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ORIGINAL PAPER
Host associations of Coenonympha hero (Lepidoptera:
Nymphalidae) in northern Europe: microhabitat rather than plant
species
Anu Tiitsaar
1
•Ants Kaasik
1
•Ly Lindman
1
•Tiina Stanevits
ˇ
1
•Toomas Tammaru
1
Received: 2 December 2015 / Accepted: 21 March 2016
ÓSpringer International Publishing Switzerland 2016
Abstract Understanding ecological requirements of
endangered species is a primary precondition of successful
conservation practice. Regrettably, we know surprisingly
little about the life history of numerous threatened insects,
and about their use of larval host plants in particular. The
brown butterflies (Nymphalidae: Satyrinae) have tradi-
tionally been considered polyphagous on grasses and
indiscriminatory in their oviposition behavior. However,
detailed studies on several species have revealed local
specialization in host plant use as well as the decisive role
of microlimatic conditions as determinants of habitat
quality. The present study addresses host plant relation-
ships in the endangered brown butterfly Coenonympha
hero (L.) at the northern limit of its European distribution.
We combine laboratory-based host preference and perfor-
mance tests with an analysis of microhabitat use by adult
butterflies in the field. Both lines of evidence suggest that
C. hero is polyphagous enough not to be associated with
one particular host species. Oviposition choices of C. hero
are not driven by host plant species but rather by structural
characteristics of the substrate. The preferred rigid needle-
like structures may serve as cues of ‘transparent’ vegeta-
tion which allows the larvae to benefit from sunlight
reaching the lower strata of the tuft. Our results suggest
that conservation efforts should prioritize microclimatic
parameters, rather than the presence of any particular host
plant species, as decisive determinants of habitat quality in
C. hero.
Keywords Satyrinae Scarce heath butterfly Preference
performance linkage Conservation Growth rate Habitat
management Grazing Monophagy Coenonympha
oedippus Habitat use
Introduction
The loss of biodiversity remains a serious concern: it has
been estimated that one third of European butterfly species
are currently declining (van Swaay et al. 2010). The
cornerstone of successful conservation practice is under-
standing the basic ecological needs of the endangered
species: primarily, the set of parameters defining a suit-
able habitat. Regrettably, we know surprisingly little about
the life history of numerous threatened insects (van Swaay
and Warren 1999). Deficient knowledge frequently turns
conservation work into a guessing game in which there is a
‘‘gut feeling’’ of how the favourable habitat looks, but it
may remain largely unknown which elements of it are
actually essential for the target species (Dolek et al. 2005;
Bru
¨ckmann et al. 2010).
In the practice of conservation work, a critical mistake
would be to assume that species’ requirements are wider than
they actually are. Indeed, there are a number of cases where
butterfly conservation has failed due to such errors
&Anu Tiitsaar
anu.tiitsaar@ut.ee
Ants Kaasik
ants.kaasik@ut.ee
Ly Lindman
ly85@ut.ee
Tiina Stanevits
ˇ
tiina.stanevits@gmail.com
Toomas Tammaru
toomas.tammaru@ut.ee
1
Department of Zoology, Institute of Ecology and Earth
Sciences, University of Tartu, Vanemuise 46, 51014 Tartu,
Estonia
123
J Insect Conserv
DOI 10.1007/s10841-016-9861-2
(Pullin 1996). The risk of this kind of misfortune appears
particularly high for the ‘‘browns’’ (Nymphalidae; Satyri-
nae), which are, in various taxonomic handbooks and field
guides, described as generalists on grasses. In addition, grass
feeding butterflies are generally believed to be indiscriminate
in their choice of oviposition site (e.g. Wiklund 1984; Berg-
man 2000). However, a different picture has emerged from
the data accumulated for some extensively studied satyrine
species (e.g. Gotthard 2004). In addition, geographic varia-
tion cannot also be neglected in this context: for example, the
larvae of the pearly heath Coenonympha arcania (Linnaeus,
1761) have been found to use 11 host plants in mainland
Europe, whereas only one has been confirmed for Sweden
(Nylin and Bergstro
¨m2009; Nylin et al. 2014).
Along with specialization to host plants per se, butterflies
are often highly selective with respect to microhabitats.
Microclimate has indeed been frequently shown to be the
crucial aspect of habitat suitability, especially at the margins
of a species’ distribution range (e.g. Roy and Thomas 2003;
Eilers et al. 2013;O
¨rvo
¨ssy et al. 2013; Lawson et al. 2014).
This type of selectivity can also limit the set of host plants
used for oviposition (Anthes et al. 2008; Gibbs and Van Dyck
2009; Bennie et al. 2013): only some of the potential host
species may grow in conditions supporting larval develop-
ment. For example, in the case of the grizzled skipper Pyrgus
malvae (Linnaeus, 1758), host plant use was shown to be
primarily driven by microhabitat preferences of the candi-
date plants (Kra
¨mer et al. 2012). Among satyrines, micro-
climatic conditions appear to be a primary criterion for
oviposition site selection in the false ringlet Coenonympha
oedippus (Fabricius, 1787): spring temperatures must be
high enough to ensure successful development of the larvae
(C
ˇelik et al. 2015). The crucial role of microclimate may
imply that even butterflies that are generalists at a larger scale
can be functional specialists due to abiotic factors restricting
the choice of oviposition sites.
The endangered (Van Swaay and Warren 1999; Van
Swaay et al. 2010,2012) scarce heath butterfly (Coeno-
nympha hero, Linnaeus, 1761; Satyrinae, Nymphalidae) is
one of the species believed to be a generalist feeding on
various grasses (Cassel et al. 2001; Cassel-Lundhagen and
Sjo
¨gren-Gulve 2007; numerous field guides), with some
reports of also using sedges (Bra
¨u and Dolek 2013).
However, the idea about a broad ecological niche of this
species is not consistent with the patchy distribution pattern
of the butterfly, nor with its high sensitivity to landscape
change (Soga and Koike 2012). Indeed, C. hero is
decreasing rapidly in many countries in Central and Wes-
tern Europe (van Swaay et al. 2012), which calls for
increasing the deficient research-based empirical evidence
on its host plant preferences and habitat use.
The objective of the current study was to explore host
plant use of C. hero in Estonia where the species still has a
favourable status. We used a combination of approaches
with a common goal to evaluate the possibility of C. hero
being specialised on a particular host species, as opposed to
being a generalist feeder on grasses. Laboratory trials were
conducted to determine host preference of ovipositing
females as well as that of newly hatched larvae. Larval
performance on different host plants was measured in
rearing experiments. To obtain further information about
host plant associations, and to select candidate plants for
our laboratory trials, we performed an analysis of habitat
use of the butterfly in Estonia. The resulting small-scale
model was based on vegetation parameters recorded in the
immediate surroundings of resting points of adult butter-
flies. Finally, we integrate the results of the different sub-
studies to discuss the likely causes of host and habitat
preferences in C. hero.
Materials and methods
Study species
Coenonympha hero is a small (wing span 27–32 mm)
slow-flying satyrine butterfly distributed over much of the
Palaearctic region, reaching the northern limit of its
European range in Estonia. This species typically inhabits
seminatural bushy meadows and woodland clearings. C.
hero is univoltine with the flight period starting from early
June and lasting to early July in northern Europe. The
grass-feeding larvae overwinter in their third instar, growth
resumes in spring, and the larvae pupate having gone
through 5 instars (Cassel-Lundhagen and Sjo
¨gren-Gulve
2007). As is the case for many satyrines (Tolman and
Lewington 1997), the larvae are cryptic and difficult to find
in their natural habitats which implies that indirect methods
must be used to study the species’ use of host plants.
For our laboratory studies on host plant relationships of
C. hero, we used wild collected females from various sites
across Estonia, and their offspring. In most cases, the wild
caught females were used in the experiments on the same
day. With of longer transportation times, females were kept
in a cool transportation box (ca 10 °C) and used in the
experiments within 48 h. The main body of laboratory
experiments were carried out at the University of Tartu in
2012 and 2013, while field work was conducted in western
Estonia in 2013. In 2015, some of the laboratory experi-
ments were repeated to include Festuca rubra, a potential
host species found to be associated with C. hero in the field
study.
J Insect Conserv
123
Oviposition preference
Wild-caught females were subjected to multiple choice
tests. In the 2012 experiments, each female was offered
five oviposition substrates simultaneously. Four of the
substrates used in these experiments were potential host
plants: Festuca ovina, Dactylis glomerata,Calamagrostis
epigejos and C. arundinacea (all Poaceae). F. ovina and D.
glomerata were selected because these plants had been
successfully used to rear C. hero caterpillars previously
(Cassel et al. 2001; Cassel and Tammaru 2003). The two
Calamagrostis spp. were added as grasses abundant in
several C. hero habitats on the Estonian mainland. F. ovina
differs from the rest of the grass species used in that it has
very narrow, needle-like leaves. To test if females may also
lay their eggs on substrates completely unsuitable as larval
hosts, we used Norway spruce (Picea abies) as a control
plant (not utilised as a host by any European butterfly). The
experiment was repeated in 2015 to include a comparison
between Festuca rubra and F. ovina, with again Picea
abies as the control.
For the multiple choice tests, adult females were housed
singly in transparent boxes (25 925 915 cm). Similarly
sized small (about 12 cm in length) plant bunches were
placed, in jars with water, circularly in equal distances
between neighbouring jars. The order was randomized for
each replicate. Sugar-water solution was offered as food for
the female using damp tissue paper located at the middle of
the box. Egg laying behaviour was initiated by 18 W flu-
orescent lamp set above the box which resulted in constant
temperature of about 27 °C inside the box. Females were
kept in the setting for 48 h, and light was on for 18 h daily.
The number of eggs laid on different substrates was
recorded thereafter.
The number of eggs laid on each plant in each trial was
analysed as dependent on the plant species using a Poisson
mixed model accounting for overdispersion, the type III
Chi squared test was based on model deviance. Female
identity was included in the models as a random factor. To
visualize rank order of plant species, the number of eggs on
each of the candidate plants was compared against the
arbitrarily chosen reference plant (F. ovina; also for all
other experiments). If not stated otherwise, all statistical
analyses were performed in the R environment (R Core
Team 2014) using package lme4 (Bates et al. 2014).
In single substrate oviposition trials, conducted in 2013,
wild caught females were placed singly in 500 ml trans-
parent boxes, accompanied by a bunch (or twigs) of one out
of three plants: F. ovina,D. glomerata or P. abies. The
selection of the substrates offered was motivated by the
results of the multiple choice tests. After 72 h, the exper-
iment was terminated, and the eggs were counted. The
influence of plant species on the number of eggs laid was
tested using an ANCOVA with host plant as the categorical
factor, and remaining life span of the female as a covariate
(an index of female age: females living longer in the lab-
oratory were likely younger when captured). Further, to
obtain the ranking order for host plants, the number of eggs
on each plant was compared to the reference plant (F.
ovina).
Larval preference
In 2012, the host plant preference of neonate larvae was
tested using a set of plant species identical to that in the
female multiple plant choice test: F. ovina,D. glomerata,
C. epigejos and C. arundinacea. The neonates were off-
spring of the butterflies used in the oviposition preference
tests. The larvae were allowed to choose between sections
of two plant species which were offered in all six possible
combinations. A Petri dish was prepared with damp filter
paper at the bottom and equally sized (ca 3 cm) leaf sec-
tions from each plant were placed on the opposite sides of
the dish (Lindman et al. 2013), with a newly hatched
caterpillar in the middle. After 24 h, larval preference was
recorded on the basis of caterpillar location and eating
marks. In the typical case, the larva was found resting on
the plant it had eaten, which made recording the preference
straightforward. The cases where larva had died during the
trial were excluded. Laboratory temperature was 23 °C
during the experiment.
To infer the overall preference rank order of the four
plant species from (all possible) pairwise comparisons, we
used Bradley–Terry model (a type of generalized linear
model, Bockenholt 2001), with a random ‘‘judge’’ factor to
incorporate the effect of brood. This analysis was per-
formed using an original SAS (SAS Institute Inc. 2008)
script, available from the authors upon request.
In 2015, the experiment was repeated so that Festuca
rubra and F. ovina were compared in pairwise settings.
The results were analysed with a binomial mixed effect
model including female identity as a random factor.
Larval performance
Larval performance on different hosts was tested using a
partly different set of candidate plants, adjusted consider-
ing the data obtained in the course of oviposition experi-
ments (above), and the field study (below). In 2013, F.
ovina and D. glomerata were included as plants preferred
in the oviposition choice experiment. In addition, Sesleria
caerulea and Helictotrichon pratense were included as
these grasses appeared to be of high abundance in the sites
in which the field study was performed. The identically
designed experiments of 2015 compared the performance
on three grass species: F. ovina (preferred for oviposition),
J Insect Conserv
123
F. rubra (positively associated with butterfly presence in
the field, see below) and D. glomerata (a grass the butterfly
is unlikely to be specialized to, due to habitat differences).
Newly hatched larvae of C. hero were placed singly in
60 ml jars, with a bunch of about 5 cm long plant sections
that were renewed on a daily basis. Larval survival was
checked daily, and surviving larvae were weighed at the
age of one week. Mortality rate was analysed as dependent
on host species using a Cox proportional hazards model for
clustered data (to accommodate the effect of brood), with
survival probability being modelled using F. ovina as the
reference plant.
Differences in larval weight between the plants were
tested by mixed ANOVA with Kenward–Roger ddf cor-
rection. The model included brood as a random factor. In
order to obtain ranking order of the plants offered, the
reference plant (F. ovina) was compared to other plants.
Host plant associations in the field
The search for plants potentially associated with the pres-
ence of C. hero relied on comparison of the points in which
a butterfly had been observed (presence points, hereafter),
with control points selected within the same habitat patch
(=site, hereafter; area 4–18 ha; Sang et al. 2010; Tiitsaar
et al. 2013). In the resulting microhabitat use model, pre-
dictor variables included abundances of particular plant
species: both those considered as potential hosts, as well as
those indicative of abiotic parameters of the site, the latter
primarily functioning as covariates in the analyses of
potential host plant associations.
The study was performed at six sites ([5 km apart) on
the islands of Saaremaa and Muhu in western Estonia. In
that area, C. hero is a relatively common species in suit-
able habitats, semi-natural calcareous grasslands with a
deep soil layer. None of the sites occupied by C. hero were
currently being managed although our preselection sample
(i.e. patches of ‘butterfly habitat’ being surveyed by the
authors: Sang et al. 2010; Tiitsaar et al. 2013; unpublished
data) included both grazed (16 sites, with C. hero being
absent from all of those) and unmanaged grasslands (45
sites). For the present study, we selected all these six sites
in which C. hero was known to occur in 2007 or 2008, and
was found again in both 2012 and 2013. All these sites
represented abandoned grassland in various stages of
overgrowth, surrounded by forest or agricultural land
which made delimiting the habitat patches straightforward.
Within the sites, we systematically searched for resting
C. hero adults. The exact resting point (i.e. the presence
point) was marked and the individual was captured to
determine its sex. Control points were selected within the
same site 10 m apart from the occupied point. Care was
taken to ensure that selection of the control points occurred
in a random manner though it was obviously reasonable
(and, mostly, also technically inevitable) to avoid habitats
unsuitable for any grassland butterflies (forests, Juniperus
thickets, water beds). Naturally, the control points cannot
be treated as true absence points as some of them might
have been occupied by C. hero butterflies at a different
time point. Nevertheless, a comparison of points occupied
and not occupied at a particular moment must contain
information relevant to microsite preferences of the but-
terfly. We aimed at selecting equal number of female, male
and control points.
Some of the captured females were retained for labo-
ratory experiments (see above), males and excess females
were released. The released individuals were marked to
avoid multiple recording. All the field data were collected
during the active flight time of butterflies (9:30–19:00,
temperature above 16 °C, and minimum of 60 % of sun-
shine). Vegetation parameters were recorded within a circle
of (r =1 m) around each of the selected points. In par-
ticular, cover of all the vascular plant species present, shrub
cover and vegetation cover were estimated visually,
whereas vegetation height was measured as average height
of dominant herbs in the circle. All estimations and mea-
surements were done by the same person, with the expert
botanist being unaware of the type of the point (presence
vs. control).
Generalized linear mixed models for binary data were
constructed to discriminate the presence points from con-
trol points, with ‘site’ being included as a random variable.
Predictor variables included the cover of the seven most
common (recorded at least 15 of 58 sampling points)
Poaceae species (as potential hosts). The rationale was that
if any particular host plant species was, indeed, an essential
determinant of the C. hero presence, it cannot be too rare at
the surveyed sites: all the sites had held C. hero for at least
3 years prior to the study. The rest of the predictors were
environmental parameters which were either measured
directly (shrub cover, vegetation height and overall vege-
tation cover) or were estimated on the basis of the floristic
composition of the sampling point. In particular, Ellenberg
cover-weighted fertility, light and moisture indices were
calculated for each point on the basis of estimated cover of
each plant species, and corresponding species-specific
Ellenberg values (Schaffers and Sykora 2000; Diekmann
2003) using the freeware program MAVIS (2000). To
avoid collinearity among predictor variables, we excluded
those Poaceae species that were already included sepa-
rately (see above). As a result, the values of thirteen dif-
ferent parameters were calculated for each sampling point.
To compare models with different sets of predictors, we
used the variable ranking procedure based on the Akaike
information criterion (as described by Anderson et al.
2000; Burnham and Anderson 2004; Johnson and Omland
J Insect Conserv
123
2004). Models with all possible combinations of predictors
were run, and the models were ranked using the AIC
C
value. Subsequently, model averaging was used to estimate
the importance of each parameter. Initially, we analysed
the data for male and female butterflies separately. How-
ever, as the results were highly consistent for the two sexes,
we present the analyses with sexes pooled, i.e. for all the
presence points compared to the control points.
Results
Oviposition preference
In 2012 a total of 27 females were used in multiple choice
tests in the laboratory. Of these, 21 females laid eggs, 522
eggs altogether (range 1–69; mean 19.3 ±3.0 SE), of
which 329 were attached to any of the plant species, and
could thus be considered in further analyses (the rest were
laid on cage walls, floor etc.). Although at least a few eggs
were recorded on all plants species (Table 1), the number
of eggs clearly differed between the plants offered (GLZ
assuming Poisson distribution, v
2
=34.1, df =4,
p\0.001). F. ovina was strongly preferred over C. arun-
dinacea,C. epigejos and D. glomerata. Surprisingly, in
2012, the number of eggs on the control plant, Norway
spruce (P. abies), was equal to the number of eggs on F.
ovina. In 2015, the 8 females which were allowed to
choose between three candidate plants clearly preferred F.
ovina over F. rubra and Picea abies (GLZ assuming
Poisson distribution, v
2
=11.7, df =2, p=0.003;
Table 1).
Single substrate oviposition trials were conducted with
34 wild caught females, equally divided between 3 plant
species: F. ovina,D. glomerata or P. abies. During the
72 h experiment, the females laid a total of 972 eggs (2–73
per female, 28.6 ±2.8 SE on average). Although eggs
were laid on all substrates offered, the number of eggs
depended on plant species (ANOVA: F
2,31
=4.62,
p=0.018). In particular, females laid significantly more
eggs on F. ovina, as compared to D. glomerata (or the
control plant P. abies, Table 2). The effect of the covari-
ate—female age—was not significant (F
1,31
=0.27,
p=0.61).
Larval preference
In 2012, a total of 757 neonatae larvae (offspring of 13
females) were used in larval preference tests; 605 of them
survived until the end of the experiment. Larval host plant
preference could unambiguously be recorded for 289 lar-
vae; the remaining ones were found in the experimental
arena in situations other than resting on any of the plant
fragments. In concordance with female host choice
experiments, larvae preferred F. ovina over other plants
(Table 3), the least preferred plant species being D.
glomerata. In 2015, the test was repeated to assess the
preference between F. ovina and F. rubra. From 45 larvae
(9 broods), a clear majority (77 %) selected F. rubra (bi-
nomial mixed-effects model: z =3.49, p\0.001).
Despite the selectivity, in both years and in all combi-
nations, all the offered plant species were accepted and
eaten by some of the larvae (see Table 3). In the 2012
experiment, the probability to make a recordable choice did
not depend on plant combination offered (v
2
=7.2,
df =5, p=0.21).
Larval performance
In 2013, 277 (43.6 %) of neonate larvae survived to the age
of 7 days, this value being higher in 2015 (62 out of 88:
70.5 %). In 2013, survival during the first week of larval
development did not differ between the grasses offered
(Cox proportional hazard model for clustered data:
Robust’s score =5.46, p=0.14). In 2015, survival on D.
glomerata and F. rubra was significantly higher compared
to F. ovina (Robust’s score =7.23, p=0.027; the contrast
between F. ovina and D. glomerata:z=-2.50,
p=0.012, F. ovina vs. F. rubra:z=-5.22, p\0.001).
Among-plant differences in growth performance, mea-
sured as larval weight at the age of 7 days, were not dramatic
(Table 4) but attained statistical significance (2013:
F
3,274
=8.37, p\0.001, 2015: F
2,43
=15.45, p\0.001).
Table 1 Results of multiple choice tests
N Range Estimate SE z value p
2012
C. arundinacea 11 0–6 -3.38 0.95 -3.56 <0.001
C. epigeios 2 0–1 -4.43 1.13 -3.93 <0.001
D. glomerata 7 0–3 -3.33 0.93 -3.58 <0.001
P. abies 154 0–45 0.12 0.78 0.16 [0.05
F. ovina 155 0–31 – – – –
2015
F. rubra 39 0–35 -3.19 1.19 -2.67 0.007
P. abies 11 0–9 -3.96 1.27 -3.13 0.002
F. ovina 145 0–35 – – – –
Significances \0.05 are marked in bold
Ovipositing C. hero females were provided plants to choose from, and
the number of eggs laid on a plant was modelled as dependent on host
plant species using Poisson mixed effects model with overdispersion
accounted for. Egg numbers laid on a given plant species were tested
against the reference plant, F. ovina. N—number of eggs laid on a
plant, summed over the females in the experiment (27 in 2012, 8 in
2015). Range—the range of the number of eggs laid on particular
plant species in a replicate
J Insect Conserv
123
In 2013, the larvae reared on F. ovina,D. glomerata and H.
pratense were similar in weight whereas larvae reared on S.
caerulea remained smaller compared to those on F. ovina
(Table 4). In 2015, larval weights were significantly lower
on F. ovina compared to either F. rubra or D. glomerata
(Table 4).
Host plant associations in the field
The microhabitat use model was based on a total of 58
points which were described from six studied C. hero sites
on Saaremaa and Muhu islands: 19 female and 19 male
presence points compared to 20 control points. The sur-
veyed grasslands were highly species rich: a total of 148
vascular plant species were recorded during the survey, 21
on average in each circle. Various species characteristic of
calcareous grasslands were prevalent: Carex flacca (docu-
mented in 42 circles), Sesleria caerulea (39), Galium
boreale (36), Briza media (35), Galium verum (35), Inula
salicina (30), Helictotrichon pratense (29), Filipendula
vulgaris (29), Festuca rubra (28), Centaurea jacea (25),
and Poa angustifolia (27). Of the potential host plants, the
estimated cover values of 7 most common grasses—H.
pubescens, H. pratense, F. rubra, F, ovina, S. caerulea, B.
media and P. angustifolia—were included as separate
predictor variables in the analyses (see ‘‘Materials and
methods’’ section for variable selection; Table 5).
In general, no model or single predictor received over-
whelming support in models discriminating between the
presence and control points (Tables 5,6). Both model
averaging and examination of top ranked models revealed
that butterfly presence was positively related to parameters
of physical environment: shrub cover, Ellenberg light and
moisture value. Of particular host plants, only the cover of
F. rubra appeared among the high ranked variables. By
contrast, butterflies appeared to avoid locations with high
cover of H. pubescens. Other variables had substantially
lower predictive power (Tables 5,6). Finally, we used a
permutation test to assess the possibility that the high AIC
rankings were a result of a chance only. Null hypothesis of
no useful information in the model was rejected with
p=0.0011, as based on z values of five highest ranked
predictor variables.
Table 2 Results of single
substrate oviposition trials with
C. hero females
Aver. Estimate SE t value p
D. glomerata 21.6 -23.94 7.20 -3.34 0.003
P. abies 27.1 -16.25 6.59 -2.47 0.012
F. ovina 43.0 – – – –
Life span after experiment -0.41 0.62 -0.64 [0.05
Significances \0.05 are marked in bold
The number of eggs laid on F. ovina was compared to the number of eggs on other plants. Aver. average
number of eggs laid during the 72 h experiment
Table 3 The results of the larval preference test
Choice % Estimate SE DF tp
C. arundinacea 46.8 -0.57 0.25 48.22 -2.29 0.03
C. epigeios 47.3 -0.57 0.25 47.79 -2.28 0.03
D. glomerata 39.8 -0.61 0.25 50.03 -2.42 0.02
F. ovina 64.3 – – – – –
Significances \0.05 are marked in bold
The probability of choosing a particular species is compared against
that of the reference plant, F. ovina (Bradley–Terry GLZ model with
random ‘‘judge’’ effect). Choice % shows how often the species was
chosen when it was one of the two plants offered
Table 4 Larval weight at
1 week of age as dependent on
host species
Aver. weight (mg) Estimate SE tvalue p
2013
H. pratense 0.77 -0.11 0.059 -1.93 [0.05
D. glomerata 1.00 0.11 0.062 1.78 [0.05
S. caerulea 0.71 -0.17 0.058 -2.98 0.003
F. ovina 0.89 – – – –
2015
F. rubra 1.11 0.68 0.096 7.13 <0.001
D. glomerata 1.14 0.68 0.12 5.86 <0.001
F. ovina 0.42 – – – –
Significances \0.05 are marked in bold
Performance on F. ovina is compared to that on other candidate plants using ttests
J Insect Conserv
123
Discussion
Laboratory experiments showed that Coenonympha hero
can indeed be considered a generalist feeder on grasses: no
potential host species offered was refused by the larvae.
Larval performance on different grasses did not show
substantial differences even if the growth tended to be
somewhat better on ‘‘fleshy’’ grasses like D. glomerata and
F. rubra, as opposed to F. ovina and S. caerulea.In
addition, females readily laid their eggs on substrates other
than plants, which is a pattern characteristic of poly-
phagous Lepidoptera (Tammaru et al. 1995; Janz and Nylin
1997; Nylin et al. 2000). Field observations on habitat use
were consistent with the lab-based results: environmental
factors other than the presence of any particular host plant
species ranked highest in the models of microhabitat use.
In some conflict with the suggested larval polyphagy,
oviposition behaviour of C. hero females was far from
indiscriminatory: the butterflies strongly preferred Festuca
ovina and, surprisingly, in one of the experiments, also the
control plant Norway spruce (P. abies). The high rank of F.
ovina as well as laying eggs on non-host plants was con-
firmed in single substrate oviposition trials. Even if not
directly testing for host preference, single-substrate tests
provide information complementary to that delivered by
multiple choice tests (Tammaru et al. 1995). In particular,
in enclosures with multiple plant species, eggs may be laid
on non-host plants due to the confounding effect of the
proximity of higher ranked hosts while one substrate
designs are free of this problem. In such experiments, the
number of eggs laid during a certain (short) period of time
is a measure of host acceptability (Javois
ˇand Tammaru
2004,2006; Gamberale-Stille et al. 2014; Friberg et al.
2015).
Despite the well expressed oviposition substrate pref-
erence, there was no evidence of preference-performance
linkage: the preferred F. ovina could not be shown to be a
host supporting larval development better than its alterna-
tives. Notably, in the experiments of 2015, F. ovina clearly
bypassed F. rubra in terms of oviposition preference
whereas the situation was the opposite for larval preference
and performance. Moreover, even if F. ovina was present at
five out of six of our fieldwork sites, the overlap with the
occupied points was marginal and the relative importance
of this covariate was low (Table 5). Furthermore, in one of
the experiments, Norway spruce, a plant definitely not
suitable for larval development, proved to be a highly
ranked oviposition substrate. Spruce twigs were readily
accepted also in the single substrate oviposition trials,
showing that the stimuli from a suitable host plant are not
essential for eliciting oviposition behaviour in C. hero (cf.
Tammaru and Javois
ˇ2000).
Combining several lines of evidence, the following
scenario appears likely. C. hero females have selective
oviposition preferring grasses (and perhaps other plants: to
be confirmed in the field) with narrow and rigid leaves as
substrates. We suggest that such a preference is not adap-
tive in terms of providing the offspring with a host plant of
the ‘right’ species but is rather ‘designed’ to provide the
larvae with suitable microclimatic conditions (see Kra
¨mer
et al. 2012;C
ˇelik et al. 2015; for similar results). The
common feature of the preferred F. ovina and P. abies is
Table 5 Vegetation parameters and their relative importance measured in model averaging
Parameter Relative importance Medians (quartiles) of The no. of points where present Unit
Presence point Control point
Ellenberg moisture 0.93 4.9 (4.5–5.6) 4.6 (4.4–4.9) – Score 1–10
Shrub cover 0.77 7.5 (0–20.0) 1.0 (0–5.0) – Coverage (%)
Ellenberg light 0.65 7.0 (6.9–7.3) 7.0 (6.9–7.1) – Score 1–10
Helictotrichon pubescens 0.60 0 (0–1.0) 0 (0–1.0) 20 Coverage (%)
Festuca rubra 0.44 0.5 (0–5.0) 0 (0–1.0) 28 Coverage (%)
Vegetation height 0.35 25.0 (20.0–30.0) 25.0 (20.0–30.0) – cm
Vegetation cover 0.34 84.0 (80.0–95.0) 90.0 (75.0–95.0) – Coverage (%)
Briza media 0.27 2.2 (0–0.6) 0.3 (0–0.8) 35 Coverage (%)
Sesleria caerulea 0.26 0.8 (0–1.0) 1.5 (0–1.3) 39 Coverage (%)
Festuca ovina 0.24 0.3 (0–1.0) 0 (0–0.3) 19 Coverage (%)
Ellenberg fertility 0.22 3.4 (2.8–3.9) 3.5 (3.2–4.0) – Score 1–10
Poa angustifolia 0.22 1.6 (0–0.3) 0.5 (0–0.3) 27 Coverage (%)
Helictotrichon pratense 0.22 4.6 (0–5.0) 0.2 (0–10.0) 29 Coverage (%)
The models were built to discriminate between butterfly presence and control points (see ‘‘Materials and methods’’ section for further details)
J Insect Conserv
123
the presence of narrow and rigid needle-like structures
which can therefore be hypothesized to serve as oviposi-
tion stimuli for C. hero. Consistently, such structural
stimuli have been proposed to be decisive in oviposition
site selection also in the related C. oedippus (Bra
¨u et al.
2010; Sielezniew et al. 2010). The females can afford to
lay their eggs without considering the species composition
of surrounding vegetation (see Cassel and Tammaru 2003;
Bra
¨u and Dolek 2013 for some field observations) as the
larvae appear polyphagous enough. Moreover, as shown by
this study, the larvae are also capable of active host
selection (see Bonelli et al. 2010; Lindman et al. 2013, for
other satyrines). Indeed, oviposition indiscriminate with
respect to host quality is expected to evolve in those spe-
cies whose hosts are abundant enough, with higher
oviposition rate (Tammaru et al. 1995; Janz and Nylin
1997; Nylin et al. 2000) and perhaps higher selectivity with
respect to abiotic conditions being the associated benefits.
In agreement with observations on some other butter-
flies (Mo
¨llenbeck et al. 2009; Beyer and Schultz 2010), it
has been recently shown for the related C. oedippus that
direct solar radiation is critical for successful development
of the larvae in spring. Being exposed to sunshine is
therefore suggested to be a factor largely determining
microhabitat suitability for that species (Bra
¨u et al. 2010;
C
ˇelik et al. 2015). We thus hypothesize that the adaptive
significance of preferring narrow-leaved grasses is in the
‘transparency’ of the plant cover: vegetation consisting of
plants like certain Festuca spp. allows sunshine to reach
the ground. The result is also in line with a positive effect
of Ellenberg light index on the presence of C. hero in the
field study.
Indeed, other environmental variables rather than the
presence of any particular plant species ranked highest in
our analysis of C. hero microhabitat use (Table 5). Even if
fully consistent with the authors’ experience and some
published observations (i.e. Bergman et al. 2004), we
cannot exclude the possibility that the positive effect of
bush cover (and perhaps also Ellenberg light index) may
have been inflated by a methodological artefact. As the
butterflies were frequently observed next to juniper bushes
exposed to the sun—which they may actually prefer as
resting sites—we could often select the control points only
by moving in the direction of decreasing bush cover
(avoiding thickets: see ‘‘Materials and methods’’ section).
Nevertheless, we cannot see a similar potentially con-
founding effect which could explain the high rank of
moisture—in the models simultaneously including bush
cover in particular.
The results are again congruent with those for C.
oedippus:S
ˇas
ˇic (2010) similarly demonstrated that the
butterfly was more frequently present in patches with a
higher Ellenberg moisture index. We have currently no
Table 6 Parameter estimates for the ten highest ranking models applied to discriminate between butterfly presence and control points
Ellenberg
moisture
Shrub
cover
Ellenberg
light
Helictotrichon
pubescens
Festuca
rubra
Vegetation
height
Vegetation
cover
Briza
media
Sesleria
caerulea
Festuca
ovina
Ellenberg
fertility
Poa
angustifolia
Helictotrichon
pratense
df logLik AICc DAICc
1.78 1.10 0.84 -0.61 – – 0.08 – – – – – – 7 -27.6 71.4 0.00
1.45 1.07 0.77 – – – 0.07 – – – – – – 6 -29.05 71.7 0.36
1.01 0.96 – -0.77 0.80 – – – – – – – – 6 -29.08 71.8 0.43
1.29 0.82 0.63 -1.02 0.74 0.67 – – – – – – – 8 -26.51 72.0 0.59
1.54 1.18 0.72 -0.81 0.57 – 0.07 – – – – – – 8 -26.64 72.2 0.85
1.04 1.01 – -1.07 0.89 0.56 – – – – – – – 7 -28.01 72.3 0.88
1.2 0.87 0.51 -0.71 0.68 – – – – – – – – 7 -28.01 72.3 0.89
1.2 0.65 0.60 – – – – – – – – – – 5 -30.60 72.4 0.98
1.40 – 0.87 -0.70 – 0.75 – – – – – – – 6 -29.36 72.4 0.99
1.55 0.58 0.77 -0.73 – 0.62 – – – – – – – 7 -28.11 72.5 1.09
Significances \0.05 are marked in bold
Habitat parameters are ranked from left to right according to their relative importance
J Insect Conserv
123
data available to address the question of why moisture and
the presence of shrubs positively affects habitat quality for
the butterfly. The reason might be as simple as sensitivity
of larvae and eggs to desiccation. Nevertheless, it appears
likely that a combination of high soil moisture and light
exposure is favoured by C. hero as this ensures that the host
grasses do not dry out in the second half of summer, i.e.
during the pre-hibernation larval development, but pro-
vides warm microclimate during spring development. The
sensitivity to host quality in terms of wilting has been
shown to be high both for C. hero (Cassel et al. 2001)as
well as for some other satyrine butterflies (Bra
¨u et al. 2010;
Lindman et al. 2013). Moreover, the mortality of C. hero
larvae in the laboratory was quite high (relative to various
other lepidopteran species reared under analogous condi-
tions, pers. obs. of the authors), even on the best host plants
and variable between years. This is in line with the idea
that C. hero is highly sensitive to environmental conditions
during larval development: an aspect of undeniable
importance also in the conservation-ecological context.
Festuca rubra was the only potential host plant species
whose cover appeared among the reasonably strong pre-
dictors of the presence of C. hero butterflies (Table 5). To
evaluate the possibility that the Estonian populations of C.
hero may, despite the potential polyphagy, still be spe-
cialised on F. rubra, we repeated most laboratory experi-
ments with this grass now included in the sample. F. rubra
was shown not to be preferred as an oviposition substrate
by C. hero females, neither did it support larval growth
notably better than the alternative generalist grass Dactylis
glomerata. We are thus inclined to conclude that the
microhabitat-scale association of C. hero and F. rubra is a
result of similar habitat requirements of these two species,
rather than reflecting a direct biological link between them.
As a part of the current study, we evaluated the use-
fulness of recording butterfly resting points as a cue for the
species’ ecological preferences. With our primary focus on
host plant associations, we found such a small-scale habitat
analysis preferable to approaches such as transect counts,
or map-based analyses of landscape use. Only in our small
study plots were we able to describe plant cover in suffi-
cient detail. Immediate surroundings of a field-recorded
individual must be informative with respect of habitat
suitability to a greater or lesser extent. Even if the resting
spots recorded do not necessarily coincide with oviposition
sites, the slow- and low flying Coenonympha butterflies
appear to be intimately linked to their habitat (Cassel-
Lundhagen and Sjo
¨gren-Gulve 2007, personal observations
of the authors) being thus promising objects for this type of
research. The clearly non-random—and, at least partly,
expected—picture emerging from the analysis of respec-
tive data for C. hero appears encouraging. We also do not
see any methodological bias in the analyses which aim at
evaluating the effect of particular plant species, especially
by means of multi-way models including abiotic parame-
ters as covariates. This is despite the potential ambiguities
which may be related to assessing the effect of the abiotic
parameters themselves (see above).
In the context of species conservation, the present
study points at the priority of microclimatic conditions
(exposure to sun, soil moisture) over the presence of
particular host plant species as determinants of habitat
suitability. As moderate shrub cover appears to be pre-
ferred by C. hero, changing the extent of shrubs as well as
causing major changes in the structure of vegetation cover
(such as grazing) should thus be applied with extreme
care. Indeed, C. hero appears to avoid grazed sites simi-
larly to C. oedippus (C
ˇelik et al. 2015)—none of the
Estonian populations of C. hero known to the authors
appears to inhabit grazed sites (unpublished data; Sang
et al. 2010). The preference of (semi)open but unmanaged
habitats implies that rotational grazing or temporary
abandonment is necessary where species conservation is
concerned.
Acknowledgments We are grateful to Isabel C. Barrio, Robert B.
Davis, Matthias Dolek, Toomas Esperk, Madli Pa
¨rn, Villu Soon,
Virve So
˜ber, Tiit Teder, Erki O
˜unap and three anonymous reviewers
for valuable comments on manuscript; Meeli Mesipuu for her
botanical expertise which made a valuable contribution to this paper;
as well as Hendrik Meister, Kristiina Saksing and Ingrid Talgre for
their help in the laboratory. The study was supported by institutional
research funding IUT (IUT20-33) of the Estonian Ministry of Edu-
cation and Research, and by the European Union through the Euro-
pean Regional Development Fund (Center of Excellence FIBIR).
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