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PRIMARY RESEARCH PAPER
Adaptation, phenology and disturbance
of macroinvertebrates in temporary water bodies
Gwendolin Porst •Owen Naughton •
Laurence Gill •Paul Johnston •Kenneth Irvine
Received: 7 January 2012 / Revised: 8 May 2012 / Accepted: 12 May 2012 / Published online: 26 June 2012
ÓSpringer Science+Business Media B.V. 2012
Abstract The temporal transition of species domi-
nance following disturbances is strongly influenced by
taxon life histories. Intemporary water bodies, seasonal
progression can be rapid. The community response of
aquatic littoral invertebrate communities to disturbance
was measured across four temporary water bodies
(turloughs) representing a hydroperiod gradient in the
karst landscape of western Ireland. Three distinct
turlough wet-phases were identified based on macroin-
vertebrate taxon richness and community composition:
filling, aquatic and drying phase. Invertebrates able to
recolonise the turlough environment quickly upon
flooding from refugia (e.g. sink-holes or little puddles)
or resting stages within the turlough basin demonstrated
highest proportion in abundances during the initial
filling phase. Over time, the number of actively
dispersing invertebrates, generally occupying turloughs
only for a part oftheir life-cycle, increased. Hydroperiod
had a significant effect on macroinvertebrate taxon
richness, with short hydroperiods supporting low faunal
diversity. Influence of hydrological disturbance gener-
ally decreased with progression of the annual wet phase,
indicated by a decrease in taxon richness variation and
an increase of biodiversity with time. Our study
highlights the importance of life-cycle strategies of
species for the occurrence of fairly predictable and
periodically occurring seasonal patterns, and empha-
sizes the importance of ecological disturbances for
colonisation cycles.
Keywords Seasonal variation Disturbance
Macroinvertebrates Turloughs Hydroperiod
Introduction
Variation in abiotic conditions over time can account
for a substantial proportion of natural seasonal change
in biotic communities. While seasonal variation is a
common feature of permanent as well as temporary fresh-
waters, faunal communities of temporary environments
Handling editor: Sonja Stendera
G. Porst K. Irvine
Zoology Department, School of Natural Sciences, Trinity
College Dublin, Dublin 2, Ireland
G. Porst (&)
Leibniz Institute of Freshwater Ecology and Inland
Fisheries (IGB), Mu
¨ggelseedamm 301, 12587 Berlin,
Germany
e-mail: porst@igb-berlin.de
O. Naughton L. Gill P. Johnston
Department of Civil and Environmental Engineering,
School of Mathematics and Engineering, Trinity College
Dublin, Dublin 2, Ireland
K. Irvine
UNESCO-IHE, Department of Water Science and
Engineering, Westvest, 2611 AX Delft, The Netherlands
123
Hydrobiologia (2012) 696:47–62
DOI 10.1007/s10750-012-1181-2
face additional physicochemical constraints because
of the recurrent disappearance of water (Williams,
1996). Structure and dynamics in communities are
generally closely related to frequency, scale and
regularity of disturbances (White & Pickett, 1985).
Episodic disturbances such as temporary, seasonal
drying events often exercise a dominant factor for
community composition in wetlands (Wiggins et al.,
1980; Schneider & Frost, 1996). The dry phase of a
temporary wetland can be considered as an ecological
disturbance for its aquatic fauna and flora, and wetland
disturbance can be characterised by hydroperiod or
habitat duration (Schneider, 1999), with short hyd-
roperiods reducing biotic interactions (Wilbur, 1987;
Schneider, 1999). Temporary waters with a long
inundation cycle, providing a comparatively low
disturbance frequency are thus expected to offer a
more stable habitat and facilitate continued colonisa-
tion of invertebrates (Williams, 1997; Holland &
Jenkins, 1998). Consequently, this favours higher
species diversity in temporary ponds or lakes with
increased habitat persistence compared with waters
with shorter and more variable inundation periods
(Duigan, 1988; Spencer et al., 1999; Jocque
´et al.,
2007).
Aquatic invertebrates living in temporary water
bodies have to mature, reproduce or disperse before
the end of the wet cycle and their life histories need
to be responsive to effects and duration of hydrope-
riod (Williams, 2006). These taxa are consequently
often typified by reliance on production of resting
eggs and effective dispersal strategies. Temporary
wetland invertebrates can, as a result, be categorised
broadly into permanent and ephemeral inhabitants
based on time of occurrence and dispersal abilities
(after Wiggins et al., 1980). Permanent residents
comprise mainly passive dispersers, such as snails or
crustaceans, which typically recolonise shortly after
flooding through hatching of resting stages or from
refugia within the temporary pond basin (Wiggins
et al., 1980; Reynolds, 1982; Jocque
´et al., 2007).
Ephemeral residents, typified by many insects, are
characterised generally by active dispersal, rapid
larval development and extensive dispersion. They
have to actively enter or leave the temporary
environment with longer periods for colonisation
compared with passively dispersing/drought resistant
taxa (Wiggins et al., 1980). Macroinvertebrates of
temporary waters are also often associated with well
defined hydrological cycles, involving filling, aquatic
and drying phases (e.g. Bazzanti et al., 1996; Boix
et al., 2004; Jocque
´et al., 2007; Florencio et al.,
2009). While work on invertebrate communities in
temporary wetlands has focussed on dry lands,
mainly in the sub tropics or Mediterranean regions,
the same principles apply to communities in temper-
ate water bodies that experience extreme variability
in hydroperiod. Temporary water bodies associated
with karst limestone, locally known as turloughs, are
common and occur across a wide range of hydro-
logical and trophic states throughout the west of
Ireland (Reynolds, 1982). Similar ecosystems,
although not common, or widespread, are found
elsewhere (Coxon, 1986; Cote
´et al., 1990; Black-
stock et al., 1993; Boix et al., 2001). Turloughs
usually fill and empty through underground passages
and estavelles (sinkholes that also act as a spring),
with some turloughs obtaining water input from
inflowing streams or rivers (Coxon, 1986; Goodwil-
lie, 1992; Goodwillie & Reynolds, 2003). While the
general pattern is to flood in autumn and empty in
summer, hydroperiod can vary greatly (Sheehy
Skeffington et al., 2006), depending on fluctuations
in the local groundwater table (Reynolds, 1982;
Reynolds et al., 1998). Water levels may also rise
sporadically during periods of high rainfall, reflecting
local weather conditions (Reynolds et al., 1998;
Visser et al., 2006). Owing to differences in size,
depth and karstic bedrock, rates of water level
change can vary enormously. Soil type, vegetation
and nutrient status may also affect local habitat
conditions and with direct influence on faunal
communities (Goodwillie & Reynolds, 2003; Sheehy
Skeffington et al., 2006).
The naturally ephemeral nature of turloughs,
which are often lacking, or low, in fish predators,
provide habitat for a range of species of conservation
importance (Sheehy Skeffington et al., 2006; Porst &
Irvine, 2009a). They are listed as priority habitats in
Annex I of the European Habitats Directive (92/43/
EEC) (EEC, 1992). Turlough species diversity has
been postulated to depend on availability of colon-
isers at times of flooding, but there is an absence of
studies on seasonal progression of their invertebrate
communities (Reynolds et al., 2004). This is a
fundamental knowledge gap that limits discriminat-
ing impact of natural compared with anthropogenic
pressure, for example from nutrient enrichment
48 Hydrobiologia (2012) 696:47–62
123
(Cunha Pereira et al., 2010), and which hinders
management and monitoring (Linke et al., 1999;
Trigal et al., 2006).
Here, we present the results of a study investigating
the seasonality of littoral macroinvertebrate commu-
nities across four turloughs representing a gradient of
seasonal hydroperiod and nutrient concentrations. The
aim of the study was to identify different wet phases
from inundation to desiccation based on turlough
macroinvertebrate communities. We wanted to
explore the influence of hydroperiod and nutrient
concentrations on the formation of macroinvertebrate
communities across the turlough flooding season. We
hypothesised that macroinvertebrate taxon richness
increases with increasing turlough hydroperiod and
that variability in species richness decreases with
turlough permanence. We postulated that the propor-
tion of ephemeral turlough residents increases over
time and that these patterns are vulnerable to trophic
regime.
Methods
Study sites
Four turloughs, representing a gradient of hydrolog-
ical regimes and nutrient concentrations were sampled
for their macroinvertebrate communities during the
turlough flooding season 2007/2008 (Table 1; Fig. 1).
Blackrock is a turlough with a short hydroperiod and
high areal reduction rate (dA/dT(m
2
/day), calculated
as the average rate of change of area between the time
of maximum areal inundation and the drying out of a
turlough during sampling season 2007/2008, with
dA=maximum areal inundation and dT=time
between maximum areal inundation and emptying of
turlough) and high nutrient concentrations. Interme-
diate conditions are found in Caranavoodaun, which
has an intermediate hydroperiod and a lower areal
reduction rate and Roo West, with an areal reduction
slightly faster than Caranavoodaun, but with a similar
Table 1 Nutrient status and hydrological regimes of the four turloughs studied
Turlough Mean TP
±SE (ug/l)
a
Areal reduction
rate dA/dT(m
2
/day)
Hydroperiod (weeks)
2007/2008
Hydroperiod
category
Blackrock 52 ±6.5 -10,875 18.6 Short
Caranavoodaun 11 ±1.4 -3,479 25.9 Intermediate 1
Roo West 10 ±1.4 -3,734 25.3 Intermediate 2
Termon 15 ±2.7 -1,042 52
b
Long
a
Mean of collected monthly total phosphorus (TP) concentrations during sampling season October 2006–March, May or June 2007
(n=6 in Blackrock; n=8 in Caranavoodaun and Roo West; n=9 in Termon). Data provided by Helder Pereira, School of Natural
Sciences, Centre for the Environment, Trinity College Dublin;
b
applies to season 2006/2007 and 2007/2008
Fig. 1 Map of Ireland
showing the location of the
four turloughs studied
Hydrobiologia (2012) 696:47–62 49
123
hydroperiod and nutrient status. The fourth turlough,
Termon, can be considered the most hydrologically
stable of the four turloughs, with the lowest areal
reduction rate and retaining some standing water
throughout the year. Nutrient concentrations are a
little higher than in Caranavoodaun and Roo West.
The turloughs will subsequently be referred to as short
(Blackrock), intermediate 1 (Caranavoodaun), inter-
mediate 2 (Roo West) and long (Termon) hydroperiod
turloughs. All study sites are designated as candidate
Special Areas of Conservation (cSAC) under the EC
Habitats Directive (EEC, 1992). The four turloughs
were selected for detailed monthly macroinvertebrate
sampling from a subset of 22 turloughs, which were
chosen for a comprehensive turlough conservation
study and which represent the hydromorphological
and geographical range of turloughs in Ireland (Porst,
2009).
Invertebrate sampling
During the turlough flooding season 2007/2008,
macroinvertebrates were sampled monthly from
December 2007, when turloughs started to flood, until
April 2008. Sampling was done with a box sampler
(50 cm long 940 cm wide 950.5 cm high), modi-
fied after O’Connor et al. (2004). Additional samples
were collected from the intermediate 1 hydroperiod
turlough in May 2008 and the long hydroperiod
turlough in June 2008 (the short hydroperiod turlough
was dry from May 2008, the intermediate 2 turlough
was inaccessible in May 2008 owing to high water
levels and dry in June 2008, the intermediate 1
turlough was dry in June 2008 and the long hydrope-
riod turlough inaccessible in May 2008 owing to high
water levels). Details on individual turlough flooding
cycles can be seen in Table 1(hydroperiod and areal
reduction rate). To test for inter-annual variation in
invertebrate temporal patterns, samples collected from
the long hydroperiod turlough in November 2006,
January, April and June 2007 during the 2006/2007
flooding season were included in the analysis. On each
sampling occasion, five well spaced replicate samples
were collected from the dominant habitat, submerged
grassland, within the accessible and wadable littoral
zone in each of the four turloughs. Exact sampling
locations, therefore, varied with water level. Macro-
invertebrates within the box where removed with a
small 1-mm mesh net, and preserved in 90% industrial
methylated spirits. In the laboratory, taxa were iden-
tified to the lowest taxonomic level possible, typically
species. Macroinvertebrates were identified using the
keys by Ashe et al. (1998), Brooks & Lewington
(1997), Edington & Hildrew (1995), Elliot & Mann
(1979), Elliot et al. (1988), Fitter & Manuel (1986),
Friday (1988), Gledhill et al. (1993), Holland (1972),
Hynes (1977), Macan (1977), Miller (1996), Nilsson
(1997), Reynoldson & Young (2000), Richoux (1982),
Savage (1989), Savage (1999) and Wallace et al.
(2003).
Statistical analysis
A one-way analysis of variance (one-way ANOVA)
tested for significant differences among average
seasonal taxon richness of turloughs, including all
replicate samples per month and turlough. The effect
of time (sampling month) on macroinvertebrate taxon
richness was tested using repeated measures analysis
of variance (RM ANOVA) in SPSS
Ò
(version 15, IBM
Company, Chicago, Illinois) on synchronized, con-
secutive sampling data from December 2007–April
2008. As RM ANOVA is restricted to a balanced
design, data from May and June 2008 could not be
included in this analysis. Least significant difference
(LSD), with Bonferroni corrections was used for post
hoc testing. Variability of taxon richness within
replicate samples was estimated by the coefficient of
variation (CV):
CV ¼SD=100X
Spearman rank-order correlation investigated the
influence of turlough hydroperiod and nutrient status
on average monthly macroinvertebrate taxon richness
and effect of turlough hydroperiod on average
monthly CV. Distance-based linear models (DISTLM)
were used to analyse the relationship between the
multivariate species data set and hydroperiod and
monthly total phosphorus (TP) concentrations of
turloughs using stepwise selection with 9999 permu-
tations in combination with the R2 criterion. DISTLM
is based on a distance-based redundancy analysis
(dbRDA) which tests the hypothesis of no relationship
between macroinvertebrate community structures and
environmental variables (Anderson et al., 2008).
To assess seasonal and inter-annual variation
within macroinvertebrate assemblages, similarity of
samples was assessed using log(x?1) transformed
50 Hydrobiologia (2012) 696:47–62
123
total abundance macroinvertebrate data for multi-
dimensional scaling (MDS) ordination based on a
Bray–Curtis similarity matrix. To test whether macr-
oinvertebrate communities followed a sequential
temporal pattern we used the ‘seriation with replica-
tion’ test of the RELATE analysis. This analysis uses
the Spearman rank correlation coefficient (q) between
community dissimilarities among samples and the
dissimilarity model matrix that would result from the
inter-point distances of the same number of samples
equally spaced along a linear sequence, i.e., in this
case sampling months. RELATE tests the null hypoth-
esis of no relation between the two similarity matrices,
which corresponds to qbeing approximately zero.
A Spearman rank correlation coefficient qclose to one
indicates a close relationship between matrices and,
thus, a high seriation (Clarke & Gorley, 2006).
A two-way crossed analysis of similarities (ANO-
SIM) tested for differences in macroinvertebrate
community structures among sampling months (fac-
tors sampling months and turlough) and among
observed wet phase groups as identified in the MDS-
ordination plot (factors phase and turlough) using
9999 permutations. A one-way ANOSIM tested for
inter-annual differences in sampling seasons and wet-
phases between sampling seasons (long hydroperiod
turlough only). ANOSIM was based in all cases on a
Bray-Curtis similarity matrix of log(x?1) trans-
formed total abundance data.
The similarity percentages routine SIMPER was
used to identify characteristic taxa contributing most
to similarities within wet phases and dissimilarities
among wet phases in each turlough. SIMPER com-
putes the percentage contributions of individual spe-
cies to respective sample differences (Clarke &
Warwick, 2001). All multivariate analyses were
carried out using the statistical package PRIMER
with PERMANOVA add-on (PRIMER
Ò
version 6
with PERMANOVA?, PRIMER-E Ltd, Ivybridge).
Results
During sampling season 2007/2008, average monthly
taxon richness (n=5 per turlough) varied among
months and turloughs of differing hydroperiod
(Fig. 2a), with a significant effect of time (month of
sampling) on invertebrate taxon richness (Repeated
measures ANOVA, F=19.88, P\0.001). Taxon
richness in sampling periods December 2007–Febru-
ary 2008 and March–April 2008 differed significantly
from each other (LSD pair-wise tests with Bonferoni
correction with P\0.05), indicating two different
flooding phases. Significant differences were found in
average seasonal taxon richness among turloughs of
differing hydroperiod (one-way ANOVA, F=11.37,
P\0.001); with highest seasonal average occurring in
the long (13.4 ±2.3 SE) and lowest in the short
hydroperiod turlough (7.2 ±0.8 SE) (Fig. 2b). Hy-
droperiod correlated positively with average monthly
taxon richness. (Spearman rank order correlation,
rs =0. 57, P\0.01), but no effect of nutrient status
on average monthly taxon richness was found. Taxon
richness CV generally decreased until February/March
2008, increasing again from March/April 2008 with
Fig. 2 a Seasonal variation of average number of macroinver-
tebrate taxa recorded per turlough (n =5 per month and
turlough). bAverage seasonal taxon richness during sampling
season 2007/2008 per turlough (n=25 in Blackrock (short
hydroperiod turlough) and Roo West (intermediate 2 hydrope-
riod turlough); n=30 in Caranavoodaun (intermediate 1
hydroperiod turlough) and Termon (long hydroperiod tur-
lough)). Error bars indicate standard errors. Significant
differences are marked with different lower case letters (a,b,c)
Hydrobiologia (2012) 696:47–62 51
123
turlough draining, and showing a negative trend with
increasing turlough hydroperiod (Fig. 3), although not
significant (Spearman rank order correlation, rs =-
0.305, P=0.168). Hydroperiod was identified to have
a significant influence on the community structure of
macroinvertebrates, explaining 12.5% of the variabil-
ity observed in the seasonal macroinvertebrate data set
(DISTLM, pseudo F=1.504, P\0.01), while no
significant relationship could be found between TP
concentrations and the species-derived multivariate
data cloud. Temporal changes also occurred in macr-
oinvertebrate community structures (ANOSIM, global
R=0.954, P\0.01) with pair-wise comparisons of
the different sampling months in the four turloughs
revealing significant differences in community com-
position among all months in all turloughs (P\0.05).
MDS ordination plots indicated gradual change of
macroinvertebrate community structures over sam-
pling season 2007/2008 in all four turloughs, as well as
during sampling season 2006/2007 in Termon
(Fig. 4). This pattern was supported by the results
from the seriation analysis (RELATE: q=0.668,
q=0.607, q=0.770 and q=0.728 in the short,
intermediate 1 and 2, and long hydroperiod turloughs
during sampling season 2007/2008, respectively, all
P\0.01, and q=0.530, P\0.01 in the long
hydroperiod turlough during sampling season
2006/2007).
MDS in combination with ANOSIM identified three
distinct groups of macroinvertebrate samples corre-
sponding with, respectively, the fillingphase (December
2007–February 2008), aquatic phase (March–April
2008) and drying phase (May–June 2008) (ANOSIM,
global R=0.741, P\0.001) (Fig. 5). In the long
hydroperiod turlough, seasonal macroinvertebrate com-
munity structures showed inter-annual similarities
(ANOSIM, global R=0.183, P\0.01), with the
seasonal pattern shifting by about 1 month (Fig. 4).
Three distinct wet phases could be detected in both
seasons (2006/2007: ANOSIM, global R=0.999,
P\0.001; filling phase: November 2006, aquatic
phase: January 2007, drying phase: April–June 2007;
for 2007/2008 wet phases see above) with significant
differences in macroinvertebrate community structures
between seasons (ANOSIM, global R=0.699, global
R=0.968 and global R=0.915 for filling, aquatic and
drying phase, respectively, with P\0.01 in all cases).
Across the four turloughs, we recorded 91 species,
42 families and 16 orders. Taxa recorded in high
numbers during the 2007/2008 sampling season
included Asellus aquaticus (long hydroperiod tur-
lough), Sympetrum sanguineum (intermediate 1 and
long hydroperiod turlough), and Galba truncatula (all
hydroperiod categories), while others such as Lacco-
bius colon (long hydroperiod turlough) or Cymatia
bonsdorffi (long hydroperiod turlough) appeared only
occasionally and in very low numbers. Highest
numbers of different species over all turloughs were
recorded for Coleoptera (mainly Dysticidae), while
highest numbers of individuals were recorded for the
orders Oligochaeta, Odonata, Diptera and Coleoptera.
SIMPER identified a general decrease of oligo-
chaetes from filling to drying phase in the intermediate
and long hydroperiod turloughs (Tables 2,3).
Ephemeroptera, Trichoptera and Odonata larvae, were
only present in intermediate 1 and long hydroperiod
turloughs. While Ephemeroptera (Cloeon dipterum,
Caenis horaria and C. luctuosa) only appeared during
the aquatic (long hydroperiod turlough) and drying
phase (intermediate 1 hydroperiod turlough), early
instar larvae of Trichoptera and Odonata taxa already
appeared during the filling phase and again as late
instar larvae (Trichoptera: mainly Triaenodes bicol-
our, Odonata: mainly S. sanguineum and Lestes
dryas) in high numbers during the drying phase in
the long hydroperiod turlough. In the intermediate 1
hydroperiod turlough, Trichoptera early instar larvae
also appeared during the filling phase showing a
steady increase over the season with highest numbers
as late instar larvae (mainly Limnephilus centralis)
Fig. 3 Seasonal variation of coefficient of variation of taxon
richness (n=5 per month and turlough; Blackrock, short
hydroperiod; Caranavoodaun, intermediate 1 hydroperiod; Roo
West, intermediate 2 hydroperiod; Termon, long hydroperiod
turlough). Error bars indicate standard errors
52 Hydrobiologia (2012) 696:47–62
123
during the drying phase of turloughs. In the interme-
diate 1 hydroperiod turlough Odonata larvae (mainly
S. sanguineum and L. dryas) were only present during
the drying phase. Considerable abundances of heter-
opterans were only detected during the drying phase in
the long hydroperiod turlough.
While Coleoptera taxa (larvae and adults) were
found early in the season in low abundances, and
increased over time in intermediate 1, intermediate 2
and long hydroperiod turloughs, water beetles were
only found in very low numbers in the short hydro-
period turlough and disappeared here completely by
the end of the aquatic phase. Whereas active-dispers-
ing taxa showed an increase in numbers during the
filling phase in the short hydroperiod turlough, which
was also the most nutrient enriched, these were later
replaced by an increase in passively dispersing species
such as Gastropods (mainly Succinea putris). Follow-
ing a drastic decline in numbers at the beginning of the
filling phase during flooding season 2007/2008, a
similar pattern of temporal increase in Asellus aquat-
icus in 2006/2007 and 2007/2008 was found, but
which only occurred, but in substantial numbers, in the
long hydroperiod turlough. A detailed inventory of
macroinvertebrate taxa found in turloughs during
sampling seasons 2006/2007 and 2007/2008 can be
found in Porst & Irvine (2009a,b).
Fig. 4 Multidimensional scaling (MDS) ordinations of macr-
oinvertebrate communities over sampling season 2007/2008 in
four turloughs and additionally sampling season 2006/2007 in
Termon (Blackrock, short hydroperiod; Caranavoodaun,
intermediate 1 hydroperiod; Roo West, intermediate 2 hydro-
period; Termon, long hydroperiod turlough). Trajectories are
indicating the chronological sequence of samples
Fig. 5 Multidimensional scaling (MDS) ordinations of macr-
oinvertebrate communities of four turloughs based on
log(x?1) transformed abundance data and Bray–Curtis
similarity matrix. Different wet phases are indicated in the plot
Hydrobiologia (2012) 696:47–62 53
123
Table 2 Summary results from SIMPER analysis showing cumulative contribution (Cum.%) of contributing taxa to wet phase
(filling phase =f.p.; aquatic phase =a.p.; drying phase =d.p.) similarities (in %) in different turlough hydroperiod categories (cut-
off level =90%)
Short hydroperiod turlough
Group filling phase Group aquatic phase
Average similarity: 63.63 Average similarity: 62.80
Species Cum.% Species Cum.%
Oligochaeta 39.5 Oligochaeta 43.55
Chironomidae 66.87 Chironomidae 61.1
Tipulidae 76.84 Ostracoda 74.66
Hydrachnidia 85.99 Asellus aquaticus 80.18
Helophorus brevipalpis 90.63 Succinea sp. 85.29
Gammarus duebeni 88.99
Galba truncatula 92.07
Intermediate 1 hydroperiod turlough
Group filling phase Group aquatic phase Group drying phase
Average similarity: 52.71 Average similarity: 55.26 Average similarity: 68.26
Species Cum.% Species Cum.% Species Cum.%
Oligochaeta 55.16 Oligochaeta 25.19 Sympetrum sanguineum 17.02
Tipulidae 65.87 Ostracoda 48.02 Pisidium/Sphaerium sp. 28.48
Agabus nebulosus 73.78 Zonitoides sp. 59.24 Cloeon dipterum 38.37
Chironomidae 80.36 Chironomidae 69.47 Chironomidae 47.1
Agabus labiatus 85.02 Dryops sp. 75.48 Agabus sp. (larva) 55.23
Dryops sp. 88.79 Berosus signaticollis 80.02 Oligochaeta 61.16
Hydrachnidia 92.55 Agabus labiatus 83.54 Cloeon simile 65.58
Hydrachnidia 86.29 Lestes sp. 70
Graptodytes bilineatus 88.66 Lymnaea peregra 74.15
Limnephilus centralis 90.67 Limnephilus centralis 78.13
Porhydrus lineatus 81.24
Coenagrion puella 84.02
Culicidae 86.79
Galba truncatula 89.54
Limnephilus lunatus 92.15
Intermediate 2 hydroperiod turlough
Group filling phase Group aquatic phase
Average similarity: 45.92 Average similarity: 55.70
Species Cum.% Species Cum.%
Oligochaeta 52.98 Oligochaeta 25.34
Agyroneta aquatica 76.19 Chironomidae 43.21
Hydrachnidia 82.84 Ostracoda 57.27
Chironomidae 87.03 Omphiscola glabra* 65.97
Tipulidae 90.66 Diptera (pupae) 72.58
Hydaticus seminiger 77.33
54 Hydrobiologia (2012) 696:47–62
123
Discussion
This study highlighted the importance of life-cycles
and dispersal of the macroinvertebrate communities to
ecological disturbance (McCook, 1994; Benedetti-
Cecchi, 2000; Sousa, 2001; Verberk et al., 2008).
Macroinvertebrate taxon richness and community
composition fluctuated monthly and, evinced from
2 years sampling in the long hydroperiod turlough,
inter-annually. Successive annual community struc-
ture concurred with timing of a seasonal response to
flooding and disturbance, with seasonal progression of
macroinvertebrate assemblages following a similar
pattern in each year.
The macroinvertebrate communities in the four
turloughs were characterised by distinct phases relat-
ing to filling and aquatic phase for taxon richness, and
filling, aquatic and drying phase for community
composition, and gradual, serial variation over the
flooding cycle. The wet-phases detected in this study
reflected mode of filling of turlough basins, with
highest water levels reached in February 2008,
followed by a decrease from March 2008 up to
desiccation (short, intermediate 1/2 turloughs) and
retreat of turlough waters (long hydroperiod turlough),
respectively. While this flooding pattern differs from
those detected in other three-phased temporary ponds
(e.g. in the Mediterranean; Boix et al., 2004; Florencio
Table 2 continued
Intermediate 2 hydroperiod turlough
Group filling phase Group aquatic phase
Average similarity: 45.92 Average similarity: 55.70
Species Cum.% Species Cum.%
Zonitoides sp. 81.47
Ilybius sp. (larva) 85.17
Graptodytes bilineatus 88.73
Agabus sp. (larva) 91.07
Long hydroperiod turlough
Group filling phase Group aquatic phase Group drying phase
Average similarity: 43.40 Average similarity: 56.14 Average similarity: 69.16
Species Cum.% Species Cum.% Species Cum.%
Asellus aquaticus 30.83 Oligochaeta 30.7 Asellus aquaticus 16.4
Oligochaeta 53.73 Chironomidae 46.65 Sympetrum sanguineum 29.26
Chironomidae 65.12 Ostracoda 57.89 Gyraulus crista 39.74
Agyroneta aquatica 73.1 Tipulidae 64.28 Bithynia tentaculata 47.91
Anisoptera sp. (larva) 77.99 Ilybius sp. (larva) 69.88 Triaenodes bicolor 55.61
Galba truncatula 82.11 Hydroporus palustris 75.07 Galba truncatula 61.16
Polycelis nigra/tenuis 84.98 Asellus aquaticus 79.53 Corixinae (Instar I & II) 65.64
Isotomurus sp. 87.58 Lymnaea trunculata 83.31 Agyroneta aquatica 69.94
Limnephilidae sp. (Instar I) 89.69 Hydaticus seminiger 86.99 Notonectidae sp. (larva) 74.19
Hydroporus palustris 91.69 Agabus sp. (larva) 89.54 Lestes sponsa 77.95
Hygrotus impressopunctatus 92.05 Radix balthica 81.39
Lestes sp. 83.97
Porhydrus lineatus 86.51
Polycelis nigra/tenuis 88.8
Hygrotus inaequalis 90.75
*putative, pending further verification
Hydrobiologia (2012) 696:47–62 55
123
Table 3 Summary results from SIMPER analysis showing cumulative contribution (Cum.%) of contributing taxa to wet phase (filling phase =f.p.; aquatic phase =a.p.; drying
phase =d.p.) dissimilarities (in %) in different turlough hydroperiod categories (cut-off level =90%)
Short hydroperiod turlough Intermediate 1 hydroperiod turlough
Groups filling phase and aquatic phase Groups filling phase and aquatic phase Groups aquatic phase and drying phase
Average dissimilarity =56.21 Average dissimilarity =60.05 Average dissimilarity =77.22
Species Cum.% Higher presence Species Cum.% Higher presence Species Cum.% Higher presence
Ostracoda 10.48 a.p. Ostracoda 15.14 Only a.p. Sympetrum sanguineum 9.69 Only d.p.
Tipulidae 19.73 f.p Zonitoides sp. 22.64 a.p. Ostracoda 17.48 Only a.p.
Hydrachnidia 28.67 Only f.p Oligochaeta 29.82 Only f.p. Pisidium/Sphaerium sp. 24.24 Only d.p.
Succinea putris 36.40 a.p. Tipulidae 35.17 f.p. Cloeon dipterum 30.42 Only d.p.
Chironomidae 43.28 f.p Berosus signaticollis 40.24 a.p. Zonitoides sp. 34.87 Only a.p.
Oligochaeta 49.52 a.p. Agabus labiatus 45.16 a.p. Agabus sp. (larva) 38.92 d.p
Asellus aquaticus 55.68 Only a.p. Chironomidae 49.99 a.p. Oligochaeta 42.47 a.p.
Galba truncatula 61.30 Only a.p. Agabus nebulosus 54.44 f.p. Radix balthica 45.67 Only d.p.
Agyroneta aquatica 66.74 Only f.p Graptodytes bilineatus 58.63 a.p. Porhydrus lineatus 48.84 Only d.p.
Gammarus duebeni 71.68 Only a.p. Dryops sp. 62.74 a.p. Cloeon simile 51.91 Only d.p.
Helophorus brevipalpis 76.13 Only f.p Limnephilus centralis 66.85 Only a.p. Limnephilus centralis 54.78 d.p.
Agabus sp. (larva) 80.14 Only a.p. Hydrachnidia 70.45 f.p. Lestes sp. 57.50 Only d.p.
Psychodidae 83.38 f.p Galba truncatula 73.42 a.p. Coenagrion puella 60.17 Only d.p.
Velia sp. (immature) 86.26 Only f.p Diptera (pupae) 76.01 Only f.p. Dryops sp. 62.66 a.p.
Diptera (pupae) 88.88 Only a.p. Limnephilidae sp. (Instar III) 78.47 Only a.p. Limnephilus lunatus 65.06 Only d.p.
Isotomurus sp. 91.02 Only f.p Limnephilus auricula 80.77 Only a.p. Agabus labiatus 67.46 Only a.p.
Hydroporus palustris 83.02 a.p. Hydrachnidia 69.83 d.p.
Ceratopogonidae 85.20 a.p. Culicidae 72.17 Only d.p.
Agabus sp (larva) 87.18 Only a.p. Limnephilus marmoratus 74.30 d.p.
Psychodidae 88.75 a.p. Berosus signaticollis 76.38 a.p.
Omphiscola glabra
a
90.25 Only a.p. Chironomidae 78.41 d.p.
Galba truncatula 80.42 d.p.
Graptodytes bilineatus 82.37 Only a.p.
Diptera (pupae) 83.88 a.p.
Asellus aquaticus 85.38 Only d.p.
Agabus nebulosus 86.86 Only a.p.
Curculionidae 88.15 Only d.p.
Limnephilus auricula 89.31 Only a.p.
Hydroporus palustris 90.45 d.p.
56 Hydrobiologia (2012) 696:47–62
123
Table 3 continued
Intermediate 2 hydroperiod turlough Long hydroperiod turlough
Groups filling phase and aquatic phase Groups filling phase and aquatic phase Groups aquatic phase and drying phase
Average dissimilarity =72.49 Average dissimilarity =68.01 Average dissimilarity =85.43
Species Cum.% Higher presence Species Cum.% Higher presence Species Cum.% Higher presence
Ostracoda 8.79 Only a.p. Asellus aquaticus 9.08 f.p. Asellus aquaticus 8.01 d.p.
Chironomidae 17.16 a.p. Ostracoda 16.31 Only a.p. Sympetrum sanguineum 15.64 Only d.p.
Omphiscola glabra
a
25.45 a.p. Anisoptera sp. (larva) 22.84 Only f.p. Oligochaeta 21.95 a.p.
Agyroneta aquatica 32.72 Only f.p. Oligochaeta 27.90 a.p. Gyraulus crista 28.03 Only d.p.
Diptera (pupae) 39.15 Only a.p. Chironomidae 32.77 a.p. Bithynia tentaculata 33.17 Only d.p.
Hydaticus seminiger 44.89 Only a.p. Tipulidae 37.55 a.p. Triaenodes bicolor 37.86 Only d.p.
Hydrachnidia 50.34 a.p. Galba truncatula 42.07 f.p. Corixinae (Instar I & II) 41.10 Only d.p.
Graptodytes bilineatus 55.04 a.p. Hydaticus seminiger 46.32 Only a.p. Radix balthica 44.20 a.p.
Zonitoides sp. 59.20 f.p. Agyroneta aquatica 50.23 f.p. Agyroneta aquatica 47.20 d.p.
Oligochaeta 63.33 f.p. Ilybius sp. (larva) 53.94 a.p. Notonectidae sp. (larva) 50.11 Only d.p.
Agabus sp. (larva) 67.19 Only a.p. Agabus sp. (larva) 57.39 Only a.p. Chironomidae 52.98 a.p.
Ilybius sp. (larva) 70.87 a.p. Polycelis nigra/tenuis 60.60 Only f.p. Galba truncatula 55.42 a.p.
Gammarus lacustris 73.91 a.p. Isotomurus sp. 63.77 Only f.p. Lestes sponsa 57.85 Only d.p.
Tipulidae 76.54 a.p. Limnephilidae sp. (Instar I) 66.75 Only f.p. Ostracoda 60.16 a.p.
Hydroporus palustris 78.98 a.p. Hydroporus palustris 69.32 a.p. Lestes sp. 62.40 Only d.p.
Agabus nebulosus 81.29 a.p. Hygrotus impressopunctatus 71.63 a.p. Tipulidae 64.57 Only a.p.
Berosus signaticollis 82.83 a.p. Limnephilidae sp. (Instar II) 73.74 Only f.p. Hydaticus seminiger 66.68 Only a.p.
Galba truncatula 84.29 a.p. Haliplus sp. (larva) 75.84 a.p. Hygrotus inaequalis 68.77 Only d.p.
Rhantus sp. (larva) 85.65 Only a.p. Porhydrus lineatus 77.93 a.p. Polycelis nigra/tenuis 70.84 Only d.p.
Psychodidae 86.97 f.p. Rhantus sp. (larva) 79.94 Only a.p. Porhydrus lineatus 72.84 d.p.
Ceratopogonidae 88.28 Only f.p. Bithynia leachi 81.20 Only f.p. Ilybius sp. (larva) 74.72 Only a.p.
Isotomurus sp. 89.53 f.p. Hydroporus erythrocephalus 82.45 a.p. Agabus sp. (larva) 76.47 a.p.
Graptodytes sp. (larva) 90.57 Only a.p. Hydrachnidia 83.66 a.p. Curculionidae 78.10 Only d.p.
Laccophilus minutus 84.82 a.p. Pisidium/Sphaerium sp. 79.41 Only d.p.
Podura aquatica 85.96 f.p. Hydroporus palustris 80.62 a.p.
Rhantus exsoletus 86.91 Only a.p. Hygrotus impressopunctatus 81.78 Only a.p.
Succinea putris 87.86 f.p. Hyphydrus ovatus 82.93 Only d.p.
Psychodidae 88.79 f.p. Dryops sp. 83.97 Only d.p.
Agabus nebulosus 89.70 Only a.p. Rhantus sp. (larva) 84.97 Only a.p.
Laccophilus sp. (larva) 90.60 Only a.p. Haliplus sp. (larva) 85.94 Only a.p.
a
Putative, pending further verification
Hydrobiologia (2012) 696:47–62 57
123
et al., 2009), characterised by short flooding phases,
followed by a longer aquatic and a relatively short
drying phase, there is nevertheless a similarity of
macroinvertebrate seasonal patterns in turloughs with
other temporary wetlands with periodic hydrological
regimes. We identified a transition in species domi-
nance during the colonisation period throughout the
investigated hydroperiod gradient, with well adapted
early season species preceding a more diversified
community and, in case of suitable low disturbance
pressures, appearance of predatory species. The spe-
cies which establish high numbers late in the flooding
season are mainly ephemeral residents, without phys-
ical adaptations to drought. Many of these taxa have to
actively enter and/or leave the turlough in order to
survive the drying phase. These findings agree with
several other studies investigating seasonal variation
in invertebrate communities in temporary waters.
Jocque
´et al. (2007) identified a two-phased hydrocy-
cle in freshwater rock pools in Botswana. These
relatively short lived pools were dominated by
passively dispersing macroinvertebrates throughout
the flooding season, with an increase in actively
dispersing, typically flying insects towards the end of
the hydrocycle. In longer-lasting temporary waters,
taxonomic and community composition criteria dis-
tinguished three (Boix et al., 2004; Florencio et al.,
2009) and four (Wiggins et al., 1980; Lahr et al., 1999)
seasonal stages of macroinvertebrate communities,
with a trend towards higher abundances or late
appearances of ephemeral insects towards the end of
the hydroperiod. Whether or not these phases equate to
successional stages is debatable, as for non-predatory
taxa there is unlikely to be a dependence of the
colonisation of the turlough on presence of antecedent
taxa and/or biotically modified habitat structure.
Our findings highlight the importance of macroin-
vertebrate life-cycle strategy to reproduction, devel-
opment and dispersal for survival in the variable
turlough environment (Bilton et al., 2001; Williams,
2006; Verberk et al., 2008). Most of the macroinver-
tebrates found in this study are typical inhabitants of
small ponds (Reynolds, 2000) but can survive in the
variable turlough environment owing to dispersal or
life-cycle strategies (Sheehy Skeffington et al., 2006).
Macroinvertebrates inhabiting turloughs during the
flooding-season can outlast the dry-period either in
wet turlough-soils, small permanently flooded puddles
within the turlough or in permanent waters outside the
turlough basin (Reynolds, 1982; Sheehy Skeffington
et al., 2006). These diverse survival and life-cycle
strategies determine timing of recolonisation during
the flooding cycle. In general, the four studied
turloughs showed comparatively high abundances of
passively dispersing invertebrates such as crustaceans,
molluscs, oligochaetes, or Asellus which colonise
newly filled ponds from dormant stages or refugia
within the turlough basin during the filling phase,
followed by a steady decrease of the proportional
abundance of these permanent residents in intermedi-
ate 1, intermediate 2 and long hydroperiod turloughs.
The filling-phase was also characterised by the arrival
of coleopterans, which showed a steady increase in
numbers over the flooding cycle in intermediate 1,
intermediate 2 and long hydroperiod turloughs in
agreement with findings by Lahr et al. (1999). Some
coleopterans such as Berosus signaticollis may sur-
vive dry periods in muddy turlough soils as adults
(Boix et al., 2001). However, most of these and other
aquatic insects, often depend on active dispersal
(Wiggins et al., 1980; Williams, 2006) from more
permanent waters, or need the presence of other
invertebrate taxa to prey on. Active dispersers/ephem-
eral residents of turloughs dominated during the
aquatic and drying phase of intermediate and long
hydroperiod turloughs. Some aquatic insects such as
Ephemeroptera (mainly C. dipterum and C. simile),
Odonata (mainly S. sanguineum and Lestes sp.) or
Trichoptera (almost exclusively Limnephilidae taxa)
were almost entirely restricted to the drying phase of
intermediate and long hydroperiod and absent from
short hydroperiod turloughs. Some authors suggest the
evolution of especially turlough-adapted life-cycles
(Foster et al., 1992; Nelson & Thompson, 2004;
Verberk et al., 2010), with a competitive advantage in
hydrologically dynamic waters (Sheehy Skeffington
et al., 2006). Turloughs are likely unsuitable for
macroinvertebrates requiring more than 1 year as
nymphs for their development, such as many Odonata
taxa (Moore, 1980; Nelson & Thompson, 2004). Thus,
macroinvertebrate species such as L. dryas or S. san-
guineum can be considered ‘turlough specialists’
(Sheehy Skeffington et al., 2006). L. dryas or S. san-
guineum with their annual life cycles can complete the
nymphal phase and emerge as aerial adults before
turloughs drain in summer (Nelson & Thompson,
2004). These ‘turlough-specialists’ can oviposit in dry
areas which will be inundated again with the autumn
58 Hydrobiologia (2012) 696:47–62
123
flood, triggering hatching of eggs, followed by rapid
larval development in early spring (Miller, 1996;
Nelson & Thompson, 2004). Another ‘turlough-spe-
cialist’ Cloeon simile normally a bivoltine taxon in
many Irish waters produces only one generation per
year in turloughs (Byrne, 1981). Many turlough
aquatic invertebrates are also likely highly vulnerable
to visually hunting predators such as fish, which are
often absent from temporary waterbodies.
The comparatively low abundances of heteropter-
ans observed in turloughs (Porst & Irvine, 2009a) may
reflect a mismatch between the typical turlough
seasonality and heteropteran life-cycles (Tobin &
McCarthy, 2004). During turlough flooding heteropt-
erans are in their adult phase (capable of flight and
generally very ready dispersers), but the fully aquatic
eggs and nymphs occur during turlough dry phases
(Savage, 1989; Tully et al., 1991). In this study,
considerable abundances of heteropterans were only
detected in the long hydroperiod turlough in June
2008, a turlough which contains some permanent
water all year round. Florencio et al. (2009) also
detected highest abundances of heteropterans at the
end of the flooding season in temporary ponds in the
Mediterranean.
While seasonal progression of macroinvertebrate
species showed similar trends in the short hydroperiod
turlough in the beginning of the flooding season when
compared with the other turlough hydroperiod types, a
change occurred towards higher abundances of pas-
sive dispersers/permanent residents during the last two
sampling months (March and April 2008) in this
turlough. The faunal community in the short hydro-
period turlough was generally dominated by taxa with
high tolerances to pollutants such as oligochaetes and
chironomids (BMWP score 1 and 2, respectively).
Ephemeral residents found in March and April 2008 in
this turlough were mainly chironomids, which can be
tolerant to nutrient enrichment (Hellawell, 1986;
Rosenberg & Resh, 1993). More susceptible ephem-
eral taxa, such as crane flies (Tipulidae; BMWP score
5) disappeared towards the end of the season. Thus, the
detected general seasonal pattern seems vulnerable to
trophic regimes of turloughs. Despite differences in
macroinvertebrate composition between sampling
seasons in the long hydroperiod turlough, a similar
seasonal pattern could be detected in both years; but
with a shift in the start of different wet phases
attributable to the later onset of flooding of about one
month compared with the previous year.
Increasing turlough taxon richness over time
indicates a temporal gradient of biodiversity and
longer exposure for colonisation, and emergence
from resting stages (Holland & Jenkins, 1998;
Spencer et al., 1999; Cayrou & Ce
´re
´ghino, 2005).
High disturbance associated with short hydroperiod
reduced taxon richness concurs with several studies
on the influence of hydroperiod in temporary
wetlands (e.g. Collinson et al., 1995; Schneider &
Frost, 1996; Kiflawi et al., 2003; Williams et al.,
2003; Waterkeyn et al., 2008). Water level changes
in the short hydroperiod turlough, a turlough in an
epikarstic flow system can be up to 9 m over 48 h
(Tynan et al., 2005; Sheehy Skeffington et al.,
2006). This high disturbance, together with a lack of
wet/damp soils or other refugia supporting survival
of macroinvertebrates during desiccation of tur-
loughs, drives low biodiversity.
Disturbance associated with short hydroperiod and
high areal reduction rates also affects invertebrate
community variation, as measured by CV. Turlough
taxon richness variation decreased after flooding until
February 2008, suggesting a stabilizing of community
structure over time following disturbance (Connell &
Slatyer, 1977). Increased taxon richness variability in
March/April 2008 coincided with the draining of
turloughs and further disturbance on macroinverte-
brate communities. Rapid changes in water level in the
short hydroperiod turlough were associated with
persistent high monthly variability in taxon richness,
leading to likely resetting of the timing for inverte-
brate colonisation back towards initial colonisation
stages. Ward & Blaustein (1994) identified flash floods
in Negev Dessert pools as overriding importance for
invertebrate communities, leading to a multiple restart
of colonisation. With increasing habitat existence,
biotic interactions become increasingly important
(Schneider & Frost, 1996; Jocque
´et al., 2007). In
contrast, in frequently disturbed environments phys-
ical stress and species adaptations to their environment
dominate the faunal matrix (Schneider & Frost, 1996).
Thus, regularly disturbed turloughs show high vari-
ability in taxon richness for the entire flooding cycle,
while variability of the macroinvertebrates in tur-
loughs with a longer hydroperiod/lower disturbance
will be greater immediately after flooding.
Hydrobiologia (2012) 696:47–62 59
123
Conclusions
From our results, we conclude that turloughs are
disturbed habitats, as individual hydroperiods and
times of flooding are characterised by pronounced
irregularities. Thus, the macroinvertebrate community
is adapted to unpredictable and sometimes compara-
tively short turlough wet seasons. Differences in life-
cycle strategies of turlough macroinvertebrates related
to hydrological disturbance have major consequences
for identifying ‘typical’ communities of temporary
water bodies. Our results provide evidence that
temporal patterns of turlough macroinvertebrate com-
munities follow what might be termed pseudo-suc-
cession, with intermittent shocks to the system caused
by rapid changes in water level. This reduces taxon
richness and increases seasonal variability of macro-
invertebrate communities. The consequences that this
has for conservation assessment could be profound as
failing to sample across the seasonal cycle might
provide a very different impression of community
structure. Turloughs are inherently highly dynamic
systems, with scales of seasonal variation related to
hydrology. Superimposed on this are impacts from
other pressures, particularly nutrients (Cunha Pereira
et al., 2010). Assessment of turloughs well-being
depends on more than occasional one-off sampling or
generalisations of turloughs as one water-body type
(Visser et al., 2006).
Acknowledgments We are grateful to Helder Pereira for
provision of nutrient data (TP concentrations) and practical
support and to Fabien Charrier, Natacha Salles, Klaus-Peter
Schwachhofer and Nova Sharkey for help in the field. We thank
Sarah Kimberley, Steve Waldren, A
´ine O’Connor, Deirdre
Lynn and Jim Ryan for general support and encouragement and
Norman Allott and Mike Dobson for constructive comments on
a previous draft of the manuscript. The study was funded by the
Irish National Parks & Wildlife Service (NPWS).
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