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97
INTRODUCTION
Rotifers are a relatively small group of invertebrates
consisting of about 2000 named species of unseg-
mented, bilaterally symmetrical pseudocoelomates
(Wallace & Snell, 1991; Wallace et al., 2006; Segers,
2007). They account for a large proportion of zoo-
plankton diversity in freshwater and brackish envi-
ronments, inhabiting practically any body of water,
from a trickle on the rocks to ponds, streams, marsh-
es and salt lakes (Pejler, 1995). Because of their small
size (40 Ìm- 2 mm), rotifers constitute only a relative-
ly minor part (about 2.5%) of zooplankton biomass,
but they are significant in continental aquatic sys-
tems. Their importance lies in their exceptionally high
reproductive rates, which are faster than these of any
metazoan (Bennett & Boraas, 1989). Because of their
high reproductive rates they occasionally numerical-
ly dominate zooplankton communities (Wallace &
Smith, 2009). Moreover, they have the ability to popu-
late vacant niches rapidly and are quite efficient gra-
zers, making primary production (phytoplankton and
bacteria) available to secondary consumers (e.g.
other zooplankton species, fish fry). Their role in the
production cycle is of considerable importance (Stark-
weather, 1987; Armengol et al., 2001; Wallace & Smith,
2009).
Despite their minute size, female rotifers are ana-
tomically complex (Wallace & Snell, 1991). Rotifer
males are dwarf and have simplified anatomy with re-
duced functions (Epp & Lewis, 1979; Ricci & Melo-
ne, 1998). The development is eutelic (i.e. constant
cell number after ontogenetic development) and
growth to final size is accomplished by mere stretch-
ing of existing cells. Rotifers are characterized by two
distinct features: a corona (a ciliated region at the an-
terior end), used for locomotion (i.e. swimming) and
food gathering, and a specialized pharynx, the mas-
tax, which serves as a jaw (Ruttner-Kolisko, 1974;
Nogrady et al., 1993).
The phylum Rotifera contains three classes. The
largest class –monogononts (more than 1500 spe-
cies)– reproduces by cyclical parthenogenesis, a life
cycle which combines asexual and sexual reproduc-
The rotifer Brachionus plicatilis:
an emerging bio-tool for numerous applications
Venetia KOSTOPOULOU1*, María José CARMONA2and Pascal DIVANACH1
1Institute of Aquaculture,Hellenic Centre for Marine Research,
P.O. Box 2214,Heraklion,71003 Crete,Greece
2Institut Cavanilles de Biodiversitat i Biologia Evolutiva,Universitat de València,
P.O. Box 22085,46071 Valencia,Spain
Received: 5 May 2011 Accepted after revision: 7 September 2011
The rotifer Brachionus plicatilis is a common brackish-water zooplankter, and one of the best-
studied rotifer species. It is characterized by high growth rate, widespread distribution, ubiquity
in aquatic systems, ease of culture, adequate size, ability to feed on a variety of feed types and a
complex life cycle. It has been used extensively as a tool in aquaculture and ecotoxicology and
constitutes a model organism in ecological and evolutionary studies. This paper explores other
possible uses of this organism in various fields: environmental control of eutrophication and
harmful algal blooms, containment of cholera, management of pollution and petroleum com-
pounds, wastewater treatment, impact of climate change on biodiversity and transfer of useful
substances.
Key words: pollution, eutrophication, climate change, disease treatment.
* Corresponding author: tel.: +30 2810 337766, fax: +30
2810 337778, e-mail: vkostop@biol.uoa.gr
Journal of Biological Research-Thessaloniki 17: 97 –112, 2012
J. Biol. Res.-Thessalon. is available online at http://www.jbr.gr
Indexed in: WoS (Web of Science, ISI Thomson), SCOPUS, CAS (Chemical Abstracts Service) and DOAJ (Directory of Open Access Journals)
tion (Fig. 1). Typically, a rotifer population grows
parthenogenetically (asexual proliferation), whereby
a repeated number of generations of amictic (asexu-
al) females produce mitotically diploid eggs. These
eggs hatch into genetically identical amictic female
offpsring. Following certain environmental cues, such
as population density and photoperiod (Carmona et
al., 1993; Gilbert, 2004; Snell et al., 2006), amictic fe-
males produce mictic (sexual) female individuals as
some fraction of their offspring. Mictic females mei-
otically give rise to haploid eggs. These eggs, if not
fertilized, develop into haploid males. The latter can
inseminate other mictic females, whose fertilized eggs
will develop into diploid encysted embryos (resting
eggs), which undergo diapause. Once produced, rest-
ing eggs sink and settle in the sediment. Resting eggs
are resistant to harsh environmental conditions, such
as drying or freezing, and may be dispersed over wide
areas by the wind, water or migrating animals (Gil-
bert, 1974; Schröder, 2005). After an obligatory dor-
mant period, and taken that conditions become fa-
vourable, resting eggs hatch into amictic females that
enter into the asexual phase of the life cycle (Ruttner-
Kolisko, 1974; Nogrady et al., 1993; Wallace et al.,
2006). A fraction of the diapausing eggs do not hatch
when the conditions are favorable, which results in a
pool of diapausing eggs in the sediment, the so-called
‘egg bank’ (Marcus et al., 1994; Hairston, 1996).
Cyclical parthenogenesis combines the advantages
of rapid multiplication, when conditions are favoura-
ble to exploit resources (parthenogenesis), with long-
term survival through resting egg production, when
conditions deteriorate (sexual reproduction). Parthe-
nogenesis eliminates the problem of mating encoun-
ters and the cost of producing males, allowing an ase-
xual population to grow faster than a sexual one –in-
trinsic growth rate difference being dependent on the
level of sexuality (Serra & Snell, 2009; Stelzer, 2011).
98 Venetia Kostopoulou et al. — Brachionus plicatilis: an emerging bio-tool for numerous applications
2N
2N
2N
2N
2N
2N
2N
2N
2N
2N
N
N
N
Amictic
female
Amictic
female
Amictic
female
Amictic
female
Egg Egg
Egg
Haploid egg
Resting
egg
Hatching
signal
Mixis
signal
Egg
Mictic
female
Unfertilized
haploid egg
Male
Spermatozoon
Sexual
reproduction
(mixis)
Parthenogenesis
mitosis
mitosis
mitosis
mitosis
meiosis
fertilization
N
FIG. 1. Schematic representation of cyclical parthenogenesis in the rotifer Brachionus plicatilis.
Cyclical parthenogenesis serves to produce clones
best adapted to prevailing conditions. These clones
are theoretically capable of successfully exploiting the
existing habitat. In that respect, population growth is
not limited by initial sparseness and a single indivi-
dual is theoretically capable of colonizing a new habi-
tat (Gerritsen, 1980). Sexual reproduction on the other
hand, produces genetic variation in offspring through
the mechanism of sexual recombination. This results
in higher rates of adaptation and inhibits the accu-
mulation of deleterious mutations (e.g. West et al.,
1999). Moreover, the linkage between dormancy and
sex allows long-term survival of rotifer populations
(Carmona et al., 2009; Serra & Snell, 2009). Sexual
reproduction, through the production of resting eggs,
offers environmental escape in space and time (Pour-
riot & Snell, 1983; Serra et al., 2004).
One of the best known monogonont rotifers is
Brachionus plicatilis (Müller, 1786). This rotifer has
been extensively studied, owing to its use in aquacul-
ture (Lubzens, 1987). Once considered a pest (“mizu-
kawari” – Hirata, 1980), it now forms an indispens-
able element of hatcheries, where it is offered as first
feed to fish larvae.
Brachionus plicatilis has been classified as an r-
strategist (Walker, 1981; Miracle et al., 1988), due to
its small size, rapid growth and low C-value (i.e. DNA
content), which has been estimated between 55 and
407 Mbp (Stelzer et al., 2011). DNA content is highly
correlated in eukaryotes with cell and nuclear volu-
me, cell cycle length and minimum generation time
(Cavalier-Smith, 1978). Based on the above, smaller
genomes will result in more rapid mitotic division and
cell cycles, conferring faster growth rates and earlier
age at first reproduction. Such rapid development will
eventually enhance the likelihood of contribution to
the gene pool of the next generation when the envi-
ronment is ephemeral (Wyngaard et al., 2005).
According to the above, B. plicatilis is capable of
quick colonization of a habitat, once appropriate con-
ditions arise. It is a strategist of ephemeral or other-
wise fluctuating habitats, such as temporary saline la-
kes and brackish coastal lagoons that often dry during
the summer months (Ruttner-Kolisko, 1974; Walker,
1981; GÔ´mez et al., 1995). The occurrence of B. pli-
catilis in extreme environments points towards its re-
markable tolerance to abiotic conditions (Epp &
Winston, 1977; Walker, 1981; Esparcia et al., 1989). It
has been detected in all continents with the exception
of the Antarctic (Segers, 2007). The widespread dis-
tribution of B. plicatilis suggests an efficient means of
dispersal via resting eggs (Walker, 1981; GÔ´mez et al.,
2002).
In most of the recent literature, B. plicatilis was
thought to be a single species, cosmopolitan and gene-
ralist. However, its revised taxonomical status has re-
vealed an under-determined ancient cryptic species
complex, comprising of at least 14 species/lineages
(Gomez et al., 2002; Suatoni et al., 2006). Such ‘hid-
den’ diversity is expected to revolutionize the study of
this taxa. For this reason, molecular tools, aiming to
facilitate the identification of the species complex, are
investigated (Papakostas et al., 2005, 2006a; Dooms et
al., 2007; Vasileiadou et al., 2009). It has already been
shown that the different species/lineages have a more
restricted distribution and ecological range of toler-
ance than the complex as a whole (Ciros-Perez et al.,
2001; Ortells et al., 2003). In nature, they have been
shown to either coexist and/or succeed one another
along the seasonal cycle (Serra et al., 1998; Ortells et
al., 2003; Montero-Pau et al., 2011). However, in a-
quaculture farms only a small fraction of the B. plica-
tilis genetic diversity is being exploited (Papakostas et
al., 2006b, 2009).
In nature, B. plicatilis feeds mainly on phytoplank-
ton, although organic detritus and bacteria can also
represent alternative feeding sources (Pourriot, 1977;
Starkweather, 1980; Arndt, 1993). In hatcheries, B.
plicatilis is also able to grow on formulated diets, pre-
pared to fulfil the specific dietary requirements of fish
larvae (Lubzens et al., 2001).
Apart from aquaculture, B. plicatilis has been also
used in basic research as a model organism. This is
due to a number of characteristics, listed in Table 1.
Population dynamics studies using the life-table ap-
proach have been numerous (Korstad et al., 1989;
Schmid-Araya, 1991; Serra et al., 1994; Yoshinaga et
al., 2000). Rotifers were among the first organisms to
be used in studies of biological aging (King, 1969;
Enesco, 1993). It has been recently argued that B. pli-
catilis could be potentially rewarding for aging re-
search (Austad, 2009). Brachionus plicatilis has been
studied in terms of its biochemistry, morphology, phy-
siology, as well as the molecular basis of aging (Lu-
ciani et al., 1983; Carmona et al., 1989; Yoshinaga et
al., 2003). Owing to its dual mode of reproduction, B.
plicatilis has been used as a bio-model regarding the
evolutionary significance of sex (e.g. Aparici et al.,
2002; Serra et al., 2004; Carmona et al., 2009). Its wi-
despread distribution has facilitated studies on cryp-
tic speciation (GÔ´mez & Snell, 1996; Serra et al.,
Venetia Kostopoulou et al. — Brachionus plicatilis: an emerging bio-tool for numerous applications 99
100 Venetia Kostopoulou et al. — Brachionus plicatilis: an emerging bio-tool for numerous applications
TABLE 1. Characteristics of the rotifer Brachionus plicatilis that make it an attractive candidate as a tool in numerous re-
search fields. References are for the listed characteristics
Characteristic
Ubiquity in aquatic systems
High growth rate compared to
other zooplankters
High ingestion rate
Adequate size for:
ñ feeding fish larvae
ñ culture in small (Ìl) volumes
Important role in energy flow and
nutrient cycling
Ease of culture
Short generation time
Ability to grow on a variety of
food sources (phytoplankton, bac-
teria, inert food)
Use as a “living capsule”, transfer-
ring administered substances to
recipient organism (predator)
Complex life cycle combining
asexual and sexual reproduction,
allowing for genetically identical
individuals (clones) as well as the
possibility of storage in the form
of cysts, which can be readily
available when needed
Resting egg production
Eutely
Transparency of body
Well-studied biology
Field
Cryptic speciation, Molecular phy-
logenetics, Ecotoxicology
Aquaculture, Basic biological re-
search
Aquaculture, Ecotoxicology
Aquaculture, Basic biological re-
search, Ecotoxicology
Ecology
Aquaculture, Basic biological re-
search, Ecotoxicology
Aquaculture, Basic biological re-
search, Ecotoxicology
Aquaculture, Basic biological re-
search
Aquaculture
Basic biological research, Evolu-
tionary ecology
Aquaculture, Ecology, Evolution-
ary ecology
Biology of development and aging
Biology of development and aging
All fields
References
Koste & Shiel (1980), Miracle &
Vicente (1983), Arndt (1988),
Green & Mengestou (1991),
Timms (1993), Turner (1993), Eg-
borge (1994), Modenutti (1998),
Zakaria et al. (2007)
Allan (1976)
Navarro (1999)
Lubzens et al. (2001)
Starkweather (1987), Armengol et
al. (2001), Wallace & Smith (2009)
Hoff & Snell (1987)
Korstad et al. (1989), Yoshinaga et
al. (2003)
Starkweather (1980), Lubzens et
al. (2001)
Lubzens et al. (2001)
Nogrady et al. (1993), Wallace &
Snell (1991)
Pourriot & Snell (1983)
Nogrady et al. (1993), Wallace
(2002)
Wallace (2002)
Ricci et al. (2000)
1997) and molecular phylogenetics (GÔ´mez et al.,
2002; Suatoni et al., 2006; Mills et al., 2007). Basic
knowledge on genomics is just emerging (Suga et al.,
2007, 2008; Montero-Pau & GÔ´mez, 2011). Rotifers
have been also considered as good indicators in eco-
toxicology (Sla´decˇek, 1983); standard methods have
been developed, that are rapid, sensitive, reliable, of
good repeatability and cost-effectiveness (Snell &
Persoone, 1989; Ferrando & Andrew-Moliner, 1992;
Moffat & Snell, 1995; Snell & Janssen, 1995; Del-
Valls et al., 1996, 1997).
Recently, it has been proposed that B. plicatilis
could be also used as model organism in evolutionary
developmental biology (evo-devo) (Boell & Bucher,
2008). This particular field aims at reconstructing
evolutionary relationships between animals going
back to the origins of bilateral symmetry. The phylo-
genetic position of rotifers lies within the Lophotro-
chozoans, which belong to the protostome branch of
Bilateria (Dunn et al., 2008). Most protostome model
systems belong to the Ecdysozoa branch, whereas Lo-
photrochozoans are underrepresented. In addition,
there is overrepresentation of segmented versus non-
segmented taxa (Boell & Bucher, 2008). Brachionus
plicatilis could therefore represent a suitable non-seg-
mented model organism, belonging to the Lopho-
trochozoans, for comparative analysis of gene expres-
sion.
It therefore becomes obvious that the rotifer B.
plicatilis is a very useful, but still unexplored tool for
numerous applications. Some of these are explored
below.
POTENTIAL APPLICATIONS
USING THE ROTIFER
BRACHIONUS PLICATILIS
Environmental management of eutrophication
Although the definition of eutrophication is still on
debate (Andersen et al., 2006), Nixon (1995) gave a
rather straightforward description: ‘an increase in the
rate of supply of organic matter to an ecosystem’. Eu-
trophication has been considered one of the major
threats to the health of marine ecosystems (e.g. Smith
et al., 2006). It is related to the input mainly of nitro-
gen and phosphorus and results in an increased growth
of algae, with direct consequences on water quality.
The latter have been well known and documented
(Cloern, 2001).
The control of algal growth in lakes can be at-
tained by bio-manipulation of food webs through pro-
cesses such as zooplankton grazing (top-down con-
trol) of algal biomass (Moss et al., 1994; Beklioglu,
1999; Schindler, 2006). To affect a dense phytoplank-
ton bloom significantly, a given organism must satis-
fy several requirements: it must be abundant, it must
coincide with algae both in space and time and it
must be able to feed on them efficiently (Calbet, 2008).
Rotifers have short developmental time, high filtra-
tion rate and can quickly reach high densities. In
comparison to other organisms, they are particularly
capable of locating and exploiting food patches until
depletion (Ignoffo et al., 2005). These characteristics
make B. plicatilis a potentially successful candidate in
the control of phytoplankton growth (eutrophication)
in brackish and marine coastal ecosystems. Rotifers
in general are considered good indicators of eutroph-
ication (Sla´decˇek, 1983; Park & Marshall, 2000; Tur-
ton & McAndrews, 2006; Zakaria et al., 2007) and B.
plicatilis in particular shows increased abundance when
conditions become eutrophic in nature (Arndt, 1988;
Gaudy et al., 1995; Haberman & Sudzuki, 1998; Za-
karia et al., 2007). Therefore, introduction of rotifers
into waters containing high concentrations of algae
may increase grazing pressure, resulting in a reduc-
tion of abnormally high levels of phytoplankton.
In the specific case of Harmful Algal Blooms
(HABs), rotifer short developmental times also con-
tribute to the appearance of resistant clones, able to
successfully graze upon such organisms (Calbet et al.,
2003). Brachionus plicatilis is able to feed on a variety
of phytoplankton species, including blue-green algae
(Snell et al., 1983). However, as demonstrated by Bu-
skey & Hyatt (1995), Turner & Tester (1997), Kim et
al. (2000) and Wang et al. (2005), such interactions
can be situation-specific. The dinoflagellate Karenia
mikimotoi and the raphidophyte Heterosigma akashi-
wo were both toxic to the rotifer B. plicatilis, which
showed distinct morphological changes and reduced
swimming speed upon contact (Xie et al., 2008; Zou
et al., 2010). On the other hand, successful biocontrol
by this rotifer was observed with the estuarine dino-
flagellate Pfiesteria piscicida and the dinoflagellate
Alexandrium tamarense (Mallin et al., 1995; Xie et al.,
2008). Nevertheless, it has not been tested yet whe-
ther the toxin remains viable in the gut of the rotifer
after consumption, leading to bioaccumulation (Mal-
lin et al., 1995). The rotifer B. plicatilis can be there-
fore used as a sensitive indicator and possibly, as a bi-
ological control tool in HABs, depending on species.
Venetia Kostopoulou et al. — Brachionus plicatilis: an emerging bio-tool for numerous applications 101
Environmental management of cholera
Eutrophication and harmful algal blooms may also
provide a reservoir for water-borne diseases, such as
cholera (Epstein, 1993). Vibrio cholerae, organism re-
sponsible for this disease, shows enhanced survival
and persistence when associated to algae and/or co-
pepods, relative to the surrounding water. The latter
organisms provide protection and nutrition to V. cho-
lerae, especially under unfavorable conditions (Hei-
delberg et al., 2002; Lipp et al., 2002). Therefore, in-
creased algal growth where V. cholera is present will
facilitate spread of cholera. Brachionus plicatilis could
prove useful in limiting the environmental dispersion
of the disease. Vibrio cholerae is naturally present in
warm, brackish waters (Lipp et al., 2002), where B.
plicatilis is also encountered. Indeed, Brachionus spe-
cies have been detected in areas where cholera is en-
demic (Tamplin et al., 1990). Freshwater rotifers have
been shown to ingest protozoan parasites that are
widely distributed in the aquatic environment (Fayer
et al., 2000; Trout et al., 2002; Nowosad et al., 2007).
It is not known whether B. plicatilis is also capable of
retaining V. cholerae, although bacterivory by this ro-
tifer is considered to be substantial (Turner & Tester,
1992). Still, indirect containment of V. cholerae through
consumption of phytoplankton could be an alternati-
ve strategy.
Environmental management of pollution
In the wider context of disturbance, pollution repre-
sents another field where rotifers could play a role. A
suitable indicator species should have certain attribu-
tes: it should be easily cultured in a small volume of
water, preferably without the occurrence of sexual
reproduction. In addition, the organism must react
clearly and death must be unequivocal (Sla´decˇek,
1983). Rotifers fulfill the abovementioned require-
ments. In nature, they are considered good indicators
of water quality (Sla´decˇek, 1983; Saksena, 1987). Bra-
chionus plicatilis in particular has been used in eco-
toxicological studies in the lab (Snell & Janssen, 1995),
as well as indicator species in the field (Sharma, 1983).
To go a step further, from detection to control,
organisms can be used to actually degrade or convert
environmental contaminants to innocuous end produ-
cts, a process known as bioremediation (Thassitou &
Arvanitoyannis, 2001). Algae and/or plants have been
used to successfully clean up hazardous waste (Gekel-
er et al., 1988; Ahner et al., 1995; Hitchcock et al.,
2003; Yoshida et al., 2009). However, concerns arise
as to the potential adverse effects of breakdown/
transformation products resulting from such process-
es (Hitchcock et al., 2003). In order to assess the im-
pact of phytoremediation products to higher trophic
levels, rotifers have been employed (Moreno-Garri-
do et al., 1999; Hitchcock et al., 2003; Rioboo et al.,
2007). In general, phytoremediation end products
had a negative influence of varying magnitude on ro-
tifers most of the times. Recovery was observed when
rotifers were returned to toxicant-free media (Rioboo
et al., 2007) or supplied with high food concentrations
(Luna-Andrade et al., 2002). Although algae have
been shown to be more resistant to toxicants than ro-
tifers (Luna-Andrade et al., 2002), observed changes
are not necessarily conclusive. For example, B. pli-
catilis shows high tolerance to i) insecticides (Serrano
et al., 1986; Snell & Persoone, 1989; Ferrando & An-
dreu-Moliner, 1991), ii) certain heavy metals (Per-
soone et al., 1989; Snell & Persoone, 1989; Snell et al.,
1991) and iii) petroleum compounds (Snell et al.,
1991; Ferrando & Andreu-Moliner, 1992). Under con-
ditions of ample food and reduced competition, bio-
merediation using rotifers can be further reinforced
to give optimal results (see Yasuno et al., 1993).
Environmental management of petroleum compounds
The tolerance of rotifers to petroleum compounds
could prove useful in the control of oil spills, espe-
cially in enclosed habitats, which are more prone than
the open ocean, due to reduced dilution capacity. Oil
spills usually cause an upsurge of microbial and plant
biomass, later to be followed by small zooplankton,
particularly rotifers (Johansson et al., 1980; Daven-
port et al., 1982; Linden et al., 1987). Brachionus pli-
catilis has been shown to actively accumulate hydro-
carbons; whether it is able to metabolize them has not
been tested yet, but remains a possibility (Echeverria,
1980; Wolfe et al., 1998). Perhaps more worrying than
episodic oil spills are the consequences arising from
the continuous presence of oil products, such as tar
balls, blobs of semi-solid oil, which are commonly en-
countered in enclosed seas associated with oil ex-
ploitation (Red Sea, Arabian Gulf, Mediterranean
Sea) (Morris, 1974; Davenport et al., 1982; Hanna,
1983; Holdway, 1986; Price & Nelson-Smith, 1986).
These balls are usually neutrally buoyant, may remain
in the water column for long periods and eventually
wash ashore coating shoreline sediment (Eagle et al.,
1979; Sen Gupta et al., 1993). Zooplankton is able to
graze upon particulate tar balls, providing in this way
102 Venetia Kostopoulou et al. — Brachionus plicatilis: an emerging bio-tool for numerous applications
a mechanism of rapid sedimentation to greater depths
through faecal pellets (Sleeter & Butler, 1982). Ro-
tifers, in particular, owing to their high ingestion rate,
could prove useful in the abatement of tar balls.
Wastewater treatment
Wastewater treatment is another area where rotifers
could play a leading role. Different systems are used
worldwide for the treatment of wastewater, such as
activated sludge, trickling filters and waste stabiliza-
tion ponds. Each of these systems operates on the
same fundamental biochemical principles (bacteria
are primarily used in pollutant removal) and differs
on the method of oxygen transfer (activated sludge
utilizes compressed air, trickling filters obtain their
oxygen by diffusion from the air and ponds use algae)
and source of wastes (activated sludge and trickling
filters are used in industrial wastes, whereas waste
ponds are used for domestic and agro-industrial wa-
stewaters) (McKinney, 1957; Patil et al., 1993; Roche,
1995; El-Deeb Ghazy et al., 2008). Freshwater rotifers
are encountered in activated sludge systems (Poole,
1984) and waste stabilization ponds (Patil et al., 1993;
Roche, 1995) and are (in a different way) instrumen-
tal in the functioning of both systems.
In the case of activated sludge systems, rotifers
can consume filamentous bacteria that create foam-
ing and bulking, as well as sludge particles themsel-
ves. In that way, they improve the settling properties
and clarity of sludge, as well as reduce biomass pro-
duction. Disposal of excess sludge is considered a ma-
jor bottleneck of wastewater treatment and rotifers
could therefore prove to be an economical and sustai-
nable solution to this problem (Lee & Welander, 1996;
Lapinski & Tunnacliffe, 2003; Fialkowska & Pajdak-
Stos, 2008). On the other hand, in waste stabilization
ponds, freshwater rotifers play an important role in
the purification of wastewater through the consump-
tion of dispersed or coagulated bacteria, organic mat-
ter and phytoplankton (Patil et al., 1993; Zhao &
Wang, 1996). It has been proposed that, owing to the
use of both algae and rotifers in aquaculture, the lat-
ter two organisms could be produced using waste-
water. This could become a low-cost alternative to ex-
pensive phytoplankton and rotifer culture and a way
to recycle nutrients. However, nutritional adequacy,
organic overloading and presence of pathogens will
have to be investigated (Uhlmann, 1980; Groeneweg
& Schluter, 1981; Roche, 1995; Cauchie et al., 2000;
Sarma et al., 2003).
Tracking climate change
Climate change is now recognized as one of the ma-
jor environmental problems facing the earth. The
burning of fossil fuels and deforestation have caused
an increase in the concentrations of heat-trapping
“greenhouse gases”, such as carbon dioxide (CO2)
and methane (CH4) in the atmosphere, resulting in
global warming (Chapin et al., 2000). Over the past
100 years, the Earth’s climate is warmed by approxi-
mately 0.6ÆC (Walther et al., 2002). These changes
are expected to trigger phenomena like sea level rise,
more frequent and intense extreme weather events
and ocean acidification, to mention a few. There is
growing evidence that climate change will contribute
to shifts in the geographic range of species, altera-
tions in the timing of important life-history events,
disruption of food webs (McCarthy, 2001; Root et al.,
2003; Richardson, 2008), even accelerated species
losses (Wrona et al., 2006). However, large uncer-
tainties remain in projecting species and system-spe-
cific responses. In addition, other stresses, in particu-
lar habitat destruction, but also increased susceptibil-
ity to pathogens and pests, could further exacerbate
the effects of climate change on organisms (Harvell et
al., 1999; McCarthy, 2001; Root et al., 2003).
Marine pelagic communities are said to be affect-
ed to a greater extent, compared to terrestrial com-
munities, because of the temperature influence on
water column stability (Edwards & Richardson, 2004;
Richardson, 2008) and the important role of the o-
cean in the uptake of anthropogenic CO2(Hays et al.,
2005; Fabry et al., 2008). Plankton in particular is con-
sidered a good indicator of climate change (Hays et
al., 2005; Richardson, 2008): (1) it is sensitive to tem-
perature changes as it is composed of ectothermic or-
ganisms, (2) it is not commercially exploited, (3) it is
short-lived, so past populations do not exert an influ-
ence on present ones, (4) it is free floating, so it can
show changes in its distribution in response to climate
change and (5) it is more sensitive than environmen-
tal variables themselves, as it can amplify subtle per-
turbations. It is therefore important to test the pro-
jected effects of global warming using a test organism
from the plankton community. Copepods have been
extensively studied, owing to their importance in the
open ocean (Richardson, 2008). However, the open
ocean, due to its size and permanence, has the capac-
ity to dampen out to a certain extent climatic fluctua-
tions. Ephemeral and extreme habitats are instead
more vulnerable to perturbations (Gaudy et al., 1995)
Venetia Kostopoulou et al. — Brachionus plicatilis: an emerging bio-tool for numerous applications 103
and should be more sensitive to climate change. They
could provide an early indication of the biological im-
pact of shifting climate. The importance of such habi-
tats also lies in their ecological value, as they are con-
sidered biodiversity hotspots (Walsh et al., 2008; An-
geler et al., 2010). Brachionus plicatilis is an inhabitant
of such habitats and could therefore serve as an indi-
cator r-type organism of climate change.
Can B. plicatilis track the effects of climate chan-
ge? Climate change is mainly manifested by a rise in
temperature, a decrease in pH, as a consequence of
acidification (Fabry et al., 2008) and drying of ephe-
meral habitats. Temperature has a direct effect on or-
ganisms. Rotifers are ectothermic organisms, so their
metabolism is directly exposed to the temperature of
their environment (Stelzer, 1998). Consequently, tem-
perature is the most important factor shaping the
population dynamics of rotifers (Galkovskaja, 1987;
Arndt, 1988; Miracle & Serra, 1989; Gaudy et al.,
1995). This is manifested by the seasonal component
that characterizes the occurrence of B. plicatilis in na-
ture (Walker, 1981; Miracle et al., 1987; Arndt, 1988;
Haberman & Sudzuki, 1998; Modenutti, 1998; Jelli-
son et al., 2001; Zakaria et al., 2007), which is expect-
ed to be affected by climate change. On the other
hand, temperature affects critical life cycle events
such as hatching of resting eggs (Pourriot & Snell,
1983), with direct consequences on the structuring of
food webs. It has been shown that differential hatch-
ing of resting eggs due to rising temperatures result-
ed in a selective advantage of rotifers over cladoce-
rans in freshwater ecosystems (Winder & Schindler,
2004; Dupuis & Hann, 2009). Therefore, B. plicatilis
offers the opportunity to study the direct as well as
the indirect effects of changing temperature.
Low pH values adversely affect survival, longevi-
ty, reproduction, Na+flux, growth rate, feeding and
respiration in zooplankton (Locke, 1991). Freshwater
rotifers have been shown to dominate zooplankton
communities in highly acidic lakes, due to their broad
pH tolerance (Berzins & Pejler, 1987; Frost et al.,
1998; Deneke, 2000). Brachionus plicatilis in particu-
lar has not received much attention as to its pH tol-
erance, although reported values cover the near neu-
tral- alkaline range (6.5-9.8) (Walker, 1981; Turner,
1993; Haberman & Sudzuki, 1998; Modenutti, 1998;
Ortells et al., 2000). Brachionus plicatilis is an inhabi-
tant of alkaline environments, so there is no available
information as to how this species will respond to
acidification. In the absence of field data, tolerance of
B. plicatilis to low pH could be experimentally mea-
sured, using indices such as swimming speed, respira-
tion and filtering rate (Epp & Winston, 1978; Locke,
1991).
Laboratory-derived data can be used to explain
observed distributions, but predictions cannot be
solely based on physiological rates. Other factors
should be taken into account, namely the overall cha-
racteristics of the changing environment or habitat
that the organism has moved to (Feder, 2010). It is
therefore crucial to follow B. plicatilis distribution in
the field and to compare it with past records, in order
to be able to discern the influence of climate change.
Being a well-studied species, it is possible to find
long-term studies on the distribution of B. plicatilis
(Sharma, 1983; De Ridder, 1987). However, due to
its recently revised taxonomic status, some data on
past distributions could correspond to other species
of the complex. To go further back in time, the rest-
ing egg bank can provide a snapshot from the past
(Montero-Pau et al., 2011).
Resting egg banks are formed and replenished
every time a population appears in the water column
and completes one “growing cycle”, usually on a year-
ly basis. The B. plicatilis is an ancient species complex
(Go´mez et al., 2002; Derry et al., 2003; Suatoni et al.,
2006), and, over the years, its occurrence has left its
mark in the sediments (Pourriot & Snell, 1983; Go´-
mez & Carvalho, 2000; Ortells et al., 2000; García-
Roger et al., 2006a). Hatching of resting eggs is feasi-
ble after the lapse of considerable time spans (Mar-
cus et al., 1994; Kotani et al., 2001; García-Roger et
al., 2006b). So, the accumulated biotic diversity stored
in resting egg banks, can serve as an indication of past
populations/climates, which can be compared to pre-
sent ones (Montero-Pau et al., 2011).
Last but not least, is the threat of extinction, stem-
ming from potential drying of ephemeral habitats,
like the ones B. plicatilis inhabits. Although resting
egg banks have the capacity to buffer transient envi-
ronmental perturbations (Hairston, 1996; Serra et al.,
2004), permanent changes cannot be overcome. A ro-
tifer population experiencing three catastrophic cra-
shes per year is certain to go extinct within 100 years
(Snell & Serra, 2000). In addition, sexual reproduc-
tion, which ensures resting egg production and long-
term survival, could be more susceptible to environ-
mental change than parthenogenesis, due to its in-
creased complexity. Sexual reproduction needs a lon-
ger time to complete, is more resource-demanding
and is more sensitive to external influences (Snell &
Boyer, 1988; Snell & Carmona, 1995; Serra et al.,
104 Venetia Kostopoulou et al. — Brachionus plicatilis: an emerging bio-tool for numerous applications
2004), in part due to its reliance on chemical commu-
nication (Snell et al., 2006).
Transfer of useful substances
The rotifer B. plicatilis is a high-value, but nutrition-
ally inadequate, prey for fish larvae, due to its lack of
essential HUFAs (Highly Unsaturated Fatty Acids).
This is why enrichment protocols have been devised
that allow the transfer of required substances, mainly
HUFAs, to fish larvae (Rainuzzo et al., 1994a; Ro-
driguez et al., 1998; Castell et al., 2003). Transfer of
HUFAs via rotifers has been shown to improve growth,
survival and total length in gilthead seabream larvae
(Rodriguez et al., 1994, 1998), pigmentation in turbot
larvae (Rainuzzo et al., 1994b), survival and incidence
of deformities in milkfish (Gapasin & Duray, 2001),
size and survival in yellowtail flounder (Copeman et
al., 2002), among others. The transfer of vitamins and
therapeutics has been also realized (Verpraet et al.,
1992; Merchie et al., 1995; Fernandez et al., 2008;
Roiha et al., 2011). Vitamin C significantly improved
stress resistance in European sea bass, whereas vita-
min A has been implicated in gilthead sea bream ske-
letogenesis. In accordance with the present use of ro-
tifers in aquaculture, B. plicatilis can be used as a
‘transfer capsule’ of desirable substances to target or-
ganisms.
Interest has also turned towards the possible in-
fluence of bacteria on disease resistance. Techniques
have been developed that allow the transfer of bene-
ficial bacteria (probiotics), as well as immunostimu-
lants, to fish larvae, through the rotifer B. plicatilis
(Skjermo & Vadstein, 1999; Makridis et al., 2000;
Martínez-Díaz et al., 2003; Pintado et al., 2010). For
example, probiotics have been shown to improve sur-
vival rate in turbot larvae challenged with Vibrio
(53% survival rate versus 8% for the control group
without probiotics as reported by Gatesoupe, 1994)
(Planas et al., 2006), survival (13-105% higher com-
pared to control) and specific growth rate (2-9%
higher compared to control) in gilthead sea bream
larvae and fry (Carnevali et al., 2004; Suzer et al.,
2008), body weight (81% with respect to control) and
tolerance to captive rearing conditions in European
sea bass juveniles (Carnevali et al., 2006). A promis-
ing area of developing research focuses on axenic ro-
tifers (gnotobiotic), which can be used as an experi-
mental in vivo system for the study of host-microbe
interactions, nutritional functions in aquatic food
chains, even evaluation of new treatments of disease
control (Tinh et al., 2006, 2007; Marques et al., 2006).
The abovementioned techniques that have been de-
veloped for aquaculture could also find applications
in other fields. In this procedure, the rotifer B. pli-
catilis could play a leading role.
CONCLUSIONS
As proposed in the present paper, the rotifer Brachio-
nus plicatilis could serve a number of possible appli-
cations. This is why initiatives should be taken as to
the study, buffering capacity and preservation of this
species complex already having many applications
(aquaculture, water quality indicator, model organ-
ism in basic research). The creation of a rotifer bank
(i.e. ex situ storage of rotifers and/or their resting eggs)
could serve such a purpose.
The proposed rotifer bank would constitute of ro-
tifer strains originating from the field and mass pro-
duction (hatcheries). These rotifer strains would be
characterized as to their taxonomic status and bio-
logical characteristics. All this information could be
used in favor of mass production: hatcheries could be
supplied with rotifers that best fit their needs. In this
way, the rotifer bank would improve the operation
and production of hatcheries. On a second level, it
would contribute to the conservation of biodiversity
and serve the advancement of science. Numerous ap-
plications are waiting to be realized in the future.
REFERENCES
Allan JD, 1976. Life history patterns in zooplankton. Ame-
rican Naturalist, 110: 165-180.
Andersen JH, Schlüter L, ^rtebjerg G, 2006. Coastal eu-
trophication: recent developments in definitions and
implications for monitoring strategies. Journal of Plank-
ton Research, 28: 621-628.
Angeler DG, Alvarez-Cobelas M, Sanchez-Carrillo S, 2010.
Evaluating environmental conditions of a temporary
pond complex using rotifer emergence from dry soils.
Ecological Indicators, 10: 545-549.
Ahner BA, Kong S, Morel FMM, 1995. Phytochelatin pro-
duction in marine algae. 1. An interspecies comparison.
Limnology and Oceanography, 40: 649-657.
Aparici E, Carmona MJ, Serra M, 2002. Evidence for an
even sex allocation in haplodiploid cyclical partheno-
gens. Journal of Evolutionary Biology, 15: 65-73.
Armengol X, Boronat L, Camacho A, Wurtsbaugh WA,
2001. Grazing by a dominant rotifer Conochilus unicor-
nis Rousselet in a mountain lake: in situ measurements
with synthetic microspheres. Hydrobiologia, 446/447:
107-114.
Venetia Kostopoulou et al. — Brachionus plicatilis: an emerging bio-tool for numerous applications 105
Arndt H, 1988. Dynamics and production of a natural po-
pulation of Brachionus plicatilis (Rotatoria, Monogono-
nta) in a eutrophicated inner coastal water of the Bal-
tic. Kieler Meeresforschungen Sonderheft, 6: 147-153.
Arndt H, 1993. Rotifers as predators on components of the
microbial web (bacteria, heterotrophic flagellates, cili-
ates) – a review. Hydrobiologia, 255/256: 231-246.
Austad SN, 2009. Is there a role for new invertebrate mod-
els for aging research? Journal of Gerontology: Biologi-
cal Sciences, 64A: 192-194.
Beklioglu M, 1999. A review on the control of eutrophica-
tion in deep and shallow lakes. Turkish Journal of Zoolo-
gy, 23: 327-336.
Bennett WN, Boraas ME, 1989. A demographic profile of
the fastest growing metazoan: a strain of Brachionus ca-
lyciflorus (Rotifera). Oikos, 55: 365-369.
Berzins B, Pejler B, 1987. Rotifer occurrence in relation to
pH. Hydrobiologia, 147: 107-116.
Boell LA, Bucher G, 2008. Whole-mount in situ hybridiza-
tion in the rotifer Brachionus plicatilis representing a
basal branch of lophotrochozoans. Development Genes
and Evolution, 218: 445-451.
Buskey EJ, Hyatt CJ, 1995. Effects of the Texas (USA)
‘brown tide’ alga on planktonic grazers. Marine Ecology
Progress Series, 126: 285-292.
Calbet A, 2008. The trophic roles of microzooplankton in
marine systems. ICES Journal of Marine Science, 65:
325-331.
Calbet A, Vaqué D, Felipe J, Vila M, Montserrat Sala M,
Alcaraz M, Estrada M, 2003. Relative grazing impact of
microzooplankton and mesozooplankton on a bloom of
the toxic dinoflagellate Alexandrium minutum. Marine
Ecology Progress Series, 259: 303-309.
Carmona MJ, Serra M, Miracle MR, 1989. Protein patterns
in rotifers: the timing of aging. Hydrobiologia, 186/187:
325-330.
Carmona MJ, Serra M, Miracle MR, 1993. Relationships
between mixis in Brachionus plicatilis and precondition-
ing of culture medium by crowding. Hydrobiologia, 256/
257: 145-152.
Carmona MJ, Dimas-Flores N, García-Roger EM, Serra
M, 2009. Selection of low investment in sex in a cycli-
cally parthenogenetic rotifer. Journal of Evolutionary Bi-
ology, 22: 1975-1983.
Carnevali O, Zamponi MC, Sulpizio R, Rollo A, Nardi M,
Orpianesi C, Silvi S, Caggiano M, Polzonetti AM, Cre-
sci A, 2004. Administration of probiotic strain to im-
prove sea bream wellness during development. Aqua-
culture International, 12: 377-386.
Carnevali O, de Vivo L, Sulpizio R, Gioacchini G, Olivot-
to I, Silvi S, Cresci A, 2006. Growth improvement by
probiotic in European sea bass juveniles (Dicentrarchus
labrax, L.), with particular attention to IGF-1, myo-
statin and cortisol gene expression. Aquaculture, 258:
430-438.
Castell J, Blair T, Neil S, Howes K, Mercer S, Reid J,
Young-Lai W, Gullison B, Dhert P, Sorgeloos P, 2003.
The effect of different HUFA enrichment emulsions on
the nutritional value of rotifers (Brachionus plicatilis)
fed to larval haddock (Melanogrammus aeglefinus). A-
quaculture International, 11: 109-117.
Cauchie H-M, Hoffmann L, Thomé J-P, 2000. Metazoo-
plankton dynamics and secondary production of Daph-
nia magna (Crustacea) in an aerated waste stabilization
pond. Journal of Plankton Research, 22: 2263-2287.
Cavalier-Smith T, 1978. Nuclear volume control by nucle-
oskeletal DNA, selection of cell volume and cell growth
rate, and the solution of the DNA C-value paradox.
Journal of Cell Science, 34: 247-278.
Chapin FS III, Zavaleta ES, Eviner VT, Naylor RL, Vi-
tousek PM, Reynolds HL, Hooper DU, Lavorel S, Sala
OE, Hobbie SE, et al., 2000. Consequences of changing
biodiversity. Nature, 405: 234-242.
Ciros-Pérez J, Go´mez A, Serra M, 2001. On the taxonomy
of three sympatric sibling species of the Brachionus pli-
catilis (Rotifera) complex from Spain, with the descrip-
tion of B. ibericus n. sp. Journal of Plankton Research,
23: 1311-1328.
Cloern JE, 2001. Our evolving conceptual model of the
coastal eutrophication problem. Marine Ecology Pro-
gress Series, 210: 223-253.
Copeman LA, Parrish CC, Brown JA, Harel M, 2002. Ef-
fects of docosahexaenoic, eicosapentaenoic, and arachi-
donic acids on the early growth, survival, lipid compo-
sition and pigmentation of yellowtail flounder (Liman-
da ferruginea): a live food enrichment experiment. A-
quaculture, 210: 285-304.
Davenport J, Angel MV, Gray JS, Crisp DJ, Davies JM,
1982. Oil and planktonic ecosystems [and discussion].
Philisophical Transactions of the Royal Society of Lon-
don Series B, 297: 369-384.
De Ridder M, 1987. Distribution of rotifers in African fresh
and inland saline waters. Hydrobiologia, 147: 9-14.
DelValls TA, Lubia´n LM, Gonza´lez del Valle M, Forja JM,
1996. Evaluating decline parameters of rotifer Bra-
chionus plicatilis populations as an interstitial water tox-
icity bioassay. Hydrobiologia, 341: 159-167.
DelValls TA, Lubian LM, Forja JM, Gomez-Parra A, 1997.
Comparative ecotoxicity of interstitial waters in littoral
ecosystems using Microtox®and the rotifer Brachionus
plicatilis. Environmental Toxicology and Chemistry, 16:
2323-2332.
Deneke R, 2000. Review of rotifers and crustaceans in
highly acidic environments of pH values ≤3. Hydrobio-
logia, 433: 167-172.
Derry AM, Hebert PDN, Prepas EE, 2003. Evolution of ro-
tifers in saline and subsaline lakes: A molecular phylo-
genetic approach. Limnology and Oceanography, 48:
675-685.
Dooms S, Papakostas S, Hoffman S, Delbare D, Dierckens
106 Venetia Kostopoulou et al. — Brachionus plicatilis: an emerging bio-tool for numerous applications
K, Triantafyllidis A, De Wolf T, Vadstein O, Abatzo-
poulos TJ, Sorgeloos P, Bossier P, 2007. Denaturing
Gradient Gel Electrophoresis (DGGE) as a tool for the
characterization of Brachionus sp. strains. Aquaculture,
262: 29-40.
Dunn CS, Hejnol A, Matus DQ, Pang K, Browne WE,
Smith SA, Seaver E, Rouse GW, Obst M, Edgecombe
G, et al., 2008. Broad phylogenomic sampling improves
resolution of the animal tree of life. Nature, 452: 745-
749.
Dupuis AP, Hann BJ, 2009. Climate change, diapause ter-
mination and zooplankton population dynamics: an ex-
perimental and modelling approach. Freshwater Biolo-
gy, 54: 221-235.
Eagle GA, Green A, Williams J, 1979. Tar ball concentra-
tions in the ocean around the Cape of Good Hope be-
fore and after a major oil spill. Marine Pollution Bul-
letin, 10: 321-325.
Echeverria T, 1980. Accumulation of 14C labeled benzene
and related compounds in the rotifer Brachionus pli-
catilis from seawater. Canadian Journal of Fisheries and
Aquatic Sciences, 37: 738-741.
Edwards M, Richardson AJ, 2004. Impact of climate chan-
ge on marine pelagic phenology and trophic mismatch.
Nature, 430: 881-884.
Egborge ABM, 1994. Salinity and the distribution of ro-
tifers in the Lagos Harbour-Badagry Creek system, Ni-
geria. Hydrobiologia, 272: 95-104.
El-Deeb Ghazy MM, El-Senousy WM, Abdel-Aatty AM,
Kamel M, 2008. Performance evaluation of a waste sta-
bilization pond in a rural area in Egypt. American Jour-
nal of Environmental Sciences, 4: 316-325.
Enesco HE, 1993. Rotifers in aging research: use of rotifers
to test various theories of aging. Hydrobiologia, 255/256:
59-70.
Epp RW, Winston PW, 1977. Osmotic regulation in the
brackish-water rotifer Brachionus plicatilis (Müller).
Journal of Experimental Biology, 68: 151-156.
Epp RW, Winston PW, 1978. The effects of salinity and pH
on the activity and oxygen consumption of Brachionus
plicatilis (Rotatoria). Comparative Biochemistry and Phy-
siology, 59A: 9-12.
Epp RW, Lewis WM Jr, 1979. Sexual dimorphism in Bra-
chionus plicatilis (Rotifera): evolutionary and adaptive
significance. Evolution, 33: 919-928.
Epstein PR, 1993. Algal blooms in the spread and persis-
tence of cholera. BioSystems, 31: 209-221.
Esparcia A, Miracle MR, Serra M, 1989. Brachionus pli-
catilis tolerance to low oxygen concentrations. Hydrobi-
ologia, 186/187: 331-337.
Fabry VJ, Seibel BA, Feely RA, Orr JC, 2008. Impacts of
ocean acidification on marine fauna and ecosystem pro-
cesses. ICES Journal of Marine Science, 65: 414-432.
Fayer R, Trout JM, Walsh E, Cole R, 2000. Rotifers ingest
oocysts of Cryptosporidium parvum. Journal of Eukary-
otic Microbiology, 47: 161-163.
Feder ME, 2010. Physiology and global climate change. An-
nual Review of Physiology, 72: 123-125.
Ferna´ndez I, Hontoria F, Ortiz-Delgado JB, Kotzamanis Y,
Estévez A, Zambonino-Infante JL, Gisbert E, 2008.
Larval performance and skeletal deformities in farmed
gilthead sea bream (Sparus aurata) fed with graded
levels of Vitamin A enriched rotifers (Brachionus plica-
tilis). Aquaculture, 283: 102-115.
Ferrando MD, Andreu-Moliner E, 1991. Acute lethal toxi-
city of some pesticides to Brachionus calyciflorus and
Brachionus plicatilis. Bulletin of Environmental Contam-
ination and Toxicology, 47: 479-484.
Ferrando MD, Andreu-Moliner E, 1992. Acute toxicity of
toluene, hexane, xylene, and benzene to the rotifers
Brachionus calyciflorus and Brachionus plicatilis. Bulletin
of Environmental Contamination and Toxicology, 49:
266-271.
Fialkowska E, Pajdak-Sto´s A, 2008. The role of Lecane ro-
tifers in activated sludge bulking control. Water Re-
search, 42: 2483-2490.
Frost TM, Montz PK, Gonzalez MJ, Sanderson BL, Arnott
SE, 1998. Rotifer responses to increased acidity: long-
term patterns during the experimental manipulation of
Little Rock Lake. Hydrobiologia, 387/388: 141-152.
Galkovskaja GA, 1987. Planktonic rotifers and temperatu-
re. Hydrobiologia, 147: 307-317.
Gapasin RSJ, Duray MN, 2001. Effects of DHA-enriched
live food on growth, survival and incidence of opercu-
lar deformities in milkfish (Chanos chanos). Aquacultu-
re, 193: 49-63.
García-Roger EM, Carmona MJ, Serra M, 2006a. Patterns
in rotifer diapausing egg banks: density and viability.
Journal of Experimental Marine Biology and Ecology,
336: 198-210.
García-Roger EM, Carmona MJ, Serra M, 2006b. Hatch-
ing and viability of rotifer diapausing eggs collected
from pond sediments. Freshwater Biology, 51: 1351-1358.
Gatesoupe FJ, 1994. Lactic acid bacteria increase the resis-
tance of turbot larvae, Scophthalmus maximus, against
pathogenic vibrio. Aquatic Living Resources, 7: 277-282.
Gaudy R, Verriopoulos G, Cervetto G, 1995. Space and
time distribution of zooplankton in a Mediterranean la-
goon (Etang de Berre). Hydrobiologia, 300/301: 219-236.
Gekeler W, Grill E, Winnacker E-L, Zenk MH, 1988. Al-
gae sequester heavy metals via synthesis of phytochela-
tin complexes. Archives of Microbiology, 150: 197-202.
Gerritsen J, 1980. Sex and parthenogenesis in sparse popu-
lations. American Naturalist, 115: 718-742.
Gilbert JJ, 1974. Dormancy in rotifers. Transactions of the
American Microscopical Society, 93: 490-513.
Gilbert JJ, 2004. Population density, sexual reproduction
and diapause in monogonont rotifers: new data for Bra-
chionus and a review. Journal of Limnology, 63: 32-36.
Go´mez A, Snell TW, 1996. Sibling species and cryptic spe-
Venetia Kostopoulou et al. — Brachionus plicatilis: an emerging bio-tool for numerous applications 107
ciation in the Brachionus plicatilis species complex (Ro-
tifera). Journal of Evolutionary Biology, 9: 953-964.
Go´mez A, Carvalho GR, 2000. Sex, parthenogenesis and
genetic structure of rotifers: microsatellite analysis of
contemporary and resting egg bank populations. Mole-
cular Ecology, 9: 203-214.
Go´mez A, Temprano M, Serra M, 1995. Ecological genetics
of a cyclical parthenogen in temporary habitats. Journal
of Evolutionary Biology, 8: 601-622.
Go´mez A, Serra M, Carvalho GR, Lunt DH, 2002. Specia-
tion in ancient cryptic species complexes: evidence
from the molecular phylogeny of Brachionus plicatilis
(Rotifera). Evolution, 56: 1431-1444.
Green J, Mengestou S, 1991. Specific diversity and commu-
nity structure of Rotifera in a salinity series of Ethiopi-
an inland waters. Hydrobiologia, 209: 95-106.
Groeneweg J, Schluter M, 1981. Mass production of fresh-
water rotifers on liquid wastes II. Mass production of
Brachionus rubens Ehrenberg 1838 in the effluent of
high-rate algal ponds used for the treatment of piggery
waste. Aquaculture, 25: 25-33.
Haberman J, Sudzuki M, 1998. Some notes on Brachionus
rotundiformis (Tschugunoff) in Lake Palaeostomi. Hy-
drobiologia, 387/388: 333-340.
Hairston NGJr, 1996. Zooplankton egg banks as biotic re-
servoirs in changing environments. Limnology and Oce-
anography, 41: 1087-1092.
Hanna RGM, 1983. Oil pollution on the Egyptian Red Sea
coast. Marine Pollution Bulletin, 14: 268-271.
Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstein
PR, Grimes DJ, Hofmann EE, Lipp EK, Osterhaus
ADME, Overstreet RM, et al., 1999. Emerging marine
diseases – Climate links and anthropogenic factors. Scien-
ce, 285: 1505-1510.
Hays GC, Richardson AJ, Robinson C, 2005. Climate chan-
ge and marine plankton. Trends in Ecology and Evolu-
tion, 20: 337-344.
Heidelberg JF, Heidelberg KB,Colwell RR, 2002. Bacteria
of the Á-subclass Proteobacteria associated with zoo-
plankton in Chesapeake Bay. Applied and Environmen-
tal Microbiology, 68: 5498-5507.
Hirata H, 1980. Culture methods of the marine rotifer, Bra-
chionus plicatilis. Mini Review and Data File of Fisheries
Research, 1: 27-46.
Hitchcock DR, McCutcheon SC, Smith MC, 2003. Using
rotifer population demographic parameters to assess
impacts on the degradation products from trinitrotolu-
ene phytoremediation. Ecotoxicology and Environmen-
tal Safety, 55: 143-151.
Hoff FH, Snell TW, 1987. Plankton culture manual. 3rd edi-
tion. Florida Aquafarms Inc., Dade City, FL.
Holdway P, 1986. A circumnavigational survey of marine
tar. Marine Pollution Bulletin, 17: 374-377.
Ignoffo TR, Bollens SM, Bochdansky AB, 2005. The effects
of thin layers on the vertical distribution of the rotifer,
Brachionus plicatilis. Journal of Experimental Marine Bi-
ology and Ecology, 316: 167-181.
Jellison R, Adams H, Melack JM, 2001. Re-appearance of
rotifers in hypersaline Mono Lake, California, during a
period of rising lake levels and decreasing salinity. Hy-
drobiologia, 466: 39-43.
Johansson S, Larsson U, Boehm P, 1980. The Tsesis oil
spill – Impact on the pelagic ecosystem. Marine Pollu-
tion Bulletin, 11: 284-293.
Kim D, Sato Y, Oda T, Muramatsu T, Matsuyama Y, Hon-
jo T, 2000. Specific toxic effect of dinoflagellate Hete-
rocapsa circularisquama on the rotifer Brachionus plica-
tilis. Bioscience, Biotechnology and Biochemistry, 64:
2719-2722.
King CE, 1969. Experimental studies of ageing in rotifers.
Experimental Gerontology, 4: 63-79.
Korstad J, Olsen Y, Vadstein O, 1989. Life history charac-
teristics of Brachionus plicatilis (rotifera) fed different
algae. Hydrobiologia, 186/187: 43-50.
Koste W, Shiel RJ, 1980. Preliminary remarks on the cha-
racteristics of the rotifer fauna of Australia (Notogaea).
Hydrobiologia, 73: 221-227.
Kotani T, Ozaki M, Matsuoka K, Snell TW, Hagiwara A,
2001. Reproductive isolation among geographically and
temporally isolated marine Brachionus strains. Hydro-
biologia, 446/447: 283-290.
Lapinski J, Tunnacliffe A, 2003. Reduction of suspended
biomass in municipal wastewater using bdelloid roti-
fers. Water Research, 37: 2027-2034.
Lee NM, Welander T, 1996. Use of protozoa and metazoa
for decreasing sludge production in aerobic wastewater
treatment. Biotechnology Letters, 18: 429-434.
Linden O, Rosemarin A, Lindskog A, Hoglund C, Johans-
son S, 1987. Effects of oil and oil dispersant on an en-
closed marine ecosystem. Environmental Science and
Technology, 21: 374-382.
Lipp EK, Huq A, Colwell RR, 2002. Effects of global cli-
mate on infectious disease: the cholera model. Clinical
Microbiology Reviews, 15: 757-770.
Locke A, 1991. Zooplankton responses to acidification: a
review of laboratory bioassays. Water, Air, and Soil Pol-
lution, 60: 135-148.
Lubzens E, 1987. Raising rotifer for use in aquaculture. Hy-
drobiologia, 147: 245-255.
Lubzens E, Zmora O, Barr Y, 2001. Biotechnology and
aquaculture of rotifers. Hydrobiologia, 446/447: 337-353.
Luciani A, Chasse J-L, Clement P, 1983. Aging in Brachio-
nus plicatilis: the evolution of swimming as a function of
age at two different calcium concentrations. Hydrobi-
ologia, 104: 141-146.
Luna-Andrade A, Aguilar-Duran R, Nandini S, Sarma SSS,
2002. Combined effects of copper and microalgal (Te-
traselmis suecica) concentrations on the population
growth of Brachionus plicatilis Muller (Rotifera). Water,
Air, and Soil Pollution, 141: 143-153.
108 Venetia Kostopoulou et al. — Brachionus plicatilis: an emerging bio-tool for numerous applications
Makridis P, Fjellheim AJ, Skjermo J, Vadstein O, 2000.
Control of the bacterial flora of Brachionus plicatilis
and Artemia franciscana by incubation in bacterial sus-
pensions. Aquaculture, 185: 207-218.
Mallin MA, Burkholder JM, Larsen LM, Glasgow HB Jr,
1995. Response of two zooplankton grazers to an ich-
thyotoxic estuarine dinoflagellate. Journal of Plankton
Research, 17: 351-363.
Marcus NH, Lutz R, Burnett W, Cable P, 1994. Age, viabi-
lity, and vertical distribution of zooplankton resting
eggs from an anoxic basin: evidence of an egg bank. Li-
mnology and Oceanography, 39: 154-158.
Marques A, Ollevier F, Verstraete W, Sorgeloos P, Bossier
P, 2006. Gnotobiotically grown aquatic animals: oppor-
tunities to investigate host-microbe interactions. Jour-
nal of Applied Microbiology, 100: 903-918.
Martínez-Díaz SF, A
´lvarez-Gonza´lez CA, Legorreta MM,
Va´squez-Jua´rez R, Barrios-Gonza´lez J, 2003. Elimina-
tion of the associated microbial community and bioen-
capsulation of bacteria in the rotifer Brachionus plicati-
lis. Aquaculture International, 11: 95-108.
McCarthy JP, 2001. Ecological consequences of recent cli-
mate change. Conservation Biology, 15: 320-331.
McKinney RE, 1957. Activity of microorganisms in organic
waste disposal. II. Aerobic processes. Applied and En-
vironmental Microbiology, 5: 167-174.
Merchie G, Lavens P, Dhert P, Pector R, Mai Soni AF,
Nelis H, Ollevier F, De Leenheer A, Sorgeloos P, 1995.
Live food mediated vitamin C transfer to Dicentrarchus
labrax and Clarias gariepinus.Journal of Applied Ichthy-
ology, 11: 336-341.
Mills S, Lunt DH, Go´mez A, 2007. Global isolation by dis-
tance despite strong regional phylogeography in a small
metazoan. BMC Evolutionary Biology, 7: 225-235.
Miracle MR, Vicente E, 1983. Vertical distribution and ro-
tifer concentrations in the chemocline of meromictic
lakes. Hydrobiologia, 104: 259-267.
Miracle MR, Serra M, 1989. Salinity and temperature in-
fluence in rotifer life history characteristics. Hydrobio-
logia, 186/187: 81-102.
Miracle MR, Serra M, Vicente E, Blanco C, 1987. Distribu-
tion of Brachionus species in Spanish mediterranean
wetlands. Hydrobiologia, 147: 75-81.
Miracle MR, Serra M, Oltra R, Vicente E, 1988. Differen-
tial distributions of Brachionus species in three coastal
lagoons. Verhandlungen der Internationalen Vereinigung
für Theoretische und Angewandte Limnologie, 23: 2006-
2015.
Modenutti BE, 1998. Planktonic rotifers of Samborombo´n
River Basin (Argentina). Hydrobiologia, 387/388: 259-
265.
Moffat BD, Snell TW, 1995. Rapid toxicity assessment us-
ing an in vivo enzyme test for Brachionus plicatilis (Ro-
tifera). Ecotoxicology and Environmental Safety, 30: 47-
53.
Montero-Pau J, Go´mez A, 2011. Development of genomic
resources for the phylogenetic analysis of the Brachio-
nus plicatilis species complex (Rotifera: Monogononta).
Hydrobiologia, 662: 43-50.
Montero-Pau J, Rasmos-Pérez E, Serra M, Go´mez A, 2011.
Long-term coexistence of rotifer cryptic species. PLOS
One, 6: e21530
Moreno-Garrido I, Lubian LM, Soares AMVM, 1999. In
vitro populations of rotifer Brachionus plicatilis Müller
demonstrate inhibition when fed with copper-preaccu-
mulating microalgae. Ecotoxicology and Environmental
Safety, 44: 220-225.
Morris RJ, 1974. Lipid composition of surface films and
zooplankton from the Eastern Mediterranean. Marine
Pollution Bulletin, 5: 105-109.
Moss B, McGowan S, Carvalho L, 1994. Determination of
phytoplankton crops by top-down and bottom-up me-
chanisms in a group of English lakes, the West Midland
Meres. Limnology and Oceanography, 39: 1020-1029.
Müller OF, 1786. Animalcula infusoria fluviatilia et mari-
na, quae defexit, systematice descripsit et ad vivum de-
lineari curavit… sistit opus hoc posthumum quod cum
tabulis aeneis L. in lucern tradit vidua ejus nobilissima,
cura Othonis Fabricii. Hauniae; I-LVI + 1-367.
Navarro N, 1999. Feeding behaviour of the rotifers Bra-
chionus plicatilis and Brachionus rotundiformis with two
types of food: live and freeze-dried microalgae. Journal
of Experimental Marine Biology and Ecology, 237: 75-87.
Nixon SW, 1995. Coastal marine eutrophication: a defini-
tion, social causes, and future concerns. Ophelia, 41:
199-219.
Nogrady T, Wallace RL, Snell TW, 1993. Rotifera, Volume
1: Biology, Ecology and Systematics. In: Dumont HJF,
ed. Guides to the identification of the microinvertebrates
of the continental waters of the world, Vol. 4. SPB Acad-
emic Publishing, The Hague, The Netherlands: 142.
Nowosad P, Kuczyn´ska-Kippen N, S≥odkowicz-Kowalska
A, Majewska AC, Graczyk TK, 2007. The use of roti-
fers in detecting protozoan parasite infections in recre-
ational lakes. Aquatic Ecology, 41: 47-54.
Ortells R, Snell TW, Go´mez A, Serra M, 2000. Patterns of
genetic differentiation in resting egg banks of a rotifer
species complex in Spain. Archiv für Hydrobiologie, 149:
529-551.
Ortells R, Go´mez A, Serra M, 2003. Coexistence of cryptic
rotifer species: ecological and genetic characterization
of Brachionus plicatilis. Freshwater Biology, 48: 2194-
2202.
Papakostas S, Triantafyllidis A, Kappas I, Abatzopoulos
TJ, 2005. The utility of the 16S gene in investigating
cryptic speciation within the Brachionus plicatilis spe-
cies complex. Marine Biology, 147: 1129-1139.
Papakostas S, Dooms S, Christodoulou M, Triantafyllidis
A, Kappas I, Dierckens K, Bossier P, Sorgeloos P, Aba-
tzopoulos TJ, 2006a. Identification of cultured Brachi-
Venetia Kostopoulou et al. — Brachionus plicatilis: an emerging bio-tool for numerous applications 109
onus rotifers based on RFLP and SSCP screening. Ma-
rine Biotechnology, 8: 547-559.
Papakostas S, Dooms S, Triantafyllidis A, Deloof D, Kap-
pas I, Dierckens K, De Wolf T, Bossier P, Vadstein O,
Kui S, et al., 2006b. Evaluation of DNA methodologies
in identifying Brachionus species used in European
hatcheries. Aquaculture, 255: 557-564.
Papakostas S, Triantafyllidis A, Kappas I, Abatzopoulos
TJ, 2009. Clonal composition of Brachionus plicatilis s.s.
and B. sp. ‘Austria’ hatchery strains based on microsa-
tellite data. Aquaculture, 296: 15-20.
Park GS, Marshall HG, 2000. Estuarine relationships be-
tween zooplankton community structure and trophic
gradients. Journal of Plankton Research, 22: 121-135.
Patil HS, Meti GM, Hosetti BB, 1993. Biology of multi cell
ponds treating municipal wastes. Internationale Revue
der gesamten Hydrobiologie, 78: 309-317.
Pejler B, 1995. Relation to habitat in rotifers. Hydrobiolo-
gia, 313/314: 267-278.
Persoone G, Van de Vel A, Van Steertegem M, De Nayer
B, 1989. Predictive value of laboratory tests with aquatic
invertebrates: influence of experimental conditions.
Aquatic Toxicology, 14: 149-166.
Pintado J, Pérez-Lorenzo M, Luna-Gonza´lez A, Sotelo
CG, Prol MJ, Planas M, 2010. Monitoring of the bioen-
capsulation of a probiotic Phaeobacter strain in the ro-
tifer Brachionus plicatilis using denaturing gradient gel
electrophoresis. Aquaculture, 302: 182-194.
Planas M, Pérez-Lorenzo M, Hjelm M, Gram L, Fiksdal
IU, Bergh Ø, Pintado J, 2006. Probiotic effect in vivo of
Roseobacter strain 27-4 against Vibrio (Listonella) an-
guillarum infections in turbot (Scophthalmus maximus
L.) larvae. Aquaculture, 255: 323-333.
Poole JEP, 1984. A study of the relationship between the
mixed liquor fauna and plant performance for a variety
of activated sludge sewage treatment works. Water Re-
search, 18: 281-287.
Pourriot R, 1977. Food and feeding habits of Rotifera. Ar-
chiv für Hydrobiologie-Beiheft Ergebnisse der Limnologie,
8: 243-260.
Pourriot R, Snell TW, 1983. Resting eggs in rotifers. Hydro-
biologia, 104: 213-224.
Price ARG, Nelson-Smith A, 1986. Observations on sur-
face pollution on the Indian Ocean and South China
Sea during the Sindbad voyage (1980-81). Marine Pollu-
tion Bulletin, 17: 60-62.
Rainuzzo JR, Reitan KI, Olsen Y, 1994a. Effect of short-
and long-term lipid enrichment on total lipids, lipid
class and fatty acid composition in rotifers. Aquaculture
International, 2: 19-32.
Rainuzzo JR, Reitan KI, Jørgensen L, Olsen Y, 1994b.
Lipid composition in turbot larvae fed live feed cultur-
ed by emulsions of different lipid classes. Comparative
Biochemistry and Physiology, 107A: 699-710.
Ricci C, Melone G, 1998. Dwarf males in monogonont ro-
tifers. Aquatic Ecology, 32: 361-365.
Ricci C, Serra M, Snell TW, 2000. Small, beautiful and se-
xy: what rotifers tell us about ecology and evolution.
Trends in Ecology and Evolution, 15: 220-221.
Richardson AJ, 2008. In hot water: zooplankton and cli-
mate change. ICES Journal of Marine Science, 65: 279-
295.
Rioboo C, Prado R, Herrero C, Cid A, 2007. Population
growth study of the rotifer Brachionus sp. fed with tri-
azine-exposed microalgae. Aquatic Toxicology, 83: 247-
253.
Roche KF, 1995. Growth of the rotifer Brachionus calyciflo-
rus Pallas in dairy waste stabilization ponds. Water Re-
search, 29: 2255-2260.
Rodriguez C, Perez JA, Lorenzo A, Izquierdo MS, Cejas
JR, 1994. n-3 HUFA requirement of larval gilthead sea-
bream Sparus aurata when using high levels of eicos-
apentaenoic acid. Comparative Biochemistry and Physio-
logy, 107A: 693-698.
Rodríguez C, Pérez JA, Badía P, Izquierdo MS, Ferna´n-
dez-Palacios H, Lorenzo Herna´ndez A, 1998. The n-3
highly unsaturated fatty acids requirements of gilthead
seabream (Sparus aurata L.) larvae when using an ap-
propriate DHA/EPA ratio in diet. Aquaculture, 169: 9-
23.
Roiha IS, Otterlei E, Samuelsen OB, 2011. Evaluating bio-
encapsulation of florfenicol in rotifers (Brachionus pli-
catilis). Aquaculture Research, 42: 1110-1116.
Root TL, Price JT, Hall KR, Schneider H, Rosenzweig C,
Pounds AJ, 2003. Fingerprints of global warming on
wild animals and plants. Nature, 421: 57-60.
Ruttner-Kolisko A, 1974. Plankton rotifers: biology and tax-
onomy. Vol. XXVI/1. Die Binnengewasser, Stuttgard.
Saksena DN, 1987. Rotifers as indicators of water quality.
Acta Hydrochimica et Hydrobiologica, 15: 481-485.
Sarma SSS, Trujillo-Herna´ndez HE, Nandini S, 2003. Po-
pulation growth of herbivorous rotifers and their preda-
tor (Asplanchna) on urban wastewaters. Aquatic Ecolo-
gy, 37: 243-250.
Schmid-Araya JM, 1991. The effect of food concentration
on the life histories of Brachionus plicatilis (O.F.M.) and
Encentrum linnhei SCOTT. Archives of Hydrobiology,
121: 87-102.
Schindler DW, 2006. Recent advances in the understand-
ing and management of eutrophication. Limnology and
Oceanography, 51: 356-363.
Schröder T, 2005. Diapause in monogonont rotifers. Hydro-
biologia, 546: 291-306.
Sen Gupta R, Fondekar SP, Alagarsamy R, 1993. State of
oil pollution in the Northern Arabian Sea after the 1991
Gulf oil spill. Marine Pollution Bulletin, 27: 85-91.
Segers H, 2007. Annotated checklist of the rotifers (Phylum
Rotifera), with notes on nomenclature, taxonomy and
distribution. Zootaxa, 1564: 1-104.
110 Venetia Kostopoulou et al. — Brachionus plicatilis: an emerging bio-tool for numerous applications
Serra M, Snell TW, 2009. Sex loss in monogonont rotifers.
In: Schön I, Martens K, Van Dijk P, eds. Lost Sex. Sprin-
ger, Berlin: 281-294.
Serra M, Carmona MJ, Miracle MJ, 1994. Survival analysis
of three clones of Brachionus plicatilis (Rotifera). Hy-
drobiologia, 277: 97-105.
Serra M, Galiana A, Go´mez A, 1997. Speciation in mono-
gonont rotifers. Hydrobiologia, 358: 63-70.
Serra M, Go´mez A, Carmona MJ, 1998. Ecological genet-
ics of Brachionus sympatric sibling species. Hydrobiolo-
gia, 387/388: 373-384.
Serra M, Snell TW, King CE, 2004. The timing of sex in
cyclical parthenogenetic rotifers. In: Moya A, Font E,
eds. Evolution from molecules to ecosystems. Oxford
University Press, New York: 135-146.
Serrano L, Miracle MR, Serra M, 1986. Differential respon-
se of Brachionus plicatilis ecotypes to various insecti-
cides. Journal of Environmental Biology, 7: 259-275.
Sharma BK, 1983. The Indian species of the genus Brachi-
onus (Eurotatoria: Monogononta: Brachionidae). Hy-
drobiologia, 104: 31-39.
Skjermo J, Vadstein O, 1999. Techniques for microbial
control in the intensive rearing of marine larvae. Aqua-
culture, 177: 333-343.
Sla´decˇek V, 1983. Rotifers as indicators of water quality.
Hydrobiologia, 100: 169-201.
Sleeter TD, Butler JN, 1982. Petroleum hydrocarbons in
zooplankton faecal pellets from the Sargasso Sea. Ma-
rine Pollution Bulletin, 13: 54-56.
Smith VH, Joye SB, Howarth RW, 2006. Eutrophication of
freshwater and marine ecosystems. Limnology and O-
ceanography, 51: 351-355.
Snell TW, Boyer E, 1988. Thresholds for mictic female pro-
duction in the rotifer Brachionus plicatilis (Muller).
Journal of Experimental Marine Biology and Ecology,
124: 73-85.
Snell TW, Persoone G, 1989. Acute toxicity bioassays using
rotifers. I. A test for brackish and marine environments
with Brachionus plicatilis. Aquatic Toxicology, 14: 65-80.
Snell TW, Carmona MJ, 1995. Comparative toxicant sensi-
tivity of sexual and asexual reproduction in the rotifer
Brachionus calyciflorus. Environmental Toxicology and
Chemistry, 14: 415-420.
Snell TW, Janssen CR, 1995. Rotifers in ecotoxicology: a
review. Hydrobiologia, 313/314: 231-247.
Snell TW, Serra M, 2000. Using probability of extinction to
evaluate the ecological significance of toxicant effects.
Environmental Toxicology and Chemistry, 19: 2357-2363.
Snell TW, Bieberich CJ, Fuerst R, 1983. The effects of
green and blue-green algal diets on the reproductive ra-
te of the rotifer Brachionus plicatilis. Aquaculture, 31:
21-30.
Snell TW, Moffat BD, Janssen C, Persoone G, 1991. Acute
toxicity tests using rotifers. III. Effects of temperature,
strain, and exposure time on the sensitivity of Brachio-
nus plicatilis. Environmental Toxicology and Water Qual-
ity, 6: 63-75.
Snell TW, Kubanek J, Carter W, Payne AB, Kim J, Hicks
MK, Stelzer C-P, 2006. A protein signal triggers sexual
reproduction in Brachionus plicatilis (Rotifera). Marine
Biology, 149: 763-773.
Starkweather PL, 1980. Aspects of the feeding behavior
and trophic ecology of suspension-feeding rotifers. Hy-
drobiologia, 73: 63-72.
Starkweather PL, 1987. Rotifera. In: Pandian TJ, Vernberg
FJ, eds. Animal energetics. Vol. 1. Protozoa through Inse-
cta. Academic Press, Orlando: 159-183.
Stelzer C-P, 1998. Population growth in planktonic rotifers.
Does temperature shift the competitive advantages for
different species? Hydrobiologia, 387/388: 349-353.
Stelzer C-P, 2011. The cost of sex and competition between
cyclical and obligate parthenogenetic rotifers. The Ame-
rican Naturalist, 177: E43-E53.
Stelzer C-P, Riss S, Stadler P, 2011. Genome size evolution
at the speciation level: the cryptic species complex Bra-
chionus plicatilis (Rotifera). BMC Evolutionary Biology,
11: 90.
Suatoni E, Vicario S, Rice S, Snell T, Caccone A, 2006. An
analysis of species boundaries and biogeographic pat-
terns in a cryptic species complex: The rotifer – Bra-
chionus plicatilis. Molecular Phylogenetics and Evolution,
41: 86-98.
Suga K, Mark Welch D, Tanaka Y, Sakakura Y, Hagiwara
A, 2007. Analysis of expressed sequence tags of the cy-
clically parthenogenetic rotifer Brachionus plicatilis.
PLOS One, 2: e671.
Suga K, Mark Welch DB, Tanaka Y, Sakakura Y, Hagi-
wara A, 2008. Two circular chromosomes of unequal
copy number make up the mitochondrial genome of
the rotifer Brachionus plicatilis. Molecular Biology and
Evolution, 25: 1129-1137.
Suzer C, C¸oban D, Kamaci OH, Saka S¸, Firat K, Otgu-
cuog˘lu Ö, Küçüksari H, 2008. Lactobacillus spp. bacte-
ria as probiotics in gilthead sea bream (Sparus aurata,
L.) larvae: effects on growth performance and digestive
enzyme activities. Aquaculture, 280: 140-145.
Tamplin ML, Gauzens AL, Huq A, Sack DA, Colwell RR,
1990. Attachment of Vibrio cholerae serogroup 01 to
zooplankton and phytoplankton of Bangladesh waters.
Applied and Environmental Microbiology, 56: 1977-1980.
Thassitou PK, Arvanitoyannis IS, 2001. Bioremediation: a
novel approach to food waste management. Trends in
Food Science & Technology, 12: 185-196.
Timms BV, 1993. Saline lakes of the Paroo, inland New
South Wales, Australia. Hydrobiologia, 267: 269-289.
Tinh NTN, Phuoc NN, Dierckens K, Sorgeloos P, Bossier
P, 2006. Gnotobiotically grown rotifer Brachionus pli-
catilis sensu stricto as a tool for evaluation of microbial
functions and nutritional value of different food types.
Aquaculture, 253: 421-432.
Venetia Kostopoulou et al. — Brachionus plicatilis: an emerging bio-tool for numerous applications 111
Tinh NTN, Linh ND, Wood TK, Dierckens K, Sorgeloos P,
Bossier P, 2007. Interference with the quorum sensing
systems in a Vibrio harveyi strain alters the growth rate
of gnotobiotically cultured rotifer Brachionus plicatilis.
Journal of Applied Microbiology, 103: 194-203.
Trout JM, Walsh EJ, Fayer R, 2002. Rotifers ingest Giar-
dia cysts. Journal of Parasitology, 88: 1038-1040.
Turner PN, 1993. Distribution of rotifers in a Floridian salt-
water beach, with a note on rotifer dispersal. Hydrobio-
logia, 255/256: 435-439.
Turner JT, Tester PA, 1992. Zooplankton feeding ecology:
bacterivory by metazoan microzooplankton. Journal of
Experimental Marine Biology and Ecology, 160: 149-167.
Turner JT, Tester PA, 1997. Toxic marine phytoplankton,
zooplankton grazers, and pelagic food webs. Limnology
and Oceanography, 42: 1203-1214.
Turton CL, McAndrews JH, 2006. Rotifer loricas in second
millennium sediment of Crawford Lake, Ontario, Ca-
nada. Reviews of Palaeobotany and Palynology, 141: 1-6.
Uhlmann D, 1980. Limnology and performance of waste
treatment lagoons. Hydrobiologia, 72: 21-30.
Vasileiadou K, Papakostas S, Triantafyllidis A, Kappas I,
Abatzopoulos TJ, 2009. A multiplex PCR method for
rapid identification of Brachionus rotifers. Marine Bio-
technology, 11: 53-61.
Verpraet R, Chair M, Leger P, Nelis H, Sorgeloos P, De
Leenheer A, 1992. Live-food mediated drug delivery as
a tool for disease treatment in larviculture. The enrich-
ment of therapeutics in rotifers and Artemia nauplii.
Aquacultural Engineering, 11: 133-139.
Walker KF, 1981. A synopsis of ecological information on
the saline lake rotifer Brachionus plicatilis Müller 1786.
Hydrobiologia, 81: 159-167.
Wallace RL, 2002. Rotifers: exquisite metazoans. Integrati-
ve and Comparative Biology, 42: 660-667.
Wallace RL, Snell TW, 1991. Rotifera. In: Thorpe JH, Co-
vich AP, eds. Ecology and classification of North Ameri-
can freshwater invertebrates. Academic Press Inc, New
York: 187-248.
Wallace RL, Smith HA, 2009. Rotifera. In: Likens GE, ed.
Encyclopedia of inland waters. Oxford, Elsevier: 689-
703.
Wallace RL, Snell TW, Ricci C, Nogrady T, 2006. Rotifera
1: Biology, Ecology and Systematics. Backhuys Publish-
ers, Leiden, The Netherlands.
Walsh EJ, Schröder T, Wallace RL, Ríos-Arana JV, Rico-
Martínez R, 2008. Rotifers from selected inland saline
waters in the Chihuahuan Desert of Mexico. Saline Sys-
tems, 4: 7-18.
Walther G-R, Post E, Convey P, Menzel A, Parmesan C,
Beebee TJC, Fromentin J-M, Hoegh-Guldberg O, Bair-
lein F, 2002. Ecological responses to recent climate
change. Nature, 416: 389-395.
Wang L, Yan T, Yu R, Zhou M, 2005. Experimental study
on the impact of dinoflagellate Alexandrium species on
populations of the rotifer Brachionus plicatilis. Harmful
Algae, 4: 371-382.
West SA, Lively CM, Read AF, 1999. A pluralist approach
to sex and recombination. Journal of Evolutionary Biolo-
gy, 12: 1003-1012.
Winder M, Schindler DE, 2004. Climate change uncouples
trophic interactions in an aquatic system. Ecology, 85:
2100-2106.
Wolfe MF, Schlosser JA, Schwartz GJB, Singaram S, Miel-
brecht EE, Tjeerdema RS, Sowby ML, 1998. Influence
of dispersants on the bioavailabitiy and trophic transfer
of petroleum hydrocarbons to primary levels of a ma-
rine food chain. Aquatic Toxicology, 42: 211-227.
Wrona FJ, Prowse TD, Reist JD, Hobble JE, Lévesque
LMJ, Vincent WF, 2006. Climate change effects on a-
quatic biota, ecosystem structure and function. Ambio,
35: 359-369.
Wyngaard GA, Rasch EM, Manning NM, Gasser K, Do-
mangue R, 2005. The relationship between genome si-
ze, development rate, and body size in copepods. Hy-
drobiologia, 532: 123-137.
Xie Z, Xiao H, Tang X, Lu K, Cai H, 2008. Interactions be-
tween red tide microalgae and herbivorous zooplank-
ton: effects of two bloom-forming species on the rotifer
Brachionus plicatilis (O.F. Muller). Hydrobiologia, 600:
237-245.
Yasuno M, Asaka A, Kono Y, 1993. Effects of pyraclofos
(an organophosphorous insecticide) on nutrient en-
riched ecosystems. Chemosphere, 27: 1813-1824.
Yoshida K, Ishii H, Ishihara Y, Saito H, Okada Y, 2009.
Bioremediation potential of formaldehyde by the ma-
rine microalga Nannochloropsis oculata ST-3 strain. Ap-
plied Biochemistry and Biotechnology, 157: 321-328.
Yoshinaga T, Hagiwara A, Tsukamoto K, 2000. Effect of
periodical starvation on the life history of Brachionus
plicatilis O.F. Muller (Rotifera): a possible strategy for
population stability. Journal of Experimental Marine Bi-
ology and Ecology, 253: 253-260.
Yoshinaga T, Kaneko G, Kinoshita S, Tsukamoto K, Wata-
be S, 2003. The molecular mechanisms of life history al-
terations in a rotifer: a novel approach in population
dynamics. Comparative Biochemistry and Physiology B,
136: 715-722.
Zakaria HY, Hussien Ahmed M, Flower R, 2007. Environ-
mental assessment of spatial distribution of zooplank-
ton community in Lake Manzalah, Egypt. Acta Adriati-
ca, 48: 161-172.
Zhao Q, Wang B, 1996. Evaluation on a pilot-scale attached-
growth pond system treating domestic wastewater. Wa-
ter Research, 30: 242-245.
Zou Y, Yamasaki Y, Matsuyama Y, Yamaguchi K, Honjo
T, Oda T, 2010. Possible involvement of hemolytic ac-
tivity in the contact-dependent lethal effects of the di-
noflagellate Karenia mikimotoi on the rotifer Brachio-
nus plicatilis. Harmful Algae, 9: 367-373.
112 Venetia Kostopoulou et al. — Brachionus plicatilis: an emerging bio-tool for numerous applications