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Basal tolerance but not plasticity gives invasive springtails the advantage in an assemblage setting

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Basal tolerance but not plasticity gives invasive springtails the advantage in an assemblage setting

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As global climates change, alien species are anticipated to have a growing advantage relative to their indigenous counterparts, mediated through consistent trait differences between the groups. These insights have largely been developed based on interspecific comparisons using multiple species examined from different locations. Whether such consistent physiological trait differences are present within assemblages is not well understood, especially for animals. Yet, it is at the assemblage level that interactions play out. Here, we examine whether physiological trait differences observed at the interspecific level are also applicable to assemblages. We focus on the Collembola, an important component of the soil fauna characterized by invasions globally, and five traits related to fitness: critical thermal maximum, minimum and range, desiccation resistance and egg development rate. We test the predictions that the alien component of a local assemblage has greater basal physiological tolerances or higher rates, and more pronounced phenotypic plasticity than the indigenous component. Basal critical thermal maximum, thermal tolerance range, desiccation resistance, optimum temperature for egg development, the rate of development at that optimum and the upper temperature limiting egg hatching success are all significantly higher, on average, for the alien than the indigenous components of the assemblage. Outcomes for critical thermal minimum are variable. No significant differences in phenotypic plasticity exist between the alien and indigenous components of the assemblage. These results are consistent with previous interspecific studies investigating basal thermal tolerance limits and development rates and their phenotypic plasticity, in arthropods, but are inconsistent with results from previous work on desiccation resistance. Thus, for the Collembola, the anticipated advantage of alien over indigenous species under warming and drying is likely to be manifest in local assemblages, globally.
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Volume 8 • 2020 10.1093/conphys/coaa049
Research article
Basal tolerance but not plasticity gives invasive
springtails the advantage in an assemblage
setting
Laura M. Phillips1, Ian Aitkenhead1, Charlene Janion-Scheepers2,3, Catherine K. King4, Melodie A. McGeoch1,
Ue N. Nielsen5,AleksTerauds
4,W.P.AmyLiu
1and Steven L. Chown1,*
1School of Biological Sciences, Monash University, Victoria 3800, Australia
2Iziko South African Museum, Cape Town 8001, South Africa
3Department of Biological Sciences, University of Cape Town, Rondebosch, Cape Town 7700, South Africa
4Australian Antarctic Division, Department of Agriculture, Water and the Environment, 203 Channel Highway, Kingston, Tasmania 7050, Australia
5Hawkesbury Institute for the Environment, Western Sydney University, Locked Bag 1797, Penrith, New South Wales, 2751, Australia
*Corresponding author: School of Biological Sciences, Monash University, Victoria 3800, Australia. Tel: +61 3 99050097.
Email: steven.chown@monash.edu
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As global climates change, alien species are anticipated to havea growing advantage relative to their indigenous counterparts,
mediated through consistent trait dierences between the groups. These insights have largely been developed based on
interspecic comparisons using multiple species examined from dierent locations. Whether such consistent physiological
trait dierences are present within assemblages is not well understood, especially for animals. Yet, it is at the assemblage
level that interactions play out. Here, we examine whether physiological trait dierences observed at the interspecic level
are also applicable to assemblages. We focus on the Collembola, an important component of the soil fauna characterized by
invasions globally, and ve traits related to tness: critical thermal maximum, minimum and range, desiccation resistance
and egg development rate. We test the predictions that the alien component of a local assemblage has greater basal
physiological tolerances or higher rates, and more pronounced phenotypic plasticity than the indigenous component. Basal
critical thermal maximum, thermal tolerance range, desiccation resistance, optimum temperature for egg development, the
rate of development at that optimum and the upper temperature limiting egg hatching success are all signicantly higher, on
average, for the alien than the indigenous componentsof the assemblage. Outcomes for critical thermal minimum are variable.
No signicant dierences in phenotypic plasticity exist between the alien and indigenous components of the assemblage.
These results are consistent with previous interspecic studies investigating basal thermal tolerance limits and development
rates and their phenotypic plasticity, in arthropods, but are inconsistent with results from previous work on desiccation
resistance. Thus, for the Collembola, the anticipated advantage of alien over indigenous species under warming and drying is
likely to be manifest in local assemblages, globally.
Key words: Biological invasions, climate change, CTmax,CTmin, growth, water balance
Editor: Nann Fangue
Received 9 January 2020; Revised 3 April 2020; Editorial Decision 4 May 2020; Accepted 11 May 2020
Cite as: Phillips LM, Aitkenhead I, Janion-Scheepers C, King CK,McGeoch MA, Nielsen UN, Terauds A, Liu1 WPA,Chown SL (2020) Basal tolerance but
not plasticity gives invasive springtails the advantage in an assemblage setting. Conserv Physiol 8(1): coaa049; doi:10.1093/conphys/coaa049.
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Research article Conservation Physiology Volume 8 2020
Introduction
Although assemblages lie within a metacommunity setting,
their dynamics are significantly mediated by the physical envi-
ronments they encounter and by interactions among species.
Because physiological traits modulate the effects of the envi-
ronment on populations (Helmuth et al., 2005), knowing the
range of trait variation for local assemblages, or significant
components of them, can provide much insight into assem-
blage structure and dynamics (Albert et al., 2012;Leibold
and Chase, 2018). The development of such understanding
is especially important given the growing need to understand
the mechanistic basis of a globally common pattern of high
local turnover through time without large changes in the
richness of assemblages (Blowes et al., 2019). Whether such
dynamics into the future will include the rising dominance
of assemblages by alien species, owing to the expectation
that changing climates will generally benefit them (Hulme,
2017), is of much interest given the economic and conserva-
tion significance of biological invasions. Such invasions are
among the most significant conservation concerns globally
(McGeoch and Jetz, 2019).
Assessments of trait variation for significant proportions
of the species in local assemblages are uncommon for animals
(Chown and Gaston, 2016). Rather, the species compared are
typically selected from different localities. Where assemblage
investigations have been undertaken, the outcomes can be
quite different to those involving interspecific comparisons
(compare, for example, Diamond et al., 2012 with Kaspari
et al., 2015). Hence, the general macroecological insight that
interspecific and assemblage-level investigations are different
and may provide complementary or even contrary insights
(Chown and Gaston, 2016).
For plants, explorations of the extent to which indige-
nous and alien species differ in their characteristics at the
assemblage level are increasing (e.g. van Kleunen et al., 2018;
Mathakutha et al., 2019;Sandel and Low, 2019). These
comparisons explicitly test the ‘ideal weed’ and ‘plasticity’
hypotheses, proposing that invasion success of a non-native
species depends on its specific traits or enhanced phenotypic
plasticity, respectively (Enders et al., 2020). By contrast, stud-
ies exploring whether the indigenous versus alien components
of assemblages vary consistently in one or more physiological
traits remain rare for animals. Most of the work on trait differ-
ences between indigenous and alien species is based on inter-
specific studies from animals collected across a wide range
of localities (e.g. Moyle et al., 2013;Bradie and Leung, 2015;
Jaroˇsík et al., 2015;Allen et al., 2017;Janion-Scheepers et al.,
2018) or for only a small component of a local assemblage
(Stachowicz et al., 2002;Chown et al., 2007). These studies
do not consider a range of species from a local setting. Yet,
they are frequently used as a basis to forecast rising success of
alien species under changing climates (e.g. Janion-Scheepers
et al., 2018). Indeed, because of the availability of the data,
interspecific comparisons remain among the most common
macrophysiological approaches adopted. Thus, insights into
whether assemblages might be dominated by alien species as
climates continue to change, and what mechanisms might lie
at the heart thereof, may at best be incomplete and at worst
inaccurate. In consequence, much need exists to determine
whether predictions made from interspecific studies are borne
out at the assemblage level.
Here, we therefore examine the extent to which empirical
outcomes from interspecific studies of the trait differences
among indigenous and invasive animal species, i.e. tests of
the ideal weed and plasticity hypotheses (Enders et al., 2020),
are borne out by a comprehensive investigation of a local
assemblage. We use Collembola as a model group. Springtails
are important in belowground systems and mediate above-
ground ecological outcomes (Bardgett and van der Putten,
2014). Understanding of physiological trait diversity in the
group is growing rapidly (Van Dooremalen et al., 2013;Ellers
et al., 2018;Jensen et al., 2019). How this diversity might be
partitioned among indigenous and invasive species has been
the subject of recent attention at the interspecific level (Jan-
ion-Scheepers et al., 2018). Recent work has been spurred by
concerns over the extent of soil invasions globally, including
among Collembola, and by suggestions that anthropogenic
change will exacerbate the impacts of invaders on soil systems
(Cicconardi et al., 2017;Coyle et al., 2017;Geisen et al.,
2019).
We consider five physiological traits that have significant
influences on fitness and are therefore frequently incorpo-
rated into models of the likely impacts of environmental
change on organisms. These are critical thermal minimum
and maximum (and the derived trait of tolerance range),
desiccation resistance and egg development rate (Birkemoe
and Leinaas, 2000;Kearney et al., 2013;Sinclair et al., 2016;
Rozen-Rechels et al., 2019). The assemblage is that of sub-
Antarctic Macquarie Island. We use this particular springtail
assemblage because it is well surveyed both in terms of the
species present and their abundances, is characterized by a
range of alien species and is representative with regard to
Collembola invasions of several islands globally (Cicconardi
et al., 2017;Baird et al., 2019). Moreover, because it is an
island assemblage, local factors are likely to be more impor-
tant in determining dynamics than regional biotic influences
(Leibold and Chase, 2018). The general climate of Mac-
quarie Island and its change over the past 40 years are also
relatively well understood (Adams, 2009;Bergstrom et al.,
2015).
Specifically, we test two predictions based on general
expectations (Daehler, 2003;Davidson et al., 2011;Hulme,
2017;Enders et al., 2020) and previous work on springtails
(Chown et al., 2007;Janion et al., 2010;Janion-Scheepers
et al., 2018). Compared with their indigenous counterparts,
alien species should have (Prediction 1) greater basal
physiological tolerances (for their definition see Chown and
Nicolson, 2004) as suggested by the ideal weed hypothesis
and (Prediction 2) more pronounced phenotypic plasticity as
suggested from the phenotypic plasticity hypothesis.
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Conservation Physiology Volume 8 2020 Research article
Materials and methods
Site description and species sampling
Collembola were collected from Macquarie Island (5430’ S,
15857’ E) in March/April of 2016 and 2017 (Supplementary
Table S1). The island is small (12 800 ha) with a cool (mean
air temperature range 3.8C to 6.6C), wet (954 mm annual
precipitation) and windy oceanic climate; vegetation varies
from coastal tussock to higher elevation fellfield areas (Selkirk
et al., 1990).
Springtail collection involved beating into a tray and aspi-
rating individuals from a variety of vegetation types and from
the soil surface into 70 ml plastic pots with a saturated Plaster-
of-Paris and charcoal powder base (9:1 mixture) (hereafter
lined plastic pots). Vegetation from the collection site was
placed in to the pots as a food source. Initial sorting into
additional lined plastic pots in the laboratory at Macquarie
Island was undertaken to initially separate species and ensures
densities of 75–100 animals per pot. Food sources were also
placed into these new pots. Turf samples (10 cm2surface area,
5 cm deep) were also collected to ensure that springtails from
all layers of soil were included. Springtails in pots and turf
samples were maintained at 5C and on a 12:12 light:dark
(L:D) cycle during the 2-week transportation back to the
laboratory in Melbourne. Here, springtails were extracted
from turf samples into lined plastic pots over 3 weeks using
Berlese–Tullgren funnels.
Springtails were identified using current available keys
for Macquarie Island Collembola (e.g. Greenslade, 2006)
[further verified with DNA barcoding (see Supplementary
Table S2)] and sorted into species. DNA barcoding, involving
the extraction and sequencing of 658 bp of the mitochondrial
cytochrome oxidase subunit I gene (COI) was undertaken by
the Canadian Centre for DNA Barcoding (CCDB, http://www.
ccdb.ca/) at the Centre for Biodiversity Genomics, University
of Guelph, Canada through the Barcode of Life Data Sys-
tems (BOLD, http://www.boldsystems.org/;Ratnasingham and
Hebert, 2007) (see also Janion-Scheepers et al., 2018). A total
of 91 individuals from 16 species was sequenced, with a
minimum of three individuals for any one species (Supple-
mentary Table S2). These sequences are available at the BOLD
(www.boldsystems.org) under the larger project ‘sub-Antarctic
Collembola’. Species were classified as either indigenous to
the island or introduced by human activity (alien) based on
previously published information (Greenslade, 2006;Phillips
et al., 2017). Most of the alien species are widespread on the
island and hence considered invasive (Terauds et al., 2011;
Phillips et al., 2017).
Colony maintenance
Springtail colonies were maintained in a controlled temper-
ature room at 10C ([10.15 ±0.23C], verified with iButton
Hygrochron®data loggers, Maxim Integrated, San Jose,USA)
on a 12:12 L:D cycle. Individuals were maintained by species
at intermediate density (75–100 individuals) in 70 ml lined
plastic pots to maintain a humid environment (>99% relative
humidity). They were fed weekly on a diet of Platanus sp. bark
(Hoskins et al., 2015) to allow for self-selection of nutrients,
with the bark also providing some shelter for individuals.
Pots were randomly re-arranged in the controlled temperature
room during feeding and during experiments to minimize
shelf effects.
For experiments measuring thermal and desiccation resis-
tance, springtails were assessed at the F0 and the F2 gen-
erations. F0 springtails were used to ensure that as much
information on the assemblage could be captured as possible,
including springtail species that we failed to rear successfully
under laboratory conditions. The F2 generations of springtails
were examined to ensure that carry-over effects from the
environment of collection, including parental effects, were
minimized while also minimizing adaptation to laboratory
conditions (Hoffmann and Sgrò, 2017). For investigations of
egg development rate, only the F2 generation was used. Eggs
were removed weekly from parental pots (F0 individuals) and
transferred to new pots to establish the F1 generation. The
same process was then used to generate the F2 generation
from F1 parents (following Janion-Scheepers et al., 2018). In
each case, eggs from multiple adults were randomly combined
within generations to maintain genetic diversity. F2 springtails
reached adulthood between 5 and 16 months after field
caught (F0) springtails entered the laboratory.
Critical thermal limits
Critical thermal limits provide a proxy for survival in active
adult organisms (Lutterschmidt and Hutchinson, 1997),
including in springtails (e.g. Everatt et al., 2013). The
critical thermal maxima (CTmax) and critical thermal minima
(CTmin) were determined for 16 species of springtails at F0
(9 alien, 7 indigenous, Supplementary Table S3), after they
had been held at 10C for 1 week to examine differences
in basal thermal tolerance between the indigenous and alien
groups (Prediction 1). At the F2 generation, 10 species were
investigated (7 alien, 3 indigenous, Supplementary Table S3).
These F2 species were also examined for adult (short-
term, non-developmental) plasticity in critical thermal limits
(Prediction 2). Adult phenotypic plasticity was assessed
by acclimating F2 springtails to one of five temperature
treatments for 7 days prior to experimentation (Supplemen-
tary Table S4). Three stable and two variable temperature
acclimations were used. Much interest exists in understanding
the extent to which fluctuating versus constant temperatures
may alter estimates of phenotypic plasticity (Colinet et al.,
2015). Recently, the importance of the influence of extreme
temperature events on the evolution of thermal tolerance has
been further emphasized, with the idea that extreme events
disproportionately drive changes in such traits (Hoffmann,
2010;Kingsolver and Buckley, 2017). Stable temperatures
were set at 5C, 10C and 15C, and variable temperatures
were set at 10C with either a high (25C) or a low (5C)
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Research article Conservation Physiology Volume 8 2020
extreme temperature spike that occurred for 1 h each day,
with a 30-min temperature ramp up/down either side of the
temperature extreme. The temperature spikes were based on
extreme event temperatures from a long-term soil surface
temperature record for the island (Leihy et al., 2018). Accli-
mation treatments were completed in controlled temperature
cabinets (MIR-154-PE, Panasonic, Osaka, Japan) and rooms.
Adults were held at the acclimation temperatures for 1 week
(following Janion-Scheepers et al., 2018;Jensen et al., 2019).
Critical thermal limits were determined for individual
adult springtails using established protocols (Janion-Scheep-
ers et al., 2018). Springtails were contained within custom-
built thermal stages (Monash University Instrument Facility,
Clayton Campus, VIC, Australia) that were heated or
cooled with programmable water baths (Grant Instruments,
Cambridge model TXF200) at 0.05C per minute. This rate
was chosen for its environmental relevance, reflecting a
commonly encountered rate of temperature change under
microclimatic conditions (Allen et al., 2016). The f loor
of the stage was lined with saturated Plaster-of-Paris to
minimize desiccation of springtails during experiments, and
temperature of the stage floor was recorded using Omega
thermometers (model: RDXL 12SD, Omega Engineering,
Norwalk, USA) with type K thermocouples. A starting
temperature of 10C (rearing temperature) was used for all
experiments. Springtails were observed every 5C until a
behavioural change occurred (e.g. moving faster/slower) after
which they were monitored every 1C and then every 0.5C
after the CTmax/CTmin was reached for the first individual
in the experiment. CTmax and CTmin were defined as the
temperature at which a loss of righting response occurred
for each individual (Everatt et al., 2013;Janion-Scheepers
et al., 2018). Different sets of individuals were used for the
CTmax and CTmin experiments. Three replicates, typically of
10–15 individuals, were completed per species per treatment
(sample sizes in Supplementary Table S3). Because variation
in critical thermal limits may be affected by differences in
body mass (Ribeiro et al., 2012), a mean body mass for each
species was determined by weighing a random sample of
50 adult individuals of each species using a high-resolution
(0.1 μg) microbalance (Mettler-Toledo XP2U, Switzerland)
(Supplementary Table S5).
Desiccation resistance
Desiccation resistance was determined for 10 species of
springtails at the F0 generation (5 alien, 5 indigenous,
Supplementary Table S3) to examine differences in absolute
desiccation resistance between alien and indigenous species
(Prediction 1). In the F2 generation, 8 species were used (6
alien, 2 indigenous, Supplementary Table S3) to investigate
plasticity in desiccation resistance in a cross-tolerance
framework with temperature (Prediction 2). Short-term
temperature acclimation has previously been shown to alter
desiccation resistance in indigenous and alien springtails
unequally, to the alien species’ advantage (Chown et al.,
2007). Here, the effects of short-term temperature acclima-
tions on desiccation resistance were examined at two acclima-
tion and two test temperatures. F2 springtails were acclimated
at either 10Cor20
C in controlled temperature rooms for
7 days prior to the desiccation experiment that was conducted
at either 10Cor20
C.
An experimental protocol for desiccation resistance, mea-
sured as survival time at 76% relative humidity, was estab-
lished based on previous methods (Kærsgaard et al., 2004;
Chown et al., 2007). Individual springtails were contained
within glass vials covered with fine mesh, which were then
housed in sealed, 70 ml plastic pots containing 15 ml of
saturated NaCl solution as a desiccant. Saturated NaCl was
used as it provides a consistent relative humidity of 76%
from 0Cto20
C. Furthermore, it has been shown that
springtails can survive between 1 and 24 h at this humidity
(Chown et al., 2007). Each pot contained two glass vials
with 5 springtails per vial and an iButton Hygrochron®
data logger (Maxim Integrated, San Jose, USA) to verify tem-
perature and relative humidity. Throughout the experiment,
conducted in controlled-temperature rooms, springtails were
examined every 10 min under a Leica M80 microscope (Leica
Microsystems Pty Ltd, Wetzlar, Germany), and time to death
(minutes) was recorded for each individual. Typically, four
replicates of 10 individuals were used per experiment, with
some exceptions for F0 experiments due to low numbers of
springtails available (see Supplementary Table S3 for sample
sizes). Following the experiment, springtails were dried at
40C for 24 h and then weighed in groups by replicate
using a high-resolution (0.1 μg) microbalance (Mettler-Toledo
XP2U, Switzerland) to obtain an estimate of individual dry
body mass.
Egg development and hatching success
Egg development time and hatching success were determined
for eight species, including six alien and two indigenous
species (Supplementary Table S3), at seven temperatures
ranging from 0C–30C, in 5C increments (Supplementary
Table S4)(Predictions 1 and 2) following previous protocols
(Birkemoe and Leinaas, 2000;Janion et al., 2010). Eggs
laid by F2 adults at 10C were collected and transferred
to each respective development temperature within 24 h of
laying. Eggs were transferred to 70 ml lined pots and kept in
controlled temperature cabinets (MIR-154-PE, Panasonic) or
rooms for the duration of development. Five replicate pots
per temperature with 10 eggs per pot were used to provide
a sample size of 50 eggs per temperature for each species.
Eggs were checked daily for hatching. Days to hatching for
each egg, and hatching success, measured as a percentage
of eggs hatched within each pot, were recorded. Eggs were
classified as unviable/dead if they were either visibly dead
(shrivelled, dissolved or extremely discoloured) or if they had
not hatched within 10 days (at 10C–30C) or within 14 days
of the previously hatched egg within the same pot (at 0C
and 5C).
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Conservation Physiology Volume 8 2020 Research article
Statistical analyses
All analyses were undertaken using R v. 3.5.2 (R Core Team,
2018) implemented in R Studio v. 1.1.463. All code and data
files are archived in the Monash Figshare repository (doi:
10.26180/5e17b874b125c and doi: 10.26180/5e17c3bc55197).
Critical thermal limits
To test Prediction 1, basal critical thermal limit differences
(CTmax,CTmin ,CTrange [difference between species mean
CTmax and mean CTmin]) among alien and indigenous species
at the F0 generation (10C acclimation) were assessed using
two approaches. The first explored differences in CTmax and
CTmin among individuals from the two groups excluding
species identity, assuming that individual trait variation is
important in a community dynamics context (Albert et al.,
2012), using a linear model with status as a fixed factor.
Because individuals were not weighed, mass was not included
as a covariate. Differences between the alien and indigenous
groups were then assessed using species means (or differences
in means for CTrang e ) within a phylogenetically explicit frame-
work using phylogenetic generalized least squares (PGLSs)
(Garland and Ives, 2000), as implemented in the caper v.0.5.2
package (Orme et al., 2013), including species mean mass
as a covariate. Given small numbers of species, a Brownian
motion model of evolution was used (Cooper et al., 2016) and
a maximum likelihood approach estimated Pagel’s λ(Pagel,
1999) to indicate the degree of phylogenetic influence in the
data. The phylogenetic tree used for the analyses was based
on Janion-Scheepers et al. (2018) and with mtCOI data used
to infer species relationships. For the final tree, branch lengths
were assigned using Grafen’s method (Grafen, 1989), and the
tree (Supplementary Figure S1) is available as a Newick file
in the Monash Figshare repository (doi: 10.26180/5e17b874
b125c). Density plots made using the package ggplot2 were
used to illustrate the range of variation in CTmax and CTmin
for each species and across individuals in the full assemblage
investigated.
Because differences in traits among F0 and F2 adults might
arise for various reasons (Hoffmann and Sgrò, 2017), means
of the critical thermal limit traits in the F0 and F2 generations,
each acclimated for 1 week at 10C, were compared among
the 10 species common to both sets of trials. A PGLS approach
using a reduced tree was initially used. Because Pagel’s λ
was estimated as zero for CTmax,CTmin and CTrange and
because of the likely measurement variation of the traits,
a ranged major axis model (RMA, Legendre and Legendre,
2012), implemented in the lmodel2 package, was used for
each trait to determine whether the slope differed from 1 and
the intercept from zero in each case by examining the 95%
confidence intervals of the estimated values.
To test Prediction 2, the effects of acclimation to 5C, 10C
and 15C were examined for the F2 CTmax and CTmin trials
by calculating an acclimation response ratio (ARR) (C/C)
(Gunderson and Stillman, 2015). The ARR was calculated
from the slope of the intraspecific relationship between accli-
mation temperature and critical thermal limits trait for each of
the 10 species investigated based on individual data for each
acclimation temperature. Systematic differences between the
indigenous and alien species were investigated using a PGLS
approach as above.
The impacts of a high (25C) or low (5C) temperature
spike for1honadaily basis as an extreme event acclimation
treatment were compared for each of the 10 species using
linear models with temperature as a fixed factor and Tukey’s
honest significant difference (Crawley, 2013).
Desiccation resistance
Desiccation resistance was measured as individual survival
time resulting in data that are bounded to the left at zero and
right skewed (Supplementary Figure S2). To assess whether
time to death differed between the F0 and F2 generations,
five species for which F0 and F2 data were available at
both acclimation and test temperatures of 10C were each
compared using a generalized linear model (GLM) assuming
a quasipoisson distribution and a log link function because
of the form of the data (O’Hara and Kotze, 2010). Because
substantial differences between the F0 and F2 generations
were found in one of the species, data from the F0 and F2
generations were not pooled for comparisons among indige-
nous and alien species, even though the two data series did
not overlap completely in the available species.
To test Prediction 1, comparisons of the indigenous and
alien species were made in two ways using the F0 data, in
keeping with the previous approach. In the first, a GLM
(assuming a quasipoisson distribution and a log link function)
was used to compare the alien and indigenous assemblages
(fixed factor), including an estimate of log10 dry body mass
for each individual (from the individuals weighed at the end
of the study) as a covariate. Thereafter, differences between
the alien and indigenous groups were assessed using species
means (here log10 of time to death to account for the skew
in the data) using PGLS as described above, including species
log10 mean dry mass as a covariate.
To test Prediction 2, the effects of thermal acclimation
(fixed factor) on desiccation resistance were analysed for
each species separately using a GLM assuming a quasipoisson
distribution and a log link function. Acclimation at higher
temperatures was expected to afford an extended survival
time to the alien but not the indigenous species (Chown et al.,
2007). Patterns of acclimation were compared visually for
each of the groups and then status (alien or indigenous)
included in a model (as above) with all species.
Egg development and hatching success
Egg development times for individuals of each species at
each temperature were converted to development rates
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Research article Conservation Physiology Volume 8 2020
Tab le 1: Means and standard deviations for critical thermal limits at the assemblage level, including linear model
comparison outcomes and species-level means, standard deviations and ranges for ARRs
Assemblage level critical thermal limits
Indigenous Alien Linear model outcomes
Mean ±SD Mean ±SD Fdf P
CTmax (C) 31.9 ±2.0 36.1 ±2.6 397.3 1512 <0.0001
CTmin (C) 2.8 ±1.0 3.9 ±1.6 86.7 1528 <0.0001
Species critical thermal limit ARRs
Indigenous Alien
Mean ±SD (range) Mean ±SD (range)
ARR CTmax (C/C) 0.049 ±0.041 0.001 ±0.017
(0.0140.095) (0.0180.027)
ARR CTmin (C/C) 0.070 ±0.045 0.062 ±0.037
(0.0250.120) (0.0110.117)
Figure 1: Density plots of thermal tolerance in individuals. (A)CTmax
and (B)CTmin for the indigenous and alien assemblages of springtails
from Macquarie Island measured in the F0 generation after 7 days at
10C acclimation
(1/days to hatching). Because single individuals were not
examined across a range of temperatures (different eggs
were assessed at each temperature), a function-valued trait
approach (Gomulkiewicz et al., 2018) was not implemented.
Mean values for development rate were obtained for each
species at each temperature and plotted against temperature.
Maximum development rate (Umax) and the temperature
at which this rate was realized (Topt) were extracted from the
means data. Prediction 1 was tested by inspecting the curves
and selecting the appropriate mean values and temperatures,
following previous approaches which have sought not to fit
curves to the empirical data (Jaroˇsík et al., 2015;Sørensen
et al., 2018). Further to test Prediction 1, hatching success
(as a proportion) was plotted against rearing temperature.
This revealed that hatching success did not decline to zero
at the lowest temperatures investigated in all of the species.
Therefore, low temperature variation in hatching success was
not investigated. Rather only the high temperature at which
hatching success declined to 50% of the sample population,
known as the upper lethal temperature 50 (ULT50) was
estimated using a GLM assuming a binomial distribution and
using a logit link function, with ULT50 values calculated
from the fitted models using the mass package (Crawley,
2013).
To test Prediction 2, for each species the slope of the
relationship or the temperature sensitivity of development
was calculated in two ways. First, a linear model was used
to estimate the slope of the relationship between mean rate
(1/days to hatching) at a given temperature and that tem-
perature (C) for each species. Data above the optimum
temperature of the relationship [i.e. the temperature at maxi-
mum rate (see Sørensen et al., 2018)] were not used. Second,
following a range of previous approaches (e.g. Dell et al.,
2011), the natural logarithm of rate was plotted against 1/kT,
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Conservation Physiology Volume 8 2020 Research article
Tab le 2: Critical thermal limits for springtail species from Macquarie Island
Species nCTmax ±SD nCT min ±SD CTrange
Alien
C. denticulata 31 37.8 ±0.4 30 4.4 ±0.7 42.3
Desoria tigrina 34 32.0 ±0.5 35 2.8 ±0.6 34.8
H. purpurescens 31 36.1 ±0.3 31 4.5 ±0.7 40.6
H. viatica 42 38.3 ±0.5 51 5.7 ±1.2 44.0
Lepidocyrtus sp.nr. violaceus 30 37.8 ±0.7 31 3.6 ±0.9 41.4
Megalothorax nr. minimus 29 31.0 ±1.4 28 0.6 ±1.0 31.6
Parisotoma notabilis 31 36.2 ±0.4 30 3.7 ±0.5 39.9
Protaphorura mata 33 38.0 ±0.5 33 4.5 ±0.5 42.5
Proisotoma sp. 32 37.0 ±0.7 40 3.8 ±0.8 40.8
Indigenous
Folsomotoma punctata 35 30.5 ±1.2 35 2.5 ±0.4 33.0
Katianna banzarei 32 29.7 ±0.6 29 1.6 ±0.5 31.3
Lepidobrya mawsoni 28 31.4 ±1.1 33 2.1 ±0.8 33.5
Mucrosomia caeca 31 33.8 ±0.8 30 3.2 ±0.6 37.0
P. insularis 33 31.3 ±0.8 34 3.6 ±0.6 34.9
Sminthurinus cf. tuberculatus 31 35.3 ±1.0 30 3.7 ±0.9 38.9
Tullbergia bisetosa 31 31.4 ±1.1 30 2.7 ±1.2 34.1
CTmax: critical thermal maximum; CTmin : critical thermal minimum; CTrange : mean CTmax minus mean CTmin ; SD: standard deviation.
where k = Boltzmann’s constant (8.617105ev.K1) and T is
temperature in Kelvin.
A PGLS approach, as described previously, was imple-
mented to investigate differences between alien (six species)
and indigenous groups (two species) in each of these four
traits (slope, Umax,Topt, ULT50). Here, Pagel’s λwas always
estimated as zero. Because one of the alien species, Hypogas-
trura purpurescens, was found to be quite different to the
others with regards to these variables, linear models used to
assess differences between the alien and indigenous groups
excluded this species.
Results
Critical thermal limits
The alien assemblage had, on average, a higher CTmax and
lower CTmin than the indigenous assemblage (Table 1),
although the alien assemblage was bimodal for CTmax
(Fig. 1), largely owing to low values for Proisotoma sp.
(Supplementary Figure S3). The PGLS models, based on
species means (Table 2), revealed significant and substantial
differences among the alien and indigenous species in
CTmax (4.1C) and CTrang e (5.1C), but not in CTmin, with
substantial phylogenetic signal in CTmin only (Table 3).
Species mean mass was not a significant covariate for any
of the traits and was omitted in the final models.
The F0 and F2 generation data did not differ among
the 10 species as indicated by the slopes and intercepts of
the RMA regressions not being different from 1 and 0,
respectively, for CTmax (slope: 1.0, 95% C.I.s: 0.91 to 1.10;
intercept: 0.24, 95% C.I.s: 3.43 to 3.57), CTmin (slope: 0.87,
95% C.I.s: 0.51 to 1.47; intercept: 0.65, 95% C.I.s: 2.04
to 1.65) and CTrang e (slope: 0.98, 95% C.I.s: 0.82 to 1.17;
intercept: 1.21, 95% C.I.s: 6.12 to 7.40).
ARRs (in C/C) did not differ between the alien and
indigenous groups for CTmin, and only marginally so for
CTmax (Tables 1, 3). Thus, the ARR for these two traits is sim-
ilar for the two groups of species, though the ARR for CTmin
(0.065 ±0.038C/C) is significantly larger than the ARR
for CTmax (0.020 ±0.031C/C) (linear model F(1,18) = 8.29,
P= 0.01) (summary data in Supplementary Table S6).
The extreme event treatments of either a low (5C) or
high (25C) temperature spike for 1 h each day had limited
and variable effects across the species, especially compared
with either the constant 5C acclimation in the former case
and the constant 15C in the latter (Table 4;Supplementary
Figures S4 and S5).
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Research article Conservation Physiology Volume 8 2020
Tab le 3: Outcomes of the PGLSs analyses for assessment of dierences between the indigenous and alien species groups for the traits
investigated in this study. In each case, the dierence between the alien and indigenous species groups are shown [status (indigenous)], and the
full model statistics provided including a maximum likelihood estimate of Pagel’s λ(MLλ). ARR = acclimation response ratio
CT values Estimate ±S.E. tP
Thermal tolerance
CTmax
Intercept 36.02 ±0.80 44.92 <0.0001
Status (indigenous) 4.11 ±1.21 3.39 0.0045
F(1,14) = 11.47, R2= 0.41, ML λ= 0.00
CTmin
Intercept 3.42 ±0.71 4.60 0.0004
Status (indigenous) 0.84 ±0.45 1.87 0.083
F(1,14) = 3.49, R2= 0.14, ML λ= 0.75
CTrange
Intercept 39.76 ±1.15 34.47 <0.0001
Status (indigenous) 5.07 ±1.74 2.91 0.011
F(1,14) = 8.47, R2= 0.33, ML λ= 0.00
ARR CTmax
Intercept 0.0076 ±0.0097 0.784 0.456
Status (indigenous) 0.0410 ±0.0176 2.323 0.049
F(1,8) = 5.40, R2= 0.33, ML λ= 0.00
ARR CTmin
Intercept 0.0622 ±0.0151 4.105 0.003
Status (indigenous) 0.0080 ±0.0277 0.290 0.779
F(1,8) = 0.08, R2= 0.0, ML λ= 0.00
Desiccation
Log10 time to death
Intercept 2.265 ±0.154 14.686 <0.0001
Status (indigenous) 0.601 ±0.244 2.464 0.039
F(1,8) = 6.07, R2= 0.360, ML λ= 0.00
Development rate
Slope
Intercept 0.0049 ±0.0005 10.131 <0.0001
Status (indigenous) 0.0008 ±0.0010 0.863 0.422
F(1,6) = 0.774, R2= 0.0, ML λ= 0.00
Slope (eV)
Intercept 0.754 ±0.052 14.613 <0.0001
Status (indigenous) 0.140 ±0.103 1.360 0.223
F(1,6) = 1.850, R2= 0.108, ML λ= 0.00
(Continued)
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Tab le 3: Continued
CT values Estimate ±S.E. tP
Topt
Intercept 23.333 ±1.128 20.679 <0.0001
Status (indigenous) 5.833 ±2.257 2.585 0.041
F(1,6) = 6.682, R2= 0.448, ML λ= 0.00
Umax
Intercept 0.103 ±0.011 9.621 <0.0001
Status (indigenous) 0.040 ±0.021 1.878 0.109
F(1,6) = 3.527, R2= 0.265, ML λ= 0.00
Hatching success (ULT50)
Intercept 23.567 ±0.943 24.989 <0.0001
Status (indigenous) 5.617 ±1.886 2.978 0.025
F(1,6) = 8.867, R2= 0.529, ML λ= 0.00
CTmax: critical thermal maximum; CTmin : critical thermal minimum; CTrange : mean CTmax minus mean CTmin ;Topt: optimum temperature: Umax : development rate at the
optimum temperature; S.E.: standard error.
Desiccation resistance
In four of the five species for which data were available
for both F0 and F2, no differences in time to death were
found between the generations (GLM: Ceratophysella den-
ticulata t=0.788, P= 0.433; Protaphorura fimata t = 0.592,
P= 0.556; Mucrosomia caeca t=0.296, P= 0.768; Pariso-
toma insularis t = 0.363, P= 0.718), whereas in the fifth,
Proisotoma sp., the F2 generation had a substantially and
significantly longer time to death than the F0 generation (F0:
80 ±32 min (median = 80), F2: 99 ±28 min (median = 90);
t = 2.99, P= 0.005). Thus, for the remainder of the investiga-
tions, the F0 and F2 generations were analysed separately.
For the F0 generation and using individual data, large
and significant differences were found between the alien
and indigenous species in time to death [alien mean:
326 ±413 min (median: 140); indigenous mean: 115 ±112
(median 60)], including with dry mass as a covariate (Table 5;
Fig. 2). The PGLS models using species means also showed
significant and substantial differences among the alien and
indigenous species in time to death but with no phylogenetic
signal in the data (Tables 3, 6).
Acclimation treatments in the F2 generation revealed that,
as expected, time to death was shorter at the higher test tem-
peratures, but that pre-exposure to an acclimation of 20C
frequently resulted in improved desiccation resistance either
at 20C (three species) or at 10C (two species), although
in two species no effects of acclimation were found (Fig. 3;
Table 7). Similar responses were found among the alien and
in the indigenous species [e.g. in Fig. 3 compare Proisotoma
sp. (alien) with M. caeca (indigenous)], with the GLM sup-
porting this interpretation given no interactions among status,
acclimation and test temperatures ( Supplementary Table S7).
Egg development and hatching success
Despite considerable differences in the form of the devel-
opment rate–temperature curves among species (Fig. 4)in
the PGLS analyses only Topt differed between the alien and
indigenous groups, with indigenous species having the lower
value (Table 3). Excluding H. pupurescens, an outlier among
the alien species (Table 8), resulted in rate-temperature slopes
which still did not differ between the groups [slope: esti-
mate (indigenous) = 0.0013 ±0.0006, t = 2.34, P= 0.066;
slope eV: estimate (indigenous) = 0.138 ±0.116, t = 1.196,
P= 0.285]. Both Topt [estimate (indigenous) = 6.5 ±2.1,
t=3.047, P= 0.029] and Umax [estimate (indigenous)
=0.050 ±0.015, t = 3.304, P= 0.021] were, however, lo-
wer in the indigenous than in the alien species group.
In all of the species, hatching success had declined to zero
by 30C, the highest temperature investigated. On average,
the temperature at which hatching success had declined to
50% (ULT50) (Table 8), was significantly lower (by 5.7C)
for the indigenous than for the alien species (Table 3), with H.
purpurescens an outlier among the alien species.
Discussion
In this springtail assemblage from Macquarie Island, the out-
comes of the tests of the two predictions are clear. Prediction
1[from the ideal weed hypothesis (Enders et al., 2020)],
of greater basal physiological tolerance in the alien than in
the indigenous species, is supported. On average, CTmax is
higher, CTrange is broader, desiccation resistance is greater
and egg development Topt and Umax and the ULT50 for egg
hatching success are higher in the alien than in the indigenous
species. Only CTmin is indistinguishable between these two
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Research article Conservation Physiology Volume 8 2020
Tab le 4: Outcomes of a linear model examining the eects on CTmax and CTmin of week-long acclimation treatments of 5C, 10C, 15C, 1 h at
5C per day (with a background temperature of 10C) and 1 h per day at 25C (with a background temperature of 10C). The full model outcome
is shown, along with Tukey HSD contrasts for the 5C extreme vs. 5Candthe25
C extreme vs. 15C (for boxplots, see Supplementary Figs S4
and S5). The error values are standard error
Species CTmax
Alien 5Cextremevs.5
C25Cextremevs.15
CFull model statistics
C. denticulata 0.4 ±0.1C, t = 2.8, P= 0.050 0.2 ±0.1C, t = 1.4, P= 0.650 F(4,186) = 2.73, P= 0.030
H. purpurescens 0.1 ±0.1C, t = 1.4, P= 0.612 0.3±0.1C, t = 3.0, P= 0.026 F(4,180) = 7.20, P<0.0001
H. viatica 0.02 ±0.1C, t = 0.1, P= 1.0 0.1 ±0.1C, t = 1.3, P= 0.682 F(4,157) = 1.63, P= 0.168
L. nr. violaceus 0.4 ±0.1C, t = 2.9, P= 0.037 0.5 ±0.1C, t = 3.6, P= 0.003 F(4,156) = 18.68, P<0.0001
P. notabilis 0.1 ±0.1C, t = 1.6, P= 0.523 0.01 ±0.1C, t = 0.1, P= 1.0 F(4,185) = 0.62, P= 0.648
P. mata 0.3 ±0.1C, t = 2.9, P= 0.038 0.2 ±0.1C, t = 1.5, P= 0.540 F(4,186) = 5.49, P= 0.001
Proisotoma sp. 0.7 ±0.2C, t = 4.3, P<0.001 0.4 ±0.2C, t = 2.3, P= 0.158 F(4,192) = 10.52, P<0.0001
Indigenous
M. caeca 0.4 ±0.1C, t = 3.0, P= 0.026 0.3 ±0.1C, t = 2.3, P= 0.159 F(4,195) = 16.22, P<0.0001
P. insularis 0.2 ±0.1C, t = 1.5, P= 0.568 0.2 ±0.1C, t = 1.7, P= 0.450 F(4,154) = 5.83, P<0.001
T. bisetosa 0.3 ±0.2C, t = 1.3, P= 0.686 0.1 ±0.2C, t = 0.3, P= 0.998 F(4,154) = 1.67, P= 0.159
Species CTmin
Alien 5Cextremevs.5
C25Cextremevs.15
C
C. denticulata 0.3 ±0.2C, t = 1.3, P= 0.711 0.1 ±0.2C, t = 0.6, P= 0.972 F(4,176) = 5.65, P<0.001
H. purpurescens 0.02 ±0.2C, t = 0.1, P= 1.0 0.3 ±0.2C, t = 1.7, P= 0.469 F(4,173) = 0.84, P= 0.503
H. viatica 0.3 ±0.2C, t = 1.5, P= 0.576 0.3 ±0.2C, t = 1.6, P= 0.513 F(4,158) = 2.45, P= 0.048
L. nr. violaceus 0.4 ±0.1C, t = 2.6, P= 0.085 0.4 ±0.2C, t = 2.7, P= 0.059 F(4,155) = 17.83, P<0.0001
P. notabilis 0.6 ±0.1C, t = 5.6, P<0.0001 0.4 ±0.1C, t = 4.1, P<0.001 F(4,179) = 28.3, P<0.0001
P. mata 0.3 ±0.1C, t = 2.5, P= 0.104 0.4 ±0.1C, t = 3.0, P= 0.026 F(4,181) = 11.01, P<0.0001
Proisotoma sp. 0.1 ±0.1C, t = 1.2, p = 0.742 0.2 ±0.1C, t = 1.5, P= 0.582 F(4,196) = 6.21, P= 0.0001
Indigenous
M. caeca 0.7 ±0.1C, t = 5.6, P<0.0001 0.1 ±0.1C, t = 1.0, P= 0.847 F(4,190) = 25.36, P<0.0001
P. insularis 0.3 ±0.1C, t = 2.6, P= 0.089 0.2 ±0.1C, t = 1.3, P= 0.699 F(4,155) = 5.40, P<0.001
T. bisetosa 0.6 ±0.2C, t = 3.1, P= 0.020 0.1 ±0.2C, t = 0.5, P= 0.985 F(4,148) = 4.77, P= 0.001
groups at the species level. At the individual level, however,
the difference in CTmin between alien and indigenous species
is clear. By contrast, Prediction 2, of greater phenotypic
plasticity in the alien than in the indigenous species [from
the phenotypic plasticity hypothesis (Enders et al., 2020)] is
not supported. Acclimation responses for CTmax,CTmin and
desiccation resistance and the slopes of the rate-temperature
relationships for egg development do not differ between the
alien and indigenous species groups.
Differences in basal tolerance, but not in phenotypic plas-
ticity, of critical thermal limits specifically, are largely in
keeping with previous work. The most extensive interspe-
cific study to date (Janion-Scheepers et al., 2018) found
that indigenous springtail species are characterized by critical
thermal maxima that are on average 3C lower than those
Tab le 5: Outcome of a generalized linear model (quasipoisson
distribution, log link) comparing individual time to death following
desiccation among the alien and indigenous assemblages for the F0
generation trial
Estimate ±S.E. tP
Intercept 9.748 ±0.512 19.030 <0.0001
Status (indigenous) 0.892 ±0.136 6.537 <0.0001
Log10 dry mass 2.265 ±0.299 7.579 <0.0001
Residual deviance 63 376; df = 323; quasipoisson dispersion parameter = 236.2617
of their alien counterparts and a CTrang e difference of about
the same magnitude, with no difference in CTmin and ARR
between the groups. In this Macquarie Island assemblage,
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Conservation Physiology Volume 8 2020 Research article
Figure 2: Relationship between time to death (log10, minutes) and
dry body mass (log10, mg) for individuals of the F0 generation of
springtail species from Macquarie Island subject to desiccation trials,
indicating substantially greater desiccation resistance, on average, of
the alien over the indigenous species. The tted lines are from a
linear model tted in ggplot2
the differences in CTmax and CTrang e are slightly larger (4C
and 5C, respectively), but otherwise the findings accord
closely. Moreover, irrespective of the acclimation conditions,
we were unable to effect much change in the value of CTmax
in any of the species we investigated, reflected also by the low
ARR values for this trait. Longer-term laboratory selection
experiments have also been unable to do so in both alien and
indigenous springtail species (Janion-Scheepers et al., 2018).
These findings of limited plasticity and adaptability in
CTmax over the shorter term are in keeping with previous
investigations of other organisms (Hoffmann et al., 2013;
Gunderson and Stillman, 2015;MacLean et al., 2019).
Such similarity does not help to explain, however, why such
substantial interspecific variation exists in the basal CTmax
of springtails. Here, for example, the largest difference in
CTmax among species is 8.6C, whereas the largest difference
in CTmin is 5.1C. In the broad-scale interspecific study
(Janion-Scheepers et al., 2018), CTmax varied among species
by 11.6and CTmin by 13C, only slightly more. Variation
in basal CTmax that either exceeds or is similar to variation
in basal CTmin in springtails (see also Jensen et al., 2019 for
among-population variation) is different to findings for many
insects and for other terrestrial ectotherms generally, but not
unlike the situation found for marine ectotherms (Sunday
et al., 2011;Araújo et al., 2013). Clearly, some of this
difference must reside in the reasons for the evolution of
much higher CTmax in springtail species that succeed when
introduced outside their native range. One reason may be that
such species tend also to experience regular disturbances,
which might be associated with broader tolerance ranges
(Coyle et al., 2017). Another may be that variation in CTmax
at the assemblage level is much greater than interspecific
analyses tend to reveal (e.g. Kaspari et al., 2015;Kühsel and
Blüthgen, 2015), which would have substantial implications
for assessments of response to global climate change. Yet
a third might be that the introduced species all come from
regions, such as continental Europe, where thermal variation
is much greater and much more predictably so than for
the sub-Antarctic (Chown et al., 2004), resulting in greater
Tab le 6: Mean time to death under desiccating conditions of 76% humidity at 10C after acclimation for 1 week at 10C
for the springtail species investigated here. Data for the F0 generation are shown with the exception of two species
[marked (F2)]
Species nMean ±SD Median Range
Alien
C. denticulata 30 205 ±85 180 100380
Desoria tigrina 26 116 ±27 120 40160
H. purpurescens (F2) 40 1052 ±203 1005 6901420
H. viatica 36 1064 ±402 970 4201740
Lepidocyrtus sp. nr. violaceus 21 233 ±111 260 40410
Parisotoma notabilis (F2) 36 20 ±8 20 1040
P. mata 32 132 ±35 135 50190
Proisotoma sp. 38 80 ±32 80 30170
Indigenous
M. caeca 34 149 ±34 140 90220
P. insularis 23 24 ±9 20 1040
Sminthurinus cf. tuberculatus 30 285 ±103 255 150440
T. bisetosa 26 47 ±13 40 3070
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Research article Conservation Physiology Volume 8 2020
Figure 3: Boxplots illustrating the eects of dierent acclimation treatments [10C (black) or 20C (orange) for 1 week] on desiccation
resistance (provided here as log10 time to death in minutes) measured under 76% relative humidity at a test temperature of either 10Cor20
C.
Summary data are available in Supplementary Table S9
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Tab le 7: Outcomes of the generalized linear models (quasipoisson distribution, log link) estimating the eects of acclimation
and treatment temperature on time to death (as a measure of desiccation resistance) in each of the species examined in this study
Species Estimate ±S.E. tP
Alien
C. denticulata
Intercept 5.245 ±0.049 107.72 <0.0001
Acclimation (20) 0.371 ±0.064 5.812 <0.0001
Test temperature (20) 0.379 ±0.077 4.899 <0.0001
Acclimation: test 0.566 ±0.116 4.874 <0.0001
Residual deviance 3702.8; df = 171; quasipoisson dispersion parameter = 21.57
H. purpurescens
Intercept 6.958 ±0.029 241.82 <0.0001
Acclimation (20) 0.047 ±0.042 1.122 0.264
Test temperature (20) 1.211 ±0.061 19.964 <0.0001
Acclimation: test 0.330 ±0.082 4.020 <0.0001
Residual deviance 5442.4; df = 152; quasipoisson dispersion parameter = 34.82
Parisotoma notabilis
Intercept 2.996 ±0.064 46.94 <0.0001
Acclimation (20) 0.353 ±0.079 4.449 <0.0001
Test temperature (20) 0.553 ±0.102 5.414 <0.0001
Acclimation: test 0.393 ±0.140 2.803 0.006
Residual deviance 448.0; df = 156; quasipoisson dispersion parameter = 2.932
P. mata
Intercept 4.919 ±0.031 160.73 <0.0001
Acclimation (20) 0.002 ±0.043 0.040 0.968
Test temperature (20) 0.556 ±0.050 11.142 <0.0001
Acclimation: test 0.008 ±0.070 0.115 0.908
Residual deviance 754.9; df = 155; quasipoisson dispersion parameter = 4.87
Proisotoma sp.
Intercept 4.603 ±0.038 120.16 <0.0001
Acclimation (20) 0.036 ±0.053 0.681 0.497
Test temperature (20) 1.152 ±0.081 14.192 <0.0001
Acclimation: test 0.547 ±0.103 5.299 <0.0001
Residual deviance 1046.2; df = 165; quasipoisson dispersion parameter = 6.294
Indigenous
M. caeca
Intercept 4.985 ±0.035 144.55 <0.0001
Acclimation (20) 0.033 ±0.049 0.673 0.502
Test temperature (20) 1.303 ±0.078 16.78 <0.0001
Acclimation: test 0.757 ±0.097 7.796 <0.0001
Residual deviance 1168.7; df = 159; quasipoisson dispersion parameter = 7.30
(Continued)
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Research article Conservation Physiology Volume 8 2020
Tab le 7: Continued
Species Estimate ±S.E. tP
P. insularis
Intercept 3.209 ±0.056 57.27 <0.0001
Acclimation (20) 0.0001 ±0.0001 0.0 1.0
Test temperature (20) 0.253 ±0.085 2.957 0.004
Acclimation: test 0.002 ±0.121 0.097 0.923
Residual deviance 479.9; df =152; quasipoisson dispersion parameter = 3.107
physiological tolerance ranges than in the indigenous species.
This latter hypothesis requires further investigation with
information that enables the exact localities of origin of
the introduced species to be identified—information that is
slowly becoming available (e.g. Baird et al., 2020).
In the case of desiccation resistance, the variation found
among species in the time to death at 76% humidity is largely
consistent with findings from other species, often examined
under less extreme desiccating conditions (e.g. Kærsgaard
et al., 2004;Elnitsky et al., 2008;Sørensen and Holmstrup,
2011). That we found a positive effect of thermal acclimation
at 20C accords with the only previous investigation of such
cross-tolerance effects for springtails (Chown et al., 2007).
However, here, a similar effect for the indigenous M. caeca
and no effects for the indigenous P. insularis and the alien
P. fimata, differ from the outcomes of that work. There,
acclimation at 5C tended to improve performance of the
indigenous species at that temperature, whereas acclimation
to 15C generally reduced it, with little difference among
acclimation treatments at a 15C test temperature. By con-
trast, acclimation to 15C improved desiccation resistance
at both the 5C and 15C test temperatures. Here, no such
consistent differences among the indigenous and alien species
were found. Basal desiccation resistance (measured as survival
time) was on average, however, higher in the alien species,
contrary to the previous work that found no such differences
(Chown et al., 2007). Thus, differences in desiccation resis-
tance among indigenous and alien springtail species cannot
yet be generalized.
Intriguingly, despite the importance of water balance in
determining the activity and distribution of ectotherms, and
especially arthropods (Chown et al., 2011;Rozen-Rechels
et al., 2019), and forecasts for substantial changes in water
availability globally (Sarojini et al., 2016), few studies have
focussed on determining the extent of differences among
indigenous and alien species in traits related to water balance.
In mosquitoes, desiccation tolerant eggs are associated with
species that have become alien but not those that are invasive
(Juliano and Lounibos, 2005). By contrast, in freshwater
molluscs, the two groups of species do not differ in desiccation
resistance (Collas et al., 2014).
Figure 4: Mean egg development rate (1/days to hatching) between
0Cand30
C for each of the species investigated here (indigenous
species are M. caeca and P. insularis, the remainder are alien). Where
values are zero, this typically indicates no development or very low
hatching success with some development in the case of the values at
0C. Summary data in Supplementary Table S10
Variation in development rate parameters has been the
subject of two major studies contrasting indigenous and alien
species. In the first (Jaroˇsík et al., 2015), the sum of effective
temperatures [1/slope of the rate-temperature relationship,
SET)] and the lower development threshold (LDT) for insects
across either part of the life cycle, or the full cycle, were
compared among indigenous and invasive species. No signif-
icant differences were found for SET, but LDTs were lower
for the invasive species (Jaroˇsík et al., 2015). In the second
study, of seven springtail species (Janion et al., 2010), the
slopes of the rate-temperature relationships for egg develop-
ment rate did not differ, although on average development
rates were higher for the alien species, with lower hatching
success at the higher temperatures for the indigenous species.
Our results are largely consistent with these outcomes, so
extending the findings for assemblage-level assessments. We
found no significant differences between groups in the slope
of the egg development-rate temperature relationship but a
higher Topt, higher Umax (when excluding H. purpurescens)
and higher ULT50 in the indigenous compared with the
invasive species. Although we did not calculate LDT (simply:
-intercept/slope of the linear part of the rate-temperature
relationship—see Jaroˇsík et al., 2015), examination of the
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Conservation Physiology Volume 8 2020 Research article
Tab le 8: Performance curve statistics for egg development rate (1/days to hatching): slope of the linear part of the curve [estimate ±s.e. (n)], the
slope given as electron volts from the equation ln rate vs. 1/kT (eV), the temperature of the fastest rate recorded (Topt), the development rate at
that temperature (Umax) [mean ±SD (n)] and the upper temperature where hatching success declined to 50% (HS ULT50) in springtails from
Macquarie Island
Species Slope ±S.E. (n)eV Topt Umax ±SD HS ULT50 ±S.E.
Alien
C. denticulata 0.00595 ±0.00019 (5) 0.742 25 0.13266 ±0.01027 (36) 24.5 ±0.8
H. purpurescens 0.00266 ±0.00026 (5) 0.744 20 0.05716 ±0.00323 (31) 19.4 ±0.5
H. viatica 0.00530 ±0.00010 (3) 0.560 25 0.10304 ±0.00783 (45) 26.3 ±0.5
Parisotoma notabilis 0.00607 ±0.00027 (3) 0.721 25 0.13516 ±0.01454 (33) 25.0 ±0.5
P. mata 0.00445 ±0.00027 (5) 0.826 25 0.09641 ±0.00717 (42) 22.8 ±0.7
Proisotoma sp. 0.00549 ±0.00031 (4) 0.928 20 0.09441 ±0.00578 (46) 23.5 ±0.5
Indigenous
M. caeca 0.00359 ±0.00024 (4) 0.791 20 0.06440 ±0.00717 (34) 19.4 ±0.5
P. insularis 0.00468 ±0.00003 (3) 0.997 15 0.06135 ±0.00206 (44) 16.5 ±0.4
rate-temperature relationships and these values (Supplemen-
tary Table S8) suggests that no differences between the groups
are to be expected. Thus, the egg development work here
supports suggestions that the temperature sensitivity of devel-
opment, a form of phenotypic plasticity (Ghalambor et al.,
2007), does not differ between the two groups of species and
in magnitude is in keeping with the variation previously found
for arthropods (Irlich et al., 2009;Dell et al., 2011). Yet, it also
shows that alien species typically have increased capacity to
complete their development at higher temperatures and to do
so at faster rates than their indigenous counterparts.
The insights presented here on assemblage level variation
in traits among indigenous and alien species are necessary
to clarify (i) how interactions among species will play out
(Leibold and Chase, 2018) and (ii) how future changes to
systems because of either local disturbances (such as urban-
ization, see e.g. Diamond et al., 2017), or global climate
alterations (Sarojini et al., 2016), will differ from place to
place and therefore assemblage to assemblage, so affecting
indigenous-alien species interactions (Hulme, 2017). In this
regard, two caveats apply to our study.
First, although we were able to investigate the most abun-
dant species in the assemblage (see Terauds et al., 2011),
we were not able to investigate the entire assemblage. At
most, we included species representing 85% of the indigenous
and >95% of the alien assemblage by abundance (Terauds
et al., 2011). Nonetheless, the Macquarie Island assemblage
now consists of 22 indigenous and 12 alien springtail species.
That we found little difference between the F0 and F2 genera-
tions in critical thermal limits, and for most species also little
difference among generations in desiccation resistance, sug-
gests that examining recently captured individuals may not
be as significant a concern as has been suggested (Hoffmann
and Sgrò, 2017), especially when attempting to estimate the
full suite of assemblage traits. The importance of investigating
additional, and especially rare, species will depend on how
important they are in the structure and functioning of the sys-
tem in question, with evidence from other systems suggesting
that rare species can be important and should be considered
(Winfree et al., 2018;Dee et al., 2019).
Second, we did not differentiate between species that live
above ground, in the litter, or deeper in the soil or among
the major orders of springtails: the Symphypleona, Poduro-
morpha and Entomobryomorpha (Bellinger et al., 2019), as is
often done (Janion et al., 2010;Bokhorst et al., 2012;Ellers
et al., 2018). In part, we did not have sufficient species to
undertake a full factorial design to enable us to do so, though
the PGLS analyses mitigated these effects to some extent. We
also think, however, that consideration at the assemblage level
as a whole of how the distribution of individuals with differ-
ent trait values might play out into the future is important at
the local scale. Changes in response traits (Naeem and Wright,
2003) will take place through either differential survival or
differential reproduction of individuals, altering the overall
composition of the assemblage and its effects on ecosystem
structure and functioning. Such whole-of-assemblage consid-
erations of individuals from a trait perspective are becoming
more common (e.g. Salo et al., 2020). Theory (e.g. Albert
et al., 2012; Leibold and Chase, 2018) also suggests that they
require further consideration when the outcome of the inter-
actions between indigenous and alien species in a particular
assemblage, under expected conditions of change, is being
investigated.
Overall, our investigations have revealed that while basal
trait values differ on average between the indigenous and
alien species groups of Collembola, with the latter having the
advantage under higher temperatures and drier conditions,
phenotypic plasticity does not differ between them. These
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Research article Conservation Physiology Volume 8 2020
outcomes suggest that as local climates become warmer and,
in some places, drier with global change, the conservation
problems associated with biological invasions (McGeoch and
Jetz, 2019) will increase, especially in soils (Coyle et al., 2017).
Supplementary material
Supplementary material is available at Conservation Physiol-
ogy online.
Funding
This work was supported by Australian Antarctic Science
Grant [4307] and by Australian Research Council Discovery
Project [DP190100341].
Acknowledgments
Rebecca Hallas manages the laboratory in which most of this
work was done. The staff of the Australian Antarctic Division
provided support in the field at Macquarie Island and in
Australia. Jodie Weller and Gwen Fenton helped ensure the
success of this project in the face of a major setback. Col-
lections at Macquarie Island were made with the permission
of the Tasmanian Parks and Wildlife Service under collection
permits FA15328, FA17039 and FL16017. We thank M.
Potapov, W. Weiner and L. Deharveng for assistance with
species identifications and three anonymous reviewers for
their helpful comments.
References
Adams N (2009) Climate trends at Macquarie Island and expectations of
future change in the sub-Antarctic. PapProcRSocTasmania143: 18.
Albert CH, de Bello F, Boulangeat I, Pellet G, Lavorel S, Thuiller W (2012)
On the importance of intraspecic variability for the quantication
of functional diversity. Oikos 121: 116126.
Allen JL, Chown SL, Janion-Scheepers C, Clusella-Trullas S (2016) Inter-
actions between rates of temperature change and acclimation aect
latitudinal patterns of warming tolerance. Conserv Physiol 4: cow053.
Allen WL, Street SE, Capellini I (2017) Fast life history traits promote
invasion success in amphibians and reptiles. Ecol Lett 20: 222230.
Araújo MB, Ferri-Yáñez F, Bozinovic F, Marquet PA, Valladares F, Chown
SL (2013) Heat freezes niche evolution. Ecol Lett 16: 12061219.
Baird HP, Janion-Scheepers C, Stevens MI, Leihy RI, Chown SL (2019) The
ecological biogeography of indigenous and introduced Antarctic
springtails. JBiogeogr46: 19591973.
Baird HP, Moon KL, Janion-Scheepers C, Chown SL (2020) Springtail phy-
logeography highlights biosecurity risks of repeated invasions and
intraregional transfers among remote islands. Evol Appl 13: 960973.
doi: 10.1111/eva.12913.
Bardgett RD, van der Putten WH (2014) Belowground biodiversity and
ecosystem functioning. Nature 515: 505511.
Bellinger PF, Christiansen KA, Janssens F (2019) Checklist of the Collem-
bola of the World. http://www.collembola.org.
Bergstrom DM, Bricher PK, Raymond B, Terauds A, Doley D, McGeoch
MA,WhinamJ,GlenM,YuanZ,KieferKet al. (2015) Rapid collapse of
a sub-Antarctic alpine ecosystem: the role of climate and pathogens.
J Appl Ecol 52: 774783.
Birkemoe T, Leinaas HP (2000) Eects of temperature on the develop-
ment of an Arctic Collembola (Hypogastrura tullbergi). Funct Ecol 14:
693700.
Blowes SA, Supp SR, Antão LH, Bates AE, Bruelheide H, Chase JM, Moyes
F, Magurran AE, McGill BJ, Myers-Smith IH et al. (2019) The geography
of biodiversity change in marine and terrestrial assemblages. Science
366: 339345.
Bokhorst S, Phoenix GK, Bjerke JW, Callaghan TV, Huyer-Brugman
F, Berg MP (2012) Extreme winter warming events more nega-
tively impact small rather than large soil fauna: shift in commu-
nity composition explained by traits not taxa. Glob Chang Biol 18:
11521162.
Bradie J, Leung B (2015) Pathway-level models to predict non-
indigenous species establishment using propagule pressure, envi-
ronmental tolerance and trait data. J Appl Ecol 52: 100109.
Chown SL, Gaston KJ (2016) Macrophysiologyprogress and prospects.
Funct Ecol 30: 330344.
Chown SL, Slabber S, McGeoch MA, Janion C, Leinaas HP (2007) Pheno-
typic plasticity mediates climate change responses among invasive
and indigenous arthropods. Proc Biol Sci 274: 26612667.
Chown SL, Nicolson SW (2004) Insect Physiological Ecology. Mechanisms
and Patterns. Oxford University Press, Oxford.
Chown SL, Sinclair BJ, Leinaas HP, Gaston KJ (2004) Hemispheric asym-
metries in biodiversitya serious matter for ecology. PLoS Biol 2:
17011707.
Chown SL, Sørensen JG, Terblanche JS (2011) Water loss in insects: an
environmental change perspective. J Insect Physiol 57: 10701084.
Cicconardi F, Borges PAV, Strasberg D, Oromi P, Lopez H, Perez-Delgado
AJ, Casquet J, Caujape-Castells J, Fernandez-Palacios JM, Thebaud
Cet al. (2017) MtDNA metagenomics reveals large-scale invasion of
belowground arthropod communities by introduced species. Mol
Ecol 26: 31043115.
Colinet H, Sinclair BJ, Vernon P, Renault D (2015) Insects in uctuating
thermal environments. Annu Rev Entomol 60: 123140.
Collas FPL, Koopman KR, Hendriks AJ, van der Velde G, Verbrugge LNH,
Leuven RSEW (2014) Eects of desiccation on native and non-native
molluscs in rivers. Freshw Bi ol 59: 4155.
Cooper N, Thomas GH, Venditti C, Meade A, Freckleton RP (2016) A cau-
tionary note on the use of Ornstein Uhlenbeck models in macroevo-
lutionary studies. Biol J Linn Soc 118: 6477.
..........................................................................................................................................................
16
..........................................................................................................................................................
Conservation Physiology Volume 8 2020 Research article
Coyle DR, Nagendra UJ, Taylor MK, Campbell JH, Cunard CE, Joslin AH,
Mundepi A, Phillips CA, Callaham MA (2017) Soil fauna responses
to natural disturbances, invasive species, and global climate change:
current state of the science and a call to action. Soil Biol Biochem 110:
116133.
Crawley MJ (2013) The R Book. John Wiley & Sons, Chichester
Daehler CC (2003) Performance comparisons of co-occurring native and
alien invasive plants: implications for conservation and restoration.
Annu Rev Ecol Evol Syst 34: 183211.
Davidson AM, Jennions M, Nicotra AB (2011) Do invasive species show
higher phenotypic plasticity than native species and, if so, is it adap-
tive? A meta-analysis. Ecol Lett 14: 419431.
Dee LE, Cowles J, Isbell F, Pau S, Gaines SD, Reich PB (2019) When
do ecosystem services depend on rare species? Trends Ecol Evol 34:
746758.
Dell AI, Pawar S, Savage VM (2011) Systematic variation in the temper-
ature dependence of physiological and ecological traits. Proc Natl
Acad Sci U S A 108: 1059110596.
Diamond SE, Chick L, Perez A, Strickler SE, Martin RA (2017) Rapid
evolution of ant thermal tolerance across an urban-rural temperature
cline. BiolJLinnSoc121: 248257.
Diamond SE, Sorger DM, Hulcr J, Pelini SL, Toro ID, Hirsch C, Oberg E,
Dunn RR (2012) Who likes it hot? A global analysis of the climatic,
ecological, and evolutionary determinants of warming tolerance in
ants. Glob Chang Biol 18: 448456.
Ellers J, Berg MP, Dias ATC, Fontana S, Ooms A, Moretti M (2018) Diversity
in form and function: vertical distribution of soil fauna mediates
multidimensional trait variation. JAnimEcol 87: 933944.
Elnitsky MA, Benoit JB, Denlinger DL, Lee RE (2008) Desiccation tolerance
and drought acclimation in the Antarctic collembolan Cryptopygus
antarcticus.J Insect Physiol 54: 14321439.
Enders M, Haveman F, Ruland F, Bernard-Verdier M, Catford JA, Gómez-
Aparicio L, Haider S, Heger T, Kueer C, Kühn I et al. (2020) A concep-
tual map of invasion biology: integrating hypotheses into a consen-
sus network. Glob Ecol Biogeogr 29: 978991. doi: 10.1111/geb.13082.
Everatt MJ, Bale JS, Convey P, WorlandMR, Hay wardSA (2013) The eect
of acclimation temperature on thermal activity thresholds in polar
terrestrial invertebrates. J Insect Physiol 59: 10571064.
Garland T, Ives AR (2000) Using the past to predict the present: con-
dence intervals for regression equations in phylogenetic compara-
tive methods. Am Nat 155: 346364.
Geisen S, Wall DH, van der Putten WH (2019) Challenges and opportu-
nities for soil biodiversity in the Anthropocene. Curr Biol 29: R1036
R1044.
Ghalambor CK, McKay JK, Carroll SP, Reznick DN (2007) Adaptive versus
non-adaptive phenotypic plasticity and the potential for contempo-
rary adaptation in new environments. Funct Ecol 21: 394407.
Gomulkiewicz R, Kingsolver JG, Carter PA, Heckman N (2018) Variation
and evolution of function-valued traits. Annu Rev Ecol Evol Syst 49:
139164.
Grafen A (1989) The phylogenetic regression. Philos Trans R Soc B 326:
119157.
Greenslade P (2006) The Invertebrates of Macquarie Island. Australian
Antarctic Division, Kingston, Australia
Gunderson AR, Stillman JH (2015) Plasticity in thermal tolerance has
limited potential to buer ectotherms from global warming. Proc Biol
Sci 282: 20150401.
Helmuth B, Kingsolver JG, Carrington E (2005) Biophysics, physiological
ecology, and climate change: does mechanism matter? Annu Rev
Physiol 67: 177201.
Homann AA (2010) Physiological climatic limits in Drosophila:patterns
and implications. J Exp Biol 213: 870880.
Homann AA, Chown SL, Clusella-Trullas S (2013) Upper thermal limits
in terrestrial ectotherms: how constrained are they? Funct Ecol 27:
934949.
Homann AA, Sgrò CM (2017) Comparative studies of critical physio-
logical limits and vulnerability to environmental extremes in small
ectotherms: how much environmental control is needed? Integr Zool
13: 355371.
Hoskins JL, Janion-Scheepers C, Chown SL, Duy GA (2015) Growth
and reproduction of laboratory-reared neanurid Collembola using a
novel slime mould diet. Sci Rep 5: 11957.
Hulme PE (2017) Climate change and biological invasions: evidence,
expectations, and response options. Biol Rev 92: 12971313.
Irlich UM, Terblanche JS, Blackburn TM, Chown SL (2009) Insect
rate-temperature relationships: environmental variation and the
metabolic theory of ecology. Am Nat 174: 819835.
Janion C, Leinaas HP, Terblanche JS, Chown SL (2010) Trait means and
reaction norms: the consequences of climate change/invasion inter-
actions at the organism level. Evol Ecol 24: 13651380.
Janion-Scheepers C, Phillips L, Sgro CM, Duy GA, Hallas R, Chown
SL (2018) Basal resistance enhances warming tolerance of alien
over indigenous species across latitude. Proc Natl Acad Sci USA 115:
145150.
Jaroˇ
sík V, Kenis M, Honˇ
ek A, Skuhrovec J, Pyˇ
sek P (2015) Invasive insects
dier from non-invasive in their thermal requirements. PLoS One 10:
e0131072.
Jensen A, Alemu T, Alemneh T, Pertoldi C, Bahrndor S (2019) Ther-
mal acclimation and adaptation across populations in a broadly
distributed soil arthropod. Funct Ecol 33: 833845.
Juliano SA, Lounibos PL (2005) Ecology of invasive mosquitoes: eects
on resident species and on human health. Ecol Lett 8: 558574.
Kærsgaard CW, Holmstrup M, Malte H, Bayley M (2004) The importance
of cuticular permeability, osmolyte production and body size for the
desiccation resistance of nine species of Collembola. J Insect Physiol
50: 515.
Kaspari M, Clay NA, Lucas J, Yanoviak SP, Kay A (2015) Thermal adapta-
tion generates a diversity of thermal limits in a rainforest ant commu-
nity. Glob Chang Biol 21: 10921102.
..........................................................................................................................................................
17
..........................................................................................................................................................
Research article Conservation Physiology Volume 8 2020
Kearney MR, Simpson SJ, Raubenheimer D, Kooijman SALM (2013) Bal-
ancing heat, water and nutrients under environmental change: a
thermodynamic niche framework. Funct Ecol 27: 950966.
Kingsolver JG, Buckley LB (2017) Quantifying thermal extremes and
biological variation to predict evolutionary responses to changing
climate. Philos Trans R Soc B 372: 20160147.
Kühsel S, Blüthgen N (2015) High diversity stabilizes the thermal
resilience of pollinator communities in intensively managed grass-
lands. Nature Comms 6: 7989.
Legendre P, Legendre L (2012) Numerical Ecology. Elsevier, Amsterdam
Leibold MA, Chase JM (2018) Metacommunity Ecology. Princeton Univer-
sity Press, Princeton
Leihy RI, Duy GA, Nortje E, Chown SL (2018) High resolution tempera-
ture data for ecological research and management on the Southern
Ocean islands. Sci Data 5: 180177.
Lutterschmidt WI, Hutchison VH (1997) The critical thermal maximum:
history and critique. Can J Zool 75: 15611574.
MacLean HJ, Sorensen JG, Kristensen TN, Loeschcke V, Beedholm K,
Kellermann V, Overgaard J (2019) Evolution and plasticity of thermal
performance: an analysis of variation in thermal tolerance and tness
in 22 Drosophila species. Philos Trans R Soc B 374: 20180548.
Mathakutha R, Steyn C, le Roux PC, Blom IJ, Chown SL, Daru BH, Ripley
BS, Louw A, Greve M (2019) Invasive species dier in key functional
traits from native and non-invasive alien plant species. JVegSci30:
9941006.
McGeoch MA, Jetz W (2019) Measure and reduce the harm caused by
biological invasions. One Earth 1: 171174.
Moyle PB, Kiernan JD, Crain PK, Quinones RM (2013) Climate change
vulnerability of native and alien freshwater shes of California: a
systematic assessment approach. PLoS One 8: e63883.
Naeem S, Wright JP (2003) Disentangling biodiversity eects on ecosys-
tem functioning: deriving solutions to a seemingly insurmountable
problem. Ecol Lett 6: 567579.
O’Hara RB, Kotze DJ (2010) Do not log-transform count data. Methods
Ecol Evol 1: 118122.
Orme D, Freckleton RP, Thomas GH, Petzoldt T, Fritz SA, Isaac NJB (2013)
CAPER: comparative analyses of phylogenetics and evolution in R.
MethodsEcolEvol3: 145151.
Pagel M (1999) Inferring the historical patterns of biological evolution.
Nature 401: 877884.
Phillips L, Janion-Scheepers C, Houghton M, Terauds A, Potapov M,
Chown SL (2017) Range expansion of two invasive springtails on sub-
Antarctic Macquarie Island. Polar Biol 40: 21372142.
R Core Team (2018) R: a language and environment for statistical
computing. R Foundation for Statistical Computing, Vienna, Austria.
Available at https://www.r-project.org/.
Ratnashingham S, Hebert PDN (2007) BOLD: the barcode of life data
system (www.barcodinglife.org). MolEcolNotes7: 355364.
Ribeiro PL, Camacho A, Navas CA (2012) Considerations for assess-
ing maximum critical temperatures in small ectothermic animals:
insights from leaf-cutting ants. PLoS One 7: e32083.
Rozen-Rechels D, Dupoué A, Lourdais O, Chamaillé-Jammes S,
Meylan S, Clobert J, Le Galliard JF (2019) When water interacts
with temperature: ecological and evolutionary implications of
thermo-hydroregulation in terrestrial ectotherms. Ecol Evol 9:
1002910043.
Salo T, Mattila J, Eklöf J (2020) Long-term warming aects ecosystem
functioning through species turnover and intraspecic trait varia-
tion. Oikos 129: 283295.
Sandel B, Low R (2019) Intraspecic trait variation, functional turnover
and trait dierences among native and exotic grasses along a pre-
cipitation gradient. JVegSci30: 633643.
Sarojini BB, Stott PA, Black E (2016) Detection and attribution of human
inuence on regional precipitation. Nat Clim Change 6: 669675.
Selkirk PM, Seppelt RD, Selkirk DR (1990) Subantarctic Macquarie Island:
Environment and Biology. Cambridge University Press, Cambridge
Sinclair BJ, Marshall KE, Sewell MA, Levesque DL, Willett CS, Slotsbo
S, Dong Y, Harley CD, Marshall DJ, Helmuth BS et al. (2016) Can
we predict ectotherm responses to climate change using ther-
mal performance curves and body temperatures? Ecol Lett 19:
13721385.
Sørensen JG, Holmstrup M (2011) Cryoprotective dehydration is
widespread in Arctic springtails. J Insect Physiol 57: 11471153.
Sørensen JG, White CR, Duy GA, Chown SL (2018) A widespread
thermodynamic eect, but maintenance of biological rates
through space across life’s major domains. Proc Biol Sci 285:
20181775.
Stachowicz JJ, Terwin JR, Whitlatch RB, Osman RW (2002) Linking
climate change and biological invasions: ocean warming facili-
tates nonindigenous species invasions. Proc Natl Acad Sci USA 99:
1549715500.
Sunday JM, Bates AE, Dulvy NK (2011) Global analysis of ther-
mal tolerance and latitude in ectotherms. Proc Biol Sci 278:
18231830.
Terauds A, Chown SL, Bergstrom DM (2011) Spatial scale and species
identity inuence the indigenous-alien diversity relationship in
springtails. Ecology 92: 14361447.
van Dooremalen C, Berg MP, Ellers J (2013) Acclimation responses to
temperature vary with vertical stratication: implications for vulner-
ability of soil-dwelling species to extreme temperature events. Glob
Chang Biol 19: 975984.
van Kleunen M, Bossdorf O, Dawson W (2018) The ecology and evolution
of alien plants. AnnuRevEcolEvolSyst49: 2547.
WinfreeR,ReillyJR,BartomeusI,CariveauDP,WilliamsNM,GibbsJ
(2018) Species turnover promotes the importance of bee diversity
for crop pollination at regional scales. Science 359:791793.
..........................................................................................................................................................
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... Recent work has demonstrated that the CFR Seira have remarkably high upper thermal limits to activity, with the fynbos shrubland species having average maximum critical thermal limits (CT max ) 5-6 °C higher than that of their forest counterparts and other Collembola species globally (Liu et al. 2020). Yet whether enhanced desiccation tolerance has also enabled the Seira species to diversify in the CFR, and in particular in the fynbos shrublands, remains to be explored. ...
... These variables were recorded at 20-min intervals for five microhabitat types, including fynbos shrub, fynbos litter, fynbos soil, Southern Afrotemperate Forest litter, and Southern Afrotemperate Forest soil (the Afrotemperate forest canopy was inaccessible) at three representative sampling localities (Kogelberg, Grootvadersbosch and Jonkershoek Nature Reserve) ( Fig. 1a) during the summer of 2017-2019. This period coincides with the peak activity and abundance of Seira species (Liu et al. 2020). In the fynbos shrublands, data loggers were placed at mid-height (ca. ...
... The Seira species investigated in this study are all indigenous and restricted to the CFR (Liu et al. 2020). Adult individuals of Seira species were collected from the fynbos shrubland and Southern Afrotemperate Forest habitats in seven protected areas across the CFR in South Africa ( Fig. 1a and Online Resource Table 1) between 2017 and 2019, during October to April. ...
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Trait–environment interactions have contributed to the remarkable plant radiations in the Cape Floristic Region (CFR) of southern Africa. Whether such interactions have also resulted in the diversification of the invertebrate fauna, independently of direct associations with plants is, however, not clear. One candidate where this may be the case is the unusually diverse Collembola genus Seira. Including 89 species in the CFR, many of which are localised habitat specialists, this genus includes many species inhabiting the warm, dry fynbos shrubland—a habitat atypical of usually desiccation-sensitive Collembola. Here, we investigate whether desiccation tolerance may have contributed to the considerable diversity of Seira in the CFR. First, we demonstrate, by measuring vapour pressure deficits (VPD) of the species’ microhabitats (fynbos shrubland and moister Afrotemperate Forests), that the fynbos shrublands are dry environments (mean ± S.E. maximum VPD 5.2 ± 0.1 kPa) compared with the Afrotemperate Forest patches (0.3 ± 0.02 kPa) during the summer activity period of Seira. Then we show that Seira species living in these shrublands are more desiccation tolerant (mean ± S.E. survival time at 76% relative humidity: 74.3 ± 3.3 h) than their congeners in the cooler, moister Afrotemperate Forests (34.3 ± 2.8 h), and compared with Collembola species globally (3.7 ± 0.2 h). These results, and a previous demonstration of pronounced thermal tolerance in the fynbos shrubland species, suggest that the diversity of Seira in the CFR is at least partly due to pronounced desiccation and thermal tolerance, which has enabled species in the genus to exploit the hot and dry habitats of the CFR.
... With rapid change in the region (Thost and Truffer, 2008;Lebouvier et al., 2011;Hodgson et al., 2014;McClelland et al., 2018), the current situation might be different. Our findings, however, in conjunction with trait-based forecasts of differential success with climate change of invasive alien compared with indigenous Collembola (Janion et al., 2010;Phillips et al., 2020), suggest that impacts may be even more profound. Surveys to determine the current situation are thus urgently required. ...
... The kinds of interspecific interactions that might lead to such an outcome have been identified for Macquarie Island and likely involve local-scale interspecific displacement (Terauds et al., 2011). Moreover, experimental assessments have also suggested that these interactions may be mediated into the future by differential responses to warming and drying by indigenous versus invasive species (Chown et al., 2007;Phillips et al., 2020; see also Bokhorst et al., 2008). Invasive species are generally more tolerant of or respond positively to warm-dry conditions compared with their indigenous counterparts. ...
... Whether or not some form of compensatory dynamics with either indigenous or invasive species will play out generally is not clear, but does seem to be the case from the outcomes of this study. Experimental data further suggest that invasive species will be favoured (Chown et al., 2007;Phillips et al., 2020). Indeed, this could be considered one potential weakness of the current study, where the species selected for investigation may already have been affected by changing climates, rather than by invasions. ...
Article
The Antarctic climate-diversity-invasion hypothesis (ACDI) predicts that in Antarctic soil systems, climate change should lead to increases in the abundance and diversity of indigenous assemblages. Where biological invasions have occurred, however, invasive alien species should have negative effects on indigenous faunal assemblages. To assess these predictions, we provide the first systematic ecological survey of the Collembola assemblages of pristine, sub-Antarctic Heard Island (53.1°S, 73.5°E) and compare the results to similarly conducted surveys of three other sub-Antarctic islands (Marion, Prince Edward, and Macquarie), characterised by assemblages including invasive Collembola. In particular, we examine differences in densities of three indigenous species (Cryptopygus antarcticus, Mucrosomia caeca, Tullbergia bisetosa) shared between the invaded islands and Heard Island. On average, density of these species was four or more-fold significantly lower on the invaded islands than on uninvaded Heard Island. Yet mean assemblage densities of springtails, accounting for variation among vegetation communities, did not differ substantially or significantly among the islands, suggesting that compensatory dynamics may be a feature of these systems. The invasion impact prediction of the ACDI is therefore supported. On Heard Island, indigenous assemblage variation is strongly related to vegetation community and less so to elevation, in keeping with investigations of Collembola assemblage variation elsewhere across the Antarctic. These findings, in the context of field experimental and physiological data on Collembola from the region, suggest that the climate-diversity predictions of the ACDI will play out in different ways across the Antarctic, depending on whether precipitation increases or decreases as climates change.
... In the sub-Antarctic, arthropods have evolved under chronically low but relatively stable environmental conditions (in terms of limited annual thermal variation and high relative humidity; Convey, 1996aConvey, , 1996b. They are thus expected to exhibit stenotypic characteristics, and a level of thermal adaptation to their native ecoregion, whereas non-native incoming species, typically originating from temperate (often boreal) regions are likely to exhibit more generalist eurythermal characteristics (Barendse & Chown, 2000;Chown & Convey, 2016;Phillips et al., 2020;Slabber et al., 2007). ...
... Often establishment, and subsequent changes in the distribution of the non-native species, have been suggested to be facilitated by climate change. Consistent with this,Phillips et al. (2020) reported that non-native collembolans were characterized by significantly higher critical thermal maxima than their native counterparts, although thermal plasticity differed little between them. Similar findings were reported byJanion-Scheepers et al. (2018) with warming tolerance being higher in non-native springtails over the climatic gradient they studied. ...
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... The aim of this work is to review the current state of scientific knowledge on thermal tolerance limits in Collembola, given their significance in the soil fauna, their global distribution, and the apparent differences in thermal tolerance traits between indigenous and introduced species in local assemblages and at broader spatial scales ( Janion-Scheepers et al., 2018 ;Phillips et al., 2020 ). Thermal tolerance data become of great help to manage those areas that species may or may not occupy under changing climates ( Evans et al., 2015 ). ...
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Global changes in soil surface temperatures are altering the abundances and distribution ranges of invertebrate species worldwide, including effects on soil microarthropods such as springtails (Collembola), which are vital for maintaining soil health and providing ecosystem services. Studies of thermal tolerance limits in soil invertebrates have the potential to provide information on demographic responses to climate change and guide assessments of possible impacts on the structure and functioning of ecosystems. Here, we review the state of knowledge of thermal tolerance limits in Collembola. Thermal tolerance metrics have diversified over time, which should be taken into account when conducting large-scale comparative studies. A temporal trend shows that the estimation of ‘Critical Thermal Limits’ (CTL) is becoming more common than investigations of ‘Supercooling Point’ (SCP), despite the latter being the most widely used metric. Indeed, most studies (66%) in Collembola have focused on cold tolerance; fewer have assessed heat tolerance. The majority of thermal tolerance data are from temperate and polar regions, with fewer assessments from tropical and subtropical latitudes. While the hemiedaphic life form represents the majority of records at low latitudes, euedaphic and epedaphic groups remain largely unsampled in these regions compared to the situation in temperate and high latitude regions, where sampling records show a more balanced distribution among the different life forms. Most CTL data are obtained during the warmest period of the year, whereas SCP and ‘Lethal Temperature’ (LT) show more variation in terms of the season when the data were collected. We conclude that more attention should be given to understudied zoogeographical regions across the tropics, as well as certain less-studied clades such as the family Neanuridae, to identify the role of thermal tolerance limits in the redistribution of species under changing climates.
... Although some complexity exists to these ideas (van Kleunen et al., 2010;Hulme, 2017), support for such consistent differences, especially in basal trait values, is growing (Allen et al., 2017;Capellini et al., 2015;Van Kleunen et al., 2018;Díaz de León Guerrero et al., 2020). Among terrestrial invertebrates, for example, on average, invasive alien species appear to have greater thermal tolerances, more pronounced desiccation resistance and faster growth rates than their native counterparts (Janion-Scheepers et al., 2018;Phillips et al., 2020;da Silva et al., 2021). These research outcomes are being incorporated into assessments of the current and likely future impacts of invasive alien species through the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services Invasive Alien Species Assessment (IPBES, 2021). ...
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In 1992, the Union of Concerned Scientists shared their ‘World Scientists’ Warning to Humanity’ with governmental leaders worldwide, calling for immediate action to halt the environmental degradation that threatens the systems that support life on Earth. A follow-up ‘Second Warning’ was released in 2017, with over 15 000 scientists as signatories, describing the lack of progress in adopting the sustainable practices necessary to safeguard the biosphere. In their ‘Second Warning’, Ripple and colleagues provided 13 ‘diverse and effective steps humanity can take to transition to sustainability.’ Here, we discuss how the field of conservation physiology can contribute to six of these goals: (i) prioritizing connected, well-managed reserves; (ii) halting the conversion of native habitats to maintain ecosystem services; (iii) restoring native plant communities; (iv) rewilding regions with native species; (v) developing policy instruments; and (vi) increasing outdoor education, societal engagement and reverence for nature. Throughout, we focus our recommendations on specific aspects of physiological function while acknowledging that the exact traits that will be useful in each context are often still being determined and refined. However, for each goal, we include a short case study to illustrate a specific physiological trait or group of traits that is already being utilized in that context. We conclude with suggestions for how conservation physiologists can broaden the impact of their science aimed at accomplishing the goals of the ‘Second Warning’. Overall, we provide an overview of how conservation physiology can contribute to addressing the grand socio-environmental challenges of our time.
... We observed the behavior of the individuals every ~ 3 °C, until the individuals perching on the walls became still, after which they were observed every 1 °C. At the moment in which the first individual reaches its CT max or CT min , that is, the loss of the righting response (Everatt et al. 2013), we recorded the temperature every 0.5 °C, following the methods of Phillips et al. (2020). The experiments continued until the last individual in the sample became inactive. ...
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Uncontrolled biological invasions have direct and indirect impacts on the structure and functioning of soil invertebrate communities in Antarctica. Among others, invasion success is strongly determined by the ability of species to tolerate broad thermal ranges. Yet, few studies have compared the thermal niches of native and invasive species. Physiological characterizations of upper and lower thermal tolerances are essential to test the extent to which eurythermality can benefit invasive species in a context of changing climates. Here, we compare cold and heat tolerance between adults of the alien winter crane fly Trichocera maculipennis and the native winged midge Parochlus steinenii in Antarctica. Specimens were collected in the field during the 2019/2020 austral summer, and ramping experiments controlling heating and cooling rates were performed to estimate upper and lower critical thermal limits of the two Diptera insect species. Adults of the alien fly remained active between − 5.3 °C and 30.1 °C. In turn, the native midge was active between − 5.0 °C and 28.6 °C. We observed no significant interspecific differences between lower critical thermal limits, but upper thermal limits were significantly higher for the alien species. Hence, the capacity to endure low summer temperatures in most of the Antarctic Peninsula is similar for adults of both species, but the alien crane fly is readily adapted to withstand warming scenarios. Therefore, the broad thermal tolerances exhibited by the alien crane fly can be taken as evidence to predict geographic range expansions, while also warn of high biosecurity risks for all operating research stations in Antarctica.
... Bahrndorff et al., 2006;Slabber et al., 2007;Allen et al., 2016;Alemu et al., 2017;Janion-Scheepers et al., 2018;Jensen et al., 2019). In these studies, typically it has been shown that CT min and CT max can both show quite substantial phenotypic plasticity (unlike in some other arthropods) (Alemu et al., 2017;Jensen et al., 2019;Liu et al., 2020), that different experimental rates can affect both thermal acclimation responses and trait values (Allen et al., 2016;Alemu et al., 2017), and that significant differences can be found in traits based on geography, climate, habitat and whether or not species are indigenous to a given area (Bahrndorff et al., 2006;Liefting and Ellers, 2008;Janion-Scheepers et al., 2018;Jensen et al., 2019;Phillips et al., 2020). Yet, almost all of the work on phenotypic plasticity and other forms of variation in thermal tolerances undertaken to date has employed constant temperature acclimation treatments to measure trait values. ...
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Much interest exists in the extent to which constant versus fluctuating temperatures affect thermal performance traits and their phenotypic plasticity. Theory suggests that effects should vary with temperature, being especially pronounced at more extreme low (because of thermal respite) and high (because of Jensen's inequality) temperatures. Here we tested this idea by examining the effects of constant temperatures (10–30 °C in 5 °C increments) and fluctuating temperatures (means equal to the constant temperatures, but with fluctuations of ±5 °C) temperatures on the adult (F2) phenotypic plasticity of three thermal performance traits – critical thermal minimum (CTmin), critical thermal maximum (CTmax), and upper lethal temperature (ULT50) in ten species of springtails (Collembola) from three families (Isotomidae 7 spp.; Entomobryidae 2 spp.; Onychiuridae 1 sp.). The lowest mean CTmin value recorded here was -3.56 ± 1.0 °C for Paristoma notabilis and the highest mean CTmax was 43.1 ± 0.8 °C for Hemisotoma thermophila. The Acclimation Response Ratio for CTmin was on average 0.12 °C/°C (range: 0.04–0.21 °C/°C), but was much lower for CTmax (mean: 0.017 °C/°C, range: -0.015 to 0.047 °C/°C) and lower also for ULT50 (mean: 0.05 °C/°C, range: -0.007 to 0.14 °C/°C). Fluctuating versus constant temperatures typically had little effect on adult phenotypic plasticity, with effect sizes either no different from zero, or inconsistent in the direction of difference. Previous work assessing adult phenotypic plasticity of these thermal performance traits across a range of constant temperatures can thus be applied to a broader range of circumstances in springtails.
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Assessing the resilience of polar biota to climate change is essential for predicting the effects of changing environmental conditions for ecosystems. Collembola are abundant in terrestrial polar ecosystems and are integral to food-webs and soil nutrient cycling. Using available literature, we consider resistance (genetic diversity; behavioural avoidance and physiological tolerances; biotic interactions) and recovery potential for polar Collembola. Polar Collembola have high levels of genetic diversity, considerable capacity for behavioural avoidance, wide thermal tolerance ranges, physiological plasticity, generalist-opportunistic feeding habits and broad ecological niches. The biggest threats to the ongoing resistance of polar Collembola are increasing levels of dispersal (gene flow), increased mean and extreme temperatures, drought, changing biotic interactions, and the arrival and spread of invasive species. If resistance capacities are insufficient, numerous studies have highlighted that while some species can recover from disturbances quickly, complete community-level recovery is exceedingly slow. Species dwelling deeper in the soil profile may be less able to resist climate change and may not recover in ecologically realistic timescales given the current rate of climate change. Ultimately, diverse communities are more likely to have species or populations that are able to resist or recover from disturbances. While much of the Arctic has comparatively high levels of diversity and phenotypic plasticity; areas of Antarctica have extremely low levels of diversity and are potentially much more vulnerable to climate change.
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Understanding the success factors underlying each step in the process of biological invasion provides a robust foundation upon which to develop appropriate biosecurity measures. Insights into the processes occurring can be gained through clarifying the circumstances applying to non-native species that have arrived, established and, in some cases, successfully spread in terrestrial Antarctica. To date, examples include a small number of vascular plants and a greater diversity of invertebrates (including Diptera, Collembola, Acari and Oligochaeta), which share features of pre-adaptation to the environmental stresses experienced in Antarctica. In this synthesis, we examine multiple classic invasion science hypotheses that are widely considered to have relevance in invasion ecology and assess their utility in understanding the different invasion histories so far documented in the continent. All of these existing hypotheses appear relevant to some degree in explaining invasion processes in Antarctica. They are also relevant in understanding failed invasions and identifying barriers to invasion. However, the limited number of cases currently available constrains the possibility of establishing patterns and processes. To conclude, we discuss several new and emerging confirmatory methods as relevant tools to test and compare these hypotheses given the availability of appropriate sample sizes in the future.
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Human‐mediated transport of species outside their natural range is a rapidly growing threat to biodiversity, particularly for island ecosystems which have evolved in isolation. The genetic structure underpinning island populations will largely determine their response to increased transport and thus help to inform biosecurity management. However, this information is severely lacking for some groups, such as the soil fauna. We therefore analysed the phylogeographic structure of an indigenous and an invasive springtail species (Collembola: Poduromorpha), each distributed across multiple remote sub‐Antarctic islands, where human activity is currently intensifying. For both species, we generated a genome‐wide SNP dataset and additionally analysed all available COI barcodes. Genetic differentiation in the indigenous springtail Tullbergia bisetosa is substantial among (and, to a lesser degree, within) islands, reflecting low dispersal and historic population fragmentation, while COI patterns reveal ancestral signatures of post‐glacial recolonisation. This pronounced geographic structure demonstrates the key role of allopatric divergence in shaping the region's diversity and highlights the vulnerability of indigenous populations to genetic homogenisation via human transport. For the invasive species Hypogastrura viatica, nuclear genetic structure is much less apparent, particularly for islands linked by regular shipping, while diverged COI haplotypes indicate multiple independent introductions to each island. Thus, human transport has likely facilitated this species’ persistence since its initial colonisation, through the ongoing introduction and inter‐island spread of genetic variation. These findings highlight the different evolutionary consequences of human transport for indigenous and invasive soil species. Yet both demonstrate the need for improved intraregional biosecurity among remote island systems, where the policy focus to date has been on external introductions.
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We investigated turnover and richness in Antarctic springtails to understand large‐scale patterns in soil faunal diversity and how these are altered by biological invasions. Antarctica and the Southern Ocean Islands. Collembola (springtails). We developed a database of all springtail species recorded from the Antarctic region. The relationship of species richness and turnover to high‐resolution environmental data was explored using generalized linear models and generalized dissimilarity models, and compared among indigenous and introduced species. Endemicity and species turnover were assessed using beta‐diversity and multi‐site zeta diversity metrics to explore whether introduced species have homogenized assemblages across the region. Indigenous, endemic and introduced species richness covaried positively with temperature. Endemic richness was further related to thermal heterogeneity, and introduced species richness to human occupancy. Indigenous and introduced species richness covaried positively. Species turnover across the region was high, and the introduction of non‐indigenous species further differentiated assemblages. Species similarity between sites was not related to distance, nor was geographic isolation correlated with species richness. Assemblage turnover was influenced by the area and temperature range of islands. Energy availability appears to be the primary covariate of species richness, with human presence additionally influencing introduced species richness, in agreement with other soil‐dwelling taxa. Dispersal limitation surprisingly does not seem to be important in structuring these assemblages, nor does island age appear to affect richness; this may in part reflect the severe glacial history of the region. The differentiating effect of introduced species on assemblages suggests that anthropogenic introductions originate from distinct source pools, challenging common assumptions for the Antarctic. Positive covariance between indigenous and introduced species richness accords with the “rich get richer” hypothesis. Thus, the most biotically diverse terrestrial areas of Antarctica may be the most prone to future biological invasion.
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Human activities are fundamentally altering biodiversity. Projections of declines at the global scale are contrasted by highly variable trends at local scales, suggesting that biodiversity change may be spatially structured. Here, we examined spatial variation in species richness and composition change using more than 50,000 biodiversity time series from 239 studies and found clear geographic variation in biodiversity change. Rapid compositional change is prevalent, with marine biomes exceeding and terrestrial biomes trailing the overall trend. Assemblage richness is not changing on average, although locations exhibiting increasing and decreasing trends of up to about 20% per year were found in some marine studies. At local scales, widespread compositional reorganization is most often decoupled from richness change, and biodiversity change is strongest and most variable in the oceans.
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The thermal biology of ectotherms is often used to infer species' responses to changes in temperature. It is often proposed that temperate species are more cold-tolerant, less heat-tolerant, more plastic, have broader thermal performance curves (TPCs) and lower optimal temperatures when compared to tropical species. However, relatively little empirical work has provided support for this using large interspecific studies. In the present study, we measure thermal tolerance limits and thermal performance in 22 species of Drosophila that developed under common conditions. Specifically, we measure thermal tolerance (CTmin and CTmax) as well as the fitness components viability, developmental speed and fecundity at seven temperatures to construct TPCs for each of these species. For 10 of the species, we also measure thermal tolerance and thermal performance following developmental acclimation to three additional temperatures. Using these data, we test several fundamental hypotheses about the evolution and plasticity of heat and cold resistance and thermal performance. We find that cold tolerance (CTmin) varied between the species according to the environmental temperature in the habitat from which they originated. These data support the idea that the evolution of cold tolerance has allowed species to persist in colder environments. However, contrary to expectation, we find that optimal temperature ( Topt) and the breadth of thermal performance ( Tbreadth) are similar in temperate, widespread and tropical species and we also find that the plasticity of TPCs was constrained. We suggest that the temperature range for optimal thermal performance is either fixed or under selection by the more similar temperatures that prevail during growing seasons. As a consequence, we find that Topt and Tbreadth are of limited value for predicting past, present and future distributions of species. This article is part of the theme issue 'Physiological diversity, biodiversity patterns and global climate change: testing key hypotheses involving temperature and oxygen'.