Content uploaded by Bram Vanschoenwinkel
Author content
All content in this area was uploaded by Bram Vanschoenwinkel
Content may be subject to copyright.
Belg. J. Zool., 143 (1) : 3-14
January 2013
Rediscovery of Branchipus schaefferi (Branchiopoda: Anostraca) in
Belgium - notes on habitat requirements and conservation management
Bram Vanschoenwinkel
1, 3,*
, Luc Brendonck
1
, Tom Pinceel
1
, Pascal Dupriez
2
&
Aline Waterkeyn
1, 3
1
Laboratory of Aquatic Ecology, Evolution and Conservation, KU Leuven, Charles Deberiotstraat 32, 3000 Leuven,
Belgium.
2
Natagora Centre-Ouest Hainaut, Rue Marécaux 5, 7333 Tertre, Belgium.
³ BINCO (Biodiversity Inventory for Conservation), Rijmenamsesteenweg 189, 3150 Haacht, Belgium
.
*
Corresponding author: bram.vanschoenwinkel@bio.kuleuven.be
ABSTRACT. Fairy shrimps (Crustacea, Anostraca) are specialized inhabitants of inland water bodies that
Branchipus schaefferi Fischer, 1834 since
1930. Nineteen populations were found in a restricted area located 55 km SE of Brussels in the Province of
distribution and habitat requirements of the species based on literature and formulate a number of guidelines
for the conservation of this species as well as other large branchiopods in densely settled areas with intensive
agriculture such as Belgium. Finally, we formulate a number of likely explanations for the lack of recent
: fairy shrimp, temporal pools, wheel tracks, conservation management
INTRODUCTION
Fairy shrimps and brine shrimps together make
clam shrimps (Spinicaudata, Laevicaudata
and Cyclestherida) and tadpole shrimps
(Notostraca) they are often referred to as large
branchiopods. Together with a number of extinct
orders they form the class Branchiopoda. Due
to their size, large branchiopods are sensitive
occur in aquatic habitats that cannot sustain
Jeppesen
et al., 2001), either because they are highly
saline, periodically dry or regularly freeze solid.
Brine shrimps (Artemia and Parartemia spp.)
and some members of the fairy shrimp genera
Branchinella, Branchinectella, Branchinecta
and Phallocryptus are typical for salt pans in
different parts of the world. Most fairy shrimp,
on the other hand, generally inhabit temporary
freshwater habitats, ranging from large wetlands,
vernal ponds and marshes to rock pools, wheel
Although the class Branchiopoda is an old group
with a near global distribution (
Brendonck et al.,
2008), Belgian records of fairy shrimp and other
large branchiopod populations are extremely
scant. Museum collections in Brussels and Liège
were inventoried by Brendonck (1989a) and
Loneux & Thiéry (1998), respectively, revealing
a historic species richness of seven. These include
three fairy shrimp species: Chirocephalus
diaphanus Prevost, 1803; Eubranchipus
(Siphonophanes) grubii Dybowski, 1860 and
Branchipus schaefferi Fischer, 1834; two clam
shrimp species: Limnadia lenticularis Linnaeus,
1761 and Leptestheria dahalacensis (Rüppel,
1837) and two tadpole shrimp species: Lepidurus
apus Linnaeus, 1758 and Triops cancriformis
Bosc, 1801.
The fairy shrimp C. diaphanus is a widespread
4 Bram Vanschoenwinkel, Luc Brendonck, Tom Pinceel, Pascal Dupriez & Aline Waterkeyn
and North Africa with a range extending
northward into Great Britain and eastward to
the Black Sea. In Belgium, C. diaphanus was
found in Halen in 1903 (Brendonck, 1989A)
and in Sint-Truiden in 1930 (
Loneux & Thiéry,
1998) and was last seen in Hamois in 1998
(
Loneux & WaLravens, 1998). Eubranchipus
(Siphonophanes) grubii is a Central and Eastern
European coldwater species and may have
been observed in Belgium in 1970 in Geel
(
k. WouTers, pers. comm. de Brendonck,
Currently, the nearest populations are located
in The Netherlands (North Brabant, Gelderland,
Overijssel and Limburg) (
Brendonck, 1989A;
soesBergen, 2008), Germany (Rhineland-
Maier, 1998;
engeLMann & hahn, 2004) and France (Alsace)
(
defaye et al., 1998). Branchipus schaefferi
is a eurytherm species that is widespread in
Europe and around the Mediterranean basin
with additional records from Northern Africa
and Asia (
BrTek & Thiéry, 1995; aL-sayed &
Z
ainaL, 2005) and was encountered only once
in Belgium (Sint-Truiden, 1930) (
Loneux &
Thiéry, 1998). The closest currently-known
(
Maier, 1998; engeLMann & hahn, 2004) and
(Alsace region) (
defaye et al., 1998). The clam
shrimp L. lenticularis is a Holarctic species
most abundant in northern temperate climates.
In Belgium, it was reported from a marsh in
Genk in 1946 and Zolder-Zonhoven in 1959
(
Brendonck, 1989A). Leptestheria dahalacensis
(Rüppel, 1837) was encountered in Belgium
Brussels, presumably having been introduced
inadvertently with mud from temporary ponds
in carp nurseries in Eastern Europe (
Brendonck
et al., 1989B). The tadpole shrimp L. apus is
widespread in Europe and has been reported in
Belgium from Balen or Halen (date unknown),
but nothing else is known about the population
(
Brendonck, 1998). The second tadpole shrimp
species, T. cancriformis, is also widespread in
Europe and historically known from Halen (in
1892 and 1903), Sint Truiden (in 1917, 1929
and 1930), Ferrières (in 1905 and 1906) and
Leuven (date unknown) (
Brendonck, 1998;
Loneux & Thiéry
currently-persisting population in Belgium is a
T. cancriformis population discovered in 2006 on
a military domain in Brasschaat in the province
of Antwerp (
WiLLeMs & de Leander, 2006).
Despite the relatively intensive monitoring of
many aquatic habitats, fairy shrimps have not
been observed in Belgium since 1998 and clam
shrimps have not been seen since 1989.
In this paper we report the rediscovery of the
order Anostraca in Belgium represented by at
least 19 populations of B. schaefferi, which has
autecology of the species based on published
literature and the biotic and abiotic characteristics
of the habitats in which it was found. Based on
this we formulate guidelines for more effective
detection, monitoring and conservation of
this species and other large branchiopods in
intensively-developed regions such as Belgium.
MATERIALS AND METHODS
Notes on the ecology and distribution
of the species
Branchipus schaefferi (Fig. 1) is a eurythermic
species that can be found from late spring until fall
in temperate regions (
hössLer et al., 1995; eder
et al., 1997) and in Southern France (
defaye et al.,
1998;
WaTerkeyn et al., 2009) or throughout the
year in warmer regions around the Mediterranean
basin such as Morocco (
BeLk & BrTek, 1995;
BrTek & Thiéry, 1995; Thiéry, 1987; Marrone
& M
ura, 2006). It is most frequently found in
small shallow ponds, puddles or wheel tracks
with turbid water and scarce vegetation (
hössLer
et al., 1995;
peTrov & peTrov, 1997; defaye
et al., 1998;
Boven et al., 2008). The species
can also be found in other habitat types, such
peTkovski, 1997; Mura,
2001) and mountain habitats (
eder et al., 1997;
defaye et al., 1998; Mura, 1999; Thiéry, 1987).
5
Branchipus schaefferi rediscovered in Belgium
Fig. 1. – Distribution of the discovered Branchipus schaefferi populations in Hainaut (A)
with thin and thick black lines representing unsealed and sealed roads, respectively. Filled
symbols represent wheel track populations, the empty symbol corresponds to a population in
a farmland pond. (B) Overview of the only two records of this species in Belgium, indicating
Truiden (†). The middle panel shows a typical B. schaefferi wheel track habitat near Binche
(Picture: B. Vanschoenwinkel) (C) and a close up of an adult male showing the antennal
isolate of a wheel track zooplankton community including many fairy shrimps. Females can
be discerned based on the presence of a blue brood pouch (Picture: B. Vanschoenwinkel) (E).
6 Bram Vanschoenwinkel, Luc Brendonck, Tom Pinceel, Pascal Dupriez & Aline Waterkeyn
Exceptionally, it can occur in permanent waters,
as is the case in Germany (hössLer et al., 1995).
It is considered a rather tolerant species, since it
can survive in ponds with short inundations, high
turbidities (Thiéry, 1987), high conductivities
(up to 4500 µS cm
-1
) (WaTerkeyn et al., 2010),
high temperatures (Marrone & Mura, 2006),
eutrophication due to cattle manure (Thiéry,
1987) and high altitudes (up to 2600 m a.s.l.)
(Thiéry, 1987).
Dormant eggs of Branchipus schaefferi
hatch within 1 to 6 days after inundation, while
maturation takes 7 to 30 days, depending on the
temperature and food conditions (
WaTerkeyn
et al., 2009 and references therein). They can
survive for up to 2.5 months (hössLer et al.,
1995; BeLadJaL et al., 2003) and grow up to
20-25 mm (Thiéry, 1991; hössLer et al., 1995;
peTkovski, 1997; defaye et al., 1998; aL-sayed
& ZainaL, 2005). The females have a brightly-
turquoise colored brood sac and can produce up
to 242 dormant eggs per day (maximum reached
21 to 27 days after hatching) (BeLadJaL et al.,
2007). Eggs are typically angular and wrinkled
and more or less spherical ranging from 195 to
290 µm in size (Thiéry et al., 1995). Different
life stages of B. schaefferi can co-occur, probably
due to several hatching peaks triggered by
additional rainfall (hössLer et al., 1995; peTrov
& peTrov, 1997; aL-sayed & ZainaL, 2005).
Branchipus schaefferi often co-exists with one
or several other large branchiopods, such as
the notostracan T. cancriformis (most often
reported), spinicaudatans (Imnadia yeyetta,
I. banatica, L. dahalacensis or L. saetosa),
or other anostracans (Tanymastix stagnalis,
Branchinecta ferox, Streptocephalus torvicornis,
C. diaphanus, C. carnuntanus, C. brevipapis)
(peTrov & cveTkovic, 1997; peTkovski, 1997;
defaye et al., 1998; Maier et al., 1999; Marrone
& Mura, 2006; Boven et al., 2008; WaTerkeyn
et al., 2009).
Study site and sampling protocol
branchiopod-like crustacean in the area in 2002
(Dupriez, pers. com.), populations of the species
were discovered in a wheel track North of Binche
(province of Hainaut; Belgium) on 23 July 2012
by Pascal Dupriez during a survey for natterjack
toads (Bufo calamita). The observation was
reported as a potential sighting to the KU Leuven
nationwide large branchiopod survey (http://bio.
kuleuven.be/de/dea/branchiopodhunters/index.
php). Thirty other potential habitats in that area
were surveyed on 25, 26 and 27 July 2012. These
included the two types of temporary ponds present
in the area: wheel tracks as well as a couple
Several wheel tracks were dry so the presence of
fairy shrimp in these could not be determined in
populations we used conservative criteria. A set of
tracks that showed obvious signs of connections
was considered as a single habitat potentially
housing a single population. Proximate tracks
were only considered as separate habitats if they
were independent depressions separated by a
clear topographic barrier. In total, water quality
variables were measured in 22 habitats (19 of
which contained B. schaefferi). Measurements
were taken between 11.00 and 15.00 under
sunny conditions and included conductivity
(EC; µS cm
-1
), water temperature (T; °C), pH,
oxygen concentration (DO; ppm), total dissolved
solids (TDS; ppm), and total suspended solids
(TSS; ppm) using a HI9828 Multiparameter
Meter (Hanna instruments, Ann Arbor, MI,
USA). Chlorophyll-a concentration (ChlA; mg
L
-1
) and turbidity were determined using a hand
Sunnyville, CA, USA). Nutrient concentrations
using a Hach DR2400 spectrophotometer (Hach
company, Loveland, CO, USA) by means of the
following methods: total N (persulphate digestion
method), total P (acid persulphate digestion
method using PhosVer® 3), reactive phosphate
(PhosVer® 3 method) and Nitrate (chromotropic
7
Branchipus schaefferi rediscovered in Belgium
acid method). The bottom of many wheel track
habitats was partly or almost entirely covered
with gravel. The gravel coverage (± 10%)
was estimated and included as an additional
predictor variable in the analyses. Habitat size
was assessed by measuring length, width, max
depth and volume calculated using the formula
for the volume of a half ellipsoid. In case pools
the volume was calculated as two separate half
ellipsoids. An aquarium net (mesh 0.5 mm)
was initially used to qualitatively check for the
presence of B. schaefferi. In order to quantify
density of fairy shrimp (number of individuals
per L), quantitative zooplankton samples were
taken by scooping a total of 12 L of water using
zooplankton net. If fairy shrimp densities were
stored in 90% non-denatured ethanol. Total
population sizes were obtained by multiplying
densities with calculated water volumes.
Analyses
The relationship between measured
environmental variables and fairy shrimp
density was analysed using multiple linear
regression. Due to large variation in fairy shrimp
densities including several outliers, analyses
were performed using density ranks rather than
the untransformed data. This transformation
helped to meet the linear regression assumption
of homoscedasticity. In order to reduce the set
of predictor variables, only variables with a
clear trend of association (Spearman correlation
variable were included in a multiple regression
model. Both stepwise forward and backward
selection procedures were used in order to remove
adjusted r² and Akaike’s information criterion
as decisive factors. First order interactions were
also considered. Associations between fairy
shrimp densities and measured environmental
variables were visualised using principal
component analysis (PCA) triplot. This plot
shows the relative positions of different habitats
along the two dominant axes of environmental
variation (PC1 and PC2) while simultaneously
showing the associations between habitats and
environmental variables (shown as vectors) and
associations between environmental variables.
Environmental variables were centered and
standardised prior to analyses. In order to obtain
an objective representation of the environmental
variation and its relationship with the response
variable of interest (fairy shrimp density), the
latter was plotted as a supplementary variable
that does not affect the ordination (Legendre &
Legendre, 1998). All analyses were performed
in Statistica 10 (Statsoft 2011, Tulsa, OK, USA).
RESULTS
B. schaefferi was found in a total of 18 wheel
tracks present in a local network of unsealed
roads in a rural area covering a total area of
approximately 7 km² North of Binche in the
Province of Hainaut. These roads were separated
wheat) by an elevated ridge of approximately 1.5
m wide and 30 cm high, preventing excessive
the species was found in a single temporary pond
area. Most habitats housed large populations
(Average: 4315; Range: 1 - 44000) of adults of
both sexes. The environmental characteristics of
the different B. schaefferi habitats are provided
in Table 1. In general, habitats were relatively
shallow, turbid and lacked aquatic vegetation.
Macroinvertebrate species richness was relatively
low in all habitats. Besides B. schaefferi, the
only branchiopod crustacean present was Moina
branchiata. Other inhabitants included at least
one ostracod species, water bugs (Corixidae),
several dipterans (Chironomidae, Culicidae,
Eristalis sp.). Principal components analysis was
used to visualize associations between densities
of B. schaefferi and environmental variables. The
8 Bram Vanschoenwinkel, Luc Brendonck, Tom Pinceel, Pascal Dupriez & Aline Waterkeyn
of total variation. The triplot suggests a positive
association between fairy shrimp population
density and reactive phosphate, and negative
associations with pH, gravel coverage, nitrate
and chlorophyll a (Fig. 2). However, gravel
was retained in the constructed regression models
associated with lower fairy shrimp densities
(Fig. 3). Associations with other environmental
DISCUSSION
The current study shows that B. schaefferi is
still present in Belgium after not being reported
of fairy shrimp in Belgium since C. diaphanus
was last detected in Hamois in 1998 (
Loneux &
WaLravens, 1998). Observation of B. schaefferi
in summer during a warm period and after heavy
rains is consistent with the known phenology of
this heat-tolerant eurythermic species (defaye et
al., 1998). Most of the remaining populations of
TSS
Fig. 2. – PCA triplot showing associations between
environmental variables (vectors), site scores (circles)
and the supplementary variable Population density
(arrow). Environmental variables were centered and
standardised prior to analysis. Population densities
were transformed to ranks.
relationship between the percentage of surface area
of each habitat covered with gravel and the density of
fairy shrimp found in the active populations during
sampling.
B. schaefferi
known from wheel tracks (Boven et al., 2008;
defaye et al., 1998), probably since these are the
most commonly-remaining temporary aquatic
landscapes. The species is well adapted to time
stress, displaying traits such as a short life cycle
and high fecundity (hössLer et al., 1995; peTrov
& peTrov, 1997; defaye et al., 1998). Therefore
it is well adapted for living in these short-lived
temporary aquatic systems, which often hold
water for only a couple of weeks.
In general, population densities in most of
the studied habitats were high (Average: 2.18
± 4.1 ind./L; Range: 0.01-18) suggesting that
these populations are well established. Although
nutrient concentrations were moderate to high,
chlorophyll a concentrations were low indicating
that this could be top-down controlled by the
grazing zooplankton community. Freshwater
zooplankton communities, and fairy shrimp in
particular, can be sensitive to pesticides or to
oxygen stress as a result of eutrophication (
Lahr,
1998; rogers, 1998). As such, the fact that
populations were doing well despite the presence
of intensive agriculture in the immediate vicinity
could illustrate that the buffer zones (elevated
ridge covered with grasses, herbs and small
shrubs) that are present between the wheel
9
Branchipus schaefferi rediscovered in Belgium
Variable Average ± st. dev. Range
Surface (m²) 32.4 ± 75.0 0.2 - 314
Depth (cm) 7.8 ± 3.8 2 - 15
Conductivity (µS/cm) 573.4 ± 274.6 133 - 1335
Dissolved oxygen (ppm) 38.6 ± 1.47 6.20 - 1.35
pH 8.10 ± 0.30 7.69 - 8.57
Temperature (°C) 32.1 ± 2.3 27.73 - 35.7
Total Dissolved Solids (ppm) 286.9 ± 137.2 67 - 668
TSS 222.8 ± 205.0 34.0 - 873.7
Chl A (mg/l) 0.011 ± 0.007 0.002 - 0.03
Total N (mg/l) 4.92 ± 3.45 0 - 10.4
Nitrate (mg/l) 4.51 ± 2.49 0 - 9
Total P (mg/l) 2.01 ± 0.76 0.68 - 3.62
Reactive phosphate (mg/l) 1.06 ± 0.78 0.22 - 2.7
TABLE 1
Environmental variables measured in the ponds containing B. schaefferi (n = 19).
However, the presence of a large population in
runoff suggests that the species may, in fact,
be quite resistant, as was also suggested by
Thiéry (1987). The species, however, remains
vulnerable to habitat destruction. In many areas
that in the studied area fairy shrimp population
densities were much lower in habitats with ample
gravel coverage. This effect can have different
origins. Gravel application can reduce the depth
and potential length of inundations (hydroperiod)
of the habitat or alter water chemistry and make
them less suitable for fairy shrimp. However, we
found no indications for associations between
gravel coverage and water levels or any of the
measured environmental variables (Spearman R;
purely physical nature. Gravel application can,
for instance, cover the dormant egg bank and
shield fairy shrimp resting eggs from receiving
hatching cues, such as light, impeding successful
recruitment. Filling of roadside ditches
presumably also led to the disappearance of the
last known Belgian population of C. diaphanus in
Hamois (
Loneux, pers. com.; vanschoenWinkeL,
pers. obs.). Consequently, it is advisable to
refrain from adding additional gravel, debris
or other sediments to existing wheel tracks if
these populations are to be preserved. In some
wheel tracks become too deep to allow passage
of vehicles we propose that they should not be
of about 10 cm of standing water after rains, as
was the situation observed for the fairy shrimp
populations in this study. Ideally, the top layer
surface sediment (± 4 cm) should be temporarily
removed prior to graveling and replaced on top of
the gravel to ensure that the resting egg bank will
not be covered and fairy shrimp may continue
to hatch during future inundations. Restricting
access of vehicles altogether is probably not
recommended as the disturbance provided by
passing vehicles is necessary to maintain these
wheel tracks. Additionally, previous research has
shown that walkers and motor vehicles can be
important dispersal vectors for large branchiopod
crustaceans (
WaTerkeyn et al., 2010). Regular
exchange of eggs between populations may
ensure healthy metapopulation dynamics
with recolonization rates compensating for
10 Bram Vanschoenwinkel, Luc Brendonck, Tom Pinceel, Pascal Dupriez & Aline Waterkeyn
occasional extinctions. The spatial organization
of the populations in this study located along an
unsealed road network could be illustrative of
using genetic analyses.
Relict populations or products of a recent
introduction?
genetic analyses, it is plausible that the
discovered populations represent relicts, rather
than a recent establishment of the species. First
of all, the presence of the species is consistent
with the species’ distribution and its historic
presence in Belgium (
Loneux & Thiéry, 1998).
Currently known populations are present in
(Rhineland-palatinate) at about 200 to 300 km
from the Belgian locality (Loneux & Thiéry,
1998). Secondly, the occurrence of a substantial
number of populations, usually consisting
of numerous individuals, suggests that the
populations are likely to have been in the area for
at least several decades. Finally, the fact that the
populations were found in an old agricultural area
with unsealed roads that are probably more than
100 years old, makes continuous and prolonged
persistence of the species in the area a likely
scenario. An upcoming phylogeographic study
across the species’ range (including specimens
from this study) documenting the phylogenetic
relationships among the remaining European
lineages, will likely provide more conclusive
evidence concerning the origin of the Belgian
populations.
A hidden existence
The current study illustrates that populations
of fairy shrimp can remain undetected, although
individuals are relatively large (1 - 4 cm) and
conspicuous and often characterized by bright
coloration, and even in relatively well-studied
and monitored regions, such as Belgium. The
reasons for this are manifold. First of all, fairy
shrimp and other large branchiopods are typically
cues (
Brendonck, 1996). If such cues do not
present themselves, it is common that years will
go by without active populations developing
WaTerkeyn et al., 2009). This is
possible since they produce long-lived resistant,
dormant eggs. For instance, the most common
C. diaphanus and
E. (S.) grubii, are usually only present during
the colder winter months and the beginning of
spring (defaye et al., 1998), at a time when there
is typically no monitoring. Secondly, even when
eggs hatch and adults develop, they can easily
remain un-noted as fairy shrimps often inhabit
small and inconspicuous systems, such as wheel
tracks and puddles in meadows and cropland
where few people wander. These habitats are
also often considered of low conservation
interest and are therefore not monitored. Thirdly,
water in wheel tracks is often turbid obscuring
potential inhabitants. Finally, active populations
in the water column often only persist for
several weeks as a result of their short life span
and the gradual increase of predation (by e.g.
inundation (spencer et al., 1999).
Towards effective conservation
Large branchiopods are threatened in many
The main reason for this is the loss of temporary
aquatic habitats as a result of intensive agriculture
and urbanisation, and the few remaining habitats
are often degraded (
BeLk, 1998). Although 29
fairy shrimp species are red listed by IUCN, and
several species are included in local red lists
(e.g. in the Alsace), at the moment there is no
legal basis for protection of large branchiopods
in Belgium. Before a species can be red listed
put into localizing and monitoring populations.
Given the hidden existence of the members
of this group, they are typically overlooked in
11
Branchipus schaefferi rediscovered in Belgium
therefore recommend that sampling campaigns
should be strategically planned and undertaken
large branchiopods are highest. For instance,
early spring (February, March) and preferably
cold water species such as C. diaphanus, S.
grubii and L. apus. On the other hand, a summer
drought followed by heavy rainfall presents ideal
conditions for hatching and development of
warm water species, such as B. schaefferi and T.
cancriformis, which can be detected from about
10 days - 3 weeks after inundation.
Due to the frequent disturbance typical of
ephemeral habitats, local populations may
regularly go extinct. Therefore, in order to persist
regionally, dispersal and recolonization from
nearby populations (metapopulation dynamics)
are likely to be important. Promising localities
where temporary water bodies are abundant and
have historically been abundant. Although the
local dispersal potential of large branchiopods is
quite high (
vanschoenWinkeL et al., 2008A,B),
successful long distance dispersal (several km)
events are rare (vanschoenWinkeL et al., 2011).
Therefore, recently-formed temporary water
bodies, such as bomb craters and human-made
temporary ponds, may be suitable in terms of
their environmental conditions, but may not be
colonized, even when large branchiopods are
present in the region. Nevertheless, occasionally
isolated relict populations have been detected
(pauLsen, 2000). Finally, over longer time scales,
temporary pond systems typically accumulate
sediments and disappear. Therefore, physical
disturbances that counteract this process can
temporary water bodies by wallowing in them
covering their skin with mud (vanschoenWinkeL
et al., 2008B). These turbid, unattractive systems
often hold a large diversity of branchiopod
crustaceans (nhiWaTiWa et al., 2011). In recent
times, many large branchiopod populations
have been found in habitats that are frequently
disturbed by humans, such as wheel tracks (e.g.
Boven et al., 2008). The last remaining Triops
population in Belgium persists in a muddy
track used by tanks and other military vehicles
(WiLLeMs & de Leander, 2006). Similarly,
military domains in Eastern Europe are known
for their diversity of large branchiopods (Maier
et al., 1998). The presence of natural habitat that
was historically set apart, unsealed roads with
puddles and wheel tracks and regular physical
disturbance by vehicles, makes military domains
particularly suitable areas that may be acting as
refuges for temporary pond fauna, such as large
branchiopods.
group of crustaceans may be limited, it is
important to realize that temporary ponds not
only house a unique crustacean fauna, but are
also of vital importance for other endangered
species of plants and animals (
WiLLiaMs, 2006).
support have been directed at protecting certain
endangered amphibians that use temporary
ponds for breeding, such as the natterjack
toad (Bufo calamita
toad (Bombina bombina). Temporary pond
restoration and construction projects performed
Bombina
typical temporary pond organisms too. For
instance, different rare macrophytes were shown
to re-emerge from old seed banks during pond
restoration projects (hiLT et al., 2006). Due to
the prolonged viability of their dormant eggs
(Brendonck, 1996), it is not unlikely that large
branchiopods may emerge from old egg banks
present in the sediment. Consequently, a habitat-
oriented conservation strategy protecting the
few remaining high quality temporary ponds
and increasing temporary pond densities in the
large number of organism groups, including
landscape dominated by agriculture, the use of
vegetation buffer zones and ridges is likely to
12 Bram Vanschoenwinkel, Luc Brendonck, Tom Pinceel, Pascal Dupriez & Aline Waterkeyn
pesticides (decLerck et al., 2006), even though
some species such as B. schaefferi may be quite
tolerant. Finally, we would also encourage the
re-evaluation of marginal aquatic systems such
as wheel tracks as they may contain unique biota,
such as B. schaefferi.
CONCLUSIONS
This paper reports the rediscovery and the
B. schaefferi in
Belgium and analyses the link between habitat
characteristics and population densities. For the
studied wheel track populations it was shown
that extensive gravel application was associated
with lower fairy shrimp population densities,
suggesting that this practice should be avoided
if populations are to be preserved. In terms of
conservation management, we conclude that
a habitat-oriented approach preserving natural
processes of desiccation and disturbance is likely
to be most effective for the conservation of fairy
shrimp as well as other typical temporary pond
organisms.
ACKNOWLEDGEMENTS
project 3E110799. Bram Vanschoenwinkel and
to thank Liselore Vanstallen, Falko Buschke
and Bernard Loison for valuable assistance
Marcel Moncousin, Marius Loison, José Godin
and André Pourtois, who made the initial
observations in 2002 hinting at the potential
presence of anostracans in the region.
REFERENCES
aL-sayed h & ZainaL k (2005). The occurence of
anostracans - fairy shrimps Branchipus schaefferi
in vernal pools of Bahrain. Journal of Arid
Environments, 61:447-460.
BeLadJaL L, peiren n, vandekerckhove TTM &
MerTens J (2003). Different life histories of the
co-occuring fairy shrimps Branchipus schaefferi
and Streptocephalus torvicornis (Anostraca).
Journal of Crustacean Biology, 23(2):300-307.
BeLadJaL L, Weekers phh & MerTens J (2007). Life
cycle and genetic differences of two Branchipus
schaefferi populations from Morocco (Anostraca:
Crustacea). Animal Biology, 57(4):409-421.
BeLk d (1998). Global status and trends in ephemeral
pool invertebrate conservation: implications for
Ecology, conservation, and management of vernal
pool ecosystems, California native plant society,
Sacramento: 147-150.
BeLk d & BrTek J (1995). Checklist of the Anostraca.
Hydrobiologia, 298(1-3):315-353.
Boven L, vanschoenWinkeL B, de roeck er,
huLsMans a & Brendonck L (2008). Diversity and
distribution of large branchiopods in Kiskunsag
(Hungary) in relation to local habitat and spatial
factors: implications for their conservation.
Marine and Freshwater Research, 59(10):940-
950.
BrTek J & Thiéry a (1995). The geographic
distribution of the European branchiopods
(Anostraca, Notostraca, Spinicaudata,
Laevicaudata). Hydrobiologia, 298(1-3):263-280.
Brendonck L (1989a). A review of the phyllopods
(Crustacea: Anostraca, Notostraca, Conchostraca)
of the Belgian fauna. In: WouTers k & BaerT L
(eds) Invertébrés de Belgique. Institut Royal des
Sciences naturelles de Belgique, Bruxelles: 129-
135.
Brendonck L (1989b). Leptestheria dahalacensis
(Rüppel, 1837), a Conchostracan new for the
Belgian fauna. Bulletin de l’institut royal des
sciences naturelles de Belgique, Biologie, 59:59-
62.
Brendonck L (1996). Diapause, quiescence,
large freshwater branchiopods (Crustacea:
Branchiopoda: Anostraca, Notostraca,
Conchostraca). In: International Symposium on
Diapause in the Crustacea: Sep 12-17 1996; St
Petersburg, Russia: Kluwer Academic Publishers:
85-97.
Brendonck L, rogers dc, oLesen J, Weeks s,
h
oeh Wr (2008). Global diversity of large
branchiopods (Crustacea: Branchiopoda) in
13
Branchipus schaefferi rediscovered in Belgium
freshwater. Hydrobiologia, 595:167-176.
defaye d, raBeT n & Thiéry a (1998). Atlas et
bibliographie des crustacés branchiopodes
(Anostraca, Notostraca, Spinicaudata) de France.
Vol. 32.
eder e, hödL W & goTTWaLd r (1997). Distribution
and phenology of large branchiopods in Austria.
Hydrobiologia, 359:13 - 22.
engeLMann M & hahn T (2004) Vorkommen
von Lepidurus apus, Triops cancriformis,
Eubranchipus (Siphonophanes) grubii,
Tanymastix stagnalis und Branchipus schaefferi
in Deutschland und Österreich (Crustacea:
Notostraca und Anostraca). Faun. Abh. 25: 3–67.
hiLT s, gross eM, hupfer M, Morscheid h,
MähLMann J, MeLZer a, poLTZ J, sandrock s,
scharf e-M, schneider s & van de Weyer k
(2006). Restoration of submerged vegetation in
shallow eutrophic lakes – A guideline and state of
the art in Germany. Limnologica - Ecology and
Management of Inland Waters, 36(3):155-171.
hössLer J, Maier g & TessenoW u (1995). Some
notes on the ecology of a German Branchipus
schaefferi population (Crustacea: Anostraca).
Hydrobiologia, 298:105-112.
Jeppesen e, chrisToffersen k, LandkiLdehus
f, Lauridsen T, aMsinck sL, rigeT f &
sondergaard M. (2001) Fish and crustaceans in
northeast Greenland lakes with special emphasis
on interactions between Arctic charr (Salvelinus
alpinus), Lepidurus arcticus and benthic
chydorids. Hydrobiologia, 442, 329-337.
Lahr J (1998). An ecological assessment of the
hazard of eight insecticides used in Desert Locust
control, to invertebrates in temporary ponds in the
Sahel. Aquatic Ecology 32:153-162.
Legendre p & Legendre L (1998) Numerical
Ecology: Elsevier.
Loneux M & Thiéry a (1998) Révision des grands
Branchiopodes conservés au Musée de Zoologie
de l’Université de Liège: Intérêt des collections
muséologiques. Les Naturalistes belges, 79(2):33-
47.
Loneux M & WaLravens e (1998). Observation
recente de Chirocephalus diaphanus (Prevost in
Jurin, 1820) en Belgique: appel aux naturalistes.
Les Naturalistes belges, 79:9-14.
Maier g, hössLer J & TessenoW u (1998).
Succession of physical and chemical conditions
and of crustacean communities in some small,
manmade water bodies. International Review of
Hydrobiology, 83(5-6):405-418.
Marrone f & Mura g (2006). Updated status
of Anostraca, Notostraca and Spinicaudata
(Crustacea Branchiopoda) in Sicily (Italy): review
and new records. Naturalista Siciliano 30:3-19.
Mura g (1999). Current status of the Anostraca of
Italy. Hydrobiologia, 405:57-65.
Mura g (2001). Life history strategy of Chirocephalus
ruffoi (Crustacea, Anostraca) in Mediterranean
temporary mountain pools. Hydrobiologia,
462:145-156.
nhiWaTiWa T, Brendonck L, WaTerkeyn a,
vanschoenWinkeL B (2011). The importance of
landscape and habitat properties in explaining
instantaneous and long-term distributions of large
branchiopods in subtropical temporary pans.
Freshwater Biology, 56(10):1992-2008.
pauLssen L (2000). De kieuwpootkreeft Chirocephalus
diaphanus (Crustacea: Branchiopoda) ontdekt in
Limburg. Natuurhistorisch Maandblad, 89:226-
229.
peTkovski s (1997). On the presence of the genus
Branchipus Schaeffer, 1766 (Crustacea :
Anostraca) in Macedonia. Hydrobiologia, 359:37-
44.
peTrov B, cveTkovic dM (1997). Community
structure of branchiopods (Anostraca, Notostraca
and Conchostraca) in the Banat province in
Yugoslavia. Hydrobiologia, 359:23-28.
peTrov B, peTrov i (1997). The status of Anostraca,
Notostraca and Conchostraca (Crustacea :
Branchiopoda) in Yugoslavia. Hydrobiologia,
359:29-35.
rogers dc: Aquatic macroinvertebrate occurrences
and population trends in constructed and natural
vernal pools in Folsom, California. In: c.W.
WiThaM eTB, d. BeLk, W.r. ferren, Jr., and
r. ornduff (eds), Ecology, conservation, and
management of vernal pool ecosystems. California
Native Plant Society, Sacramento: 224-235.
soesBergen M (2008). Oerkreeft in karrenspoor. In:
Passie voor kleine beestjes. Edited by Kleukers R,
spencer M, BLausTein L, schWarTZ ss & cohen Je
(1999). Species richness and the proportion of
predatory animal species in temporary freshwater
pools: relationships with habitat size and
permanence. Ecology Letters, 2(3):157-166.
Thiéry a (1987): Les crustacés branchiopodes
14 Bram Vanschoenwinkel, Luc Brendonck, Tom Pinceel, Pascal Dupriez & Aline Waterkeyn
Anostraca Notostraca & Conchostraca des
milieux limniques temporaires (dayas) au Maroc.
Taxonomie, biogéographie, écologie. Doctoral
thesis, Université Aix-Marseille III, Marseille.
Thiéry a, BrTek J & gasc c (1995). Cyst morphology
of European branchiopods (Crustacea: Anostraca,
Notostraca, Spinicaudata, Laevicaudata). Bulletin
du Museum National d’Histoire Naturelle, Section
A Zoologie Biologie et Ecologie Animales, 17(1-
2):107-139.
vanschoenWinkeL B, gieLen s, vandeWaerde h,
seaMan M & Brendonck L (2008A). Relative
importance of different dispersal vectors for
small aquatic invertebrates in a rock pool
metacommunity. Ecography, 31:567-577.
vanschoenWinkeL B, WaTerkeyn a, vandecaeTsBeek
T, pineau o, griLLas p & Brendonck L (2008B):
Dispersal of freshwater invertebrates by large
terrestrial mammals: a case study with wild
boar (Sus scrofa) in Mediterranean wetlands.
Freshwater Biology, 53:2264-2273.
vanschoenWinkeL B, Mergeay J, pinceeL T,
WaTerkeyn a, vandeWaerde h, seaMan M,
Brendonck L (2011). Long distance dispersal of
zooplankton endemic to isolated mountaintops
- an example of an ecological process operating
on an evolutionary time scale. PLoS ONE, 6(11).
http://dx.doi.org/10.1371/journal.pone.0026730
WaTerkeyn a, griLLas p, de roeck erM, Boven L
& Brendonck L (2009). Assemblage structure and
dynamics of large branchiopods in Mediterranean
temporary wetlands: patterns and processes.
Freshwater Biology, 54(6):1256-1270.
WaTerkeyn a, vanschoenWinkeL B, eLsen s, anTon-
pardo M, griLLas p & Brendonck L (2010).
Unintentional dispersal of aquatic invertebrates via
footwear and motor vehicles in a Mediterranean
wetland area. Aquatic Conservation: Marine and
Freshwater Ecosystems, 20:580-587.
WiLLiaMs DD (2006). The biology of temporary
waters. Oxford University Press, Oxford, UK.
WiLLeMs T & de Leander L (2006). Triops herontdekt.
Bertram, 4(3):11-15.
Received: September 28th, 2012
Accepted: February 2nd, 2013
Branch editor: Schön Isa
