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Development of Experimentally Orphaned Termite Worker Colonies of Two Reticulitermes Species (Isoptera: Rhinotermitidae)

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ABStrACt Survival and caste differentiation were observed under controlled con-ditions in orphaned experimental colonies of the subterranean termites Reticulitermes grassei and R. santonensis. Worker colonies had different sizes (30, 50, 100, 200 and 300); after 12 and 32 months the differentiation of colony members in other castes was observed. twelve months after orphan-ing, 80% of the colonies had survived. For the two species, a mean number of one soldier was observed in 7 colonies and between 1 and 3 nymphs were present in 18 colonies, whatever the initial number of workers. In 53% of the surviving colonies, the differentiation of secondary reproductives occurred and they produced viable offspring. The external morphology of R. grassei male reproductives did not differ significantly from those of workers or nymphs. Thirty-two months after orphaning, colonies with an initial number of 30 workers were comprised of secondary reproductives and their offspring. In termite species, caste differentiation pathways and thus the caste system are highly flexible. Therefore, our results show that a small number of subterra-nean termites could establish a new colony within few years and thus invade a new habitat, for example in urban areas.
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1015
Development of Experimentally Orphaned Termite
Worker Colonies of Two Reticulitermes Species
(Isoptera: Rhinotermitidae)
by
A. Pichon1, M. Kutnik1,2, L. Leniaud1, E. Darrouzet1, N. Châline1,3, S. Dupont1
& A.-G. Bagnères1*
ABSTRACT
Survival and caste dierentiation were observed under controlled con-
ditions in orphaned experimental colonies of the subterranean termites
Reticulitermes grassei and R. santonensis. Worker colonies had dierent sizes
(30, 50, 100, 200 and 300); aer 12 and 32 months the dierentiation of
colony members in other castes was observed. Twelve months aer orphan-
ing, 80% of the colonies had survived. For the two species, a mean number
of one soldier was observed in 7 colonies and between 1 and 3 nymphs were
present in 18 colonies, whatever the initial number of workers. In 53% of the
surviving colonies, the dierentiation of secondary reproductives occurred and
they produced viable ospring. e external morphology of R. grassei male
reproductives did not dier signicantly from those of workers or nymphs.
irty-two months aer orphaning, colonies with an initial number of 30
workers were comprised of secondary reproductives and their ospring. In
termite species, caste dierentiation pathways and thus the caste system are
highly exible. erefore, our results show that a small number of subterra-
nean termites could establish a new colony within few years and thus invade
a new habitat, for example in urban areas.
Keywords: subterranean termites, small colonies, survival, neotenics dif-
ferentiation, urban habitat.
1 IRBI - UMR CNRS 6035, Université François Rabelais, Faculté des Sciences et Techniques, Parc de
Grandmont, 37200 Tours, France.
2 CTBA, Allée de Boutaut, BP 227, 33028 Bordeaux Cedex, France.
3 LEEC - UMR CNRS 7153, Université Paris 13, 99 avenue J.-B. Clément, 93430 Villetaneuse,
France.
* Corresponding author, e-mail : bagneres@univ-tours.fr
1016 Sociobiology Vol. 50, No. 3, 2007
INTRODUCTION
In eusocial insects, the colony is a social unit constituted of individuals,
which are organised in dierent castes according to their behaviour, and/
or their morphology. Colonies can be classied on the basis of the mode
of foundation, the number of reproductives and the number of nest units
forming a colony (Pamilo et al. 1997). e social organization of colonies
(i.e. number of individuals, relatedness and reproductive skew among them)
can vary within species or even within populations, and ecological and social
factors can induce variations in the social organization of colonies (Ross &
Keller 1995). In some Hymenopteran species, an example of such variation
within a population is a dierence in queen number per colony. Adoption of
young queens can be favored when habitat saturation is high (e.g. Myrmica
sulcinodis (Nylander): Pedersen & Boomsma 1999) or when ecosystems are
characterized by interspecic competition and territoriality (e.g. Ectatomma
tuberculatum (Olivier): Hora et al. 2005).
Unlike others social insects like bees, wasps or ants, Isopteran species have
a highly plastic social organization. Termites are hemimetabolous insects and,
except for the primary reproductives, all individuals are immature. ey are
organised in castes (workers, soldiers and nymphs developing into reproduc-
tives) which are an example of larval polyphenism (Nijhout 2003; Korb &
Katrantzis 2004). e developmental pathways are not always irreversible
(Noirot 1989). In some species of Termopsidae and Kalotermitidae, nest
and food resources are situated in the same piece of wood (Abe 1987) and
workers have a exible development; they can switch to another caste or even
develop regressively into a former instar, which is a unique developmental
pattern (Korb & Katrantzis 2004). In numerous termite species, dierent
social organizations occur within populations, as a result of the mode of
foundation but also as a result of the exibility of individual developmental
patterns. Colonies can thus exhibit various breeding systems: foundation
by one couple of primary reproductives (a queen and a king) or by several
queens (polygyny) or kings (polyandry) (Fisher et al. 2004). If one of them
dies (or both), immature individuals can become secondary reproductives:
they have a larval morphology but their sexual organs are functional (Noirot
1956; Büchli 1958). ese individuals are named ergatoid or nymphoid
1017
Pichon, A. et al. — Development of Orphaned Subterranean Termites
neotenics when they develop from workers or nymphs respectively. Within
a colony, they can be distinguished from workers or nymphs by a longer
abdomen, darker pigmentation, slight sclerotisation and the presence of
eyes and ocelli (Weesner 1965; Plateaux & Clément 1984; Krishna 1989;
Serment & Tourteaux 1991; orne 1996, 1998). When neotenics replace
the missing parent they are named replacement reproductives. Sometimes
neotenics can also develop in the presence of primary reproductives and are
named supplementary reproductives (orne 1996; Roisin 2000). In several
termite species, the social organization can vary within a population but also
within a colony during its lifespan, if the death of one or several primary
reproductives occurs.
Some studies have focused on the origin of replacement reproductives
and the ability of colonies to survive an orphaning. Lenz and Runko (1993)
orphaned several eld colonies of the Australian termite Coptotermes lacteus
(Froggatt): primary queens were quickly replaced by nymphoid neotenics.
Colonies produced a high number of nymphs all-year round. As the original
colonies' survival was low, it was probably due to a strategy to disperse more
alates. Pawson and Gold (1996) have investigated the caste dierentiation
in orphaned colonies of the American subterranean species Reticulitermes
avipes (Kollar), R. virginicus (Banks) and R. hageni (Banks) at 5 worker
densities. Half of the colonies survived and their growth was ensured by
the high reproduction potential of replacement reproductives. e social
structure could vary between species: R. virginicus colonies produced more
reproductives than did colonies of R. avipes and R. hageni.
In Europe, a large majority of termite species are subterranean and belong to
the genus Reticulitermes. Among them, R. grassei Clément and R. santonensis
(Feytaud) have populations in natural environments in the south-western
area of France and they cause severe damage to buildings in urban areas.
e social structure of R. grassei and R. santonensis colonies within French
populations has been analysed in natural and urban local conditions (DeHeer
et al. 2005; Dronnet et al. 2005). e presence of colonies in urban areas is
certainly due to human activity, particularly the transport of soil and infested
wood. It is generally assumed that fractions of colonies are at the origin of the
populations in built-up areas and their development can be achieved because
1018 Sociobiology Vol. 50, No. 3, 2007
of the exibility of the social structure within populations, particularly the
dierentiation of workers and nymphs into secondary reproductives.
e purpose of the present study was to evaluate the ontogenic potentialities
of small orphaned groups of workers of the species R. grassei and R. santonensis
isolated from their respective colonies. As in Pawson and Gold (1996), the
development of new reproductives and their brood was observed in groups
with dierent sizes of workers. Our rst results were obtained over a period
of 12 to 32 months. When neotenics and their ospring were observed, we
collected them and tried to assess the number of parental pairs producing
the new ospring with microsatellite markers.
MATERIAL AND METHODS
Collection of termites and rearing conditions
A colony of R. santonensis was collected in April 2000 on the island of
Oléron (Charénte Maritime, France) and maintained in the laboratory until
the experiment started. e colony of R. grassei was collected in July 2003
at Grenade-sur-l’Adour (Landes, France). In both cases the termites were
initially kept in the original pieces of wood they had been feeding on in the
eld. Species identities were conrmed using cuticular hydrocarbon pro-
les (Bagnères et al. 1991; Clément et al. 2001, data not shown) and DNA
sequences of the mitochondrial cytochrome oxydase II gene (Kutnik et al.
2004, data not shown). For the experiments, approximately 4100 workers of
5th to 7th instars were collected from each colony.
Orphaning experiment
For each species, ve colony sizes were tested: 30, 50, 100, 200 and 300
workers, respectively named type 30, 50, 100, 200 and 300. Six articial
colonies (replicates) for each type were prepared, thus 30 articial colonies
per species. For each articial colony, the termites were transferred in a plas-
tic box (120 x 90 x 50 mm) containing 150 g of moistened Fontainebleau
sand and a piece of poplar wood (20 x 20 x 20 mm). A new piece of wood
was placed in the box before half of the food resource was consumed. e
relative humidity was maintained at 80% inside each plastic box. During the
experiment, articial colonies were maintained under constant darkness, at
room temperature.
1019
Pichon, A. et al. — Development of Orphaned Subterranean Termites
Aer 12 months, we evaluated the number of surviving articial colonies
and the proportion of surviving workers (initially placed in the box and
named ‘oldworkers) within these colonies. We recorded the numbers of new
nymphs, soldiers and secondary reproductives as well as their eggs, young
larvae and new workers when present in articial colonies. All termites from
each articial colony were transferred in a new plastic box (120 x 90 x 50 mm)
with Fontainebleau sand and a piece of poplar wood, and maintained in the
conditions described previously.
Aer 24 months, almost all R. grassei articial colonies of type 200 and
300 were surviving and several secondary reproductives with a relatively
high number of eggs and young larvae were observed (cf. results). us we
chose these articial colonies to evaluate if females were sexually mature and
to estimate the number of reproductives which produced the ospring. e
other surviving articial colonies (type 30 to 100 R. grassei replicates and R.
santonensis articial colonies) were kept in the same conditions to evaluate
the development of small groups of termites 32 months aer orphaning.
erefore, the experiment was divided in two parts:
I) e surviving R. grassei articial colonies of type 30, 50, 100 and all the
surviving articial colonies of R. santonensis were maintained in the condi-
tions of the experiment. Aer eight months (32 months aer beginning),
all the termites from surviving articial colonies were collected, their caste
determined, and ospring number evaluated.
II) e development of female neotenics was observed in R. grassei sur-
viving articial colonies of type 200 and 300. e female neotenics were
isolated and their abdomens were dissected under a dissecting microscope.
eir ovarian development was observed and the spermathecae were collected
and attened in a drop of Beadle buer (128.3 mM NaCl, 4.7 mM KCl,
2.3 mM CaCl2) and xed in ethanol. e presence of sperm was observed
via uorescence microscopy aer DAPI staining for nuclei was performed
(Darrouzet et al. 2002).
To evaluate the number of secondary reproductives which had reproduced,
we genotyped females and their ospring. us, for each R. grassei articial
colony of type 200 and 300, between 5 and 40 eggs or larvae from 1st to 3rd
instar were collected with female neotenics. Ospring were frozen along with
neotenic heads at -20°C.
1020 Sociobiology Vol. 50, No. 3, 2007
Microsatellite analysis
Genotypes of R grassei neotenics and their ospring (eggs and larvae) were
examined in the surviving articial colonies: 6 of type 200, named 200-1 to
200-6 and 5 of type 300, named 300-1 to 300-5.
DNA was extracted from heads of neotenics, eggs and larvae by a Chelex®
extraction method (Walsh et al. 1991). Samples were crushed, then mixed
with 200 µl of a 5% Chelex® solution and 3 µl of a 1% proteinase K solution.
Aer 1 hour of incubation at 56°C, samples were homogenized for 10 sec
and placed at 96°C during 15 min. Aer a centrifugation at 8000 g for 3
min, 100 µl of the supernatant was removed and puried with a solution of
absolute ethanol. We examined the microsatellite genotypes for 6 loci: Rf 6-1,
Rf 5-10, Rf 21-1, Rf 11-1, Rf 11-2 and Rf 24-2 (Vargo 2000, DeHeer et al.
2005). PCR was conducted in a total volume of 10 µl, containing 3 mM or 1.5
mM MgCl2, 2 µM of reverse primer and 0.5 or 1 µM of forward primer, 0.04
units of Taq DNA polymerase and 1 µl genomic DNA. One primer of each
pair was uorescence-labelled. e PCR conditions were 40 cycles of 1min
denaturation at 94°C, annealing at 57°C for 1min and elongation at 72°C for
15 sec. en PCR products were denaturated at 94°C in a blue-bromophenol
and formamide solution and run in a 6% denaturated polyacrylamide gel using
a LiCor automated sequencer (1500 V). Microsatellite alleles were detected
through their uorescence and scored using the computer program GENE
PROFILER 4.03 (Scanalytics, Inc.).
Individuals from each articial colony were strongly related, thus the link-
age disequilibrium and the deviations from Hardy-Weinberg equilibrium
were analysed using a resampling method. A single individual per articial
colony was randomly chosen; a total of 20 data sets were created. Analyses
were performed using the soware GENEPOP v3.4 (Raymond & Rous-
set 1995). General descriptive statistics, such as observed versus expected
heterozygosity were calculated for each articial colony, using the soware
GDA (Lewis & Zaykin 2001).
To determine if one or several reproductives had reproduced we classied
articial colonies as simple or extended families. In simple families, ospring
are produced by one pair of reproductives and observed ospring genotype
frequencies did not dier from those expected under Mendelian segregation
of alleles from two parents. In extended families, genotype frequencies within
1021
Pichon, A. et al. — Development of Orphaned Subterranean Termites
colonies are not consistent with being produced by one pair of reproductives.
Signicance of the dierence was determined by a G-test (p<0.05 when o-
spring were produced by more than two reproductives) (Bulmer et al. 2001,
Goodisman & Crozier 2002, Vargo 2003, DeHeer & Vargo 2004).
Data analysis
e dierences between the proportions of surviving workers, the number
of neotenics and their ospring were tested using a Kruskall-Wallis test or a
Mann-Whitney U test within R. grassei and R. santonensis articial colonies
of type 30, 50, 100, 200 and 300. To perform these tests, we made the as-
sumption that all the females observed in the articial colonies had mated
and reproduced. us, the mean number of ospring (eggs and larvae) was
estimated per female. All the analyses were performed with the soware
STATISTICA version 6 (StatSo France, 2003).
RESULTS
Development of articial colonies aer 12 months
Survival
Twelve months aer the beginning of the experiment, the number of arti-
cial colonies with surviving termites was 27/30 for R. grassei and 23/30 for
R. santonensis. Considering only the articial colonies with surviving termites,
the mean percentage of R. grassei workers initially placed in the box, dened
as ‘oldworkers, varied from 48.5% to 76% between articial colonies (Fig. 1).
e mean percentages of ‘old’ workers in articial colonies of R. santonensis
were 17.1% to 44% (Fig. 1). For both species, the proportion of surviving ‘old
workers was more important when the initial group size was small (Kruskall-
Wallis test, α = 0.05): p = 0.006 in R. grassei articial colonies (n = 27) and
p = 0.031 in R. santonensis articial colonies (n = 23).
Development of nymphs and soldiers
In R. grassei articial colonies, 1 or 2 nymphs were observed in 13 articial
colonies (table 1). In 5 R. santonensis articial colonies (only type 200 and
300), 1 to 3 nymphs had dierentiated (table 1). e presence of soldiers was
rst noticed between 3 or 4 weeks aer we orphaned the articial colonies.
One soldier (or white soldier) was observed aer 12 months in 4 articial
colonies of R grassei and in 3 articial colonies of R. santonensis (Table 1).
1022 Sociobiology Vol. 50, No. 3, 2007
Because of the very small numbers
of nymphs and soldiers produced in
the articial colonies, no statistical
test could be performed to evaluate
a dierence related to the sizes of
articial colonies.
Development of neotenics
and their ospring
Neotenics of R grassei and R.
santonensis were first observed
respectively 6 and 5 months aer the beginning of the experiment. In the
R. grassei articial colonies, all the secondary reproductives observed were
females. eir number ranged from 0 to 3 per articial colony and increased
with colony size (Kruskall-Wallis test, n = 27, p = 0.000) (Fig. 2). When
we analyzed the percentage of female neotenics (per 100 workers), values
obtained for R. grassei articial colonies were signicantly dierent among
types (Kruskall-Wallis test, n = 27, p= 0.001). In R. grassei articial colonies
of type 100, 200 and 300, the mean ospring per female ranged from 82 to
211 eggs and larvae (Fig. 3). e mean ospring recorded in type 300 articial
Fig. 1. Survival (mean ± SE) in R . grassei (white) and R. santonensis (grey) articial colonies 12 months
aer orphaning. Dierent letters indicate signicant dierences within species (p < 0.05).
Table 1. Number of nymphs and soldiers per articial
colony in R. grassei and R. santonensis. Number of
articial colonies with nymphs or soldiers are in
brackets.
R. grassei R. santonensis
Type nymphs soldiers nymphs soldiers
30 1, (2)
50 1-2, (2) 1, (1)
100 1, (3) 1, (1) 1, (1)
200 1, (1) 2-3, (2) 1, (2)
300 1-3, (5) 1, (2) 1-2, (3) 1, (1)
1023
Pichon, A. et al. — Development of Orphaned Subterranean Termites
Fig. 2. Mean number (±SE) of R. grassei (white) and R . santonensis (grey) female neotenics per
articial colony, 12 months aer orphaning. Dierent letters indicate signicant dierences within
species (p < 0.05).
Fig. 3. Mean ospring per female (±SE) in R. grassei (white) and R. santonensis (grey) articial
colonies 12 months aer orphaning. Dierent letters indicate signicant dierences within species
(p < 0.05)
1024 Sociobiology Vol. 50, No. 3, 2007
colonies was signicantly higher than
in type 100 and 200 articial colonies
(Mann-Whitney U test, p < 0.05).
In R. santonensis articial colo-
nies, the number of female neoten-
ics ranged from 1 to 4 per colony
and was not signicantly dierent
between types of articial colonies
(Kruskall-Wallis test, n = 23, p >
0.05) (Fig. 2). Male neotenics were
also observed in one articial colony of type 30 and in type 100, 200 and
300 articial colonies (table 2). Male and female neotenics were observed in
the same articial colonies and their respective numbers were not dierent
(Mann-Withney U test, p> 0.05). e mean ospring per R. santonensis
female was between 24 and 50 eggs and larvae (Fig. 3).
Development of R. grassei articial colonies of type 30, 50 and
100 and all R. santonensis articial colonies aer 32 months.
Survival
Aer 32 months of orphaning, the number of R. grassei articial colonies
with living termites was 5/6 in type 30, 6/6 in type 50 and 4/6 in type 100. e
articial colonies of type 30 and 50 had a similar proportion of ‘old’ workers
(i.e. original workers): 34% and 38% respectively (Fig. 4). is percentage
highly decreased in type 100 articial colonies (6%).
e number of surviving articial colonies of R. santonensis was very low.
Only 9/30 articial colonies had living termites, all from type 30 and 50. e
mean percentage of ‘old’workers within these articial colonies was 44 and
25% respectively (Fig. 4).
Development of nymphs and soldiers
e development of nymphs and soldiers occurred only in R. grassei articial
colonies (type 30, 50 and 100). One or two nymphs and one white soldier
were observed in two articial colonies of type 30. Two articial colonies of
type 100 had one and ve nymphs.
Table 2. Mean number of female and male neotenics
per articial colony in R. santonensis series 12 months
aer orphaning.
Neotenics Neotenics
Articial colony size (females) (males)
30 1.5 0.5
50 2 0
100 1.4 1.5
200 2 2.67
300 2.75 1.5
Mean ± SE 1.93 ± 0.53 1.23 ± 1.03
1025
Pichon, A. et al. — Development of Orphaned Subterranean Termites
Development of neotenics and their ospring
e R. grassei type 30, 50 and 100 articial colonies were able to support
the dierentiation of neotenics and the production of their ospring. In
three type 30 and type 50 articial colonies, one or two female neotenics
and one male neotenic per articial colony were recorded. e four type 100
termite articial colonies had a mean number of 1.25 males and 2.5 females.
e numbers of neotenics were not signicantly dierent among the types
and the number of females was not signicantly higher than the number of
males (Kruskall-Wallis test, n = 4, p > 0.05). e mean ospring (eggs and
larvae) per female was between 2 and 98 individuals, but brood size was not
related to the original size of the articial colonies (Kruskall-Wallis test, n
= 10, p>0.05).
In R. santonensis groups, 1 or 2 female neotenics were observed in 3 type
50 articial colonies and the brood production was much reduced, around
12 larvae per articial colony.
Development of female and male neotenics in R. grassei type 200
and 300 articial colonies.
Twenty-four months aer the beginning of the experiment, we tried to
observe male neotenics in the articial colonies of R. grassei with female
Fig. 4. Survival (mean ± SE) in R. grassei (white) and R. santonensis (grey) articial colonies 32
months aer orphaning.
1026 Sociobiology Vol. 50, No. 3, 2007
neotenics. Only one articial colony (type 200) contained 3 male neoten-
ics. e ospring production in the other articial colonies could occur
through female parthenogenesis, as observed in orphaned colonies of R.
speratus (Kolbe) (Hayashi et al. 2003, Hayashi et al. 2006). Male neotenics
were present but they did not have the morphological characteristics usually
observed on neotenics. Females from type 200 and 300 articial colonies
were dissected. Within type 200 articial colonies, 11 female neotenics were
observed and dissected. Among them, 7 had mature eggs in variable quanti-
ties. Due to a technical problem during dissections we were able to dissect
the spermathecae of 9 females (instead of 11) and 6 of them contained stored
sperm at the time we took them from the articial colonies. Within the type
300 articial colonies, we identied and dissected 10 female neotenics; ve
of them had mature eggs. During dissections of spermathecae, one was dam-
aged. us spermathecae of 9 females were dissected and we observed that all
stored sperm. We could conclude from these observations that in type 200
and 300 articial colonies of R. grassei, several neotenic females had mated
with neotenic males, but some females did not produce eggs at the time they
were isolated.
Genotyping
In R. grassei articial colonies of type 200 and 300, only 2 loci were found
to be polymorphic: Rf6-1 and Rf21-1, with 2 alleles each. We scored between
1 and 4 neotenics and between 5 and 40 eggs or larvae from each articial
colony. e resampled data sets showed that none of the two loci were in
linkage disequilibrium or had shown deviations from the Hardy-Weinberg
equilibrium.
In some articial colonies (for the locus Rf6-1, colony 200-5 as example),
genotypes of female neotenics were homozygous and some of their ospring
were heterozygotes. From this observation we conrmed the reproduction
of females with male neotenics.
In 83.3% of type 200 articial colonies, the ospring was produced by a
single pair of reproductives (simple families, G-test p> 0.05) (Table 3). e
proportion of simple families is 60% in type 300 articial colonies. In a ma-
jority of R. grassei articial colonies, more than one female neotenics were
observed but all females did not reproduce.
1027
Pichon, A. et al. — Development of Orphaned Subterranean Termites
DISCUSSION
From previous studies, we know that a Reticulitermes colony can comprise
from 50000 up to 1 million individuals in natural and urban habitats (Howard
et al. 1982; Paulmier et al. 1997). e presence of R. grassei and R. santonensis
in urban habitats is certainly related to anthropic factors. Only a fraction
of a colony could be introduced through the transport of wood or plants
with a lump of soil and then invade an entire area. Studies on the breeding
system of these species in urban environment showed that all R. santonensis
colonies and 51.8% of R. grassei colonies were headed by multiple secondary
reproductives (Dronnet et al. 2005; DeHeer et al. 2005).
Nests of Reticulitermes species are subterranean and foragers collect the
cellulose in log-woods situated on the ground. Foragers can adjust their food
uptake to the characteristics of the colony (numerous dependant individuals);
food quantity and quality can have an eect on the caste composition of a
colony (Lenz 1994). In our experimental design, a new piece of poplar wood
was supplied regularly. We considered that food resource, temperature and
relative humidity were not limiting factors to the development of articial
colonies, as in human housing.
From our preliminary results, we observed that under laboratory condi-
tions, a group of 30 workers can survive over a long period (24 months) and
produce secondary reproductives and a new generation of termites. e colony
Table 3. Numbers (N) of neotenics, eggs and larvae genotyped, observed (Ho) and expected (He)
heterozygosities, structure of the family obtained by G-test (p< 0.05: extended family) in each R.
grassei articial colony of type D (200 termites) and E (300 termites).
Colony N He neotenics Ho neotenics N (eggs) N (lar vae) He ospring Ho ospring Family type
200-1 2 0.250 0.250 10 0.252 0.278 simple
200-2 2 0.250 0.250 20 4 0.473 0.595 simple
200-3 4 0.428 0.500 20 1 0.198 0.164 extended
200-4 2 0.250 0.250 10 1 0.331 0.394 simple
200-5 2 0.250 0.250 5 0.278 0.300 simple
200-6 2 0.583 0.750 40 0.507 0.396 simple
300-1 2 0.500 0.500 20 0.328 0.418 extended
300-2 3 0.381 0.417 2 25 0.326 0.315 extended
300-3 3 0.333 0.333 25 0.333 0.411 simple
300-4 1 - - 12 0.475 0.633 simple
300-5 3 0.167 0.167 20 0.378 0.485 simple
1028 Sociobiology Vol. 50, No. 3, 2007
growth is relatively slow but it could be sucient to invade an urban habita-
tion within few years. Some authors consider that a group of 50 termites is
sucient to establish a colony (Serment & Tourteaux 1991).
e survival of the R. santonensis orphaned colonies was signicantly low.
is result is in contrast with observations made frequently on several eld
colonies of R. santonensis. e high mortality within articial colonies could
be due to the preservation of the colony in laboratory conditions during a
long period, and thus, to a decrease of its strength. However, in both species,
a majority of the articial colonies were active twelve months aer the start
of the experiment and several dierences were observed among dierent
sizes of articial colonies. e workers of articial colonies with small sizes
seemed to survive better aer 12 months than articial colonies with 200 or
300 termites. Considering all the plastic boxes used in the experiment had
the same volume, the density of individuals was variable and could have an
inuence on the mortality of colony members.
In their natural habitat, Reticulitermes soldiers usually represent between
1 and 3% of the colony members, although higher values have been reported
(Grace 1996; Forschler & Jenkins 1999; Long et al. 2003). In the present
study, a maximum number of one soldier per articial colony was observed,
whatever the colony size was. ey appeared within 3 or 4 weeks aer the
orphaning. e development time from a worker to a soldier is usually longer
than 4 weeks (Büchli 1958; Lainé & Wright 2003). erefore, we can suppose
that some workers had initiated their dierentiation in soldiers before the
orphaning happened. In a similar study on orphaned colonies of R. hageni,
R. virginicus and R. avipes, Pawson and Gold (1996) have recorded up to
4 soldiers per colony and their number was increasing with worker density.
However, the low number of soldiers in our experiment could be explained
by the local conditions: stable temperature and humidity, lack of predators
and/or competitors. Moreover, the dierentiation of dependant individuals
as soldiers could happen at the expense of colony growth.
A small number of nymphs were observed 12 months aer orphaning.
Nymphs are immature and dependent individuals; they can dierentiate
into adults (primary reproductives) or into nymphoid neotenics (secondary
reproductives). Miyata et al. (2004) have observed in a study on the pattern
of neotenic dierentiation in R. speratus that ergatoid dierentiation required
1029
Pichon, A. et al. — Development of Orphaned Subterranean Termites
a longer time than nymphoid dierentiation. Büchli (1958) hypothesized
that the dierentiation of Reticulitermes workers into neotenics was dicult
because workers could not accumulate enough resources to have a rapid dif-
ferentiation. In our experiment, these nymphs would probably dierentiate
into neotenics.
We observed male neotenics of R. grassei that were not morphologically
distinguishable from a worker or a nymph several months aer the orphan-
ing. us, male neotenics could be sexually mature and be able to inseminate
females before the external morphological characteristics, used generally to
identify male neotenics (darker pigmentation, longer abdomen, presence of
eyes, etc.), appear. Further studies are needed to conrm the presence of what
could be named ‘hidden’ male neotenics.
e number of female neotenics observed in the articial colonies, aer the
orphaning, was variable: from 1 up to 4 per colony. ese values were similar
to the number of reproductives produced by R. speratus orphaned colonies
(Watanabe & Noda 1991) but lower than the number of secondary reproduc-
tives observed in R. virginicus or R. avipes orphaned colonies (Pawson &
Gold 1996). More reproductives had dierentiated at high densities of workers
than at low densities. Similar results were found with orphaned colonies of
R. hageni, R. virginicus and R. avipes (Pawson & Gold 1996).
From several studies, it was assumed that numerous replacement repro-
ductives have a greater egg production than the primary queen (Miller 1969;
Nutting 1970; Myles 1999). However, several authors consider that the
queen fecundity was superior to those of neotenics (Noirot 1990; orne
1996, 1998; Lainé & Wright 2003). In our study, the female fecundity was
variable among articial colonies. Nevertheless, the values estimated were in
the same order than found by Pawson & Gold (1996).
We tried to assess the number of reproducing females in some R. grassei
articial colonies. e loci tested were not highly polymorphic. However, we
performed G-tests to determine if the brood was produced by one parental
pair or by several parents. Simple families (one pair of reproductives) occurred
in half of the articial colonies. Colonies could be headed by the female neo-
tenic who rst dierentiated during the experiment, which could dominate
the sexual development of other females. e other female neotenics could
be dierentiated but their ovocyte maturation could be delayed. Dissections
1030 Sociobiology Vol. 50, No. 3, 2007
revealed that several female neotenics did not have mature ovocytes. In other
articial colonies, the brood was produced by several reproductives but the
exact number of females reproducing could not be evaluated. Further stud-
ies with more polymorphic colonies could determine the exact number of
females producing the new generation and thus, the mean fecundity could
be evaluated more precisely. Moreover, other experiments could investigate
the mechanisms of a possible dominance of one female neotenic (whether
the rst to dierentiate or not).
As we chose to collect the rst results aer one year of the experiment, so
as not to disturb the colonies too frequently, we did not obtain results on
the egg and larval development times or on the aggression between workers
and newly dierentiated neotenics or among reproductives, as studied previ-
ously in other termite species (Lenz & Barrett 1982; Lenz & Runko 1993;
Roisin 1993, 2000).
Because of the low number of colonies used in this rst study, we could
not evaluate the variation of caste dierentiation and reproduction strategies
within and among the two species. However, termites of the genus Reticu-
litermes have exible developmental pathways which allow the persistence
of colonies in absence of primary reproductives. A single pair of secondary
reproductives in a colony with 100 workers can produce a new generation.
erefore a special attention must be paid to the human-mediated transport
of termites and to the control strategies of fractionate colonies.
ACKNOWLEDGMENTS
We are extremely grateful to D. Limousin for his help with the microsatel-
lite analysis. We thank Louise Brinkworth for the nancial support provided
by DowAgroSciences for Magdalena Kutnik’s PhD.
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... Soil disruption due to construction and dramatic weather events like floods can lead to a separation of termite nestmates. Isolated groups can establish a new colony through the production of supplementary reproductives in the event that groups become physically separated (Pichon et al. 2007). This is certainly the most effective way of termite dissemination and building infestation, as even very small groups (of less than 100 termites), transported with plants, soil, or wood debris, may establish new colonies at long distances from the original colony. ...
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Construction using timber has seen a resurgence in light of global climate mitigation policies. Wood is a renewable resource, and engineered wood products are proving to be competitive against concrete and steel while having several advantages. However, while the renewable nature of wood in construction is a beneficial property for climate mitigation policies, the process of biodegradation introduces a challenge for service life planning. A review of hazard mapping is presented while developing contemporary hazard maps, occurrence maps and projected hazard maps for 2050 using representative concentration pathways ( RCP ) 2.6 and 8.5. The risk of timber decay is expected to increase in most of Europe as the temperatures rise, with a decrease expected in dryer regions. Termites are likely to experience a range expansion as more areas become suitable, while human activity and an increase in extreme weather events like floods are expected to facilitate dispersion. Marine borer species already present a risk in most European coastal regions; however, the effect of changes in water temperatures are likely to shift the boundaries for individual borer species. Overall, warmer climates are expected to increase the metabolic activity of all of these organisms leading to a general reduction in service life.
... 35 Que ce soient les voies ferrées, les routes, les canaux, les voies fluviales ou autres, les moyens de transport ont permis le déplacement d'une partie de l'environnement des termites : un peu de terre ou de bois contaminés avec une trentaine d'individus peuvent suffire à créer une nouvelle colonie de R. flavipes (Pichon et al., 2007). Il apparait déterminant de comprendre quels sont les facteurs environnementaux que vont trouver les termites pour permettre leur survie puis leur développement. ...
... Compared with R. flavipes, female ergatoid formation is faster in R. speratus in response to orphaning, and the formation of nymphoids are faster than ergatoids in R. speratus (Matsuura et al. 2010;Miyata et al. 2004). Orphaning assays have also been conducted in other congeneric species including R. grassei (Pichon et al. 2007) and R. urbis (Ghesini and Marini 2009), which confirmed the inhibitory effect of reproductive pairs, but the regulation by each sex remains unclear. Head butting by workers is a behavioral indicator of reproductive disinhibition (Korb et al. 2009). ...
Article
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In social insects, the postembryonic development of individuals exhibits strong phenotypic plasticity in response to the environment, thus generating the caste system. Different from eusocial Hymenoptera, in which queens dominate reproduction and inhibit worker fertility, the primary reproductive caste in termites (kings and queens) can be replaced by neotenic reproductives derived from functionally sterile individuals. Feedback regulation of nestmate differentiation into reproductives has been suggested, but the sex specificity remains inconclusive. In the eastern subterranean termite, Reticulitermes flavipes, we tested the hypothesis that neotenic reproductives regulate worker-reproductive transition in a sex-specific manner. With this R. flavipes system, we demonstrate a sex-specific regulatory mechanism with both inhibitory and stimulatory functions. Neotenics inhibit workers of the same sex from differentiating into additional reproductives but stimulate workers of the opposite sex to undergo this transition. Furthermore, this process is not affected by the presence of soldiers. Our results highlight the reproductive plasticity of termites in response to social cues and provide insights into the regulation of reproductive division of labor in a hemimetabolous social insect.
... 35 Que ce soient les voies ferrées, les routes, les canaux, les voies fluviales ou autres, les moyens de transport ont permis le déplacement d'une partie de l'environnement des termites : un peu de terre ou de bois contaminés avec une trentaine d'individus peuvent suffire à créer une nouvelle colonie de R. flavipes (Pichon et al., 2007). Il apparait déterminant de comprendre quels sont les facteurs environnementaux que vont trouver les termites pour permettre leur survie puis leur développement. ...
Article
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This study presents research concerning subterranean termites found in the Centre-Val de Loire region. More specifically, we examined the geographical distribution of Reticulitermes flavipes, a globally invasive species. This work was conducted in collaboration with both social and life science specialists in order to better understand the factors mediating its spatial distribution. Using geomatics and the spatial analysis of R. flavipes’ distribution, we were able to define geographical areas favorable to the termite. This geographical study and the diversity of players involved in this research underscore a growing awareness of termite invasion risks in society at large.
... This flexibility is the basis of the success of termite infestation, particularly in urban areas. If a colony happen to be divided -for example when an attack by ants destroys a part of it, when an underground tunnel collapses isolating a group of workers from the rest of the colony or when infested materials are moved for building purposes -even very small groups of workers can produce secondary reproductives which may initiate a new colony (Pichon et al. 2007). ...
Conference Paper
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Wood can be modified by mechanical, thermal and chemical treatment, whose aim to improve its physical and biological properties such as strength, dimensional stability and resistance to decay. Biological resistance of modified wood meant for outdoor use is assessed mainly to wood degrading fungi, by calculating wood mass losses after fungal attacks. Several studies have demonstrated that resistance to fungi can be highly improved through different wood modification processes, by reducing moisture contents or by limiting absorption of the nutritional components from the medium. But the ability of modified wood to resist xylophageous insects, especially termites, which are a great problem for timber construction in the countries of southern Europe (such as France, Spain, Portugal and Italy) and some of their overseas territories, is often neglected. Many studies have demonstrated that termite resistance of thermally treated wood is low, and that the resistance of chemically treated wood may vary. The differences in the effectiveness of wood modification for biological resistance against fungal decay types or termite species can be easily accounted for by these organisms’ exhibit distinct degrading systems and environmental preferences. However, testing methodologies used to assess resistance to termites are deficient in certain other respects. These methodologies are not always relevant, especially when the tests are performed under laboratory conditions, for the reported mortality rates in isolated groups of termites do not reflect the behaviour of a termite colonies in natural field conditions. For this reason, above ground resistance tests or lab tests performed on bigger colonies could provide more reliable results. Another issue is that laboratory results based only on insects’ mortality cannot account for the service life expectations, such as the impact of aesthetic damages, maintenance and expected durability of wooden construction parts.
... Putting a focus on male neotenics in recent years, some researchers believed that the external morphology of some male neotenics did not differ significantly from those of workers or nymphs (Pichon et al., 2007;Fujita & Watanabe, 2010). These male neotenics were designated as inconspicuous males, or reproductive males. ...
Article
Reproductive systems of termite colonies may involve the number of individuals in the reproductive caste and the copulatory selectivity of reproductive individuals (i.e., polyandry or polygamy), both of them impacting directly the fertility and genetic diversity of the colony. Polygamy is widespread in the lower termites, whereas polyandry appears to be mostly absent in termites. In this paper, the differentiation of male and female neotenics was observed in orphaned experimental colonies of the subterranean termite Reticulitermes labralis. The artificial orphaned colonies began to produce neotenics only a week after colony establishing, with more neotenics appearing in the same group as time went by. Finally, each experimental group reserved multi-neotenics consisting of male and female neotenic individuals. Our results demonstrated that these neotenic individuals retained in the colony participated in reproduction. A genetic analysis at four microsatellite loci showed that in addition to the conspicuous morphologically male reproductives, there were inconspicuous males or workers that had copulated with the females in the orphaned colony. Multiple male and female reproductive individuals existed together in a single colony, and one female neotenic could mate with several male reproductives in a short time. Thus, multiple male and female reproductive systems and a polyandric mating system are present in R. labralis.
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The protection of wood against termites is a major global problem, especially in the tropics and subtropics, and has been the subject of considerable research to understand termite biology and to develop effective mitigation methods. Field trials are useful for this purpose, but they often lack the degree of control and reproducibility needed. As a result, many researchers use laboratory methods when evaluating new wood preservatives or the suitability of timber for specific uses. These methods have developed over many years and in many regions with differing termite species and risks. Some methods differ only slightly from one another, but others use dramatically different approaches based upon the behavior and biology of a given termite species. The range of methods can make it difficult to make comparisons in terms of termite behavior, timber species preferences, or treatment efficacy. This review assembles the methods used for evaluating termite attack, explaining the underlying termite biology connected with each method, and identifying commonalities that might facilitate comparisons between various data sets, or potentially standardizing the standards. Understanding the essential characteristics of test methodologies can help identify the most appropriate methods for assessing the effectiveness of a given treatment, but it may also help compare results from different approaches, thereby avoiding redundant tests.
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Previous behavioral and genetic studies of Reticulitermes spp. suggest that colonies can occasionally merge together. To determine if colonies of R. flavipes may merge and whether reproductives from the two original colonies may interbreed with each other, we performed a laboratory experiment in which large fragments of colonies were paired together and provided with a common foraging arena. Observations were made on the nature of the interaction between workers and on whether colonies fused. We found a lack of aggressive behavior in 55% of the 20 colony pairing assays we performed. Colony pairings that demonstrated a lack of aggression spatially fused. In spatially fused colonies unrelated nestmates shared food resources, participated in trophallaxis, and tended unrelated brood. Microsatellite analysis of the immatures and eggs within fused colonies found that all progeny derived from only one of the two colonies that merged, indicating that reproductives from the two original colonies did not interbreed. Our results show that under laboratory conditions, colony fragments of R. flavipes may fuse in some cases. Our results also demonstrate that fused colonies can produce new functional replacement reproductives. This is the first time that two separate colonies that have fused have been reported to lay eggs and produce new larvae. The molecular data support the idea, however, that after two colonies merge, all progeny arise from reproductives originating from only one of the original colonies.
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This review assembles records of neotenic reproductives in 199 species in 61 genera in 6 families and adultoid reproductives in 35 species In 14 genera in 2 families of in the order Isoptera. Neotenic reproductives are reported for 61.7% of lower termite genera, but for only 13.4% of higher termite genera (Termitidae). Secondary reproduction is assessed in relation to the following nine termite ecotypes: 1) dry endoxylophagy, 2) damp endoxylophagy, 3) xylophagous foraging, 4) arborealxylophagy, 5) epigeous nesting, 6) mound building, 7) humivory, 8) grass and litter feeding, and 9) nest inquilinism. Neotenics appear to be common in termites that occupy all xylophagous ecotypes, but rare or obsolete in mound building and humivorous termites. Hypotheses concerning the role of neotenic reproduction in termite social evolution are discussed. Cross taxa comparisons show that facultative neoteny is a primitive element in termite caste systems, supporting the hypothesis that neotenics evolved as the first physical caste in termites due to individual-level selection forces associated with the primitive endoxylophagous ecotype. The origin of the neotenic caste would have introduced a reproductive alternative to alate development, and thus provided a direct-fitness component to the fitness outlook of nondispersing colony members. This potential for reproduction without dispersal would have reduced the fitness cost of not dispersing, and thereby may have promoted selection for further diversification of termite caste potentialities as pseudergates and reproductive soldiers. Thus, it is concluded that neotenic reproduction was an important enabling mechanism in the early eusocial evolution of termites. Neotenic reproduction has evolved as a less prominent feature of the biology of most higher termites and has been lost and replaced by adultoid replacement reproduction in the Macrotermitinae, and in other groups among the Termitidae. Adultoids appear to be selected over neotenics in taxa with a stable food base, centralized nesting, secure royal cells, and highly physogastric primary queens.
Article
Caste differentiation in pseudergates obtained from mature colonies of Reticulitermes flavipes (Kollar), R. virginicus (Banks) and R. hageni Banks was investigated at 5 densities (10, 25, 50., 75 & 100). Caste differentiation occurred in all 3 species, and generally, soldiers formed before reproductives. More soldiers formed at higher pseudergate densities than at lower densities. Supplemental reproductives developed in all 3 species which included both secondary (nymphoid) and tertiary (ergatoid) forms. Reticulitermes virginicus produced more reproductives than did R. flavipes or R. hageni. Additionally, more female reproductives formed than male reproductives. Reproductives formed within 3 to 4 months after separation from the founding colony, and all 3 species produced eggs that hatched. The number of eggs for the first clutch of eggs for R. virginicus, R. flavipes and R. hageni was 41, 67 and 68, respectively. It may be appropriate to rethink termite control strategies so as to not fractionate colonies during control procedures.
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In the previous report of parthenogenesis by neotenic reproductives (neotenics) of Reticulitermes speratus, neotenics from only one population were examined for parthenogenetic ability, although this species is distributed widely in Japan. In this study we examined parthenogenesis ability of neotenics from four areas in Honshu, Japan and revealed that all of the nymphoids and ergatoids from the four areas had parthenogenetic ability. Nymphoids produced significantly more eggs and larvae than ergatoids during the 180 days of the experiment. All of the offspring produced through parthenogenesis were female, and the chromosome numbers of the offspring examined in this study were diploid numbers (2n = 42). Microsatellite polymorphism analysis revealed that the heterozygous mother neotenics produced only homozygous offspring by parthenogenesis. The parthenogenetic ability that produced female, diploid, and homozygous offspring was common among the neotenics from the four sampling areas, and consistent with the previous report. Almost all the offspring produced through parthenogenesis differentiated into nymphs.
Conference Paper
In Isoptera, the polymorphism differs from that observed in the social Hymenoptera principally in two ways: the bisexual composition of the society and the hemimetabolous development. The former relates to (and perhaps is a consequence of) the mechanism of sex determination, which differs from the haplo-diploid system of the Hymenoptera. The latter allows the immature stages to play an active role in the social organization and to be subject to different social influences. This, when combined with the versatility of the post-embryonic development, promotes a higher complexity in the caste formation. This is especially noticeable in the extraordinary diversity of the replacement or secondary reproductives, which may be either true imagines, as in Hymenoptera, or have differentiated from nymphal instars or from the workers. In this review, three main topics will be examined: the differentiation of the reproductives (both primary and secondary), their maturation and behaviour, and finally the evolution of the reproductive strategies.