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Giant water bugs (Heteroptera: Belostomatidae) are aquatic predators of freshwater habitats, and include ca. 150 species distributed throughout the world's subtropical and tropical areas. They have unique mating systems, which involve female competition, and exhibit paternal care, wherein males attend eggs laid by the females on emergent plants (Lethocerinae) or on their backs (Belostomatinae). I review here the studies on the predator–prey relationships, morphology, migration, mating behavior and conservation of this family of insects. Giant water bugs (Belostomatidae: Heteroptera) are known as aquatic predators in freshwater habitats and have unique mating systems concerning male parental care and female competition. I review the ecology in this family based on published works.
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REVIEW ARTICLE
Ecology of giant water bugs (Hemiptera: Heteroptera:
Belostomatidae)
Shin-ya OHBA
Biological Laboratory, Faculty of Education, Nagasaki University, Nagasaki, Japan
Abstract
Giant water bugs (Heteroptera: Belostomatidae) are aquatic predators of freshwater habitats, and include
ca. 150 species distributed throughout the worlds subtropical and tropical areas. They have unique mating
systems, which involve female competition, and exhibit paternal care, wherein males attend eggs laid by
the females on emergent plants (Lethocerinae) or on their backs (Belostomatinae). I review here the studies
on the predatorprey relationships, morphology, migration, mating behavior and conservation of this
family of insects.
Key words: aquatic insect, dietary item, mating system, parental care, predator.
INTRODUCTION
Giant water bugs (Heteroptera: Belostomatidae) are
large-bodied aquatic predators of freshwater habitats,
and include ca. 150 species distributed throughout the
worlds subtropical and tropical areas (Lauck & Menke
1961). The family Belostomatidae includes eight genera
in the subfamily Belostomatinae (Horvathinia,Hydro-
cyrius,Limnogeton,Abedus,Weberiella,Belostoma,
Appasus and Diplonychus) and three genera in the sub-
family Lethocerinae (Benacus,Kirkaldyia and Letho-
cerus) (Polhemus 1995; Perez Goodwyn 2006;
Estevez & Ribeiro 2011; Ribeiro et al. 2018). Their
ecologies are important to human life because belosto-
matids are food sources in South-East Asia (Gope &
Prasad 1983; Chen et al. 1998), and regarded as natural
enemies of medically important insects (Shaalan & Can-
yon 2009) and pests of sh hatcheries (Wilson 1958).
They are found in freshwater habitats such as rice
elds, marshes, ponds, lakes, and rivers (Cullen 1969;
Menke 1979; Mukai et al. 2005). Their reproductive
biology is unique and well-known (Clutton-Brock
1991; Shuster & Wade 2003; Arnqvist & Rowe 2005;
Smiseth 2014), including female competition and male
parental care (Ichikawa 1988, 1990, 1991; Smith &
Larsen 1993; Thrasher et al. 2015). Within this family,
all species exhibit paternal care for eggs, wherein the
females lay on the malesback (Belostomatinae) or on
emergent plants (Lethocerinae) (Smith 1997). Thus,
they represent classic examples of paternal care systems
in arthropods.
Some Belostomatidae species are endangered. In
Japan, the population of Kirkaldyia deyrolli
(Vuillefroy) has decreased sharply over the last ve
decades and it is designated as a threatened-vulnerable
species in the Red Data Book of Japan (Ministry of the
Environment 2015).
In this paper, I review recent ndings and existing
knowledge on the biology of Belostomatidae to facili-
tate further ecological and conservational studies on
these interesting and important aquatic species.
PREDATORPREY RELATIONSHIP
Feeding habits of Belostomatidae
In temporary shless water pools, belostomatids are
often at the top of the food chain (Waters 1977; Kes-
ler & Munns Jr 1989; Smith 1997). Previous studies
focused on the dietary items of Belostomatidae from
the viewpoints of both applied and conservational
aspects. Belostomatids prey upon a variety of aquatic
animals such as insects, cladocerans, amphipods, tad-
poles and small sh (Fig. 1) (Hoffman 1924; Rankin
1935; Cullen 1969; Tawk 1969; Menke 1979;
Okada & Nakasuji 1993; Hirai & Hidaka 2002;
Toledo 2003; Ohba & Nakasuji 2006; Zaracho 2012;
Correspondence: Shin-ya Ohba, Biological Laboratory,
Faculty of Education, Nagasaki University, Bunkyo 1-14,
Nagasaki 852-8521, Japan.
Email: ooba@nagasaki-u.ac.jp
Received 14 April 2018; accepted 12 July 2018; rst
published 25 September 2018.
© 2018 The Entomological Society of Japan
Entomological Science (2019) 22, 620 doi: 10.1111/ens.12334
Ouyang et al. 2017). Therefore, they are regarded as
effective predators of medically important freshwater
snails or mosquitoes (Table 1). Differences in feeding
habits between the two subfamilies were reviewed by
Smith (1997). Belostomatinae does not digest verte-
brates well, because the saliva does not have enzymes
capable of digesting protein-rich meals such as verte-
brate animals (Swart et al. 2006). Species belong to
Lethocerinae, the largest-bodied subfamily in Belosto-
matidae, prefer to eat mainly vertebrate animals such
as sh and anurans (Smith 1997). For example, Letho-
cerus americanus (Leidy) prefers to eat larger sh
(Schumann et al. 2012). Males and pregnant females of
a cave sh (Poecilia mexicana Steindachner) are fre-
quently preyed upon by Belostoma sp., because males
and pregnant females typically exhibit more aquatic
surface respiration activity than non-pregnant females
(Tobler et al. 2008; Plath et al. 2011). In addition,
some researchers observed Lethocerus attacking birds
(Hungerford 1919; Menke 1979) and water snakes
(Wilson 1958). In recent years, it has also been
reported that K. deyrolli eats snakes (Rhabdophis tigri-
nus (Boie), Amphiesma vibakari (Boie) and Gloydius
blomhofi(Boie)) (Mori & Ohba 2004; Ohba 2012)
and turtles (Mauremys reevesii (Gray)) (Ohba 2011b)
in their habitats in Japan. Therefore, giant water bugs
should be regarded as higher consumers of wetlands as
well as vertebrate predators.
Generally, predators catch prey that are smaller
than they are (Nentwig & Wissel 1986; Warren &
Figure 1 Foraging Kirkaldyia deyrolli. (A) Loach and (B) frog foraging by adult(s), and (C) tadpole and (D) sh foraging by youn-
ger nymphs.
Ecology of giant water bugs
7Entomological Science (2019) 22, 620
© 2018 The Entomological Society of Japan
Lawton 1987). Prey size increases as predator
nymphs grow, as shown in Diplonychus indicus Ven-
katesan & Rao (Cloarec 1992), Belostoma oxyurum
(Dufour) (Perez Goodwyn 2001b) and Appasus japo-
nicus (Vuillefroy) (Ohba et al. 2008b). However,
nymphs of K. deyrolli do not conform to this pattern
(Ohba et al. 2008b). They possess a claw on the ter-
minal segment of the raptorial foreleg that is crucial
for capturing prey. Young nymphs with highly
curved claws caught proportionally larger prey than
older nymphs with less-curved claws. When young
nymphs (rst to third instars) encounter prey animals
that are larger than themselves, they rst hook the
claws of their raptorial legs onto the animal, and
then use all their legs to pin the larger animals, fully
clasping the prey body. The young nymphs are
forced to capture prey larger than themselves because
smaller prey are less abundant during the hatchling
season (Ohba et al. 2008b). Older nymphs have an
overall well-developed body size, but smaller prey are
regularly utilized. Indeed, all K. deyrolli nymphs are
able to feed on prey of a particular length (approxi-
mately 3 cm; Fig. 1C). They change catching behav-
ior based on changes in raptorial characteristics to
maximize prey resources acquired at each develop-
mental stage (Ohba & Tatsuta 2016).
Table 1 Genera and species of Belostomatidae predators of mosquito and snail
Genus or species Prey (mosquito or snail) Conrmation method Reference
Limnogeton eberi Physa acuta /Vivipara unicolor
/Lanistes carinatus
Laboratory experiment Tawket al. 1978
Diplonychus indicus Culex fatigans / Aedes aegypti Laboratory experiment Venkatesan & Sivaraman
1984
Diplonychus (Sphaerodema)
nepoides
Culex pipiens Laboratory experiment Victor & Weigwe 1989
Belostoma umineum Pseudosuccinea columella /
Physa vernalis
Field observation and
laboratory experiment
Kesler & Munns Jr 1989
Abedus herberti Physa virgata Laboratory experiment Velasco & Millan 1998
Diplonychus indicus Culex quinquefasciatus Laboratory experiment Venkatesan & DSylva
1990
Appasus (Diplonychus)
japonicus
Culicidae / aquatic snails Field observation Okada & Nakasuji 1993
Belostoma anurum Biomphalaria glabrata Laboratory experiment Pereira et al. 1993
Diplonychus (Sphaerodema)
annulatum / D. (S.) rusticum
Lymnaea (Radix) luteola Laboratory experiment Roy & Raut 1994
Belostoma oxyurum Aedes aegypti Laboratory experiment Perez Goodwyn 2001b
Belostoma umineum Physella gyrina /Helisoma
trivolvis
Laboratory experiment Chase 2003
Diplonychus (Sphaerodema)
annulatum
Culex quinquefasciatus Laboratory experiment Aditya et al. 2004
Appasus grassei Pulmonate snail Laboratory experiment Appleton et al. 2004
Diplonychus (Sphaerodema)
annulatum / D. (S.) rusticus
Armigeres subalbatus Laboratory experiment Aditya et al. 2005
Diplonychus sp. Culex annulirostris Laboratory experiment Shaalan et al. 2007
Diplonychus rusticus Culex quinquefasciatus Laboratory experiment Saha et al. 2007a, 2008;
Saha et al. 2010
Diplonichus annulatus Culex quinquefasciatus Laboratory experiment Saha et al. 2007b, 2008;
Saha et al. 2010
Diplonychus indicus Aedes aegypti Field experiment Sivagnaname 2009
Diplonychus spp. Anopheles gambiae s.l. Field collection and PCR Ohba et al. 2010
Belostoma lutarium Physa gyrina Field experiment Wojdak & Trexler 2010
Belostomatid species Anopheles gambiae s.s. Field experiment and PCR Kweka et al. 2011
Diplonychus (Sphaerodema)
rusticum
Culex quinquefasciatus Laboratory experiment Gurumoorthy et al. 2013
Diplonychus (Sphaerodema)
urinator
Lymnaea natalensis Laboratory experiment Younes et al. 2016
Diplonychus (Sphaerodema)
urinator
Bulinus truncatus /
Biomphalaria alexandrina
Laboratory experiment Younes et al. 2017
PCR, Polymerase Chain Reaction.
S. Ohba
8Entomological Science (2019) 22, 620
© 2018 The Entomological Society of Japan
Anti-predator reactions in prey animals of
Belostomatidae
The predatorprey relationship is one of the main bio-
logical interactions in nature. The negative effects of
Belostomatidae on prey animals include behavioral
and morphological changes. The tadpoles of Ana-
xyrus (Bufo) woodhousii Girard, for instance, switch
preference from dark backgrounds to white back-
grounds when they are exposed to chemical signals
released by Belostoma lutarium (Stål) (Swart & Taylor
2004). This is because B. lutarium can kill more tad-
poles exposed to dark backgrounds than to light
backgrounds. Belostoma umineum Say induces
snails, Planorbella (Helisoma) trivolvis (Say), to
develop changes in shell shape that reduce vulnerabil-
ity to water bug predation (Hoverman et al. 2005).
Snails that build wider shells increase the coiled tube
distance for retracting their body from B. umineum
to escape predation (Hoverman & Relyea 2007,
2009). In addition to behavior and morphological
changes, chemical defense has also been reported:
Lethocerus insulanus (Montandon) suffer from the
toxicity of Bufo (Rhinella) marina (Linnaeus) tadpoles
(Crossland 1998).
Predation by Belostomatidae and environmental
changes in aquatic systems are inversely related. Tad-
pole predation by Belostomatidae (B. umineum and
L. americanus) decreases with increasing plant density
because of increased refuge area (Babbitt & Jordan
1996; Babbitt & Tanner 1997; Tarr & Babbitt 2002).
Conversely, snail (Physa gyrina Draparnaud) predation
by Belostomatidae (B. umineum) induces algae
increase in the aquatic systems (Wojdak & Luttbeg
2005). Although the snails eat algae, they stop moving
and feeding when they perceive the risk of predation by
Belostomatidae. In other words, existence of Belosto-
matidae alters the snailsactivity and then induces algal
bloom, indicating a positive indirect effect of Belosto-
matidae on algae.
Predation upon Belostomatidae
Belostomatidae are also eaten by various animals such
as birds (Digiani 2002) and snakes (Munguia-Steyer &
Macias-Ordonez 2007). Eggs of Abedus herberti
Hidalgo were found in the stomach of brown trout
(Smith & Horton 1998). The proportion of cannibal-
ism in A. japonicus and Appasus major Esaki was
found to be higher than in K. deyrolli, as estimated by
analyzing dietary items, indicating the dietary differ-
ence between the species of Belostomatinae (inverte-
brate eaters) and Lethocerinae (vertebrate eaters)
(Okada & Nakasuji 1993; Ohba & Nakasuji 2006).
Nymphs of K. deyrolli were eaten by other aquatic
insects (mainly Laccotrephes japonensis Scott) and con-
specics (Ohba 2007; Ohba & Nakasuji 2007; Ohba &
Swart 2009). Predation of L. japonensis on K. deyrolli
nymphs was weaker when tadpole (common prey of
L. japonensis adults and K. deyrolli nymphs) prey
abundance was high (Ohba & Nakasuji 2007; Ohba
2011a).
PARASITES OF BELOSTOMATIDAE
Several parasites of Belostomatidae have also been
reported: water mite (Hydracarina) attaches on Letho-
cerus species (Mohan 1991; Nesemann & Sharma
2013) and A. japonicus (Abe et al. 2015; Abe et al.
2017). Belostoma dilatatum (Dufor) is known as the
host of metacercariae cysts of Stomylotrema vicarium
Braun (Amato & Amato 2006).
MORPHOLOGICAL STUDIES
Belostomatids have raptorial forelegs to capture prey
animals and are considered to be under selective pres-
sure during predation. In Belostoma elegans (Mayr)
and Belostoma cummingsi De Carlo, there is occur-
rence of multivariate allometric growth patterns of legs
in all nymphal instars. As a result, the segments of the
middle and hind legs present allometric coefcients
with opposite polarity to those of forelegs owing to the
different functions of the legs; the main function of
forelegs is to capture the prey, whereas the middle and
hind legs are adapted to swimming (Iglesias et al.
2008). A similar result was reported in Diplonychus
rusticus (Doke et al. 2017). Nutritional conditions dur-
ing early developmental stages in insects sometimes
affect the allometric growth patterns of body parts
(Emlen & Nijhout 2000). However, claw and foreleg
development during nymphal stages is less affected by
nutritional conditions and may be indispensable to the
increased predation success in K. deyrolli (Ohba et al.
2006). The reason for this is not yet known. Kirkaldyia
deyrolli mainly preys upon vertebrate animal prey after
hatching. Low variation in forelegs may result in spe-
cialized vertebrate feeding. This low variation should
be studied in the non-vertebrate eaters in the same fam-
ily (e.g. Belostomatinae) (Smith 1997; Ohba & Naka-
suji 2006; Swart et al. 2006) to explore the feeding
specialization hypothesis.
Females are usually larger than males in Heteroptera
or heteropterans, including in species belonging to the
subfamily Lethocerinae, indicating clear sexual size
dimorphism (SSD) (Perez Goodwyn 2006; Iglesias et al.
Ecology of giant water bugs
9Entomological Science (2019) 22, 620
© 2018 The Entomological Society of Japan
2012). However, body length (total length without
head) and maximum width do not differ between indi-
viduals of opposite sex in Belostoma elegans (Iglesias
et al. 2011). Other studies show that the trends of SSD
depend on individual species (Iglesias et al. 2012;
Thrasher et al. 2015). Generally, in Belostomatinae, the
selection pressure associated with fecundity in females
and the dorsal area available for egg-laying in the
males might be identical. However, male-biased SSD is
found in the middle and hind leg segments, which are
used during mating and brooding in Belostomatinae
(Iglesias et al. 2011). The males of Belostoma species
have relatively longer middle and hind legs, showing a
selective response for paternal care that maintain effec-
tive locomotion and denote a brood-adapted morphol-
ogy. However, this should be investigated in other
species because the male brooding behavior is different
among the different genera belonging to Belostomati-
nae. For example, Abedus and Belostoma show push-
up brood pumping (Smith 1997; Munguia-Steyer et al.
2008), whereas Appasus shows surface brooding only
(S. Ohba unpubl. data). Therefore, it is necessary to
integrate SSD analysis and behavioral studies involving
different species of Belostomatinae in the future to
increase our understanding of the functions of
parental care.
Male genitalia was supposed to be important for the
correct identication of the species of Belostoma bifo-
veolatum group. However, only Belostoma bifoveola-
tum (Spinola) might be clearly distinguished from the
other two species, B. angustum Lauck and B. elegans
(Stefanello et al. 2018). Appasus major and A. japonicus
are different in body size with overlapping distribution,
but they can also be identied by their genital morphol-
ogy (Suzuki et al. 2013) and different genetic structures
(Suzuki et al. 2014). Suzuki et al. (2013) also reported
that the male genital morphology has geographical vari-
ation within each species. Studying this variation in male
genital morphology across geographical locations could
help in species identication in this family.
MIGRATION
Dispersal behavior in aquatic insects is inuenced by
abiotic and biotic factors (Boda & Csabai 2013).
Lethocerines, also called electric light bugs,are fre-
quently attracted to light in large numbers (Menke
1979; Ono 1995; Yoon et al. 2010; Nwosu & Nwosu
2012; Nagaba & Takeda 2013). It is known that the
ight activity of belostomatids is highest during the wet
season and around the full moon (Bowden 1964; Cul-
len 1969; Duvirad 1974). In K. deyrolli, migration was
triggered by food shortage (Ohba & Takagi 2005) and
air temperature higher than 15C, irrespective of day
length (Yoon et al. 2010). In B. elegans inhabiting
unstable habitats and B. oxyurum inhabiting stable
habitats, the ight muscles were well-developed in the
former species, but not in the latter (Perez Goodwyn
2001a). These differences are related to their ight ecol-
ogy: occurrence of ight migration in B. elegans is
higher than in B. oxyurum. In K. deyrolli, the weight
of ight muscle showed no signicant yearly change
despite a conspicuous difference in ght activities
(Nagaba & Takeda 2013). They have the ight poten-
tial throughout the year, but they cannot y during
cold seasons at temperatures less than 15C. This is
because before ying they must warm up their muscle
temperature to approximately 40C (Ohba & Hiro-
naka 2018) (Fig. 2).
Other than ight, belostomatids migrate by walking
and drifting. The ightless species, Ab. herberti, escapes
from the stream when torrential rain falls onto the
stream surfaces. This behavior is referred to as stream
Figure 2 Temperature of the dorsal thorax surface of
Kirkaldyia deyrolli increasing to over 40C. Once the body
temperature exceeded 40C, the bug ew away (see Ohba &
Hironaka 2018).
S. Ohba
10 Entomological Science (2019) 22, 620
© 2018 The Entomological Society of Japan
abandonment behavior(Lytle 1999; Lytle & Smith
2004). Nymphs of K. deyrolli can disperse to neighbor-
ing waters by walking across the intervening levees
(Mukai et al. 2005). In L. americanus, drifting adults
were observed during winter (DuBois & Rackouski
1992). Drifting is explained as a dispersal mechanism
following the nal molt of nymphs, and winter is
selected for dispersal to minimize predation risks
(DuBois & Gobin 2001).
PATERNAL CARE AND MATING
SYSTEMS
In the subfamily Belostomatinae
Paternal care of Belostomatinae species plays a role in
maintaining oxygen and humidity conditions of their
egg masses (Smith 1976a,b, 1997; Munguia-Steyer
et al. 2008). Paternal behavior, that is, brood pumping,
brood stroking and surface brooding, is essential to egg
development and survival (Smith 1997). Eggs increase
in volume by absorbing water through the hydropyle
(Madhavan 1974; Venkatesan & Rao 1980). Thus,
egg-caring males change brood pumping in response to
the growth of the eggs, whereas non-brooded/sub-
merged eggs suffer lower hatching rates in Abedus bre-
viceps Stål (Munguia-Steyer et al. 2008). However,
paternal care behavior incurs a cost in terms of forag-
ing efciency (Crowl & Alexander 1989), mobility
(Kight et al. 1995) and longevity (Gilg & Kruse 2003)
in Belostoma umineum. Thus, males sometimes
remove the egg pad. Such abandonment occurs more
frequently in males with a smaller egg pad, which may
bring less benet relative to the cost of parental care
(Kight & Kruse 1992). The abandonment is likely to
occur under low temperature conditions (Kight et al.
2000) and when the males are isolated from the
females (Kight et al. 2011). Males with small egg pads
are more likely to discard their eggs in autumn (when
breeding adults are young) than in spring (Kight et al.
2011). However, there are also reports that cannot
detect the cost of egg-caring in Abedus breviceps under
wild conditions (Munguia-Steyer & Macias-Ordonez
2007) or Belostoma lutarium under laboratory condi-
tions (Thrasher et al. 2015).
When the females lay egg masses, the mating pairs
sometimes repeatedly copulate during a single mating
sequence; this is known in many species of Belostoma-
tinae (Smith 1979a,b; Ichikawa 1989). Frequent copu-
lation has been interpreted as an adaptation to reduce
sperm competition (Parker 1970; Simmons 2001) and
risk of cuckoldry (Smith 1979a). In A. herberti,
dimorphism (striped- and wild-type) has been
observed. Out of 250, 245 newly hatched nymphs
were attributable to males that had brooded their
eggs, indicating that the males repeated copulation
ensures his paternity of the eggs (Smith 1979b). How-
ever, a study using microsatellite DNA markers
revealed that paternity is not so high in A. major.
Appasus major collected from the eld showed 28.4%
of the eggs on the back of males were of other male
origin (Inada et al. 2011).
In the subfamily Lethocerinae
Lethocerinae males supply water to the egg mass laid
by the partner female on the emergent vegetation above
the water surface (Ichikawa 1988; Smith & Larsen
1993; Ordonez 2003). Similarly to the species of Belos-
tomatinae, submerged eggs cannot hatch (Ichikawa
1988). In addition to watering, there are two roles of
the brooding behavior of K. deyrolli males: defense
against infanticidal females (Ichikawa 1990, 1991,
1995) and protection of the egg mass from predators
(ants) (Ohba & Maeda 2017). The egg-caring male can
protect its eggs from ants by means of physical and
chemical defense. In the chemical defense, males release
a chemical substance with a grassy smell; this probably
deters ants from attacking the eggs (Ohba & Maeda
2017). Egg predation by females occurs due to the
female biased operational sex ratio during the repro-
ductive season (Ichikawa 1990, 1991, 1993). Although
the brooding males attack the infanticidal females, they
may not be able to overcome them because females are
larger than males in this species. By destroying the eggs
of her competitor, a female can obtain the mating part-
ner of the competitor and make certain that the male
takes care of her eggs without having to search for a
mate within the limited reproductive season (Ichikawa
1990). Egg-caring males stay on the egg mass during
the night to ensure that females cannot detect the males
and the eggs (Ichikawa 1995), and shorten the egg
development period by uniform watering all eggs to
regulate the hatching synchronization within an egg
mass (Ohba 2002).
In K. deyrolli, reproduction is controlled by high
temperature during summer and short day-length in
mid-summer; water temperature is the key factor in
determining the onset of reproduction, and photope-
riod plays the major role in the induction and mainte-
nance of diapauses after the reproductive season
(Hasizume & Numata 1997). Therefore, the reproduc-
tive season overlaps with the rainy season, from late
May to July in Japan, enhancing the egg hatching rate
by high humidity.
Ecology of giant water bugs
11Entomological Science (2019) 22, 620
© 2018 The Entomological Society of Japan
Evolution of paternal care in Belostomatidae
Belostomatidae represent classic examples of paternal
care systems in arthropods. The evolution of paternal
care and mating systems are excellent examples in
behavioral ecology (Shuster & Wade 2003). Lethoceri-
nae males (called emergent-brooders) supply water
to the egg mass laid by only one partner female on the
emergent vegetation above the water surface, whereas
Belostomatinae males (called back-brooders) show
behavior such as brooding, pumping, or swimming to
the water surface to provide oxygen to the egg mass
laid by multiple partner females simultaneously
(Smith 1997).
Smith (1997) proposed a fascinating hypothesis on
the evolution of paternal care in giant water bugs.
According to him, natural selection acting on body size
allows individuals to explore new food niches, such as
large aquatic prey animals. In the same research, it was
reported that as large females produced larger eggs, the
giant water bugs faced a problem: the larger eggs have
a low surface/volume ratio, which hampers gas
exchange in water. Thus, females started laying eggs on
the emergent vegetation (in Lethocerinae) or the back
of conspecic males (in Belostomatinae) to overcome
the low surface/volume problem(Smith 1997)
(see Fig. 3).
In addition to this hypothesis, once the male care for
the eggs became indispensable for egg survival, sexual
selection might have played a secondary role in the
maintenance of paternal care in Belostomatidae.
Recently, it was hypothesized that male care has
evolved under the pressure of sexual selection (Tallamy
2000, 2001; Alonzo 2012). In addition to offspring
survival, male care behavior could enhance reproduc-
tive success through increased mating opportunities,
because it provides direct benets to mates, thereby
attracting them (Tallamy 2000; Alonzo 2012). More-
over, paternal care can also provide an honest signal of
the males ability to defend offspring (Tallamy 2000,
2001). Therefore, males of species with established
paternal care can advertise their parental intent to
females (Hoelzer 1989; Kelly & Alonzo 2009). In addi-
tion to the harvestmen (Nazareth & Machado 2010)
and assassin bugs (Thomas & Manica 2005), the sex-
ual selection hypothesis is now supported by reproduc-
tive behavioral evidence from two genera of
Belostomatinae (Ohba et al. 2016; Ohba et al. 2018),
belonging to Diplonichini (Appasus and Diplonychus)
(Ribeiro et al. 2018). However, there is little informa-
tion on the sexual selection hypothesis in other genera
of Belostomatinae and Lethocerinae. In Lethocerinae,
the females of K. deyrolli do not give the egg-caring
males their own eggs without rst destroying the eggs
of other females (i.e. by performing infanticide)
(Ichikawa 1990, 1991), whereas a male of
L. americanus was found to attend multiple egg masses
(Smith & Larsen 1993).
During courtship displays, the males of Belostomati-
dae perform a pumping (push-up) display at the water
surface. Males that displayed for longer durations
secured more copulations in Abedus indentatus
(Haldeman) (Kraus 1989). Thus, further work is
needed to establish whether push-up displays indicate
male parental ability, and whether females discrimi-
nate between males based on these displays (Smiseth
2014). The volume of published work concerning
mating systems of Belostomatidae is increasing gradu-
ally, but there is not enough information on the rela-
tionship between female choice and male care. This
information will be essential to understand the evolu-
tion of paternal care in Belostomatidae, as well as in
other arthropods.
Figure 3 Schematic gure of
evolution of two subfamilies in
Belostomatidae based on Smiths
hypothesis (Smith 1997).
S. Ohba
12 Entomological Science (2019) 22, 620
© 2018 The Entomological Society of Japan
CONSERVATION
Belostomatidae species, especially lethocerines, are not
well studied yet irrespective of their large body size,
special niche in ecosystems and unique behavior. One
of the reasons is that their habitats are gradually
degrading, and their population size is decreasing their
distribution area. Kirkaldyia deyrolli, one of the well-
studied Lethocerinae species, is distributed throughout
Japan from central Honshu to the Ryukyu Islands,
southeastern Asia, China, Taiwan, and Korea (Perez
Goodwyn 2006). In Japan, rice elds provide major
habitats for K. deyrolli (Mukai et al. 2005; Ichikawa &
Kitazoe 2009). This species was abundant in these envi-
ronments in Japan up to the end of the 1950s; they are
used as key animals in ethological studies because of
their interesting behavior, such as paternal care and
sexual conict (Ichikawa 1988, 1990, 1995; Ohba &
Maeda 2017). Japanese populations of K. deyrolli have
decreased sharply during the last ve decades, and this
species is now included in the Red Data Book of spe-
cies in all 47 Japanese prefectures (Ministry of the
Environment 2015). Contributing factors such as
decreases in suitable aquatic habitats and food
resources, as well as water pollution and urbanization,
have been identied by some previous studies (see
below). Here, I discuss the factors that threaten their
existence and propose a future conservation strategy
for K. deyrolli.
Previous studies have reported that in Japanese rice
elds K. deyrolli mainly preys upon vertebrates, includ-
ing sh, snakes, turtles and frogs (Hirai & Hidaka
2002; Mori & Ohba 2004; Ohba & Nakasuji 2006;
Hirai 2007; Ohba et al. 2008a; Ohba 2011b, 2012).
Overall, the species diversity of rice ecosystems in
Japan has been declining due to recent land consolida-
tion, modication of traditional earth ditches to
U-shaped concrete ditches and use of agricultural che-
micals such as insecticides and herbicides (Fujioka &
Lane 1997; Katano et al. 2003; Nishihara et al. 2006).
Improvements of rice elds and irrigation ditches that
have been made over the last four decades to reduce
the workload of farmers could threaten sh diversity
and abundance (Katano et al. 2003; Fujimoto et al.
2008). These improvements include covering the sides
and bottoms of irrigation ditches with concrete,
increasing the difference in water level between rice
elds and drainage ditches, and separating irrigation
ditches that supply and drain water. A large number of
loaches, Misgurnus anguillicaudatus (Cantor), migrate
to conventional paddy elds (Katano et al. 2003),
which have no vertical gaps between the paddy elds
and drainage ditches. However, a vertical gap between
the water levels of the paddy eld and the drainage
ditch disturbs the upstream migration of loaches
(Suzuki et al. 2001; Kano et al. 2010; Katayama et al.
2011). Hence, the loach populations have rapidly
decreased throughout the country. This reduction in
loach population density inuences the diets of
K. deyrolli (Ohba et al. 2012). Although loaches are
appropriate prey for reproducing in K. deyrolli adults
(Ohba et al. 2012), anuran larvae are indispensable for
rapid growth in younger instar nymphs (Ohba et al.
2008a). These studies strongly suggest that environ-
ments that contain an abundance of both frogs and
loaches are important for maintaining K. deyrolli
populations.
Water pollution by continuous insecticide use
undoubtedly impacted the abundance of K. deyrolli in
the last half of the 20th century (Ministry of the Envi-
ronment 2015), due to direct and indirect exposure by
preying on polluted prey animals (bioaccumulation)
(Ichikawa & Kitazoe 2009). Threats of insecticide and
changes in the insecticide content should be continu-
ously investigated and monitored in the future. In
another study, hormonal regulation and the potential
involvement of environmental pollutants such as
endocrine-disrupting chemicals in reproduction was
investigated using vitellogenin (Nagaba et al. 2011). It
was shown that endocrine chemicals might disrupt the
reproductive physiology in nature, providing a rst
indication that environmental pollutants could be the
cause of the rapid disappearance of K. deyrolli from
Japanese ecosystems (Nagaba et al. 2011).
Vegetation in rice elds is also an important factor
for the existence of another species of Lethocerinae,
Lethocerus indicus (Lepeletier & Serville), distributed
in South and South-East Asia; they are not found in
rice elds without vegetation (Kandibane et al. 2007).
In K. deyrolli, Mukai et al. (2005) reported the impor-
tance of vegetation in aquatic habitats as oviposition
sites. In addition to the rice elds, the vegetation of the
surrounding environment is also indispensable. The
population of K. deyrolli is higher near forested envi-
ronments (Iwai & Kobayashi 2007). The reason is that
K. deyrolli migrates to under litter in the forests around
rice elds to hibernate (Ichikawa & Kitazoe 2009). In
addition, a study investigating the environmental con-
ditions of the microhabitats of K. deyrolli in ponds and
ditches showed that high water temperature (approxi-
mately 30C), water depth (15.029.9 cm), mud bot-
tom and vegetation coverage of more than 75% are
suitable for the existence of K. deyrolli species in
Tochigi Prefecture, Japan (Kobayashi & Iwai 2007).
Therefore, an integrated conservation strategy that
includes rice elds and the surrounding environments
Ecology of giant water bugs
13Entomological Science (2019) 22, 620
© 2018 The Entomological Society of Japan
of rice elds should be considered for the protection of
this species.
Flight migration of K. deyrolli certainly occurs dur-
ing the night (Ichikawa & Kitazoe 2009). It is thought
that articial lights might have a negative impact on
K. deyrolli abundance in Korea (Ho et al. 2009) and
Japan (Ono 1995). As shown by Ohba and Hironaka
(2018), K. deyrolli y after warming up their muscle
temperature to approximately 40C (Fig. 2), indicating
higher energy cost per ight behavior. In addition,
K. deyrolli lost considerable amounts of body water
during ight migration and died of dehydration when
water was not supplied within one night (Ohba &
Takagi 2005). If K. deyrolli lands on a dry site, for
example, under articial light along streets, they could
die of dehydration, road-kills by cars, predation by
mammals and frequent collection by humans (Hirai &
Inatani 2006; Yoon et al. 2010; Ohba et al. 2013). In
the future, novel lights that do not attract K. deyrolli
should be installed in areas where the species exists.
Invasive exotic animals are known as novel threats
to K. deyrolli. The red swamp craysh, Procambarus
clarkii (Girard), is native to the southeastern USA but
was introduced to Japan during 19201930, and its
distribution expanded until 1980 (Ban 2002). The sur-
vival rate of K. deyrolli nymphs in the craysh-infested
area was clearly lower than that in the non-craysh
area (Ohba 2011c). In addition to predation by
P. clarkii,K. deyrolli that ate P. clarkii died, or nearly
so, due to unknown reasons (Ohba & Ichikawa 2016).
The invasive bullfrog, Lithobates catesbeiana (Shaw),
which is native to the USA, was introduced in Japan in
1918 (Maeda & Matsui 1999) and has spread rapidly
throughout the country. The bullfrog eats a wide range
of native aquatic animals, including belostomatids
(A. japonicus and K. deyrolli) (Hirai 2004; Hirai &
Inatani 2005). Elimination of these invasive exotic ani-
mals is strongly recommended for conservation of these
water bugs.
The Japanese common name of K. deyrolli is
tagame.Taand gamemean rice eld and turtle,
respectively. As shown in the Japanese common name,
rice elds are important habitats for this species. How-
ever, the environment of rice elds is rapidly changing,
and rice elds are deserted due to a decrease in the
number of farmers in the rural areas of Japan. In the
future, conservation using alternative habitats to rice
elds will be required. There are some examples of con-
servation of K. deyrolli in biotopes converted from fal-
low rice elds (Ichikawa 2004; Ichikawa & Ohba
2015). Conservation strategies using such biotopes
could help to conserve the populations of K. deyrolli
and other aquatic animals.
ACKNOWLEDGMENTS
I thank Fusao Nakasuji, Haruki Tatsuta, Shin-ichi
Kudo, Noritaka Ichikawa and members of Okayama
University, Kyoto University and Nagasaki University
for their kind support and continuous encouragement.
I am grateful to Felipe F. F. Moreira and José Ricardo
I. Ribeiro for their invaluable comments on an early
draft. I also thank Pablo J. Perez Goodwyn (deceased
on 8 August 2009) for his valuable information and
suggestions on the Belostomatidae until the day before
his sudden death. This work was supported in part by
Research Fellow for Young Scientists funding from the
Japan Society for the Promotion of Science (No. 22-4).
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... Giant water bugs (Heteroptera: Belostomatidae) are predacious aquatic true bugs that include some of the largest freshwater insects in the world. The subfamily Lethocerinae comprises three genera (Benacus, Kirkaldyia and Lethocerus), known for their preference for vertebrate prey during all stages of their life (Ohba 2019). In addition to consuming fish and amphibian larvae (Ohba 2011a), the members of the subfamily very often enhance their diet with aquatic vertebrates such as turtles, snakes and frogs (Mori & Ohba 2004;Ohba 2011bOhba , 2019. ...
... The subfamily Lethocerinae comprises three genera (Benacus, Kirkaldyia and Lethocerus), known for their preference for vertebrate prey during all stages of their life (Ohba 2019). In addition to consuming fish and amphibian larvae (Ohba 2011a), the members of the subfamily very often enhance their diet with aquatic vertebrates such as turtles, snakes and frogs (Mori & Ohba 2004;Ohba 2011bOhba , 2019. The genus Lethocerus consists of 22 species (Perez-Goodwyn 2006) that follow the general pattern of predation on vertebrates (Ohba 2019). ...
... In addition to consuming fish and amphibian larvae (Ohba 2011a), the members of the subfamily very often enhance their diet with aquatic vertebrates such as turtles, snakes and frogs (Mori & Ohba 2004;Ohba 2011bOhba , 2019. The genus Lethocerus consists of 22 species (Perez-Goodwyn 2006) that follow the general pattern of predation on vertebrates (Ohba 2019). ...
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... Because water and oxygen are crucial and mutually restrictive environmental factors for the embryonic development of aquatic arthropods, some aquatic arthropods evolved extraordinary behavioural adaptations for aerating and hydrating eggs might be related to their large eggs that must rely on passive diffusion of oxygen [2,35]. For example, the basal giant water bugs in the lethocerines (emergentbrooders) periodically supply water to the egg mass on the sites of oviposition (commonly emergent aquatic vegetation) [35,[41][42][43]; and belostomatines (back-brooders) even evolved brooding behaviour wherein males carry a clutch of eggs laid by the females on their backs until hatching to prevent them from desiccation and drowning [41,43,44]. The same principle is reflected in some extant water boatman species that lay eggs upon the exoskeletons of freshwater crayfish, especially the gills and first abdominal pleurite where there are the best chances for aeration, relying on the current of flowing water [29,45]. ...
... Because water and oxygen are crucial and mutually restrictive environmental factors for the embryonic development of aquatic arthropods, some aquatic arthropods evolved extraordinary behavioural adaptations for aerating and hydrating eggs might be related to their large eggs that must rely on passive diffusion of oxygen [2,35]. For example, the basal giant water bugs in the lethocerines (emergentbrooders) periodically supply water to the egg mass on the sites of oviposition (commonly emergent aquatic vegetation) [35,[41][42][43]; and belostomatines (back-brooders) even evolved brooding behaviour wherein males carry a clutch of eggs laid by the females on their backs until hatching to prevent them from desiccation and drowning [41,43,44]. The same principle is reflected in some extant water boatman species that lay eggs upon the exoskeletons of freshwater crayfish, especially the gills and first abdominal pleurite where there are the best chances for aeration, relying on the current of flowing water [29,45]. ...
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... Popularly known as 'electric light bugs', belostomatids are widely distributed throughout the American continent, with about 150 species described among eleven genera, of which eight belong to the subfamily Belostomatinae and three to Lethocerinae (Perez-Goodwyn 2006; Moreira et al. 2011;Ribeiro et al. 2017Ribeiro et al. , 2018. This group has great potential as a biological control agent (Ohba 2019). They are apex predators, and some species feed on larvae and pupae of Aedes aegypti Linnaeus, 1762 (Goodwyn 2001). ...
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Known as "electric-light bugs", belostomatids potentially act as agents of biological control. The Belostoma genus has holokinetic chromosomes, interspecific variation in diploid number, sex chromosome system and DNA content. Thus, the chromosomal complement, the accumulation of constitutive heterochromatin and the distribution of rDNA clusters by fluorescence in situ hybridization (FISH) in Belostoma angustum (BAN), Belostoma sanctulum (BSA), and Belostoma nessimiani (BNE) were evaluated. In addition, a comparative analysis of the DNA content of these species and B. estevezae (BES) was performed. BES has the highest Belostoma DNA content, while BSA has the lowest. BAN showed 2n = 29 + X1X2Y, while BSA and BNE had 2n = 14 + XY. BSA showed 18S rDNA markings on sex chromosomes, while BNE and BAN did on autosomes. The difference between BSA and BNE occurs because of the possible movement of the rDNA cluster in BNE. We suggest the occurrence of fusion in the autosomes of BSA and BNE, and fragmentation in the sex chromosomes in BAN. Also, the genome size of 1–2 pg represents a haploid DNA content of a common ancestor, from which the genomes of BES and BAN had evolved by gene duplication and heterochromatinization events.
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Knowing the trophic links between species is essential to understand their functions in the ecosystem. In this work, we report the first predation record of Rhinella crucifer by the giant water bug Lethocerus grandis. Even though most Brazilian anurans preyed by giant water bugs are smaller than this insect, a larger body size of this predator together with its anesthesic saliva may provide conditions for the subjugation of larger prey.
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Neponymphes godoii Zamboni, 2001 is redescribed and illustrated based on specimens from the Lower Cretaceous of Northeastern Brazil (Araripe Basin, Crato Formation; upper Aptian, ~114 Ma). The redescription, based both on the adult and nymphal stages, shows that the external morphological characters of N. godoii were fairly similar to those of recent members of the Belostomatini. Hence, the external morphology in this tribe has apparently not changed much since the Cretaceous.
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Specified class II nationally rare species of wild fauna/flora designations were first made in Japan for three species, the Tokyo salamander (Hynobius tokyoensis), golden venus chub (Hemigrammocypris rasborella), and giant water bug (Kirkaldyia deyrolli). These species depend on the shallow water in agroecosystems, secondary forests, and parks. The objective of this paper was to provide an overview of the factors relating to their conservation, which were as follows: (1) the landscape affects significantly on distributions of three species. H. tokyoensis and K. deyrolli both require landscapes in which wetlands and forests connect. While H. rasborella inhabits isolated ponds also, the original habitat is a flood plain where fishes seasonally move temporary pools for spawning. Therefore, channel networks are needed to protect fishes including H. rasborella. (2) Agricultural land infrastructure affects the three species, as dry paddy fields and concrete-lined ditches are unsuitable for them, as well as other aquatic animals. Several construction methods, however, have been trialed to allow fish to live in modernized ditches. (3) K. deyrolli is highly sensitive to pesticides. (4) Mid-summer drainage of paddy fields will threaten populations of H. tokyoensis and K. deyrolli as these paddy fields lose water before these species have completed their metamorphosis. Wet-paddy fields that are not completely dried, postponement of mid-summer drainage, and the installation of diversion ditches, however, could all help to mitigate this issue. (5) The impacts of abandoned cultivation and pond management are significant for these species. (6) Invasive alien species have a significant impact on H. tokyoensis and H. rasborella. (7) Habitat creation and translocation of these species has often been successful. However, the sustainability of the translocated populations is a challenge. When these species are introduced outside their natural habitats, it is thus necessary to consider the ecosystem of the destination area and the genetic background of the target species. I conclude that the combination of biotopes with wildlife-friendly farming and continuity of paddy fields with forests throughout the landscape secure the population sustainability.
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Paternal care can be maintained under sexual selection in case that it helps caring males to attract more mates. Females of two back-brooding water bug species, the belostomatids Appasus major and A. japonicus, prefer egg-caring males over non-caring males. Here, we tested under laboratory and field conditions whether females of another belostomatid species, Diplonychus rusticus, prefer egg-caring males as mating partners. Caring males received more eggs from females than non-caring males under the both conditions. Our results suggest that sexual selection plays an important role in maintaining paternal care not only in species of the genus Appasus, but also in the genus Diplonychus.
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Recent investigations into relationships among the cosmopolitan Belostomatidae have led to recognition of the Belostomatinae, Horvathiniinae and Lethocerinae clades. Here we investigate the relationships among the genera of this family (with Appasus, Benacus and Kirkaldyia now resurrected, and three fossils: Cratonepa, Iberonepa and Lethocerus vetus) by including modifications or clarifications of both somatic and genitalic characters (including some spermatheca traits), as well as multiple genes (COI, 18S rDNA and 16S rDNA). A comparative study of these genera yielded putative homology hypotheses coded as 104 morphological characters and 1829 aligned characters. A majority-rule tree utilizing the Bayesian method [the ‘master’ tree with highlighted clades estimated by maximum parsimony and maximum likelihood (ML)] is as follows: (Cratonepa, Iberonepa, (Benacus, Kirkaldyia, Lethocerus), (((Horvathinia, Hydrocyrius), Limnogeton), (((Abedus, Weberiella), Belostoma), (Appasus, Diplonychus))))). Lethocerinae and Belostomatinae (now with Horvathinia included) form two monophyletic groups. Weberiella appears as the sister group of Abedus, and Belostomatini had to be reformulated. In all trees, the monophyly of Diplonychinitrib. nov. (Appasus+Diplonychus) was recovered with high support indices. This study highlights a global tree based on combining the molecular and morphological data representing topologies from separate analyses, irrespective of the existence of missing data and the type of dataset.
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The bifoveolatum group comprises three known species (Belostoma angustum Lauck, B. bifoveolatum (Spinola), and B. elegans (Mayr)), with representatives occurring in southern and south-eastern South America, as well as along the Andes. These species, however, are cryptic with regard to body dimensions and male genitalia. Much of this cryptic variation in male genitalia is still misunderstood, so that proposed keys to bifoveolatum species are scarce and have been based only on body dimensions. In fact, it is not understood whether different parts of male genitalia covary themselves in the integrated way, or if parameres are somehow associated with male genitalia. This paper investigates whether there is expressive variation and integration in the shape of intromitent parts of male genitalia and parameres through specimens of those species from different southern South American localities, by using geometric morphometrics. We also test the hypotheses that the base of phallotheca [PHA]/dorsal arms [DA] subdivision, as well as base/apex of parameres, constitute separate modules. We semi- and landmarked PHA and DA, as well as the right paramere [PA], of 89 B. angustum males, four males of B. bifoveolatum and eight of B. elegans. To eliminate all non-shape variation, point configurations were subjected to the generalised least-squares Procrustes superimposition. A multilevel approach showed that the patterns of integration within individual, among individual and among populations centred by species are similar, with total variation concentrated in a few of the available dimensions. Accordingly, this correspondence is apparent with the very high values of matrix correlations between the covariance matrices for within-species-locality and among localities (r = 0.91 for PHA + DA and r = 0.86 for VD). Fluctuating asymmetry was not negligible for PHA + DA and it seems that there might be little agreement between it and the other levels of variation (matrix correlation using individual variation, r = 0.34. P < 0.0001; matrix correlation using variation among population, r = 0.29, P < 0.0001). After eliminating size effects, morphological integration between PHA + DA and PA was significant (RV = 0.058, P = 0.0313), which might have enabled greater elaboration of these parts resulting in their greater and faster diversification at the individual level. Our results indicated poor agreement between different levels of variation with regard to fluctuating asymmetry, such that direct developmental interaction is not important for all levels of covariation between PHA + DA and PA through bifoveolatum group of species. Our findings suggest the lack of diagnostic importance of the PHA + DA and VD to differentiate the species B. angustum and B. elegans, despite of their integration. Both DA/PHA and apex/base of PA modularity hypotheses were not refuted across all levels, which might be an indicative of the lack of integration between PA and PHA + DA at higher levels of organisation, such as among populations.
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The study of insect social behavior has offered tremendous insight into the molecular mechanisms mediating behavioral and phenotypic plasticity. Genomic applications to the study of eusocial insect species, in particular, have led to several hypotheses for the processes underlying the molecular evolution of behavior. Advances in understanding the genetic control of social organization have also been made, suggesting an important role for supergenes in the evolution of divergent behavioral phenotypes. Intensive study of social phenotypes across species has revealed that behavior and caste are controlled by an interaction between genetic and environmentally mediated effects and, further, that gene expression and regulation mediate plastic responses to environmental signals. However, several key methodological flaws that are hindering progress in the study of insect social behavior remain. After reviewing the current state of knowledge, we outline ongoing challenges in experimental design that remain to be overcome in order to advance the field. Expected final online publication date for the Annual Review of Genetics Volume 51 is November 23, 2017. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
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In 1999 the Environment Agency, Japan released the red list of brackish and freshwater fishes, in which the number of the Threatened fishes amounted to 110. One of the reasons why many fishes became endangered is implementation of land consolidation project in the paddy field area. This project aimed at reducing labor requirement in farming activities. However, watercourse networks have been disconnected by drop structures in the canals and elevation gap between outlets of paddy fields and drainage canals, which resulted in aggravation of the inhabiting environment of fishes. Therefore, it is eagerly required to reconnect watercourse networks by some artificial measures. In this connection this research was carried out to develop small-scale fishways for restoring damaged condition. In this research two kinds of fishes, Misgurnus anguillicaudatus and Oryzias latipes, were selected as sample fishes. Those are usual freshwater fishes in paddy field area of Japan, and Misgurnus anguillicaudatus represents a demersal fish, whereas Oryzias latipes represents a pelagic fish. Two types of small-scale fishways, named Cascade-M type and Chidori-X type, were developed and laboratory experiments were conducted to exam whether the developed small-scale fishways ensure upward and downward migration of sample fishes or not under the different conditions of inclination and flow rates. The result obtained were as follows; 1) the Cascade-M type fishway enabled upward and downward migration of Misgurnus anguillicaudatus (crawling type and swimming type), 2) Chidori-X type fishway enabled upward and downward migration of Misgurnus anguillicaudatus (swimming type) and Oryzias latipes, 3) Upward migration of Misgurnus anguillicaudatus became active in night time compared to day time, and 4) Oryzias latipes shows stronger rheotaxis compared to Misgurnus anguillicaudatus. © 2001, Ecology and Civil Engineering Society. All rights reserved.