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Roisinitermes Ebogoensis Gen. & Sp. n., an Outstanding Drywood Termite with Snapping Soldiers from Cameroon (Isoptera, Kalotermitidae)

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Termites have developed a wide array of defensive mechanisms. One of them is the mandibulate soldier caste that crushes or pierces their enemies. However, in several lineages of Termitinae, soldiers have long and slender mandibles that cannot bite but, instead, snap and deliver powerful strikes to their opponents. Here, we use morphological and molecular evidence to describe Roisinitermesebogoensis Scheffrahn, gen. & sp. n. from near Mbalmayo, Cameroon. Soldiers of R.ebogoensis are unique among all other kalotermitid soldiers in that they possess snapping mandibles. The imago of R.ebogoensis is also easily distinguished from all other Kalotermitidae by the lack of ocelli. Our study reveals a new case of parallel evolution of snapping mandibles in termites, a complex apparatus responsible of one of the fastest biological acceleration rates measured to date.
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Roisinitermes ebogoensis gen. & sp. n., an outstanding drywood termite... 91
Roisinitermes ebogoensis gen. & sp. n., an outstanding
drywood termite with snapping soldiers from
Cameroon (Isoptera, Kalotermitidae)
Rudolf H. Scherahn1, omas Bourguignon2,3, Pierre Dieudonné Akama4,
David Sillam-Dussès5,6, Jan Šobotník3
1 Fort Lauderdale Research and Education Center, Institute for Food and Agricultural Sciences, 3205 College
Avenue, Davie, Florida 33314, USA 2 Okinawa Institute of Science & Technology Graduate University,
1919-1 Tancha, Onna-son, Okinawa 904-0495, Japan 3 Faculty of Forestry and Wood Sciences, Czech Uni-
versity of Life Sciences, Prague, Czech Republic 4 Département des sciences biologiques, Ecole normale supérieu-
re, Université de Yaoundé I, BP 47 Yaoundé, Cameroon 5 University Paris 13 - Sorbonne Paris Cité, LEEC,
EA4443, Villetaneuse, France 6 IRD – Sorbonne Universités, iEES-Paris, Bondy, France
Corresponding author: Rudolf H. Scherahn (rhsc@u.edu)
Academic editor: P. Stoev | Received 5 July 2018 | Accepted 27 August 2018 | Published 2 August 2018
http://zoobank.org/C6973DAD-84F4-4C54-87D0-4EDFBEDFF161
Citation: Scherahn RH, Bourguignon T, Akama PD, Sillam-Dussès D, Šobotník J (2018) Roisinitermes ebogoensis
gen. & sp. n., an outstanding drywood termite with snapping soldiers from Cameroon (Isoptera, Kalotermitidae).
ZooKeys 787: 91–105. https://doi.org/10.3897/zookeys.787.28195
Abstract
Termites have developed a wide array of defensive mechanisms. One of them is the mandibulate soldier
caste that crushes or pierces their enemies. However, in several lineages of Termitinae, soldiers have
long and slender mandibles that cannot bite but, instead, snap and deliver powerful strikes to their
opponents. Here, we use morphological and molecular evidence to describe Roisinitermes ebogoensis
Scherahn, gen.& sp. n. from near Mbalmayo, Cameroon. Soldiers of R. ebogoensis are unique among
all other kalotermitid soldiers in that they possess snapping mandibles. e imago of R. ebogoensis is also
easily distinguished from all other Kalotermitidae by the lack of ocelli. Our study reveals a new case of
parallel evolution of snapping mandibles in termites, a complex apparatus responsible of one of the fast-
est biological acceleration rates measured to date.
Keywords
Ethiopian Region, mandibles, ocellus, taxonomy
ZooKeys 787: 91–105 (2018)
doi: 10.3897/zookeys.787.28195
http://zookeys.pensoft.net
Copyright Rudolf H. Scheffrahn et al. This is an open access article distributed under the terms of the Creative Commons Attribution License
(CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
RESEARCH ARTICLE
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Rudolf H. Scherahn et al. / ZooKeys 787: 91–105 (2018)
92
Introduction
Termites are extremely abundant (Martius 1994, Eggleton et al. 1996) and colonies
may contain millions of individuals attracting a wide variety of predators (Deligne et
al. 1981). Additionally, termites experience strong intra- and inter-specic competi-
tion (Levings and Adams 1984, orne and Haverty 1991). To combat against the
plethora of agonistic opponents, termites have developed a rich array of defensive strat-
egies. e most important defenses are expressed in the soldier caste that is ancestral to
all extent termites (Roisin 2000).
Soldiers are specialized sterile colony defenders possessing exaggerated morphology
of the head and mandibles (Prestwich 1984). One of their most intriguing defenses is
exemplied by long and slender snapping mandibles (Deligne et al. 1981). e snap-
ping mandibles are paired with muscles to store potential energy which, when released,
delivers a powerful strike producing one of the fastest accelerations known among
animals (Seid et al. 2008). All termite species with snapping soldiers described so far
belong to the Termitinae (Bourguignon et al. 2017), suggesting that snapping soldiers
evolved several times independently within this subfamily. Alternatively, soldiers with
snapping mandibles might have evolved once, and independently reverted to a biting
strategy in several lineages.
e monophyletic family Kalotermitidae (Inward et al. 2007) constitutes almost
half of all “lower termite” genera and species (Krishna et al. 2013) and has fossil re-
cords to the mid-Cretaceous (Engel et al. 2009). Kalotermitids live entirely in wood as
“one-piece” nesters (Abe 1987) which facilitates transoceanic dispersal (Scherahn and
Postle 2013). Kalotermitids occur in all ecozones and numerous genera have vast dis-
tributions (e.g. Calcaritermes, Cryptotermes, Glyptotermes, Kalotermes, Marginitermes,
Neotermes, and Procryptotermes). A few species of Cryptotermes (Scherahn et al. 2009)
and Incisitermes (James et al. 2013, Yasuda et al. 2003) have also been dispersed by hu-
man activity. A few species are major pests of dry wood (Su and Scherahn 2000) or
minor pests of tree crops (Constantino 2002).
e monumental revision of the Kalotermitidae by Krishna (1961) provided the
morphological diagnoses for all extant genera with the exception of the recently de-
scribed Longicaputermes (Ghesini et al. 2014). Aside from Longicaputermes, all new
kalotermitid species described after Krishnas 1961 revision, ca. 115, have been as-
signed to one of the 21 genera he recognized. e soldier caste of several genera has
unmistakable characters: e.g., the scooped out frons of Eucryptotermes, the massive
third antennal article of Marginitermes, the large ovoid head of Pterotermes, or the
spur on the fore tibia of Calcaritermes. We herein describe a new genus and species
of Kalotermitidae, Roisinitermes ebogoensis, which possesses equally unmistakable
soldiers. e soldier of R. ebogoensis is the rst outside the Termitinae to have snap-
ping mandibles.
Roisinitermes ebogoensis gen. & sp. n., an outstanding drywood termite... 93
Material and methods
Illustrations and measurements
Images of individuals were taken as multi-layer montages using a Leica M205C stere-
omicroscope with a Leica DFC 425 module run with Leica Application Suite software
version 3. Preserved specimens, stored in 85% ethanol, were positioned in a transparent
petri dish lled with Purell hand sanitizer (70% EtOH). Measurements (Tables1–2)
were obtained using an Olympus SZH stereomicroscope tted with an ocular microm-
eter. A eld photograph of live specimens placed in a small paper-lined Petri dish was
taken with a Canon EOS 5DS R combined with a Canon EF 100mm f/2.8L Macro IS
USM lens. Morphological terminology follows that of Krishna (1961).
Phylogenetic analyses
DNA was extracted from ve individuals of R. ebogoensis, after removal of the di-
gestive tract. e full mitochondrial genome was amplied with TaKaRa LA Taq in
two long PCR reactions using primers specically designed for termites (Bourguignon
etal. 2016). Long PCR fragments were pooled in equimolar concentration, and 75-
bp paired-end reads were obtained using Illumina MiSeq. We subsampled a total of
10,000 reads and assembled the full mitochondrial genome with SPAdes, under default
parameters (Bankevich et al. 2012). e total coverage of the assembly was 82-fold.
We used the mitochondrial genomes of ten species of Kalotermitidae, including
one sample of Roisinitermes ebogoensis sequenced in this study. We used four non-Ka-
lotermitidae termite species as outgroups to root the tree: Zootermopsis angusticollis,
Hodotermopsis sjostedti, Coptotermes sjostedti, and Termitogeton planus. All mitochon-
drial genomes, except that of R. ebogoensis, have been published recently (Suppl. mate-
rial1: Table S1). Each gene of the mitochondrial genome was aligned separately using
MAFFT v7.300b with the option “--maxiterate 1000 --globalpair” for higher accuracy.
For protein-coding genes, we rst aligned genes as protein, then converted protein se-
quence alignments into the corresponding codon alignments using PAL2NAL (Suyama
et al. 2006). e 22 tRNAs and the two ribosomal RNAs were aligned as DNA. e
resulting alignments were concatenated with FASTconCAT v1 (Kück and Meusemann
2010). Alignments were separated in ve partitions: one for each codon position of the
protein-coding genes, one for the combined ribosomal RNA genes, and one for the
combined tRNA genes.
We reconstructed phylogenetic trees using Maximum Likelihood and Bayesian
approaches. We ran the analyses twice, once with the third codon position included,
and once without third codon position. e Bayesian phylogenies were implemented
Rudolf H. Scherahn et al. / ZooKeys 787: 91–105 (2018)
94
in MrBayes 3.2 (Ronquist et al. 2012) with unlinked partitions, each of four chains
(three hot and one cold). e chain length was of two million generations with sam-
pling every 2000 generations. 800,000 generations were discarded as burnin, to en-
sure that the chain reached convergence, as determined by Tracer 1.5 (Rambaut and
Drummond 2007). We ran two replicates of each analysis to ensure consistency of the
results. For each partition of the data, we assigned an independent Generalized Time
Reversible model with gamma-distributed rate variation across sites and a propor-
tion of invariable sites (GTR + G +I). e reconstruction of Maximum Likelihood
phylogenies was carried out with RAxML (Stamatakis et al. 2008). We used the GTR-
GAMMA model of rate heterogeneity across sites. Node support was estimated using
1000 bootstrap replicates.
Results
Phylogenetic analysis
Our phylogenetic analyses supported the monophyly of Kalotermitidae (Figure 1).
e four analyses yielded identical tree topologies, with one exception: in the Bayesian
analysis without third codon position Rugitermes was the sister group of Neotermes +
Cryptotermes + Incisitermes + Roisinitermes, while in the other three analyses Rugitermes
+ Neotermes sp. A formed the sister group of Neotermes insularis + Cryptotermes +
Incisitermes + Roisinitermes. Roisinitermes was consistently placed next to N. insularis.
Systematics
Roisinitermes Scherahn, gen. n.
http://zoobank.org/9AE40F98-CA9E-45AC-849E-A034F19E8DAE
Type-species. Roisinitermes ebogoensis Scherahn sp. n.
Winged Imago. Ocelli not visible either by pigmentation or cuticular protrusion
(Figure 2A–C). Fore wing with unsclerotized media and cubitus arising from a com-
mon vein distal from scale suture; radial sector with 5–6 anterior branches; subcosta
very close and dicult to discern from costal margin (Figure 2D). Hind wing with
radial sector and cubitus arising from a common vein distal to suture. Tibial spurs
3:3:3; tarsi without arolia. e left imago/nymph mandible with anterior margin of
their marginal tooth ca. 1.5 times longer than length of the posterior margin of the rst
plus second marginal tooth; right mandible with posterior margin of second marginal
tooth 1.4 times as long as molar plate (Figure 3).
Diagnosis. e lack of visible ocelli is unique among all other Kalotermitidae. In
Krishnas 1961 generic key, Roisinitermes would lead to couplet 2 (Epicalotermes).
Roisinitermes ebogoensis gen. & sp. n., an outstanding drywood termite... 95
Figure 1. Phylogenetic tree of Kalotermitidae based on full mitochondrial genomes. e tree depicted
was reconstructed with RAxML using the data matrix without third codon position. Node labels are the
Maximum Likelihood bootstrap supports and the Bayesian posterior probabilities in the following order,
from left to right: posterior probability of the analysis with third codon position included, posterior prob-
ability of the analysis without third codon position, bootstrap support of the analysis with third codon
position included, bootstrap support of the analysis without third codon position, *indicates 100% boot-
strap support and 1.0 posterior probability for all four analyses.
Soldier. Monomorphic (Figs 4, 5). Eye spots prominent; large, dark brown. Frons
bilobed in dorsal view, crested with rugose longitudinal wrinkles, rugosity below frons
oriented longitudinally. Small horn-like projection at terminus of ventral genae. Man-
dibles sticklike; downward arching in lateral view. Dentition very weak; basal humps
project sharply.
Diagnosis. Stick-like mandibles unique among all other kalotermitid soldiers. In
Krishnas 1961 key, Roisinitermes leads to couplet 17 (Allotermes). In dorsal view, the
mandibular blades of Allotermes, especially A. denticulatus Krishna 1962, somewhat
resemble those of Roisinitermes as those of the former are long, rather narrow and with
rudimentary dentition. In lateral view, however, the Roisinititermes mandibles dier
from all other kalotermitids with projecting mandibles in that the Roisinitermes mandi-
bles arch downward. Although the Roisinitermes imago venation and dentition is very
similar to those of Epicalotermes, the soldier of Roisinitermes shares no major characters
with the Epicalotermes soldier.
Etymology. e genus is named in honor of Dr. Yves Roisin for his many contri-
butions to the study of termites.
Rudolf H. Scherahn et al. / ZooKeys 787: 91–105 (2018)
96
Figure 2. Imago of Roisinitermes ebogoensis gen. & sp. n. A Dorsal view of head and thorax B Oblique
view of head C Lateral view of head and thorax D Right forewing (arrow on subcosta) and right hind wing.
Roisinitermes ebogoensis Scherahn, sp. n.
http://zoobank.org/129573FB-E5DE-4673-9E1B-EF062D413FEB
Material examined. Holotype. Soldier from colony UF no. AFR3327. CAMEROON:
Ebogo II, (+3.37723N, +11.46135E), 647 m elev., 18FEB18, col. Raphael Onana,
AFR3327 ca. 500 alates, 50 soldiers, and many pseudergates, nymphs, larvae, and
eggs. Paratypes. CAMEROON, Ebogo II (+3.38273N, +11.46190E), 664 m elev.,
10DEC2016, col. Jan Šobotník and collaborators, AFR2982 4 soldiers (1 damaged),
one female dealate, and 46 brachypterous nymphs.
Diagnosis. See generic diagnosis above.
Description. Winged Imago (Figure 2, Table 1) Head and pronotum light brown-
ish orange; eye ovoid, anterior margin truncate abdominal tergites lighter, concolorous
with legsand labrum; postclypeus nearly hyaline. Compound eyes black, of medium
size and protrusion; ellipsoid but truncated near antennal socket, composed of approx-
imately 85 facets. Ocelli not visible either by pigmentation or cuticular protrusion.
Antennae with more than nine articles; formula 1>2=3=4<5. Pronotum width twice
that of median length; several long and shorter setae project from lateral margins. Fore
wing scale with basal origins of all major veins; wing membrane covered with papillae.
Tibial spurs 3:3:3; tarsi without arolia.
Soldier (Figs 4–6; Table 2) Monomorphic. In dorsal view, head capsule yellowish
orange in posterior grading to orange in middle and reddish brown from frons to ante-
Roisinitermes ebogoensis gen. & sp. n., an outstanding drywood termite... 97
clypeus. ree proximal antennal articles sepia brown; distal articles light brown. Post
clypeus and labrum yellowish with brown highlights. Eye spots prominent; large, dark
brown, elliptical; formed from a mass of discrete ommatidia. Pronotum concolorous
with posterior head capsule. Head capsule in dorsal view, subrectangular; lateral mar-
gins nearly parallel, length 1.5 times width. Posterior corners of head evenly rounded;
Figure 3. Brachypterous nymph of Roisinitermes ebogoensis gen. & sp. n. Top: Dorsal view of mandibles.
Bottom: lateral view of head and thorax.
Rudolf H. Scherahn et al. / ZooKeys 787: 91–105 (2018)
98
posterior margin rectate. In lateral and oblique view, head capsule almost cylindrical
with only slight dorso-ventral compression; frons bilobed in dorsal view, crested with
rugose longitudinal stripes, rugosity lateral below frons to mandibles. In lateral view,
frons sloping from vertex ~45°; mandibles bow upward to form a 15° arch. Setae short
and sparse on pronotum and head capsule. Periantennal carina rugose, in dorsal view
partially eclipsing the rst antennal article. Small horn-like projection at terminus of
ventral genae. Mandibles stick-like; long, blade narrower in middle than distal third,
dentition very weak; left mandible with faint equilateral tooth approx. three fths
from base, serrations along blade from tooth to tip. Right mandible with single tooth
approx. one third distance from base; blade narrowest before tooth; after tooth blade
widens slightly and then gradually narrows at tip. In dorsal view, basal humps project
sharply as rugose hemispheres. In lateral view, humps are columnar and equal in height
to that of the mandibles. Anteclypeus shallowly incised in middle; labrum linguiform
with gradual point; 4–5 long terminal setae. Antennae with 12–13 articles, third an-
tennal article subclavate, barely shorter than fourth and fth combined. Pronotum
collar-shaped; much wider than long. Anterior margin weakly concave; lateral margins
weakly convex, posterior margin forming 25° angle with incised middle. Femora mod-
erately inated, tibial spurs 3:3:3. Habitus as in Figure 6.
Brachypterous nymph (Fig. 3, Table 3) Body hyaline. Head, thorax, and abdo-
men similar in shape and pilosity of imago. Compound eyes with approx. 85 dark
Table 1. Measurements (mm) of Roisinitermes ebogoensis alates from a single colony.
Males (n=6) Females (n=6)
Measurement max min mean max min mean
Head max. width 1.05 0.95 1.00 1.05 1.00 1.03
Pronotum max. width 1.00 0.89 0.96 1.05 0.93 1.01
No. antennal articles 15 14 14.67 17.00 14.00 15.17
Max diam. eye 0.40 0.32 0.36 0.39 0.35 0.37
Body length with wings 9.63 8.63 9.10 9.88 9.50 9.65
Fore wing length (suture to tip) 7.50 6.80 7.20 7.80 7.20 7.43
Table 2. Measurements of Roisinitermes ebogoensis soldier (n=17 from two colonies).
Measurement Max Min Mean
Head length to lateral mandible base 1.92 1.60 1.79
Head width, maximum 1.28 1.18 1.22
Head height with gula, max. 1.08 0.92 1.00
Pronotum length 0.70 0.56 0.65
Pronotum width 1.18 1.05 1.13
No. antennal articles 14 10 12.70
Left mandible width @ basal humps 0.35 0.21 0.26
Left mandible width @ middle 0.18 0.16 0.17
Max. diam. eye 0.26 0.18 0.21
Length left mandible from condyle (ventral) 1.78 1.46 1.66
Roisinitermes ebogoensis gen. & sp. n., an outstanding drywood termite... 99
Figure 4. Soldier (holotype) of Roisinitermes ebogoensis gen. & sp. n. Dorsal (A), lateral (B), and ven-
tral(C) views of head and pronotum.
Rudolf H. Scherahn et al. / ZooKeys 787: 91–105 (2018)
100
Figure 5. Dorsal view of frons and mandibles of Roisinitermes ebogoensis gen. n. sp. n. Inset: oblique
ventral view of columnar hump (arrow).
facets; both eyes and facets smaller than imago. Antennae with 15 articles; formula
1>2>3=4=5. Left mandible with anterior margin of marginal tooth 1.5 times longer
than length of the posterior margin of the rst plus second marginal tooth. Right man-
dible with posterior margin of second marginal tooth 1.4 times as long as molar plate.
Biology and distribution. e type colony of R. ebogoensis was collected in the
forest on an island in the Nyong River near the Ebogo II village. e colony lived in a
Table 3. Measurements (mm) of Roisinitermes ebogoensis brachypterous nymph (n=10).
Measurement Max Min Mean
Head max. width 1.10 1.00 1.07
Pronotum max. width 1.16 1.08 1.11
No. antennal articles 15 15 15
Maximum diam. eye 0.20 0.20 0.20
Roisinitermes ebogoensis gen. & sp. n., an outstanding drywood termite... 101
relatively thin (3 cm) and long (over 3 m) broad-leaf tree branch suspended from the
canopy approximately 2 m above the ground. e colony contained roughly 2,000
members. A second colony of R. ebogoensis was collected in a nearly pristine rain forest
near the village of Ebogo II. e colony was taken from a dead liana branch (ca. 15
mm diam.) hanging from the canopy at a height of approx. 1 m above the ground.
Liana stems have been generally overlooked as a colonization site for Kalotermitidae
(Scherahn et al. 2018). In light of Emersons 1925 description of Cryptotermes cubio-
ceps from a single soldier collected from a dead liana, this host should be probed rou-
tinely as a colonization site for kalotermitids.
Etymology. e species is named for the village of Ebogo II, the type locality for
this termite.
Discussion
Kalotermitids inhabit a single woody item and are largely unable to move to a new
food source once the original is exhausted. e lone exception is Paraneotermes sim-
plicicornis that builds underground galleries connecting several wood pieces (Light
1937). e ability to feed on sound wood represents a defensive adaptation in itself
as the hard food source acts as an ecient physical barrier against intruders. Kaloter-
mitids thus show low soldier-to-worker ratios (see Haverty 1977) and soldiers reach
a high level of polymorphism, reected especially in the development of the headcap-
Figure 6. Live habitus of soldier and brachypterous nymphs of Roisinitermes ebogoensis gen.et sp. n.
Rudolf H. Scherahn et al. / ZooKeys 787: 91–105 (2018)
102
sule and mandibles. Some genera such as Bicornitermes, Cryptotermes, Eucryptotermes,
Calcaritermes, or Glyptotermes, possess very short mandibles and a plug-like headcap-
sule to prevent intruder entry into a nest gallery (phragmosis). In C. cryptognathus
from Jamaica, the mandibles are reduced to small stubs that do not project beyond the
frontogenal boundaries of the head capsule, and therefore cannot be used to bite op-
ponents (Scherahn et al. 1998). Some other genera (e.g., Biditermes, Epicalotermes,
Incisitermes, Kalotermes, Neotermes) possess long mandibles with robust dentition
(crushing mandibles sensu Prestwich 1984) used to injure an opponent mechanically.
is is often combined with release of defensive secretions originating in the labial
glands (Šobotník et al. 2010, Sillam-Dussès et al. 2012). Epicalotermes pakistanicus
has particularly long and serrated mandibles (Akhtar 1974). e defensive strategy
of Roisinitermes soldiers does not match any of these; instead, Roisinitermes employs a
unique strategy of snapping, achieved by long and slender mandibles pressed against
each other in a defensive encounter. When this potential energy is released, the left
mandible springs over the right and the resultant snap is forced onto the opponent if
it is in the path of the strike. is singular mandibular modication was previously
known in several lineages of Termitinae (Deligne et al. 1981, Prestwich 1984, Seid et
al. 2008), and was portrayed as a defensive strategy unique to this group. Roisinitermes
represents the rst undisputable evidence of parallel evolution of snapping soldiers.
Our phylogenetic analyses consistently placed Roisinitermes on a long branch,
next to N. insularis. Neotermes insularis is a large termite species from Northern Aus-
tralia with soldiers endowed with biting mandibles of crushing type. e smaller
Roisinitermes shares no obvious similarity with N. insularis, supporting its generic
status. Currently, the number of mitochondrial genomes available for Kalotermitidae
is limited to a handful of genera, and there is a possibility that future phylogenetic
analyses will support anities between Roisinitermes and yet-to-be sampled taxa. In
any case, the highly unusual morphology of Roisinitermes suggests that it shares no
close relatives among modern Kalotermitidae. Future studies should focus on whether
the mechanisms used by soldiers of Roisinitermes to snap are like those of the distantly
related Termitinae.
Acknowledgements
e authors thank Eliška Cintulová, Crystal Clitheroe and Barbora Křížková for assis-
tance on R. ebogoensis full mitochondrial genome sequencing. J.Š. is grateful to Ebogo
II inhabitants for their help during the eldwork, and for helping saving the Ebogo
forest for future generations. J.Š. and D.S.-D. thank Aleš Buček, František Jůna, and
Margot Archambeu for their hard work during the eld campaigns. e eld work
was supported by the Czech Science Foundation (project no. 16-05318S), by the
Internal Grant Agency of Faculty of Forestry and Wood Sciences, CULS (IGA No.
A_27_18) and by the Grand Agency of the Czech University of Life Sciences (CIGA
No. 20184307).
Roisinitermes ebogoensis gen. & sp. n., an outstanding drywood termite... 103
References
Abe T (1987) Evolution of life types in termites. In: Kawano S, Connell JJH, Hidaka T (Eds) Evo-
lution and coadaptation in biotic communities. University of Tokyo Press, Tokyo, 125–148.
Akhtar MS (1974) New termites from Pakistan. Biologia (Lahore) 20: 23–61.
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Niko-
lenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahh N, Tesler G, Alekseyev
MA, Pavel AP (2012) SPAdes: A new genome assembly algorithm and its applications
to single-cell sequencing. Journal of Computational Biology 19: 455–477. http://dx.doi.
org/10.1089/cmb.2012.0021
Bourguignon T, Lo N, Cameron SL, Šobotník J, Hayashi Y, Shigenobu S, Watanabe D, Roisin
Y, Miura T, Evans TA (2015) e evolutionary history of termites as inferred from 66
mitochondrial genomes. Molecular Biology and Evolution 32: 406–421. http://dx.doi.
org/10.1093/molbev/msu308
Bourguignon T, Lo N, Šobotník J, Sillam-Dussès D, Roisin Y, Evans TA (2016) Oceanic dis-
persal, vicariance and human introduction shaped the modern distribution of the termites
Reticulitermes, Heterotermes and Coptotermes. Proceedings of the Royal Society B-Biological
Sciences 283: 20160179.
Bourguignon T, Lo N, Šobotník J, Ho SY, Iqbal N, Coissac E, Lee M, Jendryka MM, Sillam-
Dussès D, Křížková B, Roisin Y, Evans TA (2017) Mitochondrial phylogenomics resolves
the global spread of higher termites, ecosystem engineers of the tropics. Molecular Biology
and Evolution 34: 589–597. http://dx.doi.org/10.1093/molbev/msw253
Cameron SL, Lo N, Bourguignon T, Svenson GJ, Evans TA (2012) A mitochondrial genome
phylogeny of termites (Blattodea: Termitoidae): robust support for interfamilial relation-
ships and molecular synapomorphies dene major clades. Molecular Phylogenetics and
Evolution 65: 163–173. http://dx.doi.org/10.1016/j.ympev.2012.05.034
Constantino R (2002) e pest termites of South America: taxonomy, distribution and sta-
tus. Journal of Applied Entomology 126: 355–365. http://dx.doi.org/10.1046/j.1439-
0418.2002.00670.x
Deligne J, Quennedey A, Blum MS (1981) e enemies and defense mechanisms of termites.
In: Hermann HR (Ed.) Social Insects, vol 2. Academic Press, New York, 1–76.
Eggleton P, Bignell DE, Sands WA, Mawdsley NA, Lawton JH, Wood TG, Bignell NC (1996)
e diversity, abundance and biomass of termites under diering levels of disturbance in
the Mbalmayo Forest Reserve, southern Cameroon. Philosophical Transaction of the Royal
Society B-Biological Sciences 351: 51–68. http://dx.doi.org/10.1098/rstb.1996.0004
Emerson AE (1925) e termites of Kartabo, Bartica District, British Guiana. Zoologica (New
York) 6: 291–459.
Engel MS, Grimaldi DA, Krishna K (2009) Termites (Isoptera): their phylogeny, classication,
and rise to ecological dominance. American Museum Novitates no. 3650: 1–27. http://
dx.doi.org/10.1206/651.1
Ghesini S, Simon D, Marini M (2014) Kalotermes sinaicus Kemner (Isoptera, Kalotermitidae):
new morphological and genetic evidence, and assignment to the new genus Longicaputermes
gen. nov. Insectes Sociaux 61: 123–131. http://dx.doi.org/10.1007/s00040-013-0335-1
Rudolf H. Scherahn et al. / ZooKeys 787: 91–105 (2018)
104
Haverty MI (1977) e proportion of soldiers in termite colonies: a list and a bibliography
(Isoptera). Sociobiology 2: 199–216.
James ER, Burki F, Harper JT, Scherahn RH, Keeling PJ (2013) Molecular characterization
of parabasalian symbionts Coronympha clevelandii and Trichonympha subquasilla from the
Hawaiian lowland tree termite Incisitermes immigrans. Journal of Eukaryotic Microbiology
60: 313–316. https://doi.org/10.1111/jeu.12027
Inward DJG, Vogler AP, Eggleton P (2007) A comprehensive phylogenetic analysis of termites
(Isoptera) illuminates key aspects of their evolutionary biology. Molecular Phylogenetics
and Evolution 44: 953–967. http://dx.doi.org/10.1016/j.ympev.2007.05.014
Krishna K (1961) A generic revision and phylogenetic study of the family Kalotermitidae (Isop-
tera). Bulletin of the American Museum of Natural History 122: 303–408.
Krishna K (1962) New species of the genera Allotermes Wasmann, Bicornitermes Krishna, Epi-
calotermes Silvestri, and Procryptotermes Holmgren (Isoptera: Kalotermitidae). American
Museum Novitates no. 2119: 1–25.
Krishna K, Grimaldi DA, Krishna V, Engel MS (2013) Treatise on the Isoptera of the World:
Vol 1. Introduction. Bulletin of the American Museum of Natural History 377: 1–200.
http://dx.doi.org/10.1206/377.1
Kück P, Meusemann K (2010) FASconCAT: Convenient handling of data matrices. Molecular Phy-
logenetics and Evolution 56: 1115–1118. http://dx.doi.org/10.1016/j.ympev.2010.04.024
Levings SC, Adams EA (1984) Intra- and interspecic territoriality in Nasutitermes (Isoptera:
Termitidae) in a Panamanian mangrove forest. Journal of Animal Ecology 53: 705–714.
https://doi.org/10.2307/4653
Liao Y, Chen H, Lu S, Xie Y, Zhang D (2018) e complete mitochondrial genome of dry-
wood termite, Incisitermes minor (Isoptera: Kalotermitidae). Mitochondrial DNA Part B
Resources 3: 324–325. http://dx.doi.org/10.1080/23802359.2017.1422397
Light SF (1937) Contributions to the biology and taxonomy of Kalotermes (Paraneotermes) sim-
plicicornis Banks (Isoptera). University of California Publications in Entomology 6: 423–463.
Martius C (1994) Diversity and ecology of termites in Amazonian forests. Pedobiologia 38: 407–428.
Prestwich GD (1984) Defense mechanisms of termites. Annual Review of Entomology 29:
201–232. https://doi.org/10.1146/annurev.en.29.010184.001221
Rambaut A, Drummond AJ (2007) Tracer. http://www.beast.bio.ed.ac.uk/Tracer
Roisin Y (2000) Diversity and evolution of caste patterns. In: Abe T, Bignell DE, Higashi
M (Eds) Termites: Evolution, Sociality, Symbioses, Ecology. Kluwer Academic Publishers,
Dordrecht, Netherlands, 95–119. http://dx.doi.org/10.1007/978-94-017-3223-9_5
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu Suchard
MA, Huelsenbeck JP (2012) MrBayes 3.2: ecient Bayesian phylogenetic inference and
model choice across a large model space. Systematic Biology 61: 539–542. http://dx.doi.
org/10.1093/sysbio/sys029
Scherahn RH, Postle A (2013) New termite species and newly recorded genus for Australia:
Marginitermes absitus (Isoptera: Kalotermitidae). Austral Entomology 52: 199–205. htt-
ps://doi.org/10.1111/aen.12023
Scherahn RH, Chase JA, Mangold JR, Hochmair HH (2018) Relative occurrence of the fam-
ily Kalotermitidae (Isoptera) under dierent termite sampling methods. Sociobiology 65:
88–100. http://dx.doi.org/10.13102/sociobiology.v65i1.2097
Roisinitermes ebogoensis gen. & sp. n., an outstanding drywood termite... 105
Scherahn RH, Křeček J, Ripa R, Luppichini P (2009) Endemic origin and vast anthropogenic
dispersal of the West Indian drywood termite. Biological Invasions 11: 787–799. http://
dx.doi.org/10.1007/s10530-008-9293-3
Scherahn RH, Křeček J, Su NY, Roisin Y, Chase JA, Mangold JR (1998) Extreme mandi-
ble alteration and cephalic phragmosis in a drywood termite soldier (Isoptera: Kaloter-
mitidae: Cryptotermes) from Jamaica. Florida Entomologist 81: 238–240. http://dx.doi.
org/10.2307/3496093
Seid MA, Scherahn RH, Niven JE (2008) e rapid mandible strike of a termite soldier. Cur-
rent Biology 18: R1049–R1050. http://dx.doi.org/10.1016/j.cub.2008.09.033
Sillam-Dussès D, Krasulová J, Vrkoslav V, Pytelková J, Cvačka J, Kutalová K, Bourguignon, T,
Miura T, Šobotník J (2012) Comparative study of the labial glands secretion in termites
(Isoptera). PLoS ONE 7: e46431. http://dx.doi.org/10.1371/journal.pone.0046431
Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML Web
servers. Systematic Biology 57: 758–771. http://dx.doi.org/10.1080/10635150802429642
Su NY, Scherahn RH (2000) Termites as pests of buildings. In: Abe Y, Bignell DE, Higashi T
(Eds) Termites: evolution, sociality, symbioses, ecology. Springer, Netherlands, 437–453.
http://dx.doi.org/10.1007/978-94-017-3223-9_20
Suyama M, Torrents D, Bork P (2006) PAL2NAL: Robust conversion of protein sequence
alignments into the corresponding codon alignments. Nucleic Acids Research 34: 609–
612. http://dx.doi.org/10.1093/nar/gkl315
Šobotník J, Jirošová A, Hanus R (2010) Chemical warfare in termites. Journal of Insect Physi-
ology 56: 1012–1021. https://doi.org/10.1016/j.jinsphys.2010.02.012
orne BL, Haverty MI (1991) A review of intracolony, intraspecic, and interspecic agonism
in termites. Sociobiology 19: 115–145.
Yasuda I, Kinjo K, Yaga S (2003) A new record of Incisitermes minor (Hagen) from Okinawa
Island. Japanese Journal of Entomology New Series 6: 103–104.
Supplementary material 1
Table S1
Authors: Rudolf H. Scherahn, omas Bourguignon, Pierre Dieudonné Akama, Da-
vid Sillam-Dussès, Jan Šobotník
Data type: molecular data
Explanation note: Sources and GenBank accession numbers of mitochondrial se-
quences used for Fig. 1.
Copyright notice: is dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). e Open Database License
(ODbL) is a license agreement intended to allow users to freely share, modify, and
use this Dataset while maintaining this same freedom for others, provided that the
original source and author(s) are credited.
Link: https://doi.org/10.3897/zookeys.787.28195.suppl1
... We gathered a dataset comprising sequence data from 2,800 samples, including 1205 previously published mitochondrial genomes (Cameron & Whiting, 2007;Tokuda et al., 2012;Wei et al., 2012;Cameron et al., 2012;Chen et al., 2014Chen et al., , 2021Bourguignon et al., 2015Bourguignon et al., , 2016Kai et al., 2015;Li et al., 2015Li et al., , 2018Bourguignon et al., 2017;Dietrich & Brune, 2016;Meng et al., 2016;Su et al., 2016;Wang et al., 2016Wang et al., , 2019Wang et al., , 2022Wang et al., , 2023Zhao et al., 2016;Han et al., 2017;Hervé & Brune, 2017;Lee et al., 2017;Liao et al., 2018a;Scheffrahn et al., 2018Wu et al., 2018;Forni et al., 2019;He et al., 2019b;a;Ye et al., 2019;Romero Arias et al., 2021, 2024Heimburger et al., 2022;Hellemans et al., 2022c;a, 2025;Buček et al., 2022b;Arora et al., 2023b;Qian et al., 2023;Yu et al., 2023;Carrijo et al., 2023;Gergonne et al., 2024) ...
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Insects have the highest species richness among animals, but the extent of their diversity and the timing of their diversification remain unclear. Insect diversification is difficult to infer due to the incompleteness of the fossil record. Phylogenetic trees of extant species reconstructed from an exhaustive sampling can be useful to address major evolutionary questions. Here, we investigated the diversification of termites, which comprise 2,995 described species, using estimates of speciation, extinction, and net diversification rates inferred from molecular phylogenies including 2,800 samples representing 1,377 putative species. Termites originated in the Early Cretaceous ~132 million years ago. Estimated extinction rates were close to zero despite fossil evidence of extinction; therefore, we focused our interpretations on the net diversification rates. Our analyses detected two significant rate shifts. The first shift occurred at the end of the Cretaceous, initially in the Kalotermitidae, then in the Neoisoptera as they started outcompeting Kalotermitidae. The second shift involved multiple lineages of Neoisoptera, especially Termitidae, which diversified as they colonized the world after the global cooling initiated at the Eocene-Oligocene transition. Our results indicate that termites became the dominant insect decomposers of tropical ecosystems as global climate change impacted ecosystems.
... The family Schizoglyphidae is the sister group to the remaining extant Astigmata [1]. This family is distinctive for retaining several plesiomorphic traits, including the relative position of the genital opening and attachment organ, as well as the structure of the attachment organ and gnathosoma compared to other astigmatid families [20]. This monotypic family includes a single observation of two specimens of the extant Schizoglyphus biroi Mahunka, 1978, found in New Guinea (Indonesia) on a tenebrionid beetle. ...
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... The family Schizoglyphidae is the sister group to the remaining extant Astigmata [1]. This family is distinctive for retaining several plesiomorphic traits, including the relative position of the genital opening and attachment organ, as well as the structure of the attachment organ and gnathosoma compared to other astigmatid families [20]. This monotypic family includes a single observation of two specimens of Schizoglyphus biroi Mahunka, 1978, found in New Guinea (Indonesia) on a tenebrionid beetle. ...
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Full-text available
Background Among minute-sized and wingless arthropods, astigmatid mites stand out for their diverse range of symbiotic associations (parasitic, neutral and mutualistic), with both invertebrate and vertebrate hosts. When inhabiting discontinuous and ephemeral environments, astigmatid mites adapt their life cycle to produce a phoretic heteromorphic nymph. When feeding resources are depleted, phoretic nymphs disperse to new habitats through phoresy, attaching to a larger animal which transports them to new locations. This dispersal strategy is crucial for accessing patchy resources, otherwise beyond the reach of these minute arthropods. In Astigmata, the phoretic nymph is highly specialized for dispersal, equipped with an attachment organ and lacking a mouth and pharynx. Despite the common occurrence of phoretic associations in modern mites, their evolutionary origins remain poorly understood. Among Astigmata, the family Schizoglyphidae represents an early derivative lineage with phoretic tritonymphs; however, our knowledge of this family is limited to a single observation. Results Here, we report the oldest biotic association of arthropods fossilised in amber (~130 Ma, Lebanon): an alate termite with 16 phoretic deutonymphs of Schizoglyphidae (Plesioglyphus lebanotermi gen. et sp. n.). The mites are primarily attached to the membranes of the host’s hindwings, using their attachment organs, pretarsal claws and tarsal setae. Additionally, we report new modern phoretic tritonymphs of this same family, on one of the earliest lineages of termites. These data collectively indicate that schizoglyphid-termite associations represent the oldest continuous mite-host associations. Notably, schizoglyphid mouthparts retain a distinct mouth and pharynx, absent in modern Astigmata. Conclusion The discovery of Schizoglyphidae mites in Lebanese amber represents the oldest known continuous association between acariform mites and their hosts. This finding demonstrates the long-term evolutionary significance of phoresy in Astigmata, evidencing a relationship sustained for over 130 Ma. It indicates that these early mites lived inside termite nests as inquilines and used alate termites for dispersal. This ancient association offers key insights into the coevolution of both mites and termites, highlighting a potential for the future discoveries of similar mites. This fossil —a stem-group Astigmata— is important for the accurate calibration of acariform mite phylogenies, advancing our understanding of these mites evolutionary history.
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Borings filled with coprolites in silicified conifer woods from the Lower Cretaceous (Albian) of the Kachaike Formation, Santa Cruz Province, Argentina are described for the first time. Coprolites are approximately hexagonal in cross-section, like those produced by extant Kalotermitidae, and occur inside borings in the secondary xylem. The presence of this family in the mid-Cretaceous ecosystems of Patagonia indicates arid climatic conditions consistent with previous geological, palynological and paleoxylological studies for this time interval in the Austral Basin. This also adds to other worldwide records of termites from the Lower Cretaceous, supporting their ecological importance as consumers and recyclers of lignified organic matter in dry forests from this period on to today.
... Soldiers with snapping mandibles are commonplace in termites, and there is growing evidence that this defensive device evolved several times in the family Termitidae (Inward et al. 2007), as well as once in Kalotermitidae (Scheffrahn et al. 2018). When the soldier presses its mandibles against each other, they accumulate elastic energy, which is converted into kinetic energy as soon as the mandible shafts slip past each other, delivering a very quick and powerful strike (Seid et al. 2008). ...
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Asymmetrical snapping mandibles have evolved several times in termites. In the Neotropics, asymmetrical snapping mandibles are found in soldiers of four genera: Neocapritermes , Planicapritermes , Cornicapritermes and Dihoplotermes . Here, I describe Schievitermes globicornis , new genus and species, from French Guiana. This genus is characterized by an absence of a frontal prominence and slightly asymmetrical mandibles in the soldier caste. The morphology and anatomy of the worker reveal a wood-based diet, and suggest that Schievitermes , Planicapritermes and Neocapritermes constitute a monophyletic group, which is consistent with mtDNA data.
... The systematics of Kalotermitidae has greatly benefited from the revision of Krishna (1961) who proposed a robust interpretation and delineation of the kalotermitid genera. More recently, this pioneering work was complemented with the description of two additional genera (Ghesini & Marini 2014;Scheffrahn et al. 2018). ...
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Reticulitermes, Heterotermes and Coptotermes form a small termite clade with partly overlapping distributions. Although native species occur across all continents, the factors influencing their distribution are poorly known. Here, we reconstructed the historical biogeography of these termites using mitochondrial genomes of species collected on six continents. Our analyses showed that Reticulitermes split from Heterotermes + Coptotermes at 59.5 Ma (49.9–69.5 Ma 95% CI), yet the oldest split within Reticulitermes (Eurasia and North America) is 16.1 Ma (13.4–19.5 Ma) and the oldest split within Heterotermes + Coptotermes is 36.0 Ma (33.9–40.5 Ma). We detected 14 disjunctions between biogeographical realms, all of which occurred within the last 34 Ma, not only after the break-up of Pangaea, but also with the continents in similar to current positions. Land dispersal over land bridges explained four disjunctions, oceanic dispersal by wood rafting explained eight disjunctions, and human introduction was the source of two recent disjunctions. These wood-eating termites, therefore, appear to have acquired their modern worldwide distribution through multiple dispersal processes, with oceanic dispersal and human introduction favoured by the ecological traits of nesting in wood and producing replacement reproductives. © 2016 The Author(s) Published by the Royal Society. All rights reserved.
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Of the more than 2,300 termite species in the world, 183 species are known to damage buildings and 83 species cause significant damage. Subterranean termites, including mound building and arboreal species, account for 147 (80%) of the economically important species. The genus Coptotermes contains the largest number of pest species (28), whereas the genus Cryptotermes, especially Cr. brevis, is the most widely introduced. The world-wide economic impact figure of termites is uncertain, but the control cost for termite pests in the United States was estimated at $1.5 billion annually in 1994. Because of differences in their life histories, control measures differ between subterranean and drywood species. Insecticide barriers are used for exclusion of soil-borne subterranean termites, whereas slow-acting baits are used for population control of subterranean termite colonies in and near structures. Whole-structure treatments (fumigation and heat), compartmental treatments (heat or cold), and local treatments (wood surface treatments or insecticide injection) are the primary tools for drywood termite control.