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Megaselia scalaris (Diptera: Phoridae): an opportunistic endoparasitoid of the endangered
Mexican redrump tarantula, Brachypelma vagans (Araneae: Theraphosidae)
Author(s): Salima Machkour-M'Rabet, Ariane Dor, and Yann Hénaut
Source: Journal of Arachnology, 43(1):115-119.
Published By: American Arachnological Society
DOI: http://dx.doi.org/10.1636/B14-28.1
URL: http://www.bioone.org/doi/full/10.1636/B14-28.1
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SHORT COMMUNICATION
Megaselia scalaris (Diptera: Phoridae): an opportunistic endoparasitoid of the endangered Mexican
redrump tarantula, Brachypelma vagans (Araneae: Theraphosidae)
Salima Machkour-M’Rabet
1
,Ariane Dor
2
and Yann He´naut
3
:
1
Laboratorio de Ecologı
´a Molecular y Conservacio´n,
GAIA-BIO, El Colegio de la Frontera Sur (ECOSUR). Av. del Centenario Km. 5.5, C.P. 77014, Chetumal, Quintana
Roo, Mexico. E-mail: smachkou@ecosur.mx;
2
Consejo Nacional de Ciencia y Tecnologı
´a (CONACYT) assigned to
Grupo de Ecologı
´a de Artro´podos y Manejo de Plaga (GEMA), El Colegio de la Frontera Sur (ECOSUR). Carretera
Antiguo Aeropuerto Km 2.5, C. P. 30700, Tapachula, Chiapas, Mexico;
3
Laboratorio de Conducta Animal, GAIA-
BIO, El Colegio de la Frontera Sur (ECOSUR). Av. del Centenario Km. 5.5, C.P. 77014, Chetumal, Quintana Roo,
Mexico
Abstract. Despite the importance of tarantulas in the areas of medicine and veterinary science, there is very little
information on parasitoid-tarantula interactions. The present study describes the case of an endangered tarantula,
Brachypelma vagans Ausserer 1875, infested by an endoparasitoid in the field. Using DNA barcoding, we identified the
parasitoid as the phorid Megaselia scalaris. With more than 500 fly larvae inside the host, this particular infestation can be
considered severe. The size range of the larvae indicates infestation by all three larval instars. We discuss the possible
mechanism by which the parasitoid is attracted to the tarantula and make important recommendations regarding
improvements in tarantula-rearing conditions. Finally, this case study exemplifies the efficiency of molecular technology for
parasitoid identification.
Keywords: Spider, parasitism, DNA barcoding, humpbacked flies, larvae morphology
Current knowledge on tarantula parasites and parasitoids is very
limited. This is surprising considering the popularity of these spiders
as pets and in zoos (Saul-Gershenz 1996), their use in medical (Park
et al. 2008; Machkour-M’Rabet et al. 2011) and veterinary
applications (Pizzi 2009), and that several tarantula species are
protected. Consequently, any additional knowledge associated with
tarantula parasites/parasitoids is relevant and indispensable.
Parasitoids are organisms characterised by first instars that grow
on or inside the host and always kill it as part of their life cycle
(Godfray & Shimada 1999), usually attacking different developmental
stages of their host. Many species of spider are parasitized by a
variety of insects (Eason et al. 1967), most of which belong to the
arthropod orders Hymenoptera and Diptera (Korenko et al. 2011), as
well as some nematodes (Poinar 1985, 1987; Penney & Bennett 2006),
and kleptoparasitic spiders (He´ naut et al. 2005). Considering only
dipteran parasitoids, those in the family Acroceridae are the most
representative (Schlinger 1993), although some species from the
Tachinidae, Chloropidae, and Drosophilidae families also parasitize
spiders (Eason et al. 1967; Disney 1994). The Phoridae family
comprises over 3000 species of small humpbacked flies found
worldwide and includes scavengers, herbivores, predators, and
parasites/parasitoids (Boehme et al. 2010). Parasitoid species of these
flies are reported to parasitize mainly spider egg sacs. For example,
larvae of Phalacrotophora epeirae Brues 1902, feed on the egg mass of
spiders of various families (Muma & Stone 1971; Hieber 1992;
Guarisco 2001). In addition, parasitoids of the genus Megaselia have
been associated with numerous families of spiders including
Araneidae (Finch 2005), Theridiidae and Lycosidae (Rollard 1990).
Tarantulas belong to the family Theraphosidae comprising 947
species (Platnick 2014). Although reports of tarantula parasitoids are
extremely rare, the most recognized species is Pepsis spp. (Hymenop-
tera: Pompilidae) (Vardy 2000, 2005; Costa et al. 2004). Pizzi (2009)
mentions that ichneumonid ectoparasites (Hymenoptera) possibly lay
their eggs on captive tarantulas and also refers to two nematode
families: Mermithidae and Panagrolaimidae, which parasitize wild and
captive tarantulas respectively. Dermestid larvae (Coleoptera) parasit-
ize captive Brachypelma smithi (Pickard-Cambridge 1897) specimens
(Pare´ et al. 2001). Species of two Diptera families, Phoridae (Weinman
& Disney 1997) and Acroceridae (von Eickstedt 1971, 1974; Cady et al.
1993), have also been reported as tarantula parasitoids.
Despite the high number of tarantula species in Mexico, only one
study mentions the interaction between a parasitoid (Pepsis spp.) and
a theraphosid spider (species of Aphonopelma Pocock 1901) (Punzo
2007). Of the 11 tarantula genera in Mexico (Platnick 2014), only
Brachypelma Simon 1891 is protected under CITES (Appendix II).
Throughout the last decade, efforts have been made to understand
Brachypelma species and to contribute to their protection and
conservation (e.g.: Machkour-M’Rabet et al. 2011, 2012; Vilchis-
Nestor et al. 2013; Dor & He´ naut 2011, 2013; Dor et al. 2008, 2011).
A wild Mexican redrump tarantula, Brachypelma vagans Ausserer
1875 presented signs of weakness, leading to speculation that the
spider was infested by fly larvae. After a short period of time, the
tarantula died. No previous reports describe any manifestations or
characteristics of a parasite infestation in this particular species of
spider. Therefore, this occurrence presented a rare and exceptional
opportunity to describe the case of an endoparasitoid infecting a
protected species of tarantula.
The identification of a dipteran parasitoid, particularly as a larval
instar, is problematical for the non-specialist taxonomist. DNA-based
technology provides a possible solution to the problem of species
identification. Hebert et al. (2004) developed an identification method
known as ‘‘DNA barcoding’’, which uses part of the mitochondrial
COI gene. This method is suitable for characterizing a large number
of organisms (e.g.: Hebert et al. 2004; Prado et al. 2011), particularly
parasitoids (Smith et al. 2007; Janzen et al. 2009; Zaldı
´var-Rivero´n
et al. 2010), therefore, providing a unique opportunity to identify this
specific tarantula parasitoid.
The aims of our study were i) to describe the manifestations
presented by this spider during infestation and ii) to identify the
endoparasitoid and describe the infestation.
2015. The Journal of Arachnology 43:115–119
115
The tarantula specimen was found in the village of ‘‘Laguna
Guerrero’’ (Quintana Roo, Mexico) and taken to a laboratory
maintained under standard conditions (25uC, 75%RH, natural light
cycle). The tarantula was solitarily housed inside a plastic box (15 3
10 320 cm) to be reared for eventual reproduction. After a short
period of time, the spider became inactive and showed no interest in
food (adults of Tenebrio molitor Linnaeus 1758, Coleoptera:
Tenebrionidae). Eventually, the tarantula stopped moving, as in
pre-moulting behaviour, and its abdomen became abnormally
distended. After two days, the tarantula adopted a huddled up
position (all legs adducted, placing the tarsal tips under the sternum)
and died. It was placed in 96%ethanol and after a few days,
numerous dipterous larvae, assumed to have emerged from the spider,
were observed in the alcohol (larvae deposited in the Zoological
Museum of ECOSUR, Chetumal, Mexico).
All the larvae were collected from the alcohol and the tarantula was
dissected to remove any remaining individuals from the carcass. The
larvae were counted and their length measured (Stemi DV4 Zeiss
stereomicroscope with measuring eyepiece, 32X magnification) to
determine the larval instar. Twenty-five first and second-instar larvae
were sent to the ‘‘Laboratorio de Microscopı
´a Electro´ nica de
Barrido’’ (Scanning Electron Microscopy Laboratory) at ECOSUR
(Tapachula, Mexico) to confirm the presence of different larval
instars and identify their morphological characteristics. Due to
damage, third-instar larvae were not sent to the microscopy
laboratory. Larvae were washed with 100%ethanol using a fine
brush, submitted to several baths of 100%ethanol to remove any
external elements and then dehydrated in 100%ethanol for 12 hours.
They were subjected to critical point drying under CO
2
before being
attached to double-sticky tape on aluminum stubs and coated with
palladium-gold (20 nm thick) in a sputter-coating apparatus (Denton
Vacuum, Desk II) for viewing under a scanning electron microscope
(Topcon, SM-510).
For the molecular analysis by ‘‘DNA barcoding’’, five larvae were
placed in a lysis 96-well plate with a drop of 96%ethanol. Genomic
DNA was extracted from larval tissue and the extraction process was
conducted following Montero-Pau et al. (2008). Amplification and
sequencing of the DNA followed the protocols of Prado et al. (2011).
Sequences and all collateral data from specimens are available on
BOLD website (www.boldsystems.org) in the project entitled
‘‘PARTA’’.
Using the tools provided by BOLD-IDS, the obtained DNA barcode
permitted identification to order and family level: Diptera and
Phoridae respectively. The BLASTHtool from GenBank was then
used for species level identification, providing a match with Megaselia
scalaris Loew 1866 (99%similarity).
The B. vagans individual presented a high level of parasitism,
hosting 524 larvae from a wide range of sizes representing the three
larval-instars. The size frequency analysis suggests that second-instar
individuals were dominant (Fig. 1). Following Sukontason et al.
(2002) and Boonchu et al. (2004), the binomial distribution of size
frequencies (Fig. 1) and the larvae ultrastructures (Fig. 2A–F) were
used to determine the size range for each larval-instar. The size of
second-instar larvae ranged from 1.0 mm to 3.5 mm (n5466; 88.9%
of total larvae), with a mean of 2.08 mm 60.02 (6SE) (Fig. 2A). The
characteristic ultrastructures of the spiracular slits of the posterior
abdominal spiracles (Fig. 2B) and the triangular-shaped labium,
typical of second instar larvae, were identified (Fig. 2C). Some
individuals were first-instar (from 0.5 mm to 0.9 mm; n555; 10.5%
of total larvae) with a mean size of 0.65 mm 60.014 (Fig. 2D). These
larvae showed rudimentary posterior abdominal spiracles that
presented a broad-based posterior spiracular hair (Fig. 2E) and a
characteristic bi-lobed labium (Fig. 2F). There were only three third-
instar individuals (from 3.6 mm to 3.8 mm; n53; 0.6%of total
larvae) with a mean size of 3.7 mm 60.058. As these larvae were
damaged, no morphological characteristics were identified.
Megaselia scalaris is a cosmopolitan phorid fly with larvae that feed
on a high diversity of decaying organic material, making this species a
facultative predator, parasite, and parasitoid in invertebrate labora-
tory colonies (Costa et al. 2007; Disney 2008).
Megaselia is known to parasitize theraphosid spiders in Colombia
(Weinmann & Disney 1997) and spiders of the genus Theraphosa
Thorell 1870 in French Guiana (Marshall & Uetz 1990). However,
this is the first report of a living endangered Mexican tarantula species
hosting a parasitoid in the wild. Although no observations were
made, M. scalaris adults were probably attracted by the accumulated
remains (prey and moult) in the tarantula burrow (Machkour-
M’Rabet et al. 2007). These flies became parasitoids of the living
spider by using the book lung as an entrance point and subsequently
penetrating the opisthosoma and internal organs (Pizzi 2009). This
hypothesis is substantiated by several studies that describe phorid
adults feeding on the spider’s prey (Sivinski & Stowe 1980; Weinmann
& Disney 1997) and being attracted to the stabilimentum of the
spider’s web by the strong smell of decaying matter (He´naut et al.
2010). Weinmann & Disney (1997) reported the presence of phorid
larvae on living specimens of two theraphosid species, Megaphobema
robustum Ausserer 1875 and Pamphobeteus Pocock 1901, in Colom-
bia. The phorid species were identified as Megaselia dimorphica
Disney 1997 and Megaselia praedafura Disney 1997. Marshall (pers.
obs. in Marshall & Uetz 1990) reported a Megaselia fly associated
with Theraphosa spiders in French Guiana. In another study, Pe´rez-
Miles et al. (2005) suggest that the silk that covers the burrow
entrance during the day provides protection against parasitoids.
The tarantula’s death was not unexpected as the level of infestation,
(over 500 larvae) was considered very high, One study reports 138
specimens of M. scalaris on a piece of sardine (Moretti et al. 2009).
This number of larvae is not exceptional when considering the high
fecundity of M. scalaris females that can lay up to 600 eggs (references
in Disney 2008). The high level of infestation by different fly instars
could be the result of a single female oviposition over a period of
several weeks, or ovipositions from different females at different
times.
Parasitoidism by phorid flies poses a potential risk to tarantula
breeding for pets or scientific use. Therefore, it is crucial that these
spiders are adequately managed and protected. Constant cleaning,
maintaining optimal temperature and humidity, control of new
individuals through a quarantine period, and the mechanical
protection of spiders from parasitoid arrival would substantially
reduce the risk of infestation by this dipteran on Brachypelma spp.
Furthermore, the identification of a parasitized B. vagans in the field
highlights the potential risk for natural populations of these
endangered tarantulas. More research is necessary to evaluate the
impact of fly parasitoids on wild tarantula populations
Megaselia scalaris was successfully identified using DNA barcod-
ing. Because morphological determination to the species level is
Figure 1.—Frequency of larval sizes (mm) for the endoparasitoid
Megaselia scalaris (Diptera: Phoridae) taken from a specimen of
Brachypelma vagans (Araneae: Theraphosidae).
116 THE JOURNAL OF ARACHNOLOGY
especially difficult for larvae and pupae, the use of a DNA-based
method is an excellent alternative. We hope that this DNA barcoding
technique will become a straightforward laboratory routine for non-
specialists in molecular ecology in order to rapidly resolve issues of
specimen identification.
ACKNOWLEDGMENTS
This paper represents a contribution from the Mexican Barcode of
Life, in particular the Chetumal node where the extraction and
amplification were performed by Arely Martı
´nez Arace (ECOSUR -
Chetumal). Thanks to the Canadian Centre for DNA Barcoding for
sequencing the samples, Humberto Bahena-Basave (ECOSUR -
Chetumal) and Guadalupe Nieto (ECOSUR – Tapachula) for
technical assistance. Julian Flavell is thanked for revising the English.
This research was financed by CONACYT project 000000000158138.
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MACHKOUR-M’RABET ET AL.—ENDOPARASITOID OF BRACHYPELMA VAGANS 119
