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RESEARCH ARTICLE
Ellenberg’s indicator values support
prediction of suitable habitat for pre-diapause
larvae of endangered butterfly Euphydryas
aurinia
Remigiusz Pielech
1
, Krzysztof Zając
2
, Marcin Kadej
2
*, Marek Malicki
3
, Adam Malkiewicz
2
,
Dariusz Tarnawski
2
1Department of Forest Biodiversity, Institute of Forest Ecology and Silviculture, University of Agriculture,
Krako
´w, Poland, 2Department of Invertebrate Biology, Evolution and Conservation, Institute of
Environmental Biology, University of Wrocław, Wrocław, Poland, 3Department of Botany, Institute of
Environmental Biology, University of Wrocław, Wrocław, Poland
*marcin.kadej@uwr.edu.pl
Abstract
In spite of the great popularity of Ellenberg’s Indicator Values (EIVs) in plant ecology, animal
ecologists seldom use EIVs to address ecological questions. In this study we used EIVs to
test their potential usefulness for the prediction of suitable habitat for pre-diapause larvae of
the endangered butterfly species Euphydryas aurinia. Nine transects crossing grasslands in
SW Poland with abundant populations of E.aurinia were designed. We sampled 76 vegeta-
tion plots along the transects. In addition, the presence of the larval webs of E.aurinia in
sampled plots was also recorded. We then calculated the mean community EIVs of light,
nitrogen, soil reaction, moisture and temperature for each sample plots. Generalized linear
mixed-effects models (GLMMs) were used to assess which factors determine the local
occurrence of larval webs of E.aurinia. We found the larval webs only in 12 plots, while the
host plant was present in 39 of the examined plots. The presence of the host plant was
the most important predictor in both models including all plots or including only plots with
host plants. The other significant predictor was the mean EIV of light, and its importance
increased in models considering all plots. We attributed the importance of the EIV of light to
the site openness and density of the vegetation layer. A positive relationship between this
predictor and the presence of larval webs indicates that sites with looser vegetation, a lower
contribution of shrubs and tall herbs and better penetration of photosynthetically active radi-
ation to lower vegetation layers are preferred by E.aurinia for oviposition. Moreover, the sig-
nificance of EIV of light may be linked with management practices. Many light-demanding
species decline after cessation of mowing as a result of litter accumulation and the domi-
nance of tall herbs. An absence of light-demanding species decreases the community’s
mean EIV of light and thus indicates the influence of meadow abandonment.
PLOS ONE | https://doi.org/10.1371/journal.pone.0179026 June 8, 2017 1 / 12
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OPEN ACCESS
Citation: Pielech R, Zając K, Kadej M, Malicki M,
Malkiewicz A, Tarnawski D (2017) Ellenberg’s
indicator values support prediction of suitable
habitat for pre-diapause larvae of endangered
butterfly Euphydryas aurinia. PLoS ONE 12(6):
e0179026. https://doi.org/10.1371/journal.
pone.0179026
Editor: Manuela Pinzari, Universita degli Studi di
Roma Tor Vergata, ITALY
Received: November 14, 2016
Accepted: May 23, 2017
Published: June 8, 2017
Copyright: ©2017 Pielech et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
files.
Funding: This work was supported by the
University of Wrocław no. 1076/S/IBŚ/2017 to DT
and MK. The funder had no role in study design,
data collection and analysis, decision to publish, or
preparation of the manuscript.
Competing interests: The authors have declared
that no competing interests exist.
Introduction
Since its introduction in the mid-70s, Ellenberg’s Indicator Values (EIVs) have become an
extensively used tool in ecological studies. It is especially popular in plant ecology, where EIVs
are used to characterize environmental conditions when detailed site-specific measurements
are absent. The application of EIVs includes research on vegetation change [1–3], interpreta-
tion of ecological gradients [4,5] and describing ecological preferences of both plant species
[6,7] and plant communities [8,9]. Some authors, however, have claimed that the interpreta-
tion of analyses based on EIVs may be biased due to circular reasoning [10], weak correlations
with field measurements [11–13] or inter-correlations between different EIVs [14]. In spite of
these reservations, EIVs have enjoyed great popularity and are generally believed to be an
important tool in applied plant ecology [15]. On the contrary, animal ecologists seldom use
EIVs to address ecological questions, and only a few researchers have tested this approach so
far. Significant relationships have been found between EIVs and the diversity of Sciomyzid flies
[16], butterflies [17–20] and molluscs [21]. In addition, EIVs are sometimes used to character-
ize the ecological properties of habitats of studied animal assemblages, e.g. ants [22] or mol-
luscs [23]. Some of these studies have highlighted the advantages of the utilization of EIVs in
the study of animal autoecology, but this approach is still underexplored and needs more
detailed examination.
In this study we used EIVs to test their potential usefulness in the prediction of suitable
habitat for pre-diapause larvae of Euphydryas aurinia. The species is regionally endangered
in many European countries and a great deal of effort has been put so far into supporting its
conservation. Some research suggests that host plant abundance is the only important pre-
dictor of the presence-absence and abundance of larval webs of E.aurinia [24]; however,
others showed that vegetation structure and habitat management were also important
[18,25,26]. We share the latter opinion on the basis of the field observations of E.aurinia
habitats in Poland. The species frequently occurs in meadows with a high density of its host
plant; however, there are usually apparently-similar meadows in a close vicinity with abun-
dant populations of known host plants and the absence of E.aurinia. It is obvious that the
ecological niche of the individual species does not overlap exactly with the niche of their host
plant [18]. The requirements of either larvae or adults may be limited to a narrower range of
ecological conditions than the requirements of the host plants. Understanding this spatial
pattern of species distribution at the local scale is essential for its successful conservation.
The aim of this work was to examine the relation between the EIVs and the spatial distribu-
tion of the pre-diapause larvae of E.aurinia.
Material and methods
Studied species
The marsh fritillary Euphudryas aurinia (Rottemburg, 1775) (Lepidoptera: Nymphalidae) is
widely distributed in the Palaearctic from Ireland in the West to Yakutia in the East and to
North-west China and Mongolia in the South. In many European countries it is reported to
be experiencing declines in distribution or population size [27] and the species has become
included in Annex II of the Bern Convention on the Conservation of European Wildlife and
in Annexes II and IV of the EEC/EU Habitat Directive (92/43 EU of 21 May 1992), and it is
legally protected in many European countries. However, both at the level of the Europe and
the European Union [28] as well as worldwide [27] it is listed under the least concern category.
In Poland, E.aurinia is listed as endangered in the Polish red list [29].
Ellenberg’s indicator values as predictors of Euphydryas aurinia habitat
PLOS ONE | https://doi.org/10.1371/journal.pone.0179026 June 8, 2017 2 / 12
The species occurs in different types of open or semi-open habitats, such as pastures [30],
hay meadows [18,25] or woodland clearings [31]. E.aurinia has a univoltine life cycle. Adults
fly from the third week of May until the third week of June in western Poland. In June (the
first three weeks) females lay eggs in batches on the underside of the leaves of the Devil’s-bit
scabious, Succisa pratensis (probably the only initial host plant for pre-diapause caterpillars in
western Poland). Young larvae live together in webs that are built by them directly on the host
plant. At the end of the summer or early in the autumn, the caterpillars of the IV instar build
stronger webs, located low to the ground, in which they hibernate until spring. They pupate
around beginning/mid-May [32,33].
Study area
All field investigations were carried out within the rural district of Lwo
´wek Śląski in Lower
Silesia (SW Poland), covering a total area of approximately 10 km
2
(50˚ 57’N, 15˚ 22’E). The
study area is located in the western part of the mountainous region of the Sudetes, at the foot
of the massif of the Izerskie Mts. (see [34] for details). The altitude above sea level ranges from
360 to 420 m. The annual average temperature in the research area is 7.5˚C, yearly precipita-
tion is ca. 800 mm and the vegetation period is 180 days [35]. The research area is character-
ized by a large proportion of arable land and forest, which is interposed with patchily
distributed fragments of grassland. The different grassland community types within the
research area were investigated. Some of the investigated grasslands had been abandoned for
up to 10 years, while the others were still managed with various intensities (sporadic to inten-
sive mowing). All grasslands were developed on moderately acid and nutrient poor soils,
which had been developed by draining former marshland. According to the phytosociological
nomenclature [36,37], the vegetation of the investigated grassland is classified as Molinion
caeruleae and Calthion palustris meadows, while small fragments of Violion caninae grasslands
may also occur. Some of abandoned meadows are colonized by communities dominated by
tall nitrophilous herbs (communities of Aegopodion podagrariae) and shrub (communities of
Sambuco-Salicion capreae) with domination by Rubus spp., Rosa canina, young individuals of
Betula pendula and Populus tremula. The study area is located in a Special Area of Conserva-
tion, Łąki Go
´r i Pogo
´rza Izerskiego (PLH020102), which was established within the Natura
2000 network. This area is one of the most important refuges of E.aurinia in south-western
Poland [38].
Data collection and processing
During a few years preceding this study, field surveys had been conducted within the study
area. The surveys were aimed at making an inventory of larval webs by E.aurinia, and they
yielded a detailed map of its distribution. We then used this map to design nine linear tran-
sects with lengths between 100 and 260 m, which were randomly placed within meadows
with a known occurrence of E.aurinia in previous years. In effect, each transect crossed
patches with high densities of S.pratensis, as a known host plant of pre-diapause larvae in
this region, as well as patches without its presence. Along each transect we sampled vegeta-
tion plots (2 m ×2 m) placed every 20 meters. In total, 76 plots were sampled in August
2014. Due to the particular phenology of the Molinion meadows, we sampled vegetation
plots ca. two months after the females of E.aurinia laid their eggs on the host plants. At the
beginning of June, when the eggs are laid, many of the plant species that compose these
meadow communities are at an early stage of their development and lack some important
diagnostic features. Thus, at this stage it is impossible to differentiate among some species of
Asteraceae,Apiaceae,Juncaceae or Poaceae families, but the proper determination of all plant
Ellenberg’s indicator values as predictors of Euphydryas aurinia habitat
PLOS ONE | https://doi.org/10.1371/journal.pone.0179026 June 8, 2017 3 / 12
species within the sampled plots is crucial to calculate the mean EIVs. Within each plot we
recorded all vascular plants and estimated their cover using the Braun-Blanquet scale (r—
solitary; +—<1%; 1—1–5%; 2—6–25%; 3—26–50%; 4—51–75; 5—76–100%). In addition,
the presence of the larval webs of E.aurinia in the sampled plots was also recorded. All col-
lected samples were entered into a Turboveg database [39]. The average means of the EIVs
were calculated for each sample [40]. When calculating the community means of the EIVs,
we took only the presence/absence data into consideration. We did not used the weights
determined from the abundance of each plant species because the abundance of each species
could have change between the eggs laid (June) and the vegetation being sampled (August).
Finally, the abundance of host plant (S.pratensis) was transformed into an ordinal scale
using the method proposed by van der Maarel [41].
Statistical analyses
To assess which factors determine the local occurrence of the larval webs of E.aurinia, general-
ized linear mixed-effects models (GLMMs) with a binomial error distribution and log-link
function were performed. We made two separate models that took into account (1) all the
studied plots of vegetation samples and (2) only the plots with the presence of S.pratensis. For
the purpose of both analyses we included six potential predictors of larval web occurrence:
abundance of the host plant (variable “Succisa”) and the average community means of the
EIVs of “light,” “moisture,” “nutrients,” “soil reaction” and “temperature.” The interpretation
of the ecological meaning of the EIVs was presented, e.g. as by Horsa
´k et al. [21]. The transect
was used in our analyses as a random effect. Prior to modeling we checked all variables for col-
linearity using the Spearman rank correlation matrix and the variance inflation factor (VIF).
Acceptable levels of correlation were assumed at r
S
<|0.6| and VIF values below 3 [42,43].
Due to the high correlation between “soil reaction” and “nutrients” and, for the data set based
only on releve
´s with the occurrence of S.pratensis, between “soil reaction” and “moisture” also
(S1 Table), we decided to exclude the “soil reaction” variable from both multivariate models.
After this step, we did not find any significant collinearity between the remaining variables (all
VIF scores were below 2; see S1 Table). All explanatory variables were standardized to a mean
of 0 and standard deviation of 0.5 before inclusion in the models to allow for comparisons of
their respective effect sizes [44,45].
To identify factors affecting the pre-diapause larvae of marsh fritillary presence in the study
plots we used a model selection procedure based on information theory [46]. We used Akaike
Information Criterion (AICc) to select the best reduced model. We ranked all subsets of mod-
els according to their ΔAICc values together with the associated weight value (w
i
). Models with
an ΔAICc <2 were considered to be equally good [46]. To assess whether the final models pro-
vided a good fit to the data we calculated the conditional and marginal R
2GLMM
[47,48]. The
conditional R
2
value showed the proportion of the variance in the raw data explained by the
model, including both fixed and random effects, while the marginal R
2
value showed the pro-
portion of the variance explained only by the fixed effects.
The relative importance of each variable was estimated, on a scale 0–1, by summing the
AICc weights across all models that included the explanatory variable of interest [46]. To
derive the parameter estimates (β) we used model averaging over the 95% confidence set (thus
we used all models with sum of Akaike weights 0.95 [46]). Only beta coefficients in which
the 95% confidence intervals (95% CI) did not overlap with zero were considered as signifi-
cant. Additionally, we used principal component analysis (PCA) for the visualization of vegeta-
tion samples in relation to explanatory variables.
Ellenberg’s indicator values as predictors of Euphydryas aurinia habitat
PLOS ONE | https://doi.org/10.1371/journal.pone.0179026 June 8, 2017 4 / 12
All statistical analyses were performed in open source statistical software R (version 3.2.2,
http://www.r-project.org/), with the packages: arm (version 1.8–6) [49], lme4 (version 1.1–10)
[50] and MuMIn (version 1.15.1) [51]. Plots were performed using the packages plotrix (ver-
sion 3.6) [52] and ggbiplot (version 0.55, downloaded from https://github.com/vqv/ggbiplot,
December 2015). The variance inflation factor (VIF) was calculated using the ‘vif.mer’ function
(downloaded from https://github.com/aufrank/R-hacks/blob/master/mer-utils.R, December
2015) in R.
Results
The presence of the larval webs of E.aurinia was found in 12 out of 76 studied vegetation sam-
ples (releve
´s), only on S.pratensis. The host plant was present in 39 examined plots. The key
importance of the presence of S.pratensis (as the host plant) for the occurrence of larval webs
of E.aurinia was confirmed by the results of the GLMMs. The model selection showed that,
taking into account all samples, the two models’ explanations of the presence of larval webs
were equally good (Table 1).
The best models explained over 80% of the variation and included three explanatory vari-
ables. The abundance of the S.pratensis was the most important variable explaining the pres-
ence of larval webs, followed by “light” and “temperature” factors (Fig 1).
Only the positive relation of the first two predictors with the occurrence of larval webs was
statistically significant (Fig 2).
The same three predictors were present in the best three models explaining the presence of
larval webs in the second model for vegetation samples only with the occurrence of S.pratensis
(Table 1). However, in this model the relative importance of the S.pratensis abundance was
much lower, and the most important predictor was “light” (Fig 1), which explained 36% of the
variation alone (Table 1). “Light” was also the only variable in the second model with a statisti-
cally significant effect, although the larval webs tended to be more frequent with an increase in
the abundance of the host plant (Fig 2). For both groups of models, “transect” as a random
effect was not a significant term in the GLMM. The distribution of the sampled plots with the
occurrence of the larval webs and those without the species, in relation to a gradient of explan-
atory variables, is shown in Fig 3.
Discussion
Our research has shown that the distribution of the larval webs of marsh fritillary is
closely associated with the presence of S.pretensis, which seems to be the only initial host
Table 1. Best generalized linear mixed models ((ΔAICc <2) describing the presence of the larval webs of Euphydryas aurinia in study plots.
No. Model df R
2
mR
2
c AICc ΔAICc w
i
All plots
1 ~ Succisa + Light + (1|Transect) 4 0.81 0.81 43.567 0 0.343
2 ~ Succisa + Light + Temperature + (1|Transect) 5 0.82 0.82 44.840 1.272 0.182
Plots with host plant presence
1 ~ Succisa + Light + (1|Transect) 4 0.54 0.54 43.369 0 0.299
2 ~ Light + (1|Transect) 3 0.36 0.36 45.205 1.837 0.119
3 ~ Succisa + Light + Temperature + (1|Transect) 5 0.58 0.58 45.271 1.903 0.116
R
2
m–the marginal R
2
value shows the proportion of the variance explained only by the fixed effects, R
2
c–the conditional R
2
value shows the proportion of
the variance in the raw data explained by the model, including both fixed and random effects.
https://doi.org/10.1371/journal.pone.0179026.t001
Ellenberg’s indicator values as predictors of Euphydryas aurinia habitat
PLOS ONE | https://doi.org/10.1371/journal.pone.0179026 June 8, 2017 5 / 12
plant of the caterpillars in the study population, as in many other regions of central
Europe [53]. As we expected, based on the results of other authors [18,26,30,54–56], the
abundance of the host plant was an important determinant of the occurrence of pre-dia-
pause larvae. However, our results indicated that after taking into account only samples
with the presence of the host plant, the importance of this factor decreased, in favor of the
EIV of “light”.
This factor should not be linked with the total solar radiation reaching the site, but rather
with the site openness and density of the vegetation layer [21]. A positive relation between this
predictor and the presence of larval webs indicates that sites with looser vegetation, decreasing
representation of species characteristic of forests and shrubs and better penetration of photo-
synthetically active radiation to lower vegetation layers are preferred by marsh fritillary for ovi-
position. Moreover, the significance of the EIV of “light” may be attributed to management
practices. Many light-demanding species decline after the cessation of mowing as a result of lit-
ter accumulation and the dominance of tall herbs [57–61]. The absence of light-demanding
species decreases the community mean EIV of “light” and thus indicates the influence of
meadow abandonment.
Based on this ecological interpretation, our results are consistent with those reported by
other researchers, who showed that the females of E.aurinia chose individual S.pratensis
in open vegetation structures that were fully exposed to the sun and surrounded by lower
Fig 1. Comparison of the relative variable importance (RVI) used to explain the presence of larval webs of Euphydryas aurinia in two data sets:
Including all plots and only those with the presence of Succisa pratensis.The RVI was computed as the sum of the AICc weights over all models
including the explanatory variable.
https://doi.org/10.1371/journal.pone.0179026.g001
Ellenberg’s indicator values as predictors of Euphydryas aurinia habitat
PLOS ONE | https://doi.org/10.1371/journal.pone.0179026 June 8, 2017 6 / 12
vegetation as host [18,25,26]. Larvae of E.aurinia may increase their growth rate behaviorally
by sun basking, thus microclimate conditions shaped by the looser structure of the vegeta-
tion and better access for the light may be particularly important in the case of a low temper-
ature environment [62]. Moreover, the rosette of Succisa leaves is situated close to the
ground and is easily accessible for egg-depositing females in an open vegetation structure
[25]. The accessibility and sun-exposure of the host plants are, next to visibility, the most
important factors determining the female oviposition in the Mediterranean subspecies E.a.
provincialis [63].
The presence or abundance of the host plant is of course the most important factors deter-
mining habitat quality for E.aurinia. However, there are also some other environmental
requirements that have to be met to enable its successful reproduction. Assessing habitat qual-
ity only on the basis of the number of host plants may be somewhat misleading. For example,
individuals of S.pratensis in abandoned populations have higher growth rates and produce
more flower heads per plant (in spite of higher mortality rates and lower seedling establish-
ment) [64]. As we stated above, these abandoned sites are at the same time unfavourable for E.
aurinia. Thus, various variables related to the vegetation structure and dynamics can both
fine-tune the prediction of the insect’s distribution and habitat quality assessment. As we show
in this research, EIVs may be a useful tool in that field.
Fig 2. Average parameter estimates and 95% confidence intervals (CIs) for all standardized variables in two data sets. One group includes all
plots (red color) and one only those with the presence of Succisa pratensis (green color). Parameters were averaged for the 95% confidence set of the
models.
https://doi.org/10.1371/journal.pone.0179026.g002
Ellenberg’s indicator values as predictors of Euphydryas aurinia habitat
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Supporting information
S1 Table. Spearman correlation coefficients between explanatory variables and variance
inflation factors (VIFs) for variables in final models. Significant correlations (p<0.05) are
indicated in bold.
(DOC)
Acknowledgments
This research was supported by a grant from the University of Wrocław no. 1076/S/IBŚ/2017.
The field work was conducted with the permission of the General Directorate for Environmen-
tal Protection in Poland (permit no. DOP-OZGZ.6401.35.2012.JRO).
Fig 3. PCA ordination diagram of all 76 study plots of vegetation based on six explanatory variables,with differentiation of the three groups of
plots presented with different colors and circled with 95% confidence interval ellipses. Red points and ellipsoid represents plots with Euphydryas
aurinia occurrence; green points and ellipsoid represents plots with Succisa pratensis occurrence and without E.aurinia; and blue points and ellipsoid
represent plots without S.pratensis and E.aurinia. Arrows indicate the direction of the explanatory variables. Eigenvalues: PC1–2.397, PC2–1.514.
https://doi.org/10.1371/journal.pone.0179026.g003
Ellenberg’s indicator values as predictors of Euphydryas aurinia habitat
PLOS ONE | https://doi.org/10.1371/journal.pone.0179026 June 8, 2017 8 / 12
Author Contributions
Conceptualization: KZ RP DT MK.
Data curation: KZ RP.
Formal analysis: KZ RP.
Funding acquisition: DT MK.
Investigation: AM DT MK MM.
Methodology: KZ RP.
Project administration: DT MK.
Resources: AM DT MK MM KZ RP.
Supervision: DT MK KZ RP.
Validation: KZ RP MK AM DT MM.
Visualization: KZ.
Writing – original draft: KZ RP.
Writing – review & editing: RP KZ DT MM AM MK.
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