J OURNAL OF C RUSTACEAN B IOLOGY, 34(2), 135-143, 2014
LARGER HATCHING FRACTIONS IN AVIAN DISPERSED
ANOSTRACAN EGGS (BRANCHIOPODA)
D. Christopher Rogers 1,2,∗
1 Kansas
Biological Survey, and the Biodiversity Institute, Kansas University, Higuchi Hall, 2101 Constant Avenue,
Lawrence, KS 66047-3759, USA
2 University of New England, Armidale, NSW 2351, Australia
ABSTRACT
Anostracan crustacean eggs were collected from various materials leaving and entering branchiopod habitats. The eggs were cultured
from allochthonous dust and mud, bird faeces and stomach contents. Eggs that passed through aquatic bird digestive tracts hatched in
significantly larger fractions than eggs dispersed by other vectors and eggs from resident habitat egg banks. Predator dispersed eggs would
necessarily have a greater chance of reaching suitable habitat than eggs that are randomly dispersed (such as by wind). This larger hatching
fraction would amplify the priority effects of habitat monopolisation should the eggs be deposited in unoccupied habitat.
K EY W ORDS: Anostraca, egg bank, monopolization hypothesis, priority effects
DOI: 10.1163/1937240X-00002220
I NTRODUCTION
Anostraca are typically found in episodic aquatic habitats
(Brendonck et al., 2008; Rogers, 2009) with the majority of
taxa found in episodically astatic wetlands with little or no
connectivity to other aquatic habitats (Rogers, 2009). These
habitats are islands of water in an upland sea as well as
in a sea of time due to their ephemeral nature (Ebert and
Balko, 1984). Habitats of this type vary tremendously in
their degree of episodicity in that they may dry partially or
completely every year, every few years, every few decades,
or may only receive and retain water every few years or
few decades (Williams, 1987). Some Arctic and Antarctic
habitats hold liquid water for a few weeks or months, and
are frozen solid the rest of the year. Anostracans occur in
vernal pools, woodland pools, river flood pools, rock outcrop
pools (gnammas, tinajas), playa lakes, saltpans, permafrost
wetlands, potholes and seasonal wetlands (Rogers, 2009).
When the habitat inundates with seasonal rainfall, snow
melt, or rising ground water, branchiopod eggs hatch from
the substrate. The animals grow to adult stages and produce
as many eggs as possible before the habitat dries, and the
adults die (Eriksen and Belk, 1999; Brendonck et al., 2008;
Rogers, 2009).
Dispersal studies using gene flow, point to dispersal being
a rare or infrequent event due to strong patterns of genetic
differentiation and founder effects among localised populations of passively dispersing seasonally astatic wetland organisms (Belk and Cole, 1975; Dumont et al., 1991; Fugate, 1992; Lynch and Spitze, 1994; De Meester, 1996; De
Meester et al., 2002; Bohonak and Jenkins, 2003). However,
numerous studies demonstrate that passive dispersal occurs
(Proctor, 1964; Horne, 1966; Moore and Faust, 1972; Rid∗ E-mail:
doch et al., 1994; Bohonak, 1999; Brendonck and Riddoch,
1999; Brendonck et al., 2000; Beladjal et al., 2007; Hulsmans et al., 2007; Sanchez et al., 2007; Vanschoenwinkel
et al., 2008a, b, c, 2009, 2011; Beladjal and Mertens, 2009;
Brochet et al., 2010; Waterkeyn et al., 2010; Schwentner et
al., 2012) via mammals, birds, fish, amphibians, crayfish, insects, and wind. This has been termed the “dispersal-gene
flow paradox” by De Meester et al. (1996, 2002, and literature cited therein). De Meester et al. (2002) proposed the
“Monopolisation Hypothesis” to explain the strong priority
effects of founder populations. Simply put this hypothesis
suggests that the rapid adaptation and growth of founder
populations impede gene flow; thus, genetic studies do not
reflect gene flow, but rather reflect colonisation patterns.
The nature of the branchiopod egg bank strongly reinforces the habitat monopolisation by the founder population.
Each egg clutch has only a small fraction hatching with each
inundation of the habitat until the clutch is exhausted (Botnariuc, 1947). This is a bet hedging strategy that protects
the population: if the pool fills with all the eggs hatching
out at the same time and then the pool dries before any of
the crustaceans can reproduce, then the population would be
lost (Ellner et al., 1998). However, if only a fraction of each
clutch hatches with each inundation, then some eggs should
remain for more favourable seasons, if some are lost in drier
years. Depending on species (genetics) and population (epigenetics), typical hatching fractions will vary between 0.2
and 70% (Lavens et al., 1986; Lavens and Sorgeloos, 1987;
Brendonck, 1996; Mura and Zarattini, 1999; Zarattini et al.,
2002 (and literature cited therein); Zarattini, 2004; Rogers,
In Review). Therefore, it follows that the lower the hatching fraction, the greater the mixing and potential inbreeding
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© The Crustacean Society, 2014. Published by Brill NV, Leiden
DOI:10.1163/1937240X-00002220
136
JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 34, NO. 2, 2014
of generations within a given habitat. For example, if a single female produces a 300-egg clutch, and only 6% fraction
hatches with each inundation, then a clutch fraction could
hatch each year for 17 years. Since the adults move at random within their habitat, the odds of any one individual from
any one generation reproducing with another of the same
generation is very low.
Compounding this effect is soils in some pool habitats
shrink and crack as they dry, with the margins collapsing
into the cracks. By this process the soil column will “turn
over” through time (Rattan, 2008), mixing the surface debris
with the upper soil horizon removing and returning eggs
to the egg bank. Branchiopod eggs have rhodopsin in the
shells, which after being activated by water, reacts to the
light, and activates the quiescent embryo (Murugan and
Dumont, 1995); the rhodopsin activation trigger is thought to
prevent buried eggs from hatching. Depending on substrate
type, soils may turnover every 3 to 100 years or more
(McManus, 1999). This turnover has the potential to mix
eggs of different generations across even greater lengths of
time.
This can be further exacerbated by other animals that
may use the habitat. I have collected limnephilid caddisfly
larvae (Insecta: Trichoptera) where the eggs of anostracans,
notostracans, and spinicaudatans as well as cladoceran
ephippia were incorporated into their protective cases. The
caddisfly larvae bury themselves in the wetland substrate
during pupation, abandoning their cases upon emergence:
eventually substrate turnover should bring those eggs back
to the surface. Wild and domestic ungulates (cattle, water
buffalo), tapir, and elephants are all known to wallow in
astatic wetlands, churning and turning over the substrate
(Sanoamuang and Sangphan, 2006; Vanschoenwinkel et al.,
2008a, b, c, 2011; Waterkeyn et al., 2010). Furthermore,
wind will disperse eggs from and potentially into habitats
(Cáceres and Soluk, 2002; Vanschoenwinkel et al., 2008a,
b, c, 2009).
This mixing effect would necessarily create a buffering
effect in a given population, stabilizing the population
genetic structure (Thornhill and Alcock, 1983; Schram,
1986; Ellner and Hairston, 1994; Hairston and Kearns,
2002). New genes sporadically flowing into a population
would be quickly lost in the background noise of the
larger population (Thornhill and Alcock, 1983; Ellner and
Hairston, 1994; Hairston and Kearns, 2002) as it would
be unlikely that minority new colonists would mate with
each other instead individuals of the established conspecific
population.
Specific dispersal pathways as relating to gene flow
and dispersal are less predictable when multiple vectors
are involved, especially as actual dispersal (the number of
eggs leaving a given habitat) and effective dispersal (the
number of eggs reaching suitable habitat) may be quite
different. Although the eggs readily disperse, there is no
guarantee that the eggs will reach suitable habitat. Eggs
transported by a vector that specifically moves between
anostracan habitats would provide a greater chance of the
eggs reaching a potentially suitable habitat, than eggs that
are more randomly dispersed. Anostracan eggs are passively
dispersed, however eggs moved by a predator such as a duck,
which selects for the same habitat, would be a “directed”
passive dispersal vector, whereas wind would be a “random”
passive dispersal vector.
Anostracans are well known as important food resources
for many aquatic bird taxa (e.g., Cottam, 1939; Proctor,
1964; Horne, 1966; Swanson et al., 1974; Krapu, 1974; MacDonald, 1980; Donald, 1983; Camara et al., 1987; Pegrsson
and Nystrom, 1988; Saunders et al., 1993; Brochet et al.,
2010). Therefore, I hypothesise that “directed” passively dispersed anostracan eggs should be selected for a higher hatching frequency than “randomly” passively dispersed eggs.
M ETHODS AND M ATERIALS
I quantitatively collected anostracan eggs at three pools from water bird
droppings and from the habitat substrate. The eggs were cultured, and per
cent hatch was compared. Additionally, I qualitatively collected eggs from
various dispersal vectors in North and South America.
Quantitative Study
Mallard (Anas platyrhynchos L., 1758), killdeer (Charadrius vociferus L.,
1758), and greater yellowlegs (Tringa melanoleuca Gmelin, 1789) were
observed with a spotting scope while they were on pool margins and
dry “upland” areas, adjacent to three temporary pools in a railroad toedrain in San Joaquin County, north of Lodi, CA, USA. This habitat is
artificial, unvegetated, and in season contains the anostracan Branchinecta
mesovallensis Belk and Fugate, 1999 in large numbers. The physical
parameters of the three pools are presented in Table 1. All three pools
are situated close together, such that the birds could easily walk from one
pool to another. When the birds were observed to defecate, the faeces
were collected. Only faeces freshly deposited above the pool margins,
observed when produced, were collected. Faecal samples for each bird
species were collected into separate containers. Three 20 ml faecal samples
were collected, one from each of the bird species, aggregated from multiple
individuals. Droppings from many birds per species were used, and were
collected over five days from 25-30 March 2013. The soil beneath and
around the faeces (10 cm × 10 cm × 5 cm depth) was collected separately
and for each faecal sample was collected into separate containers to
determine contamination of the dropping (if any) (labelled in Results as
“faecal soil samples” in Table 2 and “faecal soil” in Table 3). An additional
soil sample (10 cm × 10 cm × 5 cm depth) was collected from each of the
three pools from the deepest portions of the pools, where eggs would most
likely accumulate.
The collected samples were prepared for examination in the laboratory
by dissolving the matrix (soil, faeces) in water and sieving the material
through 300- and 150 μm pore size screens. The small size of these
screens ensures that the 200 μm shrimp eggs (Hill and Shepard, 1997) were
retained. The portion of each sample retained in the screens was dissolved in
a brine solution to separate the organic material from the inorganic material.
The organic fraction was poured off of the brine solution into a 150 μm pore
size screen, and rinsed with tap water. This fraction was then transferred
to labelled Petri dishes, and allowed to air dry. The dried organic fraction
was then examined under a microscope for the presence of anostracan
eggs. The eggs were counted and only undamaged eggs were used in the
culturing experiments and the statistics. Damaged eggs were discarded. The
undamaged eggs were subjected to hatching conditions (culture methods
below) three times. The eggs were dried completely between each culture
attempt.
Hatching fractions were calculated as percentages of the total amount
of eggs recovered from a given sample. Hatching fractions were compared
Table 1. Location and dimensions of the quantitative study site pools,
Lodi, San Joaquin County, CA, USA.
Pool
1
2
3
Latitude
Longitude
38°10 26.00
38°10 28.42
38°10 29.82
121°14 35.80
121°14 35.89
121°14 35.93
Length Width Average depth
82 m
15 m
42 m
11 m
4m
6m
30 cm
10 cm
20 cm
137
ROGERS: ANOSTRACAN DISPERSAL AND EVOLUTION
Table 2.
Specific numbers of recovered anostracan eggs from all studies.
Source
Total eggs recovered
Total damaged eggs
% damaged eggs
Total undamaged eggs
% undamaged eggs
631
2501
4346
5860
416
180
150
331
205
350
147
472
1625
3113
4395
111
99
15
66
41
56
41
75
65
72
75
27
55
10
20
20
16
28
159
876
1233
1465
305
81
135
265
164
294
106
25
35
28
25
63
45
90
80
80
84
72
Mallard
Killdeer
Yellowlegs
Duck stomach
Tangle trap
Vehicle displaced dust
Vehicle mud (Brazil)
Vehicle mud (USA)
Boot mud (NM)
Boot mud (CA)
Cattle mud
using multiple Welch’s T -tests (Welch, 1947), with the null hypothesis that
all eggs should hatch in similar fractions.
Qualitative Study
Various materials entering or leaving the pools were collected and examined
for branchiopod crustacean eggs. The small sample sizes and serendipitous
nature of most collections prevented attempts at quantitative analyses. As
appropriate, averages and standard deviations were calculated. I attempted
to collect eggs from various sources and when I did, I attempted to hatch
them, except for the Brazilian material, which remained in that nation. Only
intact eggs were used. Damaged eggs were discarded.
The pools were located in Minas Gerais State, Brazil, and California,
New Mexico, Nevada, Oregon and Washington states, USA.
Wind Blown Material.—Wind carried dust carried was collected using
tangle traps. A tangle trap is a square of card covered with an adhesive
chemical. Tangle traps were attached to 1.5-m stakes, and stuck upright into
the ground every 10 m for 100 m along the prevailing wind direction leading
from one side of a dry desert pool in Lassen County, CA, USA, that supports
the anostracan Branchinecta hiberna Rogers and Fugate, 2001. The stakes
held the tangle traps one meter above the ground surface, keeping the trap
above the vegetation. After seven days the traps were collected, returned to
the laboratory and examined for anostracan eggs.
Dust displaced from the substrate from a pool in Washoe County, NV,
USA, was collected from adjacent vegetation, after some unknown person
or persons in off road vehicle(s) had driven around inside the dry pool
(presumably for recreational purposes) for some period of time. The dust
was collected randomly from the surrounding vegetation in five 5 ml
samples. To speculate, this type of substrate disturbance might mimic
effects of large ungulate herds, whirl winds (dust devils or whirly-whirlys),
or high velocity winds. This pool supports the anostracan Branchinecta
mackini Dexter, 1956.
Mud.—Mud was collected leaving pools by various means. Mud was
removed from the wheel wells of vehicles that were driven through pools
by local citizens in Nova Lima, Minas Gerais, Brazil and Otay Mesa, CA,
USA. The vehicle in Brazil was an off road recreational vehicle, which
passed through a pool supporting the anostracan Branchinecta ferrolimneta
Rogers and Ferreira, 2007. The vehicle in the USA belonged to the US
Border Patrol, which had passed through pools supporting the anostracans
Branchinecta sandiegonensis Fugate, 1993 and Streptocephalus woottoni
Eng et al., 1990. One 100 ml sample was collected from each vehicle. In
both instances, the drivers were hailed and mud samples were requested
from their vehicles. Both parties were surprised but allowed me to collect
the mud.
Table 3. Undamaged anostracan eggs recovered from bird faeces and soil at the Lodi, USA site. Note: 28 faecal soil samples that did not contain eggs are
not included. Ave = average, SD = standard deviation.
Sample/aggregates
Eggs collected
Taxa recovered
% hatch
Ave/SD
Culture 1
Culture 2
Culture 3
311
Branchinecta mesovallensis
Branchinecta lindahli
Branchinecta mesovallensis
Branchinecta mesovallensis
Branchinecta lynchi
Linderiella occidentalis
21.38
13.21
36.42
29.39
14.32
41.80
20.13
15.09
34.82
26.03
7.48
28.62
11.32
8.81
22.03
15.84
3.36
16.40
17.61/4.48
12.37/2.64
31.09/6.44
23.75/5.76
8.39/4.52
28.94/10.37
Faecal soil samples
4
41
21
18
24
8
34
16
22
Branchinecta mesovallensis
Branchinecta mesovallensis
Branchinecta mesovallensis
Branchinecta mesovallensis
Branchinecta mesovallensis
Branchinecta mesovallensis
Branchinecta mesovallensis
Branchinecta mesovallensis
Branchinecta mesovallensis
6.25
0.00
4.88
0.00
5.56
0.00
4.55
0.00
4.17
0.00
0.00
0.00
4.76
0.00
0.00
4.55
8.82
0.00
6.25
12.50
4.88
9.52
5.56
0.00
0.00
0.00
4.17
4.17/2.95
4.17/5.89
3.25/2.30
4.76/3.89
3.70/2.62
0.00/0.00
3.03/2.14
2.94/4.16
2.78/1.96
Soil sample pool A
Soil sample pool B
Soil sample pool C
1799
2634
6197
Branchinecta mesovallensis
Branchinecta mesovallensis
Branchinecta mesovallensis
4.67
3.87
2.86
6.73
3.57
4.49
5.50
3.00
3.29
5.63/0.84
3.48/0.36
3.54/0.69
Mallard faeces/5
159
Killdeer faeces/18
Greater Yellowlegs faeces/14
876
922
138
JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 34, NO. 2, 2014
Mud was collected from the boots and vehicle floor mats of field
biologists studying temporary pools from: 1) New Mexico and 2) northern
California. In New Mexico, several pools were visited, which contained
Streptocephalus mackini Moore, 1966, S. dorothae Mackin, 1942 and
Thamnocephalus platyurus Packard, 1879. In California, several pools were
visited, which contained B. mackini, B. gigas Lynch, 1937, B. coloradensis
Packard, 1874, B. disimilis Lynch, 1972, Eubranchipus bundyi Forbes,
1876, and E. serratus Forbes, 1876. A single 120 ml sample was collected
from the New Mexico field survey and a single 100 ml sample was collected
from the California field survey.
Mud was collected from the hooves of cattle that had been wading
at Poison Lake, Lassen County, California. Poison Lake supports the
anostracans Branchinecta coloradensis and Eubranchipus serratus. One
combined 125 ml sample was collected from mud dropped by three separate
cows, during the same site visit.
Waterfowl Gastrointestinal Contents.—Several duck hunters donated gastrointestinal tracts of 11 ducks to this study from southern Oregon (Lake
County) and northern Nevada (Humboldt County), USA. The stomach contents were emptied into Petri dishes, by washing the contents out with distilled water. The specific origins of the birds are not known; however, they
were all taken in areas where the vast majority of aquatic habitats were temporary wetlands supporting anostracan populations. Only seven ducks (six
mallards and one bufflehead) had branchiopod eggs. The remaining four
ducks (one mallard, three American widgeon) lacked branchiopod eggs.
Culture
Eggs collected were cultured to adult stages when possible. Most of the
eggs captured from dust or birds were damaged. Damaged eggs were not
cultured. Herein, hatching fraction is calculated as the percentage of each
species cultured from the total number of eggs recovered from a given
sample.
Each collection of eggs was cultured separately and culture for each
was attempted once, with the exception of the material collected from
the Lodi, CA, USA site. The Lodi site egg samples were cultured three
times, and average per cent hatch and standard deviation was calculated for
each. Adult anostracans were reared from the recovered eggs using methods
following US Environmental Protection Agency (1985), Belk et al. (1990),
Maeda-Martinez et al. (1995a, b) and Jawahar and Dumont (1995). All dry
eggs were removed from the filtered debris left over from the soil sieving.
Undamaged eggs were placed in 30-liter containers in an incubator (Thermo
Scientific, Precision Incubator). Distilled water was added to the containers,
which were then incubated at 9-12°C, 14-17°C, 9-22°C and 23-27°C.
Nauplii were transferred to 2.5-liter culture chambers. Nauplii were
fed on champagne maker’s yeast or standard Daphnia-food that includes
fish food, fish oil, baker’s yeast, and the alga Selenastrum capricornutum.
The nauplii were then reared to maturity. Adult anostracans reared from
culture were killed in 90% ethyl alcohol, and identified under a stereo
dissection microscope. Identifications were made based upon comparisons
with specimens in my collections, the original species descriptions and
professional experience.
R ESULTS
Anostracan eggs were collected using all of the methods employed. The specific results are presented in Tables 1-7. It
Table 4.
should be noted, that not only were anostracan eggs captured and viably cultured, but also the eggs (or ephippia)
of tadpole shrimp, clam shrimp, cladocerans, copepods, and
ostracodes, as well as turbellarian cocoons, and adult ostracodes aestivating in their closed carapaces (adult ostracodes in closed carapaces were collected in some dust and
mud samples; within an hour of being hydrated they began to swim, even after being kept dry for several months
(see Horne, 1993)). Sponge gemmules and bryozoan statoblasts were also recovered but no attempt was made to culture them.
Quantitative Study
The specific results are presented in Tables 2, 3 and 4. Five
Mallard faecal samples and 14 Greater Yellowlegs faecal
samples were collected from pool 1. Eighteen Killdeer faecal samples were collected from all three pools. The faeces
for each species were combined to make a single sample.
The three bird faecal samples (one for each species) together
yielded 1957 eggs from the three species, two of which,
Branchinecta lindahli Packard, 1883 and Linderiella occidentalis (Dodds, 1923), do not occur in the study pools but
are known from other habitats within a 6 km radius. The eggs
from each sample were cultured three times. The combined
Mallard faecal samples had 159 undamaged Branchinecta
eggs (out of 631 total). Of the 143 eggs that hatched from
the combined Mallard faecal samples, 83 were B. mesovallensis (average hatching fraction of 17.46%), and 59 were
B. lindahli (average hatching fraction of 12.37%). The combined Killdeer samples had 876 undamaged Branchinecta
eggs (out of 2501 total), with 775 hatching out as B. mesovallensis (average hatching fraction of 31.09%). The combined Greater Yellowlegs samples had 311 undamaged Linderiella occidentalis eggs (out of 617 total; average hatching
fraction of 28.94%) and 922 undamaged Branchinecta eggs
(out of 3729 total), comprised of B. mesovallensis (average
hatching fraction of 23.75%) and B. lynchi (average hatching
fraction of 8.39%).
Only Branchinecta eggs were used for the t-tests and
these were aggregated as “Branchinecta” for each bird
species. Hatching fractions among bird samples and among
pool samples were not significantly different (Table 3).
Faecal soil samples had such low numbers of eggs present
(Table 2) that any variation in hatching percentage among
samples would likely be due to sampling error. Hatching
fractions between pool sediment samples and faecal soil
Undamaged anostracan eggs recovered from bird faeces and soil at the Lodi, USA site. Welch’s T -test results. ∗ Significant result.
Comparison
Pool 1 vs Pool 2
Pool 1 vs Pool 3
Pool 2 vs Pool 3
Mallard vs Killdeer
Mallard vs Yellowlegs
Killdeer vs Yellowlegs
Pools vs faecal soil
Faecal soil vs bird faeces
Pools vs bird faeces
P value
95% CI
Mean
T value
df
Standard Error of Difference
0.0296
0.0539
0.9094
0.8766
0.8151
0.907
0.3132
>0.0001∗
>0.0001∗
0.3472 to 3.9595
−0.0567 to 4.2300
−1.5949 to 1.4616
−19.7397 to 17.519
−26.1758 to 21.8558
−24.4884 to 22.3884
−9.0500 to 2.9366
77.5752 to 89.2248
72.7375 to 87.9492
2.1533
2.0867
−0.0667
−1.1
−2.16
−1.05
3.0567
83.4000
80.3433
3.3102
2.703
0.1211
0.1654
0.2497
0.1244
1.2092
31.9030
29.3285
4
4
4
4
4
4
3
10
3
0.651
0.772
0.55
6.71
8.65
8.442
2.528
2.614
2.739
139
ROGERS: ANOSTRACAN DISPERSAL AND EVOLUTION
Table 5.
Undamaged anostracan eggs recovered from qualitative studies.
Source
Sample size
No. of replicates
Total eggs recovered
No. of taxa expected
No. of taxa recovered
Tangle traps
Displaced dust
Vehicle mud (CA)
Boot mud (NM)
Boot mud (CA)
Mud from livestock
Bird gastrointestinal contents
10 cm2
5 ml
100 ml
120 ml
100 ml
125 ml
Not constant
10
5
1
1
1
1
7
416
81
265
164
294
106
1465
1
1
2
3
6
2
–
3
1
2
6
8
3
6
samples was not significantly different (Table 3). Hatching
fractions between bird faecal samples and pool samples and
hatching fractions between bird faecal samples and faecal
soil samples were extremely statistically significant.
Qualitative Study
Wind Blown Material.—The tangle traps captured 416 eggs
(Tables 2 and 5). The eggs were not cultured, as they could
not be removed from the adhesive without destroying them.
Eighty-one undamaged eggs (45% of eggs recovered)
were collected from the dust displaced by the off road
vehicular activities (Tables 2, 5 and 6). Eggs of Branchinecta
mackini were reared from the samples, with a hatch of
2.47%.
Mud.—The specific results are presented in Tables 2, 5 and
6. Mud collected from vehicles in Brazil contained 135
undamaged eggs of Branchinecta (90% of recovered eggs),
but they were not cultured (as no permits were granted to
remove the material from the country). Mud from vehicles
in the USA contained 249 undamaged eggs of Branchinecta
sandiegonensis (83% of recovered eggs) and 16 undamaged
eggs of Streptocephalus woottoni (80% of recovered eggs).
Both species were cultured (1.88 and 1.51%, respectively).
Mud collected from the boots and vehicle floor mats of
field biologists studying temporary pools across northern
Table 6.
New Mexico yielded 164 undamaged eggs (80% of recovered eggs). (It is not possible by light microscopy to separate the various Streptocephalus or Thamnocephalus by
egg morphology from their congeners.) Although only three
species were expected from the mud collected, six species
were reared: S. mackini (6.74% hatch), S. dorothae (3.86%),
S. henridumontis Maeda-Martínez et al., 2005 (1.23%), T.
platyurus (0.61%), T. mexicanus Linder, 1941 (0.61%) and
Branchinecta packardi Pearse, 1912 (5.52%).
Mud collected from the boots and vehicle floor mats of
field biologists collecting in northern California, yielded 294
undamaged eggs (84% of eggs recovered). Six species were
expected, but eight species were reared: B. mackini (1.53%
hatch), B. coloradensis (3.75%), B. disimilis (1.36%), B.
gigas (0.34%), Eubranchipus bundyi (0%), E. serratus (0%),
B. hiberna (2.73%) and B. lindahli Packard, 1883 (3.07%).
The mud collected from cattle hooves at Poison Lake,
USA had 106 eggs recovered from two expected species and
one unexpected species: Branchinecta coloradensis (1.89%
hatch), Eubranchipus serratus (0%), and the unexpected B.
oriena (1.88%).
Waterfowl Gastrointestinal Contents.—The specific results
are presented in Tables 2, 5 and 7. Seven out of 11 ducks
had anostracan eggs present in the contents washed from
Recovered anostracan undamaged egg hatchability.
Source
Taxa expected
Taxa recovered
Displaced dust
Vehicle mud (CA)
Branchinecta mackini
Branchinecta sandiegonensis
Streptocephalus woottoni
Streptocephalus mackini
Streptocephalus dorothae
Thamnocephalus platyurus
Branchinecta mackini
Branchinecta sandiegonensis
Streptocephalus woottoni
Streptocephalus mackini
Streptocephalus dorothae
Thamnocephalus platyurus
Streptocephalus henridumontis
Branchinecta packardi
Thamnocephalus mexicanus
Branchinecta mackini
Branchinecta coloradensis
Branchinecta dissimilis
Branchinecta gigas
Eubranchipus bundyi
Eubranchipus serratus
Branchinecta hiberna
Branchinecta lindahli
Branchinecta coloradensis
Eubranchipus serratus
Branchinecta oriena
Boot mud (NM)
Boot mud (CA)
Branchinecta mackini
Branchinecta coloradensis
Branchinecta dissimilis
Branchinecta gigas
Eubranchipus bundyi
Eubranchipus serratus
Mud from livestock
Branchinecta coloradensis
Eubranchipus serratus
Branchinecta oriena
% hatch
2.47
1.88
1.51
6.74
3.68
0.61
1.23
5.52
0.61
1.53
3.75
1.36
0.34
0
0
2.73
3.07
1.89
0
1.88
140
Table 7.
JOURNAL OF CRUSTACEAN BIOLOGY, VOL. 34, NO. 2, 2014
Anostracans and undamaged anostracan eggs recovered from duck gastrointestinal tracts.
Duck species
Identifiable adult branchiopods in stomach contents
Mallard
No
348
Mallard
No
131
Mallard
Branchinecta sp.
Mallard
Branchinecta coloradensis
224
Mallard
Eubranchipus sp.
No
189
22
Mallard
Bufflehead
Branchinecta coloradensis
Branchinecta mackini
28
591
3
their gastrointestinal tracts. A total of 1465 undamaged eggs
(25% of total recovered eggs) from seven species were
recovered and five species were reared from these eggs.
All of the species represented from the cultures are known
from within 50 km of where the ducks were taken. All the
duck gastrointestinal tracts were kept in a freezer for several
months prior to examination, which may have had an effect
on egg viability.
The six mallards had six species recovered from their gastrointestinal tracts, and the one bufflehead had three species
recovered from its gastrointestinal tract. The mallards had
1436 eggs that yielded B. lindahli (9.48% hatch), B. coloradensis (average 9.97% hatch), B. mackini (6.87% hatch),
B. disimilis (average 9.44% hatch), B. hiberna (average
6.75% hatch), and Eubranchipus serratus (0% hatch). The
single bufflehead sample had 594 eggs that yielded B. coloradensis (8.25% hatch), B. mackini (9.43% hatch) and B.
gigas (0% hatch).
Culture
The specific results are presented in Tables 2-7. No eggs
were cultured from the tangle traps, as it was not possible to remove the eggs without damaging them. Eggs collected from all other methods had some percentage hatch.
The greatest hatching fractions came from eggs that were
collected from bird gastrointestinal tracts and faeces.
D ISCUSSION
The significantly higher per cent hatching fractions in eggs
that passed through birds demonstrates stronger selection
for “directed” passive dispersal. Since potential egg vectors such as aquatic birds and insects are more likely to
travel directly from one suitable habitat to another, there
should logically be stronger selection for these “directed”
passively dispersed eggs as opposed to randomly dispersed
eggs, since there is a greater likelihood of these individuals
surviving and reproducing. Since predator transported eggs
have a higher hatching fraction than randomly dispersed
eggs, a predator transported founding population would have
a significantly larger colonial population in an unoccupied
Eggs collected
92
Taxa recovered
Branchinecta lindahli
Branchinecta coloradensis
Branchinecta coloradensis
Branchinecta mackini
Branchinecta disimilis
Branchinecta hiberna
Branchinecta coloradensis
Branchinecta hiberna
Branchinecta coloradensis
Eubranchipus serratus
Branchinecta disimilis
Branchinecta coloradensis
Branchinecta coloradensis
Branchinecta mackini
Branchinecta gigas
Branchinecta coloradensis
% hatch
9.48
9.77
8.40
6.87
9.78
5.43
11.96
8.04
8.93
0
9.09
13.64
7.14
9.43
0
8.25
habitat. This would further amplify the founder population
monopolisation of new habitats (sensu De Meester et al.,
2002) and strengthen priority effects, in that the first generations would hatch at a higher fraction than subsequent generations, allowing the founding population to more rapidly
monopolize habitat resources than randomly dispersed eggs,
and establish an egg bank that could resist additional colonial events.
These results are similar to those from studies involved
in frugivory and seed ingestion and dispersal, wherein
seeds ingested and defecated by frugivorus vertebrates
(birds, mammals) had higher germination fractions than
noningested seeds (Murray et al., 1994; Godínez-Alvarez
et al., 2002; Côrtes and Uriarte, 2012 and references cited
therein) and that some frugivores tended to disperse the
seeds to optimal germination habitats (Godínez-Alvarez et
al., 2002, and references cited therein). Furthermore, it has
long been known that branchiopod eggs are resistant to
avian digestive enzymes (Proctor, 1964; Horne, 1966, 1993),
and that certain treatments of anostracan eggs by peroxides
will increase hatching fraction percentages (Robbins et al.,
2010). Horne (1966) found that the eggs of Artemia were
resistant to avian digestive enzymes but found no difference
in hatching fractions across treatments. Dumont et al. (1992)
increased hatching fractions (referred to as accelerated
hatching) in anostracan eggs (Thamnocephalus platyurus
Packard, 1877 and Streptocephalus dichotomus Baird, 1860)
treated with retinoic acid and calcium ionophores.
It should also be noted that there were much higher
numbers of damaged eggs from birds than from any other
source. This makes sense as the ingested anostracans would
be ground in the bird’s crop and stomach. Although the
difference between the number of undamaged “directed”
passively dispersed eggs and randomly passively dispersed
eggs is greatly different, it is doubtful that this would
mitigate hatching fraction size differences, such that all
vectors are not equally successful in transporting eggs to
viable habitats.
These results also support the findings of similar studies,
in that anostracan eggs are actively leaving the natal habitats,
141
ROGERS: ANOSTRACAN DISPERSAL AND EVOLUTION
can be captured in transit, and are viable (Proctor, 1964;
Horne, 1966; Moore and Faust, 1972; Riddoch et al., 1994;
Bohonak, 1999; Brendonck and Riddoch, 1999; Brendonck
et al., 2000; Beladjal et al., 2007; Hulsmans et al., 2007;
Sanchez et al., 2007; Vanschoenwinkel et al., 2008a, b, c,
2009, 2011; Beladjal and Mertens, 2009; Brochet et al.,
2010; Waterkeyn et al., 2010). Anostracans are an important
component in aquatic bird diets (MacDonald, 1980; Camara
et al., 1987; Brochet et al., 2010), and this is further
underlined by the fact that anostracans are intermediate hosts
for a variety of avian parasites (Mura, 1995; Sánchez et al.,
2006).
Bohonak and Jenkins (2003) produced a review of passive
dispersal studies, wherein aquatic habitats were constructed
and subsequent colonisation was tracked over time. They
concluded that passive dispersal was not especially common
based on (among other things) the lack of complex communities developing in the constructed aquatic habitats. However, these and other similar colonisation studies were conducted in places where temporary aquatic habitats are few
and far between, e.g., Illinois, USA (Jenkins and Underwood, 1998; Cáceres and Soluk, 2002) and Virginia, USA
(Jenkins, 1995). In North America there are 46 anostracan
species in the arid region west of the Continental Divide,
there are 29 species found in the semiarid region of the Great
Plains between the Continental Divide and the Mississippi
River, and a mere eight species (all either localised endemics
or widespread to the west) occur in the temperate forested regions between the Great Plains and the Atlantic Ocean (Belk
and Brtek, 1995, 1997; Brendonck et al., 2008). The great diversity in the arid west is due to the vast amounts of seasonally astatic aquatic habitats suitable for anostracans, whereas
the depauperate fauna in the east is a reflection of the lack of
suitable habitats (Tiner, 2003).
Habitat monopolisation through rapid population growth
coupled with rapid adaptation and the buffering effect of the
constantly mixing and staggered egg bank confound genetic
studies attempting to measure effective gene flow. This suggests that the constantly mixing egg bank creates a tight,
co-adapted gene pool that resists change. This greatly increased inbreeding potential within the founder colony minimizes phenotypic variation and maintains existing successful phenotypes, and resists new genetic input from outside
the habitat. The lack of genetic variability between individual habitats in close proximity (Abreu-Grobois, 1987; Pila
and Beardmore, 1994; Gajardo et al., 1995; Brendonk et al.,
2000; Naihong et al., 2000) would argue that sufficient gene
flow can occur to establish metapopulations.
Widespread species occur in habitats that are generally
contiguous geographically or regularly visited by predatory
vectors (Schwentner et al., 2012). An anostracan species that
occurs in spatially concentrated habitats in a given area will
have selective pressures for both long and short distance
dispersing eggs due to the ready availability of suitable
habitat. Frequent, active gene exchange among local habitats
will limit local selection and develop local metapopulations,
particularly in areas where numerous pools may become
interconnected during heavy rain events (such as El Niño
events in North America, or La Niña events in Australia
and Chile) (Eriksen and Belk, 1999; Schwentner et al.,
2012). However, a geographically isolated founder colony
from a stochastic long distance dispersal event will have
long distance dispersal selected against, since there is a
remarkably low chance of dispersing to another suitable
habitat. This will impose a strong filter, selecting for eggs
that remain, further reinforcing the founder form. This may
be reflected in the fact that roughly more than a third of the
300 or so described anostracan species are known from three
or fewer localities (Belk and Brtek, 1995, 1997; Brendonck
et al., 2008; Rogers, 2009, 2013) (granted, sampling bias
may account for some of this, but not for all, especially those
in well surveyed areas such as North America and Europe).
Thus, speculatively, new species must evolve allopatrically,
in geographically isolated, unoccupied habitats, via small,
genetically isolated founder populations.
Anostracans are subject to non-directional dispersal, via
multiple passive vectors. Many strong filters act on anostracan eggs, such as egg banks, vector type, egg structural
integrity, and habitat suitability. Precinctiveness is linked
with reduced genetic variability and dispersability in colonial populations. The buffering effect of the egg bank in
established populations creates a tight, co-adapted, inbreeding gene pool that resists phenotypic variation and maintains
existing successful phenotypes, resisting new genetic input
from outside populations. Therefore, anostracan speciation
must occur allopatrically via colonisation of new or recently
unoccupied habitats.
ACKNOWLEDGEMENTS
I am grateful to Martin Schwentner, Jorgen Olesen, Lynda Beladjal, Ed
Martinko, Brian Timms and Martin Thoms for providing useful comments
on earlier drafts. I am very grateful to Alosiso Ferreira for all his help in the
field in Brazil, and to Frederick Schram for his guidance and patience.
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