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Oviposition Preference of Botanophila Flies (Diptera: Anthomyiidae) Towards Stroma Size of Epichloe¨ (Hypocreales: Clavicipitaceae) Hosts

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Oviposition Preference of Botanophila Flies (Diptera: Anthomyiidae) Towards Stroma Size of Epichloe¨ (Hypocreales: Clavicipitaceae) Hosts

K. GORZYNSKA, Z. OLSZANOWSKI,3 A. LEUCHTMANN,4 AND M. LEMBICZ1

1,2

  • ´
  • ´

Ann. Entomol. Soc. Am. 107(2): 532Ð538 (2014); DOI: http://dx.doi.org/10.1603/AN13094

ABSTRACT Stromata of grass-infecting fungi from the genus Epichlo e ¨ (Clavicipitaceae: Ascomycota) serve as a food source and egg-laying surface for ßies of genus Botanophila (Diptera: Anthomyiidae). Larger stromata should make it possible for ßies to lay more eggs and provide more food to offspring. This hypothesis was tested in four different grassÐfungus associations that occur in central

Poland. In two of these associations, Epichlo e ¨ bromicola on Elymus repens and Epichlo e ¨ typhina on

Puccinellia distans, ßies showed a preference for longer stromata, and egg density on these stromata was signiÞcantly higher than in the other two associations. A negative correlation between egg density and offspring success was observed in only one association, E. bromicola–El. repens. However, offspring success in this association did not differ signiÞcantly from offspring success in associations with lower egg density on the stromata, in which ßies showed no preference for the stroma length. Long-term observations (2000Ð2010) of ßyÐfungus interaction in the E. typhinaÐP. distans association showed that ßy preference toward stroma length may vary over time but with no clear tendency. No signiÞcant correlations were found between the larval density on a stroma and either larval weight or mortality. The results of the current study question our assumptions that egg laying depends on the stroma length and the fate of eggs laid (i.e., their hatching success and the condition, in terms of weight and survival, of the larvae) on egg density. It is possible that ßies choose stromata based on attributes other than size.

KEY WORDS Anthomyiidae, Botanophila sp., Epichlo e ¨ sp., oviposition preference

In nature, organisms always co-occur with other or- ßowers and, after hatching, larvae feed on developing ganisms from different taxa and most of these co- seeds (e.g., Pellmyr and Huth 1994, Anstett et al. occurring organisms interact with each other. At pres- 1997). Our research, which focuses on interactions ent, we know that relationships between organisms between Botanophila ßies and Epichlo e ¨ fungi (Leuchpresent a continuum of intensity and of gains and tmann 2007; Go´rzyn´ska et al. 2010, 2011; Lembicz et al. losses that vary in time and space (Bronstein 1994a,b; 2013), follows this line of study.

  • 2001). Many studies show that there are places in
  • The ancestors of those Botanophila ßies that later

space where a species does not enter any interaction became connected with Epichlo e ¨ fungi, were likely (so called “cold spots”) and places in which the rela- grass herbivores initially, similar to many modern reptionship between partners is strongest (so called “hot resentatives of the family Anthomyiidae. Those indispots”; Gomulkiewicz et al. 2000, Thompson and Cun- viduals who also ate fungal fruiting bodies called stroningham 2002). Hence, interspeciÞc interactions are mata, which appeared on grasses at some point in time,

  • difÞcult to deÞne unambiguously.
  • gained an advantage over other individuals because

A spectacular example of interactions that are cur- stromata were a richer source of nutrients than grass rently studied is the relationship between Botanophila tissues (Bultman 1995). At present, stromata of fungi ßies (Diptera: Anthomyiidae) and fungi from the ge- are the only known food source for some Botanophila nus Epichlo e ¨ (Clavicipitaceae: Ascomycota). This re- species (Kohlmeyer and Kohlmeyer 1974). However, lationship resembles interactions between some in- the Epichlo e ¨ÐBotanophila interaction is not entirely sects and ßowering plants in which insects both restricted to the feeding relationship. Botanophila fepollinate and parasitize a plant (pollinating seed par- males lay eggs on Epichlo e ¨ stromata and transfer sperasites). During pollination, insects lay eggs in visited matia of two different types in their faeces, thus enabling cross-fertilization of these heterothallic fungi (Bultman and White 1988; Bultman et al. 1995, 1998; Bultman and Leuchtmann 2008). Some volatile compounds produced by Epichlo e ¨ fungi are also known to attract ßies (Steinebrunner et al. 2008b). Botanophila ßies have long been considered the main, if not only, vector of fungal spermatia (Bultman

1 Department of Plant Taxonomy, A. Mickiewicz University, Umultowska 89, 61-614 Poznan´, Poland.

2 Corresponding author, e-mail: [email protected]. 3 Department of Animal Taxonomy and Ecology, A. Mickiewicz University, Umultowska 89, 61-614 Poznan´, Poland.

4 Plant Ecological Genetics, Institute of Integrative Biology (IBZ), Universita¨tstrasse 16, 8092 Zu¨rich, Switzerland.

0013-8746/14/0532Ð0538$04.00/0 ᭧ 2014 Entomological Society of America

March 2014

GO´ RZYN´ SKA ET AL.: OVIPOSITION PREFERENCE OF FLIES ON Epichlo e ¨ STROMATA

533

Table 1. Number of stromata collected in particular grass–fungus association and their origin

No. of collected stromata
GrassÐfungus

association

  • Site
  • Location
  • Fly taxa

2000 2001 2002 2003 2006 2008 2009 2010

55

D. glomerataÐE. typhina  Morasko 52Њ 27.857Ј N Botanophila phrenione (Se´guy)
16Њ 55.868Ј E Botanophila dissecta (Meigen)
Pakos´c´ 1 52Њ 47.531Ј N B. phrenione

30 30 30 30
30 30 30 30

  • 55
  • 127

144 146 143 149
29
145 149 150 148
130 147 147
18Њ 06.118Ј E

  • P. distansÐE. typhina
  • Janikowo 52Њ 46.384Ј N B. phrenione

67 60
30 30 30
18Њ 08.032Ј E

52Њ 46.544Ј N B. phrenione

18Њ 06.190Ј E 52Њ 47.284Ј N n.d. 18Њ 06.257Ј E

  • Giebnia
  • 30

30
Pakos´c´1

Pakos´c´ 2 52Њ 47.293Ј N B. phrenione

146
54
18Њ 06.721Ј E Taxon 1

El. repensÐE. bromicola  Pakos´c´ 1 52Њ 47.397Ј N Botanophila lobata (Collin)

18Њ 06.064Ј E Taxon 1

  • H. lanatusÐE. clarkii
  • Morasko 52؇ 27.910Ј N B. phrenione

67
16Њ 55.370Ј E

et al. 1998); thus, the insectÐfungus interaction was m2, which were located within fungus-infected grass recognized as obligatory. At present, we know that stromata can be fertilized without the ßyÕs contribution (Rao and Baumann 2004; Go´rzyn´ska et al. 2010,

2011); therefore, the fungus can reproduce sexually in the absence of the insect. However, the Botanophila life cycle depends strictly on the fungus because the ßy larvae, like the adults, feed on fungal stromata until their metamorphosis. The nutritional dependence of Botanophila larvae on fungal stromata suggests that a pregnant ßy will select larger stromata on which to lay eggs, to ensure that more food will be available to its offspring. Based on this assumption, the aim of this study was to evaluate 1) the relationships between stroma size and both ßy presence and the number of eggs laid, 2) the effect of egg density on offspring success, and 3) the effect of larval density on larval survival and weight. The investigations were conducted in four different grassÐ fungus associations. One of these associations has been observed since 2000, which made it possible to determine whether this interaction has changed over time. populations. Stromata were collected at the end of June, after the maximum number of eggs was laid. Measurements. The presence or absence of evidence of insect visits was determined based on the occurrence of eggs on stromata, which were observed under a microscope (Olympus SZ61-TR; Olympus, Tokyo, Japan). To determine the relationship between stroma length and egg number, stroma length was measured and the number of eggs on each stroma was determined. The number of eggs comprised both the number of unhatched eggs and larvae. In addition, density of insects on a stroma was determined as the mean number of eggs per 1 mm of stroma. To characterize the effect of egg density on the offspring success, the following parameters were determined for each stroma: 1) egg density per 1 mm2, 2) offspring success, expressed as the percentage of hatched eggs, and 3) stroma length. The comparison of the aforementioned traits was conducted between the four grassÐfungus associations for the stromata collected in 2010, within the Puccinellia

distans–Epichlo e ¨ typhina (P.d.ÐE.t.) association for the

years 2000Ð2010, except 2004, 2005, and 2007, and

between the P.d.ÐE.t. and Dactylis glomerataÐE. typhina (D.g.ÐE.t.) associations in the locality Pakos´c´

1 for the years 2000, 2003, 2008, and 2009. The last comparison was conducted to show whether there are any differences in the studied traits of the ßyÐfungus

Materials and Methods
Collection of Material. The research was conducted

from 2000 to 2010 and involved three fungal species occurring on four grass species in six localities situated in central Poland (Table 1). In each of these localities, Epichlo e ¨ stromata were sampled from study plots of 25 relationship, if this relationship occurs in the same

Table 2. Presence of Botanophila eggs on fungal stromata and the relationship between stroma length and egg presence in each grass–fungus association in 2010

Stroma lenght (mm) Ϯ SD
GrassÐfungus

association
Egg presence

n (%)
N

P LeveneÕs test

t

df

P

  • Eggs present
  • No eggs

P.d.ÐE.t. D.g.ÐE.t. El.r.ÐE.b. H.l.ÐE.c.

440 130
54
134 (30.4) 115 (88.5)
54 (100)
17.23 Ϯ 3.85 48.19 Ϯ 13.37 28.50 Ϯ 4.91 31.36 Ϯ 5.16
14.85 Ϯ 3.79 45.20 Ϯ 14.18
Ð
NS NS Ð
6.04 0.81 NS
438 128 Ð
Ͻ0.001 NS Ð

  • NS
  • 67
  • 11 (16.4)
  • 28.63 Ϯ 6.81
  • NS
  • 1.26
  • 65

P.d.ÐE.t., Puccinellia distansÐEpichlo e ¨ typhina; D.g.ÐE.t., Dactylis glomerata–Epichlo e ¨ typhina; H.l.ÐE.c., Holcus lanatusÐEpichlo e ¨ clarkii; El.r.Ð E.b., Elymus repens–Epichlo e ¨ bromicola.

534

ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA

Vol. 107, no. 2

Table 3. Correlation between stroma length and Botanophila egg number and between egg density and offspring success in each grass–fungus association in 2010

GrassÐfungus association
Stroma length Ϯ SD
Egg density Ϯ SD
Offspring success Ϯ SD

N

Egg no. Ϯ SD

  • r
  • P
  • N
  • r
  • P

P.d.ÐE.t. D.g.ÐE.t. El.r.ÐE.b. H.l.ÐE.t.

440 130
54
15.58 Ϯ 3.96 47.84 Ϯ 13.45 28.50 Ϯ 4.91 29.07 Ϯ 6.61
0.34 Ϯ 0.56 2.06 Ϯ 1.52 1.91 Ϯ 0.94 0.21 Ϯ 0.51
0.291 0.158 0.474 0.198
Ͻ0.001 NS Ͻ0.001 NS
134 115
54
0.07 Ϯ 0.02 0.05 Ϯ 0.03 0.07 Ϯ 0.03 0.04 Ϯ 0.01
0.70 Ϯ 0.44 0.76 Ϯ 0.36 0.87 Ϯ 0.22 0.27 Ϯ 0.47
Ϫ0.073
0.003 Ϫ0.412
0.708
NS NS Ͻ0.01

  • Ͻ0.05
  • 67
  • 11

locality, with the contribution of the same fungal spe- 3) larval density and weight, and 4) larval density and cies but involves a different host grass species. mortality. All statistical analyses were conducted using In 2010, in the locality Pakos´c´ 1, 33 stromata of E. Statistica v. 8.0 software (Statistica, Tulsa, OK).

typhina from D. glomerata and 27 stromata of Epichlo e ¨ bromicola from Elymus repens were collected to de-

Results

termine the effect of larval density on larval survival and weight. For each stroma the following parameters

Stroma Size—Egg Number. In 2010, the number of

were determined: 1) size, 2) the number of live larvae, fungal stromata with ßy eggs differed signiÞcantly 3) the number of dead larvae, 4) the number of eggs between the four studied grassÐfungus associations

2
3

before hatching, and 5) the number of eggs (un- (␹ ϭ 224.5; P Ͻ 0.001). The highest number of hatched eggs and larvae). Egg and larval density (per stromata with eggs (100%) was recorded in the pop1 mm2), larval mortality rate (the ratio of dead larvae ulation of El. repens infected with E. bromicola (El.r.Ð to the total number of larvae), and offspring success E.b.), while the lowest number of stromata with eggs (the ratio of hatched eggs to the total number of eggs) was found in the population of Holcus lanatus (Table were calculated. Live larvae were collected from stro- 2). The correlation between ßy presence and stromata mata and weighed with an accuracy of 0.0001 g on a length was statistically signiÞcant only for the P.d.ÐE.t.

  • laboratory balance (A&D, HM-120).
  • association, in which insects more frequently visited

Statistical Analyses. The correlation between a longer stromata (t438 ϭ 6.04; P Ͻ 0.0.001; Table 2). A nominal variable (group afÞliation) and quantitative signiÞcant correlation between stroma length and variable (differences in egg density, offspring success, number of eggs laid was found in the P.d.ÐE.t. (r ϭ and larval weight, and the relationship between ßy 0.291; Nϭ440; PϽ0.001) and El.r.ÐE.b. (rϭ0.291; Nϭ presence on a stroma and stroma length) was deter- 54; P Ͻ 0.001) associations (Table 3). mined using either the t-test for independent vari- In long-standing observations of the infected popables, when two groups were compared, or one-way ulations of P. distans, signiÞcant differences in the analysis of variance (ANOVA), when more than two number of stromata with eggs were found between

2

groups were compared. If signiÞcant results were individual years (␹ ϭ 331.8; P Ͻ 0.001). The per-

7

found, post hoc Tukey HSD tests were performed. centage of stromata with eggs exceeded 50% only in Before the analyses were conducted, the assumptions one year (2003), while in other years, this value was of both tests were checked. The KolmogorovÐSmirnov highly variable, reaching its minimum in 2001 (1.36%) test was performed to check normal distribution, (Table 4). A signiÞcant positive connection between while the LeveneÕs test was used to check for a ho- stroma length and ßy presence was found in four out mogeneity of variance in groups. WelchÕs t-test was of eight years of observations (Table 4).The correlaused when variations were not homogeneous. Pear- tion between stroma length and egg number was sigsonÕs correlation analysis was performed to check the niÞcant in Þve out of eight years (Table 5). relationship between 1) the number of eggs and In all studied vegetative seasons, except 2002, egg stroma length, 2) offspring success and stroma length, density differed signiÞcantly between the E. typhina

Table 4. Presence of Botanophila eggs on fungal stromata and the relationship between stroma length and egg presence in the P. distans–E. typhina association for the years 2000–2010

Stroma lenght (mm) Ϯ SD
Egg presence

n (%)

Year

N

P LeveneÕs test

t

df

P

  • Eggs present
  • No eggs

  • 2000
  • 127

147 120 120
60
731 592 440
2,337
59 (46.46)
2 (1.36) 8 (6.67)
69 (57.50)
7 (11.67)
68 (9.3) 74 (9.3)
134 (30.45) 421 (18.01)
14.53 Ϯ 2.82 12.00 Ϯ 2.83 13.75 Ϯ 2.55 16.68 Ϯ 3.09 13.14 Ϯ 2.48 14.06 Ϯ 3.29 13.45 Ϯ 3.33 17.23 Ϯ 3.85 15.44 Ϯ 3.71
11.19 Ϯ 2.40 15.63 Ϯ 3.08 12.64 Ϯ 2.77 16.02 Ϯ 2.73 12.70 Ϯ 2.63 12.46 Ϯ 3.21 11.37 Ϯ 2.83 14.85 Ϯ 3.79 12.85 Ϯ 3.46
NS Ð
7.21 Ð
125 Ð117 118
58
729 590 438
2334
Ͻ0.001 ÐNS NS NS Ͻ0.001 Ͻ0.001 Ͻ0.001 Ͻ0.001

2001a

  • 2002
  • NS

NS NS NS NS NS NS
1.10 1.20 0.42 3.85 5.75 6.04
13.71
2003 2006 2008 2009 2010 Overall

a There were not enough cases in one group to conduct analysis.

March 2014

GO´ RZYN´ SKA ET AL.: OVIPOSITION PREFERENCE OF FLIES ON Epichlo e ¨ STROMATA

535

Table 5. Correlation between stroma length and Botanophila egg number and between egg density and offspring success in the P. distans–E. typhina association for the years 2000–2010

Year
2000

N

Stroma length Ϯ SD Egg no. Ϯ SD

  • r
  • P
  • N

Egg density Ϯ SD Offspring success Ϯ SD

  • R
  • P

127 147 119 120
60
731 592 440
12.77 Ϯ 3.09 15.58 Ϯ 3.10 12.71 Ϯ 2.76 16.41 Ϯ 2.95 12.75 Ϯ 2.59 12.61 Ϯ 3.25 11.63 Ϯ 2.97 15.57 Ϯ 3.96 13.32 Ϯ 3.65
0.76 Ϯ 1.00 0.01 Ϯ 0.12 0.09 Ϯ 0.37 0.78 Ϯ 0.81 0.13 Ϯ 0.39 0.09 Ϯ 0.30 0.14 Ϯ 0.40 0.34 Ϯ 0.56 0.22 Ϯ 0.52
0.59 Ͻ0.001 59 Ϫ0.14
0.03 0.19 Ͻ0.05 0.10 NS 0.15 Ͻ0.001 68 0.21 Ͻ0.001 74 0.29 Ͻ0.001 134 0.27 Ͻ0.001 420
0.11 Ϯ 0.05 0.07 Ϯ 0.00 0.11 Ϯ 0.06 0.08 Ϯ 0.03 0.09 Ϯ 0.02 0.08 Ϯ 0.02 0.09 Ϯ 0.05 0.07 Ϯ 0.02 0.08 Ϯ 0.04
0.20 Ϯ 0.38 0.00 Ϯ 0.00 0.25 Ϯ 0.46 0.58 Ϯ 0.44 0.00 Ϯ 0.00 0.51 Ϯ 0.50 0.45 Ϯ 0.49 0.70 Ϯ 0.44 0.52 Ϯ 0.48
Ϫ0.23 NS Ϫ0.44
0.08 NS 0.027 Ϫ0.16 Ϫ0.07
NS NS NS NS NS NS NS NS
2001 2002 2003 2006 2008 2009 2010
NS NS
18
69
7

Overall 2,336
Ϫ0.21 Ͻ0.001

  • stromata from two co-occurring populations, P. distans
  • Offspring success in the populations of P. distans

and D. glomerata, in the locality Pakos´c´ 1. Each year, differed signiÞcantly between the years of observathe egg density was higher on the stromata from D. tions (F7,412 ϭ 9.61; P Ͻ 0.001). No signiÞcant correglomerata population (Table 6). In both associations, lation between egg density and offspring success in a signiÞcant relationship between the number of ßy individual years was recorded (Table 5). However, eggs and stroma length was found only in 2009; in this when data from all years were considered the correyear, ßies visited the longer stromata more frequently lation was signiÞcant (r ϭ Ϫ0.21; N ϭ 420; P Ͻ 0.001). (Table 7). These data showed that the higher egg density, the less

Egg Density and Offspring Success. In 2010, the eggs hatch.

  • offspring success of Botanophila eggs on the stromata
  • Offspring success differed signiÞcantly between the

growing on H. lanatus (H.l.ÐE.c.) was signiÞcantly two co-occurring grass populations in the locality higher than with the other plant species (F3,310 ϭ 7.99; Pakos´c´ 1 in each studied growing season, except 2006. P Ͻ 0.001). In both the P.d.ÐE.t. and D.g.ÐE.t. associ- In the Þrst two years, offspring success was higher in ations, no correlation was found between offspring D.g.–E.t., whereas in the last two years it was higher in success and egg density, while in the El.r.ÐE.b. asso- P.d.ÐE.t. (Table 8). The correlation between offciation, offspring success increased as egg density de- spring success and egg density in both associations creased (P ϭ 0.708; N ϭ 11, P Ͻ 0.05; Table 3). Con- in each year was not statistically signiÞcant, nor was versely, in the H.l.ÐE.c. association, offspring success the correlation signiÞcant between these parameincreased with egg density (P ϭ 0.708; N ϭ 11, P Ͻ ters from the overall data from all the years of the

  • 0.05).
  • study (Table 9).

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    BULLETIN OF THE Dipterists Forum Bulletin No. 84 Autumn 2017 Affiliated to the British Entomological and Natural History Society Bulletin No. 84 Autumn 2017 ISSN 1358-5029 Editorial panel Bulletin Editor Darwyn Sumner Assistant Editor Judy Webb Dipterists Forum Officers Chairman Rob Wolton Vice Chairman Howard Bentley Secretary Amanda Morgan Meetings Treasurer Phil Brighton Please use the Booking Form downloadable from our website Membership Sec. John Showers Field Meetings Field Meetings Sec. vacancy Now organised by several different contributors, contact the Secretary. Indoor Meetings Sec. Martin Drake Publicity Officer Erica McAlister Workshops & Indoor Meetings Organiser Conservation Officer vacant Martin Drake [email protected] Ordinary Members Bulletin contributions Stuart Ball, Malcolm Smart, Peter Boardman, Victoria Burton, Please refer to guide notes in this Bulletin for details of how to contribute and send your material to both of the following: Tony Irwin, Martin Harvey, Chris Raper Dipterists Bulletin Editor Unelected Members Darwyn Sumner 122, Link Road, Anstey, Charnwood, Leicestershire LE7 7BX. Dipterists Digest Editor Peter Chandler Tel. 0116 212 5075 [email protected] Secretary Assistant Editor Amanda Morgan Judy Webb Pennyfields, Rectory Road, Middleton, Saxmundham, Suffolk, IP17 3NW 2 Dorchester Court, Blenheim Road, Kidlington, Oxon. OX5 2JT. [email protected] Tel. 01865 377487 [email protected] Treasurer Phil Brighton [email protected] Dipterists Digest contributions Deposits for DF organised field meetings to be sent to the Treasurer Dipterists Digest Editor Conservation Peter Chandler Robert Wolton (interim contact, whilst the post remains vacant) 606B Berryfield Lane, Melksham, Wilts SN12 6EL Tel. 01225-708339 Locks Park Farm, Hatherleigh, Oakhampton, Devon EX20 3LZ [email protected] Tel.
  • Chapter 12. Biocontrol Arthropods: New Denizens of Canada's

    Chapter 12. Biocontrol Arthropods: New Denizens of Canada's

    291 Chapter 12 Biocontrol Arthropods: New Denizens of Canada’s Grassland Agroecosystems Rosemarie De Clerck-Floate and Héctor Cárcamo Agriculture and Agri-Food Canada, Lethbridge Research Centre 5403 - 1 Avenue South, P.O. Box 3000 Lethbridge, Alberta, Canada T1J 4B1 Abstract. Canada’s grassland ecosystems have undergone major changes since the arrival of European agriculture, ranging from near-complete replacement of native biodiversity with annual crops to the effects of overgrazing by cattle on remnant native grasslands. The majority of the “agroecosystems” that have replaced the historical native grasslands now encompass completely new associations of plants and arthropods in what is typically a mix of introduced and native species. Some of these species are pests of crops and pastures and were accidentally introduced. Other species are natural enemies of these pests and were deliberately introduced as classical biological control (biocontrol) agents to control these pests. To control weeds, 76 arthropod species have been released against 24 target species in Canada since 1951, all of which also have been released in western Canada. Of these released species, 53 (70%) have become established, with 18 estimated to be reducing target weed populations. The biocontrol programs for leafy spurge in the prairie provinces and knapweeds in British Columbia have been the largest, each responsible for the establishment of 10 new arthropod species on rangelands. This chapter summarizes the ecological highlights of these programs and those for miscellaneous weeds. Compared with weed biocontrol on rangelands, classical biocontrol of arthropod crop pests by using arthropods lags far behind, mostly because of a preference to manage crop pests with chemicals.
  • Diptera : Anthomyiidae)

    Diptera : Anthomyiidae)

    Title SOME ANTHOMYIID FLIES FROM MONEGROS, SPAIN (DIPTERA : ANTHOMYIIDAE) Author(s) Suwa, Masaaki; Blasco-Zumeta, Javier Insecta matsumurana. New series : journal of the Faculty of Agriculture Hokkaido University, series entomology, 60, Citation 43-54 Issue Date 2003-12 Doc URL http://hdl.handle.net/2115/9917 Type bulletin (article) File Information 60_p43-54.pdf Instructions for use Hokkaido University Collection of Scholarly and Academic Papers : HUSCAP INSECTA MATSUMURANA NEW SERIES 60: 43-54 DECEMBER 2003 SOME ANTHOMYIID FLIES FROM MONEGROS, SPAIN (DIPTERA: ANTHOMYIIDAE) By MASAAKl SUWA and JAVIER BLASCO-ZUMETA Abstract SUWA, M. and BLASCO-ZUMETA, J. 2003. Some anthomyiid flies from Monegros, Spain (Diptera: Anthomyiidae). Ins. matsum. n. s. 60: 43-54, 20 figs. Ninteen species ofAnthomyiidae are recorded from Monegros, Spain. One ofthem, Botanophila sp., seems to be an undescribed species closely related to B. turcica (Hennig), though it is not given a name as the single available secimen is severely damaged. Delia echinata (Seguy), a widely distributed species in the Holarctic region, is recorded as new to the mainland of Spain. Among the species dealt with here coprophagous or saprophagous species are comparatively rich. Authors' addresses. M. SUWA: Systematic Entomology, Graduate School ofAgriculture, Hokkaido University, Sapporo, 060-8589 Japan; J. BLASCO-ZUMETA: Hispanidad 8, 50750 Pina de Ebro, Zaragoza, Spain. 43 INTRODUCTION The Anthomyiidae are mostly known from temperate to subarctic ranges in the northern hemisphere. They have well been investigated in Europe, especially in central and northern parts, and about 460 species have been recorded from Europe as a whole. The Spanish fauna of Anthomyiidae has, however, rather poorly been investigated, about 60 or a little more species being known to occur in the mainland (Czerny & Strobl, 1909; Hennig, 1966- 1976; Ackland, 1977; Michelsen & Baez, 1985).
  • The Botanophila–Epichloë Association in Cultivated Festuca in Oregon: Evidence of Simple Fungivory S

    The Botanophila–Epichloë Association in Cultivated Festuca in Oregon: Evidence of Simple Fungivory S

    Blackwell Publishing, Ltd. The Botanophila–Epichloë association in cultivated Festuca in Oregon: evidence of simple fungivory S. Rao1,*, S.C. Alderman2, J. Takeyasu1 & B. Matson2 1Department of Crop & Soil Science, Oregon State University, Corvallis OR 97331, USA; 2USDA-ARS, National Forage Seed Production Research Center, Corvallis, OR 97331, USA Accepted: 14 February 2005 Key words: Festuca rubra, fine fescue, exotic fungus, Epichloë festucae, fly–fungus interaction, choke disease, Oregon, Diptera, Anthomyiidae, Ascomycetes, Clavicipitaceae, Botanophila lobata Abstract We investigated the Botanophila (Diptera: Anthomyiidae)–Epichloë (Ascomycetes: Clavicipitaceae) interaction in cultivated Festuca spp. (fine fescue) in Oregon in western USA. Epichloë spp. are endo- phytic fungi of grasses in the subfamily Pooideae. They develop a felt-like stroma on the surface of grass culms and a dense mycelium within the culms that typically prevents seed head emergence. As a result, seed yields are suppressed, and hence the disease is known as choke. Studies of Epichloë spp. on wild grasses indicate that the fly–fungus interaction is an obligatory mutualism. During oviposi- tion, Botanophila transfers Epichloë spermatia between stromata of opposite mating types, and the perithecia that develop after fungal fertilization serve as food for Botanophila larvae. In the current study, we surveyed 19 cultivated fields of Festuca spp. in Oregon, and observed choke caused by Epichloë festucae Leuchtmann, Schardl and Siegl in 10 of these. However, perithecia were observed in only four fields, and on only 1.0–2.6% of stromata. Perithecial development was also low, and rarely covered 50% of the stroma surface. Despite the absence or low frequency of fertilized stromata, Botanophila lobata Collin larvae were present in all choke-infested fields.
  • The Occurrence and Preference of Botanophila Flies (Diptera: Anthomyiidae) for Particular Species of Epichloë Fungi Infecting Wild Grasses

    The Occurrence and Preference of Botanophila Flies (Diptera: Anthomyiidae) for Particular Species of Epichloë Fungi Infecting Wild Grasses

    Eur. J. Entomol. 110(1): 129–134, 2013 http://www.eje.cz/pdfs/110/1/129 ISSN 1210-5759 (print), 1802-8829 (online) The occurrence and preference of Botanophila flies (Diptera: Anthomyiidae) for particular species of Epichloë fungi infecting wild grasses MARLENA LEMBICZ1, KAROLINA GÓRZYŃSKA1, ZIEMOWIT OLSZANOWSKI2, VERNER MICHELSEN3 and ADRIAN LEUCHTMANN4 1 Department of Plant Taxonomy, A. Mickiewicz University, Umultowska 89, 61-614 Poznań, Poland; e-mails: [email protected]; [email protected] 2 Department of Animal Taxonomy and Ecology, A. Mickiewicz University, Umultowska 89, 61-614 Poznań, Poland; e-mail: [email protected] 3 Zoological Museum, Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark; e-mail: [email protected] 4 ETH Zürich, Plant Ecological Genetics, Institute of Integrative Biology (IBZ), Universitätstrasse 16, 8092 Zürich, Switzerland; e-mail: [email protected] Key words. Diptera, Anthomyiidae, Botanophila, egg morphology, fungi, Clavicipitaceae, Epichloë, molecular phylogeny, Poland Abstract. Specific associations between species frequently occur in ecological interactions. The aim of this study was to determine the preferences of anthomyiid flies of the genus Botanophila for particular species of fungi as sites for laying eggs and as food for both larvae and adults. The associations of their eggs, larvae and flies with the stromata of different species of Epichloë fungi infecting 7 species of grass in Poland were analyzed. Scanning electron microscopy of the surface of their eggs and an analysis of the genetic sequences of their mitochondrial cytochrome oxidase (COII) were used to identify the taxa of the flies studied. Three types of eggs were distinguished based on their shape, colour and the presence of dorsal folds and sculpturing on the shells.
  • Field Guide for the Biological Control of Weeds in Eastern North America

    Field Guide for the Biological Control of Weeds in Eastern North America

    US Department TECHNOLOGY of Agriculture TRANSFER FIELD GUIDE FOR THE BIOLOGICAL CONTROL OF WEEDS IN EASTERN NORTH AMERICA Rachel L. Winston, Carol B. Randall, Bernd Blossey, Philip W. Tipping, Ellen C. Lake, and Judy Hough-Goldstein Forest Health Technology FHTET-2016-04 Enterprise Team April 2017 The Forest Health Technology Enterprise Team (FHTET) was created in 1995 by the Deputy Chief for State and Private Forestry, USDA, Forest Service, to develop and deliver technologies to protect and improve the health of American forests. This book was published by FHTET as part of the technology transfer series. http://www.fs.fed.us/foresthealth/technology/ Cover photos: Purple loosestrife (Jennifer Andreas, Washington State University Extension), Galerucella calmariensis (David Cappaert, Michigan State University, bugwood.org), tropical soda apple ((J. Jeffrey Mullahey, University of Florida, bugwood.org), Gratiana boliviana (Rodrigo Diaz, Louisiana State University), waterhyacinth (Chris Evans, University of Illinois, bugwood.org), Megamelus scutellaris (Jason D. Stanley, USDA ARS, bugwood.org), mile-a-minute weed (Leslie J. Mehrhoff, University of Connecticut, bugwood.org), Rhinoncomimus latipes (Amy Diercks, bugwood.org) How to cite this publication: Winston, R.L., C.B. Randall, B. Blossey, P.W. Tipping, E.C. Lake, and J. Hough-Goldstein. 2017. Field Guide for the Biological Control of Weeds in Eastern North America. USDA Forest Service, Forest Health Technology Enterprise Team, Morgantown, West Virginia. FHTET-2016-04. In accordance with

  • Diptera) Morphology, Taxonomy, Identification and Distribution

    ISSN 0044-5088 Zoologica Original Contributions to Zoology, founded in 1888 Ed. H.F. Paulus, Vienna Volume 162 " N" Manual of Central European Muscidae (Diptera) Morphology, taxonomy, identification and distribution sample pages E Schweizerbart Science Publishers eschweizerbart_xxx Zoologica Original Contributions to Zoology Founded 1888 by R. Leuckart, C. Chun, continued by W. Kükenthal, R. Hesse, W.E. Ankel Edited by Hannes F. Paulus Volume 162 František Gregor, Rudolf Rozkošný, Miroslav Barták and Jaromír Vaňhara Manual of Central European Muscidae (Diptera) Morphology, taxonomy, identification, and distribution with 54 plates sample pages Schweizerbart Science Publishers Stuttgart • 2016 eschweizerbart_xxx František Gregor, Rudolf Rozkošný, Miroslav Barták and Jaromír Vaňhara: Manual of Central European Muscidae (Diptera): Morphology, taxonomy, identification, and distribution Authors’ addresses: František Gregor, 638 00 Brno, Loosova 14, Czech Republic Rudolf Rozkošný and Jaromír Vaňhara, Masaryk University, Faculty of Science, Department of Botany and Zoology 611 37 Brno, Kotlářská 2, Czech Republic, [email protected] , [email protected] Miroslav Barták, Czech University of Life Sciences, Faculty of Agrobiology, Food and Natural Resources, Department of Zoology and Fisheries, 165 21 Praha 6 – Suchdol, Czech Republic, [email protected] We would be pleased to receive your comments on the content of this book: [email protected] Front cover: Hydrotaea ignava, female, orig. F. Gregor Reviewed by: Dr. A.C. Pont, Oxford University, Great Britain ISBN 978-3-510-55049-4 ISSN 0044-5088 Information on this title: www.schweizerbart.com/9783510550494 © 2016 E. Schweizerbart’sche Verlagsbuchhandlung (Nägele u. Obermiller), Stuttgart, Germany All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical photocopying, recording, or otherwise, without the prior written permission of E.
  • Botanophila Flies, Vectors of Epichloë Fungal Spores, Are Infected by Wolbachia

    Botanophila Flies, Vectors of Epichloë Fungal Spores, Are Infected by Wolbachia

    Research Collection Journal Article Botanophila flies, vectors of Epichloë fungal spores, are infected by Wolbachia Author(s): Pagel, Lydia; Bultman, Thomas L.; Górzyńska, Karolina; Lembicz, Marlena; Leuchtmann, Adrian; Sangliana, Anne; Richards, Nicola Publication Date: 2019 Permanent Link: https://doi.org/10.3929/ethz-b-000328708 Originally published in: Mycology 10(1), http://doi.org/10.1080/21501203.2018.1515119 Rights / License: Creative Commons Attribution 4.0 International This page was generated automatically upon download from the ETH Zurich Research Collection. For more information please consult the Terms of use. ETH Library Mycology An International Journal on Fungal Biology ISSN: 2150-1203 (Print) 2150-1211 (Online) Journal homepage: https://www.tandfonline.com/loi/tmyc20 Botanophila flies, vectors of Epichloë fungal spores, are infected by Wolbachia Lydia Pagel, Thomas Bultman, Karolina Górzyńska, Marlena Lembicz, Adrian Leuchtmann, Anne Sangliana & Nicola Richards To cite this article: Lydia Pagel, Thomas Bultman, Karolina Górzyńska, Marlena Lembicz, Adrian Leuchtmann, Anne Sangliana & Nicola Richards (2019) Botanophila flies, vectors of Epichloë fungal spores, are infected by Wolbachia, Mycology, 10:1, 1-5, DOI: 10.1080/21501203.2018.1515119 To link to this article: https://doi.org/10.1080/21501203.2018.1515119 © 2018 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group. Published online: 08 Sep 2018. Submit your article to this journal Article views: 175 View Crossmark data Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=tmyc20 MYCOLOGY 2019, VOL. 10, NO. 1, 1–5 https://doi.org/10.1080/21501203.2018.1515119 Botanophila flies, vectors of Epichloë fungal spores, are infected by Wolbachia Lydia Pagela, Thomas Bultman*a, Karolina Górzyńskab, Marlena Lembiczb, Adrian Leuchtmannc, Anne Sanglianaa and Nicola Richardsd aBiology Department, Hope College, Holland, MI, USA; bDepartment of Plant Taxonomy, A.