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Do Biotic and Abiotic Factors Influence the Prevalence of a Common Parasite of the Invasive Alien Ladybird Harmonia axyridis?

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Hesperomyces virescens (Ascomycota, Laboulbeniales), a fungal ectoparasite, is thus far reported on Harmonia axyridis from five continents: North and South America, Europe, Africa, and Asia. While it is known that He. virescens can cause mortality of Ha. axyridis under laboratory conditions, the role of biotic and abiotic factors in influencing the distribution of He. virescens in the field is unknown. We collected and screened 3,568 adult Ha. axyridis from 23 locations in seven countries in Central Europe between October and November 2018 to test the effect of selected host characters and climate and landscape variables on the infection probability with He. virescens. Mean parasite prevalence of He. virescens on Ha. axyridis was 17.9%, ranging among samples from 0 to 46.4%. Host sex, climate, and landscape composition did not have any significant effect on the infection probability of He. virescens on Ha. axyridis. Two color forms, f. conspicua and f. spectabilis, had a significantly lower parasite prevalence compared to the common Ha. axyridis f. novemdecimsignata.
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fevo-10-773423 April 12, 2022 Time: 10:2 # 1
ORIGINAL RESEARCH
published: 13 April 2022
doi: 10.3389/fevo.2022.773423
Edited by:
Mathew Samuel Crowther,
The University of Sydney, Australia
Reviewed by:
Gabriele Rondoni,
University of Perugia, Italy
Tamara Szentivanyi,
Centre for Ecological Research,
Hungarian Academy of Science,
Hungary
*Correspondence:
Danny Haelewaters
danny.haelewaters@gmail.com
Present Address:
Danny Haelewaters,
Department of Biology, Ghent
University, Ghent, Belgium
Specialty section:
This article was submitted to
Population, Community,
and Ecosystem Dynamics,
a section of the journal
Frontiers in Ecology and Evolution
Received: 09 September 2021
Accepted: 10 March 2022
Published: 13 April 2022
Citation:
Haelewaters D, Hiller T,
Ceryngier P, Eschen R, Gorczak M,
Houston ML, Kisło K, Knapp M,
Landeka N, Pfliegler WP, Zach P,
Aime MC and Nedv ˇ
ed O (2022) Do
Biotic and Abiotic Factors Influence
the Prevalence of a Common Parasite
of the Invasive Alien Ladybird
Harmonia axyridis?
Front. Ecol. Evol. 10:773423.
doi: 10.3389/fevo.2022.773423
Do Biotic and Abiotic Factors
Influence the Prevalence of a
Common Parasite of the Invasive
Alien Ladybird Harmonia axyridis?
Danny Haelewaters1,2,3, Thomas Hiller4, Piotr Ceryngier5, René Eschen6,
Michał Gorczak7,8 , Makenna L. Houston2, Kamil Kisło8, Michal Knapp9,
Nediljko Landeka10 , Walter P. Pfliegler11, Peter Zach12, M. Catherine Aime2and
Oldˇ
rich Nedv ˇ
ed1,3
1Faculty of Science, University of South Bohemia, ˇ
Ceské Budˇ
ejovice, Czechia, 2Department of Botany and Plant Pathology,
Purdue University, West Lafayette, IN, United States, 3Biology Centre of the Czech Academy of Sciences, Institute
of Entomology, ˇ
Ceské Budˇ
ejovice, Czechia, 4Department of Ecology of Tropical Agricultural Systems, University
of Hohenheim, Stuttgart, Germany, 5Institute of Biological Sciences, Cardinal Stefan Wyszy ´
nski University, Warsaw, Poland,
6CABI, Delémont, Switzerland, 7Institute of Evolutionary Biology, Faculty of Biology, University of Warsaw, Warsaw, Poland,
8Botanic Garden, Faculty of Biology, University of Warsaw, Warsaw, Poland, 9Department of Ecology, Faculty
of Environmental Sciences, Czech University of Life Sciences Prague, Prague, Czechia, 10 Public Health Institute of the Istrian
Region, Pula, Croatia, 11 Department of Molecular Biotechnology and Microbiology, University of Debrecen, Debrecen,
Hungary, 12 Institute of Forest Ecology, Slovak Academy of Sciences, Zvolen, Slovakia
Hesperomyces virescens (Ascomycota, Laboulbeniales), a fungal ectoparasite, is thus
far reported on Harmonia axyridis from five continents: North and South America,
Europe, Africa, and Asia. While it is known that He. virescens can cause mortality of Ha.
axyridis under laboratory conditions, the role of biotic and abiotic factors in influencing
the distribution of He. virescens in the field is unknown. We collected and screened
3,568 adult Ha. axyridis from 23 locations in seven countries in Central Europe between
October and November 2018 to test the effect of selected host characters and climate
and landscape variables on the infection probability with He. virescens. Mean parasite
prevalence of He. virescens on Ha. axyridis was 17.9%, ranging among samples from
0 to 46.4%. Host sex, climate, and landscape composition did not have any significant
effect on the infection probability of He. virescens on Ha. axyridis. Two color forms, f.
conspicua and f. spectabilis, had a significantly lower parasite prevalence compared to
the common Ha. axyridis f. novemdecimsignata.
Keywords: community ecology, Hesperomyces, Laboulbeniales, parasite prevalence, precipitation, temperature,
spatial modeling, agricultural landscape
INTRODUCTION
Parasites may be the least studied life form on the planet (Price, 1980;Windsor, 1990, 1995).
In their call for a “global parasite conservation plan,Carlson et al. (2020) proposed 12 major
goals within four themes. These themes are data collection and synthesis (aimed at describing
parasites and incorporating them into biodiversity surveys, among others), risk assessment and
prioritization (documenting drivers of parasite declines and develop regional and global Red
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Haelewaters et al. Biotic Factors Influencing Hesperomyces virescens
Lists), conservation practice (e.g., building parasite conservation
capacity), and outreach and education. One of the most common
parasites of the globally invasive harlequin ladybird Harmonia
axyridis (Coleoptera, Coccinellidae) is Hesperomyces virescens,
which was for the first time observed on this host in 2002
(Garcés and Williams, 2004).
Hesperomyces virescens (Ascomycota, Laboulbeniales) is a
biotrophic fungus that has a very wide distribution with
confirmed reports in North and South America, Europe, Africa,
and Asia (Haelewaters et al., 2017). Based on the results of an
integrative taxonomic approach, we know that He. virescens is
a complex of multiple species segregated by hosts (Haelewaters
et al., 2018a). Thus far, two species have been formally described
in the complex, He. halyziae (Haelewaters and De Kesel,
2020) and He. parexochomi (Crous et al., 2021). The other
species, including the one associated with Ha. axyridis, are
awaiting formal description. The parasite prevalence of He.
virescens on Ha. axyridis differs among geographic regions and,
exceptionally, may be as high as 96.5% in a given ladybird
population, as reported in Meise, Belgium (February 2012,
n= 107) and in Westmoreland, New Hampshire, United States
(December 2012; n= 83) (Haelewaters et al., 2017). As
a result, He. virescens has recently gained traction among
entomologists as a potential biological control agent against
Ha. axyridis.
Little information is available about the ecology of He.
virescens. A recent experimental study demonstrated that
infection with He. virescens affects the survival of Ha. axyridis on
its own and when ladybirds are co-infected with either of two
entomopathogenic fungi, Beauveria bassiana and Metarhizium
brunneum (Haelewaters et al., 2020). Thus far, however, potential
effects of biotic and abiotic factors on the distribution of He.
virescens and its parasite prevalence on Ha. axyridis are unknown.
This information is fundamental for studies in conservation,
applied ecology, and biocontrol strategies (Ferrier, 2002;Rushton
et al., 2004;Magan, 2021). In this study, we collected adult
specimens of Ha. axyridis across Central Europe and evaluated
how selected host traits and climate and landscape variables
affect infection patterns with He. virescens. Variables tested
included host sex, host color form, color of elytra, proportion of
agricultural and forested areas (European Environment Agency,
2020), temperature, and precipitation (Fick and Hijmans, 2017).
MATERIALS AND METHODS
Ladybirds were collected either by hand or using a mouth-
operated aspirator from October to November 2018 in different
Central European countries (Figure 1): Croatia (Istria County),
the Czech Republic (Central Bohemian Region, South Bohemian
Region, Plzeˇ
n Region), Germany (State of Bavaria), Hungary
(Hajdú-Bihar County), Poland (Mazovian Voivodeship),
Slovakia (Nitra Region), and Switzerland (Canton of Jura).
Contributors were asked to collect at least 100 specimens from
each ladybird population. Geographic coordinates were recorded
and can be found in Supplementary File 1. Specimens were
preserved in 70% ethanol until examination in the laboratory.
Ladybirds were screened under 40–50×magnification for
the presence of non-hyphal thalli of He. virescens (sensu De
Kesel, 2011;Haelewaters et al., 2018a). For each ladybird, the
following traits were recorded: sex (see McCornack et al., 2007);
color form [non-melanic f. novemdecimsignata (also referred
to as succinea), and melanic f. conspicua, f. axyridis, and f.
spectabilis]; color of elytra (for non-melanics) or spots (for
melanics) (yellow, orange, red; Fiedler and Nedvˇ
ed, 2019).
For novemdecimsignata specimens, we described whether spots
were well-circumscribed (0), missing or fewer in number than
typically present (), or large and touching each other (+)
(Fiedler and Nedvˇ
ed, 2019). For each population, no matter the
number of sampled ladybirds, we screened 100 randomly selected
specimens. When available, we screened and processed additional
specimens of the melanic forms to avoid statistical restrictions
due to these forming in low percentages. Screening results for
all processed ladybirds are available in Supplementary File 1.
After processing, voucher specimens were deposited in the
Purdue Entomology Research Collection (West Lafayette, IN,
United States) under the following accession numbers: PERC
0147670–0147680.
All statistical analyses were performed using the R software,
version 3.6.3 (R Core Team, 2020). To identify the variables
influencing the infection probability of He. virescens on Ha.
axyridis, we used generalized mixed effect models (GMEM) with
a binomial data distribution (infected yes/no) [function glmer(),
R package lme4;Bates et al., 2015]. We included host sex, host
color form, color of elytra, the proportion of agricultural, and
forested areas in a buffer surrounding each sampling location
(100 m, 300 m, 600 m, 1 km, and 2.5 km), and climate variables.
Urban area was excluded from the analysis because it was highly
collinear with the other predictor variables. For each buffer
radius, a separate model was calculated, resulting in five distinct
models. The landscape variables were obtained by extracting the
landscape composition of Copernicus Corine Land Cover images
taken in 2018 (European Environment Agency, 2020) with the
help of R package raster, using the function extract (Hijmans
et al., 2020). We pooled values in the categories “broad-leaved
forest,” “coniferous forest,” and “mixed forest” into the forested
area variable, whereas the agricultural area variable consisted
of values for the categories “non-irrigated arable land,” “fruit
trees and berry plantations,” “pastures,” “complex cultivation
patterns,” and “land principally occupied by agriculture, with
significant areas of natural vegetation” (Supplementary File 2).
We further calculated three models using a “ring buffer” or
annulus (sensu Rey et al., 2020), one for each of the following
radius combinations: 100 m inner and 300 m outer radius,
300 m inner and 600 m outer radius, and 600 m inner and
1 km outer radius.
Climate variables were extracted from WorldClim with a
resolution of 30 arc seconds (ca. 1 ×1 km) (Fick and Hijmans,
2017) (Supplementary File 2). As variables for temperature
and humidity are generally collinear, we decided to summarize
the following variables using a principal component analysis
(PCA) [prcomp(), R package stats;R Core Team, 2020]: annual
mean temperature, mean maximum temperature in the hottest
month, mean minimum temperature in the coldest month,
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Haelewaters et al. Biotic Factors Influencing Hesperomyces virescens
FIGURE 1 | Parasite prevalence by sampled population.
annual precipitation, precipitation during the wettest month,
and precipitation during the driest month. We extracted the
values for the first two dimensions for all sampling sites
(Supplementary File 2). Statistical processing revealed two
principal dimensions that explained 64 and 30.1% of the climatic
variation, respectively. Finally, we included the random intercept
collection nested within sampling region to address repeated
sampling at the same location and also spatial autocorrelation as
suggested by Zuur et al. (2010).
Hypothesis testing was done using likelihood ratio tests, with
pvalues calculated based on χ2distributions, declaring an effect
significant when p0.05. Nine models were compared, namely,
the Null Model and the model with variables of interest within
the different buffer radii (100 m, 300 m, 600 m, 1 km, and
2.5 km) and annulus radii (100–300 m, 300–600 m, and 600 m–
1 km). Model selection happened using the Akaike Information
Criterion (Akaike, 1974). For all models, we calculated pseudo-
R2values to estimate model fit by accounting for the variation
explained by both fixed and random effects [function r2(), R
package performance;Lüdecke et al., 2020].
RESULTS
We screened a total of 3,568 ladybirds, resulting in a mean
infection prevalence of 17.9%, ranging from 0 to 46.4% among
sampled populations (Figure 1). The population with the highest
prevalence of He. virescens was from Levice in southwestern
Slovakia. Two populations showed no visible signs of He.
virescens infection, both of which were from Poland. Forty-seven
individuals were excluded from statistical analyses, including
a single f. intermedia specimen from Warsaw, Poland and 46
specimens with missing information on elytral color. Likelihood
ratio tests confirmed that each of the eight models explained
the observed variance better than chance (Table 1), while the
conditional pseudo R2-values estimated model fit at around 0.33,
indicating good fit (Table 1). We only found variables on host
individual characters to have significant effects on the parasite
prevalence of He. virescens on Ha. axyridis (Tables 2,3). The
significant effect of color form was consistent in all five models,
with the color forms f. conspicua and f. spectabilis being less often
infected compared to the common form f. novemdecimsignata(0).
There was a trend for f. novemdecimsignata(-) to be less
likely infected by He. virescens compared to the common
form f. novemdecimsignata(0). This trend was consistent over
all candidate models but not significant. Finally, the color of
elytra had a significant effect on the infection probability, with
individuals with red elytra being more likely and individuals with
yellow elytra less likely infected compared to individuals with
orange elytra. Host sex, climate, and habitat composition resulted
in not having any significant effect on the infection probability of
He. virescens on Ha. axyridis.
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TABLE 1 | Results of model (dependency of Hesperomyces virescens prevalence
on Harmonia axyridis on coloration and climate and habitat properties) evaluation
showing candidate models being significantly better than the null model and
estimated pseudo-R2values indicating model fit.
Model AIC χ2pvalue pseudo-R2
Null Model 2,934.0
Buffer 100 m 2,880.7 77.3 <0.001*** 0.35
Buffer 300 m 2,880.1 77.9 <0.001*** 0.33
Buffer 600 m 2,879.3 78.6 <0.001*** 0.32
Buffer 1 km 2,879.6 78.4 <0.001*** 0.32
Buffer 2.5 km 2,880.8 77.2 <0.001*** 0.35
Annulus 100–300 m 2,880.1 77.9 <0.001*** NA
Annulus 300–600 m 2,879.2 78.8 <0.001*** 0.32
Annulus 600 m–1 km 2,879.8 78.2 <0.001*** 0.33
Significance levels at: ***p <0.001.
DISCUSSION
Ha. axyridisHe. virescens
The first published record of He. virescens on Ha. axyridis in
Europe was made in the winter of 2006–2007, from Meise
in Belgium (De Kesel, 2011). Other country records followed
quickly, from the Netherlands (2008), Germany (2008–2009),
Croatia and the Czech Republic (2013), Hungary and Poland
(2014), Slovakia (2015), Bulgaria and Greece (2017), and most
recently European Russia and Switzerland (2018) (Herz and
Kleespies, 2012;Ceryngier and Twardowska, 2013;Ceryngier
et al., 2013;Pfliegler, 2014;Gorczak et al., 2016;Ceryngier
and Romanowski, 2017;Haelewaters et al., 2017;van Wielink,
2017;Orlova-Bienkowskaja et al., 2018; this paper). Many of
these papers show that the parasite prevalence of He. virescens
differs significantly over time and in space (Raak-van den
Berg et al., 2014;Haelewaters et al., 2017). Differences in
Laboulbeniales prevalence among locations have been attributed
to host population density and habitat type (Scheloske, 1969;De
Kesel, 1996), but to date, no data were thus far available with
regard to the He. virescensHa. axyridis association.
Effect of Biotic Factors
A remarkable finding from our study is that the melanic color
forms f. conspicua and f. spectabilis were less often infected
with He. virescens compared to the common nineteen-spotted
f. novemdecimsignata(0). Two other studies investigated the
relationship between the degree of melanization and infection
patterns. Haelewaters et al. (2018b) observed a slight trend to
higher intensity of parasitism in more melanic males of Ha.
axyridis f. novemdecimsignata.Fiedler and Nedvˇ
ed (2019) found
(i) a positive association between putative age groups of Ha.
axyridis estimated as carotenoid content and infection with
He. virescens and (ii) a negative association between elytral
melanization of Ha. axyridis f. novemdecimsignata specimens
and infection. The latter was explained by the fact that younger
ladybirds emerged later in the year, with lower temperatures
inducing extensive melanization; since they were younger, they
had less opportunities to be parasitized by He. virescens. Our
results are in line with the findings of Fiedler and Nedvˇ
ed (2019),
but a definitive answer as to how elytral melanization affects the
susceptibility to infection with He. virescens remains unclear. The
black coloration of melanic forms of Ha. axyridis is negatively
correlated with the total content of alkaloids (Bezzerides et al.,
2007), which serve as defense against predators and pathogens
(Röhrich et al., 2011). Then, heavier melanization should result in
more infection with He. virescens, but our results are inconsistent
with this hypothesis. Future work—performing bioassays in
controlled settings and analyzing expression levels of immune
genes—is needed to shed light on the susceptibility of different
color morphs to He. virescens.
The results of our modeling approach show a significant
correlation between elytral color and the infection probability of
Ha. axyridis with He. virescens. Carotenoid accumulation, and
thus red color intensity, is a function of ladybird age (Bezzerides
et al., 2007;Nedvˇ
ed et al., 2019). In our study, older individuals
of Ha. axyridis accumulated more He. virescens inoculum.
Similar observations were made by Fiedler and Nedvˇ
ed (2019),
particularly that individuals with red elytra are more likely to
be infected. Hesperomyces virescens transmits among ladybirds
through physical contacts (during mating and in overwintering
aggregations), but auto-transmission by grooming or cleaning
also occurs. These factors contribute to parasite prevalence (at the
level of population) and thallus density (at the individual level)
being positively correlated with host age (Riddick and Schaefer,
2005;Nalepa and Weir, 2007;Haelewaters et al., 2017) and thus,
incidentally, with elytral color.
Effect of Abiotic Factors
Mean parasite prevalence did not significantly change according
to any of the temperature variables tested [Kruskal–Wallis test,
function kruskal.test(), R package stats; R Core Team, 2020], but
our sampling scheme was somewhat limited, with only localities
in Central European countries. For a broader understanding of
the associations between He. virescens and Ha. axyridis within
Europe, we recommend incorporation of data from northern and
southern European countries in order to compile a dataset with a
larger range in temperature. Collections also need to be expanded
to city centers (e.g., in parks, community gardens, edges of
playgrounds). A negative correlation was found between parasite
prevalence of He. virescens sensu lato on Adalia bipunctata and
distance from the city center of London (Welch et al., 2001).
Prevalence in central London was as high as 40% (n= 105),
whereas it was 0% outside of the urban area at a distance of
25 km. This could be linked to increased temperatures in urban
environments (urban heat island effect), but this has not yet been
tested. Adriaens et al. (2008) highlighted the idea that Ha. axyridis
is less frequently found in natural landscapes compared to more
urbanized and anthropogenic landscapes. Habitat preference may
also be an important factor in the parasitism with He. virescens.
Factors promoting Ha. axyridis may indirectly promote He.
virescens. Particularly, a higher dominance of Ha. axyridis in
a given ladybird community will be beneficial for ascospore
transmission among individuals. The number of generations
of Ha. axyridis in Central Europe varies from two to three
and is probably dependent on habitat summer temperatures
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TABLE 2 | Obtained parameters of each candidate model addressing the prevalence of infection by Hesperomyces virescens for different buffer radii (100 m, 300 m,
600 m, 1 km, 2.5 km).
100 m buffer 300 m buffer
Estimate Std. Error z value pvalue Estimate Std. Error z value pvalue
(Intercept) 1.597 0.507 3.149 0.002 ** 1.652 0.480 3.441 0.001 ***
f. axyridis 0.299 0.768 0.389 0.697 0.303 0.769 0.394 0.693
f. conspicua 0.944 0.282 3.347 0.001 *** 0.942 0.282 3.344 0.001 ***
f. spectabilis 0.469 0.156 2.996 0.003 ** 0.469 0.156 2.999 0.003 **
f. novemdecimsignata(-) 0.224 0.122 1.846 0.065 . 0.225 0.121 1.853 0.064 .
f. novemdecimsignata(+) 0.020 0.170 0.117 0.907 0.022 0.170 0.128 0.898
red 0.599 0.124 4.839 0.000 *** 0.594 0.124 4.797 0.000 ***
yellow 0.663 0.154 4.310 0.000 *** 0.665 0.154 4.318 0.000 ***
sex m 0.003 0.102 0.032 0.975 0.003 0.102 0.030 0.976
agricultural 0.036 0.123 0.293 0.769 0.090 0.108 0.835 0.403
forest 0.029 0.097 0.304 0.761 0.044 0.096 0.453 0.651
Dim1 0.327 0.210 1.556 0.120 0.279 0.205 1.360 0.174
Dim2 0.090 0.127 0.713 0.476 0.100 0.122 0.822 0.411
600 m buffer 1 km buffer
Estimate Std. Error z value pvalue Estimate Std. Error z value pvalue
(Intercept) 1.679 0.461 3.644 0.000 *** 1.654 0.466 3.549 0.000 ***
f. axyridis 0.303 0.768 0.395 0.693 0.302 0.768 0.393 0.694
f. conspicua 0.944 0.282 3.352 0.001 *** 0.948 0.282 3.364 0.001 ***
f. spectabilis 0.469 0.156 3.005 0.003 ** 0.471 0.156 3.017 0.003 **
f. novemdecimsignata(-) 0.223 0.121 1.839 0.066 . 0.221 0.121 1.824 0.068 .
f. novemdecimsignata(+) 0.023 0.170 0.136 0.892 0.023 0.170 0.133 0.894
red 0.591 0.124 4.771 0.000 *** 0.593 0.124 4.780 0.000 ***
yellow 0.666 0.154 4.331 0.000 *** 0.668 0.154 4.341 0.000 ***
sex m 0.002 0.101 0.018 0.985 0.002 0.101 0.016 0.987
agricultural 0.135 0.105 1.291 0.197 0.123 0.104 1.178 0.239
forest 0.039 0.090 0.432 0.666 0.027 0.088 0.304 0.761
Dim1 0.248 0.198 1.249 0.212 0.264 0.200 1.321 0.187
Dim2 0.113 0.120 0.946 0.344 0.120 0.122 0.981 0.327
2.5 km buffer
Estimate Std. Error z value pvalue
(Intercept) 1.571 0.502 3.129 0.002 **
f. axyridis 0.300 0.769 0.390 0.697
f. conspicua 0.946 0.282 3.356 0.001 ***
f. spectabilis 0.470 0.156 3.005 0.003 **
f. novemdecimsignata(-) 0.224 0.121 1.841 0.066 .
f. novemdecimsignata(+) 0.021 0.170 0.122 0.903
red 0.598 0.124 4.808 0.000 ***
yellow 0.665 0.154 4.319 0.000 ***
Sex m 0.002 0.101 0.020 0.984
Agricultural 0.030 0.157 0.189 0.850
Forest 0.034 0.113 0.299 0.765
Dim1 0.334 0.216 1.544 0.123
Dim2 0.086 0.136 0.634 0.526
Significance levels at: .p<0.1, **p <0.01, ***p <0.001.
and prey availability. Population densities can increase due to
the use of various prey patches enabled by high mobility in
combination with the weak tendency for diapause extending
the breeding period (Honek et al., 2018). In urbanized areas,
the breeding season of Ha. axyridis is advanced by 2–3 weeks
(Honek et al., 2021).
In addition to our buffer radius models, which are often
used for forest management on a landscape scale (Brouwers
et al., 2010), we also employed annulus radii to better model
the behavior of Ha. axyridis in autumn. Our sampling localities
are not where ladybirds became infected with He. virescens. As a
result, the habitat variables might not be accurate for the habitats
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TABLE 3 | Obtained parameters of each candidate model addressing the prevalence of infection by Hesperomyces virescens for different annulus radii (100–300 m,
300–600 m, 600 m–1 km).
100–300 m 300–600 m 600 m–1 km
Estimate Std. Error z value pvalue Estimate Std. Error z value pvalue Estimate Std. Error z value pvalue
(Intercept) 1.651 0.478 3.454 0.001 *** 1.671 0.460 3.636 0.000 *** 1.634 0.472 3.464 0.001 ***
f. axyridis 0.304 0.769 0.395 0.693 0.302 0.768 0.393 0.694 0.301 0.768 0.393 0.695
f. conspicua 0.943 0.282 3.346 0.001 *** 0.946 0.282 3.357 0.001 *** 0.949 0.282 3.369 0.001 ***
f. spectabilis 0.469 0.156 3.001 0.003 ** 0.470 0.156 3.010 0.003 ** 0.472 0.156 3.021 0.003 **
f. novemdecimsignata(-) 0.225 0.121 1.853 0.064 . 0.222 0.121 1.832 0.067 . 0.221 0.121 1.820 0.069 .
f. novemdecimsignata(+) 0.022 0.170 0.129 0.898 0.023 0.170 0.135 0.892 0.022 0.170 0.130 0.897
red 0.594 0.124 4.795 0.000 *** 0.591 0.124 4.773 0.000 *** 0.594 0.124 4.789 0.000 ***
yellow 0.665 0.154 4.320 0.000 *** 0.667 0.154 4.333 0.000 *** 0.668 0.154 4.341 0.000 ***
sex m 0.003 0.101 0.030 0.976 0.002 0.102 0.015 0.988 0.002 0.101 0.016 0.987
agricultural 0.093 0.106 0.877 0.381 0.139 0.104 1.336 0.181 0.111 0.105 1.058 0.290
forest 0.046 0.097 0.472 0.637 0.037 0.089 0.419 0.675 0.024 0.087 0.269 0.788
Dim1 0.275 0.204 1.348 0.178 0.249 0.197 1.262 0.207 0.279 0.201 1.388 0.165
Dim2 0.101 0.121 0.829 0.407 0.114 0.119 0.957 0.338 0.119 0.124 0.964 0.335
Significance levels at: .p<0.1, **p <0.01, ***p <0.001.
that the ladybirds occupied when they became infected with
the fungus. Generally, we estimate that Ha. axyridis ladybirds
fly 500 m during autumn migration. Detailed observations of
ladybirds in ˇ
Ceské Budˇ
ejovice, Czech Republic allowed the exact
measurement of migration distance from before flight and after
flight, which was 200–500 m toward the north (O. Nedvˇ
ed,
unpublished). The longest flights measured were around 1,800 m
in laboratory flight mills (R˚
užiˇ
cka, 1984). When Nalepa et al.
(2005) conducted their experiments to test the role of visual
contrast in autumn behavior of Ha. axyridis in 4 ha of open
pasture, the required flight was about 200 m (Nalepa et al., 2005).
In open fields in Japan, the median flight distance was around
400 m (Seko et al., 2008). We tested three different annulus radii
(100–300 m, 300–600 m, and 600 m–1 km), but the results of
our candidate models were highly similar to the buffer radius
models. Aggregations of ladybirds are often formed on walls of
building oriented toward the south or west (Kidd et al., 1995;
Raak-van den Berg et al., 2012;Haelewaters et al., 2018b). As
a result, we suggest that the annulus modeling approach could
be made even more specific by obtaining landscape variables
for an annulus section (or ring pie chart) facing the direction
where ladybirds likely migrated from. This is methodologically
complex and out of the scope of this paper, but is a consideration
for future studies.
Community ecology research of Laboulbeniales is still
in its infancy, with thus far only two published studies.
Szentiványi et al. (2019) investigated whether climatic variables
(temperature, humidity) influenced the distribution of ant-
and bat fly-associated Laboulbeniales. They found that both
the presence and prevalence of Laboulbeniales on their hosts
were positively associated with low annual mean temperature
and humidity. In addition, based on the study of more
than 9,374 workers of the invasive ant Lasius neglectus in
66 colonies, Gippet et al. (2021) found that the presence
of Laboulbenia formicarum on the ants was positively linked
to warmer and dryer conditions at lower elevations. These
are seemingly contrary results, and our data render drawing
general conclusions for these microfungi even more complex.
However, the direction of the effects of some of these
variables may be species-specific, as suggested by Dumolein
(2021). One could make the case that the combined analysis
of presence/absence data in Szentiványi et al. (2019) may
obscure true interactions, and thus that separate analyses would
give a more accurate picture of how bioclimatic variables
affect the distribution of the two assessed study systems—the
bat fly-associated Arthrorhynchus spp. vs. the ant-associated
Rickia wasmannii. We note that the studies of Szentiványi
et al. (2019) and Gippet et al. (2021) used outside climatic
data as obtained from MERRAclim, but many of these ant–
Laboulbeniales and bat fly–Laboulbeniales interactions and the
host dynamics resulting in fungal transmission take place in
ant nests and bat roosts, respectively. Ant nest and bat roosting
environments are characterized by their own microclimatic
conditions, which likely play a role in shaping the distribution
of these species of Laboulbeniales. Efforts should be redirected at
collecting temperature and relative humidity data (e.g., through
automated readers) within these environments to test for the
effect of these microclimate-specific abiotic traits on parasitism
with Laboulbeniales.
Our results are the first for the Ha. axyridisHe. virescens
study system based on specimens collected during autumn
migration. Understanding the factors influencing the infection
of Laboulbeniales on invasive ladybirds—including climatic and
landscape variables as well as seasonality and host behavior (e.g.,
Raak-van den Berg et al., 2014;Haelewaters et al., 2015, 2017;
Markó et al., 2016)—will help understand their global spread
as they cross many different ecosystems and environmental
conditions. Resolving this question will also inform potential
biocontrol strategies because it will inform us under which
conditions He. virescens may (or may not) thrive. The collection
of standardized multi-year, multi-site field data will help in this
regard in addition to controlled laboratory experiments.
Frontiers in Ecology and Evolution | www.frontiersin.org 6April 2022 | Volume 10 | Article 773423
fevo-10-773423 April 12, 2022 Time: 10:2 # 7
Haelewaters et al. Biotic Factors Influencing Hesperomyces virescens
DATA AVAILABILITY STATEMENT
The original data from this study are included in the
article/Supplementary Material, further inquiries can be
directed to the corresponding author.
AUTHOR CONTRIBUTIONS
DH and ON designed the study. DH, TH, PC, RE, MG, KK,
MK, NL, WPP, PZ, and ON collected the data. DH, TH, PC,
and MH performed data analysis. DH, MCA, and ON acquired
funding. DH and TH drafted the manuscript. DH revised the
manuscript. All authors edited and approved the final version
of the manuscript.
FUNDING
This work was supported by a Junior Postdoctoral Fellowship
from the Research Foundation–Flanders (1206620N to
DH); the Polish Ministry of Science and Higher Education
(grant no. DI2014012344 to MG); funds from the project
Improvement in Quality of the Internal Grant Scheme at CZU,
CZ.02.2.69/0.0/0.0/19_073/0016944 (students grant 71/2021);
the Scientific Grant Agency of the Ministry of Education,
Science, Research and Sport of the Slovak Republic and the
Slovak Academy of Sciences (VEGA, grant no. 2/0032/19 to PZ);
a USDA National Institute of Food and Agriculture Hatch project
(1010662 to MCA), and the Czech Science Foundation (grant
no. 20-10003S to ON). RE was supported by CABI with core
financial support from its member countries (and lead agencies)
including the United Kingdom (Foreign, Commonwealth and
Development Office), China (Chinese Ministry of Agriculture
and Rural Affairs), Australia (Australian Centre for International
Agricultural Research), Canada (Agricultural and Agri-Food
Canada), Netherlands (Directorate-General for International
Cooperation), and Switzerland (Swizz Agency for Development
and Cooperation).
ACKNOWLEDGMENTS
We thank Aaron D. Smith (Purdue Entomological Research
Collection) for curatorial support, Thomas E. Martin (Operation
Wallacea) for textual edits, Michal ˇ
Reˇ
richa (Czech University
of Life Sciences Prague) for help with the processing of
Czech specimens, and two reviewers for critical feedback that
considerably improved the manuscript.
SUPPLEMENTARY MATERIAL
The Supplementary Material for this article can be found
online at: https://www.frontiersin.org/articles/10.3389/fevo.2022.
773423/full#supplementary-material
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Conflict of Interest: The authors declare that the research was conducted in the
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Frontiers in Ecology and Evolution | www.frontiersin.org 8April 2022 | Volume 10 | Article 773423
... Living and dead specimens were sexed and assigned a color morph (novemdecimsignata = succinea, spectabilis, conspicua; sensu Roy et al., 2016) using a stereomicroscope at 10× magnification. For novemdecimsignata specimens (except in CBA and HV samples), we categorized carotenoid coloration [orange (O), red (R)] and described whether spots were well-circumscribed, separate, and 19 in number (0); missing or fewer in number than 19 (-), or large and touching each other (+) (Fiedler and Nedvěd, 2019;Haelewaters et al., 2022a). All ladybird specimens were screened for parasitism with He. harmoniae by looking for three-dimensional thalli (Blackwell et al., 2020;Fig. ...
... Excluding the spring sample (CBS), the overall prevalence on ladybirds collected in Č eské Budějovice was 38 % (n = 141). In earlier studies during which Ha. axyridis specimens were collected during autumn flight in Č eské Budějovice, the parasite prevalence ranged from 19 % (n = 486, collected in 2018; Haelewaters et al., 2022a) to 26 % (n = 1102, collected in 2014; Fiedler and Nedvěd, 2019). These numbers confirm previous observations that parasitism of Ha. axyridis by He. harmoniae varies significantly over time, which may be the result of a combination of biotic and abiotic variables (Haelewaters et al., 2017b(Haelewaters et al., , 2022aRaakvan den Berg et al., 2014). ...
... In earlier studies during which Ha. axyridis specimens were collected during autumn flight in Č eské Budějovice, the parasite prevalence ranged from 19 % (n = 486, collected in 2018; Haelewaters et al., 2022a) to 26 % (n = 1102, collected in 2014; Fiedler and Nedvěd, 2019). These numbers confirm previous observations that parasitism of Ha. axyridis by He. harmoniae varies significantly over time, which may be the result of a combination of biotic and abiotic variables (Haelewaters et al., 2017b(Haelewaters et al., , 2022aRaakvan den Berg et al., 2014). ...
Article
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Many observations have been done in nature but experimental studies of interactions of multiple enemies on Ha.axyridis are rare. In light of this knowledge gap, we tested whether the host phenotype and presence of bacterialendosymbionts Spiroplasma and Wolbachia affected parasitism of Ha. axyridis by the ectoparasitic fungus Hes-peromyces harmoniae (Ascomycota: Laboulbeniales). We collected 379 Ha. axyridis in the Czech Republic, pro-cessed specimens, including screening for He. harmoniae and a molecular assessment for bacteria, and calculatedfecundity and hatchability of females. We found that high hatchability rate (71 %) was conditioned by highfecundity (20 eggs daily or more). The average parasite prevalence of He. harmoniae was 53 %, while theinfection rate of Spiroplasma was 73 % in ladybirds that survived in winter conditions. Wolbachia was onlypresent in 2 % of the analyzed ladybirds. Infection by either He. harmoniae or Spiroplasma did not differ amonghost color morphs. In the novemdecimsignata morph, younger individuals (with orange elytra) were more heavilyparasitized compared to old ones (with red elytra). Fecundity and hatchability rate of females were unaffected byinfection with either He. harmoniae or Spiroplasma. However, female ladybirds co-infected with He. harmoniaeand Spiroplasma had a significantly lower fecundity and hatchability compared to females with only one or nosymbiont.
... Principal components of the PCA can then be used as explanatory variables in regression models [24]. Among the different components, we have focused on the first two dimensions, PC1 and PC2 which collectively explained the higher variability of the data [25]. Values for PC1 and PC2 were extracted for all sampling sites. ...
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Fungi in the order Laboulbeniales (Ascomycota, Laboulbeniomycetes) are obligate, microscopic ectoparasites of arthropods. These fungi, unlike their close relatives, never form hyphae. Instead, they produce a three-dimensional thallus that consists of several hundred to a thousand vegetative cells derived from a two-celled ascospore by determinate mitotic divisions. Of 2,325 described species, 80 % are known from beetles (Coleoptera). Hesperomyces is a genus of 11 species associated with ladybirds (Coleoptera, Coccinellidae) and false skin beetles (Biphyllidae). One species, Hesperomyces virescens, is known from all continents except Australia and Antarctica, and has been reported on 30 ladybird hosts in 20 genera. Previous work, based on geometric morphometrics, molecular phylogeny, sequence-based species delimitation methods, and host information, pointed out that He. virescens is a complex of multiple species segregated by host. Here, we formally describe the most recorded species in the complex, Hesperomyces harmoniae-parasite of the harlequin ladybird Harmonia axyridis, a globally invasive species. Using DNA isolates of Hesperomyces from multiple host species, including the host on which He. virescens was originally described (Chilocorus stigma), we found that He. harmoniae forms a single clade in our phylogenetic reconstruction of a two-locus riboso-mal dataset. Hesperomyces harmoniae is currently known from five continents and 31 countries: Canada, El Salvador, Mexico, the USA (North America); Argentina, Colombia, Ecuador (South America); Austria, Belgium, Bulgaria, Croatia, Czech Republic, France, Germany, Greece, Hungary, Italy, Luxembourg, Montenegro, The Netherlands, Poland, Romania, Russia, Serbia, Slovakia, Switzerland, the UK (Europe); South Africa (Africa); China, Japan, and Turkey (Asia).
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Ladybirds (Coleoptera: Coccinellidae) are an important beneficial group that, as other insects, are negatively affected by many human-mediated threats, including climate change, agricultural intensification, habitat loss, pollution, and biological invasions. Ecological impacts from these threats have altered the richness, abundance, and distribution of insect species, impacting their survival and compromising the numerous services they provide. The development and implementation of conservation strategies for ladybirds is hindered by a lack of knowledge of the conservation status of most species and the factors driving their population dynamics. Here we review the ecological threats faced by ladybirds, and current projects and actions that should aid the conservation and recovery of their populations. We also identify knowledge gaps in biodiversity assessment and conservation approaches, and suggest mitigating actions following Harvey et al. (2020) as a roadmap for ladybird conservation and recovery over short-, intermediate-, and long-term timescales.
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Novel species of fungi described in this study include those from various countries as follows: Antartica, Cladosporium austrolitorale from coastal sea sand. Australia, Austroboletus yourkae on soil, Crepidotus innuopurpureus on dead wood, Curvularia stenotaphri from roots and leaves of Stenotaphrum secundatum and Thecaphora stajsicii from capsules of Oxalis radicosa. Belgium, Paraxerochrysium coryli (incl. Paraxerochrysium gen. nov.) from Corylus avellana. Brazil, Calvatia nordestina on soil, Didymella tabebuiicola from leaf spots on Tabebuia aurea, Fusarium subflagellisporum from hypertrophied floral and vegetative branches of Mangifera indica and Microdochium maculosum from living leaves of Digitaria insularis. Canada, Cuphophyllus bondii from a grassland. Croatia, Mollisia inferiseptata from a rotten Laurus nobilis trunk. Cyprus, Amanita exilis on calcareous soil. Czech Republic, Cytospora hippophaicola from wood of symptomatic Vaccinium corymbosum. Denmark, Lasiosphaeria deviata on pieces of wood and herbaceous debris. Dominican Republic, Calocybella goethei among grass on a lawn. France (Corsica), Inocybe corsica on wet ground. France (French Guiana), Trechispora patawaensis on decayed branch of unknown angiosperm tree and Trechispora subregularis on decayed log of unknown angiosperm tree. Germany, Paramicrothecium sambuci (incl. Paramicrothecium gen. nov.) on dead stems of Sambucus nigra. India, Aureobasidium microtermitis from the gut of a Microtermes sp. termite, Laccaria diospyricola on soil and Phylloporia tamilnadensis on branches of Catunaregam spinosa. Iran, Pythium serotinoosporum from soil under Prunus dulcis. Italy, Pluteus brunneovenosus on twigs of broadleaved trees on the ground. Japan, Heterophoma rehmanniae on leaves of Rehmannia glutinosa f. hueichingensis. Kazakhstan, Murispora kazachstanica from healthy roots of Triticum aestivum. Namibia, Caespitomonium euphorbiae (incl. Caespitomonium gen. nov.) from stems of an Euphorbia sp. Netherlands, Alfaria junci, Myrmecridium junci, Myrmecridium juncicola, Myrmecridium juncigenum, Ophioceras junci, Paradinemasporium junci (incl. Paradinemasporium gen. nov.), Phialoseptomonium junci, Sporidesmiella juncicola, Xenopyricularia junci and Zaanenomyces quadripartis (incl. Zaanenomyces gen. nov.), from dead culms of Juncus effusus, Cylindromonium everniae and Rhodoveronaea everniae from Evernia prunastri, Cyphellophora sambuci and Myrmecridium sambuci from Sambucus nigra, Kiflimonium junci, Sarocladium junci, Zaanenomyces moderatricis-academiae and Zaanenomyces versatilis from dead culms of Juncus inflexus, Microcera physciae from Physcia tenella, Myrmecridium dactylidis from dead culms of Dactylis glomerata, Neochalara spiraeae and Sporidesmium spiraeae from leaves of Spiraea japonica, Neofabraea salicina from Salix sp., Paradissoconium narthecii (incl. Paradissoconium gen. nov.) from dead leaves of Narthecium ossifragum, Polyscytalum vaccinii from Vaccinium myrtillus, Pseudosoloacrosporiella cryptomeriae (incl. Pseudosoloacrosporiella gen. nov.) from leaves of Cryptomeria japonica, Ramularia pararhabdospora from Plantago lanceolata, Sporidesmiella pini from needles of Pinus sylvestris and Xenoacrodontium juglandis (incl. Xenoacrodontium gen. nov. and Xenoacrodontiaceae fam. nov.) from Juglans regia. New Zealand, Cryptometrion metrosideri from twigs of Metrosideros sp., Coccomyces pycnophyllocladi from dead leaves of Phyllocladus alpinus, Hypoderma aliforme from fallen leaves Fuscopora solandri and Hypoderma subiculatum from dead leaves Phormium tenax. Norway, Neodevriesia kalakoutskii from permafrost and Variabilispora viridis from driftwood of Picea abies. Portugal, Entomortierella hereditatis from a biofilm covering a deteriorated limestone wall. Russia, Colpoma junipericola from needles of Juniperus sabina, Entoloma cinnamomeum on soil in grasslands, Entoloma verae on soil in grasslands, Hyphodermella pallidostraminea on a dry dead branch of Actinidia sp., Lepiota sayanensis on litter in a mixed forest, Papiliotrema horticola from Malus communis, Paramacroventuria ribis (incl. Paramacroventuria gen. nov.) from leaves of Ribes aureum and Paramyrothecium lathyri from leaves of Lathyrus tuberosus. South Africa, Harzia combreti from leaf litter of Combretum collinum ssp. sulvense, Penicillium xyleborini from Xyleborinus saxesenii, Phaeoisaria dalbergiae from bark of Dalbergia armata, Protocreopsis euphorbiae from leaf litter of Euphorbia ingens and Roigiella syzygii from twigs of Syzygium chordatum. Spain, Genea zamorana on sandy soil, Gymnopus nigrescens on Scleropodium touretii, Hesperomyces parexochomi on Parexochomus quadriplagiatus, Paraphoma variabilis from dung, Phaeococcomyces kinklidomatophilus from a blackened metal railing of an industrial warehouse and Tuber suaveolens in soil under Quercus faginea. Svalbard and Jan Mayen, Inocybe nivea associated with Salix polaris. Thailand, Biscogniauxia whalleyi on corticated wood. UK, Parasitella quercicola from Quercus robur. USA, Aspergillus arizonicus from indoor air in a hospital, Caeliomyces tampanus (incl. Caeliomyces gen. nov.) from office dust, Cippumomyces mortalis (incl. 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In 2016–2019, seasonal changes in the abundance of the harlequin ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) were established in the city center of Prague, Central Europe, and in its outskirts. Adults were sampled from lime trees ( Tilia spp.) at regular intervals throughout the growing season. The abundance of H. axyridis paralleled the course of abundance of its prey, the aphid Eucallipterus tiliae L., which peaks either early or late in the season. As a result, the seasonal dynamics of H. axyridis were unimodal, with a peak in the early (late June—early July of 2017 and 2019) or late (late July—mid-September of 2016 and 2018) period of the season. In the early period, there was a small (1–4 days) difference in the timing of the peak of H. axyridis between the city center and the outskirts. In the late period, the peak occurred significantly earlier (by 13–21 days) in the city center due to the warmer climate there than in the outskirts. The difference in the timing of the population peak between both locations disappeared after recalculating the calendar to thermal time (number of day degrees above 10.6°C thresholds elapsed from the end of H. axyridis hibernation). The warm mesoclimate of the city center advances the seasonal dynamics of H. axyridis , contributing to the success of this invasive species in urban habitats.
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Understanding the distribution of parasites is crucial for biodiversity conservation. Here, we studied the distribution of the ectoparasitic fungus Laboulbenia formicarum in native and invasive Lasius ants in a 2000 km² area. We screened over 16,000 ant workers in 478 colonies of five different species. We found that Lab. formicarum was rare in native Lasius species but infected 58% of the colonies of the invasive species Las. neglectus. At landscape scale, Lab. formicarum presence could not be explained by geographic and genetic distances between Las. neglectus colonies but was associated with hotter and dryer climatic conditions and its prevalence in colonies increased with urbanization. Within infected colonies, fungal prevalence varied from 0 to 100 percent within meters and was negatively correlated with impervious ground cover. In a changing world, our findings emphasize the importance of land-use and climatic factors in shaping the distribution and prevalence of fungal parasites.
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Harmonia axyridis is an invasive alien ladybird in North America and Europe. Studies show that multiple natural enemies are using Ha. axyridis as a new host. However, thus far, no research has been undertaken to study the effects of simultaneous infection by multiple natural enemies on Ha. axyridis. We hypothesized that high thallus densities of the ectoparasitic fungus Hesperomyces virescens on a ladybird weaken the host's defenses, thereby making it more susceptible to infection by other natural enemies. We examined mortality of the North American-native Olla v-nigrum and Ha. axyridis co-infected with He. virescens and an entomopathogenic fungus-either Beauveria bassiana or Metarhizium brunneum. Laboratory assays revealed that He. virescens-infected O. v-nigrum individuals are more susceptible to entomopathogenic fungi, but Ha. axyridis does not suffer the same effects. This is in line with the enemy release hypothesis, which predicts that invasive alien species in new geographic areas experience reduced regulatory effects from natural enemies compared to native species. Considering our results, we can ask how He. virescens affects survival when confronted by other pathogens that previously had little impact on Ha. axyridis.
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In this paper we present an updated checklist of thallus-forming Laboulbeniomycetes (Ascomycota, Pezi-zomycotina), that is, the orders Herpomycetales and Laboulbeniales, from Belgium and the Netherlands. Two species are newly described based on morphology, molecular data (ITS, LSU ribosomal DNA) and ecology (host association). These are Hesperomyces halyziae on Halyzia sedecimguttata (Coleoptera, Coc-cinellidae) from both countries and Laboulbenia quarantenae on Bembidion biguttatum (Coleoptera, Car-abidae) from Belgium. In addition, nine new country records are presented. For Belgium: Laboulbenia aubryi on Amara aranea (Coleoptera, Carabidae) and Rhachomyces spinosus on Syntomus foveatus (Co-leoptera, Carabidae). For the Netherlands: Chitonomyces melanurus on Laccophilus minutus (Coleoptera, Dytiscidae), Euphoriomyces agathidii on Agathidium laevigatum (Coleoptera, Leiodidae), Laboulbenia fas-ciculata on Omophron limbatum (Coleoptera, Carabidae), Laboulbenia metableti on Syntomus foveatus and S. truncatellus (Coleoptera, Carabidae), Laboulbenia pseudomasei on Pterostichus melanarius (Coleoptera, Carabidae), Rhachomyces canariensis on Trechus obtusus (Coleoptera, Carabidae), and Stigmatomyces hydrel-liae on Hydrellia albilabris (Diptera, Ephydridae). Finally, an identification key to 140 species of thallus-forming Laboulbeniomycetes in Belgium and the Netherlands is provided. Based on the combined data, we are able to identify mutual gaps that need to be filled as well as weigh the impact of chosen strategies (fieldwork, museum collections) and techniques in these neighboring countries. The aim of this work is to serve as a reference for studying Laboulbeniomycetes fungi in Europe.
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The ectoparasitic fungus Hesperomyces virescens was studied on its invasive host, the harlequin ladybird Harmonia axyridis, in the Czech Republic. A primary aim was to examine the relationship between fungal infection and elytral coloration of the ladybird. Furthermore, the role of host sex and mating status of females were analyzed. Beetles (n = 1,102) were sampled during autumn migration, and then sexed, weighed, and screened for infection. Females were dissected for detection of sperm in their spermathecae. Ladybirds were sorted according to color form and absorbance spectrophotometry was used to quantify carotenoid contents in their elytra. In individuals of the nonmelanic succinea form, the degree of melanization was measured using digital photographs and putative age groups were estimated based on background color of elytra. Sexual differences in infection patterns indicated transmission during copulation: males were infected mostly on elytra and venter, and females had infection almost exclusively on elytra. Mated females had higher infection rate than virgins. There was no influence of genetic color form on the fungal infection. Putative age groups (visual sorting to yellow, orange, and red) correlated with fungal infection. Infected individuals had elevated elytral carotenoid levels in comparison to uninfected individuals, which could be explained by host age. Infection-free succinea beetles were extensively melanized because they emerged later in the season at lower temperatures which induced melanization. Overall, we highlight that H. axyridis is a multivoltine species whose age, if not taken into account in ecophysiological studies, might present a considerable confounding factor.
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This Chapter presents a review of the importance of using realistic approaches to successfully identify biocontrol agents based on their ecology and that of the fungal pathogen or pest. The major environmental hurdles are the relative range of abiotic conditions for the activity of the pathogen and the antagonist. It is thus important to have biocontrol agents which match the ecological windows of the pathogen to try and develop effective control. The use of environmental screening, dynamics of utilization of C-sources and establishment are all directly related to the ecological windows of the pathogen and the potential antagonist. In addition, the impact of extreme climatic events will further impact on the efficacy of BCAs and may require systems which can identify more resilient candidate BCAs for fungal pathogens and pest control in the near future.
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Found throughout the tree of life and in every ecosystem, parasites are some of the most diverse, ecologically important animals on Earth—but in almost all cases, the least protected by wildlife or ecosystem conservation efforts. For decades, ecologists have been calling for research to understand parasites' important ecological role, and increasingly, to protect as many species from extinction as possible. However, most conservationists still work within priority systems for funding and effort that exclude or ignore parasites, or treat parasites as an obstacle to be overcome. Our working group identified 12 goals for the next decade that could advance parasite biodiversity conservation through an ambitious mix of research, advocacy, and management.