Life cycle and phenology of an Antarctic invader: the flightless chironomid midge, Eretmoptera murphyi

Abstract

Knowledge of the life cycles of non-native species in Antarctica is key to understanding their ability to establish and spread to new regions. Through laboratory studies and field observations on Signy Island (South Orkney Islands, maritime Antarctic), we detail the life stages and phenology of Eretmoptera murphyi (Schaeffer 1914), a brachypterous chironomid midge introduced to Signy in the 1960s from sub-Antarctic South Georgia where it is endemic. We confirm that the species is parthenogenetic and suggest that this enables E. murphyi to have an adult emergence period that extends across the entire maritime Antarctic summer season, unlike its sexually reproducing sister species Belgica antarctica which is itself endemic to the Antarctic Peninsula and South Shetland Islands. We report details of previously undescribed life stages, including verification of four larval instars, pupal development, egg gestation and development, reproductive viability and discuss potential environmental cues for transitioning between these developmental stages. Whilst reproductive success is limited to an extent by high mortality at eclosion, failure to oviposit and low egg-hatching rate, the population is still able to potentially double in size with every life cycle.

Electronic supplementary material
The online version of this article (doi:10.1007/s00300-018-2403-5) contains supplementary material, which is available to authorized users.

Full text

Vol.:(0123456789)
1 3
Polar Biology (2019) 42:115–130
https://doi.org/10.1007/s00300-018-2403-5
ORIGINAL PAPER
Life cycle andphenology ofanAntarctic invader: theightless
chironomid midge, Eretmoptera murphyi
Jesamine C.Bartlett1· PeterConvey2· ScottA.L.Hayward1
Received: 18 January 2018 / Revised: 12 September 2018 / Accepted: 14 September 2018 / Published online: 29 September 2018
© The Author(s) 2018
Abstract
Knowledge of the life cycles of non-native species in Antarctica is key to understanding their ability to establish and spread
to new regions. Through laboratory studies and field observations on Signy Island (South Orkney Islands, maritime Antarc-
tic), we detail the life stages and phenology of Eretmoptera murphyi (Schaeffer 1914), a brachypterous chironomid midge
introduced to Signy in the 1960s from sub-Antarctic South Georgia where it is endemic. We confirm that the species is
parthenogenetic and suggest that this enables E. murphyi to have an adult emergence period that extends across the entire
maritime Antarctic summer season, unlike its sexually reproducing sister species Belgica antarctica which is itself endemic
to the Antarctic Peninsula and South Shetland Islands. We report details of previously undescribed life stages, including
verification of four larval instars, pupal development, egg gestation and development, reproductive viability and discuss
potential environmental cues for transitioning between these developmental stages. Whilst reproductive success is limited to
an extent by high mortality at eclosion, failure to oviposit and low egg-hatching rate, the population is still able to potentially
double in size with every life cycle.
Keywords Chironomidae· Signy Island· Embryogenesis· Pupal development· Population growth
Introduction
The sub-Antarctic islands, with a longer history and greater
level of human influence than any other part of the Antarctic
(Convey 2013), have a greater number of non-native species
than the more extreme maritime and continental Antarctic
regions further south (Convey and Lebouvier 2009; Frenot
etal. 2005). However, in recent years and decades, there
have been increasing records of species establishing in the
maritime Antarctic with anthropogenic assistance, particu-
larly in the South Shetland Islands and northern Antarc-
tic Peninsula (e.g. Greenslade etal. 2012; Volonterio etal.
2013; Hughes etal. 2015; Molina-Montenegro etal. 2012).
With synergy between high and increasing levels of human
activity in this region of the Antarctic, and recent rapid rates
of regional climate change, further establishment of non-
native species is predicted, presenting fundamental chal-
lenges to the protection and conservation of Antarctic ter-
restrial biodiversity, and to the management and governance
processes in the Antarctic (Chown etal. 2012; Chown and
Convey 2016; Hughes and Worland 2010; Tin etal. 2009).
The brachypterous midge Eretmoptera murphyi (Chi-
ronomidae, Orthocladiinae) is a non-native species on Signy
Island (South Orkney Islands, maritime Antarctic), to which
it is thought to have been inadvertently introduced in the
1960s, in association with plant transplant experiments
(Block etal. 1984; Convey and Block 1996). Its larvae have
the capacity to rapidly cold harden, cryoprotectively dehy-
drate (Everatt etal. 2012, 2015; Worland 2010), respire in
water and withstand ice entrapment (Everatt etal. 2014).
These traits have allowed it to succeed in the maritime
Antarctic, which is more extreme in comparison with the
species’ native sub-Antarctic South Georgia. The sub-Ant-
arctic has a relatively stable and chronically cool oceanic-
influenced climate year-round. This presents fundamentally
Electronic supplementary material The online version of this
article (doi:https ://doi.org/10.1007/s0030 0-018-2403-5) contains
supplementary material, which is available to authorized users.
* Scott A. L. Hayward
s.a.hayward@bham.ac.uk
1 School ofBiosciences, University ofBirmingham,
EdgbastonB152TT, UK
2 British Antarctic Survey, NERC, High Cross, Madingley
Road, CambridgeCB30ET, UK
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

116 Polar Biology (2019) 42:115–130
1 3
different pressures for terrestrial invertebrates to that of
the much more extreme seasonality of the maritime Ant-
arctic, where overwintering microhabitat temperatures can
regularly fall below −10°C, contrasting with minima only
marginally below zero on South Georgia (Convey 1996a;
Convey and Block 1996). To date, studies of E. murphyi
have primarily focussed on the ecophysiology of late instar
larvae (Everatt etal. 2012, 2015; Worland 2010; Hughes
etal. 2013). However, a much more detailed characterisa-
tion of all life stages is required to determine how current
and predicted future climate changes may affect this species’
development and phenology.
Life history strategies ofpolar arthropods
Driven by the short growing seasons and environmental
extremes, polar invertebrates often exhibit ‘adversity-
selected’ life history strategies in comparison with their
temperate counterparts (Convey 1996b). They have slow
growth rates (Convey 1996b), extended and free-running
life cycles with reduction of obligate overwintering stages
(Fogg etal. 2008), considerable investment in stress tol-
erance mechanisms (Convey 1996b; Hayward etal. 2003;
Everatt etal. 2015) and the ability to opportunistically take
advantage of even short periods of conditions suitable for
growth and activity; for instance, the Antarctic oribatid mite,
Alaskozetes antarcticus, has a life cycle duration of around
5years, whilst comparable temperate species are typically
annual or biennial (Convey 1994; Block and Convey 1995).
Consequently, multi-year life cycles are common in polar
arthropods and many lack a true diapause, instead entering a
state of temporary quiescence during winter or other shorter
periods of unsuitable conditions. Thus, the most commonly
shared life history feature across polar arthropods is the flex-
ibility which enables the challenges of adverse conditions to
be overcome, although some ‘programmed’ elements may
remain so that key life stages can take advantage of regu-
lar environmental triggers each season (Convey 1996a, b;
Danks 1999; Worland and Convey 2008).
Chironomid midges are a group of higher insects that are
particularly well represented at high latitudes in both hemi-
spheres relative to other insect groups (Chown and Convey
2016; Convey and Block 1996; Coulson etal. 2014). Polar
representatives typically conform to the normative polar life
history strategy as defined by Danks (1999), having a fixed
and synchronous spring emergence after overwintering in
a late larval stage, and a brief adult reproductive stage dur-
ing summer, but an otherwise flexible life history. Asexual
reproduction is prevalent in all major polar arthropod and
microinvertebrate groups (Chown and Convey 2016; Convey
1996a) and especially so in sub-Antarctic Psychodidae, a
family of biting midges (Duckhouse 1985). However, asex-
ual reproduction has not yet been definitively proved in any
maritime Antarctic insect species (Convey 1996a) despite
being strongly suspected in E. murphyi (Convey 1992; Cran-
ston 1985).
Life histories ofAntarctic chironomids
The life histories and biology of the native Antarctic chi-
ronomids Parochlus steinenii (Gercke 1889) (Podonomi-
nae) and Belgica antarctica (Jacobs 1900) (Orthocladiinae)
have been well studied (e.g. Allegrucci etal. Allegruci
etal., 2006, 2012; Convey and Block 1996; Harada etal.
2014; Hahn and Reinhardt 2006; Sugg etal. 1983; Usher
and Edwards 1984). These are typically characterised by
larval development taking place over 2years, overwintering
as either early or late instars, followed by synchronised mass
emergence of adults in summer (Convey and Block 1996;
Harada etal. 2014; Sugg etal. 1983). Belgica antarctica
occurs along the Antarctic Peninsula and is the only higher
insect endemic to the Antarctic continent (Convey and Block
1996; Kelley etal. 2014). It experiences environmental con-
ditions similar to those of E. murphyi on Signy Island, and
the assumption is that both species have similar ecologi-
cal niches. Recent molecular evidence also suggests that E.
murphyi should be assigned to the genus Belgica (Allegrucci
etal. 2012), further supporting likely common life history
strategies. However, questions remain as to whether the long
evolutionary history of E. murphyi on sub-Antarctic South
Georgia has provided the opportunity for the evolution of
a temperate-style life history pattern that would show less
flexibility than that of a more typical polar insect.
In the field on Signy Island E. murphyi is thought to emerge
en masse, possibly in response to abiotic factors such as
increased spring daylength, the seasonal melt of basal snow
(Block etal. 1984; Gardiner etal. 1998) or as a heritage trait
from related chironomids (Armitage etal. 1995). Convey
(1992) showed that rates of egg development decrease with
an increase in temperature (2–12°C) and that the females
invest greatly in reproduction with ca. 85 eggs being laid in a
single hydrosensitive egg sac—representing a dry mass twice
that of the female post-oviposition. Once larvae hatch they
are thought to overwinter twice (Hughes etal. 2013; Worland
2010), once in an early larval stage and later in the fourth
instar, although this has not been explicitly demonstrated.
It is assumed that E. murphyi has four larval instars like B.
antarctica, although previous size class distribution analyses
and taxonomic studies have identified only two distinct classes
via assessments of larval mass or field observations (Cranston
1985; Hughes etal. 2013). One reason underlying the current
lack of explicit knowledge of E. murphyi’s life history has
been the challenge of establishing a long-term laboratory cul-
ture, with all data obtained to date derived from short periods
of field observations combined with laboratory experiments
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

117Polar Biology (2019) 42:115–130
1 3
relying on field-collected material (Convey 1992; Everatt etal.
2014; Hughes etal. 2013).
Patterns ofclimate change inthewestern Antarctic
Peninsula andScotia Arc
In recent decades, rapid regional warming and other physi-
cal environmental changes have been documented in parts of
Antarctica, in particular in the region of the western Antarctic
Peninsula and Scotia Arc (Turner etal. 2009, 2014), including
Signy Island (Cannone etal. 2016; Royles etal. 2012; Smith
1990). Signy Island was recognised early on as a paradigmatic
location at which to study terrestrial biological processes in
the maritime Antarctic, and how these might change under
the influence of changing environmental drivers (Smith 1990).
Within terrestrial ecosystems, the primary consequences of
these environmental changes are longer active seasons (ear-
lier spring thaw combined with later autumn freeze), greater
integrated thermal energy availability (increased temperatures)
and greater availability of liquid water to terrestrial organisms.
Thus, and unlike the general consequences in many regions of
the world, regional warming in parts of the Antarctic relaxes
the current extreme environmental constraints on biological
processes, and recent syntheses recognise that many of the
native biota in these regions, including polar terrestrial inver-
tebrates, are likely to benefit from the changes being observed
(Bale and Hayward 2010; Convey 2011; Convey etal. 2014).
It is also increasingly recognised that this relaxation of envi-
ronmental constraints, with or without the direct influence of
human assistance in transporting propagules, will lower the
barriers to new species arriving and establishing in Antarctica
(Frenot etal. 2005; Hughes etal. 2006).
Aims ofthis study
Against this background, the primary aims of this study are to
provide the first detailed characterisation of different devel-
opmental stages within the life cycle of E. murphyi, and to
investigate the potential role of abiotic triggers in the timing of
major life history transitions on Signy Island, such as pupation,
adult eclosion or oviposition. These are then considered in the
context of the implications of climate change for this species’
life history and distribution on the island and, potentially, more
widely in the maritime Antarctic.
Materials andmethods
Sample collection andprocessing
All samples were either obtained from, or observed
insitu, on the Backslope and in the immediate vicinity
of the British Antarctic Survey (BAS) research station
on Signy Island (South Orkney Islands, maritime Ant-
arctic, 60°43′0″S, 45°36′0″W; Fig.1a, b). Samples col-
lected during the 2014/2015 austral summer by BAS staff
were returned to the United Kingdom by ship in + 4°C
cold storage (10weeks), and then maintained at + 4°C
at the University of Birmingham until use. Studies were
conducted in the field on Signy Island between December
2016 and March 2017. All laboratory cultures and experi-
ments, both at the University of Birmingham and on Signy
Island, were maintained on local Signy peat soil substrate,
which is both the species’ habitat and food source on the
island. The substrate was kept moist with a soil solution
comprising 3:1 deionised water to Signy soil (hereafter
termed ‘field water’) to ensure that conditions deviated as
little as possible from the natural environment.
Eretmoptera murphyi’s current distribution on Signy
Island is centered around the research station and adja-
cent Backslope, and therefore all monitoring and sam-
pling occurred within a few hundred metres of the station
(Fig.1b). All images and morphological measurements
were obtained using a Leica EZ4 digital microscope and
associated software. Individual larvae or adults were
extracted from the soil/moss substrate by washing through
stacked sieves (2-mm, 0.5-mm mesh sizes) and handpicked
from the remaining soil solution. Moss and peat substrate
was broken apart with fine tweezers prior to washing to
ensure individuals were not trapped amongst the fibres.
Weather conditions were noted in association with all field
experiments and collection days, with particular attention
to recording strong sunshine and significant precipitation
events.
Measurement oflarvae
Larvae were assigned to instars based on size. They were
initially separated into approximate size classes by eye,
followed by detailed width and length measurements using
images taken with a digital microscope with in-built cam-
era (Leica EZ4). The microscope software was calibrated
for each image using a micrometre stage graticule. Width
measurements were taken by measuring the length of the
intersegmental groove between segment IV (SIV) and seg-
ment V (SV)—the intersection of the cephalothorax and
abdomen. Length measurements were taken from head to
anus, but did not include mandibles or posterior parapods
(the latter only in the case of L1). This information on dis-
tinct size classes then informed the selection of L4 larvae
for studies of pupal development and larval instar occur-
rence in phenological surveys, described below.
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

118 Polar Biology (2019) 42:115–130
1 3
Fig. 1 Maps showing the
Location of the South Orkney
Islands and Signy Island in the
Southern Ocean. Inset—Map
of Signy Island, with Research
Station (and thus current area
of E. murphyi distribution)
highlighted. Created using Arc-
Map®10.4.1 software by Esri.
Copyright © Esri
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

119Polar Biology (2019) 42:115–130
1 3
Environmental triggers forpupation
In laboratory samples maintained at 4°C under constant
darkness, progression to pupae from the L4 instar is infre-
quent and unpredictable (PC, JB, pers. obs.). We therefore
hypothesised that other environmental signals might be
required to trigger pupation. In a simple test of this, batches
of L4 larvae (n = 20) were placed under the following con-
ditions representing different temperature, light and water
availability scenarios on Signy Island during the transi-
tions from winter to spring and summer (Table1). Control
conditions were constant darkness at 5°C. To determine if
light was a trigger for pupation, samples were transferred to
19L:5D (5°C), which approximates summer photoperiods
on Signy. A fluctuating temperature regime of 5°C dur-
ing illumination and 0°C during darkness was also used, to
approximate typical Signy summer diurnal conditions. To
determine if spring melt/access to water was a trigger for
pupation, larvae were maintained either under “wet” condi-
tions (1:1 soil mass-to-‘field water’ volume ratio) or “dry”
conditions (no additional water was added to the substrate)
in petri dishes.
Larvae were maintained under these experimental con-
ditions for 60days from 18 December 2015 to 18 Febru-
ary 2016, and cumulative pupation recorded. Any pupae
obtained were maintained under the same temperature and
light conditions, but with saturated soil, until either death or
eclosion to imago.
Pupal development
Initial observations suggested morphologically distinct
phases of pupal development, so n = 31 individual pupae
were observed and imaged as they occurred in laboratory
stocks throughout the study (i.e. from both the 2014/2015
BAS collection and 2016/2017 collections). To clearly docu-
ment the discreet phases, digital images were taken of all
pupae under the different treatments applied, with width and
length data recorded as well as other key morphological and
physiological changes including development of gonads,
development from stemmata to compound eyes and changes
to cuticle pigmentation (Table2). This definition of pupal
phases informed the experimental design for field monitor-
ing of pupal and imago development during the 2016/2017
season.
Pupal andimago development intheeld
Field monitoring of pupal development took place during
January 2017 adjacent to Signy Research Station. Individual
pupae (n = 20) were placed in open petri dishes containing
local substrate within a larger arena placed on the ground,
and temperature data were recorded for the duration of the
observations. The arena was constructed using 2-L plastic
tubs with modified lids of nylon mesh, in order to keep the
arena open to the environment whilst preventing damage by
local wildlife, predominantly the Brown Skua (Stercorarius
antarcticus). Pupae were assessed daily from 20 December
2016 to 6 January 2017. Temperature readings inside the
arena were taken each day at the time of surveying using
a soil temperature probe and digital thermometer (RS Pro-
206-3738 with Type K thermocouple probe) and ambient
readings collected with an adjacent temperature logger
external to the arena (Tinytag Transit TG-0050). Pupae were
followed through their development via assessment with a
hand lens and allocated to the developmental stages as noted
Table 1 Environmental treatments used to assess influence of temper-
ature, light and soil saturation on pupation
Dominant light
condition
Temperature
(°C )
Light regime
(L:D)
Soil moisture
Light 5 19:5 Wet
Dry
Light 2 19:5 Wet
Dry
Dark 5 0:24 Wet
Dry
Dark 5–0 19:5 Wet
Dry
Table 2 Description of pupal phases and classification guide for development tracking
Average development time within each phase ± SEM. n = 31 pupae assessed in laboratory conditions (5°C, saturated soil, dark). Eye type: S =
stemmata; C = compound eye. Size is total body length
Pupal Phase Size (mm) Physically mobile Eye type Pigmentation Legs Gonapophysis Repro-
ductively
viable
Development
time in phase
(days)
1 1–1.5 Ver y S None Sheathed None No 3.00 ± 0.82
2 1.5 Somewhat S&C Cephalothorax & legs Sheathed Yes No 4.67 ± 2.75
3 2 Sessile C Full, opaque Sheathed Yes No 2.14 ± 2.59
4> 2 Somewhat C Full, opaque Free Yes Yes 1.00 ± 1.31
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

120 Polar Biology (2019) 42:115–130
1 3
above and in Table2, followed by recording their eclosion
date and any subsequent oviposition by adults.
Adult emergence
Three 0.5-m2 quadrats were set out on a moss bank adjacent
to the research station and all were monitored twice daily for
5min at 1000 and 1600 local time, noting the presence of
adults active on the surface, between 20 December 2016 and
6 January 2017. Ground surface temperature readings were
taken each day during the observation periods, as described
above.
Egg maintenance andlarval development
Laboratory cultures established from the 2014/2015
stocks enabled the rearing of larvae to pupation and sub-
sequent emergence with successful oviposition. From
these laboratory eggs, an initial four-phase classification
system of embryonic development was established to aid
development stage identification (Table3). All laboratory
adults that emerged and then oviposited under one of the
experimental environmental conditions described above
were subsequently maintained with their egg sacs at 5°C
on saturated substrate to maintain sac structure. Hydrated
egg sac diameters were measured, and numbers of eggs
were recorded. Eggs were assessed every 48h, and devel-
opmental stage recorded.
Monitoring ofegg development intheeld
Recently laid egg sacs (n = 11) collected from field sam-
ples were placed in open 2-cm petri dishes with saturated
substrate in an external arena and monitored every 48h
until development ceased, or the eggs hatched (a maxi-
mum of 39days), and then again on day 45 to confirm that
Table 3 Description of egg development stages and classification guide for development tracking
Typical duration of each stage given and mean success rate/progression to next phase ± SEM. Success rate = % that successfully complete each
development stage
Egg stage Image Description Develop-
ment
(days)
Success rate (%)
1—Opal
1mm
Opaque white eggs granulated and slightly iridescent in appearance.
No pigmentation
10–14 66 ± 2.72
2—Yellow
1mm
Outer-casing turning yellow/brown. Still granulated and no sign yet of
embryonic form.
5–7 100
3—Early embryo
200µm
Shape of embryo becomes clearer and red stemmata eyes become
evident.
7–10 92.2 ± 0.97
4—Late embryo
100µm
Pharate larva visible with some evidence of internal organs, eyes and
mandibles clearly visible.
7–10 82 ± 2.29
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

121Polar Biology (2019) 42:115–130
1 3
no further delayed development had occurred. Tempera-
ture readings inside the arena were noted daily as above.
The development stage of each egg (Table3) within each
egg sac was recorded using a dissecting microscope. On
day 45, all egg sacs were dissected, and any remaining
unhatched eggs individually inspected. A total of n = 740
eggs were assessed.
Phenology ofsummer‑occurring life stages
Weekly soil cores (n = 5) were taken from a site adjacent to
the research station where E. murphyi was abundant, using a
steel 5-cm × 10-cm corer. This took place between 23 Janu-
ary and 6 March 2017 (= late summer season). Soil cores
were returned to the Signy laboratory in a sterile sealed bag
and processed within 24h. Cores were divided into vegeta-
tion and soil/peat substratum and weighed using a Sartorius
precision balance (E6202) before being carefully washed
separately through stacked sieves as described above. All life
stages were extracted, sorted into groups (adults; pupae; L4
larvae; L3 larvae; L2 larvae; eggs unhatched, eggs hatched)
and counted. L1 larvae were not included as their small size
would have resulted in sample processing being too time
consuming. All sieved substrate was dried for 24h at 60°C
and re-weighed to obtain constant dry mass, against which
all counts were normalised. An additional core was collected
each week, divided into vegetation and soil components and
used to make pH and salinity measurements with a Hanna
combo water reader (HI-98129). Throughout the field period
in 2016/2017, the presence of pupae or adults on the surface
were recorded, from which the final dates of sighting of both
pupae and adults were established.
Results
Environmental description
The Signy field site was generally very stable through-
out the 2016/2017 season. The mean pH in the vegeta-
tion layer was 5.3 ± 0.13 SE, n = 7, and underlying soil pH
was 5.5 ± 0.11 SE, n = 7. Salinity was also largely stable,
with only one spike during a week of high storm activity
detected in the vegetation layer, when it rose to 425µS
from an average of 174 ± 45µS SE, n = 7. Salinity in the
soil layer remained close to 70 ± 10µS SE, n = 7.
Larval classication
Size class analysis proved to be suitable for separating the
four larval instars, with each size class being significantly
different from each other in both width at SIV and length
(Fig.2), and no overlap between instar size classes.
Fig. 2 Classification of the four larval instars by a total body length
and b width at segment four/five intersection; n = 10 individuals for
each of L1, 3 and 4, n = 12 individuals for L2. All instars signifi-
cantly different from each other for length: ANOVA F(3,31) = 372.2,
p < 0.0001; width: ANOVA F(3,34) = 780.7, p < 0.0001. c Larval
instars side by side: Top to bottom, L1 to L4
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

122 Polar Biology (2019) 42:115–130
1 3
Larval survival andenvironmental triggers
forpupation
Larval survival (Fig.3) was greatest in the control/dark
5°C conditions (70% survival after 60days), and was
significantly different from the light treatments (two-way
ANOVA with Tukey’s multiple comparisons column fac-
tor, F(3,20) = 9.71: Light 2 °C—32.5% survival after
60days, p = 0.008; Light 5°C—30% survival after 60days,
p < 0.001). Overall survival dropped significantly over time
across all treatments (two-way ANOVA with Tukey’s multi-
ple comparisons, F(4,20) = 11, p < 0.0001) and soil moisture
only had a small effect on survival in the warmest lit condi-
tions of Light 5°C (Mann–Whitney U = 3, p = 0.046,). Of all
environmental conditions tested, the fluctuating freeze/thaw
cycle of + 5°C/0°C with corresponding 19:5/L:D, which is
the condition most reflective of Signy summer conditions,
led to the greatest level of pupation, although this was not
significantly different from other treatments (Kruskal–Wal-
lis, H = 13.7, p = 0.6).
Pupal classication anddevelopment
Pupae exhibited four distinct phases of development before
completing the molt to imago (Table2). Broadly, the first
and second phases were differentiated by an increased level
of pigmentation and development of the gonads. The third
phase was quite sessile, deeply pigmented and with the legs
still encased in leg sheaths. There was a thickening of the
cuticle in this stage. The final fourth phase was a partial
eclosion, where the legs were free of the sheath but the
imago not fully eclosed from the exuvia. Mean develop-
ment time in the field from initial pupation to eclosion was
14days (± 5 days, n = 12), with the longest period spent
in the seconnd phase of pupation (Table2). There was no
difference in development rates of pupae incubated at con-
stant or fluctuating temperature in laboratories in the UK,
compared with those in the field conditions with a fluctuat-
ing temperature on Signy Island (Kruskal–Wallis, H = 1.3,
p = 0.54).
Eclosion, imago development andphenology
Only 45% of pupae (n = 20) placed within the external field
arenas successfully eclosed, and 55% of these adults ovipos-
ited. There was no correlation between numbers of individu-
als eclosing and either ambient temperature on the ground
surface over the preceding 24h or within the pupation arena
at the time of sampling (surface temperature: rs =0.21,
p = 0.4; arena temperature: rs =0.31, p = 0.2). There was,
however, a strong correlation between the temperature out-
side the arena and the spot temperature taken within it at the
time of surveying, verifying that the arena did not increase
temperature artificially (rs =0.88, p < 0.0001). Monitoring
of quadrats for the presence of adults showed no correlation
with daily ambient mean temperatures (r2 = 0.07), although
anecdotally adult presence was associated with calm clear
days (Online Resource 1).
Egg classication andmonitoring
Egg sacs (n = 30) had a mean dry mass of 0.14 mg
(± 0.06mg) and water content of 96% (± 1.29%) fresh
mass. Egg sacs contained a mean of 48 (± 12.48 n = 30)
individual eggs and had a diameter of 1.78 (± 0.4 n = 30)
mm, with size not being significantly correlated to either
number of eggs or water content (r2 = 0.08 and 0.009,
respectively). Changes in the proportion of different egg
stages within egg sacs (Table3) until hatching are pre-
sented in Fig.4a. Stage 1 (opal) spanned c. 14days across
all samples, although very consistently across all egg
sacs approximately 40% of eggs did not develop beyond
this stage (Fig.4b). The eggs then turned yellow, before
the early embryo with stemmata evident become visible
around day 19. Late embryos, with visible mandibles and
pharate larvae, appeared around day 25 and eggs hatched
by day 31. Development within an individual egg sac was
not tightly synchronised. After 45days of field observa-
tions of n = 740 eggs, 40% (± 2.72%) did not progress
past the first ‘opal’ stage (Fig.4b). Nearly all remaining
eggs progressed through the yellowing phase, but 7.6%
(± 0.97%) did not progress beyond the early embryo and
16% (± 2.29%) beyond the late embryo, with only 35% of
all eggs (± 2.44%) going on to hatch. There was no differ-
ence in development rates of eggs incubated at constant
temperature compared with those under field conditions
Fig. 3 a Larvae survival over 60days after exposure to varied light,
temperature and substrate saturation levels (n = 20 for each condi-
tion). Survival over time across all treatments (2-way ANOVA Tuk-
ey’s post hoc comparisons, F(4,20) = 11, p = < 0.0001). Soil moisture
effect the only significant variable in Light 5°C (Mann–Whitney U,
p = 0.046). b Total pupations from larvae during experimental condi-
tions (Kruskal–Wallis, H = 13.7; p = 0.6)
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

123Polar Biology (2019) 42:115–130
1 3
with fluctuating temperature (Mann–Whitney U = 17,
p = 0.62) (Fig.5). Phenology andenvironmental factors
Seasonal life-stage monitoring in the field over the late sum-
mer showed that the E. murphyi population had progressed
Fig. 4 a Egg development in field conditions on Signy Island. Stages of individual egg (n = 740) development within each egg sac (n = 11)
recorded over time, shown with CI of 95%. b Maximum stage reached after 45days of monitoring (Tukey’s plot) with outliers
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

124 Polar Biology (2019) 42:115–130
1 3
through pupal and adult stages before the end of January
(Fig.6a). The last pupae were found on 3 January 2017 and
the last adult was seen on 19 January 2017 (Fig.6b). By
13 February 2017, no further viable unhatched eggs were
found in the samples (determined by the presence of hatched
eggs alongside those that had stalled development at a much
earlier stage), with only hatched eggs collected thereafter.
Unhatched eggs that were considered undeveloped/unviable
appeared to decompose, becoming opaque, soft and bloated,
often combined with visible fungal development. The phe-
nological soil core surveys did not include any counts of
adults or pupae (Fig.6b), so these were discounted from
analysis. There was no significant difference in the appear-
ance of the larval instars or trend over time (Kruskal–Wallis,
H = 1.3, p = 0.53; r2 = 0.1). The appearance of unhatched and
then hatched eggs did show a visible difference (Fig.6b),
with a distinct increase in the number of hatched eggs over
time compared to a decline in unhatched (Mann–Whitney
U = 202, p = 0.008).
Population success
Analysis of reproductive output (Table4) suggests that the
E. murphyi population can potentially double with each life
cycle. Considering the percentage of larvae that survive over
60 days, pupae that successfully eclose, adults that success-
fully oviposit and the viability of eggs laid, this will amount
to an average 50,000 additional L1 added to the population
every two years, based on the most recent distribution data
reported by Hughes and Worland (2010) (Table4).
Discussion
Larval andpupal development
The developmental stages described here for larval instars
are consistent with the only taxonomic study of E. murphyi
(Cranston 1985) and provide a first description of the L1
and L2 instars. Like the sister species B. antarctica (Sugg
etal. 1983), and typical for chironomids, there are four lar-
val instars, which in our data do not overlap in size classes
for either width or length and provide a clearer assessment
Fig. 5 Mean (± SE) time (days) taken to complete egg or pupal stage
under different temperature conditions. Also shown, the mean period
from eclosion to oviposition and adult longevity post eclosion. Field
conditions are shown as the mean temperature experienced (F: x̄)
over the relevant period. Pupae and adult development periods over-
lapped and thus were subject to the same average field temperatures.
Lab temperatures were either static 5°C or 12h 5/12h 0°C. Sam-
ple sizes—Egg development: “F: x̄ 3.5″, n = 6 egg sacs; “+ 5″ n = 7.
Pupae development: “F: x̄ 4.2″ n = 5; “+ 5″ n = 4. Oviposition “F: x̄
4.2″ n = 5; “+ 5″ n = 4. Adults “F: x̄ 4.2″ n = 5; + 5 n = 4
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

125Polar Biology (2019) 42:115–130
1 3
of all instars than the use of body mass classes (cf. Hughes
etal. 2013). Our observations of pupae indicate that meta-
morphosis takes around 14 d, and can be divided into four
morphologically distinct phases, providing a new level of
detail for E. murphyi and for chironomids in general, whose
pupal stage is understudied (Armitage etal. 1995). Appar-
ent obligate parthenogenesis in E. murphyi enables oviposi-
tion to occur prior to the completion of eclosion. Whilst this
alone is not unique among asexual chironomids (Armitage
etal. 1995; Langton etal. 1988), it does offer E. murphyi a
Fig. 6 a Mean (weekly) hours
of daylight and darkness as well
as high and low air temperatures
on Signy Island, annotated with
key points in the development
of E. murphyi life stages: SM
basal snow melt, mid Nov 2016;
LP last pupae seen 3 Jan 2017;
LA last adult seen 19 Jan 2017;
LE last unhatched eggs seen
30 Jan 2017; SR snow returned
27 Feb 2017. b Abundance of
different E. murphyi life stages
found in soil cores from a single
site collected from late Janu-
ary to the beginning of March
2017, shown as mean percent-
age of total population (±SE).
A adults, P pupae; L2, L3 and
L4 larval instars; EU egg sacs
where majority (> 50%) of eggs
were unhatched, EH egg sacs
where the majority (> 50%) of
eggs had hatched
Table 4 Life stage success table using population densities of larvae reported by Hughes and Worland (2010)
Average larval densities are taken from the whole sample site. ~70% of L4 larvae survive; 45% of larvae successfully eclose, 55% then oviposit,
with a mean of 48 eggs per oviposition and 35% go on to hatch
Population density Larvae density (m2) Approximate lar-
vae survival (m2)
Successfully
eclose (m2)
Successfully
oviposit (m2)
Total Eggs laid (m2) Total Hatched (m2)
High 150,000 105,000 47,250 25,987 1,247,400 361,746
Average 21,000 14,700 6,615 3,638 174,636 50,644
Low 500 350 157 87 4,158 1,205
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

126 Polar Biology (2019) 42:115–130
1 3
distinct advantage in a polar habitat such as on Signy Island,
enabling it to reproduce even if conditions or physiology do
not permit eclosion. Our data do not provide evidence for
a temperature or moisture/spring thaw trigger for pupation.
Fluctuating temperatures of the spring season (+ 5/0°C),
did result in more pupae; however, this was not statisti-
cally different from other treatments. Block etal. (1984)
reported that pupae of E. murphyi appeared shortly after
spring thaws, and a similar observation has been reported in
an aquatic Antarctic midge, Parochlus steinenii (Hahn and
Reinhardt 2006; Rauschert 1985), but further early season
sampling will be required to clarify the cues required to initi-
ate pupation.
Adult emergence andparthenogenesis
The emergence of E. murphyi adults does not take place in a
synchronous mass event as reported in B. antarctica (Sugg
etal. 1983) but continues over a 2–3-month period (Online
Resource 1). In the 2016/2017 summer season, adults were
already noted to be active when Signy station was opened
in mid-November (Station Leader M. Jobson, pers. comm.),
coinciding with an early spring thaw. Hatched eggs were
already present in the soil in late December 2016 which,
based on the egg development times recorded in this study,
means they would have been laid in late November at the
earliest. This could give E. murphyi a distinct advantage
over sexual reproducers, such as B. antarctica, the only
chironomid that successfully completes its life cycle on the
Antarctic Peninsula. Whilst B. antarctica is limited by the
need to have males and females emerge synchronously to
reproduce sexually, E. murphyi is not even limited by the
need to complete eclosion. Staggering the emergence period
means that any adverse weather encountered in the summer
months would not necessarily impede the species’ continued
survival on the island, as posited by Hughes etal. (2013).
The lack of mass emergence also suggests that E. murphyi
has a more flexible life history, and emergence may be trig-
gered by significant environmental cues for favourable con-
ditions rather than any obligate physiology.
Parthenogenetic reproduction is a common feature within
the Chironomidae, and in the Orthocladiinae usually takes
the complete form of parthenogenesis known as thelytoky
(Moller Pillot 2014; Scholl 1956; Thienemann 1954). In
thelytoky, genetic fertilisation is absent and so females
only produce female progeny, as is seen in E. murphyi
(Convey 1992; Cranston 1985). It is likely that E. murphyi
exhibits apomictic thelytoky, the most widespread from of
thelytoky in Orthocladiinae (Scholl 1956, 1960) and that
the lack of progression of a significant proportion of eggs
beyond the initial development stage seen here is the result
of a mechanical failing at an early maturation stage of mito-
sis (Porter and Martin 2011), possibly as the result of an
environmental stressor. It is thought that the adoption of
thelytoky by arthropods is an advantageous strategy. It may
particularly benefit polar species, through the elimination of
males, which have been shown to be more susceptible to the
cold and extremes in temperature (Oliver and Danks 1972;
Rinehart etal. 2000; David etal. 2005; Colinet and Hance
2009). Thus, the need for synchronous mass emergence is
redundant. (Downes 1962; Porter and Martin 2011).
Egg development
A total of 740 individual eggs were studied to document
embryogenesis and hatching. Unusually for the sub-family
Orthocladiinae, eggs are laid in an almost uniform spherical
mass rather than in a rope-like mass or bale, a trait that is
otherwise used to define the group (Nolte 1993) and that is
also exhibited by B. antarctica. Individual egg morphology
is consistent with previous descriptions of Orthocladiinae
(Armitage etal. 1995; Nolte 1993; Thienemann and Stren-
zke 1940), and particularly that of B. antarctica (Harada
etal. 2014). Eretmoptera murphyi individuals produced an
average clutch size of 48 eggs in this study, of which only
29% hatched successfully. This is a small clutch size for a
chironomid midge, which typically produce hundreds if not
thousands of eggs, but not unusual for terrestrial Orthocladi-
inae which have been recorded to lay eggs in numerous small
batches or even individually (Nolte 1993). Another Antarc-
tic chironomid, P. steinenii lays an average of 191 eggs per
batch, sometimes over multiple batches (Hahn and Reinhardt
2006), whilst Harada etal. (2014) describe a mean batch size
of 41 eggs per string for B. antarctica with a gestation of just
16days. Neither of these studies documented the percentage
of eggs that go on to hatch.
With ground surface temperature variation of as much as
24.8°C (see Online Resource 2) in a 12-h period on Signy
Island, temperature stress may account for the long egg
development time and high mortality observed. Despite the
low clutch size and hatching success, our data indicate that
at least 13 eggs will hatch for every E. murphyi adult. With
population densities as high as 150,000 ind.m2 (Hughes
and Worland 2010), this could result in as many as 1.2 mil-
lion eggs being laid per m2 in parts of the species’ current
distribution and, consequently, further local dispersal if no
checks are held on the population at other points in the life
cycle. However, as nearly half of all pupae failed to eclose
to adult under field conditions, and 55% of adults failed to
successfully oviposit, these two life stages appear to repre-
sent a major limitation. Whether this indicates lower stress
tolerance in these life stages requires further study, given
that only larval stages have been studied in detail to date.
Even taking this into account, with an average density of E.
murphyi within its distribution on Signy Island of 21,000
ind. m2 (Hughes and Worland 2010), we estimate that the
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

127Polar Biology (2019) 42:115–130
1 3
species could have the potential to double its population over
every life cycle of two years. If so, a simple back-calculation
would suggest an introduction date of a single individual
in the early 1970s, which is generally consistent with the
assumed introduction event with plant transplants in the lat-
ter part of the 1960s (Burn 1982; Block etal. 1984).
Phenology
Although all larval instars were present throughout the study
period (Fig.6b), their relative densities were highly vari-
able over time. These data appear to reflect more the patchi-
ness of larval distribution than the sequential occurrence
of particular instars over time. Whilst eggs are immobile
and thus easier to represent through repeated sampling in a
fixed location, larvae are mobile. Patchiness in larval distri-
bution, including aggregations of larvae, was also reported
by Hughes and Worland (2010), and is a characteristic of
Antarctic terrestrial invertebrate communities (Usher and
Booth 1984). Any increase in hatched eggs naturally infers
an increase in the number of L1 in the soil but, due to the
very small size of this instar, it was not practicable to include
them in this survey. Unhatched eggs do not overwinter. Bel-
gica antarctica is also thought to overwinter only in the
larval stage and in all four instars (Sugg etal. 1983). How-
ever, during soil core analyses, L1 and L3 E. murphyi larvae
were noted to be molting towards the end of the season,
indicating that L2 and L4 are likely to be the primary over-
wintering larval instars, as suggested by Convey (1996a) and
Hughes etal. (2013).
A mid-range climate forecast for the Antarctic Peninsula
and South Orkney Islands suggests that mean annual air
temperatures are expected to increase by 1.5–2°C by 2100
(Larsen etal. 2014). Temperature warming is thought to
benefit polar terrestrial invertebrates by reducing the stress
of low-temperature extremes and giving greater liquid water
availability (Bale and Hayward 2010; Convey 2006, 2011;
Convey etal. 2014) and, in the case of non-native species,
making available locations that were previously uninhab-
itable. By increasing our knowledge of E. murphyi’s life
cycle, we can better understand any threat it may pose to
Signy Island terrestrial ecosystems, and its potential as an
invasive invertebrate at other at-risk areas, such as along the
Antarctic Peninsula (Fig.7).
Fig. 7 Summary of Eretmoptera murphyi’s life cycle
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

128 Polar Biology (2019) 42:115–130
1 3
Conclusions
This study provides the first comprehensive documentation
of the life cycle of E. murphyi, a flightless chironomid midge
that is currently expanding its distribution following anthro-
pogenic introduction to Signy Island. The species’ reliance
on parthenogenesis is confirmed and new information pro-
vided on the characteristics of all life stages, their develop-
ment rates, the phenology of previously undescribed eggs
and pupae and the emergence of adults. Adults do not show
synchronised emergence, rather appearing throughout the
first half of the summer season, which suggests a flexible
life history strategy where emergence is not dependent on
any discrete environmental cue. Ground temperature vari-
ability and spikes in field temperature may explain the long
development time of eggs compared to previous laboratory
studies, and their low percentage of successful maturation.
Despite the limitations on survival at each of the life stages,
the population is potentially able to double in size every life
cycle/2years, highlighting the ability of this species to fur-
ther expand its population and distribution on Signy Island.
This study provides a springboard for further description
and physiological studies of all life stages of this species,
which will increase our understanding of the risks it poses
as a non-native species on Signy Island, and the potential to
colonise new areas, if given opportunity.
Acknowledgements J Bartlett is funded by a Natural Environment
Research Council (NERC) through The Central England NERC
Training Alliance (CENTA) Doctoral Training Partnership (DTP)
(RRBN19276). Her PhD studentship is supported by the University
of Birmingham and the British Antarctic Survey (BAS). P. Convey
is supported by NERC core funding to the BAS ‘Biodiversity, Evolu-
tion and Adaptation’ Team. Fieldwork in this study was supported by
BAS through a NERC–CASS grant (CASS-121) and permitted by the
British Foreign and Commonwealth Office through Specialist Activi-
ties in Antarctica (No 22/2016). The authors also thank staff at Signy
Research Station for their practical and moral support, and thank the
reviewers for their helpful comments. This study contributes to the
SCAR ‘State of the Antarctic Ecosystem’ (AntEco) programme.
Compliance with ethical standards
Conflict of interest We confirm that no part of this study has been pub-
lished before or is under consideration for any other journal by either
myself or my co-authors. None of the authors have any conflicts of
interest to disclose and all authors have approved this manuscript and
its submission to Polar Biology.
Ethical approval We confirm that the use of invertebrates complied
with all relevant ethical standards and that field work in Antarctica
was conducted with permissions from the UK Foreign Office and that
returned samples were permitted by the Department for the Environ-
ment, Farming and Rural Affairs (DEFRA).
Open Access This article is distributed under the terms of the Crea-
tive Commons Attribution 4.0 International License (http://creat
iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use,
distribution, and reproduction in any medium, provided you give appro-
priate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made.
References
Allegruci G, Carchini G, Convey P, Sbordoni V (2012) Evolutionary
geographic relationships among orthocladine chironomid midges
from maritime Antarctic and sub-Antarctic islands. Biol J Linn
Soc 106:258–274
Allegruci G, Carchini G, Todisco V, Convey P, Sbordoni V (2006) A
molecular phylogeny of Antarctic Chironomidae and its impli-
cations for biogeographical history. Polar Biol 29:320–326
Armitage P, Pinder L, Cranston P (1995) The Chironomidae: biology
and ecology of non-biting midges. Springer, Dordrecht
Bale JS, Hayward SAL (2010) Insect overwintering in a changing
climate. J Exp Biol 213:980–994
Block W, Burn AJ, Richard KJ (1984) An insect introduction to the
maritime Antarctic. Biol J Linn Soc 23:33–39
Block W, Convey P (1995) The biology, life cycle and ecophysiol-
ogy of the Antarctic mite Alaskozetes antarcticus (Michael). J
Zool 236:431–449
Burn AJ (1982) A cautionary tale—two recent introductions to the
maritime Antarctic. Comité National Francais des Recherches
Antarctiques 51:521
Cannone N, Guglielmin M, Convey P, Worland MR, Favero-Longo
SE (2016) Vascular plant changes in extreme environments:
effects of multiple drivers. Clim Change 134:651–665
Chown SL, Convey P (2016) Antarctic entomology. Ann Rev Ento-
mol 61:119–137
Chown SL, Lee SL, Hughes KA, Barnes J, Barrett P, Bergstrom DM,
Convey P, Cowan DA, Crosbie K, Dyer G, Frenot Y, Grant SM,
Herr D, Kennicutt MC, Lamers M, Murray A, Possingham HP,
Reid K, Riddle MJ, Ryan PG, Sanson L, Shaw JD, Sparrow DM,
Summerhayes C, Terauds A, Wall DH (2012) Challenges to
the future conservation of the Antarctic. Science 337:158–159
Colinet H, Hance T (2009) Male reproductive potential of Aphidius
colemani (Hymenoptera: Aphidiinae) exposed to constant or
fluctuating thermal regimens. Environ Entomol 38:242–249
Convey P (1992) Aspects of the biology of the midge Eretmoptera
murphyi introduced to Signy Island Maritime Antarctic. Polar
Biol 12:653–657
Convey P (1994) The influence of temperature on individual growth
rates of the Antarctic mite Alaskozetes antarcticus. Acta Oecol
15:43–53
Convey P (1996a) Overwintering strategies of terrestrial inverte-
brates in Antarctica—the significance of flexibility in extremely
seasonal environments. Eur J Entomol 93:489–505
Convey P (1996b) The influence of environmental characteristics
on life history attributes of Antarctic terrestrial biota. Biol Rev
71:191–225
Convey P (2006) Antarctic climate change and its influences on ter-
restrial ecosystems. In: Bergstrom D, Convey P, Huiskes A (eds)
Trends in Antarctic terrestrial and limnetic ecosystems: Ant-
arctica as a global indicator. Springer, Dordrecht, pp 253–272
Convey P (2011) Antarctic terrestrial biodiversity in a changing
world. Polar Biol 34:1629–1641
Convey P (2013) Antarctic ecosystems. In: Levin SA (ed) Encyclo-
pedia of biodiversity, 2nd edn. Academic Press, Waltham
Convey P, Block W (1996) Antarctic Diptera: ecology, physiology
and distribution. Eur J Entomol 93:1–13
Convey P, Lebouvier M (2009) Environmental change and human
impacts on terrestrial ecosystems of the sub-Antarctic islands
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

129Polar Biology (2019) 42:115–130
1 3
between their discovery and the mid-Twentieth Century. Pap
Proc R Soc Tasmania 143:33–44
Convey P, Bindschadler RA, di Prisco G, Fahrbach E, Gutt J, Hodg-
son DA, Mayewski PA, Summerhayes CP, Turner J (2009) Ant-
arctic climate change and the environment. Ant Sci 21:541–563
Convey P, Chown S, Clarke A, Barnes D, Bokhurst S, Cummings V,
Ducklow H, Frati F, Green A, Gordon S, Griffiths H, Howard-
Williams C, Huiskes A, Laybourn-Parry J, Berry Lyons W,
McMinn A, Morley S, Peck L, Quesada A, Robinson S, Schia-
parelli S, Wall DH (2014) The spatial structure of Antarctic
biodiversity. Ecol Monogr 84:203–24
Coulson S, Convey P, Aakra K, Aarvik L, Ávila-Jiménez M, Babenko
A, Biersma E, Bostrom S, Brittain JE, Carlsson AM, Christoffer-
sen K, De Smet WH, Ekrem T, Fjellberg A, Fureder L, Gustafs-
son D, Gwiazdowicz DJ, Hansen LO etal (2014) The terrestrial
and freshwater invertebrate biodiversity of the archipelagos of the
Barents Sea; Svalbard, Franz Josef Land and Novaya Zemlya. Soil
Biol Biochem 68:440–470
Cranston PS (1985) Eretmoptera murphyi Schaeffer (Diptera: Chi-
ronomidae), an apparently parthenogenetic Antarctic midge. Br
Antarct Surv Bull 66:35–45
Danks H (1999) Life cycles in polar arthropods: flexible or pro-
grammed? Eur J Entomol 96:83–102
David JR, Araripe LO, Chakir M, Legout H, Lemos B, Petavy G,
Rohmer C, Joly D, Moreteau B (2005) Male sterility at extreme
temperatures: a significant but neglected phenomenon for under-
standing Drosophila climatic adaptations. J Evol Biol 18:838–846
Downes JA (1962) What is an Arctic insect? Can Entomol 94:143–162
Duckhouse D (1985) Psychodidae (Diptera, Nematocera) of the sub-
antarctic islands, with observations on the incidence of partheno-
genesis. Int J Entomol 27:173–184
Everatt MJ, Worland MR, Bale JS, Convey P, Hayward SAL (2012)
Pre-adapted to the maritime Antarctic? Rapid cold hardening of
the midge, Eretmoptera murphyi. J Insect Physiol 58:1104–1111
Everatt MJ, Convey P, Mirbahai L, Worland MR, Bale JS, Hayward
SAL (2014) Can the Antarctic terrestrial midge, Eretmoptera mur-
phyi, tolerate life in water? Ecol Entomol 39:732–735
Everatt MJ, Convey P, Bale JS, Worland MR, Hayward SAL (2015)
Responses of invertebrates to temperature and water stress: a polar
perspective. J Therm Biol 54:118–132
Fogg G, Thomas DN, Convey P, Fritsen C, Gilli JM, Gradinger R,
Laybourne-Parry J, Reid K, Walton DWH (2008) The biology of
polar habitats. Oxford University Press, Oxford
Frenot Y, Chown SL, Whinam J, Selkirk PM, Convey P, Skotnicki
M, Bergstrom DM (2005) Biological invasions in the Antarctic:
extent, impacts and implications. Biol Rev 80:45–72
Gardiner MJ, Ellis-Evans JC, Anderson G, Tranter M (1998) Snowmelt
modelling on Signy Island South Orkney Islands. Ann Glaciol
26:161–166
Gercke C (1889) Vorlufige Nachricht über die Fliegen Süd-Georgiens,
nach der Ausbeute der Deutschen Station 1882–83. Jahrbuch der
Hamburgischen Wissenschaftlichen Anstalten 6:153–154
Greenslade P, Potapov M, Russell D, Convey P (2012) Global Col-
lembola on Deception Island. J Insect Sci 12:111
Hahn S, Reinhardt K (2006) Habitat preference and reproductive traits
in the Antarctic midge Parochlus steinenii (Diptera: Chironomi-
dae). Antarct Sci 18:175–181
Harada E, Lee R, Denlinger D, Goto S (2014) Life history traits of
adults and embryos of the Antarctic midge Belgica antarctica.
Polar Biol 37:1213–1217
Hayward SAL, Worland MR, Convey P, Bale JS (2003) Temperature
preferences of the mite, Alaskozetes antarcticus, and the col-
lembolan, Cryptopygus antarcticus from the maritime Antarctic.
Physiol Entomol 28:114–121
Hughes KA, Worland MR (2010) Spatial distribution, habitat prefer-
ence and colonization status of two alien terrestrial Invertebrate
species in Antarctica. Antarct Sci 22:221–231
Hughes KA, Ott S, Bölter M, Convey P (2006) Colonisation processes.
In: Bergstrom DM, Convey P, Huiskes L (eds) Trends in Antarctic
terrestrial and limnetic ecosystems. Springer, Dordrecht, pp 35–54
Hughes KA, Worland MR, Thorne M, Convey P (2013) The non-native
chironomid Eretmoptera murphyi in Antarctica: erosion of the
barriers to invasion. Biol Invasions 15:269–281
Hughes KA, Pertierra L, Molina-Montenegro M, Convey P (2015)
Biological invasions in terrestrial Antarctica: what is the current
status and can we respond? Biodiv Conserv 24:1031–1055
Jacobs C (1900) Diagnoses d’insectes recueillis par l’Expédition ant-
arctique Belge. Diptera Annales de la Société Entomologique de
Belgique 44:106–107
Kellogg V (1900) An extraordinary new maritime fly. Biol Bull
1:81–87
Langton P, Cranston P, Armitage P (1988) The parthenogenetic
midge of water supply systems, Paratanytarsus grimmii (Sch-
neider) (Diptera: Chironomidae). Bull Ent Res 78:317–328
Larsen JN etal (2014) Polar regions. In: Barros VR etal (eds) Cli-
mate change 2014: impacts, adaptation, and vulnerability. Part
B: regional aspects. Contribution of Working Group II to the fifth
assessment report of the Intergovernmental Panel on Climate
Change. Cambridge University Press, Cambridge, pp. 1567–1612
Molina-Montenegro MA, Carrasco-Urra F, Rodrigo C, Convey P, Vall-
dares F, Gianoli E (2012) Occurrence of the non-native annual
bluegrass on the Antarctic mainland and its negative effects on
native plants. Conserv Biol 26:717–723
Moller-Pillot H (2014) Chironomidae Larvae, Vol. 3: Orthocladi-
inae:Biology and Ecology of the Aquatic Orthocladiinae. Hotei/
KNNV, Zeist, Netherlands. pp 7–21
Nolte U (1993) Egg masses of Chironomidae (Diptera). A review,
including new observations and a preliminary key. Scand Ento-
mol 120:1–75
Oliver DR, Danks HV (1972) Sex ratios of some high Arctic Chirono-
midae (Diptera). Can Entomol 104:1413–1417
Porter D, Martin J (2011) Cytogenetics of a parthenogenetic Arctic spe-
cies of Micropsectra (Diptera, Chironomidae). Comp Cytogenet
9:315–28
Rauschert M (1985) Beobachtungen an der Chironomidae Parochlus
steineni auf der Insel King George (Südshetlandinseln, Antarktis)
(Diptera, Chironomidae). Deutsche Entomologische Zeitschrift
32:183–188
Rinehart JP, Yocum GD, Denlinger DL (2000) Thermotolerance and
rapid cold hardening ameliorate the negative effects of brief expo-
sures to high or low temperatures on fecundity in the flesh fly
Sarcophaga crassipalpis. Phys Entomol 25:330–336
Royles J, Ogée J, Wingate L, Hodgson A, Convey P, Griffiths H (2012)
Carbon isotope evidence for recent climate-related enhancement
of CO2 assimilation and peat accumulation rates in Antarctica.
Global Change Biol 18:3112–3124
Schaeffer C (1914) Collembola. Siphonaptera, Diptera and Coleoptera
of the South Georgia Expedition. Brooklvn Inst Mus Sci Bull
2:90–94
Scholl H (1956) Die Chromosomen parthenogenetischer Mücken.
Naturwissenschaften 43:91–92
Scholl H (1960) Die oogenese einiger parthenogenetischer Orthocla-
diinen Diptera. Chromosoma 11:380–401
Smith R (1990) Signy Island as a paradigm of biological and envi-
ronmental change in Antarctic terrestrial ecosystems. In: Kerry
KR, Hempel G (eds) Antarctic ecosystems: ecological change and
conservation. Springer, Berlin, pp 32–50
Sugg P, Edwards JS, Baust J (1983) Phenology and life history of
Belgica antarctica, an Antarctic midge (Diptera: Chironomidae).
Ecol Entomol 8:105–11
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

130 Polar Biology (2019) 42:115–130
1 3
Thienemann A (1954) Chironomus. Leben, Verbreitung und
wirtschaftliche Bedeutung der Chironomiden. Die Binnen
gewässer 20:278–282
Thienemann A, Strenzke K (1940) Terrestrische chironomiden III–IV.
Zwei parthenogentische Formen Zool Anz 132:24–40
Tin T, Fleming ZL, Hughes KA, Ainley DG, Convey P, Moreno CA,
Pfeiffer S, Scott J, Snape I (2009) Impacts of local human activi-
ties on the Antarctic environment. Antarct Sci 21:3–33
Turner J, Chenoli SN, abu Samah A, Marshall G, Phillips T, Orr A
(2009) Strong wind events in the Antarctic. J Geophys Res. https
://doi.org/10.1029/2008J D0116 42.
Turner J, Barrand N, Bracegirdle T, Convey P, Hodgson DA, Jarvis
M, Jenkins A, Marshall G, Meredith MP, Roscoe H, Shaklin J,
French J, Goosse H, Guglielmin M, Gutt J, Jacobs S, Kennicutt
MC, Masson-Delmotte V, Mayewski P, Navarro F, Robinson S,
Scambos T, Sparrow M, Summerhayes C, Speer K, Klepikov A
(2014) Antarctic climate change and the environment: an update.
Polar Rec 50:237–259
Usher MB, Booth RG (1984) Arthropod communities in a maritime
Antarctic moss-turf habitat: three-dimensional distribution of
mites and Collembola. J Anim Ecol 53:427–441
Usher MB, Edwards M (1984) A dipteran from south of the Antarctic
Circle: Belgica antarctica (Chironomidae) with a description of
its larva. Biol J Linn Soc 23:19–31
Volonterio O, Ponce de León R, Convey P, Krzeminska E (2013) First
record of Trichoceridae (Diptera) in the maritime Antarctic. Polar
Biol 36:1125–1131
Worland MR (2010) Eretmoptera murphyi: pre-adapted to survive a
colder climate. Physiol Entomol 35:140–145
Worland MR, Convey P (2008) The significance of the moult cycle to
cold tolerance in the Antarctic collembolan Cryptopygus antarcti-
cus. J Insect Physiol 54:1281–1285
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

1.
2.
3.
4.
5.
6.
Terms and Conditions
Springer Nature journal content, brought to you courtesy of Springer Nature Customer Service Center GmbH (“Springer Nature”).
Springer Nature supports a reasonable amount of sharing of research papers by authors, subscribers and authorised users (“Users”), for small-
scale personal, non-commercial use provided that all copyright, trade and service marks and other proprietary notices are maintained. By
accessing, sharing, receiving or otherwise using the Springer Nature journal content you agree to these terms of use (“Terms”). For these
purposes, Springer Nature considers academic use (by researchers and students) to be non-commercial.
These Terms are supplementary and will apply in addition to any applicable website terms and conditions, a relevant site licence or a personal
subscription. These Terms will prevail over any conflict or ambiguity with regards to the relevant terms, a site licence or a personal subscription
(to the extent of the conflict or ambiguity only). For Creative Commons-licensed articles, the terms of the Creative Commons license used will
apply.
We collect and use personal data to provide access to the Springer Nature journal content. We may also use these personal data internally within
ResearchGate and Springer Nature and as agreed share it, in an anonymised way, for purposes of tracking, analysis and reporting. We will not
otherwise disclose your personal data outside the ResearchGate or the Springer Nature group of companies unless we have your permission as
detailed in the Privacy Policy.
While Users may use the Springer Nature journal content for small scale, personal non-commercial use, it is important to note that Users may
not:
use such content for the purpose of providing other users with access on a regular or large scale basis or as a means to circumvent access
control;
use such content where to do so would be considered a criminal or statutory offence in any jurisdiction, or gives rise to civil liability, or is
otherwise unlawful;
falsely or misleadingly imply or suggest endorsement, approval , sponsorship, or association unless explicitly agreed to by Springer Nature in
writing;
use bots or other automated methods to access the content or redirect messages
override any security feature or exclusionary protocol; or
share the content in order to create substitute for Springer Nature products or services or a systematic database of Springer Nature journal
content.
In line with the restriction against commercial use, Springer Nature does not permit the creation of a product or service that creates revenue,
royalties, rent or income from our content or its inclusion as part of a paid for service or for other commercial gain. Springer Nature journal
content cannot be used for inter-library loans and librarians may not upload Springer Nature journal content on a large scale into their, or any
other, institutional repository.
These terms of use are reviewed regularly and may be amended at any time. Springer Nature is not obligated to publish any information or
content on this website and may remove it or features or functionality at our sole discretion, at any time with or without notice. Springer Nature
may revoke this licence to you at any time and remove access to any copies of the Springer Nature journal content which have been saved.
To the fullest extent permitted by law, Springer Nature makes no warranties, representations or guarantees to Users, either express or implied
with respect to the Springer nature journal content and all parties disclaim and waive any implied warranties or warranties imposed by law,
including merchantability or fitness for any particular purpose.
Please note that these rights do not automatically extend to content, data or other material published by Springer Nature that may be licensed
from third parties.
If you would like to use or distribute our Springer Nature journal content to a wider audience or on a regular basis or in any other manner not
expressly permitted by these Terms, please contact Springer Nature at
onlineservice@springernature.com