Morphological changes of different castes of the subterranean termites (Odontotermes proformosanus) in fungus combs of termitophiles 1 2

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1 The Journal of Plant Protection Sciences, 2(2) : 19-26, 2010 Morphological changes of different castes of e subterranean termites (Odontotermes proformosanus) in fungus combs of termitophiles 1 2 Parvin Noor and Md. Nashir Uddin 1 Biological Research Division, BCSIR Laboratories, Dhaka, 2 Planning and Development Division, BCSIR, Dr. Qudrat- I- Khuda Road, Dhandmondi, Dhaka Bangladesh, p.noor@yahoo.com A B S T R A C T Termitidae is e largest family of termites. The workers of e subfamily Macrotermitinae have e extra-ordinary phenomena of making fungus combs inside e termitophiles. Considering e consistency of fungus-bed in e termitophiles, an attempt has been made to observe e morphological changes of nymphs while ey stayed wiin e fungus comb. Biological attributes indicated at Odontotermes proformosanus are polymorphic in nature and have exopterygote post-metamorphic development. During e period of study, eggs and nymphs were collected in different seasons from e fungus combs of termite mounds. Eggs of O. proformosanus were found profusely in fungus comb in e mons of March, May, September and October of 2006 to 2008 Average lengs and standard deviation (mean±sd) of e eggs were (0.66 ± 0.09), wid (0.04 ± 0.07) mm and egg shape ratio is Eggs were mostly of broad type. st st Distinct quiescent period was also observed. Morphological changes completed wiin 1 to 5 stages. In e 1 stage, total leng ranged from mm. Terminal form of workers and soldiers were attained at e 5 stage ( mm in body leng). During e period of observation, it was found at total leng of e nymph, head leng and head capsule wid are significantly correlated at 0.01 level in eir five different development stages. Keywords: Fungus comb, Odontotermes proformosanus, morphological changes, nymphs, termitophiles. Introduction Termites are found in a wide range of terrestrial environments and are distributed roughout e tropical, subtropical and temperate regions of e world (Krishna & Weesner 1970, Wood & Pearce 1991). All are eusocial and e colony composed of distinct castes, which include workers, soldiers, nymphs and larvae (Krishna 1989). Nymphs are prealate forms, which function as reproductive stock for e colony. Larvae are e undifferentiated young of e reproductive stocks, which are hatched from eggs as tiny, immature, incapable of feeding (Howard & Haverty 1980). The largest family Termitidae of termites is divided into subfamilies Serritermitinae, Amitermitinae, Termitinae, Macrotermitinae and e Nasutitermitinae. The worker castes are always quite easily separated from e young, undifferentiated, immature forms of e oer castes. Often ere are different forms of e workers and soldiers eier in size, shape or bo wiin e same colony. Workers have a vital role in e colony. Workers feed all e dependents castes; maintain colony atmospheric homeostasis and build and repair e nest. But e workers of e subfamily Macrotermitinae show e extra-ordinary phenomenon of making fungus combs inside e termitophiles (Hickin 1971). Several suggestions have been made concerning e role of fungus gardens in termite colonies. They have been considered to be a source of food and vitamins (Grassé 1937) and also temperature (Luscher 1951) and humidity regulating devices. It is generally agreed at e fungus attacks lignin-cellulose complexes making cellulose accessible to termite digestion (Lee & Wood 1971). However, e mechanism by which fungus growing termites utilize cellulose

2 20 has been a matter of speculation (Noirot & nymphs and eggs were observed and under Noirot-Timoéé 1969, Abo-Khatwa 1978). microscope wi ocular-micrometer The nests of Macrotermitinae are unique in at magnification (18 4x). Egg size and shape were all excreta are used to construct fungus combs measured and classified according to Roonwal and e workers furer utilize e fungus combs (1975). To observe e morphological as food and nursery chambers (Wood & Sands differentiation of different caste, total leng of 1978). A large number of workers, soldiers and e nymph, head leng and head capsule wid young nymphs live in fungus combs. were measured, following e measurement Sometimes cluster of eggs were noted wiin index of Roonwal and Chhotani (1989). e fungus comb. The study of e post- According to em, ratio of head leng, head embryonic development of termites is wid and total body leng of e nymph were unusually difficult. Direct observation of e presented as head leng: head wid: total numbers of instars and of e course of caste body leng, where calculations were showed differentiation is impossible in natural colonies considering total body leng of nymph equals and e plasticity shown in e development of to one. To find out e morphological change of e castes from nymphs of different stages nymphs, e relationship of total leng, head renders it difficult to be certain as to how far leng and head capsule wid of nymph e some of e developmental processes revealed collected data were analyzed statistically and in artificial colonies are a regular feature of e mean, standard deviation, Duncan's natural development (Imms 1957). Grassé Multiple Range Test (DMART) and oer (1949) has given a useful interpretative calculations were evaluated considering 1% summary of available information and e level of significance by a computer packace diversity of modes of development. So, programme called SPSS (Statistical Package for considering e consistency of fungus-bed in Social Science) of version 14, now frequently e termitophiles, an attempt has been made in being used to analyze all sort of data and is e present study to observe e morphological version was developed by SPSS Inc. in changes of nymphs while ey remain wiin Result and Discussion e fungus comb. A queen and a king were collected at e time of Materials and Meods digging from a termite mound (Fig.1 a,b). The Odontotermes proformosanus of Termitidae queen collected was 7.5 cm long and 2.0 cm family was selected as e study material for e wide. Leng of e king was 1.5 cm. Colour of morphological changes of different castes. e egg was milky white. Various number of Fungus combs were collected randomly by eggs found in fungus combs in different mons digging different termite mounds at a dep of were collected from different termite mounds. It cm from e ground roughout e study was noticed at e number of eggs were huge period from Savar, a suburban area of Dhaka in March, May, September and October, city in Bangladesh. Nymphs and eggs were medium in August and few in e mons of separated from e fungus comb wi a camel April, July and December of 2006 to Eggs hairbrush and kept in petridishes. Collected were not arranged in any orderly manner and

3 21 were attached loosely to e fungus combs transparent indistinct denticles emerged in (Fig.1c). The eggs of O. proformosanus were immature workers and elongated transparent mostly of broad type (Ratio was more an 0.45) mandible wiout denticle in immature soldiers and a few were of medium type (Ratio was 0.40 (Fig.2.d). Among e 30 nymphs studied (Table ). Total leng of e eggs varied from 0.5-1) mean and standard deviation in total leng, 0.8 mm, wi mean and standard deviation head leng and capsule wid were 2.03 ± ±0.09 mm. Wid of e eggs ranged from mm, 0.89 ± 0.27 mm and 0.64 ± 0.10 mm and e mm; mean ± SD, 0.4 ± 0.07 mm ratio of total leng and head leng 32:0.72:1. rd (Fig.1d). Different developmental post- In e 3 nymphal stage, when e total leng embryonic stages wiin eggs were noted was mm, pre-soldiers (Fig.2 e, f) and chronologically. The eggs were oval and milky pre-workers (Fig.2 g,h) could easily be white. Distinct embryo was observed wiin e recognized. Soft, transparent denticle emerged egg (Fig.1e). Post-embryonic condition was in e mandibles of immature worker and noted in e centre of brown coloured egg, wi soldier. Mandible of e immature workers blackish border. The content of e egg was became more or less stout. It was also noticed black wiin e eggshell ( Fig.1 f, g). Pharate at in few immature workers and soldiers larval stage was noted (Fig.1 h). Prequiescent denticle did not develop. Pronotum was found to stage of e larva and eir ecdysing stages were be fully developed in bo soldiers and workers. visible (Fig.1 i, j, k). Quiescent phase of termite Head and abdomen were milky white in colour. was distinctly visible in O. proformosanus Under is group, 30 nymphs were measured (Fig.1l ) wi flexed head, orax and immobile (Table 1). Ranges of total leng, head leng limbs noted in e plates. Incubation period and capsule wid of e nymphs were 3.23 ± could not be determined. 0.31, 1.25 ± 0.37 and 0.98 ± 0.21mm From table 1 it was found at O. proformosanus respectively, wi e ratio of total leng and st was polymorphic in nature. Lengs of e 1 head leng 0.36:0.36:1. stage were ranged from mm. The In e 4 stage, total leng of nymph varied nymphs were milky white in colour. Head and from 3.6 to 4.0 mm. Pronotum and mandibular pronotum were not distinct, mandible was not denticles of e pre-soldier could distinctly be developed, soldier and worker could not be differentiated (Fig.2 j). Mandible turned into differentiated (Fig.1.m, n). In some of e light brown and head into yellowish brown. nymphs wiin e range of mm, Abdomen and pronotum were found milky transparent soft mandible wiout denticle was white. Total leng ( mm) of some noticed. A total of 42 nymphs were observed in preworkers became yellowish white (Fig.2 i). st 1 stage, where ey varied total leng in 1.14± Twenty one nymphs of is group were 0.26 mm, head leng in 0.51± 0.16 mm and measured (Table 1). Mean and standard head capsule wid in 0.42 ± 0.12 mm and e deviation of nymphs, when total leng was 3.80 ratio of total leng and head leng was ± 0.14 mm, head leng 1.61± 0.20 mm and nd 0.36:0.81:1 (Fig. 2 a,b). In e 2 nymph stage, capsule wid 1.12 ± 0.21mm. The ratio of total mm (Fig.2 c, d), soft mandible structure leng and head leng was 0.28: 0.67:1. could be recognized. Short mandible wi

4 22 The 5 stage measured 4.1 to 4.5 mm. Their leng and head leng was 0.34:0.84:1. abdomen turned brown, e outer edge of e Mean of total nymph leng (TL), head leng mandibles turned dark brown and became (HL), and head capsule wid (CW) of e five stronger. Nymphs ranged from mm were groups, revealed at total leng of nymphs confirmed as soldiers and workers (Fig. 2.k, l). nd were found increasing uniformly up to 2 stage A total of 22 nymphs of is group were studied rd and again from 3 stage to 5 stage but a sharp (Table 1). Mean and standard deviations of total nd rd increase was noticed from 2 to 3 stage. leng, head leng and capsule wid of However, e head leng and head capsule nymphs were 4.31± 0.14 mm, 1.76± 0.37 mm wid were found to increase more or less at a and 1.25 ± 1.9 mm likewise. The ratio of total Table 1. Morphological changes observed in different nymphal stages of O. proformosanus collected from fungus combs No. of nymph Different stages (mm) 42 1 st Stage ( ) 30 2 nd Stage ( ) 30 3 rd Stage ( ) 21 4 Stage ( ) 22 5 Stage ( ) TL (mm) Mean + SD HL (mm) Mean + SD CW (mm) Mean + SD Ratio of TL and HL 1.143±0.26 e 0.514± 0.16 d 0.417± 0.12 d 0.36:0.81: ±0.27 d 0.893± 0.27 c 0.643± 0.10 c 0.32:0.72: ±0.31 c 1.250±0.37 b 0.977± 0.21 b 0.36:0.36: ±0.14 b 1.609±0.20 a 1.121± 0.21 b 0.28:0.67: ±0.14 a 1.755±0.37 a 1.248± 0.19 a 0.34:0.84:1 TL = Total leng of e nymph, Hl = Head leng of e nymph, CW = Head capsule wid * Means followed by same alphabet do not differ significantly ( P=0.01) by DMRT Morphological characteristics H e a d a n d p r o n o t u m n o t differentiated. In some nymph's s o f t m a n d i b u l a r s t r u c t u r e developed wiout denticle. Colour of e nymphs' milky white. Dentition of e mandible just emerged, transparent in colour. Immature worker recognized. Elongated mandible not fully developed. Immature soldiers presumed. Mandible developed wi tender denticle, transparent; preworker a n d p r e s o l d i e r e a s i l y differentiated. Head and abdomen milky white in colour. Mandible wi denticle and pronotum distinctly differentiated. Mandible colour turned into light brown, head yellowish brown. Abdomen and pronotum milky white. Colour of e abdomen turned brown. Mandible became hard and its outer edge brown. Nymphs ranging from mm leng were mostly recognized as mature soldier and worker. Abdomen colour turned into yellowish brown.

5 23 uniform rate (Fig.3). From table 2, caste development was found to be strongly associated wi e change of e total leng, head leng (r=0.89) and head capsule wid (r=0.91). Association of head leng wi total leng (r=0.89) and wi head capsule wid (r=0.90) was also strongly significant. Relative grow was strongly significant in case of head capsule wid and total nymph leng (r=0.91) and also wi head leng (r=0.90). Correlations in e five developmental stages showed to be significant at 0.01 levels (2-tailed). Leng (mm) TL HL CW Ist 2nd 3rd 4 5 Nymphal stages Fig. 3 Correlation of total leng, head leng and head wid of e nymphs of O. proformosanus. In e present study types of eggs found in e fungus combs were mostly broad, while some medium eggs were also noted. This agrees wi Roonwall and Chhotani's (1989) finding at advanced Termitidae family consists mostly of e broad type of egg. Hill (1925) mentioned at Mastotermes lays cluster of eggs cemented togeer wi a gelatinous secretion. In e present investigation cluster of eggs were found to be much more an e number cited by Hill. Moreover, eggs in e fungus combs were found wiout cementing materials, eggs were arranged in an irregular manner and attached loosely. Juvenile stage observed in e present study was also mentioned by Hopkins (2003). He cited at immature termite like all juvenile insect, must periodically go rough e molting process in which ey shed eir skin i.e. exoskeleton in order to grow. Weyer (1935) and Synder (1913) mentioned about a quiescent period, which is most pronounced in e ecdysis at gave rise to soldiers and primary reproductives. In Macrotermitinae (Termitidae) e insect lies on its sides wi head flexed upon e ventral aspect of e orax and e limbs and oer parts remain immobile. Present investigation corresponds wi e quiescent period of O. proformosanus as shown in e (Fig.1l). Imms (1957) pointed out at caste differences appeared during e course of postembryonic development. The major and minor forms of workers and soldiers may be distinguished in e preceding nymphal stages. st In e present investigation it was found in e 1 stage at caste could not be differentiated, but nd differentiation could be detected from e 2 stage. Hickin (1971) stated at some soldiers d e v e l o p e d f r o m n y m p h s t h a t a r e indistinguishable from e nymphs at would produce workers. In addition, e soldier can be produced from a fully developed worker. In e st present observation it was found at in e 1 stage appearance of e nymph was like worker, nd differentiation was found in e 2 stage. The soldiers are mostly dimorphic (Table 1) which is corresponding to Hickin and Weesner (1960) statement. Transitional form of e nymph was referred by Hickin (1971) as white soldier, on account of absence of pigmentation in em and generally observed only between one and two rd week. The 3 instar, pigmented individual of T. tenuirostris and 4 instar apterous individual of G. perplexus and A. wheeleri may be validly designated as definite workers (Light & Weesner 1955). It was noticed in e present study at no rd pigmentation could be observed up to 3 stage of e nymphs. Pigmented mature worker was

6 24 obtained at 4 stage of nymph. This observation agrees wi at of Light and Weesner (1955) on G. perplexus and A. wheeleri. H i c k e n ( ) m e n t i o n e d t h a t i n Macrotermitidae ere are ree stages of nymph. This statement does not agree wi e present work, where four stages of nymph were observed (Table. 1). According to Imms (1957) dimorphism occurred in Macrotermes esterase, O.obesus, O.redemanni, O.horni and in many species of e genus Trinervitermes. The present study revealed at O. proformosanus workers and soldiers were dimorphic. The terminal form of workers and soldiers were attained at 5 stage (Table 1 and Fig. 2 k, l). In e present study it was found at, mandibles nd rd Acknowledgement were soft and transparent in 2 and 3 stage. In e 4 stage e mandibles were hard, having nd rd pigmentation. In 2 and 3 stage denticles were The auors pray for eternal peace of eir deceased reverend teacher Professor Mahmud- ul-ameen, Department of Zoology, Dhaka University for his supervision during e course of investigation. also soft and transparent (Fig.2c-h). Pigmentation and hardness of denticles were also noticed in 4 stage. Fernando (1960) observed at before e development of a soldier, e larva (all nymphs) not distinguishable from oer larvae moults into larval soldier wi characteristic head and mandibles but is pigmentless. Fernando's observation is corresponding wi e present study. The life cycle of termite is one of incomplete metamorphosis. The eggs hatch into larva. Worker, soldier or alate were reached eir terminal form rough several instars. A large number of populations of different castes were found in e fungus comb of Macrotermitinae termitophiles. Throughout e study period it was observed at e morphological changes and differentiation were associated wi e changes of leng, head leng and head capsule wids of e nymphs of O. proformosanus. Table 2. Relative grow of total leng, head leng and head capsule wid of nymphs of O. proformosanus. Total nymphal leng (mm) Head leng (mm) Head capsule wid (mm) Total nymphal leng (mm) Head leng (mm) Head capsule wid (mm) Pearson correlation Sig. (2-tailed) N Pearson correlation Sig. (2-tailed) N Pearson correlation Sig. (2-tailed) N **.913**.893** **.900** 1 - ** Correlation is significant at e 0.01 level (2-tailed).

7 25 1(a) 1(g) 1(b) 1(h) 1(c) 1(i) 1(d) 1(j) 1(e) 1(k) 1(l) 1(f) 1(m) 1(n) Fig1. Post metamorphosis stages of Odontotermes proformosanus (a) king and queen after collection from e nest; (b) king; (c) fungus comb wi irregularly arranged eggs; (d) close view of eggs. (e) egg wi initial metamorphic stage; (f-g) distinct pharate embryo inside e egg shell; (h) pharate embryonic stage. (i-k) ecdysing stages of e larva; (l) larval quiescent period; (m-n) larval stages of e termite. (Fig. d-n magnification 10x 40x). 2(a) 2(b) 2(c) 2(d) 2(h) 2(i) 2(j) 2(k) 2(e) 2(l) 2(f) 2(m) 2(g) 2(n) Fig 2. Morphological changes of nymphs of O. proformosanus (a-b) 1st stages of e nymph; (c) 2nd stage of e worker ; (d) 2nd stage of e soldier wi poorly developed mandibles; (e-f) 3rd stages of dorsal and ventral views of e immature solider wi transparent mandibles ; (g-h) ventral and dorsal view of e 3rd stage worker; (i) 4 stage, mature worker (j) 4 stage of e soldier transparent mandible wi denticles; (Magnification 10x 25x); (k) 5 stage, fully developed soldier; (l) fully developed workers on e surface of e fungus comb; (n) supplementary queen; (n) collected winged adult.

8 26 Literature Cited Krishna K Order: Isoptera. In An introduction to e Study of Insects. (Eds Borror D Triflehorn Abo-Khatwa N Cellulase of fungus-growing CA Johnson NF). Saunders College termites: A new hypoesis on its origin. Publishing, Philadelphia, USA. Pp Experientia 34 (5): Lee KE Wood TG Termites and Soils. Academic Fernando HK Termites of economic importance Press London and New York. pp in Ceylon. Termites in e humid tropics. Proceedings of New Delhi Symposium, Light SF Weesner FM The production and UNESCO, pp replacement of soldiers in incipient colonies of Reticulitermes hesperus Banks. Insectes Grassé PP Recharches sur la systématique et la Sociaux 2: biologie des termites de l' Afrique et la biologie des termites de l' Afreque occidentale Luscher M Significance of fungus garden in f r a n c a i s e. A n n a l e s d e l a S o c i é t é termite nests. Nature 167: Entomologique de France 106: Noirot C Noirot-Timoéé C The digestive Grassé PP Ordre des isoptères ou termites. In system, pp In Biology of Termites (Eds Traité de Zoologie (Ed Grasse PP), Paris, Krishna K Weesner FM). Vol. 1. Academic Masson. Insectes 9 : Press, New York, USA. Hickin NE The biology of termites. In Termites: A Roonwal ML On a new phylogenetically World Problem. Hutchinson, London, UK, pp. significant ratio (Wid/Leng) in termite eggs (Isoptera). Zoologischer Anzeiger 195(1-2): Hill GF 1925 Notes on Mastotermes darwiniensis Froggatt (Isoptera). Proceedings of e Royal Roonwal ML Chhotani OB The fauna of India and Society of Victoria 37: e adjacent countries. Isoptera (Termites). Zoological Survey of India 1: Hopkins JD Subterranean Termite Identification and Biology University of Arkansas, Division Snyder TE 1913 Changes during quiescent stages in e of Agriculture Cooperative extension services, metamorphoses of termites. Science 38: 487- pp Howard RW Haverty MI Reproductives in mature Weesner FM Evolution and biology of termites. colonies of Reticulitermes flavipes: Annual Review of Entomology. 5: abundance, sex ratio, and association wi Wood TG Sands WA The role of termites in soldiers. Environmental Entomology 9: 458- ecosystems, pp In Production 60. Ecology of Ants and Termites (Ed Brain MV) Imms AD Isoptera. In A General Text Book of Cambridge University Press, UK. Entomology- including e anatomy, Wood TG Pearce M J Termites in Africa e physiology, development and classification of environmental impact of control measures and insects. (Eds Richards CW Davies RG). damage to crops, trees, rangeland and rural Meuen and Co. Ltd. London, UK. pp buildings. Sociobiology 19: Weyer F 1935 Epielneuerungim Mitteldarm der Krishna K Weesner FM Biology of termites. Vol. I Te r m i t e n w a h r e n d d e r H a u t u n g. & II. Academic press, New York, London, Zoomorphology. Tiere. 30: pp.643.