Laboulbeniales (Ascomycota) of the Boston Harbor Islands I:
Species Parasitizing Coccinellidae and Staphylinidae,
with Comments on Typification
Danny Haelewaters, Serena Y. Zhao, André De Kesel, Rebecca E. Handlin, Isabel R. Royer, Brian D. Farrell, and Donald H. Pfister
Northeastern Naturalist, Volume 22, Issue 3 (2015): 459–477
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2015
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2015 NORTHEASTERN NATURALIST 22(3):459–477
Laboulbeniales (Ascomycota) of the Boston Harbor Islands I:
Species Parasitizing Coccinellidae and Staphylinidae,
with Comments on Typification
Danny Haelewaters1,*, Serena Y. Zhao1, André De Kesel2, Rebecca E. Handlin1,
Isabel R. Royer3, Brian D. Farrell4, and Donald H. Pfister1
Abstract - This paper, based on a recent comprehensive sampling of insects, is the first
report of Laboulbeniales from the New England region since the 1930s. We present 7 new
records of laboulbenialean parasites on Staphylinidae (rove beetles) and Coccinellidae (lady
beetles) from the Boston Harbor Islands National Recreation Area. These are Clonophoromyces
nipponicus Terada & I.I. Tav., Hesperomyces virescens Thaxt., Ilyomyces cf. mairei
F. Picard, Laboulbenia philonthi Thaxt., Peyritschiella protea Thaxt., Stichomyces conosomatis
Thaxt., and Teratomyces actobii Thaxt. One of these parasite species, C. nipponicus,
has not been found previously outside of its type locality in Japan. Examination of Roland
Thaxter’s 1891–1932 slides led to the designation of lectotypes for L. philonthi, P. protea,
S. conosomatis, and T. actobii. The following synonymy is established: Teratomyces brevicaulis
Thaxt. = T. actobii. In addition, we discovered new localities for H. virescens (from
Canada, Cuba, Guatemala, and Japan) and L. philonthi (from Canada, Grenada, Panama,
Trinidad, and Venezuela).
Introduction
Existing museum collections provide host specimens from a wide range of collection
locations and dates for the study of arthropod ectoparasites. Collections
made in the context of an all taxa biodiversity inventory (ATBI) provide sample
populations from host collections that should exhibit minimal bias in parasite distribution
and diversity. Parasite density for obligate ectoparasites can be determined
because they are fairly easily observed on the exoskeleton of a given host; these
parasites persist on dead individuals, and thus, historical collections of infected
hosts serve as records of species relationships and population dynamics through
time. They also provide a measure of parasite abundances and host usage across a
single habitat or system. In this paper, we present fungal parasites of 2 host families
collected in a survey of all arthropods in an island system.
The Order Laboulbeniales
The Laboulbeniales form an order of fungi (phylum Ascomycota, class
Laboulbeniomycetes) that obligately parasitize arthropod hosts. They are
1Farlow Herbarium of Cryptogamic Botany, Harvard University, 22 Divinity Avenue,
Cambridge, MA 02138. 2Botanic Garden Meise, Domein van Bouchout, 1860 Meise, Belgium.
3Lexington High School, 251 Waltham Street, Lexington, MA 02421. 4Museum of
Comparative Zoology, Harvard University, 26 Oxford Street, Cambridge, MA 02138. *Corresponding
author - dhaelewaters@fas.harvard.edu.
Manuscript Editor: David H. Richardson
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ectoparasites, that is, they occur externally on various parts of the insect. Phylogenetic
analyses of DNA sequences indicate that the class Laboulbeniomycetes,
which also includes the order Pyxidiophorales, is sister to the Sordariomycetes—a
clade that includes saprotrophs and pathogens of plants, animals, and fungi, and
that generally produce perithecia (Blackwell and Malloch 1989, Schoch et al.
2009, Weir and Blackwell 2001).
Roland Thaxter, a professor at Harvard University (Cambridge, MA) from 1891
to 1932, undertook the first systematic study of the Laboulbeniales, and his 5 monographic
volumes (1896, 1908, 1924, 1926, 1931) and many non-illustrated papers are
still among the most-often cited papers in Laboulbeniales research. Despite Thaxter’s
intense local collecting activities, there is no evidence that he explored the sites now
included in the Boston Harbor Islands (BHI) National Recreation Area.
The Laboulbeniales lack hyphae and, unique among related fungi, they exhibit
determinate growth resulting in a well-defined thallus, which can be interpreted as a
reduced hyphal system (Santamaría 1998, Tavares 1985). Thalli are often less than
300 μm in length, and consist of a receptacle with a perithecium or multiple perithecia
and appendages bearing antheridia, which produce spermatia. (Some species in
the genera Aporomyces, Laboulbenia, and Rickia, however, seem to lack antheridia
[Rossi and Santamaria 2008, 2015; Thaxter 1926]. We currently do not know how
these fungi reproduce.) The thallus attaches to the host integument at the foot cell,
and at least some species form haustoria—simple or branched rhizoidal structures
that penetrate the host’s integument to provide additional stability and surface area
for nutrient uptake (Benjamin 1971; Gäumann and Dodge 1928; Thaxter 1896,
1908). Presumably, haustoria penetrate the host’s integument to make contact with
the cavity (haemocoel) and draw nutrient material from it. Although only observed
in some genera, it is thought that all Laboulbeniales produce haustoria whether
simple and minute or well developed (Benjamin 1971).
Laboulbeniales species can be monoecious (with both male and female sexual
organs on the same thallus) or dioecious (with separate female and male thalli),
and they rely on host contact to disperse their sticky, 2-celled ascospores (De Kesel
1993, 1995). Most Laboulbeniales exhibit a high degree of host specificity, with a
host spectrum ranging from a single species to several related or congeneric species
(De Kesel 1996, Majewski 1994, Scheloske 1969, Tavares 1985, Thaxter 1896).
Phylogenetically unrelated insects living together in the same microhabitat (e.g., in
ant nests or saltmarshes; Blum 1924, De Kesel and Haelewaters 2014) may become
infected by the same species of Laboulbeniales. This finding implies that the parasite’s
success is dependent on host characteristics as well as environmental features
(De Kesel 1996).
Although some studies have suggested that insects infected with Laboulbeniales
do not experience adverse effects on their fitness (Benjamin 1971, Scheloske 1969,
Whisler 1968), negative effects on hosts have been reported (Báthori et al. 2015;
Kamburov et al. 1967; Riddick 2006, 2010; Strandberg and Tucker 1974). Laboulbeniales
can alter reproductive behaviors of infected hosts, such as oviposition
patterns (Strandberg and Tucker 1974), and cause injury to the host’s appendages
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and abdominal tissues (Gemeno et al. 2004, Thaxter 1908). Some researchers have
suggested that heavily infected hosts with high numbers of thalli on the head, eyes,
antennae, mouthparts, legs, and/or elytra may no longer be able to detect food efficiently,
mate, or behave as predators (Nalepa and Weir 2007, Scheloske 1969).
Laboulbeniales have also been implicated in playing an influential role in the population
dynamics of their hosts (Kamburov et al. 1967).
Laboulbeniales infect hosts selectively across the phylum Arthropoda, including
representatives of the subphyla Cheliceriformes (order Acari; mites), Myriapoda
(class Diplopoda; millipedes), and Hexapoda (class Insecta; true insects) (Haelewaters
et al. 2012, Weir and Hammond 1997). The majority of known Laboulbeniales
parasitize 9 orders among the Insecta: Blattodea (cockroaches and termites), Coleoptera
(beetles), Dermaptera (earwigs), Diptera (true flies), Hemiptera (true bugs),
Hymenoptera (bees, wasps, and ants), Mallophaga (bird lice), Orthoptera (crickets
and allies), and Thysanoptera (thrips). Note that termites, previously ranked in the
order Isoptera, were recently included in the order Blattodea, based on phylogenetic
data (Beccaloni and Eggleton 2013). Although undeniably diverse, about 80% of
the known fungal-parasite species are found on beetles (Weir and Hammond 1997).
Parasite prevalence, often used as a measure for population dynamics of Laboulbeniales,
is reportedly highest in species that overwinter as adults, have overlapping
generations, form dense or continuous stable populations, and live in moist, damp
habitats (De Kesel et al. 2011, Huldén 1983; recent examples in De Kesel 2011 and
Wang et al., in press).
The family Coccinellidae includes species with aggregating behavior and overwintering
patterns that are conducive to infection by Laboulbeniales (De Kesel
2011), and the family Staphylinidae includes the most commonly infected taxa in
both the tropics and temperate regions (Weir and Hammond 1997).
Methods
The Harvard Museum of Comparative Zoology houses a collection of the
Coccinellidae and Staphylinidae from the BHI that includes 1431 individuals
representing more than 85 species. These specimens were collected for the ATBI
from 13 islands using a variety of methods: litter sampling; pitfall, malaise, light,
and bowl traps; and hand collecting (for details, see Rykken and Farrell 2013).
We examined pinned insects under dissecting microscopes at 10–50x magnification
to record the diversity of the Laboulbeniales on their hosts. When we found
infected insects, we removed individual fungal thalli from the host using Minuten
Pins (BioQuip #1208SA, Rancho Dominguez, CA) inserted onto wooden rods.
We removed thalli or groups of thalli at the foot and then mounted them in eosin
dye in glycerol (1 g eosin powder per 2 ml 25% glycerol), PVA Mounting Medium
(BioQuip #6371A), or Amann solution (Benjamin 1971). We placed a tiny
amount of Hoyer’s medium on each slide with the tip of a Minuten pin, positioned
thalli in the Hoyer’s, allowed the specimen to dry briefly, and placed a drop of
the mounting medium on the cover slip, which was then dropped sideways onto
the Hoyer’s medium. In this way, the briefly fixed, dried thalli remained in place
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when we added the cover slip, which was ringed with transparent or white nail
varnish. We viewed mounted specimens at 400–1000x magnification for identification
using numerous relevant systematic and taxonomic sources (listed in
the Literature Cited). Slides are deposited at the Farlow Herbarium (FH; Harvard
University, Cambridge, MA).
Study site: Boston Harbor Islands
BHI consists of 34 islands and peninsulas in waters near Boston, MA. The islands
range in size from 3 to 150 ha and lie as far as 20 km from shore. The islands
support a variety of habitats, including marine and estuarine intertidal wetlands and
freshwater marshes (Tiner et al. 2003). The vegetation of the islands reflects succession
after varying levels of human disturbance, and individual island floras are
heavily influenced by usage history (Elliman 2005). Although fungi have not been
specifically targeted in surveys of the islands, the invertebrates of the BHI are well
documented (Rykken and Farrell 2013).
An ATBI, initiated by the National Park Service in 2005, sought to document
all species inhabiting the islands, with particular attention to Arthropoda. The
documented diversity of the BHI (Rykken and Farrell 2013) likely captures the true
diversity of the islands. We expected lower diversity relative to the mainland, as is
commonly found in island ecosystems (Gillespie and Roderick 2002) because of the
islands’ geographic isolation, small size, and level of human disturbance (Davidson
et al. 2011). Island areas and distances from the mainland are available at the National
Park Service website (http://www.nps.gov/boha/).
Results
We screened 253 Coccinellidae, 27 (10.7%) of which were infected with
Laboulbeniales, and 1178 Staphylinidae, 20 (1.7%) of which were infected. For an
overview of the BHI sites with Laboulbeniales records, see Figure 1.
Screening records by host are included in the Supplementary Materials (see
Supplemental File 1, available online at https://www.eaglehill.us/NENAonline/
suppl-files/n22-3-N1361-Haelewaters-s1, and for BioOne subscribers, at http://
dx.doi.org/10.1656/N1361.s1).
In the course of the study we also found new localities for Hesperomyces virescens
Thaxt. (from Canada, Cuba, Guatemala, and Japan) and Laboulbenia philonthi
Thaxt. (from Canada, Grenada, Panama, Trinidad, and Venezuela).
Taxonomy
Clonophoromyces nipponicus Terada & I.I. Tav. (Fig. 2), Transactions of the
Mycological Society of Japan 34:357 (1993)
Distribution and hosts. Previously known only from Japan, where it was found
on Bryoporus gracilis (Sharp, 1888) (Staphylinidae, Tachyporinae) (Terada and
Tavares 1993).
New records from the BHI. Suffolk County, THOMPSON ISLAND, 42º18'47"N,
71º0'33.6"W, 3–13 July 2007, J. Rykken, on Bryoporus testaceus LeConte,
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1863, MCZ-ENT00601078, slides FH 00313408 (6 thalli from left metatarsus),
FH 00313409 (2 thalli from sternites), FH 00313410 (2 thalli from tergites),
FH 00313411 (1 thallus from left tarsus III), and FH 00313412 (4 thalli from tergites);
same data, MCZ-ENT00601079, slide FH 00313511 (1 adult thallus from
left elytron); Suffolk County, THOMPSON ISLAND, 42º18'47"N, 71º0'33.6"W,
6–13 June 2007, J. Rykken, on Bryoporus testaceus, MCZ-ENT00601092, slides
FH 00313413 (3 thalli from tergites), FH 00313414 (1 thallus from mouthparts),
and FH 00313413 (5 thalli from legs).
Figure 1. Overview of the Boston Harbor. Islands in grey and black are part of the Boston
Harbor Islands National Recreation Area. Those in black have been reported in this paper:
B = Bumpkin Island, C = Calf Island, G = Grape Island, GB = Great Brewster Island, L =
Langlee Island, S = Snake Island, T = Thompson Island, and W = World’s End peninsula.
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Remarks. Species of Clonophoromyces Thaxt. are rarely collected. To date, 2
species have been described, both of which are known from their type locality only
(Terada and Tavares 1993, Thaxter 1931). The genus is characterized by cell II-carrying
secondary axes, each of which produces a perithecium and accessory axes on the
second cell. Clonophoromyces nipponicus differs from C. grenadinus Thaxt. in many
characters (summarized in Terada and Tavares 1993), the most striking of which is
that each secondary axis in C. nipponicus produces 2 accessory axes and a perithecium
rather than the 1 accessory axis and a perithecium produced by C. grenadinus.
Figure 2. Clonophoromyces nipponicus from Bryoporus testaceus (Coleoptera, Staphylinidae).
A: Adult thallus with broken primary axis, only basal part of cell III is left (slide FH
00313511). B: Young thallus with several developing secondary axes on cell II (slide
FH 00313415). C: Young thallus with broken foot and intact primary axis (slide FH
00313409). Scale bar = 50 μm.
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The material from the BHI is nearly identical to the original description of
C. nipponicus, except for cell I. In North American thalli, cell I is widely suffused
with dark brown color, whereas in the Japanese thalli, cell I is only colored strictly
at the base (Terada and Tavares 1993). Color variation, however, is a seldom-used
character for distinguishing species.
Hesperomyces virescens Thaxt., Proceedings of the American Academy of Arts
and Sciences 25:264 (1891)
≡ Stigmatomyces virescens (Thaxt.) Thaxt., Proceedings of the American Academy
of Arts and Sciences 29:106 (1894)
= Hesperomyces hyperaspidis Thaxt., Memoirs of the American Academy of Arts
and Sciences 16:111 (1931)
Distribution and hosts. Described on Chilocorus stigma (Say, 1835) [as C. bivulnerus]
(Coccinellidae, Coccinellinae) from California, US. This is a widespread
species known from all continents except Antarctica, hosted by several genera of
Coccinellidae (reviewed in Ceryngier et al. 2012, Santamaría et al. 1991).
New records from the BHI. Plymouth County, WORLD’S END PENINSULA,
42º15'51.9"N, 70º52'37.8"W, 16 August 2006, J. Rykken, on Harmonia axyridis
(Pallas, 1773), MCZ-ENT00602410, slide FH 00313516 (8 adult thalli from left
elytron); Plymouth County, LANGLEE ISLAND, 42º15'38.6"N, 70º53'13.3"W,
7–8 September 2005, J. Rykken, on H. axyridis, MCZ-ENT00602433, slide FH
00313517 (12 thalli from right elytron); Plymouth County, LANGLEE ISLAND,
42º15'37.2"N, 70º53'11.4"W, 21 September 2005, J. Rykken, on H. axyridis, MCZENT00602435,
slide FH 00313518 (11 thalli from right elytron); Suffolk County,
CALF ISLAND, 42º20'28"N, 70º53'46"W, 19 June 2007, J. Rykken, on H. axyridis,
MCZ-ENT00602436, slide FH 00313519 (6 thalli from right elytron); Plymouth
County, LANGLEE ISLAND, 42º15'37.2"N, 70º53'11.4"W, 7–8 September 2005,
J. Rykken, on H. axyridis, MCZ-ENT00602441, slide FH 00313520 (3 thalli
from tip of right elytron); Plymouth County, BUMPKIN ISLAND, 42º16'51"N,
70º53'58"W, 10–19 July 2006, M. Wheat, on H. axyridis, MCZ-ENT00602442,
slide FH 00313521 (9 adult thalli from right elytron); Suffolk County, THOMPSON
ISLAND, 42º19'2"N, 71º0'31"W, 9 October 2006, B. Farrell & OEB10, on
H. axyridis, MCZ-ENT00602484, slide FH 00313522 (6 adult thalli from tip of left
elytron); same data, MCZ-ENT00602487, slide FH 00313523 (22 thalli from tip
of left elytron); Plymouth County, WORLD’S END PENINSULA, 42º15'39.7"N,
70º52'14.5"W, 6–20 July 2006, J. Rykken, on Psyllobora vigintimaculata (Say,
1824), BHI-010084, slide FH 00313107 (2 thalli).
Additional new records (non-BHI). CANADA, Québec, Berthierville, 4 August
1917, G. Maheux, on Hippodamia tredicimpunctata tibialis (Say, 1824), D.
Haelew. 526, in Collection d’insectes du Québec (CIQ), slide FH 00313524 (9 adult
thalli from elytral tips); CUBA, Santiago de Cuba Province, Parque Nacional de
Baconao, Gran Piedra, no date, no collector, on Cycloneda sanguinea (L., 1763),
D. Haelew. 614, in American Museum of Natural History collection, slide FH
00313529 (3 thalli from left elytron); GUATEMALA, Huehuetenango Department,
La Laguna, 15º45'48.1"N, 91º50'56.9"W, 9 May 2013, R.S. Zack, on Cycloneda
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sanguinea sanguinea (L., 1763), D. Haelew. 167, in James Entomology Collection
of Washington State University, slides FH 00313509 (9 thalli from left elytron) and
FH 00313510 (17 thalli from left elytron); JAPAN, Hokkaido Prefecture, Hokuto,
Murayama, 1918, no collector, on Propylea sp., D. Haelew. 555, in Collection
d’insectes du Québec (CIQ), slides FH 00313527 (5 thalli from tip of right elytron),
and FH 00313528 (7 adult thalli from tip of right elytron).
Remarks. On the Boston Harbor Islands, H. virescens has only been found on
the native Psyllobora vigintimaculata and the invasive Harmonia axyridis (Multicolored
Asian Lady Beetle). Infection rates are 3.2% (n = 34) and 20.6% (n = 126),
respectively.
Other lady beetle species at the BHI were found uninfected: Anatis labiculata
(Say, 1824) (n = 1); Brachiacantha ursina (Fabricius, 1787) (n = 2); Coccinella
septempunctata L., 1758 (n = 34); Coleomegilla maculata (DeGeer, 1775) (n = 10);
Cycloneda munda (Say 1835) (n = 8); Hippodamia convergens Guérin-Menéville,
1842 (n = 2); H. variegata (Goeze, 1777) (n = 14); Hyperaspis binotata (Say,
1826) (n = 4); and Propylea quatuordecimpunctata (L., 1758) (n = 18). Of these,
C. septempunctata, C. munda, and H. convergens have been previously observed
with H. virescens in the US (Harwood et al. 2006, Thaxter 1931). The genera Brachiacantha
Dejean, 1837; Hyperaspis Redtenbacher, 1844; and Propylea Mulsant,
1846 are known to host H. virescens (Ceryngier et al. 2012). The native C. maculata
has been found with Hesperomyces coleomegillae W. Rossi & A. Weir and Hesperomyces
palustris W. Rossi & A. Weir in Costa Rica, Cuba, Ecuador, and the US
(Goldmann et al. 2013; D. Haelewaters, unpubl. data).
On 2 slides (FH 00313516 and FH 00313517) taken from H. axyridis, we found
thalli with long median outgrowths of the perithecial tip together with thalli having
short median outgrowths. This observation has also been made on Adalia bipunctata
(L., 1758) from French Guyana (Bernardi et al. 2014) and Cycloneda sanguinea
sanguinea (L., 1763) from Guatemala (this study).
Ilyomyces cf. mairei F. Picard, Bulletin Scientifique de la France et de la Belgique
50:446 (1917)
Distribution and hosts. Described from France on Stenus elegans Rosenhauer,
1856 (Staphylinidae, Steninae) and subsequently only reported on Stenus aceris
Stephens, 1833 from France (Balazuc’s material, originally labelled as I. lavagneii
(F. Picard) F. Picard; Santamaría 2003), on Stenus sp. from Spain (Santamaría,
1992), and on Stenus clavicornis (Scopoli, 1763) from the US (Haelewaters 2013).
Record from the BHI. Suffolk County, THOMPSON ISLAND, 42°18'59.6"N,
71°0'39.9"W, 3 July 2007, J. Rykken, on Stenus clavicornis (Scopoli, 1763),
MCZ-ENT00601500, slides FH 00313250 (7 juvenile thalli from elytra) and FH
00313251 (1 juvenile thallus from elytra).
Remarks. The first and only record for North America, 8 thalli of I. cf. mairei
were found on 1 specimen of S. clavicornis from Thompson Island (MCZENT00601500),
collected in 2007 (Haelewaters 2013). Stenus rove beetles are
common in riparian habitats but only very rarely are reported with Laboulbeniales
(Santamaría 2003). Prior studies reported the genus Ilyomyces on representatives
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of the subfamily Steninae (Coleoptera, Staphylinidae) from France (Picard 1917,
Santamaría 2003), Spain (Santamaría 1992, 2003), and Indonesia (Weir 1995), with
I. mairei previously only known in Europe (Picard 1917; Santamaría 1992, 2003).
Ilyomyces cf. mairei in North America is reported on Stenus clavicornis, a congener
of its European hosts, S. aceris and S. elegans. Stenus clavicornis is native to
Europe and has been known in North America since 1968 (Majka and Klimaszewski
2008). Ilyomyces species have been reported on several Stenus species in Europe,
and this incidence at the BHI likely represents either unintended co-colonization
of North American habitats by the staphylinid host and its fungal parasite; host
pursuit, in which host-range expansions are followed by the parasite from the same
origin populations; or host-shift events, although this would imply that the parasite
Figure 3. Laboulbenia
philonthi from Philonthus
carbonarius (Coleoptera,
Staphylinidae). A: Adult
thallus, showing scar of
the trichogyne (arrowhead)
(slide FH 00313515). B,
C: Juvenile thalli (slide FH
00313515). Scale bar = 100
μm.
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was already present in the US on another (ecologically) similar host, which as yet
has not been proven (De Kesel and Haelewaters 2014, Haelewaters 2015, Nicholls
et al. 2010, Roy et al. 2011).
Laboulbenia philonthi Thaxt. (Fig. 3), Proceedings of the American Academy of
Arts and Sciences 28:174 (1893)
Lectotype, designated here. USA, Massachusetts, Belmont/Waltham, Waverley
neighborhood, “April 23, 1813” [sic], no collector, on Philonthus sp., slide FH
00313494 (5 adult thalli). We recorded the collection date as written by Thaxter,
but infer the collecting year to be 1893 based on surrounding materials.
Distribution and hosts. So far reported in Europe from: Austria, Czech Republic,
France, Germany, Great Britain, Greece, Italy, Latvia, Lithuania, the Netherlands,
Poland, and Spain; as well as from Korea, Turkey, Argentina, Ecuador, Guatemala,
Mexico, and the US (Haelewaters et al. 2014, Majewski 2008, Santamaría et al.
1991). It parasitizes representatives of the genus Philonthus Stephens, 1829, and
related genera (Staphylinidae, Staphylininae).
New records from the BHI. Suffolk County, CALF ISLAND, 42º20'25.5"N,
70º53'48.9"W, 28 August–4 September 2007, J. Rykken, on Philonthus lomatus
Erichson, 1840, MCZ-ENT00601709, slide FH 00313392 (3 juvenile and
3 adult thalli from tergites); Norfolk County, GRAPE ISLAND, 42º16'7.4"N,
70º55'14.7"W, 2–10 July 2008, S.W. Cho, on P. lomatus, MCZ-ENT00601705,
slides FH 00313512 (1 juvenile thallus from tergite) and FH 00313513 (4
thalli from tergites); Plymouth County, BUMPKIN ISLAND, 42º16'52.4"N,
70º54'8.1"W, 23–30 August 2006, M. Wheat, on Philonthus carbonarius
(Gravenhorst, 1802), MCZ-ENT00601692, slide FH 00313520 (2 adult thalli
from tergite); Suffolk County, GREAT BREWSTER ISLAND, 42º19'58.2"N,
70º53'48.3"W, 24 July–2 August 2006, R. Becker, on P. carbonarius, MCZENT00601693,
slide FH 00313515 (11 thalli from tergites).
Additional new records (non-BHI). CANADA, Québec, Granby, 4 July 1939,
P.E. Mercier, on Philonthus aurulentus Horn, 1884, D. Haelew. 535, in Collection
d’insectes du Québec (CIQ), slides FH 00313525 (1 juvenile and 4 adult thalli
from tergites) and FH 00313526 (1 juvenile and 5 adult thalli from right metatibia);
GRENADA, Saint Andrew Parish, Grand Etang, no date, no collector, on Philonthus
sp., Thaxter 2923, slide FH 00313495 (1 juvenile and 10 adult thalli from “tip
abdomen”); TRINIDAD, Port of Spain, no date, no collector, on Philonthus sp.,
Thaxter 2865, slide FH 00313496 (7 juvenile thalli); PANAMA, termite nest, no
date, no collector, on Philonthus sp., Thaxter 3197, slide FH 00313497 (2 adult
thalli); VENEZUELA, Los Chorros, no date, L.R. Reynolds (communicated by
F.J. Psota to R. Thaxter), on Philonthus sp., Thaxter 3394, slide FH 00313498 (13
thalli); same data, on Oligotergus fasciatus (Nordmann, 1837) [as Philonthus segmentarius],
Thaxter 3396, slide FH 00313499 (13 adult or submature thalli); same
data, on Oligotergus fasciatus (Nordmann, 1837) [as Philonthus anceps], Thaxter
3395, slide FH 00313500 (27 thalli).
Remarks. Thaxter (1896, 1908) collected this species only on the American
continent, with records from the New England region, California, and Florida in
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the US; and from Mexico and Guatemala. Hence, the suggestion was made that
L. philonthi “appears to be strictly American” (Thaxter 1908), which is not the
case as exemplified by the more recent numerous records across 3 climate zones
in Europe: subboreal (De Kesel and Krastina 2006), temperate (Haelewaters et al.
2014, Majewski 2009, Santamaría et al. 1991), and mediterranean to subtropical
(Santamaría et al. 1991). Between the time of Thaxter (1908) and this study, only 1
American collection has been made, in Ecuador (Proaño Castro and Rossi 2008).
Because Thaxter (1893, 1896, 1908) designated no type specimen, we decided
to re-examine Thaxter’s slides of L. philonthi, which are deposited at FH.
This led to our selection of a slide to serve as lectotype.
Study of Thaxter’s material also revealed new, unpublished records of this species
for Grenada, Trinidad, Panama, and Venezuela, and extends the total thallus
length recognized for this species. In his original description, Thaxter (1893) stated
that the total length from foot to perithecial tip was 290–360 μm. Thalli from Poland
and the Iberian Peninsula measure up to about 550 μm (Majewski 1994) and 558 μm
(Santamaría 1998). The Venezuelan material, however, provided us with the longest
thalli observed so far, up to 830 μm in length (slide FH 00313498). Thaxter (1908)
mentioned that L. philonthi is the common species on Philonthus spp. in temperate
South America, which may be supported by the current new records.
Peyritschiella protea Thaxt. (Fig. 4), Proceedings of the American Academy of
Arts and Sciences 35:427 (1900)
Lectotype, designated here. GERMANY, Freistaat Thüringen, no date, no
collector, on Bledius tricornis (Herbst, 1784), Thaxter 392, in British Museum collection,
slide FH 00313501 (9 thalli from legs).
Distribution and hosts. Recorded on the following staphylinid genera: Anotylus
Thomson, 1859; Bledius Samouelle, 1819; Manda Blackwelder, 1952;
Oxytelus Gravenhorst, 1802; Planeustomus Jacquelin du Val, 1857; Styloxys
Gozis, 1886 (subfamily Oxytelinae). The genus Philonthus Stephens, 1829 (subfamily
Staphylininae) is mentioned as a host only twice, from Poland and Tibet
(Lee 2006, Majewski 1994). Peyritschiella protea is widespread in Europe (Santamaría
et al. 1991), but seldom reported from other continents: Asia (Tibet [Lee
et al. 2006]), Africa (Algeria [Maire 1920]), and North America (Cambridge, MA,
US [Thaxter 1908]).
New records from the BHI. Suffolk County, GREAT BREWSTER ISLAND,
42º20'1.7"N, 70º53'48.1"W, 14–21 June 2006, J. Rykken, on Anotylus insecatus
(Gravenhorst, 1806), MCZ-ENT00601478, slides FH 00313424 (2 thalli from
tergites) and FH 00313425 (4 thalli from last tergite); Suffolk County, GREAT
BREWSTER ISLAND, 42º19'58.2"N, 70º53'48.3"W, 24 July–2 August 2006,
R. Becker, on A. insecatus, MCZ-ENT00601477, slides FH 00313426 (10 thalli
from tergites) and FH 00313427 (3 thalli from head); Suffolk County, GREAT
BREWSTER ISLAND, 42º20'1.7"N, 70º53'48.1"W, 14–21 June 2006, J. Rykken,
on A. insecatus, MCZ-ENT00601479, slides FH 00313428 (1 thallus from right
elytron) and FH 00313429 (1 thallus from left elytron); Suffolk County, GREAT
BREWSTER ISLAND, 42º20'1.7"N, 70º53'48.1"W, 21–28 June 2006, S. Madden,
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on A. insecatus, MCZ-ENT00601472, slide FH 00313430 (1 thallus from pygidium).
Remarks. This is the second report of this species in the US. The first collection
was made at the Fresh Pond (Cambridge, MA) and consists of a single (!) thallus
(slide FH 00313502).
Figure 4. Peyritschiella protea from Anotylus insecatus (Coleoptera, Staphylinidae).
A: Adult thallus with 1 perithecium arising from the fourth layer of the receptacle (slide FH
00313424). B: Adult thallus with 1 perithecium produced at the third layer of the receptacle,
another perithecium at the fourth layer (slide FH 00313424). Scale bar = 50 μm.
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2015
471
Stichomyces conosomatis Thaxt., Proceedings of the American Academy of Arts
and Sciences 37:38 (1901)
Lectotype, designated here. USA, Massachusetts, Belmont/Waltham, Waverley
neighborhood, October 1901, R. Thaxter, on Sepedophilus littoreus (L., 1758), slide
FH 00313505 (11 thalli; 2 fully adult, others in different stages of development).
Distribution and hosts. On species of the genus Sepedophilus Gistel, 1856
(Staphylinidae, Tachyporinae) in various European countries: Belgium, Great
Britain, the Netherlands, Poland, and Spain; as well as in North America (US),
South America (Ecuador), Africa (Algeria), and Asia (Japan) (Bernardi et al. 2014,
Haelewaters et al. 2012, Majewski 2008).
New records from the BHI. Suffolk County, GREAT BREWSTER ISLAND,
42º19'59.3N, 70º53'46.1"W, 23–30 August 2006, J. Rykken, on Sepedophilus testaceus
(Fabricius, 1792), MCZ-ENT00601267, slide FH 00313423 (3 thalli from
left-hand side of pronotum); Norfolk County, GRAPE ISLAND, 42º16'15.3"N,
70º55'2.7"W, 2–10 July 2008, S.W. Cho, on S. testaceus, MCZ-ENT00601268,
slide FH 00313432 (1 adult thallus from right elytron).
Remarks. Among Thaxter’s material, there is a series of 9 slides of S. conosomatis,
labeled as having been collected in Belmont and Waverley, both in close
proximity in eastern Massachusetts. Collections in this series were made in 1900
and 1901, and we assume that Thaxter had all 9 slides available when he made the
description of S. conosomatis (Thaxter 1901). Because the slide that Thaxter indicated
as holotype (FH 00313506, unpublished) is in unsatisfactory condition, we
decided to designate a lectotype (= FH 00313505).
This species was commonly found on Sepedophilus littoreus (L., 1758) [as
Conosoma pubescens; see Herman 2001 for the complex taxonomic history of this
species] in the New England states (Thaxter 1901, 1931). This is the first published
record from the US since Thaxter’s contributions.
Most thalli of S. conosomatis have only 1 perithecium and 0, 1, or 2 perithecial
primordia. Both Tavares (1985) and Majewski (1994) described the development
of secondary perithecia upon the cell above cell II. Since cell III never bears
perithecia, this cell should be considered cell II'. Of the examined thalli on slide
FH 00313423, 2 thalli have a perithecial primordium in addition to a normal (but
broken) perithecium, both borne on cell II; in the other thallus, the third cell of the
receptacle axis (cell II') gives rise to the single perithecium.
Teratomyces actobii Thaxt., Proceedings of the American Academy of Arts and
Sciences 29:98 (1894)
= Teratomyces atropurpureus Maire, Bulletin de la Société d'histoire naturelle
d'Afrique du Nord
11:145 (1920)
= Teratomyces brevicaulis Thaxt., Proceedings of the American Academy of Arts
and Sciences 29:99 (1894), syn. nov.
Lectotype, designated here. USA, Maine, Kittery Point, 18 August 1893, [R.
Thaxter], on Erichsonius nanus (Horn, 1884) [as Actobius], slide FH 00313507
(1 thallus).
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2015 Vol. 22, No. 3
Distribution and hosts. Described from the US on Erichsonius nanus (Horn,
1884) [as Actobius nanus] (Staphylinidae, Staphylininae). Also reported from
various European countries (Huggert and Eriksson 2010, Santamaría et al. 1991),
Algeria (Maire 1920), and Sri Lanka (Thaxter 1931) on different species of Erichsonius
Fauvel, 1874 and Parerichsonius Coiffait 1963.
New records from the BHI. Suffolk County, SNAKE ISLAND, 42º22'0.4"N,
70º58'44.3"W, 25 September 2007, J. Rykken, on Erichsonius brachycephalus
Frank, 1975, MCZ-ENT00601563, slides FH 00313356 (3 juvenile thalli from tergite),
FH 00313357 (1 juvenile thallus from last tergite), FH 00313358 (1 juvenile
thallus from penultimate tergite).
Remarks. Of several available slides of collections from Kittery Point, ME,
in agreement with the original description (Thaxter 1894), slide FH 00313507 is in
good condition and contains a thallus with diagnostic characters. This specimen is
designated above as the lectotype.
The genus Teratomyces Thaxt. consists of 10 species, 9 described by Thaxter
(1893, 1894, 1896, 1900, 1901, 1931) and 1 by Rossi (2010). Additionally, 2 collections
of Teratomyces have been made that are undescribed (New Zealand [Hughes
et al. 2004], Bolivia [Weir and Rossi 2001]). Identification of species is difficult in
this genus. Species delimitation is based on characters such as receptacle structure
and color, length of cell VI, number of perithecia, and length and color of appendage;
these characters can vary among thalli from a single host specimen (Hughes et
al. 2004). The extent of morphological variability is often subject to debate in its
use in defining species limits, especially when “morpho-species” occur on a single
host specimen.
Although our material from the BHI is immature, the receptacle structure and
especially the typical variability in blackening make us believe that it belongs to
T. actobii (Thaxter 1896). Thaxter (1931) stated that T. actobii was a common species
in the New England area, where he collected it several times in Maine (Kittery
Point) and Massachusetts (Arlington). Other species of Teratomyces present in
New England are T. mirificus on Acylophorus pronus Erichson, 1840; T. quedianus
on Hemiquedius ferox (LeConte, 1878) [as Quedius]; and T. brevicaulis on Erichsonius
nanus [as Actobius]. In T. quedianus, cell II is elongate, tapering downwards;
its blackening typically extends to the basal part of cell III. These characteristics
separate it clearly from T. actobii. The distinction between the latter species and
T. brevicaulis is based on the size of cell VI (stalk cell of perithecium) and the
larger clavate appendage cells in T. brevicaulis. Confusion arises because both species
are sometimes found on a single host specimen (Thaxter 1896). In all of the
Thaxter slides we examined, the distinction between T. actobii and T. brevicaulis as
described by Thaxter is clear except for 1 record on Erichsonius basalis Motschulsky,
1858 [as Actobius] from Sri Lanka (slide FH 00313508; see Thaxter 1931);
these specimens combine features of T. actobii (the receptacle varies from hyaline
to black) and of T. brevicaulis (having a short cell VI and slender perithecium of
T. brevicaulis. For this reason, we consider T. actobii and T. brevicaulis to be synonyms
thereby accepting considerable within-species morphological variability.
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Both names were introduced in the same publication (Thaxter 1894). We choose
to use the T. actobii for this species over T. brevicaulis because this name has been
more widely used. We were unable to find any position-relatedness for either of the
two forms; both were removed from legs and abdomen.
Generating DNA-sequence data will be the final key to unlock the phylogenetic
relationship among morpho-species in Teratomyces.
Discussion
These observations are the first to document the Laboulbeniales of the Boston
Harbor Islands, and the first reports of Laboulbeniales on Coccinellidae and Staphylinidae
in the New England area since the time of Roland Thaxter (1858–1932).
The study of Laboulbeniales can bring new insight to the community dynamics
of host–parasite interactions. Insects disperse with their parasites; thus, there is potential
for infection of native hosts by infected introduced insect species. Although
more research is needed, we hypothesize that host pursuit (Nicholls et al. 2010)
followed by host shift is the mechanism at play in (the distribution of) Ilyomyces
cf. mairei on the BHI.
Helmus et al. (2014, references therein) demonstrated that the acceleration
of global shipping has increased establishment rates of exotic species, including
beetles. The rapid and far-reaching transport of these beetles provides increased opportunities
for dispersal together with their associated fungi. In addition, Humans
often actively transport and spread insects used or studied for biological control.
The study of obligate and non-motile ectoparasites of insects, such as the Laboulbeniales,
provides an avenue to document effects of human-mediated host dispersal
on parasite dynamics and distributions. However, further research is needed to fully
characterize the diversity of the Laboulbeniales. Advances in molecular methods
for the Laboulbeniales will no doubt accelerate determinations of parasite identities
and host relationships.
In this study, we documented new records and revised species ranges from a
relatively well-sampled region. With more thorough documentation of species
diversity, future studies should characterize the mechanisms governing the distribution
of these fascinating fungal parasites. With respect to Laboulbeniales
research, the BHI collection at the Harvard Museum of Comparative Zoology is
still largely unexplored. Of the Laboulbeniales discussed in the present paper,
some species were previously known from the US (H. virescens) or specifically
from New England (L. philonthi, P. protea, S. conosomatis, T. actobii). Others
had not been reported from North America (I. cf. mairei, C. nipponicus) and are
new records for the continent. We found the Laboulbeniales on the predicted
host genera. Bryoporus testaceus, Hippodamia tredicimpunctata tibialis, and
Stenus clavicornis are new host species for C. nipponicus, H. virescens, and I. cf.
mairei, respectively.
Future work will include screening the Carabidae and other families in the BHI
collection, as well as continued sampling on the Boston Harbor Islands.
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2015 Vol. 22, No. 3
Acknowledgments
The National Park Service at the Boston Harbor Islands National Recreation Area
is acknowledged for facilitating the ATBI during which the host insects were collected.
The National Park Service issued our scientific research and collecting permit (#BOHA-
2012-SCI-0009). Thanks are due to Ina Kodra (Harvard College) and Edgar Franck
(University of Massachusetts Boston) for mounting some of the above-mentioned specimens;
Katherine LoBuglio (Harvard University) and Marc Albert (Boston Harbor Islands
Stewardship Program) for support and valuable input to the manuscript; and Mario
Fréchette (Ministry of Agriculture, Fisheries and Food in Quebec, Canada) and Louis Hesler
(US Department of Agriculture) for identification of lady beetles. A study trip to the Collection
d'insectes du Québec was supported by graduate student funding to D. Haelewaters
from the Department of Organismic and Evolutionary Biology at Harvard University.
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