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Coexistence of surface and cave amphipods in an ecotone environment


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Interspecific interactions between surface and subterranean species may be a key determinant for species distributions. Until now, the existence of competition (including predation) between these groups has not been tested. To assess the coexistence and potential role of interspecific interactions between surface Gammarus fossarum and subterranean Niphargus timavi, and to determine their micro distributions, we conducted a series of field and laboratory observations. We aimed to determine: (1) species substrate preference, (2) whether the presence of G. fossarum influences the habitat choice of N. timavi, and (3) possible predation effects on micro habitat choice of small juveniles. Throughout a small river in SW Slovenia, N. timavi was predominantly found in leaf litter and gravel, but rarely in sand. In the sand however, we exclusively found juveniles. In contrast, surface G. fossarum sheltered mainly in leaf litter. A similar, body size dependent, micro distribution was observed in G. fossarum, where small individuals were generally found in gravel and sand. The presence of G. fossarum affected the micro distribution of juvenile, but not adult, N. timavi. In the laboratory we observed predation and cannibalism in both species. Niphargus timavi, however, appeared to be a more efficient predator than G. fossarum. In particular, juvenile N. timavi were most vulnerable to preying by adults of both species. This probably affected the distribution of juvenile N. timavi that chose finer substrates when placed with adult individuals in an aquarium with granules of different size. To understand the distribution of subterranean species, the summed effect of intraspecific interactions, as well as surface - subterranean species interactions, in particular between individuals of different size, should be taken into account.
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Contributions to Zoology, 80 (2) 133-141 (2011)
Coexistence of surface and cave amphipods in an ecotone environment
Roman Luštrik1, 3, Martin Turjak1, Simona Kralj-Fišer2, Cene Fišer1
1 University of Ljubljana, Biotechnical faculty, Department of Biology, PO Box 2995, SI-1001 Ljublja na, Slovenia
2 Jovan Hadži Institute of Biology, Scientic Research Centre of the Slovenian Academy of Sciences and Arts, PO
Box 30 6, SI-1001 Ljublja na, Slovenia
3 E-mail:
Key words: Amphipoda, cannibalism, competition, ecotone, microhabitat preference, predation
Interspecic interactions between surface and subterranean spe-
cies may be a key determinant for species distributions. Until
now, the existence of competition (including predation) between
these groups has not been tested. To assess the coexistence and
potential role of interspecic interactions between surface Gam-
marus fossarum and subterranean Niphargus timavi, and to de-
termine their micro distributions, we conducted a series of eld
and laboratory observations. We aimed to deter mine: (1) species
substrate preference, (2) whether the presence of G. fossarum
inuences the habitat choice of N. timavi, and (3) possible preda-
tion effects on micro habitat choice of small juveniles. Through-
out a small river in SW Slovenia, N. timavi was predominantly
found in leaf litter and gravel, but rarely in sand. In the sand
however, we exclusively found juveniles. In contrast, surface G.
fossarum sheltered mainly in leaf litter. A similar, body size de-
pendent, micro distribution was observed in G. fossarum, where
small individuals were generally found in gravel and sand. The
presence of G. fossarum affected the micro distribution of juve-
nile, but not adult, N. timavi. In the laboratory we observed pre-
dation and cannibalism in both species. Niphargus timavi, how-
ever, appeared to be a more efcient predator than G. fossarum.
In particular, juvenile N. timavi were most vulnerable to preying
by adults of both species. This probably affected the distribution
of juvenile N. timavi tha t chose ner substrates when placed wit h
adult individuals in an aquarium with granules of different size.
To understand the distribution of subterranean species, the
summed effect of intraspecic interactions, as well as surface –
subterranean species interactions, in particular between indi-
viduals of different size, should be taken into account.
Introduction ................................................................................... 133
Material and methods .................................................................. 134
Field experiment and data analysis .................................. 134
Laboratory work and data analysis .................................. 135
Results ............................................................................................. 135
Field experiment results ....................................................... 135
Laboratory work results ....................................................... 137
Discussion ...................................................................................... 137
Acknowledgements ...................................................................... 140
References ...................................................................................... 14 0
Environmental changes may result in range expansions
of some species (e.g. Jażdżewski et al., 2004). Invasions
due to expanding species ranges inherently lead to ad-
ditional interspecic relationships. These are often
asymmetric and can eventually dramatically change the
local fauna, the survival of which in turn depends exclu-
sively on the number of appropriate refugia (Savage,
1981, 1982; Dick, 2008). Although poorly studied, caves
are not an exception. Sket (1977) reported how mild
pollution of sinking rivers enabled immigration and
survival of surface species deep in the caves, which sig-
nicantly reduced abundance of cave-specialized spe-
cies, so-called troglobionts. It is assumed that surface
species outcompete subterranean species if resources
are abundant, but conversely, subterranean species out-
compete surface species in food-limited environments
(reviewed in Culver and Pipan, 2009). If these hypoth-
eses were true, they might be of key importance for un-
derstanding distributions of subterranean species. First,
surface fauna may be a major factor in preventing move-
ment of subterranean species to the surface (Sket, 1981;
Culver and Pipan, 2009). Second, troglobiotic fauna of
small cave systems may be vulnerable to pollution
mainly on account of changes in competitive strengths
of surface versus subterranean species.
Despite the presumed importance of interspecic
interactions between surface and subterranean species
for their distributions, the existence of competition (in-
cluding predation) between them has not been explic-
itly tested before. A hypothesis about competitive and
predation interactions between surface and subterra-
nean species could be tested in ecotones, such as
springs (sensu Connell, 1980), which was the approach
taken in this study.
Our research focused on two amphipod species.
Amphipods represent a substantial portion of aquatic
134 Luštrik et al. – Coexistence of amphipods
fauna, both in biomass and in species numbers (e.g.
Conlan, 2008). They are widely distributed in both
surface and subterranean waters (Pinkster, 1978; Boto-
saneanu, 1986). The role of negative interactions such
as competition or predation has been studied exten-
sively across surface species (MacNeil et al., 1997)
with particular emphasis on invasive species (Bollache
et al., 2008; Dick, 2008). Moreover, there are also a
few reports indicating negative interspecies interac-
tions between subterranean species (e.g. Culver et al.,
1991; summarized in Culver and Pipan, 2009). Thus,
amphipods may serve as the appropriate model organ-
isms for studying interspecic interactions between
surface and subterranean species.
Recent observations of a spring in SW Slovenia
identied an appropriate natural setting with two am-
phipod species for this study. Gammarus fossarum
Koch, 1835 (Gammaridae) represents surface species
(note that this name might cover a number of cryptic
species). The species Niphargus timavi S. Karaman,
1954 (Niphargidae) can be found in surface (springs)
and subterranean habitats (Fišer et al., 2006; it could
be categorized as eutroglophile sensu Sket, 2008).
Both species coexist along the studied stretch of brook.
The spatio-temporal shares of both species vary sig-
nicantly throughout the year, suggesting that both
species may compete for space and food. We predicted
that G. fossarum, either as a result of its higher repro-
ductive potential or through enhanced predation, could
constrain the distribution of N. timavi in surface habi-
tats (Fišer et al., 2006, 2007). Indeed, the stomachs
contents corroborate the hypothesis that both species
overlap in feeding behaviour (Fišer et al., 2010).
To assess the coexistence and the potential role of
interspecic interactions between surface and subter-
ranean amphipod species, we conducted a series of
eld and laboratory observations. The setup was de-
signed to determine: (1) whether both species show
similar substrate preference, (2) whether the presence
of G. fossarum affects habitat choice of N. timavi, and
(3) whether predation has any effect on microhabitat
choice of younger and weaker juveniles (MacNeil et
al., 2008).
Material and methods
Field experiment and data analysis
We positioned 12 sampling stations along the Kolaški
potok (brook) near Ilirska Bistrica in SW Slovenia.
About 250 m below the primary spring, the brook
sinks and re-emerges as resurgence after about 150 m.
Niphargus timavi is present along the entire brook,
while Gammarus fossarum appears to be conned to
the reaches below the point of resurgence (details in
Fišer et al., 2007). Samples were collected in upstream
(control) and downstream stretches (test).
In February and March 2008, we sampled each site
for four times. We submerged six plastic cups, two for
each substrate: decaying leaf litter (predominately
beech tree leaves), sand (2-5 mm in diameter) and
gravel (5-60 mm) based on unied classication (Buol
et al., 2008). Cups were 12 cm in radius and 7 cm in
height, with 33 drilled holes (d = 10 mm). To prevent
accidental drift of the cups, we lodged them with
rocks. Thereafter, we inspected each plastic cup week-
ly and washed out all animals. Sampled amphipods
were preserved in 70% ethanol in loci, preventing any
loss due to predation after sample collection. Samples
were sorted according to species and size in the labo-
r at o r y.
The following questions were proposed:
1 Does either species show a preference for a particu-
lar substrate? To answer this, we pooled individuals
for each species by substrate categories. We tested
for differences in numbers of individuals present in
different substrate categories.
2 Does the presence of G. fossarum affect the habitat
choice of N. timavi? To answer this question, we
pooled individuals for each species by substrate
type; however, the data for N. timavi from the upper
part of the stream (above the resurgence, where
only N. timavi occurs) were treated separately from
the data collected in the lower stretch (below the
resurgence, where both species are present). We
rst tested whether the substrate preferences of N.
timavi (i.e. gravel vs. sand) in the upper and lower
stretches of the stream differ. Afterwards, we tested
whether the number of individuals of N. timavi
within a selected substrate differed between the up-
per and lower stretches of the stream (i.e. gravel
above versus gravel below the resurgence).
3 For each species we asked whether individuals of
different size invaded the same substrate. We select-
ed subsamples from various sampling sites in order
to attain at least 50 individuals of each species from
all substrate types. We estimated their body size by
measuring body length (measured from the genal
lobes, along the insertia of pereopod coxae – insertia
of pleopods – insertia along uropods) (Fišer et al.,
2009). We opted for non-parametric tests because
135Contributions to Zoology, 80 (2) – 2011
data were not normally distributed. Differences in
substrate preferences of different sized individuals
were analysed using Kruskal-Wallis test; pairwise
comparisons were done by Mann-Whitney U test
(using SPSS 14).
Laboratory work and data analysis
Given that arthropods present a part of both species’
diet (see Fišer et al., 2010), we tested whether either
species showed predatory or cannibalistic behaviour.
Collected animals were separated by species, trans-
ferred to glass aquaria in a speleolaboratory (a dark,
insulated room kept at approximately 10°C) and fed ad
libitum with leaf litter from the study site for four days.
Thereafter, we transferred the animals to Petri dishes.
The number of animals in the dishes was counted eve-
ry 24 hours for four days.
Prey size may affect the prey choice of predatory
amphipods (MacNeil et al., 2008), which implies that
fully developed individuals would prey only on small-
er individuals. To test this, we prepared con- and inter-
specic pairs of large males (>12 mm) of G. fossarum,
N. timavi and N. timavi + G. fossarum, each pair in a
separate Petri dish. All combinations were run in ve
parallels for two weeks. All 30 individuals survived
this testing period as expected, and so only small (<4
mm) and mid-sized (5-7 mm) individuals were used as
the potential prey in the experiments described below.
Furthermore, we placed three individuals of one or
a mix of both species into a Petri dish. The experimen-
tal set up was constrained by limited numbers of avail-
able small N. timavi. Each Petri dish contained either
one large G. fossarum or large N. timavi (predator) and
one out of nine possible pairs of small and/or mid-
sized G. fossarum and/or N. timavi individuals. In do-
ing so, we obtained four categories of prey (small- and
mid-sized individuals of both species), the vulnerabil-
ity of which was estimated by their survival. This ex-
perimental design allowed the estimation of prey vul-
nerability in a pair (i.e. which individual survives long-
er), however, generalizations on vulnerability of prey
category were implicit, since individual predators could
not select among all possible prey categories. Predation/
cannibalism rates were estimated from survival rates,
which were calculated from how many individuals of
each prey category survived to the next day.
We asked whether N. timavi and G. fossarum dif-
fered in predatory behaviour. To answer this, we
pooled the numbers of survivors per day for each pred-
atory species. The data were log-transformed and the
predation rate was then estimated as the slope of the
linear regression line. To test whether predation rates
of the two species were the same, we compared the
slopes of the two regression lines (coefcients) using
the Snedecor and Cochran test (Snedecor and Coch-
ra n, 1976).
To determine whether prey categories differed in
vulnerability, we pooled the data by the focal prey cat-
egories per predator species. For instance, if we were
interested in small N. timavi preyed upon by N. timavi,
we pooled the data from Petri dishes where prey of N.
timavi were two small N. timavi, small N. timavi +
small G. fossarum, small + mid-sized N. timavi and
small N. timavi + mid-sized G. fossarum. To assess
which category was most vulnerable, we pairwise test-
ed the differences in slopes of regression lines for each
prey category as described above (Snedecor and Co-
chra n, 1976).
Furthermore we asked, whether small niphargids
search shelter in ne sand due to cannibalistic pressure
or due to seeking the contact with substrate. We lled
four aquaria (100 mm × 50 mm × 200 mm) with dif-
ferently sized glass pebbles, with each layer being 50
mm thick. Top, middle and bottom layers were con-
structed with pebbles of diameter 10, 5 and 2 mm, re-
spectively. Well-aerated water from the site was used
to ll the aquaria. Due to small number of subjects per
aquarium and short experiment duration (circa one
day), no additional water aeration was provided. We
considered small juveniles to be less than 5 mm in
length and adults larger than 15 mm. We observed the
distributions of one juvenile when a) alone, b) in the
presence of an adult male and c) in the presence of an
adult female. Distribution of juveniles was examined
every 20 minutes for ve hours. Differences in distri-
butions were tested using contingency tables and χ2.
Field experiment results
Both, Gammarus fossarum and Niphargus timavi dif-
ferently inhabited the substrate types (Kruskal-Wallis:
χ2 = 7.83, d.f. = 2, p < 0.05 * and χ2 = 21.150, d.f. = 2, p
< 0.001 ***, respectively). Gammarids more often shel-
tered in leaf litter (Fig. 1, Table 1) than in gravel and
sand (Mann-Whitney U = 376.00, p < 0.05 *; U = 284.00,
p < 0.05 *, respectively). However, they did not distin-
guish between gravel and sand (U = 407.50, p > 0.1). In
contrast, Niphargus timavi showed no differ
ence in
136 Luštrik et al. – Coexistence of amphipods
choosing between leaf litter and gravel (Figs 1-2, Table
2; U = 525.00, p > 0.1), but it preferred either of those
substrates to sand (gravel – sand: U = 142.00, p < 0.001
***; leaf litter- sand: U = 185.00, p < 0.001 ***).
In general, the substrate choice of N. timavi tended
to be effected by the presence of G. fossarum (Kruskal-
Wall is: χ2 = 2.51, d.f. = 1, p > 0.1; Figs 1- 2, Table 2). In
the presence of G. fossarum, N. timavi showed similar
preferences for substrates (Kruskal-Wallis: χ2 =
22.668, d.f. = 2, p < 0.001 ***). It showed no prefer-
ences when choosing gravel or leaf litter (U = 82.00, p
> 0.1), but avoided sand (gravel – sand: U = 3.00, p <
0.001 ***; leaf litter – sand: U = 15.50, p < 0.001 ***).
Furthermore, the numbers of individuals in leaf litter
and gravel in the upper, compared to lower stretch of
the brook, showed no difference (U = 122.00, p > 0.1
and U = 105.00, p > 0.1, respectively). However, in
comparison to the upper stretch, more individuals in-
vaded sand in the lower stretch of the brook (U =
13.00, p < 0.001 ***), on account of smaller individu-
als (see Table 4).
Both species showed similar patterns in size-de-
pendent micro distribution - smaller individuals of
both species invaded their adult stage non-preferential
substrates signicantly more often than larger indi-
viduals. Individuals of N. timavi found in sand were
signicantly smaller than individuals found in gravel
Table 1. Differences in abundances of G. fossarum in different
substrates in the lower stretch of the brook. Mann-Whitney U-
Test, statistically signicant differences in boldface.
Leaf litter Gravel
Gravel U = 376.00
p < 0.05*
Sand U = 284.00 U = 407.50
p < 0.05* p > 0.1
Table 2. Differences in abundances of N. timavi in different
substrates. Values above the diagonal refer to data in the upper
stretch of the brook where N. timavi lives alone, the values be-
low the diagonal refer to data in the lower stretch of the brook
where N. timavi and G. fossarum coexist. Diagonal cells refer to
comparison of abundances of N. timavi within the same sub-
strate in the lower and upper stretch of the brook. Mann-Whit-
ney U-Test, statistically signicant differences in boldface.
Leaf litter Gravel Sand
Leaf litter U = 122.00 U = 525.00 U = 185.00
p > 0.1 p > 0.1 p < 0.001***
Gravel U = 82.00 U = 105.00 U = 142.00
p > 0.1 p > 0.1 p < 0.001***
Sand U = 15.50 U = 3.00 U = 13.00
p < 0.001*** p < 0.001*** p < 0.001***
leaf littergravelsand
Gamma rus fossarum
Niphargus timavi
number of individuals
leaf litter
number of individuals
Fig. 1. Number of individuals of G. fossarum and N. timavi in
three different substrates in the lower stretch of the brook (below
the resurgence) where the two species coexist.
Fig. 2. Number of individuals of N. timavi in the upper stretch of
the brook (above the resurgence) where the species appears
137Contributions to Zoology, 80 (2) – 2011
or leaf litter (sand-gravel: U = 757.00, p < 0.001 ***;
sand – leaf litter: U = 1008.50, p < 0.001 ***), while
body lengths of individuals found in gravel and leaf
litter did not differ (U = 974.00, p > 0.1, Tables 3-4).
For G. fossarum, leaf litter was invaded by signicant-
ly larger individuals than gravel (U = 829.50, p < 0.01
**). Invaders of leaf litter showed a trend with mar-
ginal statistical signicance to be larger than those in-
vading sand (U = 1015.50, p = 0.057). For G. fossarum,
no difference in sizes was detected between the two
types of non-preferential substrates (U = 1222.00, p >
0.1; Tables 3-4).
Laboratory work results
Niphargus timavi appeared to be a superior predator
over G. fossarum. Thirty adult N. timavi consumed
about 60% of available prey items in 24 hours and 21%
of prey survived the full ve days test period. By con-
trast, G. fossarum consumed only 24% of available
prey in the rst 24 hours and consumed only 39% of
available prey items in the ve day test period. This
pattern was consistent across prey categories. In all
cases, N. timavi preyed faster and more efciently than
G. fossarum.
Niphargus timavi preyed more efciently upon
small- over mid-sized individuals of both species. By
contrast, G. fossarum most efciently hunted small N.
timavi, while it preyed on the rest of the prey catego-
ries with roughly the same efciency (Table 5, Fig. 3).
Our data indicate that juvenile N. timavi present the
most vulnerable size (age) class in this particular
The presence of an adult changed the distribution of
juvenile niphargids. When no adult was present, juve-
niles inhabited mostly the middle layer, whereas it was
evenly distributed in the other two layers. In the pres-
ence of an adult, a juvenile was almost never found in
the layer with large pebbles, being more often found in
the layers with middle and small sized pebbles (large
pebbles: χ2 = 0.24, p < 0.01**; middle sized pebbles: χ2
= 0.235, p < 0.01**; small pebbles: χ
2 = 0.202, p <
0.05**, Table 6).
Our study shows that G. fossarum chose leaf litter
more often than gravel and sand, implying only acci-
dental and temporary use of the later two habitats. By
contrast, N. timavi chose no single substrate, but was
found in sufciently large spaces among either particle
grains or leaves. Moreover, the presence of G. fossa-
rum had only little effect on N. timavi microdistribu-
tion where the two populations overlapped (in the
lower stretch of the brook).
Differently sized individuals of both species dis-
tributed non-randomly among substrates. Body size
differences in habitat choice were greater in N. timavi
than in G. fossarum, but in both species smaller indi-
viduals sought shelter in substrates that were preferred
less by adults (gravel, sand).
Table 3. Differences in body lengths in different substrates for N.
timavi (above diagonal) and G. fossarum (below diagonal).
Mann-Whitney U-Test, statistically signicant differences in
boldface, trends in italics.
Leaf litter Gravel Sand
Leaf litter U = 974.00 U = 1008.50
p > 0.1 p < 0.001***
Gravel U = 829.50 U = 757.00
p < 0.01** p < 0.001***
Sand U = 1015.50 U = 1222.00
p > 0.05(*) p > 0.1
Table 4. Body sizes of Niphargus timavi and Gammarus fossa-
rum in three different substrates in the lower stretch of the brook
(below the resurgence), where the two species coexist.
Substrate Descriptive Niphargus Gammarus
statistic timavi fossarum
Gravel min 1.91 0.51
1. quartile 3.57 4.9
median 5.47 7.18
mean ± SD 6 ± 3.08 6.35 ± 2.62
3. quartile 7.89 8.08
max 13.63 11.15
Leaf litter min 1.17 4.3
1. quartile 3.13 5.58
median 3.73 8.37
mean ± SD 5.12 ± 2.94 8.28 ± 2.81
3. quartile 6.54 10.47
max 11.4 13.25
Fine sand min 1.1 0.81
1. quartile 2.32 2.27
median 2.52 6.56
mean ± SD 3.19 ± 2.18 6.76 ± 3.99
3. quartile 2.93 10.3
max 13.2 13.81
138 Luštrik et al. – Coexistence of amphipods
Niphargus timavi was a more efcient predator and
cannibal than G. fossarum. This predatory behaviour
may broaden available food sources, which might be
advantageous in the food-limited subterranean environ-
ment. Juvenile N. timavi, the most vulnerable prey cat-
egory, invaded sand seeking not only contact with sub-
strate, but also in response to predatory pressure from
large N. timavi whose movement through the sand was
constrained. Interpreting the micro distribution of small
N. timavi in this light matches with the eld results,
a b
Fig. 3. Effectiveness of predation (cannibalism) by adult G. fos-
sarum () and N. timavi (∆) upon differently sized individuals
of both species: a) small N. timavi, b) middle N. timavi, c) small
G. fossarum, d) middle G. fossarum and e) total effectiveness
for all aforementioned groups by adults of both species. See Ma-
terials and methods for class sizes. The slopes of all regression
lines-pairs are statistically different (p < 0.05*).
139Contributions to Zoology, 80 (2) – 2011
which seem to indicate that hiding behaviour of small
N. timavi was most pronounced in the lower stretch of
the stream, where occasional G. fossarum predation ac-
companies cannibalistic acts by larger N. timavi. Simi-
lar segregations of juvenile individuals have also been
observed at least in Niphargus rhenorhodanesis Schel-
lenberg 1937 (Mathieu et al., 1987), Thermosphaeroma
thermophilum (Richardson, 1897) (Jormalainen and
Shuster, 1997), Gammarus pseudolimnaeus Bouseld,
1958 (Williams and Moore, 1986), Gammarus pulex
(McGrath et al., 2007) and Pseudoniphargus grandi-
manus Stock, Holsinger, Sket and Iliffe, 1986 and Pseu-
doniphargus carpalis Stock, Holsinger, Sket and Iliffe,
1986 by Stock et al. (1986).
In contrast, G. fossarum showed less inter- and in-
traspecic interactions. The distribution of differently
sized animals in different substrates may simply reect
rivalry for the preferred substrate, where the largest
individuals outcompete smaller ones. Similar results
were obtained in observations in aquaria (unpublished
Micro distribution of N. timavi and G. fossarum ap-
parently depends on a broad array of biotic and abiotic
factors. The role of the substrate, interspecic competi-
tion, intraguild predation or a combination of all of the
above have been broadly acknowledged to structure
various communities (Crowder and Cooper, 1982; Po-
lis, 1984, 1989; Skadsheim, 1984; Adams et al., 1987;
Dick, 1996, 2008; MacNeil et al., 1997, 2008; Beisel et
al., 1998; Dick and Platvoet, 2000; Dick et al., 2002;
van Riel et al., 2006; McGrath et al., 2007; Kley et al.,
2009; MacNeil and Briffa, 2009). Nevertheless, at least
in certain cases, intraspecic relationships has been ne-
glected or obscured on account of interspecic rela-
tionships (Sket, 1981; Culver and Pipan, 2009). In this
particular study, the hypothesis of competition between
surface and subterranean fauna remains generally un-
supported. However, juvenile N. timavi were observed
to take refuge in ner substrates (sand) more often in
the presence of cannibalism and predation by their con-
specics and G. fossarum, respectively. Large-scale ef-
fects may arise due to additive effects of predation and
cannibalism upon the smallest (the most vulnerable)
individuals of N. timavi, thereby signicantly decreas-
ing the number of individuals in the next generation.
To conclude, the two species differed in their habi-
tat choice. Smaller and weaker individuals of N. timavi
and G. fossarum inhabited microhabitat less preferred
by adults, probably due to cannibalism and competi-
tion, respectively. Despite the difference in habitat
choice between the two species, the occasional preda-
tion of G. fossarum upon juvenile N. timavi in addition
to cannibalism may accelerate the decrease of
niphargid population along the brook (as observed by
Fišer et al., 2007). To understand distribution of sub-
terranean species, the summed effect of intraspecic
Table 5. Differences in predation preferences by N. timavi (above diagonal), G. fossarum (below diagonal) and the differences between
species. Each cell indicates the most vulnerable prey category and probability that coefcients of the two regression lines are the same.
Statistically signicant values are indicated in boldface, statistical trends are indicated in italics. Diagonal cells list the probability that
both species equally prey the particular prey category.
Small N. timavi Middle N. timavi Small G. fossarum Middle G. fossarum
Small N. timavi N. timavi small N. timavi small N. timavi
p > 0.05 (*) p < 0.05 * p > 0.1 p < 0.05 *
Middle N. timavi small N. timavi N. timavi small G. fossarum
p < 0.01 ** p < 0.01 ** p < 0.05 * p > 0.1
Small G. fossarum small niphargid small G. fossarum N. timavi small G. fossarum
p < 0.05 * p > 0.05 (*) p < 0.01 ** p < 0.05 *
Middle G. fossarum small N. timavi N. timavi
p < 0.01 ** p > 0.1 p > 0.1 p < 0.05 *
Table 6. Distribution of small sized niphargids in layers of arti-
cial substrate of different grain size when alone and in the pres-
ence of adult conspecic under laboratory settings.
Substrate size Alone Adult present
10 mm pebbles 12 2 4
5 mm pebbles 33 47 32
2 mm pebbles 15 11 24
140 Luštrik et al. – Coexistence of amphipods
interactions as well as surface – subterranean species
interactions, in particular between differently sized in-
dividuals, should be taken into account.
The paper is dedicated to the memory of Miha Valič, who ac-
companied Cene Fišer in the very rst eld observations in 2004.
The Tibetan ‘Turquoise Goddess’ brought Miha to eternity in au-
tumn 2008. We would like to thank Antonija Bogdan, Melinda
Gal, Maja Herbaj, Mojca Horvat, Melita Korošec, Žana Kovačec,
Boštjan Markelc, Sara Novak, Eva Ogorevc, Luka Predojević,
Mateja Pustovrh, Tina Sečen, Darja Slana, Mojca Škrget and
Anže Zorin for assisting in the eld and laborator y. We are grate-
ful to Peter Trontelj, Yael Kisel, Maar ten de Groot, Boris Sket,
Daiqin Li and two reviewers for giving valuable comments on
our manuscript and language. The work was partially funded by
the Slovenian Ministry of Education and Spor t.
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Received: 24 March 2010
Revised and accepted: 10 January 2011
Published online: 14 April 2011
Editor: R. Vonk
... There is also a substantial variation in the shape of the gnathopod, which determines the size of the grip (Fišer et al., 2019). Third, Niphargus species feed on diverse food resources, including decaying plant material, detritus, and carcasses, but also exhibit active predatory behavior (Ercoli et al., 2019;Fišer et al., 2010;Pacioglu et al., 2020), including cannibalism (Luštrik et al., 2011;Sket, 1958). Finally, the wellestablished phylogeny of Niphargus (Delić et al., 2020) enables us to test for trait-function relationships while accounting for statistical error stemming from phylogenetic relatedness. ...
... Pairs of species in which the overlap proportion was below 0.05 in at least 95% of the estimates are boldfaced. PC: pairwise comparison between species (abbreviations of species names as in Figure 1); CI, confidence interval from scavenging, past behavioural studies and field observations strongly support the predatory nature of some Niphargus species (Luštrik et al., 2011;Sket, 1958). ...
Identifying the relationships between morphology and trophic niche is at the core of functional morphology. Low resource diversity and fluxes of organic carbon are expected to constrain trophic specialisation of morphological structures because food resources are too scarce to promote trophic differentiation. However, species from low‐productivity habitats often exhibit specialised biological traits such as resistance to starvation and high food‐finding abilities, which may in turn release constraints on trophic and morphological differentiation among species. Groundwaters are food resource‐limited because of the lack of photosynthetic production and limited inputs of organic carbon from surface ecosystems. We tested for co‐variation between morphology and trophic habits in co‐occurring Niphargus amphipods from five groundwater caves of the Dinaric Karst, Europe. We predicted that the size of gnathopods—the accessory feeding appendages—would positively co‐vary with trophic position: species with larger gnathopods should more easily grab and immobilise prey. We quantified gnathopod size and shape by means of morphometric measurements and assessed isotopic niche, trophic position, and carbon signatures using nitrogen (δ ¹⁵ N) and carbon (δ ¹³ C) stable isotopes. We tested for correlation between morphological traits and trophic position and δ ¹³ C signatures while accounting for phylogenetic relationships among species. All co‐occurring species differed morphologically in at least one gnathopod measurement and all of them differed in their isotopic niches. As predicted, gnathopod size increased with the increasing trophic position. This co‐variation probably reflects differences in detritivorous and predatory habits among species: amphipods with larger gnathopods, hence larger muscle and more powerful grip, could more easily subdue prey. Moreover, we found a significant correlation between gnathopod shape and the normalised δ ¹³ C values, indicating that shape of the gnathopods may be related to exploitation of different food resources. We show that low‐productivity subterranean habitat species can exhibit strong trophic specialisation of morphological structures. Gnathopod size and shape of Niphargus amphipods are functional traits that co‐vary with trophic habits. Our findings pave the way for investigating how co‐variation of morphological and trophic traits may control energy flow and species’ coexistence at lower bounds of habitat productivity.
... In subterranean habitats, prey scarcity precludes the evolution of sit-and-wait predators; thus, all predators are actively searching for the prey. Niphargus prey on smaller specimens (conspecifics, microcrustaceans and annelids) that more efficiently escape the predator by sheltering rather than escaping (Luštrik et al., 2011). Locomotion efficiency thus improves the search for the prey rather than chase, and, conversely, the escape strategy depends on predator detection and hiding rather than fast escape. ...
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Species performance depends on the concerted interplay of their functional traits. Natural selection acts on the performance of the species and influences entire suits of interdependent functional traits, thereby driving the evolution of functional diversity (FD) within a clade. In a given habitat, interdependent functional traits are expected to integrate into only a few adaptive combinations. When a clade diversifies in different habitats, the FD within habitats (herein called α ‐FD) diversifies in response to local selections, while between the habitats, alternative adaptive combinations of interdependent traits that are specific to the habitat emerge. This multivariate selection leads to two hypotheses. First, realized α ‐FD within one habitat represents only a small fraction of the variation of functional traits, and second, realized FDs across habitats (hereafter called β ‐FD) are equal to or greater than would be in the absence of the interdependence of functional traits. We tested these hypotheses using 185 species of the highly diverse subterranean amphipod genus Niphargus living in three habitats: river interstitial, cave lakes, and cave streams. We (i) explored integration of functional traits related to locomotion and feeding biology and tested (ii) if realized α ‐FD within each habitat is lower than it would be without trait interdependence, and (iii) if realized β ‐FD in pairwise comparisons of habitats is higher than it would be without trait interdependence. In all three habitats, the length of the appendages as a proxy of the locomotion speed was positively correlated with the trophic position of the species. On the contrary, the body shape correlations were habitat dependent: species in high trophic positions were slender, stout or invariant in shape in interstitial, cave streams and cave lakes, respectively. Using null models, we show that only a fraction of functional trait combinations was realized in each habitat, whereas β ‐FD between habitats was equal to or greater than the null expectations. The results indicate preserved potential for diversification in species within and between habitats. This potential can be realized through hybridization and can drive diversification in adaptive radiations. Moreover, this perspective on the evolution of FD is compatible with several central ecological and evolutionary concepts, such as adaptive landscape or ecological niche theory. Read the free Plain Language Summary for this article on the Journal blog.
... The low survival rates of the surface species might be linked to both competition and predation by the stygobiont one, and suggests the need for a further control condition for the epigean species in future studies. Niphargus amphipods are often considered generalist species feeding on detritus (Luštrik et al. 2011;Tachet 2010), but opportunistic predatory behaviours can be more frequent than usually reported (Ercoli et al. 2019;Fišer et al. 2010), and predator species have been recently recognised (Premate et al. 2021). However, we never observed direct predation by Niphargus on E. stammeri. ...
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Border habitats such as interfaces and ecotones are promising research targets being likely areas of high species richness and genetic and phenotypic diversity. Springs are intriguing habitats exploited by both subterranean and surface species. For subterranean species, springs can provide higher trophic resources but can be risky in terms of predation and UV radiation, while for surface species, springs can be safer but less productive environments. We coupled field surveys and laboratory experiments to understand how predation risk and physical constraints, like light occurrence, affect spring exploitation by both a subterranean (Niphargus thuringius) and a surface crustacean amphipod species (Echinogammarus stammeri). From March to May 2021, we surveyed multiple springs and evaluated the activity (both during day and night) of the amphipods and of their predators. Furthermore, in a subterranean laboratory, we reared 80 N. thuringius and 80 E. stammeri under safe and risky conditions with both constant darkness and diel light variation assessing their activity and survival. Risky conditions were represented by the occurrence of meso-predators alone or coupled with the presence of a top predator. In the field, N. thuringius activity was negatively related to the density of predators, while laboratory experiments revealed a main role played by light treatments and night period. E. stammeri activity in the field was higher close to surface while in laboratory conditions decreased during time. In laboratory conditions, predation risk negatively affected survival of both amphipods. Our findings reveal that physical constraints play a key role in affecting the exploitation of ecotones and can mediate antipredator responses, thus providing selective pressures for the exploitation of border environments. Significance statement Understanding environmental pressures acting on ecotones is a key point to verify if new adaptations may occur at the border between two distinct habitats. Using both field and laboratory approaches, we show that, in springs, the behaviour of subterranean invertebrates is affected by surface physical constraints which can mediate the effects of predation risk. Behavioural strategies to avoid predation, such as nocturnal activity, may promote spring ecotone exploitation by groundwater animals, such as amphipod crustaceans.
... It is hypothesized that spring ecotones are more resource limited than adjacent surface water dominated systems (Cristiano et al. 2019), but there is little data on resource use within spring ecotones. If spring ecotones are resource limited, then there may be intense competition among taxa found within these habitats (Luštrik et al. 2011). Co-occurrence of diverse organisms from different environmental settings (e.g., epigean, crenic, and hypogean) in spatially confined spring openings may be due to their ability to avoid competitive exclusion through resource partitioning (Monterroso et al. 2020). ...
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Spring orifices are ecotones between surface and subterranean aquatic ecosystems. Invertebrates of different origins (e.g., surface, spring obligate, and subterranean) coexist in these spatially restricted environments, potentially competing for resources. However, processes that allow for population coexistence in these presumably low resource environments are not well understood. We examined invertebrate communities at two spring complexes in Texas, USA and assessed resource use and food web structure at spring orifices using stable isotopes of carbon (δ13C) and nitrogen (δ15N). Using bulk δ13C and δ15N of organisms and potential food sources, we elucidated dietary sources and found that invertebrate communities exhibited resource partitioning and contained two main food chains (periphyton versus terrestrial organic matter [OM]). In both spring complexes, several endemic spring orifice associated and subterranean taxa derived most of their diet from terrestrial OM. Analysis of compound-specific stable isotopes (i.e., δ13C of essential amino acids, EAAs) from two co-occurring elmid species indicated that the endemic spring orifice-associated species (Heterelmis comalensis) derived > 80% of its EAAs from bacteria, whereas the widespread surface species (Microcylloepus pusillus) derived its EAAs from a more equitable mix of bacteria, fungi, and algae. We additionally calculated niche overlap among of several taxonomically related groups (aquatic beetles and amphipods) that co-occur in spring ecotones and posterior probability estimates indicated little to no niche overlap among related species. Results indicate that invertebrates at subterranean—surface aquatic ecotones are partitioning food resources and highlight the importance of connections to riparian zones for persistence of several endemic invertebrates.
... The existence of the direct competitive relationship between the epigean and cave amphipods has not yet been confirmed (Luštrik et al., 2011). It is assumed that this may be due to the spatial divergence of species of different ecological groups between biotopes. ...
... Monolistra isopods generally feed on detritus and biofilms occurring on the substrate and composed of fungi and bacteria [38,39]. Niphargus crustaceans show a generalist diet comprising both plant debris and other arthropods, and display both a detritivore and a predatory/cannibalistic behavior [40,41]. Planarians are predators and can hold the highest position of the food web in small interstitial groundwater habitats or where salamanders do not occur. ...
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Several species of surface salamanders exploit underground environments; in Europe, one of the most common is the fire salamander (Salamandra salamandra). In this study, we investigated if fire salamander larvae occurring in groundwater habitats can affect the abundance of some cave-adapted species. We analyzed the data of abundance of three target taxa (genera Niphargus (Amphipoda; Niphargidae), Monolistra (Isopoda; Sphaeromatidae) and Dendrocoelum (Tricladida; Dedrocoelidae)) collected in 386 surveys performed on 117 sites (pools and distinct subterranean stream sectors), within 17 natural and 24 artificial subterranean habitats, between 2012 and 2019. Generalized linear mixed models were used to assess the relationship between target taxa abundance, fire salamander larvae occurrence, and environmental features. The presence of salamander larvae negatively affected the abundance of all the target taxa. Monolistra abundance was positively related with the distance from the cave entrance of the sites and by their surface. Our study revealed that surface salamanders may have a negative effect on the abundance of cave-adapted animals, and highlited the importance of further investigations on the diet and on the top-down effects of salamanders on the subterranean communities.
Dispersal, the movement of individuals across space, has important consequences at individual, population, species, community, and ecosystem levels. Dispersal depends on phenotypic traits influencing the propensity of an organism to disperse and extrinsic environmental features. Factors selecting for dispersal include environmental unpredictability, kin competition, and inbreeding avoidance, although the last two factors have received no attention from groundwater evolutionary ecologists. The predictability of the groundwater environment may jointly select for slow life histories and low dispersal, but there is probably substantial heterogeneity in life history and dispersal propensity across groundwater habitats. There is evidence that specialization to thermally stable subterranean habitats may select against dispersal because organisms with narrow thermal tolerances are more likely to encounter lethal temperatures during dispersal. A generally held view of groundwater aquifers is that of islands with little opportunities for gene flow among populations of nearby aquifers. Landmark studies in population genetics have corroborated this view by revealing groundwater populations that are deeply structured genetically according to extant hydrological connections. However, there is genetic evidence that hydrological barriers among aquifers are labile, thereby facilitating transient dispersal between distant aquifers. Surface rivers and their hyporheic zone may provide dispersal corridors between aquifers but their permeability to animal movement varies considerably over time. Reconstruction of species range dynamics suggests speciation promoted by local adaptation can be followed by phases of dispersal leading to secondary contact and relaxing of interspecific competition as ranges overlap. In Europe, groundwater species range size increases with increasing latitude, a pattern driven by the effect of long-term climatic variability on dispersal. While our understanding of animal movement in groundwater is largely incomplete, there is an urgent need to integrate knowledge gained on dispersal and range dynamics into assessing the potential for species range shift in the face of environmental change.
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A lack of knowledge about the long-term cultivation requirements of groundwater fauna is hampering the establishment of biological criteria to identify chemical threats to groundwater. As a contribution to solving this problem, we have carried out comprehensive laboratory studies on the diet and survival rates of the groundwater amphipod Niphargus aquilex. Preference tests indicated higher consumption of common ash (Fraxinus excelsior) than black alder (Alnus glutinosa) foliage. Compared to detritus from the sampling site, however, survival rates of N. aquilex significantly increased when living oligochaetes were added to ash foliage as an additional food source. Our results indicate that N. aquilex has evolved an omnivorous feeding strategy as an adaptation to the limited availability of nutrient-rich food sources in aquifers. The high acceptance of animal food sources and the predatory behaviour of N. aquilex underline the importance of and requirement for protein in its diet and suggest a high trophic position in groundwater food webs. Based on our results, we provide an optimized culturing protocol that opens up new perspectives for using N. aquilex as an organism for testing the biological quality of groundwater.
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In this chapter, we review the status of the hypothesis that the dichotomy between shallow and deep subterranean habitats is a fundamental one, updating the original book-length presentation of this hypothesis (Culver and Pipan 2014), and consider the status of dim light habitats, such as leaf litter and partially de-roofed caves (Mejía-Ortíz et al. 2018).
Caves and other subterranean habitats with their often strange (even bizarre) inhabitants have long been objects of fascination, curiosity, and debate. The question of how such organisms have evolved, and the relative roles of natural selection and genetic drift, has engaged subterranean biologists for decades. Indeed, these studies continue to inform the general theory of adaptation and evolution. Subterranean ecosystems generally exhibit little or no primary productivity and, as extreme ecosystems, provide general insights into ecosystem function. The Biology of Caves and other Subterranean Habitats offers a concise but comprehensive introduction to cave ecology and evolution. Whilst there is an emphasis on biological processes occurring in these unique environments, conservation and management aspects are also considered. The monograph includes a global range of examples from more than 25 countries, and case studies from both caves and non-cave subterranean habitats; it also provides a clear explanation of specialized terms used by speleologists. This accessible text will appeal to researchers new to the field and to the many professional ecologists and conservation practitioners requiring a concise but authoritative overview. Its engaging style will also make it suitable for undergraduate and graduate students taking courses in cave and subterranean biology. Its more than 650 references, 150 of which are new since the first edition, provide many entry points to the research literature.
Desired Attributes Definition of the Classes Nomenclature Structure of the System Perspective
In the Oslofjord (Norway) distribution and life cycle traits of 4 Gammaridae species (Crustacea, Amphipoda) were studied. Three species occurred at the 2 study shores and showed some segregation to different intertidal levels. A temporal microhabitat utilization is suggested to lessen the possibility of interference competition among species living at similar intertidal levels. The importance of microhabitat segregation is supported by the fact that competitive exclusion occurred in coexistence experiments, and that differences were measured in resistance to desiccation. Environmental heterogeneity may explain the considerable overlap in breeding periods, periods of main juvenile release and animal size. Reproductive effort (total egg volume per brood) and egg size varied seasonally within species. Individual females produced small broods of large eggs in winter and larger broods of smaller eggs in spring; a reverse trend was observed from summer to autumn. These changes were coupled with increased survival probability of newly hatched juveniles in spring and summer. -from Author
The interspecific interactions of three pairs of cave isopods and amphipods, previously thought to be competitors, were examined by analyzing washouts and losses from laboratory streams and from manipulation experiments in streams of Organ Cave, West Virginia. None of the pairs were in fact competitors. The isopod Caecidotea holsingeri was an amensalist of the amphipod Stygobromus spinatus in the laboratory, but the two did not interact in the field. The amphipod Gammarus minus was a predator on C. holsingeri both in laboratory streams and in the field, and C. holsingeri was a competitor of G. minus, at least in laboratory streams. Stygobromus emarginatus was an amensalist of G. minus in laboratory streams and in the field; but in the field G. minus was a commensalist of S. emarginatus. This combination of commensalism and amensalism produces the dynamics of a predator-prey system. Interactions in both laboratory streams and cave streams were asymmetric and often had characteristics of several kinds of interspecific interactions. Negative interactions dominated in laboratory streams while positive interactions were more common in the field experiments. Negative interactions had an effect on microdistribution only at the level of individual stones in a riffle. Positive interactions may contribute to the positive association of some species at larger scales.