on the dynamic resilience perspective suggest that
these anthropogenic ecosystem disturbances may modify the community dynamics
and spatial distribution of species in ways that are not yet fully understood. An
emerging concern is that these disturbances may together create a negative spiral,
whereby ecosystem disturbances make ecological communities more susceptible to
environmental change-induced regime shifts and regime shifts make ecosystems
more vulnerable to human disturbance. In order to avoid such a resilience melt-
down, we should be more aware of the causal linkages between ecological context
and ecosystem resilience, conventionally studied independently. One may think that
it is virtually impossible to completely describe the real world, and that such
attempts are not promising. Although it is certainly challenging, one possibility may
stem from the fact that there are the general rules governing the occurrence of
regime shifts that are mediated by ontogenetic niche shifts. These rules describe the
ways in which top-down regulation by predators and bottom-up regulation by
resources control the positive feedback that is necessary for the development of
alternative stable states (Nakazawa 2011a, b). We may be able to predict the occur-
rence of regime shifts in complex ecosystems by determining the extent to which
basic mechanisms that underlie alternative stable states are density-dependent and
how they interact with other factors and processes. In this chapter, I have focused on
ontogenetic niche shifts as generators of alternative stable states. However, the same
arguments apply to regime shifts caused by other mechanisms and are therefore
generally applicable to ecosystem management.
4.5.2 Implications for Lake Ecosystem Management
The occurrence of regime shifts that are mediated by ontogenetic niche shifts would
be likely in lake ecosystems (e.g., Persson et al. 2007). This is because aquatic ani-
mals grow by several orders of magnitude in size between hatching and death and
they typically exhibit clear ontogenetic niche shifts (Hildrew et al. 2007), and also
because lakes are basically closed systems to which simple theoretical analysis is
relatively applicable. I also emphasize that lake ecosystems are highly susceptible
to various anthropogenic disturbances including biodiversity degradation and habi-
tat modification resulting from human activity (Myers and Worm 2003; Eby et al.
2006; Collinge 2009). As a consequence, the dynamic resilience perspective may be
useful to manage lake ecosystems successfully.
From this viewpoint, I end this chapter by briefly discussing possible implications
of the present theoretical predictions for ecosystem management of Lake Biwa.
4.5 Toward Integrated Ecosystem Management 87
Fortunately, a large amount of biological and environmental data has been accumu-
lated by regular monitoring and sampling programs in Lake Biwa. These data may
provide valuable opportunities to consider the possibility. First, Lake Biwa was
invaded by piscivorous fishes (bluegill and largemouth bass) in the 1960–1970s
(Nakai 1999; Nakazawa et al. 2007), as with many temperate lakes in North America
and Europe (Rahel 2000; Hickley and Chare 2004). The dynamic resilience perspec-
tive suggests that these species invasions might have significantly influenced how the
native lake community responds to, and absorb, environmental disturbances by alter-
ing cascading top-down effects upon lower trophic levels (see Fig. 4.2). If this mech-
anism operates, some species may have become less likely to recover from
environmental change-induced population declines in the presence of the introduced
piscivores. Secondly, lakes are not completely closed systems but can be link to one
another by rivers, canals, and mobile animals. Furthermore, aquatic organisms often
form spatial population structure in large lakes. For example, previous studies using
stable isotopes and DNA markers have shown that some species would not be eco-
logically or genetically uniform in Lake Biwa with a surface area of about 670 km2
(Takai and Sakamoto 1999; Iguchi et al. 2008; but see Takahashi and Ohara 2004). I
also note that Lake Biwa is connected with many influent rivers and nearby satellite
lakes. Some fish species exhibit ontogenetic or breeding migration between Lake
Biwa and these surrounding waters (Shibata et al. 2010). Therefore, lakeshore devel-
opment in the past may have affected the ecosystem resilience mediated by spatial
structure through decreases in or degradation of littoral habitats (see Fig. 4.3; also see
Nakanish and Sekino 1996). Finally, climate change can also impact on lake ecosys-
tems. Recent studies showed that warming is an important driver of plankton com-
munity dynamics in Lake Biwa (Hsieh et al. 2010, 2011; Tsugeki et al. 2010),
although long-term variations in intra-annual population dynamics (i.e., phenologi-
cal shifts) remain unclear especially for higher trophic levels. Intriguingly, these eco-
system responses to climate change and eutrophication seem interactive. This may
imply that climate change also affects the ecosystem resilience to environmental
disturbance (see Fig. 4.4). Overall, although these theoretical implications are not yet
fully elucidated by empirical evidence, the dynamic resilience perspective suggests
that the ecosystem management of Lake Biwa (and other lakes) may benefit by being
more interdisciplinary and taking into account multiple ecosystem disturbances
associated with biodiversity, landscape, and climate.
In conclusion, we are still in the early stages of understanding how the resilience
of complex lake ecosystems is determined and how it is altered by anthropogenic
disturbances. Both theoretical and empirical advances are needed to refine the exist-
ing conception of ecological resilience and to develop more effective ecosystem
management that integrates biodiversity conservation, habitat protection, and cli-
mate change adaptation. Models and experiments that explicitly consider additional
factors are inevitably more complex than those that ignore them. However, given the
importance in ecological dynamics, the potential gains in understanding warrant the
additional effort required to include these factors. I conclude that ecosystem man-
agement should be made using the dynamic resilience perspective. The scenario-
based approach I outlined here will serve as the initial step.
Acknowledgements I thank anonymous reviewers for valuable comments on the manuscript.

This research was supported by the Japan Society for Promotion of Science Research Fellowship
for Young Scientists.
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Functional diversification of fishes, which play important ecological roles as

Otsu, Japan Noboru Okuda

1 Origin and Diversification of Freshwater Fishes in Lake Biwa .............. 1

3 Biodiversity Researches on Microbial Loop in Aquatic Systems............ 51

Keywords Adaptation • Ancient lake • Divergence time • Ecological speciation •

1.1 Introduction: Lake Biwa and Its Fish Fauna

N. Okuda et al., Biodiversity in Aquatic Systems and Environments: 1

Table 1.1 Fishes in Lake Biwa and its tributaries

4 Hypomesus nipponensis Wakasagi x

22 Hypophthalmichthys molitrix Hakuren x

24 Gnathopogon elongatus Tamoroko x x?

38 Hemibarbus labeo Korainigoi x

Table 1.1 (continued)

55 Paramisgurnus dabryanus Karadojo x

68 Gambusia affinis Kadayashi x

1.2 A Brief Review on the Origins and Evolution

the gudgeon Gnathopogon caerulescens (from G. elongatus), Carassius cuvieri

1.3 Molecular Phylogenetic Approaches

Recent experimental and theoretical developments in molecular genetics can allow

1.3.1 Origin of Endemic Lineages

Although not treated as distinct taxonomic units, populations of some species in

1.3.2 Population Establishment by Endemic

Fig. 1.5 Bayesian skyline

1.4 Conclusions and Perspectives

Keywords Biodiversity • Eco-evolutionary feedback • Ecological speciation •

2.1 Why is Biodiversity Important?

What is the ecological significance of conserving biological diversity within a spe-

N. Okuda et al., Biodiversity in Aquatic Systems and Environments: 21

ecological findings that the intraspecific diversity of a keystone species impacts

2.2 Biodiversity at Three Levels

According to the Convention on Biological Diversity (CBD), biological diversity

2.3 What is Phenotypic Polymorphism?

sense, however, it is applicable to the case in which intraspecific phenotypic varia-

2.4 Phenotypic Polymorphism in Aquatic Ecosystems

In aquatic organisms, phenotypic polymorphism is often observed in traits related

2.4.1 Trophic Polymorphism and Adaptive Divergence

foraging behavior is partly inherited in the progeny, behavioral specialization can

such as plankton (Robinson 2000). Such a morphological divergence is closely

2.4.2 Ecological Speciation and Species Pair

2.4.3 The Ancient Lake Biwa as an Evolutionary Hot Spot

Feeding habits and morphology Molecular phylogeny

Allopatric lacustrine population G. elongatus elongatus Allopatric lacustrine population

Allopatric fluvial population

Sympatric lacustrine population

Allopatric fluvial population

2.4.4 Life History Polymorphism

In freshwater fishes, another example of phenotypic polymorphism is often found in

An alewife Alosa pseudoharengus (Clupeidae) is one example where relationships

2.4.5 Rapid Evolution of Trophic Polymorphism

effect arising from introduction of a small number of individuals with subsequent

2.4.6 Genetic Mechanisms of Trophic Polymorphism

Although it remains unknown how phenotypic polymorphism is maintained within

2.5 Niche Construction

A member of a biological community embedded within an ecosystem has a number

functioning through ecological interactions between individuals or between biotic

a Trophic cascade b Nutrient transportation

Fish predator Fish predator

4.3 Regime Shifts Mediated by Ontogenetic Niche Shifts

4.4.1 Food-Web Topology

4.4.2 Spatial Configuration

4.4.4 Other Factors

dRJ / dt = rJ (1 R J / K J )R J a J , J CJ R J a A , J CA R J (4.7a)

4.5 Toward Integrated Ecosystem Management

4.5.1 From Static to Dynamic Resilience Perspectives

4.5.2 Implications for Lake Ecosystem Management