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Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind
British Trust for Ornithology, BTO, The Nunnery, Thetford, Norfolk IP24 2PU, United Kingdom
CEH Lancaster, Lancaster Environment Centre, Library Avenue, Bailrigg, Lancaster, LA1 4AP, United Kingdom
c
Biomathematics & Statistics Scotland, BioSS Ofce, The James Hutton Institute, Craigiebuckler, Aberdeen, AB15 8QH, Scotland, United Kingdom
d
Buttery Conservation, Manor Yard, East Lulworth, Wareham, Dorset, BH20 5QP, United Kingdom
e
Rothamsted Research, West Common, Harpenden, Herts, AL5 2JQ, United Kingdom
b
a r t i c l e
i n f o
Article history:
Received 28 May 2015
Received in revised form 24 January 2016
Accepted 27 January 2016
Available online 5 March 2016
Keywords:
Climate change
Community composition
Indicator
Lepidoptera
Seasonal
Temperature
a b s t r a c t
The impacts of climate change on species and ecosystems are increasingly evident. While these tend
to be clearest with respect to changes in phenology and distribution ranges, there are also important
consequences for population sizes and community structure. There is an urgent need to develop ecological
indicators that can be used to detect climate-driven changes in ecological communities, and identify how
those impacts may vary spatially. Here we describe the development of a new community-based seasonal
climate change indicator that uses national population and weather indices. We test this indicator using
Lepidopteran and co-located weather data collected across a range of UK Environmental Change Network
(ECN) sites. We compare our buttery indicator with estimates derived from an alternative, previously
published metric, the Community Temperature Index (CTI).
First, we quantied the effect of temperature on population growth rates of moths and butteries
(Species Temperature Response, STR) by modelling annual variation in national population indices as
a function of nationally averaged seasonal variation in temperature, using species and weather data
independent of the ECN data. Then, we calculated average STRs for annually summarised species data
from each ECN site, weighted by species abundance, to produce the Community Temperature Response
(CTR). Finally, we tested the extent to which CTR correlated with spatial variation in temperature between
sites and the extent to which temporal variation in CTR tracked both annual and seasonal warming trends.
Mean site CTR was positively correlated with mean site temperature for moths but not butteries.
However, spatial variation in moth communities was well explained by mean site summer temperature
and buttery communities by winter temperature, respectively accounting for 74% and 63% of variation.
Temporal variation in moth and buttery CTR within sites did not vary with the mean annual temperature
but responded to variation in the mean temperature of specic seasons. There were positive correlations
between moth seasonal CTRs and seasonal temperatures in winter, spring and summer; and buttery
seasonal CTRs and seasonal temperatures in winter and summer. Buttery CTR and CTI both correlated
spatially and temporally with winter temperature.
Our results highlight the need for seasonality to be considered when examining the impact of climate
change on communities. Seasonal CTRs may be used to track the impact of changing temperatures on
biodiversity and help identify potential mechanisms by which climate change is affecting communities. In the case of Lepidoptera, our results suggest that future warming may reassemble Lepidoptera
communities.
2016 Elsevier Ltd. All rights reserved.
1. Introduction
127
128
(1)
and 29 September (at set times and providing certain weather conditions, dened by the protocol, were met). Butteries seen within
5 m of the transect were recorded. Counts of 47 buttery species
(Rennie et al., 2015a) and 552 species of moth (Rennie et al., 2015b)
were recorded on these sites although only species for which we
could produce national population indices were included in the
analysis (see Section 2.1).
In addition to biological recording, dry bulb air temperature was
also recorded at co-located automatic weather stations at each site.
Temperature measurements were made at 5 s intervals and stored
within the ECN database as hourly means. We used these data
(Rennie et al., 2015c) to calculate monthly mean temperatures from
which we then derived seasonal and annual mean temperatures.
In order to relate temperature measurements to the ECN biological
data, annual mean temperatures were calculated from October in
the year prior to sampling to September, the nal month of buttery monitoring. Relatively few moth species are particularly active
in their adult stage beyond September.
Moth trapping was not carried out at one of the ECN sites (Snowdon: 53.07 N, 4.03 W) due to the absence of a secure power supply,
whilst on one site (Cairngorms: 57.12 N, 3.83 W) buttery monitoring only took place for four years, so this site was excluded from
the buttery data. In addition, in this analysis we excluded moth
data from two sites (Alice Holt and Rothamsted) because data from
these sites were included in the 13-site dataset that was used to create the national moth indices which we used to characterise species
response to temperature (SI Fig. 1). Thus data from nine and eleven
ECN sites were used respectively for moths and butteries.
We modelled annual site temperature and annual seasonal temperatures against year using Linear Mixed Models (LMMs) with site
included as a random factor.
2.5. Spatial variation in communities
At each of the ECN sites, we calculated the annual moth and
buttery CTR and buttery CTI from the annual mean STR of
moth and buttery individuals and the annual mean STI of buttery individuals (Devictor et al., 2008). We modelled the mean
moth and buttery CTR and buttery CTI at each site across all
years against the mean site temperature using linear models. We
repeated this for mean seasonal CTRs and seasonal mean site temperatures and modelled buttery CTI against seasonal mean site
temperatures.
2.6. Temperature-related community change within sites
We examined the temperature-related community changes by
regressing changes in CTR with temperature. We used LMMs to
model the moth and buttery CTR anomaly (CTRA = CTR mean site
CTR) against mean annual temperature anomaly (x = mean annual
temperature mean site temperature):
CTRA = a + bx
(2)
129
Table 1
The parameter estimates, standard errors, r2 and P-values of the relationship between mean annual and seasonal moth and buttery CTR, annual buttery CTI and mean site
temperatures.
Temperature
Moth CTR
Buttery CTR
Buttery CTI
Annual
0.026 0.007
r2 = 0.662, P = 0.008
0.013 0.004
r2 = 0.650, P = 0.009
3.52 103 5.80 103
r2 = 0.050, P = 0.564
0.017 0.003
r2 = 0.839, P = 0.001
5.05 103 2.26 103
r2 = 0.007, P = 0.830
0.174 0.049
r2 = 0.581, P = 0.006
0.177 0.066
r2 = 0.443, P = 0.025
0.161 0.047
r2 = 0.562, P = 0.008
0.149 0.038
r2 = 0.625, P = 0.004
0.187 0.051
r2 = 0.601, P = 0.005
Winter
Spring
Summer
Autumn
and buttery CTI over time with site as a random factor using LMMs
as above.
3. Results
3.1. Temperature trends over time
Across sites, mean annual air temperature did not change significantly (temperature change = 6.34 103 5.91 103 C year1 ,
t = 1.07, P = 0.285). Winter temperatures were largely stable
(0.021 0.013 C year1 , t = 1.64, P = 0.103) whilst summer temperature declined during the study duration (0.019 0.009,
t = 2.21, P = 0.028). Spring and autumn temperatures increased
(spring temperature change = 0.040 0.008 C year1 , t = 5.05,
P < 0.001; autumn temperature change = 0.026 0.010, t = 2.50,
P = 0.013). The seasonal temperature range across ECN sites and
years were similar across all seasons: ranges in winter, spring,
summer and autumn temperatures were respectively 9.2 C, 8.6 C,
9.1 C and 9.1 C.
3.2. Spatial variation in communities
Mean moth CTR and buttery CTI metrics for each site were
positively correlated with mean site temperature while buttery
site CTR did not vary signicantly with site temperature (Table 1,
Fig. 1: black lines). Spatial variation in moth community composition, indicated by mean site summer and winter CTRs, was related
to mean site summer and winter temperatures respectively while
for butteries, winter and autumn CTRs were related to mean site
winter temperature and autumn temperatures (Table 1). Buttery
CTI correlated positively with all seasonal temperatures. A maximum of 83.9% and 68.1% of spatial variation in moth and buttery
communities based on CTR could be explained by mean seasonal
temperatures, respectively in summer and winter (Table 1, Fig. 2:
black lines). A maximum of 62.5% of variation in buttery CTI could
be explained by variation in summer temperatures.
3.3. Temperature-related community change within sites
We assessed the ability of the CTR indicator to track annual
variation in temperature by correlating CTR anomalies with temperature anomalies. Moth and buttery CTR and buttery CTI did
not vary signicantly with annual site temperature, although P < 0.1
for moth CTR and buttery CTI (Table 2, Fig. 1: coloured lines).
We also examined the relationship between seasonal CTR
anomalies and seasonal temperature anomalies. We found that
moth winter, spring and summer CTR varied signicantly and
positively with respective seasonal temperatures. Buttery winter
and summer CTR varied signicantly and positively with winter
and summer temperatures while buttery CTI varied positively
with winter temperatures (Table 2, for plots of all seasonal CTRs
and annual CTI varying with seasonal temperatures see SI Fig. 2).
130
Fig. 1. (a) Moth and (b) buttery annual Community Temperature Response (CTR) and (c) buttery Community Temperature Index (CTI) plotted against annual average
temperature across ECN sites between 1993 and 2012. Each site is shown with a unique symbol and colour combination: the colour indicates the average temperature at the
site with the coldest site shown in dark blue and the warmest site in red. The black crosses show the average site temperature and average site CTR (or CTI) and the black
lines show the between-site relationship between them. The coloured lines show the within-site relationship between CTR/CTI and temperature. (For interpretation of the
references to colour in this gure legend, the reader is referred to the web version of this article.)
Fig. 2. Seasonal community temperature responses (CTR) in (a) summer for moths and (b) winter for butteries and (c) buttery CTI, plotted against mean summer and
winter temperature across ECN sites between 1993 and 2012. The seasons shown here are the seasons that explained most temporal and spatial variation in moth and
buttery community composition. Each site is shown with a unique symbol and colour combination: the colour indicates the average temperature at the site with the coldest
site shown in dark blue and the warmest site in red. The black crosses show the average seasonal site temperature and average seasonal site CTR and the black lines show the
between-site relationship between them. The coloured lines show the within-site relationship between seasonal CTR and temperature. (For interpretation of the references
to colour in this gure legend, the reader is referred to the web version of this article.)
Table 2
The parameter estimates, standard errors, r2 values and P-values of the relationship between annual and seasonal moth and buttery CTR anomalies, buttery CTI anomaly
and annual and seasonal temperature anomalies.
Temperature
Annual
Winter
Spring
Summer
Autumn
Moth CTR
0.020 0.010
r2 = 0.022, P = 0.058
5.36 103 1.93 103
r2 = 0.046, P = 0.006
0.019 0.004
r2 = 0.1058, P < 0.001
0.015 0.004
r2 = 0.070, P < 0.001
2.43 103 2.41 103
r2 = 0.002, P = 0.552
Buttery CTR
4
Buttery CTI
3
6.99 10 7.95 10
r2 = 0.004, P = 0.380
6.53 104 1.66 104
r2 = 0.072, P < 0.001
5.40 104 4.53 104
r2 = 0.007, P = 0.234
2.96 103 8.60 104
r2 = 0.054, P = 0.001
8.97 105 3.87 104
r2 < 0.001, P = 0.817
0.052 0.029
r2 = 0.015, P = 0.082
0.032 0.013
r2 = 0.028, P = 0.018
6.10 103 1.93 102
r2 < 0.001, P = 0.752
1.36 103 1.88 102
r2 < 0.001, P = 0.942
3.44 103 1.62 102
r2 < 0.001, P = 0.846
variation in community composition through time: seasonal temperatures accounted for a maximum of 10.5% of variation in moth
communities and 7.2% of variation in buttery communities.
These results suggest that different processes govern spatial and
temporal variation in buttery and moth populations, although
as the results for summer temperature and moths, and winter
temperature and both groups show, they can be linked. It is also
worth noting that despite the signicant seasonal correlations with
temperature, our models explained only a small proportion of variation in community composition through time.
There was no signicant long-term trend in moth annual CTR,
whilst the buttery annual CTR trend was signicantly negative.
It is likely that these results are a combination of the complex interactions between seasonal CTR and variable temperature
trends between seasons, potentially exacerbated by unknown nonclimatic factors also driving these trends (Clavero et al., 2011;
Barnagaud et al., 2012). Thus, summer temperature declined in
the period we examined while winter temperatures remained stable, which, based on the seasonal CTR responses for butteries,
could account for the counter-intuitive decline in buttery CTR
through time. Although there was no signicant long-term trend
in moth CTR, given contrasting spring and summer temperature
trends through the time-period studied, both of which affected
annual variation in CTR, this is again to be expected. These results
suggest that both moth and buttery communities are likely to
undergo signicant future long-term changes in response to predicted future warming across all seasons, which, in the presence of
a strong warming trend, we would expect our measures of CTR to
track, at least in some seasons.
4.2. Assessing CTR as a climate change indicator
In this study we compared the ability of our CTR indicators
to track buttery community change in response to temperature
with CTI, a climate change indicator based on a species spatial association with temperature (Devictor et al., 2008, 2012).
There was a strong correlation between CTI and all measures of
spatial variation in temperature (Table 1), which is unsurprising
given the indicator is based upon the spatial association of species
with spring and summer temperature. Neither indicator tracked
annual variation in temperature, but both indicators tracked winter temperatures effectively, both spatially (Table 1) and temporally
(Table 2), although as already outlined, the spatial association was
stronger than the temporal (Fig. 2b and c). Both indicators appear to
track temporal variation in temperature with broadly similar levels
of accuracy although winter temperature could explain marginally
more spatial and temporal variation in buttery CTR (respectively
explaining 68.1% and 7.2% of variation) than CTI (respectively 44.3%
and 2.8%). This suggests that our measures of CTR may be a useful addition to the range of climate change indicators available,
although further validation is required.
Our method for quantifying STR relies on the assumption that
populations respond linearly to temperature. We would not, however, expect a linear response across the full climatic range of
most species; populations of a species are more likely to correlate positively and negatively with temperature at the cold and
warm edges of its range respectively. For many species, the range
of temperature variation across the UK may be small enough to
only cover a portion of its climatic range and thus be adequately
modelled with a linear relationship between population and temperature. However, our models would identify species with small
climatic ranges centred in the UK as unresponsive to climate. This
is likely to reduce the sensitivity of the indicator, and will limit
the spatial extent in which this indicator can be used. If STRs were
calculated using continental-scale data then many temperaturesensitive species would be classied as unresponsive. Alternative
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