Confirmation of Avian Dispersal of a Seed Chalcid Wasp in North America and a New Host Record for Megastigmus aculeatus (Hymenoptera Megastigmidae)

Abstract

Dispersal of chalcid wasp larvae inhabiting the seeds of angiosperms by wild birds in North America has never been verified. I describe adult Megastigmus aculeatus Swederus (Hymenoptera: Megastigmidae) that successfully emerged from seeds extracted from the droppings of six species of native North American non-captive birds. Rosa setigera is also confirmed as a host for this wasp for the first time.

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2024 THE GREAT LAKES ENTOMOLOGIST 69
Megastigmus Dalman (Hymenoptera:
Megastigmidae), is a cosmopolitan genus of
more than 150 species of tiny (<4 mm) wasps
(Janšta et al. 2018, Noyes 2019). It is be-
lieved that all of the ~25 Nearctic species are
phytophagous, with larvae that develop and
pupate entirely within the seeds of woody
plants, one insect per seed (Grissell and
Schauff 1990, Huber et al. 2021). Because
they can depress seed yields and recruit-
ment, some species are considered pests of
commercially-valuable plants, particularly
conifers and pistachios (Jarry et al. 1997,
Rice and Michailides 1988, Fabre et al. 2004,
Doğanlar et al. 2009). Understanding their
means of dispersal is an important aspect of
their ecology. These insects are weak iers,
unable to fly far under their own power
(Milliron 1949, Balduf 1959). Long-distance
movement has been attributed primarily to
passive downwind drift of adults (Jarry et
al. 1997, Lander et al. 2014) or human-me-
diated displacement of seeds (Evans 1983,
Auger-Rozenberg and Roques 2012).
Many angiosperm host plants of
Megastigmus have eshy fruits eaten by
birds, which frequently defecate the seeds
intact (Snow and Snow 1988). Yet viewing
birds as dispersal agents of fruit-inhabiting
insects has long remained speculative. Until
relatively recently, it was unclear whether
or how often birds might eat fruits infested
with insects (Valburg 1992, Traveset et al.
1995, Garcia et al. 1999), or whether insects
living in fruits could survive vertebrate gut
passage, even if the insects were inside the
seeds (Chung and Waller 1986, Sallabanks
and Courtney 1992, Guix and Ruiz 1995). A
review focusing specically on seed-inhabit-
ing insects surviving full vertebrate gut pas-
sage (Hernández 2011) provided only seven
documented examples, just four involving
birds. The insect featured in two of the bird
studies (Nalepa and Piper 1994, Hernández
2009) was the rose seed chalcid Megastigmus
aculeatus Swederus, a Eurasian species now
widely distributed around the world (Weiss
1917, Balduf 1959).
In the rst of these examples, Nalepa
and Piper (1994) collected non-native Rosa
multiora seeds (achenes) in North Carolina,
USA, and used x-rays to determine those
containing Megastigmus larvae. The au-
thors encased the occupied seeds in banana
mash within hollowed-out rose hypanthia
and fed them to a captive native Northern
Mockingbird (Mimidae: Mimus polyglottos).
Seeds passed by the bird were kept in glass
containers. From 180 seeds, nearly 90 adult
wasps emerged, which the authors identied
as the slightly smaller, darker Megastigmus
aculeatus var. nigroavus Hoffmeyer, which
may represent a valid species (Roques and
Skrzypczyńska 2003). The experiment
demonstrated that the insects could survive
avian gut passage within the seeds and
emerge successfully—suggesting that bird
dispersal of this Megastigmus could occur
in nature.
In the other example, Hernández
(2009) collected droppings from free-living
birds in Spain as part of a dietary study. Fe-
cal samples were placed in plastic bags, but
not examined for ~20 months, at which time
58 dead adult M. aculeatus were found to
have emerged from among 1,755 Rosa canina
seeds in the samples. Droppings could not be
assigned to donor bird species, but feeding
observations indicated that ~80% of visits
Conrmation of Avian Dispersal of a Seed Chalcid Wasp in
North America and a New Host Record for
Megastigmus aculeatus
(Hymenoptera: Megastigmidae)
Julie A. Craves
Department of Entomology, Michigan State University, East Lansing, MI 48824, USA
(email: jcraves@umich.edu; ORCID: 0000-0002-9391-2767).
Abstract
Dispersal of chalcid wasp larvae inhabiting the seeds of angiosperms by wild birds in
North America has never been veried. I describe adult Megastigmus aculeatus Swederus
(Hymenoptera: Megastigmidae) that successfully emerged from seeds extracted from the
droppings of six species of native North American non-captive birds. Rosa setigera is also
conrmed as a host for this wasp for the rst time.
Keywords: seed chalcid, Rosa, bird dispersal, Megstigmus, Chalcidoidea
1
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70 THE GREAT LAKES ENTOMOLOGIST Vol. 57, Nos. 1–2
to R. canina were by Eurasian Blackbirds
(Turdidae: Turdus merula), with the rest by
other Turdus species.
Reports of vertebrate dispersal of
seed-inhabiting chalcid wasps since the
review provided by Hernández (2011) have
remained sparse and involved mammals
(Rouco and Norbury 2013, Bobadilla et al.
2020). The experiment of Nalepa and Piper
(1994), with manipulated fruit fed to a single
captive bird, is apparently the only published
evidence of avian dispersal of a Megastigmus
seed chalcid wasp in North America.
Here I describe the emergence of adult
M. aculeatus var. nigroavus from seeds of
the non-native R. multiora, as well as from
Rosa seeds in the droppings of six species of
native wild birds in southeastern Michigan,
USA. I also conrm the native Rosa setigera
as a host of M. aculeatus, which was previ-
ously undocumented.
Wasps found in previously
collected seeds
As part of a larger research project,
I collected a large sample of seeds of com-
mon bird-dispersed, eshy-fruited plants in
Wayne and Washtenaw counties, in south-
eastern Michigan, USA, from 2013–2015
(Craves 2017). I kept a subset as a reference
collection, with each species in a separate
small, clear plastic, zip-top bag stored
at room temperature. In 2019, browsing
through this collection, I noticed that the bag
containing seeds of R. multiora contained
small dead wasps. Utilizing keys in Crosby
(1913), Milliron (1949), Balduf (1959), Gris-
sell and Schauff (1990), and Roques and
Skrzypczyńska (2003), I identied the wasps
as M. aculeatus, distinguished by characters
including ovipositor sheaths distinctly longer
than the body; the lack of a broad, cloudy
infuscation surrounding the stigma; and the
outer half of the axilla black. While there is
reportedly substantial variability in the col-
oration of female M. aculeatus (Nalepa and
Grissell 1993, Roques and Skrzypczyńska
2003), my specimens appeared to be iden-
tiable to M. aculeatus var. nigroavus via
the black coloration on the vertex of the head
encompassing the ocelli region and on the
dorsal surface of the abdomen (Fig. 1). Both
light-colored and dark-colored M. aculeatus
occur in North America (Balduf 1959, Nalepa
and Grissell 1993).
Of the 38 R. multiora seeds in the
bag, eight had exit holes corresponding to
eight fully-emerged adult female wasps. One
seed had an exit hole containing a partially
emerged adult wasp (Fig. 2). The rest of the
seeds were intact. Having found wasps in the
R. multiora sample, I checked the reference
sample of R. setigera, but no wasps were
present in the bag.
Figure 1. Dorsal view of a female Megastigmus aculeatus var. nigroavus showing the dark col-
oration between the eyes, the back of the head, the axilla, scutellum, and abdomen indicating it is
this dark form, which may be a valid species.
2
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2024 THE GREAT LAKES ENTOMOLOGIST 71
Wasps found in seeds extracted
from bird droppings
This interesting discovery prompted
me to go through the thousands of bird fe-
cal samples I had collected from my earlier
research on fruit in bird diets (for sample
collection methods, see Craves 2015). Nearly
all of the samples were from birds captured
in mist nets, or from birds monitored in
the same study area on the campus of the
University of Michigan-Dearborn, Wayne
County, Michigan, USA (study site details in
Craves 2009). A small number were collect-
ed during similar banding and monitoring
activities in Washtenaw County, Michigan,
ve miles west of Ann Arbor in Section 5 of
Lodi Township.
Each sample was comprised of all the
seeds in a single bird dropping, with a label
recording the donor bird species and collec-
tion date. Like the reference collection, the
samples were stored at room temperature in
small plastic bags. There were 272 samples
containing 1,473 rose seeds, and the samples
came from the following bird species: Cedar
Waxwing (Bombycillidae: Bombycilla ced-
rorum), Gray Catbird (Mimidae: Dumetella
carolinensis), Eastern Bluebird (Turdidae:
Sialia sialis), Swainson’s Thrush (Turdidae:
Catharus ustulatus), Hermit Thrush (Turdi-
dae: C. guttatus), American Robin (Turdidae:
Turdus migratorius), and Yellow-rumped
Warbler (Parulidae: Setophaga coronata).
Fifty-one of the 272 samples (18.7%)
contained dead M. aculeatus var. nigroavus
(Table 1), identical to those in the reference
samples and identied using the same keys.
The majority of the samples containing these
dead wasps (88.2%) came from American
Robins. However, wasps were found in
samples from each of the other bird species
except for the warbler. Wasps had emerged
from 104 seeds (7.1%). Again, the majority
came from seeds in samples from American
Robins (89.4%).
Verifying Rosa host species
The seeds of most Rosa are similar and
cannot be reliably distinguished, so they are
not identied to species in my samples. R.
multiora is the dominant rose at both study
sites. At the Wayne County site, R. setigera is
fairly common, and Rosa palustris is absent;
both of these species are native to North
America. At the Washtenaw County site,
both R. setigera and R. palustris (also native)
are present but uncommon. M. aculeatus
var. nigroavus has been purported to ex-
clusively use R. multiora as a host (Amrine
2002, contra Milliron 1949, Balduf 1959). To
explore this claim and clarify the source of
wasps in my samples, I collected hips from R.
setigera at both sites, and from R. palustris
in Washtenaw County, in December 2019.
I kept the R. setigera hips outdoors over
the winter, and the R. palustris hips were
refrigerated for 90 days and then kept at
room temperature. In spring 2020, 33 adult
M. aculeatus var. nigroavus emerged from
a total of 696 seeds of R. setigera collected
at the Wayne County site. This rose has not
been previously documented as a host for M.
Figure 2. Two dead Megastigmus aculeatus var. nigroavus females and vacated
Rosa multiora seeds (achenes). One seed shown with a wasp that expired before
fully emerging.
3
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72 THE GREAT LAKES ENTOMOLOGIST Vol. 57, Nos. 1–2
aculeatus or M. aculeatus var. nigroavus
(Balduf 1959, Roques and Skrzypczyńska
2003). Five Megastigmus nigrovariegatus
Ashmead, a native chalcid, emerged from a
total of 255 seeds of R. palustris; it is a known
host for this species (Milliron 1949, Balduf
1959, Roques and Skrzypczyńska 2003).
Discussion
I conrm wild bird dispersal of the
rose seed chalcid wasp M. aculeatus var.
nigroavus in North America via fecal sam-
ples assignable to donor bird species. The
six bird species whose samples produced
wasps represent most of the common frugiv-
orous bird species whose seasonal presence
overlaps with the availability of ripe rose
hips in southern Michigan, from mid- to
late September through mid-February. The
majority of the fecal samples containing
rose seeds at my sites came from American
Robins, one of the most abundant, ubiquitous
songbirds in North America, occupying a
broad range of habitats and very gregarious
in the non-breeding season (Vanderhoff et
al. 2020). Robins are highly frugivorous and
typically swallow fruit whole, passing intact
seeds (Parrish 1997, Craves 2015). These
characters make robins excellent, efcient
seed dispersers. Medium-sized birds such
as those in the families Turdidae, Mimidae,
and Bombycillidae typically disperse seeds
~100 m (Jordano et al. 2007, Wotton and
McAlpine 2015), although distances depend
on factors including bird abundance, fruiting
plant density, and gut retention time (Carlo
and Morales 2008).
Megastigmus wasps have one gen-
eration per year; they overwinter as nal
instar larvae, pupate in spring, and emerge
in summer (Milliron 1949). Some species of
Megastigmus can undergo prolonged dia-
pause for up to ve years or more (Roux et al.
1997, Fabre et al. 2004, Auger-Rozenberg et
al. 2012, Suez et al. 2013). At least four years
had elapsed between my collection of the R.
multiora seeds for the reference collection
and when I discovered the dead wasps. The
reference collection had been examined in
the interim but the wasps, if present, could
have been overlooked.
All the wasps which emerged from
seeds in fecal samples and from hips I col-
lected were female. Males are often reported
to comprise ~1% of sampled populations of
M. aculeatus (e.g., Mays and Kok 1988, Na-
lepa 1989, Amrine 2002, Hernández 2009).
This is due to thelytokous parthenogenesis,
in which unfertilized eggs develop into
females. It is known in at least eight other
Megastigmus species and is apparently in-
duced by Wolbachia, intracellular bacteria
which are widespread in invertebrates and
often manipulate host reproduction (Boivin
et al. 2014).
Rosa multiora and R. setigera are
closely related, representing two of the only
three members of Rosa Section Systylae
(Lewis et al. 2014), so perhaps use of R.
setigera as a host by M. aculeatus is not
surprising. The third member of this section
is Rosa lucieae, an Asian species introduced
in North America, often in cultivars and hy-
brids (Lewis et al. 2014). Derivatives of this
rose may be potential hosts of M. aculeatus.
New species of Megastigmus seed
chalcids continue to be detected all over the
world (Sureshan 2009, Ghramh and Shati
2011, Chen et al. 2023, Popescu and Gostin
2023), as do new distribution records for
known species, including M. aculeatus (Le-
diuk et al. 2012, Kaplan 2022, Verheyde et
al. 2023). The minute size and cryptic nature
of chalcid wasps can make them tedious to
survey or monitor using traditional collecting
methods (Noyes 1982), and seeds infested
prior to adult emergence can only be reliably
detected via x-rays (Nalepa 1992). Retaining
and examining droppings of birds (and other
Table. 1. Summary of adult Megastigmusaculeatusvar.nigroavus wasps found in Rosa
seeds (achenes) extracted from fecal samples of birds, by bird species. A “sample” refers
to a single dropping that contained Rosa seeds.
Samples
with Number of Samples Number
Bird species Rosa seeds Rosa seeds with wasps of wasps
Cedar Waxwing, Bombycilla cedrorum 8 72 1 1
Gray Catbird, Dumetella carolinensis 10 63 2 3
Eastern Bluebird, Sialia sialis 15 37 1 1
Swainson’s Thrush, Catharus ustulatus 1 7 1 1
Hermit Thrush, Catharus guttatus 17 65 1 5
American Robin, Turdus migratorius 220 1225 45 93
Yellow-rumped Warbler, Setophaga coronata 1 4 0 0
Total 272 1473 51 104
4
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2024 THE GREAT LAKES ENTOMOLOGIST 73
vertebrates) known to feed on fruits is a
low-tech add-on to studies collecting fecal
samples for dietary, population, food web,
or seed dispersal assays. Angiosperm hosts
for Megastigmus seed chalcids in the genera
Amelanchier, Ilex, Pistacia, Rosa, Schinus,
and Sorbus (Noyes 2019) all have fruits
regularly consumed by birds, making these
types of investigations ripe for discovery.
Voucher specimens. Two adult
female Megastigmus aculeatus var. nigro-
avus ex: Rosa setigera hips collected on 26
December 2019 in Dearborn, Wayne County,
Michigan, USA have been deposited in the
Albert J. Cook Arthropod Research Col-
lection at Michigan State University with
the catalog number MSUC_ARC_246428.
Specimens of Megastigmus aculeatus var.
nigroavus ex: Rosa multiora from Jackson
County, Michigan (MSUC_ARC_246429),
and Megastigmus nigrovariegatus ex: Rosa
palustris from Washtenaw County, Michi-
gan (MSUC_ARC_246430) have also been
deposited in the same collection.
Acknowledgments
The author thanks Darrin O’Brien and
Dana Wloch, who spent many hours helping
to count and collect fruit, and monitor and
band birds, and process their fecal samples.
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