Hindawi Publishing Corporation
Psyche
Volume 2012, Article ID 192017, 13 pages
doi:10.1155/2012/192017
Review Article
Nematode Parasites and Associates of Ants: Past and Present
George Poinar Jr.
Department of Zoology, Oregon State University, Corvallis, OR 97331, USA
Correspondence should be addressed to George Poinar Jr., poinarg@science.oregonstate.edu
Received 14 August 2011; Accepted 9 October 2011
Academic Editor: Jean Paul Lachaud
Copyright © 2012 George Poinar Jr. This is an open access article distributed under the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Ants can serve as developmental, definitive, intermediate, or carrier hosts of a variety of nematodes. Parasitic ant nematodes include members of the families Mermithidae, Tetradonematidae, Allantonematidae, Seuratidae, Physalopteridae, Steinernematidae,
and Heterorhabditidae. Those nematodes that are phoretically associated with ants, internally or externally, are represented by the
Rhabditidae, Diplogastridae, and Panagrolaimidae. Fossils of mermithids, tetradonematids, allantonematids, and diplogastrids associated with ants show the evolutionary history of these relationships, some of which date back to the Eocene (40 mya).
1. Introduction
Nematodes are one of the most abundant groups of animals
known. Studies on their evolutionary history suggest that
they probably arose in the Precambrian, which explains their
wide abundance today in the terrestrial and marine environments. While only some 20,000 have been described, their
species diversity has been estimated to be as high as 10 million [1].
One would assume that with their strict housekeeping
habits, ants would not tolerate nematodes in or around
their nests and would quickly dispose of any nest mates that
might have become infected. However nematodes have been
able to use some astonishingly sophisticated tactics to successfully parasitize these social insects. The present work
covers the systematics, life history, pathology, and records of
all described extant and fossil nematodes associated with formicids. This includes representatives of the nematode families Mermithidae, Tetradonematidae, Allantonematidae, Seuratidae, Physalopteridae, Steinernematidae, Heterorhabditidae, Rhabditidae, Diplogastridae, and Panagrolaimidae.
Fossil records of mermithids, tetradonematids, allantonematids, and diplogastrids associated with ants reveal the evolutionary history of these associations, some of which date back
40 million years.
2. Mermithidae
The family Mermithidae includes parasites of invertebrates,
especially insects. Because of their large size, mermithids are
easily detected in ants upon dissection (Figure 1) or as they
leave their hosts (Figure 2). Most mermithid species, including those that attack ants, parasitize only a specific host species, genus, or family while others can infect representatives
of several insect orders. Mermithids that attack aquatic insects, such as midges (Chironomidae, Ceratopogonidae) and
mosquitoes (Culicidae), have a direct life cycle. Direct life
cycles occur when, after growth and development is completed in the host, the mermithid emerges, molts to the adult
stage, mates, and oviposits in the host’s environment. The infective stage mermithid emerges from the egg, actively locates
and enters a host, and initiates development in the hemocoel.
Some mermithids have an indirect life cycle, which is
more complicated but allows hosts to be parasitized in environments hostile to nematodes. In an indirect cycle, the mermithid emerges from the host, molts, mates, and oviposits
in the environment. But instead of emerging from the egg to
search for a developmental host, the infective stage remains
in the egg, waiting to be ingested by an invertebrate that
serves as a paratenic host. When mermithid eggs are ingested by a paratenic host, the hatching infective stage penetrates
the gut wall and enters the body cavity. But instead of developing, the mermithid encysts and enters a diapause. The encysted nematode can be carried through the different stages
of host metamorphosis, but for its cycle to be completed, the
paratenic host must be captured and fed to the brood of the
developmental host. At the completion of the mermithids
growth phase in the development host (like an ant), the latter
is attracted to an aquatic or semiaquatic habitat favorable
2
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Table 1: Section from Gould [2] referring to the first reported
instance of mermithid parasitism of ants.
Figure 1: Mermithid exposed in the gaster of Camponotus sp. from
the Sierra Nevada, California.
Table 2: Mermithid nematodes described from ants.
Mermithid
Agamomermis cephaloti
Agamomermis costaricensis
Agamomermis ecitoni
Allomermis solenopsi
Camponotimermis bifidus
Comanimermis clujensis
Heydenius formicinus
Heydenius myrmecophila
Meximermis ectatommi
Pheromermis lasiusi
Pheromermis myrmecophila
Pheromermis villosa
∗
∗
Figure 2: Parasitic juveniles of Allomermis solenopsi removed from
the gaster of a fire ant worker. Photo courtesy of S. D. Porter, USDAARS.
to the nematode. This is when the mermithid exits, leaving
the dying host behind. The developmental host is usually not
only larger, but usually in a completely different taxonomic
category and environment from the paratenic host. While the
developmental host can live in a relatively dry habitat, the
paratenic host usually inhabits an aquatic, semiaquatic, or
damp biome. Also, both hosts can be widely separated taxonomically and may not even belong to the same phylum.
The first written account of a nematode parasite of ants
was made by the Reverend William Gould in his 1747 book
An account of English Ants (Table 1) [2].
The “white and long kind of worm, which is often met
within their bodies” certainly refers to mermithid nematodes. For a number of years, mermithids were listed under
“Filaria,” “Gordius,” or “Mermis,” and that is why mermithid
systematics can be confusing and why early names for
Gould’s ant mermithid included Gordius formicarum Diesing
[3] and Filaria formicarum von Siebold [4].
The first described ant mermithid was Pheromermis
myrmecophila from Lasius spp. [5]. However it was originally
described in the genus “Mermis”, then assigned to the genus
∗
Host
Cephalotes minutus
Odontomachus hastatus
Eciton burchellii
Solenopsis invicta
Camponotus aethiops
Formica fusca
Camponotus aethiops
Prenolepis henschei
Linepithema sp.
Ectatomma ruidum
Lasius niger
Lasius spp.
Lasius flavus, L. niger
Reference
[11]
[11]
[11]
[12]
[13]
[14]
[15]
[11]
[11]
[16]
[5]
[17]
fossil.
Pheromermis [6], then moved to the genus Allomermis [7]
and lastly to the genus Camponotimermis [8]. Its position
in the genus Pheromermis was recently confirmed by Kaiser,
who showed its similarity with the European ant mermithid,
Pheromermis villosa [9]. Over the years, a large number of
ant species have been reported parasitized by mermithids.
A list of Holarctic parasitized ants was presented by Passera
[10] and Neotropical parasitized ants by Poinar et al. [11]. A
compilation of all described mermithids from ants is presented in Table 2.
Fossils, such as the postparasitic juvenile of Heydenius formicinus emerging from a male Prenolepis henschei
(Figure 3) [15], as well as from a worker ant (Figure 4) in Baltic amber [1] show that ants have been parasitized by mermithids for at least 40 million years and probably much
longer. The fossil record of Neotropical mermithid parasites
of ants is represented by a parasitic juvenile of Heydenius
myrmecophila adjacent to its ant host, Linepithema sp. in 20–
30-million-year-old Dominican amber (Figure 5) [11]. It is
assumed that the traumatic events of the ant host entering
the resin caused the mermithid to emerge prematurely from
an opening in the gaster of the ant.
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3
Figure 5: Heydenius myrmecophila adjacent to its Linepithema ant
host in Dominican amber.
Figure 3: The fossil nematode, Heydenius formicinus, emerging
from a male Prenolepis henschei in Baltic amber.
(a)
(b)
Figure 4: Heydenius formicinus adjacent to its worker ant host in
Baltic amber.
Depending on the caste and length of time the mermithid
is associated with its host, various degrees of host intercastes
and abnormalities appear. Wheeler [18] was the first to provide an explanation for these phenomena by correlating the
unusual morphological conditions with mermithid infections (Figure 6). Parasitized queen ants (mermithogynes)
are shorter, have a smaller thorax (stenothoracy), reduced
wings (brachyptery), enlarged abdomen (physogastry), and
smaller head (microcephaly) than their uninfected counterparts. Parasitized worker ants (mermithergates or macroergates) often develop morphological features characteristic
of queens and soldiers. Attacked male ants (mermithaners)
have shorter wings but enlarged heads, eyes, and gasters.
Infected soldiers (mermithostratiotes) have reduced heads,
an ocellus, and changes in pilosity (Figure 7) [19–24].
The life cycle of most ant mermithids remains a mystery.
Crawley and Baylis [5] assumed that P. myrmecophila has a
direct cycle, where infection is brought about by the eclosing
(c)
Figure 6: Plate (modified) of Pheidole dentata (referred to as P.
commutata) from [18] showing the first evidence that mermithid
nematodes could cause intercastes of ants. (a) Normal soldier; (b)
normal worker; (c) parasitized worker (mermithergate).
preparasitic mermithid entering the ant host. When development is completed, the postparasitic juvenile emerges, molts
to the adult stage in the ant’s habitat, mates, oviposits and the
cycle continues. However, no one has demonstrated a direct
cycle for any mermithid parasite of ants. In 1934, Vandel [25]
studied a mermithid parasite of Pheidole pallidula and realized that the infection must be initiated in the ant larva. He
assumed that the nematodes were in the soil surrounding the
ant colony so the infective stages could penetrate directly into
4
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Figure 7: Two mermithid-infected soldiers (mermithostratiotes)
(arrows) of Pheidole pallidula adjacent to smaller workers and an
uninfected soldier (with large head). Note smaller heads on infected
soldiers. Photo courtesy of Luc Passera.
Figure 8: Pheromermis villosa in a carpenter ant from Holland.
the ant larva; however he was unable to confirm the infection process.
The first life cycle of an ant mermithid was achieved
by Kaiser with the European Pheromermis villosa [17, 26]
(Figure 8). Kaiser showed that P. villosa had an indirect cycle
involving oligochaetes as paratenic hosts. Workers of Lasius
spp. collecting protein for the brood capture oligochaetes
containing the infective stages of P. villosa and, unknowingly,
feed them to the developing larvae. At this point, the nematode becomes active, penetrates into the ant larva’s hemocoel, and initiates development. It was a significant discovery and raises the question whether all mermithid infections
of ants have indirect life cycles. Other possible paratenic hosts
for Pheromermis could be small aquatic insects that ingest
mermithid eggs from the bottom debris of seepage areas or
the edges of other water sources. The wasp parasite, Pheromermis pachysoma [6], also has an indirect cycle and uses caddis
flies as paratenic hosts, which the eusocial wasps (Vespidae)
feed to their brood [27].
Thus far, seven genera of mermithids are known to infect
ants, namely, Agamomermis, Allomermis, Camponotimermis,
Comanimermis, Heydenius, Meximermis, and Pheromermis
(Table 2). All of the ant hosts of these mermithids feed their
brood animal protein (in contrast to other genera, such as
the leaf cutting ants), and this behavior suggests they have an
indirect life cycle involving a paratenic host. The two genera,
Agamomermis and Heydenius, are collective group genera for
immature extant and fossil mermithids, respectively [1].
There are some morphological and behavioral patterns
that characterize mermithids with indirect cycles. They
normally have smaller eggs with thicker shells than the eggs
of direct development soil or freshwater mermithids. Also
their eggs are completely embryonated when laid. Finally,
the deposited eggs will not hatch in the environment even
though the enclosed parasitic juvenile is fully developed.
Hatching only occurs when a potential invertebrate paratenic
host ingests the eggs. The eggs of Pheromermis spp. are small,
numerous, fully embryonated when laid and do not hatch in
the environment. Fully embryonated eggs ensure that the infective stages are ready to enter paratenic hosts as soon as they
are ingested [6, 17].
The ant mermithid, Allomermis solenopsi [12], possess an
unusual morphological feature on the mature eggs that could
play a crucial role in its life cycle. The surface of the eggs is
covered with elongate, erect, spiny adhesive processes. How
these function in the life cycle is unknown, but the related
species, A. trichotopson, possesses similar structures [28].
Since A. solenopsi parasitizes the fire ant, Solenopsis invicta
in Brazil (Figure 2), the related A. trichotopson, whose host is
unknown, may infect Solenopsis geminata in Jamaica. Could
these egg processes somehow be connected with parasitism
of Solenopsis spp.?
Can mermithids be manipulated to control ants? Aside
from killing the ant host upon emergence, mermithids drain
the host of food, reduce the flight muscles and fat body, and
cause morphological modifications as mentioned above [9,
17, 24, 26]. Since mermithid-infected Solenopsis has reduced
reproductive organs and die shortly after the nematodes
emerge [11, 12, 29], it has potential as a biological control
agent. However, if the cycle is always indirect as shown for P.
villosa, it would be very difficult to artificially infect the ant
brood. It would be necessary to first infect the paratenic host
and then supply large numbers of these infected invertebrates
to worker ants for transport back to the nest. Working with a
mermithid that has a direct cycle would be easier; however
there is still the problem of raising and disseminating the
nematodes.
3. Tetradonematidae
The tetradonematids are a diverse group of nematodes that
have traditionally been aligned with the Mermithidae. However, aside from some distinctive morphological characters,
female tetradonematids normally mature, mate, and produce
eggs within the host, which does not occur with mermithids.
Two tetradonematids have been described from extant ants.
Tetradonema solenopsis is a parasite of the red imported
fire ant, Solenopsis invicta, in Brazil [30, 31]. Very little is
known about this nematode aside from the scant description
showing that females contained eggs and worker infection
levels reached 12.5%. Parasitized ants that succumbed to
the infections could be recognized by their slightly enlarged
gaster with scallop-appearing dorsal sclerites.
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5
Figure 11: Eggs of Myrmeconema neotropicum released from the
gaster of an infected Cephalotes atratus worker in Peru.
Figure 9: Mature female of Myrmeconema neotropicum in the early
stages of egg production removed from a pupa of Cephalotes atratus.
Arrow shows position of vulva.
Figure 12: Worker of Cephalotes atratus infected with Myrmeconema neotropicum. The raised, red abdomen occurs when the nematode eggs are infective and ready for transport by birds. Photo courtesy of Stephen P. Yanoviak.
Figure 10: Mature females of Myrmeconema neotropicum packed
with eggs in the gaster of a Cephalotes atratus worker in Peru.
The second tetradonematid from extant ants is Myrmeconema neotropicum from Cephalotes atratus in Peru and
Panama [32]. Myrmeconema is the only nematode that causes
its ant host to radically change color (from black to red),
which is crucial for completion of its life cycle [33]. This color
change was a mystery for early taxonomists and the variety
Cephalotes atratus var. rufiventris was erected solely on the
basis of its red abdomen, which was later shown to be the
result of Myrmeconema infections [32].
Developing females of M. neotropicum occur in ant pupae
(Figure 9) but do not produce masses of eggs until they are
carried into the adult ant (Figure 10). As the females deteriorate, eggs are released into the ant’s hemocoel (Figure 11). At
this stage of development, the gasters of the infected worker
ants turn from black to red and are held high in the air
(Figure 12) [33]. Birds mistake the red gasters for fruits and
the nematode eggs are passed through the birds’ digestive
system and end up in the droppings, which are deposited on
leaves and branches. Cephalotes workers collect and feed the
infested excreta to their brood, which is how the larvae become infected [33].
Aside from their red gasters, parasitized ants are smaller
with reduced head widths. They are sluggish, clumsy, generally less aggressive, and about 40% heavier than nonparasitized workers. They do not bite when handled, and their
alarm/defense pheromone supply is significantly reduced or
absent.
Myrmeconema is probably widely distributed throughout
the Neotropics since this association has been in existence for
some 20–30 million years. The fossil worker ant, Cephalotes
serratus in Dominican amber, is surrounded by the eggs of
Myrmeconema antiqua (Figure 13) [1]. The ant has a hole in
its abdomen that quite possibly was made by a bird. Many of
the eggs, which closely resemble those of M. neotropicum in
size and shape, contain fully developed juveniles (Figure 14).
All indications suggest that M. antiqua had a similar life history to the extant M. neotropicum and involved bird carriers.
6
Figure 13: Worker of Cephalotes serratus infected with Myrmeconema antiqua in Dominican amber. Note microscopic eggs widely
distributed in the amber that were released from a hole in the ant’s
gaster.
Figure 14: Detail of eggs of Myrmeconema antiqua in various stages
of development in Dominican amber.
4. Allantonematidae
It is curious why so few cases of allantonematid infections
have been reported in ants. Since ants are probably one of the
most investigated insect groups, is the absence of tylenchid
parasitism due to a lack of observations or its rarity? The
first and only described allantonematid parasite of extant
ants is Formicitylenchus oregonensis that was parasitizing a
queen Camponotus ant in Western Oregon, USA [34]. The
queen had already chewed off her wings and appeared to be
searching for a nesting site. There was a single large parasitic
female (Figure 15) and 120 third-stage juvenile nematodes
in the ant’s gaster. The third-stage juveniles exited through
the ants reproductive and digestive tracts and molted twice
to reach the adult stage. The enlarged pharyngeal glands in
the free-living females suggest that they penetrate the cuticle
to enter the body cavity of the host, probably ant larvae.
Although the complete life cycle is unknown, the nematodes
are clearly distributed by infected queen ants. The gonads
of the infected ant were greatly reduced, and her eggs were
Psyche
Figure 15: Female of the allantonematid Formicitylenchus oregonensis removed from the body cavity of Camponotus vicinus in
Oregon, USA.
abnormal. Since carpenter ants can be damaging to structures, F. oregonensis can be considered as a potential biological control agent.
Since the original report of this parasite, the present
author recovered a worker carpenter ant also infected with F.
oregonensis, thus indicating that Formicitylenchus is probably
restricted to ant hosts, especially members of the genus Camponotus. Formicitylenchus shows a close relationship with
the allantonematid beetle parasite, Metaparasitylenchus [34].
It is possible that their last common ancestor parasitized
beetles and the host shift from arboreal beetles to arboreal
ants occurred during the anagenesis of Formicitylenchus. The
close physical association between wood-boring beetles and
Camponotus ants may be significant. Rogers [35] commented
that “. . .the potential parasite would be expected to find its
hosts in organisms which occupy the same niche largely independent of their phylogenetic position. In fact the specificity of many parasites is based on the ecological relationship
of the hosts, especially in groups which have only recently
become parasitic.”
Another reason that allantonematid parasitism of ants
may be more widespread than presumed is the discovery of
juveniles of a fossil allantonematid, Palaeoallantonema cephalotae, in the ant, Cephalotes serratus, in Dominican amber
[1] (Figure 16). Just before this fossil was discovered, Steven Yanoviak submitted an extant worker of Cephalotes christopherseni from Peru that was also infected with an allatonematid. The parasitic female (Figure 17) of this still undescribed species and the developing juveniles inside her body
(Figure 18) show features typical of the family.
5. Seuratidae
The discovery of adults of Rabbium paradoxus [36] inside the
gaster of worker Camponotus castaneus in Florida (Figure 19)
was a surprise since all known nematodes of the Seuratidae
are heteroxenous and develop to the adult stage in the digestive tract of vertebrates [37]. However, in R. paradoxus, the
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Figure 16: Three juveniles of the allantonematid, Palaeoallantonema cephalotae, that emerged from a worker Cephalotes ant in
Dominican amber.
Figure 17: Parasitic female of an undescribed allantonematid from
workers of Cephalotes christopherseni in Peru.
Figure 18: Juveniles developing inside the body of the female
allantonematid shown in Figure 17.
7
Figure 19: Adults of Rabbium paradoxus adjacent to their ant host,
Camponotus castaneus, in Florida.
Figure 20: Head of a female of Rabbium paradoxus. Arrow shows
anteriorly located vulva.
vertebrate host is obviously not required for adult development. The females of R. paradoxus have an anteriorly
placed vulva (Figure 20), and the eggs embryonate inside the
uterus (Figure 21). Since the other member of the genus, R.
caballeroi, occurs in the gut of lizards in the Bahamas [38],
it is likely that R. paradoxus originally had (or still has) a lizard definitive host. If the complete life cycle occurs just in
ants, then C. castaneus would serve as both intermediate and
definitive hosts. C. castaneus is a generalist feeder and will ingest vertebrate feces so it could acquire nematode eggs from
lizard droppings. Parasitized worker ants had swollen gasters
and showed unusual behavior by foraging during the day
instead at night. This would make them easily captured by
vertebrate predators.
8
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7. Rhabditidae, Diplogastridae, and
Panagrolaimidae
Figure 21: Embryonated eggs in the uterus of Rabbium paradoxus.
The original life cycle of R. paradoxus may have been similar to that of the seuratoid Skrjabinelazia galliardi, a parasite
of sphaerodactyline lizards in Brazil [37]. The female nematodes living in the gut of the lizard produce eggs that are
passed out and ingested by insects. These eggs hatch in the
insect gut and the juveniles enter the body cavity without further development. Growth is resumed when the insect intermediate hosts are eaten by lizards [38]. Unfortunately, the
complete life cycle of R. paradoxus remains a mystery, but its
precocious development is quite interesting.
6. Physalopteridae
There are few reports of heteroxenous nematodes utilizing
ants as intermediate hosts, that is, hosts where the nematodes
develop only to the third-stage infective juveniles. Maturity
to the adult stages occurs when the intermediate host is eaten
by a vertebrate definitive host. One such nematode is the
physalopterid, Skrjabinoptera phrynosoma that lives in the
stomach of the Texas horned lizard, Phrynosoma cornutum,
and uses the harvester ant, Pogonomyrmex barbatus, as an intermediate hosts [39]. However instead of depositing isolated
eggs that would pass from the lizard, the gravid nematodes
die with the retained eggs enclosed in thick walled capsules.
The females with their enclosed eggs pass out of the lizard
and are collected by worker ants that feed them to their
brood. The nematode eggs hatch in the gut of the ant larvae
and the juveniles enter the fat body, where they develop only
to the third stage. These juveniles are carried through the
pupal and into the adult stage of the ant, where they eventually reside in membranous capsules. The nematodes complete
their development to the adult stage when infected ants are
eaten by the lizards. Worker ants with more than 10 nematodes were still active but had enlarged, lighter colored gasters.
The interesting, pivotal stage in this life cycle is the attractiveness of the dead, egg-laden female nematodes to worker
ants.
This category includes juvenile nematodes living in the postpharyngeal glands of ants (internal phoresis) or being carried
on the outside surface of ants (external phoresis) (Table 3).
While these might not be considered parasites, in some
instances where the association has been examined critically
[40] damage has been inflicted on the ant’s postpharyngeal glands and some of the nematodes increased in size during
their stay in this location. Thus at most, they could be considered weak parasites. If they break through the glands and
introduce microbes into the body cavity of the ant, they could
even be regarded as pathogenic. However the latter scenario
has not been documented.
Most of the nematodes in the postpharyngeal glands are
dauer juveniles of free-living microbotrophs living in the
ant’s environment. The dauers enter the glands when external conditions become unsuitable (low humidity or diminished food supply). These resistant dauer juveniles can survive for relatively long periods. The nematodes may leave the
glands when the environment is more suitable (moist with
associated microbes), if the ant dies and the dauer initiates
development within the decomposing ant, or when the nematodes are transferred from ant to ant during trophallaxis.
Janet [43] was the first to discover postpharyngeal rhabditids (Oscheius dolichurus) in Lasius flavus and Formica rufa in France. Wahab [42] was the first to systematically study
these associations in the ant genera Lasius, Formica, Tetramorium, and Myrmica in Germany (Table 3). More recently
Köhler [41] examined nematodes in the heads of ants
collected from sap fluxes and rotten wood on trees in Germany. The most common ant that visited these fluxes was Lasius brunneus and, from a total of 262 workers collected, 43.5%
carried nematodes, with Koerneria histophora being the most
common associate. While most ants carried a single nematode, numbers occasionally reached up to 85 dauers per ant.
Köhler [41] also found diplogastrid dauers in 4 males and a
queen of L. brunneus. The infection rate of ants associated
with L. brunneus workers varied depending on the weather
cycle. There were more nematodes in ants during the dry period in August than during the rainy months of April and May.
Also important in determining the rate of nematodes being
carried by the ants was the location of the nests. Rates of infestation by nematodes in L. brunneus were much higher
when the ants were collected from sap fluxes and rotten wood
[41], than were collected from under stones and leaf litter
[42].
Köhler [41] was able to infest ants by placing them in a
Petri dish with rotten wood containing waving dauer stages.
Both Wahab [42] and Köhler [41] provided evidence that the
dauers can be transmitted from ant to ant via trophallaxis, which was supported in part by the experiments of Naarmann [53] showing that Formica ants mix food with secretions from the postpharyngeal gland before regurgitating it
to nest mates. These ant-dauer associations probably occur
worldwide since Markin and McCoy [40] reported Diploscapter lycostoma in the postpharyngeal glands of the Argentine Ant, Linepithema humile in California and Nickle & Ayre
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9
Table 3: Juvenile nematodes of Rhabditida and Tylenchina associated with ants.
Nematode
Diplogasteroides spengelii
Diploscapter lycostoma
“
“
∗
Formicodiplogaster
myrmenema
Halicephalobus similigaster
Koerneria histophora
“
Oscheius dolichurus
“
“
“
“
“
Pristionchus lheritieri
∗
Unknown
Unknown
∗
Family
Diplogastridae
Rhabditidae
“
“
Host
Lasius brunneus
Formica spp., Lasius spp.
Myrmica rugulosa
Linepithema humile
Reference
[41]
[42]
[42]
[40]
Diplogastridae
Azteca alpha
[1]
Panagrolaimidae
Diplogastridae
“
Rhabditidae
“
“
“
“
“
Diplogastridae
“
Lasius brunneus
Lasius spp.
Lasius brunneus
Formica rufa,
Lasius flavus
Tetramorium caespitum
Camponotus herculeanus
Lasius claviger
Lasius brunneus
Formica rufa, Lasius spp.
Azteca spp.
“
Formica obscuriventris
[41]
[42]
[41]
[42, 43]
[42, 43]
[42]
[44]
[44]
[41]
[42]
[1]
Present work
(Figure 22)
Fossil.
Figure 22: Dauer juveniles of a diplogastrid in the postpharyngeal
glands of Formica obscuriventris clivia from Oregon.
[44] found Oscheius dolichurus in the head glands of Camponotus herculeanus and Lasius claviger in Ontario, Canada.
The author has also found dauer diplogastrids in the postpharyngeal glands of workers of Formica obscuriventris in
Oregon (Figure 22).
The association between dauer nematodes and ants is at
least 20–30 million years old. Evidence for this is the discovery of dauer juveniles of the fossil diplogastrid, Formicodiplogaster myrmenema, carried by Azteca alpha workers in Dominican amber [1] (Figures 23 and 24). The dauer stages
appear to be associated with the abdomen of the ants, suggesting that they were being carried in the segmental membranes of the gaster (external phoresis). None of the fossil
stages occurred around the mouthparts of the ants. Also, developing stages of F. myrmenema were associated with nest
material adjacent to worker Azteca ants in Dominican amber
Figure 23: Three dauer juveniles of Formicodiplogaster myrmenema
adjacent to a worker of Azteca alpha in Dominican amber.
[1]. This indicates that F. myrmenema was developing in the
nests of A. alpha, which is probably the case with extant
nematodes in the head glands of ants. Whether the dauers
of F. myrmenema were also in the postpharyngeal glands of
the fossil ants is unknown.
10
Psyche
Table 4: Ants infected by entomopathogenic nematodes (Steinernema carpocapsae and Heterorhabditis bacteriophora) under laboratory
and/or field conditions.
Ant
Acromyrmex octospinosus
Camponotus sp.
Camponotus sp.
Myrmica sp.
Pogonomyrmex sp.
Solenopsis spp.
Solenopsis geminata
Solenopsis invicta
Solenopsis invicta
Solenopsis richteri
Solenopsis richteri
Nematode
S. carpocapsae
S. carpocapsae
S. carpocapsae
S. carpocapsae
S. carpocapsae
S. carpocapsae
S. carpocapsae
S. carpocapsae
H. bacteriophora
H. bacteriophora
S. carpocapsae
System
Aqueous
Sucrose
Aqueous
Aqueous
Sucrose
Alginate capsules
Aqueous
Aqueous
Aqueous
Aqueous
Aqueous
Reference
[45]
[46]
[47]
[47]
[48]
[46]
[49]
[50, 51]
[52]
[52]
[50]
8. Steinernematidae and Heterorhabditidae
Figure 24: Detail of a dauer juvenile of Formicodiplogaster myrmenema adjacent to a worker of Azteca alpha in Dominican amber.
Figure 25: Developing stages of Steinernema carpocapsae removed
from the body of an infected queen of Solenopsis invicta.
Included in this section are the so-called entomopathogenic
nematodes belonging to the genera Steinernema and Heterorhabditis. It is quite likely that entomopathogenic nematodes infect ants under natural conditions, but no reports
are known. Infection is initiated by a third-stage infective
juvenile that enters the host’s body cavity, apparently per os
[50]. After reaching the hemocoel, the infective stage initiates development and, in so doing, releases a symbiotic bacterium (Xenorhabdus spp. in Steinernema nematodes and
Photorhabdus spp. in Heterorhabditis nematodes) that is carried in the infective stage’s gut lumen. The bacterium kills
the insect soon after it is released in the body cavity. The
nematodes feed on the mixture of bacteria and insect hemolymph and develop to the adult stage in the body cavity.
With adequate nourishment, the nematodes undergo a second generation but when nourishment is limited, the juveniles form third-stage infective juveniles. By introducing the
bacteria that quickly kill the hosts, these nematodes avoid
specific defense responses and have a wide host range, attacking representatives of many insect orders and even other
arthropods [54].
Laboratory experiments have shown that these nematodes can infect a number of ant species (Table 4) and they
also have been used in the field against pest ants [50, 52, 54–
56]. Poole [50] attempted to control field populations of ants
(Solenopsis richteri and S. invicta) with Steinernema carpocapsae. Using a dose of 1 million infective stages per mound for
S. invicta, the nematodes caused 35% mortality in the fall and
80% mortality in the spring. With S. richteri, the death rate
was 80% in the spring and 36% in the fall. Poole [50] noted
that workers were infected less than other stages, possibly because of their greater activity and grooming behavior. However, workers regurgitated infective stages to the alates and
larvae. Queen ants were more susceptible and up to 3,000 infective stage juveniles could be produced in some infections
(Figure 25).
Further field trials of S. carpocapsae and Heterorhabditis
bacteriophora against the red imported fire ant, S. invicta,
Psyche
11
Table 5
(1)
(2)
(3)
(4)
(5)
(6)
(7)
Nematodes represented as dauer or postdauer juveniles in the pharyngeal
glands of ants
Nematodes developing in the body cavity of ants
Only juvenile nematodes present
Adult nematodes with or without juveniles
Elongate nematodes normally over 15 mm in length at completion of
development; not enclosed in membranous capsules
Nematodes under 10 mm in length; enclosed in membranous capsules
Nematodes reproducing in dead ants; infective juveniles produced
Nematode adults, eggs and/or juveniles in living ants; infective juveniles absent
Males with a bursa; females with a pointed tail
Males without a bursa; females with a bluntly rounded tail, often bearing a
small point at tip
Eggs and juveniles present
Eggs, but no juveniles present
Vulva positioned at middle or lower half of body
Vulva positioned in upper fourth of body
gave control rates of 37.5% with S. carpocapsae but less with
H. bacteriophora [52]. In field trials comparing applications
of Steinernema carpocapsae and amidinohydrazone against S.
invicta, Morris et al. [55] estimated that nematode applications at a rate of 2 million per gallon per mound resulted in
47% mortality.
Controlling fire ants in the field is difficult because of
the small mound opening through which the nematodes are
introduced. Also, it is desirable to have recycling of the nematodes in the nests, but healthy ants appear to remove infected
individuals before the cycle is completed. Since the number
of nematodes needed to overwhelm a colony of ants is quite
high using inundative methods, consideration was given to
the development of baits or other more efficient delivery systems [46, 48, 52, 55, 56]. These other methods are still under
investigation.
Rhabditidae, Diplogastridae and
Panagrolaimidae
(2)
(3)
(4)
Mermithidae
Physalopteridae
(5)
(6)
Heterorhabditidae
Steinernematidae
Allantonematidae
(7)
Tetradonematidae
Seuratidae
osoma, the smallest of which measures 633 µm in diameter
[39].
In 1907, Janet [58] found nematodes 7-8 mm in length
developing in the head cavities and emerging from the labial
region of workers of Formica fusca. Just before the nematodes emerged, the infected ants began trembling and eventually died. The head cavities of infected ants were empty upon
nematode exit. This behavior of developing in the head of
ants is known for some phorid flies but not for nematodes. Whether this was a mermithid with an unusual developmental location or a heteroxenous nematode using the ant as
an intermediate host is unknown.
10. Identification Key to Nematode
Families Associated with Ants
See Table 5.
9. Unknown Nematodes
Gösswald [57] reported the presence of several encysted
nematodes in the flight muscles of a queen Teleutomyrmex
schneideri in Germany. The cysts were quite small, being
only 25 µm in diameter. Except for their small size, the cysts
are similar in appearance to those of the vespid mermithid, Pheromermis pachysoma, formed in the body wall of Trichoptera paratenic hosts [27] and the ant parasite, P. villosa,
in the body of oligochete paratenic hosts [26]. However,
the Pheromermis cysts are 60–100 µm and 80 µm in diameter, respectively. It is possible that juvenile nematodes of a
mermithid parasite were acquired after the queen was fully
formed and the nematodes preferred to encyst rather than
initiate development. The other likelihood is that the nematodes were the infective stages of a heteroxenous nematode
parasite and were waiting for transfer to a vertebrate definitive host. However, the only cysts of heteroxenous nematodes known from ants are those of the physalopterid, S. phryn-
11. Conclusions
Representatives of most invertebrate parasitic nematode
families attack ants, with the exception of sphaerulariids, entaphelenchids, and oxyurids. While mermithids are the most
commonly encountered nematode parasites of ants, the complete life cycle of only a single species is known. The life cycle
of ant mermithids can be quite complicated when it involves
paratenic hosts living in completely different habitats. Even
less is known about the life cycles of other ant parasitic
nematodes, certainly not enough to consider using them
as biological control agents. While the inundative application of entomopathogenic nematodes (Steinernema and Heterorhabditis) can control ants in isolated colonies, establishing nematodes for the sustained control of ant populations
has not been achieved.
There are probably many additional nematode parasites
of vertebrates utilizing ants as intermediate hosts. Reptiles,
12
mammals, and amphibians eat ants, and it follows that nematodes other than Skrjabinoptera phrynosoma would have
devised methods of cycling themselves through ants to reach
their definitive hosts. In the mysterious case involving Rabbium paradoxus, the presence of adults of a heteroxenous nematode in an ant raises the question of whether formicids can
serve as sole hosts or this is just a case of precocity.
Fossils show that mermithids were infecting ants over 40
million years ago and tetradonematids and allantonematids
had established parasitic associations with ants some 20–30
million years ago. Such fossils, which can be used to calibrate
molecular clocks, provide minimum dates for the occurrence
of nematode lineages and show the antiquity of nematodeant relationships.
Acknowledgments
The author thanks S. D. Porter, Luc Passera and Stephen P.
Yanoviak for supplying photos and Brad Vinson for supplying the queen of Solenopsis invicta infected with Steinernema
carpocapsae. Grateful appreciation is extended to Roberta
Poinar for commenting on earlier versions of the paper.
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