Bulletin of Entomological Research (2003) 93,439-445 DOI: 10.

1079/BER2003258

Termite colony ontogeny: a long-term

assessment of reproductive lifespan, caste
ratios and colony size in Reticulitermes
flavipes (Isoptera: Rhinotermitidae)
C.E. Long*, B.L. Thorne and N.L. Breisch
Department of Entomology, University of Maryland, 4112 Plant Science
Building, College Park, MD 20742, USA

Abstract
Thirty Reticulitermes flavipes (Kollar) colonies established by alates collected
from two separate field sites were raised in the laboratory for eight years. Twenty-
one of the colonies were founded by alates from one field source and nine from
another, providing demographic data from two unrelated parental lineages.
Colony totals ranged from 3620 to 11641 individuals, with no significant difference
in size between lineages. Soldier caste proportion of the colony total and mean wet
weights for workers, soldiers and kings were significantly different between the
two lineages. This suggests that at least a portion of the variability observed in
caste ratios and body size may be heritable. One founding reproductive had died
in five of the colonies (17%); none lost both parents. The queenless colonies
contained exclusively female replacement reproductives (neotenics); the kingless
colony contained a female-skewed mixture of male and female neotenics. All the
nests that lost a founding parent contained significantly more pre-alate nymphs
than the nests with both a king and a queen. Comparisons with published reports
of ontogenetic patterns in other termites and social insects are discussed.

Introduction throughout the life of the colony, allowing for repeated,

Eusocial insect colony ontogeny includes the examination
of demographic profiles over time, including population size,
caste ratios and the production of fertile progeny. By studying
the way in which social colonies function and grow, their
ergonomic and ecological dynamics can be better understood.
Research with other eusocial insects has illustrated the impact
of resource availability and quality on colony growth
(Tschinkel, 1988), caste ratios (McGlynn &Owen, 2002) and
the production of sexual offspring (McGlynn et al., 2002) as
well as the impact of various reproductive dynamics on
colony growth and survivorship (Arcila et al., 2002). Similar
termite colony ontogeny research has focused primarily on
families of termites which occupy centralized mounds (Costa-
Leonardo et al., 1996), trees (Luykx, 1986, 1993) or epigeal
nests (ThMome, 1984). These structures house the reproductives
*Fax: (301) 314 9290
E-mail: cmall@wam.umd.edu
relatively non-destructive observation and manipulation.
Relatively little work has been done on species of
subterranean ternites (Lenz & Barrett, 1982; Lenz &Runko,
1993) which forage and nest in diffuse resources and
underground galleries. Such colonies may abandon their
nesting areas in response to disturbance or environmental
change, and a non-destructive method of repeatedly
surveying and assessing entire field colonies is currently
unavailable. Thus, analysis of subterranean termite colony
structure depends on destructive sampling (Howard &
Haverty, 1980; Howard et al., 1982) or indirect methods such
as mark-release-recapture field sampling (Grace et al., 1995;
Grace, 1996), inferences based on genetic analysis of collected
insects (Reilly, 1987; Jenkins et al., 1998, 1999; Vargo, 2000;
Bulmer et al., 2001) and the direct observation of laboratory-
reared colonies (Hlaverty &Howard, 1981; Thorne et al., 1997).
Population data were gathered from 30 eight-year-old
Reticulitermes flavipes (Kollar) (Isoptera: Rhinotermitidae)
laboratory colonies which were initiated with sibling alate
440 C.E. Long et al.
pairs in 1993. According to the literature, these are the
oldest, complete, R. flavipes colonies to be studied to date.
The termites lived in confined spaces free of predation and
competition, ate ad libit;m and were shielded from seasonal
extremes of temperature and humidity. These factors are
likely to have impacted on individual life spans, robustness,
and rates of colony growth. Although the magnitude of
values provided by these colonies may differ from field
values, the patterns and trends they illustrate augment our
knowledge regarding otherwise unattainable elements of
R. flavipes colony ontogeny, demography and development.
This demographic data focuses on three factors: (i) colony
growth and the lifespan of primary reproductives; (ii) the
number and sex ratio of neotenics; and (iii) a potential
genetic basis for caste proportions.
Materials and methods
Culturing techniques and population census
In 1993, 82 incipient colonies were established using pairs
of sibling alates from three separate dispersal flights in
Prince George's County, Maryland, USA. In order to
delineate the colonies produced by alates from the three
distinct field collections, the laboratory colonies were
classified as deriving from either lineage 1, 2 or 3, with each
lineage defined as the product of alates from a single field
colony. Although genetic analysis of these colonies is
pending, the geographical distance between the original
alate sources was sufficient (several kilometres) to assume
that the resulting laboratory lineages are not closely related.
Thus, differences observed between the identically-raised
lineages are likely to be genetic in origin.
The establishment and initial rearing of the colonies is
described in Thorne et al. (1997). In 1994, the termite diet of
decayed pine and hardwood sawdust was replaced with a
combination of weathered pine survey stakes and decayed
paper birch Bethla papyrifera (Marshall) (Betulaceae). Wood
was replenished when inspection indicated depletion.
Distilled water was provided regularly. In 1998, the colonies
were transferred to 185 x 187 mm (5.1 litre) clear plastic
containers (Pioneer Plastics, Inc., North Dixon, Kentucky,
USA). The laboratory was maintained at a constant
temperature of 23°C.
Since their founding in 1993, nearly two-thirds of the
original 82 colonies have died, including all of the pairings
involving lineage 2. Some of this mortality was attributed to
resource depletion or desiccation, but often no explanation
was evident. Within the first two years, 20 colonies died and
seven lost at least one of their primary reproductives,
leaving the 55 colonies containing functional primary
reproductives censused in 1995 (Thorne et al., 1997). Twenty-
five additional colonies were lost over the next six years.
Subsets of colonies were randomly selected for census in
1997 and 1999. Data from the 1999 tallies are included here,
but too few of the colonies examined in 1997 survived in
order to provide robust comparative analysis. In 2001, eight
years after initiation, 30 pairs remained, including 21 lineage
1 colonies and nine lineage 3 colonies.
The 30 surviving colonies were censused for the total
number of primary and secondary reproductives, workers
(neutral individuals), soldiers and presoldiers (hereinafter
collectively termed soldiers), larvae (instars 1-2) and
nymphs (see Laine & Wright, 2003). Egg number was
categorized into one of four ranges: 1-50, 51-100,101-300, or
> 301. Mean worker and soldier wet weights were calculated
for each colony using three replicates of ten individuals. Wet
weights were collected for each primary reproductive and, if
applicable, for the total number of male and female
neotenics within each colony. Colonies with functional
primary queens were designated 'queenright' (Wilson, 1971;
H-Iolldobler & Wilson, 1990), and by extension those with
primary kings were termed 'kingright.'
Statistical analyses
Comparative analyses were performed (SAS Institute,
2000) on data from both queenright and queenless colonies,
between colonies founded by alates from lineage 1 and
lineage 3, and between census totals from 1995, 1999 and
2001. When variances were equal, data were pooled and the
Student's t-test determined whether significant differences
existed. The Satterthwaite adjustment was used to
accommodate for unequal variances (SAS Institute, 2000).
Correlations were calculated with Pearson correlation
coefficients.
Results
Summany statistics of eighlt-year census
Colony totals of R. flavipes in 2001 ranged from 3620 to
11641 individuals, averaging 7193 (SE ± 357), with the
majority being workers. Soldiers constituted a mean of 2.6 ±
0.03 % of nest totals, which is consistent with the expected
average of 2% for R. flavipes. All colonies contained larvae,
with totals ranging from 37 to 2672. Mean queen wet weight
was 9.3 ± 0.4 mg, almost double mean king wet weight, 4.6 t
0.001 mg.
Differences between parental lineages
Data from the two unrelated alate lineages were analysed
for differences in total population size, caste proportions and
individual body weight. Across both founding lineages,
colonies contained a wide array of soldier proportions,
ranging from 0.57 to 6.9%. Lineage 1 colonies repeatedly
exhibited a significantly higher proportion of soldiers than
lineage 3 nests, containing more than twice as many soldiers
in 1995,1999 and 2001 (fig. 1). Lineage I soldier numbers in
2001 were unaffected by the reproductive status of the
colonies, appearing in equivalent numbers in the presence of
either primary or secondary reproductives (P = 0.189, t =
1.34, df = 20).
The colonies derived from lineage 3 contained
significantly more members than those founded by lineage 1
alates during the initial 1995 census, but in subsequent years
total colony population sizes from the two parental lines
were equivalent (table 1). Comparisons between
reproductive mean wet weights over time were varied: kings
from the lineage I colonies and queens originating from
lineage 3 were slightly smaller in 2001 than they had been in
1999, lineage 3 kings were unchanged over the two year
interval and the lineage 1 queens were heavier.
Across all castes, individuals from lineage I were
consistently larger than their lineage 3 counterparts at each
census (table 1). Lineage 1 workers weighed more at all three
census dates, significantly so in 1995 and 2001. Workers from
 Reticutlitermesflavipes colony ontogeny 441

350 - the queenless colonies were excluded from this analysis; a

colony's reproductive status appears to influence worker
3 - *a size. Insufficient data exist to compare soldier weights over
300 - time, but in 2001, lineage 1 soldiers were significantly larger
25 than those in lineage 3 (P = 0.036, t = 0.63, df = 28). On
.CD 250 - average, lineage 1 reproductives were larger than those in
0 lineage 3. In all censuses, lineage 1 kings were significantly
O 200
- heavier than lineage 3 kings. Lineage 1 queens were larger
_ 200 * than their lineage 3 counterparts on all three dates,
significantly so in 1995 (table 1).
E 150-
1 h Queenright vs. queenless colonies
C
s; 100- n
The 1995 population census focused on incipient
colonies; seven of the 62 surviving colonies had lost their
50 primary reproductives and were excluded from the count.
Colonies which had lost primary reproductives were
0 included in the current survey to gain insight into the effects
of shifting reproductive dynamics on colony demographics.
Of the 30 eight-year-old colonies, 26 (88%) retained their
5 primary queens and 29 (97%) their primary kings.
b Neotenics were present in five (17%) of the colonies at the
4.5 - 2001 census; three of these families lost their queens (but
retained their kings) prior to the 1999 count, providing
4 - insight into the relatively long term effects of queenlessness.
10 I T I I Chi-squared analysis indicated2
that queen survivorship was
,, 3.5 - similar for both lineages (X = 0.160). In 2001, the queenless
colonies were equivalent to their queenright counterparts in
O- 3 |* T - 11 | total size, worker number, and egg rank (table 2). Larvae
c number was the only divergent category, with queenright
*- 2.5 - colonies containing significantly more larvae (P = 0.0007, t =
0
0_ -4.16, df = 17). Workers from queenless colonies were
2 2 significantly larger than those from queenright nests. Soldier
r- 1.5 2 | L l A weights and numbers were equivalent among the two
a~ 1.5 -

1
0.5 - Fig. 1. A comparison of soldier number (a) and the soldier
caste's proportion of the colony total (b) in colonies derived from
0 lo _l | _l | _l l l two unrelated lineages (C, lineage 1; l, lineage 2) of
Reticulitermesflavipes in 1995,1999 and 2001. *Denote significant
1995 1999 2001 differences among means (P < 0.05).

Table 1. A comparison of demographic data (mean ± SE) from two unrelated lineages of Reticulitermes
flavipes colonies in 1995,1999 and 2001.
Year Lineage 1 Lineage 3 t-test results
Colony size 1995 a 348 ± 35 500 ± 49 P = 0.032*
- 1999
b 4555 :478 5518±: 559 P = 0.213
2001 7324±:470 6891:t487 P = 0.587
Worker wt (mg) 1995c 2.1 ±L0.04 1.9 ± 0.06 P = 0.006*
1999 2.9 ± 0.1 2.6 ± 0.1 P = 0.091
2001 2.7 ± 0.1 2.4 ± 0.1 P = 0.042*
Queen wt (mg) 1995 6.4 : 0.2 5.0±t 0.2 P < 0.0001*
1999 8.6 + 0.4 9.3±: 0.5 P = 0.300
2001 d 9.3 ± 0.4 9.0 ± 0.4 P = 0.622
King wt (mg) 1995 4.1 :± 0.2 3.6±: 0.04 P = 0.0158*
1999 5.0 ± 0.01 4.1 ± 0.2 P = 0.0002*
2001e 4.8 : 0.001 4.1 d: 0.001 P < 0.0001*

* Denotes significant differences among means, where P < 0.05.

a Unless noted, lineage I N = 42 and lineage 3 N = 13 for 1995 data.
b Lineage 1 N = 9, lineage 3 N = 10 for 1999 data.
cWeights were collected from 44 colonies in 1995; lineage 1 N = 32, lineage 3 N = 12.
d Lineage 1 N = 17, lineage 3 N = 9.
e Lineage 1 N = 20, lineage 3 N = 9.
442 C.E. Long et al.
Table 2. A comparison of demographic data (mean * SE) from eight-year-old queenright
and queenless Reticulitermesflavipes colonies.
Queenright (N - 17) Queenless (N = 4) t-test results
Colony total 7548 ± 535 6373 ± 923 P = 0.339
Workers 6560 ±460 4999 ±705 P=0.156
Larvae 729 ± 139 63 + 30 P = 0.0007*
Soldiers 163 ± 18 229 * 51 P = 0.189
Nymphs 0.72 * 0.28 550a ± 86 P = 0.0001*
Eggs 175 ±64 63 ±30 P=0.130
Worker wt (mg) 2.7 ± 0.1 3.0 ± 0.2 P = 0.031*
Soldier wt (mg) 3.1 ± 0.1 3.0 ± 0.1 P = 0.94
*Denotes significant differences among means, where P < 0.05.
*One recently orphaned colony was excluded from this computation, thus N = 3.

colony types. In both 1999 and 2001, the three queenless and
one kingless colonies contained vastly more nymphs than
the queenright colonies (table 2).
Although all three queenless colonies increased in total
size during the two year interval between counts, average
numbers of female neotenics (10.5 :± 3.5) remained static
between 1999 and 2001 (P = 0.851, t = -0.20, df = 4). In the
one colony in which the primary queen outlived the king, 75
female and 52 male neotenic offspring developed. In order to
test the egg-laying capability of the queen and her coexisting
neotenic daughters, the queen and a subset of the female
neotenics were held individually for 72 h. In this time
period, each of the females produced eggs. The viability of
these eggs and the maternal origin of the nearly 1000 eggs
found in this colony is unknown.
Discussion
Lifespan of primary reproductives
These 30 laboratory colonies provided a rare, and possibly
unique, opportunity to monitor complete R. flavipes colonies
for an extended period of time. In 2001, when the colonies
were eight years old, 88% of the founding queens and 97% of
the founding kings were alive. These laboratory cultures add
novel data to Keller's (1998) compilation of ant and termite
queen lifespans, which illustrated broad variability in
maximum queen lifespans, ranging from a 5.9-year-old
Zooterinopsisangusticollis(Hagen) (Isoptera: Hodotermitidae)
reproductive parent may initiate the development of
immature colony members into secondary reproductives or
neotenics. In the family Rhinotermitidae it is thought that
multiple female neotenics differentiate simultaneously after
queen loss. As a group, these replacement females are
believed to have greater egg-laying capacity than individual
primary queens (Miller, 1969; Nutting, 1970; Myles, 1999). In
R. flavipes dolonies, this increased reproductive potential is
thought to accelerate colony growth and account for field
populations estimated to be in the hundreds of thousands, if
not millions (Snyder, 1920, 1934, 1954; Pickens, 1934; Myles
& Nutting, 1988; Grace, 1996).
Neotenic individuals were identified in five of the 30
colonies (17%) in this study, all of which retained one of their
primary parents: four contained a surviving king and one a
surviving queen. Three of the queenless colonies lost their
primary females prior to 1999, providing relatively long-
1.2 -
1.1 - o o 0 o
1 -
.0

queen to Macrotermes mnichaelseni (Sj6stedt) (Isoptera: a)

0.9 -
Termitidae) queens that lived for 19 years. Reproductives of
both genders grew steadily over time during this study, with 0~~~
3CD S *S %
the queens nearly double the size of their mates. In censuses aCD
°
conducted when the colonies were two and six years old, 0.8 -

queen weights and total colony sizes were statistically 0 as 0~~~

independent, exhibiting no correlation. As predicted by 0
Thorne et al. (1997), the correlation between these two 0.7 -
elements have became significant as the queens have
matured (fig. 2). This relationship has also been observed in
Nasutitermes (Thorne, 1984) and Odontotermes (Buo-Yao, 0.6 - ,
. &
. ,
. 5
z
,

1988), as well as in the ant genus Camponotuts (Fowler, 1986). 2000 4000 6000 8000 10000 12000
Total colony size
Number and sex ratio of neotenics and their impact on colony
growth rate
Fig. 2. Queen weights and total colony sizes are positively
In 61.7% of lower and 13.4% of higher termite species correlated in 17 eight-year-old colonies of Retictlitennesflavipes; r
studied (Myles, 1999), the loss of either primary = 0.54, P = 0.0048.
 Reticutlitermesflavipes colony ontogeny
tertm"data from colonies whose egg production had shifted
from primary tqk secondary reproductive females. All four
queenless colonies contained exclusively female neotenics.
The one kingless nest contained a female-skewed group of
neotenics containing both genders.
Although all three of'the,R. flavipes colonies that were
queenless in 1999 incrased hin tal size during the two year
interval between counts, the average number of female
neotenics (10.5 : 3.5) was unchantgdifrom 1999 to 2001. The
unexpectedly low numbers of fema bneotenics may be
associated with small colony size (relative to field colonies)
or spatial constraints of the laboratory nesting areas;
however, the response of the one kingless but queenright
colony suggests that the numbers of neotenics that
differentiate in a colony is influenced by more than just
colony or nest size. In this colony, the primary queen
outlived the king, and 127 neotenics of both genders
developed. This single example is insufficient to support any
conclusions, but ongoing studies, including experimental
queen- and king-removal treatments compared to king and
queen controls, will be of significant interest.
Gender ratios vary within neotenic cohorts that develop
in response to the loss of either male and female primary
reproductives. Coptotermes lactenis (Froggatt) (Isoptera:
Rhinotermitidae) nests which lost both primary
reproductives produced cohorts of heavily male-biased
neotenics (Lenz & Runko, 1993), while comparably
orphaned R. flavipes colonies produced female-skewed
neotenic subpopulations (Howard & Haverty, 1980). Grasse
& Noirot (1969) determined that the loss of Kalotermes
flavicollis (Fabricius) (Isoptera: Kalotermitidae) primary
queens resulted in development of both male and female
neotenics but loss of the king led only to the differentiation
of males. In contrast, colonies of Armitermes euamignathus
(Silvestri) (Isoptera: Termitidae) (Costa-Leonardo et al.,
1996) colonies which lost their queens but retained their
kings produced only female neotenics. Lenz & Runko (1993)
noted that orphaned colonies of C. lacteuts produced
equivalent female neotenic biomass, but that it was
apportioned among either a few large females or numerous
small females. It is possible that the colonies in this study
followed a strategy of producing a few large female
neotenics. Gauging the relative size of these replacemnent
females is difficult given the rarity of data from similarly
aged neotenics which are the product of comparably sized
colonies. Future laboratory manipulation of R. flavipes
colonies as well as the continued monitoring of these nests
will be important in this regard.
In addition to development of secondary reproductives,
it has been observed that recently orphaned C. lacteus nests
produce numerous nymphs of both genders (Lenz &Runko,
1993). It has been calculated that orphaned colonies are at
greater risk of failure than complete nests; thus, nymph
production is undertaken to maximize the survival of a
colony's genes via alate dispersal (Lenz &Runko, 1993). In
both 1999 and 2001, the three queenless and one kingless
colonies in our study contained vastly more nymphs than
the queenright colonies. Nymphal individuals may have
been produced in anticipation of an alate dispersal flight
(Lenz & Runko, 1993) or subterranean colony budding
(Snyder, 1920), neither of which were possible in the
laboratorv due to the lack of environmental cues and remote
galleries, respectively.
443
Potentialgenetic basisfor caste proportionsand sizes of
- individuals
The termite soldier caste is physically distinct and
exclusively defensive; soldiers are unable to collect food and
are wholly dependent on their nestmates for sustenance
(Haverty, 1977). The percentage of soldiers in a colony is
thought to be consistent within species (Howard & Haverty,
1980; Noirot & Darlington, 2000), although interspecific
competition, predation pressure and seasonality account for
some fluctuation (Haverty & Howard, 1981; Howard &
'Haverty, 1981). By working in the laboratory with colonies
derived from two groups of unrelated alates, the extemal
challenges that might impact caste proportion were greatly
reduced, increasing the likelihood that differences in caste
ratios were due to heritable traits.
Soldier ratios within R. flavipes field colonies range from
0.67 to 10.8% (Banks & Snyder, 1920; Grace, 1996). Across
both lineages, the study colonies contained a mean of 2.6 ±
1.6% soldiers, consistent with the published average of 2%
for R. flavipes (Howard &Haverty, 1980). However, lineage 1
colonies repeatedly exhibited a significantly higher
proportion of soldiers than lineage 3 colonies, containing
more than twice as many soldiers over eight years. These
proportions were unaffected by the reproductive status of
the colonies, appearing in equivalent numbers in the
presence of either primary or secondary reproductives, a
finding consistent with Luykx's (1986) work with colonies of
Incisiterines schwarzi (Banks) (Isoptera: Kalotermitidae).
These findings suggest that genotypic variation underlies a
portion of the deviation in soldier ratios observed in
conspecific field colonies.
The colonies from our two lineages also exhibited
significant, consistent variability in body size. Across all
castes, individuals from lineage 1 were larger than their
lineage 3 counterparts. Average worker body sizes peaked in
1999 and fell slightly in 2001. This finding is in contrast with
Grace et al. (1995) who found that the mean worker size in a
C. formosanuts colony increased by approximately 15% after a
comparable time interval.
Among polymorphic ant species, caste proportion may
be influenced by both environmental variables, including
food availability (McGlynn & Owen, 2002), conspecific
competition (Passera et al., 1996), and predation (Herbers,
1980), as well as internal variables such as colony age
(Gibson, 1989) and the number of queens in the colony
(Kenne et al., 2000). There has been little examination of the
role intrinsic, genotypic factors may play in the
determination of social insect caste ratios.
This analysis of eight-year-old, complete, laboratory-
reared R. flavipes colonies provides demographic
information regarding colony growth rate and longevity,
lifespan of founding reproductives, the response of colonies
to the loss of founding kings and queens, and the
contribution of intrinsic factors in determining caste ratios
and individual body sizes. These fundamental elements of
colony ontogeny and demography delineate pattems of
growth, investment, reproduction and survivorship that
impact both intra- and extra-colony dynamics in these
eusocial societies. Ontogenetic field studies have been used
to predict territorial expansion rates of both feral (Oldroyd et
al., 1997) and Africanized honey bees (Otis, 1982), and
similar forecasts of R. flavipes reoccupation of disturbed
landscapes would be valuable. Insight gained from
444 C.E. Long et al.
subterranean termite laboratory colonies will aid in the
development of nest growth models similar to those
available for species of ants which, like R. flavipes, depend on
heterogeneous and unpredictable food resources (Chew,
1987; McGlynn et al., 2002) or which have the flexibility to be
either mono- or polygynous (Tschinkel, 1988; Arcila et al.,
2002).
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(Accepted 13 June 2003)
i CAB International, 2003
COPYRIGHT INFORMATION

TITLE: Termite colony ontogeny: a long-term assessment of

reproductive lifespan, caste ratios and colony size in
Reticulitermes flavipes (Isoptera: Rhinotermitidae)
SOURCE: Bull Entomol Res 93 no5 O 2003
WN: 0327404110007

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