Nakridletia ord.n. - Enigmatic insect parasites support sociality and endothermy of pterosaurs

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Introduction
A major portion of the diverse range of insects, as well as herbivores,
parasitoids or vertebrate ectoparasites,have parasitic feeding
strategies (Sukhdeo and Bansemir 1996, Labandeira 2002). Insect
ectoparasites in particular are associated with harming the host,
despite the fact that host-parasite relations are often phylogenetically
significant and positive to both of them, with entire ecosystems often
regulated by parasites. No flea species (Siphonaptera), parasitic
helminth (Platyhelminthes), parasitic nematode (Nematoda), mite, or
tick (Acari) with the exception of only one of the 5.000 extant louse
species (Phthiraptera) is listed as threatened by the IUCN, despite
impassioned pleas for parasite conservation beginning more than a
decade ago (Whiteman & Parker 2005) (endangered status was
proposed for the louse parasitising the endangered iberian lynx, Lynx
pardinus (Perez & Palma 2001)).
In addition to the close relationship with most of animal species, insect
ectoparasites are found to significantly influence human history, with
louse identified from mummies (Ewing 1924, Horne 1979, El Najjar et
Mulinksi 1983, Rick et al. 2002), prehistoric coprolites (Fry 1977,
Reinhard & Largent 1989), historic deposits (Kenward 1999) and
storerooms (Mumcuoglu et al. 2003), as well as pre-pottery sites (Zias
& Mumcuoglu 1991). They were reported to have significantly
influenced war (Peacock 1916), can change behaviour and cause
psychical trauma or neurosis (Held & Bernstein 1989; Boll-Klatt, Beurich
& Schmeling-Kludas 2003).
The harm, often associated with infections and multiple infestations,
is also known in humans (e.g., Sasaki et al. 2006). Louse-borne
infectious diseases affected nearly one-third of Napoleon's soldiers
returning from Russia (buried in Vilnius), which might have been a major
factor in the French retreat from Russia (Raoult et al. 2006). Other
transferred vectors include those of Rickettsia prowazekii, the aetio-
logical agent of louse-borne epidemic typhus (LBET)(Robinson et al.
2003) or Trench fever (Bartonella quintana) (Sasaki et al. 2006). Plague
killed one third of the European population in the 14th century.
Bee-eaters are infested by three species of chewing lice (Meropoecus
meropis, Meromenopon meropis and Brueelia apiastri) of which
M. meropis infests 94% of all adults (Darolova et al. 1998).
There are thirty five distinct lineages, with multiple Acinetobacter and
Staphylococcus species, represented by eight widely divergent groups
of Bacteria, associated with ectoparasitic chewing lice of North
American pocket gophers (Reed et Hafner 2002).
Nakridletia ord.n.
– enigmatic insect parasites support sociality and endothermy of pterosaurs
Orders are gross formal ranks of insects. All ~350.000 named species of beetles belong to the single order Coleoptera; moths, skippers and
butterflies form the order Lepidoptera. All solitary, social and parasitic wasps, with bees and ants are housed within Hymenoptera. Altogether,
insects are placed within 42 orders (Rasnitsyn & Quicke 2002), of which 31 are living (Klass et al. 2002). Parasitic fleas and lice (Siphonaptera,
Phthiraptera), predatory ice-crawlers and gladiators (Grylloblattodea, Mantophasmatodea) are all wingless as well as about 5% of insect species
(Whiting et al. 2003).
Parasitism and/or wingless require a general morphological reorganisation and thus the absence of insect orders parasitising extinct sauria was
surprising. Now we designate a new insect order, Nakridletia, for excelently preserved Strashila incredibilis Rasnitsyn, 1992 (Strashilidae),
Parazila saurica Vršanský et Ren, gen. et sp.n. and Vosila sinensis Vršanský et Ren, gen. et sp.n. (Vosilidae) - giant pterosaur parasites from
the Upper Jurassic of Siberia (Rasnitsyn 1992) and the Middle Jurassic of China (Ren et al. 2002, Rasnitsyn & Zhang 2004, Chen et al. 2004,
Liu et al 2004, Gao & Ren 2006) respectively. The latter also represents the oldest direct evidence for ectoparasitism.
Pediculid lice-like adaptations, characteristic for infestation of stenothermous, restricted to endotherm social hominoids (Ferris 1951), indicate
endothermy and perhaps also the sociality of pterosaurs.
Key words: fossil insects, new order, ectoparasites, pterosaur parasites, Jurassic, Mecopteroidea
Peter Vršanský1,2,3, Dong Ren1* and Chungkun Shih1
1College of Life Science, Capital Normal University, 105 Xisanhuanbeilu, Haidian District, Beijing, 100037, P. R. China rendong@mail.cnu.edu.cn
2Geological Institute, Slovak Academy of Sciences, Dúbravska cesta 9, P.O. BOX 106, 840 05 Bratislava, Slovakia geolvrsa@savba.sk
3Paleontological Institute, Russian Academy of Sciences, Profsoyuznaya 123, 11 78 68 Moscow, Russia lab@palaeoentomolog.ru
* Author for correspondence
Nakridletia ord.n. (Insecta) – pterosaur parasites Vršanský, Ren and Shih, August 2010. Amba projekty 8(1): 1-16, Bratislava
ISBN: 978-80-970488-6-0

The harm of lice-related (Bovicola bovis) damage is known on cattle
(light spot, which is reversed only after 13 weeks (Coles et al. 2003)),
and the chewing lice Damalinia was reported to cause widespread hair-
loss syndrome in black-tailed deer of the Pacific northwest in western
Oregon and Washington (Bildfell et al. 2004).
Ectoparasites are also common in water mammals such as otters
(Kim & Emerson 1974, Kim 1975), or marine seals - after infection with
viruses (e.g., alphaviruses), the lice on southern elephant seals (Mirounga
leonina) remain infected for life - nearly all have neutralizing antibodies
against the virus, even no virus-associated pathology (Linn et al. 2001).
Diverse fleas (14 species of 5 families) are common north of the Arctic
Circle in Norway (Hastriter et al. 2004).
Fossil insect ectoparasites are scarce because of their potential for
preservation.
Systematic palaeoentomology
Class Insecta Linné, 1758
Superorder Papilionidea Laicharting, 1781 (=Mecopteroidea auct.)
Order Nakridletia, ord.n.
Proposed type for the case of typification: Strashila incredibilis
Rasnitsyn, 1992. [Figs. 2,4]
Composition: Strashila Rasnitsyn, 1992 (Strashilidae Rasnitsyn, 1992);
Vosila Vršanský et Ren, gen.n. and Parazila Vršanský et Ren, gen.n.
(Vosilidae Vršanský et Ren, fam.n.)
Stratigraphic and geographic range: ?Bathonian Middle Jurassic –
?Tithonian Upper Jurassic. Asia.
Differential diagnosis. The present order may be housed within
Holometabola based on the structure of terminalia with aedeagus and
articulated volsellae with gonostyli. The sucking beak is characteristic
for the Mecopteroidea. The dorsoventrally flattened, wingless order
Nakridletia differs from all Mecopteroidea (and also from all other
ordina) in having gill-like abdominal appendages. Head is large, with
large eyes. Meso and metanotum is unique (similar to that of lice) in
being extremely short, male terminalia permanently protruded.
General habitus similar to some lice (non-homometabolans), but except
for the terminalia, the difference is the long hind leg nipper with
processus present apically (dorsal in lice).
Description. Head large with large eyes. Pronotum concealing head,
without paranotalia. Meso and metanota almost reduced, wings entirely
reduced. Abdominal segment margins apparent at least laterally. Male
terminalia protruded. Legs with 5-segmented tarsi, 1st segment with
apical spur. Hindlegs extremely enlarged, femur strong, tibia long, strong
with apical processus forming nipper with 1st tarsal segment.
Remarks. Rasnitsyn (1992) noticed a beak in Strashilla which is unde-
tectable now, as a cause of partial damage to the specimen by
application of alcohol.
Laterally distant coxae are uncharacteristic for the Holometabola and
Polyneoptera, but characteristic of parasites and/or embryonised (in
heteroptera diverge secondarily).
Derivation of name: nakridletia is after nakridle (Slavic for on wings).
A proposed English vernacular name is Paraglida or paragliders after
paragliding or wing-over flight.
Vosilidae Vršanský et Ren, fam.n.
Type species. Vosila sinensis sp.n. Daohugou, Inner Mongolia, China.
Middle Jurassic.
Composition. Besides the type species, Parazila saurica sp.n.
Daohugou, Inner Mongolia, China. Middle Jurassic.
Differential diagnosis. Differs from the Strashilidae in possessing gill-
like abdominal appendages and more massive hind femora.
Description. Cuticle of head, nota and legs strong. Head hypognathous,
large, with large eyes. Antennae moniliform. Wings reduced. Tarsi
5-segmented, the 2nd segment articulated subapically, pretarsus very
long. Hindlegs extremely enlarged and widened femur and tibia, latter
with apical process forming nippers with the basitarsus– aperture
rounded. Body lacking sclerotisation, with subequal terga and gill-like
appendages. Male terminalia large, external.
Remarks. For comparison with Strashila see the differential diagnosis
of Vosila.
Vosila Vršanský et Ren, gen.n.
Type species: Vosila sinensis Vršanský et Ren, sp.n.. Daohugou, China.
Middle Jurassic.
Differential diagnosis. Differing from Strashila in having more robust
pronotum and meso and metanotum, all femora more massive, hindleg
nipper aperture round, and pretarsi very long. The ratio of legs is very
different from Strashila: Forelegs femur, tibia, tarsus 0,8mm; 1,2mm;
2,4mm; compared with 0,7mm:1,6mm:2,5mm (1: 1,5: 0,63: 0,5: 0,38:
0,38: 1,13 vs. 1: 2,5: 0,7: 0,6: 0,6: 0,6: 0,8: 0,5); midlegs 1,1mm:
1,3mm: 1,8mm compared with 1,0mm:1,6mm, 2,8mm (1: 1,18: 0,45:
0,36: 0,18: 0,27: 0,82 vs. 1: 1,7: 0,6: 0,5: 0,4: 0,4: 0,7: 0,4); hindleg
1,8mm: 2,8mm: ? compared with 3,2mm:3,4mm:3,0mm (1: 1,6: 0,6:
0,33… vs. 1: 1,1: 0,35: 0,15: 0,07: 0,07: 0,17: 0,12). Generally, Vosila
has fewer chaeta. Unlike Strashila, the abdominal appendages with
large gill-like structures, but without lateral abdominal prolongations.
Description. Dorsoventrally flattened insect with strong cuticle (except
for abdomen). Head hypognathous, large, perhaps triangular, with
distinct large eyes. Antennae moniliform. Pronotum slightly transversal,
wings reduced. Legs coxae short, tarsi 5-segmented, the 2nd segment
articulated subapically, pretarsus very long. Hindlegs extremely
enlarged and widened femur and tibia, latter with apical process forming
nippers with the basitarsus– aperture rounded. Body lacking scleroti-
sation, with subequal terga and gill-like appendages. Male terminalia
large, external.
Composition: type species only.
Derivation of name: a jigsaw: vosila means that which is transferred,
voš [:wash:] means louse and võs [:was:] is also Latin for you, sila means
power and šila means sewed.
Figure 1. Supposed pterosaur parasites of the order Nakridletia ord.n. (Vosilidae): Vosila sinensis Vršanský et Ren, gen. et sp.n. Middle Jurassic,
Daohugou, Inner Mongolia, China. Holotype CNU-PARA-001. a1) general habitus; a2) gill-like appendages. Abdomen 5mm long. b) Parazila saurica
Vršanský et Ren, gen. et sp.n. Holotype CNU-NN-PARA-002 b1) general habitus b2) gill-like apperndages. Overal body length 5.7mm.
Nakridletia ord.n. (Insecta) – pterosaur parasites Vršanský, Ren and Shih, August 2010. Amba projekty 8(1): 1-16, Bratislava Nakridletia ord.n. (Insecta) – pterosaur parasites Vršanský, Ren and Shih, August 2010. Amba projekty 8(1): 1-16, Bratislava
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Vosila sinensis Vršanský et Ren, sp.n. [Figs. 1a, 3a]
Holotype. CNU-PARA-001. A complete specimen. Daohugou, Inner
Mongolia, China. ?Bathonian Middle Jurassic.
Description. Head covered by slightly transversal, quadrate pronotum
(1.1/1.2mm). Meso and metanotum extremely narrow. Abdomen almost
lacking sclerotisation, about 5mm long and 1mm wide when unfed.
Abdominal appendages consisting of three distinct parts (Fig. 1b3). The
basalmost articulation is weakly sclerotised, narrow, with proximal part
with an aperture. The central hardly sclerotised part consists of three
lobes, two proximal parts closely associated. To the central part, plain,
gill-like appendages are articulated. Three to the distal lobe, eight to the
central lobe, and a sigle to the proximal lobe. All gill-like appendages
cover over 2mm2.
Terminalia protruded from body, about 0,5mm long.
Foreleg femur robust, with numerous long sensilla, tibia only with 5
sensilla. Basitarsus with terminal claw and row of very small sensillar
pitts. Segment 2 attached subapically. Measuremens 0,8mm; 1,2mm;
0,5mm; 0,4mm; 0,3mm; 0,3mm; 0,9mm. Midleg femus robust, with
numerous spurs, tibia with two longitudinal ridges. Measuremens
(Femur, tibia, basitarsus, tarsi) 1,1mm; 1,3mm; 0,5mm; 0,4mm; 0,2mm;
0,3mm; 0,9mm. Hindlegs asymmetrical. Right coxa very long (1.3mm),
femur not very robust with numerous sensilla (1,8mm), tibia very long
(2.8mm). Left femur extremely robust with two logitudinal ridges and
numerous sensilla. Tibia with apical processus, very long, with two longi-
tudinal ridges. Measuremens 1,8mm; 2,8mm; 1,1mm; 0,6mm (data of
terminal tarsal segments missing). Nipper aperture formed by the apical
processus and basitarsus round and wide.
Character of preservation: 1 complete specimen.
Derivation of name: after China.
Parazila Vršanský et Ren, gen.n.
Type species. P. saurica sp.n. (by monotypy and present designation).
Differential diagnosis. Nota wider than body, hind border of third and/or
fourth abdominal segment (probably sternum) strongly arcuate, mid
femora more than half hind femora width, gill-like abdominal
appendages pectinate backward (unlike in Vosila with pectination on
both sides).
Description. Pronotum pentangular, slightly narrowed posteriorly, widest
anteriorly, with posterior median elongation. Mesonotum nearly
reduced, extremely short and narrow. Metanotum distinct, wider than
pronotum. Mid femur robust (length/width 1:4). Hind trochanter compar-
atively long, subconical, femora and tibiae extremely robust. Abdomen
narrow, tapering backward, with seven pairs of gill-like appendages,
basalmost as long as abdomen wide, following gradually shorter. Fourth
segment with obscure sclerotised arcuate structure. Last visible
abdominal segment narrow, subcylindrical. Male terminalia about as
wide as penultimate visible segment, about twice as wide as ultimate
one, transversal, with base (fused gonocoxae) width some 2.5 times
length, with wide orifice between forceps bases. Forceps long and very
thick.
Species included. Type only.
Remarks. The large pentangular pronotum is perhaps an apomorphy.
Obscure triangular sternal elongation of the body is a shared apomorphy
with Strashila, as in Vosila it is quadrate in outline, but in Strashila it
occurs in the second segment. Strengthened mid femora is a shared
apomorphy (possibly synapomorphy) with Strashila. Gill-like
appendages are synapomorphic with Vosila (more primitive state with
gill-like appendages nearly missing in Strashila), but the pectinate shape
and polarization of veins on one side are more primitive than palm-like
in Vosila. Reduced mesonotum is a shared apomorphy (perhaps a
homoplasy with Strashila).
Hind legs are preserved in opposite direction to each other, which may
indicate they may have been used in both positions: nipper posteriorly
as in original description (Rasnitsyn 1992) as well as anteriorly as
indicated by Grimaldi (2005).
The known species of Parazila is smaller than Vosila. Pronotum is of
comparable length, but wider in Parazila (length/ width ratio 0,86: 0,92).
As in Vosila, hindlegs are deeply asymmetrical. According to the reverse
asymmetry in both genera, it is possible that Vosila is preserved in
reverse (negative) position (impossible to approve). So the right femur
of Parazila is very robust (length width ratio 2,16), of comparable habitus
and length than left one in Vosila. Tibia is much longer in Vosila (2.8mm:
1,7mm)
Derivation of name: modified after parasitus (Latin for parasite). Gender
feminine.
Parazila saurica Vršanský et Ren, sp.n. [Figs. 1b, 3b]
Holotype. CNU-NN-PARA-002, nearly complete male with head invisible
(apparently hidden under enlarged pronotum), fore legs, most of
antennae and part of mid and hind legs lost. Middle Jurassic
Jiulongshan Formation. Daohugou, Inner Mongolia, China. Deposited in
the Capital Normal University, Beijing, China.
Description. Overal body length 5.7mm. Pronotum transversal, with
median elongation (length/width 1.17/1.42mm). Mesonotum nearly
reduced (0.32/1.28mm), metanotum massive (0.35/1.84mm).
Abdomen wide at most 1.13mm. Mid coxa distinct (0.64/0.28mm),
femur massive (1.42/0.35mm). Hind legs asymmetrical (see genus
remarks). Rigth trochanter elongate (0.71/0.35mm), femur
1.77/0.82mm, tibia 0.73/0.46mm. Left leg with apparently longer
trochanter (0.92/0.35mm), less robust femur (1.70/0.74mm) and more
robust tibia (?/0.67mm). Lateral abdominal appendages decreasing in
length posteriorly, complete length of the best preserved fourth one is
1.24mm, the seventh one 0.57mm. The fourth appendage consists of
five triples of outgrowths attached to distinct more massive base.
Terminalia length/ width 0.53/0.71mm, forceps longer than half width
of terminalia, about twice as long as wide, curved inward and rounded
apically.
Remarks. All legs are characterized by distinct ridges occurring also in
both Vosila sinensis and Strashila incredibilis: these might be either
real life time structures or a postmortem deformation of less rigid
cuticular areas.
Derivation of name: after saurus (Latin for reptile).
Character of preservation: one nearly complete specimen.
Figure 2. Supposed pterosaur parasite of the order Nakridletia ord.n.
(Strashilidae): Strashila incredibilis Rasnitsyn, 1992. Late Jurassic,
Mozgon near Chita, Siberian Russia. Holotype PIN 3084/60.
Body 7mm long. Orig.
Discussion
Terrestrial ecosystems prior to parasitoid and parasite diversifications
were simpler in food web structures (Labandeira 2002) with the rather
rapid appearance of major parasitoid taxa during the Middle Jurassic –
Early Cretaceous. The transition to parasitoism was accomplished by
modifications in the reproductive biology of numerous holometabolous
lineages (Godfray 1994).
An important development in early parasitoids was a shift in larval food
sources, from less nutritious plant tissues to more proteinaceous animal
tissues which were often supplied by the adult (Malyshev 1968).
Nevertheless, the hematophagy more likely originated from inquiline
associations in vertebrate nests by a shift from nest detritivory of
epidermis, feces, sebum, and other exudates to blood feeding (Balashov
1999) – this hypothesis is most relevant to the origin of ectoparasitsism
in Phthirapthera, since many members of the closely related Psocoptera
are nest associates of the vertebrate host (Waage 1979) as well as in
Strashilidae – with the present species representing the oldest record
of any ectoparasite.
Except for Strashila, the oldest possible flea Sauropthyrus longipes
Ponomarenko,1976 comes from the Early Cretaceous of the
Transbaikalian Siberia (Ponomarenko 1976, 1988), and the flea
Tarwinia australis Jell et Duncan, 1986 from the Early Cretaceous of
Australia (Riek 1970).
The 44myr old bird (ancestor to modern Anseriformes (swans, geese
and ducks) or Charadriiformes (shorebirds)) louse Megamenopon
rasnitsyni (Insecta: Phthiraptera: Amblycera: Menoponidae) from the
crater of the Eckfeld maar in Germany has feather remnants in the
foregut, indicating an early origin for lice, perhaps inherited from early-
feathered theropod dinosaurs (Wappler et al. 2004).
Voigt (1952) described and illustrated eggs of sucking lice
(Phthiraptera: Anoplura) attached to mammal hair imbedded in Baltic
amber, as well as a Miocene Lutzomyia swarm was preserved with
strands of mammalian hair (Peñalver & Grimaldi 2005).
Another pterosaur parasite, Saurodectes vrsanskyi Rasnistyn et
Zherikhin, 1999 was excluded from Anoplura (Dalgleish et al. 2006) and
perhaps also deserves its own order. The same author excluded fossil
mites from Anoplura (Kumar 2004, Kumar and Kumar 1999, 2001).
Before the phylogenetic relation of the new order is analysed, immense
homoplasies (convergences) with lice are explained . The independ-
ently achieved characteristics of the Strashilidae and the Pediculidae
lice parasitising humans are 1) Nipper on hindlegs formed by apical
tibial processus, basitarsus and its terminal spur (2); 3) Leg asymmetry
resulting in lateral movements – possibly related to their heterozygoty;
4) Abdominal stigma-joined processi, with attached gill-like filaments
(Pthirus pubis segments 1-5 closely crowded - stigmata of segments
3-5 apparently lying in one lateral processes); 5) Notum reduced to large
extant; 6) protruded male terminalia. 7) Dorsoventally flattened head
and probably 8) reduced labial palps (large palp would be visible in the
specimen).
Differences might be restricted to compound eyes and antennae which
are reduced (3-5 antennal segments) in lice.
Nakridletia ord.n. (Insecta) – pterosaur parasites Vršanský, Ren and Shih, August 2010. Amba projekty 8(1): 1-16, Bratislava Nakridletia ord.n. (Insecta) – pterosaur parasites Vršanský, Ren and Shih, August 2010. Amba projekty 8(1): 1-16, Bratislava
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Nevertheless, nipper (1)+2)): is paradoxically formed at the dorsal part
of the tibia in the new order and gill-like filaments (4)) are wide, unlike
sensilla-based in lice. The relation of both taxa might be definitely
excluded based on the presence of the primitive, 5-segmented tarsi of
all legs, a characteristic lost in the Pennsylvanian (Mississippian)
Psocoptera. The close relation of the psocopteran family Liposcelididae
and lice is well documented, excluding the possibility of the Strashilidae
belonging to lice. Liposcelididae are the sister taxon to the louse
suborder Amblycera, making parasitic lice (Phthiraptera) a polyphyletic
order - parasitism independently arose twice within Psocodea, once in
the common ancestor of Amblycera and once in the common ancestor
of all other parasitic lice (Johnson et al. 2004). The most primitive stem
group represented by Cretoscelis burynitica of the family Liposcelididae
was reported from the mid-Cretaceous (~100 Myr) of Myanmar, with
lice diversification time estimated at 145myr, and with an indication that
the hosts of lice would have been early mammals, early birds and
possibly other feathered theropod dinosaurs, and/or haired pterosaurs
(Grimaldi & Engel 2006).
In particular, the apomorphic presence of articulations between the
basal plate, mesomere and ventral plate (= sclerite on the permanently
everted endophallus) is observed consistently throughout the psocid
families Pachytroctidae and Liposcelididae and the louse suborder
Amblycera, providing support for a clade composed of these three
groups, although possible homoplasy was detected in some Ischnocera
(Yoshizawa & Johnson 2006) – supporting the polyphyly of lice.
Alternatively, parasitism may have evolved once and been subsequently
lost in the Liposcelididae (Murrell and Baker 2005). The close rela-
tionship between Phthiraptera and Liposcelididae, and the elevated
substitution rate of mtDNA appears to originate in the common ancestor
of Phthiraptera and Liposcelididae, and directly corresponds to an
increased G+C content (Yoshizawa & Johnson 2003). Thus, the relation
of lice and Strashilidae may be definitively excluded.
The phylogenetic relations of the Strashilidae are within holometabolans.
Based on the structure of male terminalia, with characteristic aedeagus,
the presence of a sucking beak, and articulated volsellae with gonostyli,
Strashilidae can be placed within Mecopteroidea (Rasnitsyn 1992). Their
unique morphology and a separate ordinal rank can be finally concluded
only after excluding the eventual placement within basal fleas. All things
being the equal, all living fleas are laterally compressed and this character
is considered as plesiomorphical within fleas (Grimaldi 2005), and
Mecoptera paraphyletic in respect to fleas as a sister group to Boreidae
are supported by molecular evidence based on 18S rDNA (Whiting 2002).
Byers (1996) indicates fleas have more in common with nematocerous
Diptera than with Mecoptera, and the sperm structure of Boreidae and
Siphonaptera differs significantly (Dallai et al. 2003), but the Mecoptera
+ Siphonaptera form a relatively well-supported monophyletic group.
However, the placement of Nannochorista as a sister group to the fleas
is not supported by a more extensive molecular and morphological
analysis (Whiting 2002), which argues for a sister group relationship
with Boreidae. The monophyly of Siphonaptera and Ceratophylloidea
(Leptopsyllidae+ Ceratophyllidae+ Ischnopsyllidae) is well supported.
However, phylogenetic relationships among fleas are poorly known
(Lewis & Lewis 1985).
In contrast, Strashilidae are flattened dorsoventrally, and possess a wide
pronotum, which excludes the possibility of presenting stem fleas - their
ordinal rank is thus entirely natural.
Another argument against the relation of the Strashilidae and
Siphonaptera is that the parasitism of fleas to flying vertebrates is a
phylogenetical novelty. Peculiarities of the host-parasite relationships
in the family Ischnopsyllidae consist of their connection with relatively
young bat families Vespertilionidae and Molossidae. Ischnopsyllidae
originated during the Paleocene or, more likely, during the terminal
Eocene- Oligocene in south-eastern Asia – from here on the tribes
Chriopteropsyllini and Ischnopsyllini spread over in Afrotropical, Indo-
Malayn and Golartic regions, the tribe Porribiini in Australia, while the
tribe Sternopsyllini in the Neotropical region. Ancestors of the tribe
Sternopsyllini reached South America via Australia and Antarctica. Fleas
of the tribe Nycteridopsyllini penetrated into North America from Asia
later via the Beringian bridge (Medvedev 1990).
The terminalia of Strashilidae are characteristic of holometabola and
related to the Mecopteroidea, but with primitive volselae, which allows
the attribution of the Strashilidae as a sister group to the Mecoptera, and
possibly Mecopteroidea. Terminalia of the Protomecoptera are unknown.
The analyses of coevolutionary relationships between host and parasite
phylogenies, is made extremely difficult by the complex interplay of
cospeciation, host switching, sorting (extinction), duplication (intrahost
speciation) and inertia (lack of parasite speciation) events, all of which
may produce incongruence between host and parasite phylogenies
(Paterson et Banks 2001)
The evolutionary history of mammal-flea associations has been shown
to involve mainly association by colonization with frequent host
switching, rather than association by descent (Traub, 1980; Krasnov &
Shenbrot, 2002; Lu & Wu, 2003).
Page et al. (1998) pointed out that the cytochrome b is evolving two to
three times more rapidly in lice than in birds, and louse cytochrome b
is highly divergent compared to that of most other insects.
Investigations into the coevolutionary history of seabirds (orders
Procellariiformes and Sphenisciformes) and their lice (order
Phthiraptera) and examination of the codivergent nodes revealed that
seabirds and lice have cospeciated synchronously and that lice have
evolved at around 5.5 times the rate of seabirds. (Paterson et al 2000).
Hafner & Nadler (1988) find a high degree of concordance in the
branching patterns of the trees, which suggests that there is a history
of cospeciation in this host–parasite assemblage. In several cases
where the branching patterns were identical in the host and parasite
phylogenies, the branch lengths were also very similar, suggesting that
the speciation of these hosts and ectoparasites was roughly contempo-
raneous and causally related.
The occurrence of numerous parasites in a single pterosaur host is ques-
tionable. In living hosts, some threshold of defence against parasites in
the host species is present, which limits the host's ability to cope with
multiple parasite species (e.g. because of presumably costly defence
systems - Schmid-Hempel & Egert 2003) but instead maintains their
pressure (expressed as a number of parasite species) at a 'tolerable'
level (Combes 2001).
Very little can be extracted about either principal (currently the one used
by the majority of individuals in the parasite population) and/or the
original (the one in which the parasite first evolved) host of the
Strashilidae. Attributing Strashilidae as pterosaur parasites is based on
the presence of strong claws on all extremities, long strong hindlegs
with distinct nippers (chela), adapted for membrane phoresy such as in
living bat insect ectoparasites (c.f., long legs of the Streblidae flies); and
an unsclerotised body apparently serving as a blood reservoir (Rasnitsyn
1992). These adaptations are even more apparent in the present genus
Vosila, where sclerite margins are unsclerotised in the center –
a homologue to that of living lice, and the nipper is plesiomorphically
adapted for phoresy on hairs with a circular diameter (compared with
pinsette-like in Strasila adapted for advaced, plain, hairs).
A blood feeding adaptation excludes the possibility of hair and/or
feather feeding, but cannibalism in pre-imaginal stages remains
obscure. In fleas, the larvae (except for Uropsylla tasmanica) are not
parasitic and feed on organic matter found in the nest of the host, but
third-instar larvae readily cannibalise naked pupae, however a complete
cocoon structure can protect pupa from cannibalism (Lawrence & Foil,
2002). Interspecific cannibalism during periods of food shortage might
be complicated by intraspecific cannibalism. A strong female bias
caused by their larger size during periods of lowest food availability
allows them to cannibalise males under conditions of food shortage
(Krasnov et al. 2005a).
Rich and diverse sensillar apparatus suggest a high variety of cues in
searching for hosts. Living fleas determine vibrations, increased concen-
tration of CO2, increased temperature, light (Benton & Lee 1965, Cox
et al. 1999, Humphries 1968) as well as host odour (Crum et al. 1974
and Vaughan & Mead-Briggs 1970).
The aquatic habits which may be excluded by analogy with living water
mammal ectoparasites. E.g., Antarctophthirus ogmorhini from the
Weddell seal Leptonychotes weddellii are: (1) the cuticle of the ventral
and lateral surfaces is 1:3 thinner than that of the dorsal surface, (2)
the body has numerous stiff spines which are covered by a thick layer
of the seal's sebum that closely surrounds the body of the louse, (3) the
whole body is covered by a close layer of leaf-like scales which are
apparently able to trap air bubbles and thus to provide a small zone of
air close to the surface of the cuticle (Mehlhorn et al 2002). However,
the function of gill-like appendages remains obscure.
In the future, the presence of ectoparasites may be investigated
indirectly by studying the presumable hosts. By analogy, feral pigeons
(Columba livia) with impaired preening, owing to slight bill deformities,
have higher louse loads (Phthiraptera: Insecta: Ischnocera) than
pigeons with normal bills. High louse loads reduce the survival of
pigeons, suggesting that lice select for efficient preening and against
bill deformities. In a reciprocal experiment, preening with a normal bill
selects for a small body size in lice, which may facilitate their escape
from preening (Clayton et al. 1999).
Most individuals of the parasite occur on a few host individuals, while
most host individuals have only a few, if any, parasites (Anderson & May
1978). Possible traits for preservation of the present specimens are
disarticulation from the host during preening near or directly in the water
or, although never found associated, from a dead vertebrate. The hosts'
diving behaviour can effectively influence ectoparasite (lice)
communities (Felso & Rozsa 2006). The present specimens apparently
fossilised completely without blood. Both specimens perhaps originated
from an exhausted animal which soon died in the water.
Generally, females survive longer than males at all air temperatures,
except for the highest temperature when the survival time of both sexes
was similarly low; males of both species survived for less time than
females at all RHs (Krasnov et al. 2002a). The preserved specimens
also perhaps represent at least once fed individuals, because newly
emerged fleas survived for a significantly longer time.
Even based on only four specimens, it must be noted that the sex is
most commonly female-biased in ectoparasites. One possible
explanation comes from the preservation potential, influenced by water
content, which is significantly higher in fed males: CO2emission rates
of the larvae exceed that of the adults by 2.6-fold and the pupae by 7.3
times. Water content differed between fed (range approx. 67–69% of
body mass) and newly emerged adults (range approx. 73–75% of body
mass). Although no differences were noted between the water content
of newly emerged males and females, fed males had significantly higher
water content than fed females. Adult males being the lightest 0,102mg
when unfed and fed adult females ca. 0,263mg (0,210 unfed) being the
heaviest. The decrease in water content of the females compared to the
males may reflect a greater accumulation of fat for subsequent egg
production (Fielden et al 2004)).
Krasnov et al. (2005c) validated the nutritional and/or energetic cost
of host resistance, measured as host-mediated parasite fitness loss, as
well as possible adaptive stress-induced immunosuppression (egg
production was significantly higher in fleas parasitizing underfed than
control animals. Survival of new generation imagos was lowest in fleas
from parents on hosts with the highest food limitation. By contrast,
survival of parent fleas was highest on hosts offered 30% of
maintenance energy intake. Food availability for hosts affected the
survival of eggs and larvae produced by fleas on these rodents, but did
not affect the survival of pupae. The highest larval survival was recorded
in fleas on rodents with 30% of maintenance energy intake).
The rarity of fossil parasites is not necessarily associated with the rarity
of host. Based on 57 flea-mammal associations from Slovakia, Stanko
et al. (2006) suggests that different flea-host associations are governed
by different regulating mechanisms, but different regulation
mechanisms may act simultaneously within the same flea-host associ-
ations (relationships between flea abundance or prevalence and host
abundance were either negative (23) or absent (34)).
The same source data (Krasnov et al. 2006b) reveal that mean
abundance and species richness of fleas increased with an increase in
host age, although the pressure of flea parasitism in terms of number
of fleas per unit host body surface decreased with host age. They also
found two different patterns - a peak of flea aggregation and a trough
of flea prevalence in animals of middle age classes, and an increase of
both flea aggregation and flea prevalence with host age.
Host size can be investigated by analogy - according to a positive rela-
tionship between body size and hair-shaft diameter (e.g., in pocket
gophers), a positive relationship between body size and head-groove
width (in chewing lice) and a positive relationship between gopher hair-
shaft diameter and louse head-groove width. Changes in body size of
chewing lice are driven by a mechanical relationship between the
parasite's head-groove dimension and the diameter of the hairs of its
host. Louse species living on larger host species may be larger simply
because their hosts have thicker hairs, which requires that the lice have
Nakridletia ord.n. (Insecta) – pterosaur parasites Vršanský, Ren and Shih, August 2010. Amba projekty 8(1): 1-16, Bratislava Nakridletia ord.n. (Insecta) – pterosaur parasites Vršanský, Ren and Shih, August 2010. Amba projekty 8(1): 1-16, Bratislava
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a wider head groove. The study of gopher hair-shaft diameter and louse
head-groove dimensions suggests that there is a 'lock-and-key' rela-
tionship between these two anatomical features (Morand et al. 2000).
Reed et al. (2000) examined the relationship between mammalian hair
diameter and body mass at interordinal, intrafamilial, intrageneric, and
intraspecific taxonomic levels and showed a significant, positive
allometric relationship between hair diameter and body size. The
allometric coefficient (alpha) ranged from 0.13 to 0.33. Within pocket
gophers (Geomyidae), a significant positive relationship exists between
hair diameter and rostral groove dimensions of their chewing lice,
Geomydoecus, which use the rostral groove to grasp the hairs of their
host. Coupled with previous evidence of a strong allometric relationship
between rostral groove width and louse body size, findings suggest that
hair diameter of the host is an important determinant of body size in
chewing lice that parasitize pocket gophers.
Large-bodied host species often harbor large-bodied parasites
(Harrison's rule). Whatever the reason, this rule does not hold true
in all body lice possibly because selection on body size is mediated
by community-level interactions between body lice (Johnson et
al. 2005).
The absence of nutrition finally resulting in the death of the host might
result in a decrease in size of the parasite (lice are variable in size
because conditions might change – Saxena 1988). Therefore, by
analogy, it is possible that the preserved specimens are on the lower
levels of the size variability scale.
Lice cannot establish viable populations on novel hosts that differ in
size from the native host. Lice could remain attached to, and feed on,
hosts varying in size by an order of magnitude. However, they could not
escape from preening on novel hosts that differed in size from the native
host (Clayton et al. 2003), which might be further support for the strict
specificity of the Strashilidae. This general prediction that parasites of
large-bodied host species, which tend to be long-lived, should specialize
on these hosts, whereas parasites of small host species, which
represent more ephemeral and less predictable resources, should
become generalists appears supported by independent living fleas
(Krasnov et al. 2006ac).
Fleas also develop specific anatomical features such as sclerotinised
helmets, ctenidia, spines and setae which anchor the flea within the host
fur to resist the host's grooming efforts, which correlates with particular
characteristics of the host's fur and grooming pattern (Traub 1985).
Figure 4. Supposed pterosaur parasite of the order Nakridletia ord.n. (Strashilidae): Strashila incredibilis Rasnitsyn, 1992. Late Jurassic, Mozgon
near Chita, Siberian Russia. Holotype PIN 3084/60 submerged in alcohol, under polarized light. a1) general habitus; a2) details of head and antenna;
a3) terminalia; a4) hind tarsus (PIN 3084/60 counterpart). Body 7mm long.
Figure 3. Supposed pterosaur parasites of the order Nakridletia ord.n. (Vosilidae), Middle Jurassic, Daohugou, Inner Mongolia, China: Vosila sinensis
Vršanský et Ren, gen. et sp.n. Holotype CNU-PARA-001. a1) general habitus; a2) detail of fore and middle femur and tarsus with sensillae; a3)
gill-like appendages (a2-3 submerged in alcohol). Abdomen 5mm long. b) Parazila saurica Vršanský et Ren, gen. et sp.n. Holotype. CNU-NN-PARA-002
submerged in alcohol; b1) general habitus b2) gill-like apperndages. Overal body length 5.7mm.
Nakridletia ord.n. (Insecta) – pterosaur parasites Vršanský, Ren and Shih, August 2010. Amba projekty 8(1): 1-16, Bratislava Nakridletia ord.n. (Insecta) – pterosaur parasites Vršanský, Ren and Shih, August 2010. Amba projekty 8(1): 1-16, Bratislava
8 – –9

Additionally, there is a positive correlation between body size and range
size (Brown 1995, Gaston and Blackburn 1996a, Gaston and Blackburn
1996b). Habitat specialization of a parasitic species can be considered
the equivalent of its host specificity, because a host represents the
habitat for a parasite. In general, host specific fleas have more restricted
geographical ranges than host opportunistic fleas. Flea species with a
broad geographic range are not only capable of exploiting more host
species, but they also exploit host species from a wider range of taxa
(Krasnov et al 2005e)
Further support for the specificity of the Strashillidae is within flea hosts
- larger hosts have fewer flea species, but fleas were more prevalent.
Increased host species richness correlated with flea species eye size
(Bossard 2006), extremely well developed in the Strashilidae.
Interestingly, increased flea species richness was correlated with larger
geographical ranges and the stable locomotion of hosts. Hosts from
habitats of moderately low productivity (sage and grass) and size 10-
33 g, had the highest flea species richness.
The effect of blood sucking parasites on the pterosaur host was perhaps
significant. Fifty fleas feeding on a gerbil consumed 3.68+/-1.19 mg of
blood, in total amounting to 34.3+/-1.8% of body mass of a starving
flea and only about 0.17% of the blood volume of the host. The average
daily metabolic rate of the parasitized gerbils (7.75 kJ g(-0.54)d(-1))
was 16% higher than that of non-parasitized gerbils (6.69 kJ g (-0.54)d(-
1)). In addition, at zero metabolizable energy intake, the parasitized
gerbils lost body mass at a faster rate than the non-parasitized gerbils
(4.34 vs 3.95% body mass d(-1)) (Khokhlova et al. 2002).
The host represents a geographic locality for the parasite, and the
distance between hosts - an extrinsic barrier – allopatric speciation in
one geographical area (Mc Coy 2003). More species are known to have
originated on the same host, such as human lice, and also some
Ichnocerans (Cruickshank et al 2001).
Phylogenetically, Strashilidae are more related to fleas, as
holometabolans, rather than lice, but the life cycle, by morphological
analogy, is presumed to be similar to lice. Lice are the only permanent
insect ectoparasites, exhibiting a high degree of host specificity, having
no parallel in most other metazoans. Their transmission occurs mostly
opportunistically when hosts are in close contact with each other, such
as during breeding. Specializations of ~3000 species in the diet of lice
underpin their major taxonomic divisions and they can be broadly
separated into those that feed on skin debris, feathers and fur, and those
that have specialized in blood feeding.
The origin of parasitism in Strashilidae appears to have a similar pattern
to lice. While Pthirapterans are abundant on birds, only 6% of the almost
2000 flea species parasitize birds (Marshall 1981).
The superficial resemblance with the primate attacking Pediculidae is
surprising, being most probably the result of the social life of pterosaur
or eventually an unknown group of flying homeiothermous vertebrates.
Anoplura and also Pediculidae indicate close relationships between
hosts of related taxa.
The Strashilidae exhibit a high degree of specialisation: Vosilidae in
possessing unique gill-like filaments, Strashilidae with a pinsette-like
nipper being adapted for phoresy by attachment on plain hairs.
Nevertheless, sharing a host can not be excluded – e.g., a significant
positive relationship between the numbers of host species infested by
flea sister species was found (Mouillot at al. 2006).
The rationale for the nestedness (the nestedness-anti-nestedness
continuum observed in endoparasites is via selective accumulation of
parasite species rather than interactions among those parasite species
(Poulin and Valtonen 2001)) in parasite communities is that nested
species subsets are a common pattern in many types of communities
found in insular or fragmented habitats (Patterson and Atmar 1986,
Bolger et al. 1991). Hosts can be considered as biological islands at
three levels: host individual influenced by epizootical processes, host
population influenced by biogeographical processes, and host species
(Kuris et al. 1980).
Lice can infest all places with trichia, including eyelashes (Shan 1990).
Apparent asymmetry in hidlegs of both species is also notable where
the right femur is significantly more robust. This might be the result of
lateral crab-like movements, similar to that of Pthirus pubis (Pediculidae)
which also resembles crustaceans in notum fusion and in the nipper.
Earlier, it was presumed, that parasites, with their reduced morphological
complexity fitted well into their mode of life and were good examples of
evolution's inexorable march into dead ends (Noble and Noble 1976).
Nevertheless, transitions from specialist to generalist strategies have
occurred more frequently than the reverse during the evolutionary history
of tachinid flies, a group of endoparasitoids of insect hosts - generalist
tachinid species tend to be the most derived, i.e., they tend to occupy
branch tips in the phylogeny of the group (Stireman 2005).
Among flea species, generalists exploiting many host species consis-
tently achieve a higher abundance (mean number of fleas per individual
host) than specialists using only one or very few host species (Krasnov
et al. 2004c) and evolutionary changes in host specificity are clearly
reversible (Krasnov et al 2006c). Asymmetrical competition where the
generalist is expected to be more sensitive to competition than the
specialist is supported for parasites (Dawson et al. 2000; Perlman &
Jaenike, 2001).
Nevertheless, the extinction of the present order might have been
caused by their presumed strict specialisation, which disallowed host
switching, as was commonly observed in population peaks of living fleas
(Krasnov et al. 2004b).
Additionally, Poulin et al. (2006) found positive relationships between the
number of host species used and clade rank across all of his 297 studied
species, as well as within one of four large families and one of seven large
genera investigated separately, suggesting the specificity may have
tended to decrease in many flea lineages, a process that could have been
driven by the benefits of exploiting a wide range of host species.
Krasnov et al. (2004a) suggests that host specificity in fleas is to a large
extent phylogenetically constrained, while still strongly influenced by
local environmental conditions - in the majority of cases, the taxonomic
distinctness of the hosts exploited by a flea is no different from that of
random subsets; host specificity varies significantly more among flea
species than within flea species and in the vast majority of flea species,
neither of our two measures of host specificity correlated with either
the regional number of potential host species or their taxonomic
distinctness, or the distance between the sampled region and the center
of the flea's geographical range. However, in most flea species host
specificity correlated with measures in the deviation of climatic
conditions (precipitation and temperature) between the sampled region
and the average conditions computed across the flea's entire range.
Although there was a conducted and experimental interspecific
hybridization between Nosopsyllus fasciatus and N. mokrzeckyi
(Yakunin & Kunitskaya 1992), the genetic differentiation between
populations of conspecific lice on different host species in two studied
genera of lice identified substantial, 10-20% sequence divergence - in the
range of that often observed between species of these two genera.
(Johnson et al. 2002). The louse 12S rRNA domain III secondary structure
displays considerable variation compared to other insects, in both the
shape and number of stems and loops, which confirms the highly
distinctive nature of molecular evolution in these insects (Page et al. 2002).
Extanct insect ectoparasites can be attributed to two main ecological
groups, each represented by a separate order: 1) hemimetabolous lice –
i.e., without pupa, living the entire cycle on the host and 2) holometabolous
fleas with alternating periods on the hosts and periods in the hosts'
burrows or nests – the larvae are free-living, feeding on organic debris.
According to the morphology (see below), the life cycle of the
Strashilidae was perhaps more similar to lice – i.e., certain stages spend
their lives on the host, unlike most fleas, in which all immature stages
except adults are spent off the host. Specifically, like, restricted to
mammals Anoplura, feeding solely on blood, unlike Amblycera which
chew away at younger feathers and soft areas of the skin, causing
localized bleeding from which some can drink, and also unlike the avian
site specific Ischnocera drilling through thick skin.
Nevertheless, many flea larvae also feed not only on organic debris but
also on the dried blood of the host obtained through the faeces of adults
(Krasnov et al. 2005d).
In contrast to fleas, which survived separated from their host (Meles
meles) for 89 days, with 50% mortality at 35 days, lice survived only 3
days, which can significantly support the badger's habit of frequently
swapping dens with a mean period of return of 6 days. This is unlikely
to bring about significant mortality of adult fleas but may effectively
eradicate lice (Cox et al. 1999). Pthirus pubis, is relatively immobile
when on the host, remaining attached and feeding for hours or days on
one spot without removing its mouth parts from the skin. Neither larvae
not adults can survive more than twenty-four hours without feeding -
bluish-gray discoloration of the skin is due to poisonous saliva injected
by the crab louse, similar to the melanoderma caused by the body louse
(Riley & Johannsen 1938).
The mature adults live for about 15 to 25 days. Neither nymphs nor
adults move about very much. While feeding, a crab louse grabs human
hairs with at least one of its second or third legs which are adapted for
this purpose. Lice do move about slowly after molting.
Dispersion is mostly by adult stages, and is unaffected by sex, age and
blood gender of host and neither population density nor hunger (Takano-
Lee et al. 2005). Low infestation is also characteristic for time after
hibernation (Sosnina & Davidov 1975).
After emergence from the pupa and cocoon, adult fleas must locate a
suitable host to complete their life cycle (Ioff 1941). Since a host may
not always return in a regular or predictable manner to its nest or resting
area, the survival of fleas depends in part on their ability to use other
host species (Sarfati et al. 2005). This is apparently not the case for
Vosilidae, which are presumed to be strictly specific.
By analogy, birds in arid regions have fewer ectoparasitic lice than birds
in humid regions. Low humidity reduces the number of lice, even when
host defenses are held constant, which confirms this abiotic factor being
substantial for parasite pressure and suggests that humidity may
influence host life history evolution through its impact on ectoparasites
(Moyer et al. 2002).
Dispersal of avian ectoparasites can occur through either vertical trans-
mission from adult birds to their offspring in the nest or through
horizontal transmission between adult birds or through phoresy. Chewing
lice are mainly horizontally transmitted among adults (bee-eater) and
mainly among pair members, whereas vertical transmission between
parents and nestlings is less frequent (Darolova & Krištofík 2001).
Parasites face a trade-off between the choice to attack less defended
but lower-quality, vs more defended but higher-quality hosts. The repro-
ductive output of a parasite will be higher when exploiting energy
deprived hosts if the fitness increment due to reduced host defences is
higher than the fitness decline due to lower quality of resources
extracted from a host (Krasnov et al. 2005cd).
Darskaya (1970b) and Vatschenok (1988) proposed a classification of
fleas based on their annual cycle patterns as follows: (1) adult fleas active
and reproduce all year-round; (2) adult fleas active all year-round, but
reproduce in warm season only; (3) adult fleas active and reproduce in
warm season only; (4) adult fleas active and reproduce most of the year,
except for the hottest and driest periods when fleas survive in cocoons;
and (5) adult fleas active and reproduce only in the cold season.
The parasite population might have multiple peaks, and/or activity may
be restricted to a particular season such as winter in arid areas. At the
beginning of the activity, it is often female-biased, often cocooning
during the summer. The female bias during the early phase of activity
may be considered as reproductive pre-adaptation allowing for a fast
population increase (Krasnov et al. 2002b).
Hawlena et al. (2005) found flea distribution changed as a function of
flea density-from juvenile-biased flea parasitism (the "poorly fed host"
hypothesis) at low densities to adult-biased flea parasitism (the "well-
fed host" hypothesis) at high densities. Other factors that influenced
flea preference were soil temperature and the presence of ticks.
The host may not always return in a regular or predictable manner to
its nest or resting area where the immature fleas develop. The survival
and reproduction of fleas are therefore dependent on a combination of
environmental factors, including favourable climatic conditions for the
development of the immature stages and for adults to survive unpre-
dictable and sometimes lengthy periods without a bloodmeal. This
dependence results in seasonal changes of flea life history parameters,
e.g. their abundance, pattern of parasitizing of hosts and rate of repro-
duction (Marshall 1981).
Insect ectoparasites such as the present extinct species, were exposed
to strong and/or specific immune attacks because of the association
with host major immune defence systems in blood and skin associated
Nakridletia ord.n. (Insecta) – pterosaur parasites Vršanský, Ren and Shih, August 2010. Amba projekty 8(1): 1-16, Bratislava Nakridletia ord.n. (Insecta) – pterosaur parasites Vršanský, Ren and Shih, August 2010. Amba projekty 8(1): 1-16, Bratislava
10 – –11

lymphoid tissues (Wikel 1996). Additionally, digestion in ectoparasites
such as fleas is intracellular and they lack a peritrophic membrane
(Vatschenok 1988) which, in many arthropods, separates ingested food
from the gut epithelium and, thus, may restrict penetration of ingested
immune effector components (Eiseman & Binnengton 1994).
Even surface feeding sheep louse (Bovicola ovis) ingesting lipid, scurf,
bacteria and loose stratum corneum squames, stimulate an immune
response in sheep and this response may play a part in regulating the
size of louse populations (James 1999).
Apparently, even the weak attack of a parasite triggers the immune
system. However, this system could not overcome an attack by a large
number of fleas, perhaps due to their additive immunosuppression effect
and the cost of the immune system (Schmid-Hempel & Egert 2003).
Activation of an immune response and even maintenance of a competent
immune system is an energetically demanding process that requires trade-
off decisions among competing energy demands for growth, reproduction,
thermoregulation, work and immunity (Sheldon & Verhulst 1996).
As a result, in many non-tropical vertebrate animals, disease prevalence
is increased during periods of food shortage compared with periods
when food is readily available (Lochmiller, Vestey & McMurray 1994).
However, if food limitation occurs in a predictable manner (e.g., seasonally),
it can be advantageous to suppress other functions, including repro-
duction, rather than suppress the immune function. Indeed, the 'winter
immunoenhancement hypothesis' was suggested by Nelson & Demas
(1996) to explain the increase in the immune parameters during winter
reproduction break in small mammals from temperate environments
(Lochmiller & Dabbert 1993; Lochmiller et al. 1994).
Furthermore, stress, such as food limitation, may activate the hypo-
thalamic–pituitary–adrenal axis and increase plasma levels of
glucocorticoid steroids (Råberg et al. 1999) which are largely immuno-
suppressive. Indeed, reduced food availability was shown to elevate
corticosterone concentrations and suppress immune function (Demas
& Nelson 1998). Råberg et al. (1999) argued that immunosuppression
via neuroendocrine mechanisms is adaptive because it allows the
avoidance of hyperactivation and subsequent immunopathology during
stressful situations.
An important link to the living host includes males being generally less
immunocompetentand more susceptible to parasites than females (e.g.
Olsen and Kovacs, 1996; Poulin, 1996; Schalk and Forbes, 1997),
resulting from the immunosuppressive function of androgens (Folstad
and Karter, 1992) and a higher level of circulating immune complexes
in females than in males (Khokholova et al 2004).
Some components of host immune defences may operate simultane-
ously against all kinds of parasites, whereas investment by the host into
specific defences against one type of parasite may come at the expense
of defence against other parasites, which suggests the existence of a
process of apparent facilitation among unrelated taxa in the organization
of parasite communities (Krasnov et al. 2005b). Authors proposed
explanations based on host immune responses, involving acquired
cross-resistance to infection and interspecific variation in immunocom-
petence among hosts.
Acknowledgemens.
We thank Prof. AP Rasnitsyn, Graeme Butler and an anonymous
reviewer for fruitful advice, revision of the manuscript and linguistical
correction, Dr. J. Krištofík and Dr. Cyprich for lice literature supply and
help, and Martin Česanek for editorial help and layout. Supported by
the UNESCO-Amba, IGCP 458; National Natural Science Foundation of
China (Nos. 30430100, 40872022), the Nature Science Foundation
of Beijing (No. 5082002), Scientific Research Key Program
(KZ200910028005) and PHR Project of Beijing Municipal Commission
of Education; VEGA 6002, 2/0125/09, MVTS and the Literary Fund.
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Finalized: December 19, 2008
Printed and disseminated: August 25, 2010
Free access: http://fossilinsects.net/lib.htm
ISBN: 978-80-970488-6-0
Nakridletia ord.n. (Insecta) – pterosaur parasites Vršanský, Ren and Shih, August 2010. Amba projekty 8(1): 1-16, Bratislava
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