The life history of Perla bipunctata Pictet, 1833 (Plecoptera: Perlidae) in the upper River Liffey, Ireland

Abstract

Perla bipunctata is the most common species of Perlidae in Ireland occurring in fast flowing, clean rivers and small streams. Although a common component of freshwater biological studies, little is known about the autecology of this stonefly. Monthly kick and Surber samples were taken over a 1-year period in the upper reaches of the River Liffey (4th order) to determine the life history of larvae. Perla bipunctata has a merovoltine life cycle taking no less than three years to complete the immature stages. Life history plots suggest two periods of egg hatching, followed by two separate cohorts developing over different lengths of time. Mature larvae from both cohorts synchronise and emerge as adults over a short period in early summer. The merovoltine life cycles of long lived invertebrates like P. bipunctata emphasise the importance of such species in reflecting the ecological quality of freshwaters over a long period of time.

Full text

The life history of Perla bipunctata Pictet, 1833 (Plecoptera: Perlidae)
in the upper River Liffey, Ireland
Hugh Feeley*, Jan-Robert Baars and Mary Kelly-Quinn
Freshwater Biodiversity, Ecology and Fisheries Research Group (freBEF), UCD School of
Biology and Environmental Science, Science Education and Research Centre (West),
University College Dublin, Ireland
(Received 15 December 2008; final version received 8 April 2009)
Perla bipunctata is the most common species of Perlidae in Ireland occurring in
fast flowing, clean rivers and small streams. Although a common component of
freshwater biological studies, little is known about the autecology of this stonefly.
Monthly kick and Surber samples were taken over a 1-year period in the upper
reaches of the River Liffey (4th order) to determine the life history of larvae. Perla
bipunctata has a merovoltine life cycle taking no less than three years to complete
the immature stages. Life history plots suggest two periods of egg hatching,
followed by two separate cohorts developing over different lengths of time.
Mature larvae from both cohorts synchronise and emerge as adults over a short
period in early summer. The merovoltine life cycles of long lived invertebrates like
P. bipunctata emphasise the importance of such species in reflecting the ecological
quality of freshwaters over a long period of time.
Keywords: Perlidae; Perla bipunctata; life history; merovoltine; cohort splitting;
Ireland
Introduction
Large predacious stoneflies are a conspicuous component of the benthic invertebrate
fauna of clean freshwater habitats in Europe (Hynes 1941; Frutiger 1987) and thus
have an important indicator value. In Ireland the majority of stonefly species have
short life cycles, usually seasonal and univoltine (Costello 1988; Smith, Good,
Murphy, Giller and O’Halloran 2000). The larger species, including Perla bipunctata
(Pictet, 1833), Dinocras cephalotes (Curtis, 1827) and Diura bicaudata (L., 1758),
although not as well studied, appear to take at least two or three years to complete
their aquatic immature life stages. However, some large stonefly species may not
necessarily take a long time period to develop, for example Perlodes microcephalus
(Pictet, 1833) displays a univoltine life cycle (Hynes 1941). Hynes (1941, 1976, 1977)
indicates that in Great Britain P. bipunctata may have a three year cycle but in
Ireland no information on its life history has been published to date. Other
autecology studies in Europe have shown that some perlid species take up to three
years and even longer to complete their life cycles (Ulfstrand 1968; Frutiger 1987;
*Corresponding author. Email: hugh.feeley@ucd.ie
Aquatic Insects
Vol. 31, No. 4, December 2009, 261–270
ISSN 0165-0424 print/ISSN 1744-4152 online
Ó2009 Taylor & Francis
DOI: 10.1080/01650420903113737
http://www.informaworld.com
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Huru 1987; Sa
´nchez-Ortega and Alba-Tercedor 1991; Cereghino and Lavandier
1998; Iannilli, Tierno de Figueroa and Fochetti 2002; Haidekker and Hering 2008).
The British Isles differ from continental Europe in having only two perlid species,
Perla bipunctata and Dinocras cephalotes.Perla bipunctata is found throughout
Europe, although its distribution is limited in comparison to other Perlidae (e.g. D.
cephalotes) (Elliott 1991; Fochetti and Tierno de Figueroa 2004; Tierno de Figueroa,
Marfil-Daza and Lo
´pez-Rodrı
´guez 2005). Dinocras cephalotes and P. bipunctata
both have been shown to have a widespread occurrence across Great Britain (Hynes
1977). However, in Ireland, D. cephalotes is very restricted in comparison to the
widespread occurrence of P. bipunctata (Hynes 1977; Costello 1988; Baars and
Kelly-Quinn 2006). This makes Irish populations of P. bipunctata distinct. Perla
bipunctata is amongst the largest European Perlidae reaching a maximum length,
excluding cerci and antennae, of 14–18 mm in males and 30–33 mm in females
(Hynes 1941, 1977).
The assessment of the ecological quality of water bodies is central to the
implementation of the Water Framework Directive (WFD) (European Union 2000).
Life history information is of fundamental importance for virtually all ecological
studies of freshwater invertebrates (Butler 1984) and thus is an integral component in
the interpretation of biological data in relation to the WFD. Life histories may vary
between populations, depending on abiotic factors such as temperature and biotic
factors such as feeding, growth, development, dormancy, dispersal and reproduction
(Butler 1984). The present study aimed to address a knowledge gap in the life history
of P. bipunctata in Ireland.
Materials and methods
Site information
A single stream site (4th order) on the upper reaches of the River Liffey, below
Ballyward Bridge, Co. Wicklow on the east coast of Ireland (6828016.1700 W, 538110
5.2400N) was sampled monthly over a 1-year period. The catchment of this river drains
predominantly peaty soils with base-poor geology (granite, Ordovician sediments,
schists and genesis felsite). However, some mineral and calcareous intrusions imme-
diately upstream make this river generally circum-neutral although it is episodically
acidic during high flows. The river is approximately 23 m wide and at low flow has an
average depth of 19.9 cm (+5.95 cm SE, n¼60, range ¼12–28 cm). The sampling
reach was in an open agricultural landscape with the riparian banks dominated by
grasses (Juncus effusus L. and J. inflexus L.), gorse (Ulex europaeus L.) and hawthorn
(Crataegus monogyna Jacques), all of which did not create significant shading of the
river. The substrate was largely boulder and cobble dominated, with some coarse gravel.
The patches of instream vegetation (*2% cover) were dominated by bryophytes and
Ranunculus species, including R. flammula L. and R. hederaceous L.
Field sampling and laboratory work
Three kick (1-minute, multihabitat) samples and 12 Surber samples were taken
monthly over a 50 m stretch of the River Liffey from February 2006 to January
2007. Kick samples were taken using a standard pond net (1 mm mesh). The Surber
sampler had a 25 625 cm quadrate attached to a 1mm mesh bag. The mesh size of
1 mm was determined to be of sufficient size to capture the smallest P. bipunctata
262 H. Feeley et al.
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larvae. Samples consisted of numerous other macroinvertebrate taxa (e.g. Baetis
rhodani,Isoperla grammatica) that were much smaller than the smallest P. bipunctata
larvae recorded each month. Samples were kept small so as not to deplete the overall
population and affect the community composition at the site.
Two random Surber samples were taken from each of six transects across the
width of the river to determine instream densities of larvae per unit area. All samples
collected were preserved in 70% industrial methylated spirits. The samples were
sorted and all perlid specimens collected were removed, counted, and measured to
the nearest 0.01 mm using a 100-unit eyepiece graticule on a stereo dissecting
microscope (Olympus ZX12).
To determine the most reliable measure of larval size, three different
measurements (interocular width, abdominal length and central head length) were
tested to see which showed the strongest correlation to wet and dry mass. Wet mass
was determined by blotting larvae to remove excess liquid and leaving them to air
dry for 30 minutes before measuring. Dry mass was determined by oven drying the
specimens at 608C for 48 hours. Following regression analyses, interocular width was
chosen as the measure of larval size (r¼0.85, n¼100, p50.001, correlations with
wet mass). The abdominal length (length of abdomen, excluding cerci) of specimens
(r¼0.91, n¼42, p50.001) and the central head length measurements (r¼0.85,
n¼42, p50.001), defined as the distance from posterior head margin to the
ecdysal line, could also have been used. However, these measurements were difficult
to determine accurately and, as a result, all subsequent analyses, were based on
interocular width (IOW).
Larvae were collected for the life history study every 30 days (+2/3 days) with
the exception of November 2006 when site access was restricted due to flooding.
Sampling was resumed in December 2006. No information on instar numbers is
known, and as a result the larvae were grouped into categories representing a
0.2 mm change in IOW. These categories were chosen somewhat arbitrarily but were
similar to comparable studies on other large stonefly species and resulted in the
identification of apparent cohorts within the interocular range of 0.8–3.6 mm. These
categories may, however, incorporate several instars. From laboratory experiments
(Feeley, unpublished), the time recorded, between instars, of all sizes, was in excess
of four weeks in water temperatures higher than river sites. This provided some
guideline to interpret the life history graphs.
Differences in sexual size dimorphism were taken into account. The sex was
determined according to the morphology of the third last abdominal segment (see
Hynes 1977, p. 79), although this characteristic was found not to be reliable on small
specimens (51.75 mm IOW). As a result small individuals were divided equally into
males and females according to the sex ratio of the larger individuals based on the
pooled data (all specimens 41.75 mm IOW). The sex ratio was analysed using a
Chi-squared test. Emergence was determined by a visual inspection of the riverbank
vegetation and substrate for adults. This was carried out along the 50 m reach of the
sampling site on both banks of the river each month.
Results
Based on the relationship between size distributions and mass of P. bipunctata,
larvae displayed exponential growth, although males and females differed in size
(Table 1, Figures 1 and 2). Life history patterns of each sex were, however, shown to
Aquatic Insects 263
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be similar (Figure 2), and thus only development times of the females are shown in
Figure 3.
From the smallest specimens recorded during field sampling the hatching period
and subsequent larval recruitment seemed to occur from October to January and
then again from March to June (Figures 2 and 3). Larvae appear to have the highest
growth rates from April through to September (Figures 2 and 3). From September to
March larvae exhibited little growth, seen especially in the largest and smallest larvae
of both sexes (Figures 2 and 3). Based on size distributions over the 12 month period,
the limited window for development and the possible development time, the larvae
appeared to take three (March to June recruitment) to three and a half years
(October to January recruitment) to complete their life cycle (Figure 3).
Both cohorts synchronised to emerge as adults in early summer of their third
year. In May and June 2006, adult P. bipunctata were found in abundance under the
larger rocks on the riverbank, and exuviae were found on emergent rocks as well as
Table 1. A range of larval interocular widths, central head lengths, and abdominal length
and wet and dry mass of both sexes of Perla bipunctata collected in the River Liffey
{
.
Sex
Number of
individuals
Interocular
width (mm)
Central head
length (mm)
Abdominal
length (mm) Wet mass (g)
Dry
mass (g)
Male 20 1.06 to
2.5
0.82 to
2
2.25 to
7.45
0.0057 to
0.1336
0.0006 to
0.0264
Female 22 1.08 to
3.3
0.82 to
2.8
3.6 to
14.3
0.0083 to
0.3581
0.0009 to
0.0837
{
Specimens ranged from the extremes of small and large larvae incorporating a range of individuals in
between.
Figure 1. Relationship between wet mass and interocular width showing the exponential
growth models for both male (r¼0.82, n¼39, p50.001) (solid line, closed squares) and
female (r¼0.89, n¼61, p50.001) (broken line, open circles) Perla bipunctata from the
River Liffey.
264 H. Feeley et al.
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steep riverbanks and the stems of riparian vegetation. Site visits again in the first
week of June 2007 confirmed adult emergence during this period. The adult
emergence period was also reflected in a notable reduction in the number of larger
larvae in July (Figures 2 and 3). The presence of large larvae (3.0–3.4 mm IOW)
again from September onwards may reflect higher growth rates over the summer as
larvae prepare to overwinter before their emergence as adults the following May and
June.
Perla bipunctata had a relatively low mean density ranging from 3.3 ind/m
2
to
10.6 ind/m
2
in the monthly Surber samples (Table 2). The highest densities were
recorded in June. No density samples were taken with the Surber sampler in
November, December and January due to flooding. However, kick sampling
captured a relatively low abundance of individuals, ranging from 10.3 to 19 per min.
With the exception of December, which was affected by flooding and extended
Figure 2. Life history plots of Perla bipunctata larvae from February 2006 to January 2007:
(a) male larvae, (b) female larvae. Each column represents 100%.
Aquatic Insects 265
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Figure 3. The life history patterns of female Perla bipunctata larvae (displayed as %)
collected in the River Liffey from February 2006 to January 2007. The possible cohorts
developing from different emergence periods are superimposed as lines. AH – Autumn
Hatching, SH – Spring Hatching, AY1 – Autumn Year 1, SY1 – Spring Year 1, AY2 –
Autumn Year 2, SY2 – Spring Year 2, AY3 – Autumn Year 3, SY3 – Spring Year 3, AY3.5 –
Autumn Year 3.5.
Table 2. Monthly larval densities, abundances and sex ratios of Perla bipunctata larvae
sampled in the upper reaches of the River Liffey.
Month
{
Density (ind/m
2
) Abundance (ind/1 min) nSex ratio (<:,)
February 8.0+0.6 14.3+4.3 64 0.8 : 1
March 6.3+0.3 14.0+4.3 61 1 : 0.8
April 6.3+0.4 11.7+6.1 54 0.7 : 1
May 5.6+0.5 19.0+7.6 59 0.8 : 1
June 10.6+0.7 18.0+2.0 75 0.6 : 1
July 3.3+0.2 10.6+1.8 40 0.9 : 1
August 10.0+0.6 13.6+6.5 70 0.6 : 1
September 6.0+0.5 11.0+2.0 55 0.7 : 1
October 6.6+0.6 17.3+5.2 70 0.7 : 1
December –* 50.3+16.4
{
151 1 : 0.8
January (2007) –* 17.0+4.5 75 0.8 : 1
{
Samples taken in 2006 unless otherwise specified. *No samples taken due to flooding.
{
Due to flooding
kick sampling was carried out for 2 minutes. Values quoted as means+standard error.
sampling, the total number of larvae captured varied little, ranging between 40
and 75 individuals each month (Table 2). The sex ratio of P. bipunctata was
roughly 1:1, ranging from 0.6:1 to 0.8:1 (w
2
¼11.6, df ¼1, p¼0.01) (Table 2). The
temporal variability in the sex ratio is probably due to the relatively low sample
number.
266 H. Feeley et al.
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Discussion
The present study has shown that the life history of P. bipunctata in the River Liffey
is merovoltine and takes an estimated three to three and a half years to complete
depending on larval recruitment/hatching period, agreeing with observations by
Hynes (1941, 1976, 1977). Larval recruitment took place in two periods, suggesting
two different larval cohorts that develop separately with some degree of overlap. The
larvae recruited in spring and early summer seem to go on to have a cycle of three
years while larvae recruited in autumn and early winter have a slightly longer life
cycle of three and a half years.
The long life cycle reflects larval growth and development that seems to be
limited to mid to late spring, summer and early autumn. Other studies on large perlid
life histories have shown that larvae require high temperatures for growth and
development, with larval size remaining relatively similar throughout the winter and
early spring (Heiman and Knight 1969, 1975; Frutiger 1987; Huru 1987; Moreira
and Peckarsky 1994). This reduced development period, therefore, leads to a long life
cycle. Consequently, the most fitting time span is three to three and a half years,
taking into account the overlap in cohorts and the eventual size reached in both
sexes. The smaller size of males does not reflect a shorter life cycle. Hynes (1941)
determined that size difference between sexes occurs in their third year.
The development of two separate merovoltine life cycles within the same
population, although reported for several other perlid species, has not been reported
for P. bipunctata anywhere before. This splitting of cohorts may result from either a
reduced development rate in the egg stage or a diapause. Elliott (1991) showed that
temperature fluctuation had no effect on the rate of egg development of P. bipunctata
except when temperatures dropped below 68C. However, unlike other perlid species
(Elliott 1989; Zwick 1996a) no dormancy occurred and their eggs continued to
develop although at a much lower rate. This development, known as an oligopause,
is seen in many insect species in areas with moderate winters (Leather, Walters and
Bale 1993). The presence of the smallest larvae from October in this study reflects a
brief hatching period before a temperature drop associated with the winter months.
The continued presence of the smallest larvae through to January may reflect a low
growth rate associated with lower winter temperatures as seen in other Perlidae
(Heiman and Knight 1969, 1975; Frutiger 1987). The remaining eggs, although not
quiescent, develop much slower and then begin to hatch again from April through to
June when the temperatures of early spring and summer become more favourable.
The second possibility is the occurrence of a diapause in egg development.
Embryonic diapause is widespread in Plecoptera (Pritchard, Harder and Mutch
1996). Several studies have shown evidence of this across many different stonefly
families and species (e.g. Elliott 1989; Lillehammer, Brittain, Saltveit and Nielsen
1989; Moreira and Peckarsky 1994; Townsend and Pritchard 1998; Taylor,
Anderson and Peckarsky 1999; Iannilli et al. 2002; Schultheis, Hendricks and Weigt
2002; Nesterovitch and Zwick 2003; Stewart and Sandberg 2003; Lieske and Zwick
2008; Schultheis, Booth, Vinson and Miller 2008). Zwick (1996a) discovered that D.
cephalotes populations in Germany and Norway entered a diapause that resulted in a
‘seed bank’ of dormant eggs in the streambed. The diapause was for longer than one
generation under specific conditions governed by genetic variations, determined by
temperature, which allowed larvae to fit into seasonal environmental patterns (Zwick
1996a). Therefore, a diapause in P. bipunctata eggs may extend its life cycle further to
four or possibly even five years from initial egg deposition to eventual adult
emergence (Elliott 1991).
Aquatic Insects 267
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As Ireland has a mild temperate climate it is unlikely a diapause or dormancy
occurs, but an oligopause is possible. However, whether temperatures remain low
enough in the River Liffey to induce the lower egg development rates, identified by
Elliott (1991), is difficult to determine without temperature data. What is clear is that
the life cycle of P. bipunctata in the River Liffey has a delay in egg hatching and
therefore larval emergence, resulting in a cohort split. This may reflect a ‘bet-
hedging’ strategy (Hairston, Olds and Nunns Jr. 1985) as populations adapt to avoid
adverse abiotic conditions such as the influence of low temperature thresholds
(Pritchard et al. 1996; Zwick 1996a,b; Gillooly and Dodson 2000; Yoshimura, Isobe
and Oishhi 2006), the availability of food and intraspecific competition (Harper
1973; Moreira and Peckarsky 1994). It may also be a result of genetic variability
within the population (Frutiger 1996; Schultheis et al. 2002, 2008).
Mature P. bipunctata larvae in the River Liffey have only one period of
emergence that occurs during May and June. The low density and abundance of
large larvae in July also reflected the adult emergence period of May and June. The
existence of a single adult emergence period highlights a synchronising of formally
split cohorts. Other studies into large predaceous Perlidae (e.g. Sa
´nchez-Ortega and
Alba-Tercedor 1991; Moreira and Peckarsky 1994; Iannilli et al. 2002) have also
shown the existence of two larval cohorts with life cycles of differing durations that
eventually synchronise to emerge simultaneously. A synchronised adult emergence is
probably controlled by environmental factors such as temperature thresholds
(Sweeney and Vannote 1986), or perhaps genetics (Schultheis et al. 2002).
Based on the broad European distribution of P. bipunctata (Elliott 1991; Fochetti
and Tierno de Figueroa 2004; Tierno de Figueroa et al. 2005), one would expect this
species to be very adaptable to climatic differences, developing life history tactics that
enable an adaptation to the seasonal conditions of its environment as pointed out for
other widespread Perlidae (Frutiger 1996). However, Perlidae are characterised by
long life cycles and, as a result, there is a great variation in larval sizes present in
riverine systems throughout the year, often due to an overlap among different cohorts
(Hynes 1976; Cereghino and Lavandier 1998). Consequently, it may be difficult to
accurately determine the factors that contribute to larval recruitment, growth and
development, and the calculation of growth rates. As a result, further studies on the
egg development, number of instars, growth and temperature requirements are needed
for P. bipunctata in Ireland for a complete understanding of its life cycle.
A minimum life cycle of three to three and a half years is an important finding,
especially for an ecologically sensitive species such as P. bipunctata (Lucey 1991;
Hawkes 1997). The presence of larvae across all cohorts in a riverine system reflects a
healthy population for at least the previous three years and consequently, at least
three years of relatively clean water quality and good ecological status (see European
Union 2000). Ultimately, further increase in the knowledge of the life histories of key
indicator species such as P. bipunctata will help refine knowledge on their indicator
potential and improve the interpretation of monitoring data for evaluation of river
ecosystem health and water quality in Ireland, and across Europe, as required by the
WFD.
Acknowledgements
We would like to thank Dr Maria Callanan for her help with fieldwork and Dr Ronan Matson
for his expertise on the plant species. The comments made by two anonymous reviewers are
very much appreciated.
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