68 Journal of Jazan University - Applied Sciences Branch Vol.1 No.1 December 2011 (Muharram 1433 H) Floral Biology and Visitors Behaviour Floral Biology and Visitors Behaviour of Acutangula (Decne.) N.E.Br. in Jazan Region, Southwestern Saudi Arabia

Y.S.Masrahi* and H.A.Bosly (*) Department of Biology, Faculty of Science, Jazan University, K.S.A.

Abstract Caralluma acutangula (Decne.) N.E.Br. is one of the most succulent of () in the Tihama hill slopes of Jazan, Southwestern Saudi Arabia. The flowers of the attract many visitors, some of which are pollinators which are represented by Diptera, especially from families Muscidae, Sarcophagidae, and Cal- liphoridae. To attract the pollinators flowers use and deception for brood and food site (Sapromyophily) thus the female flies are the most frequent visitors. This mimicry with structure of flowers affects the behaviour of flies and leads to the attachment of pollinia to the proboscis and transfers them to receptors (guide rails). Other visitors are butterflies, represented only by Plain Tiger ( – ) whose larvae feed on flowers. Some predators of Thomisidae spiders hide between flowers to catch Diptera prey. This study sheds some light on a complex system between flowers and their visitors in arid habitats.

Keywords: Caralluma acutangula,Flowers,Diptera,Mimicry, Pollination,Danaus chrysip- pus, Thomisidae.Jazan,Saudi Arabia. 1. INTRODUCTION The Asclepiadoideae (subfamily Apocy- colour patterns, and structural morphologies naceae) constitute a group showing com- (Faegri and Van der Pijl,1979;Sakai,2002). plex floral structures and pollination in On the other hand, some flowers repre- angiosperms (Kunze,1991; Albers and sent sites to attract many kind of visitors Meve,2002). Caralluma is a stem succulent vary in the behavior, some of them are of Asclepiadoideae, comprises about pollinators,while others prey on the pollina- 60 species distributed in arid and semiarid tors or even feed on the flowers itself (Du- regions of Africa and Asia (Bruyns,2000b; kas,2004). Müller and Albers,2002; Gilbert,2003). In No studies have been published on pol- Saudi Arabia, this genus is represented by lination and flower visitors of Caralluma, 6 species, restricted to the southwestern part except some scattered observations (see of the country (Müller and Albers,2002; Meve and Liede,1994), compared with Masrahi,2011). other genera like , , Reproduction success in higher and (Kunze,1991 and references depends on the activity of pollinators in pol- within; Masinde, 2004). lination. The flowers of many angiosperms This study documents floral biolo- have evolved many intricate mechanisms to gy and visitors behaviour in Caralluma attract pollinators including highly scented acutangula,which represents one of the floral parts, mimicry of brood and food sites, most succulent species of Asclepiadoideae in Southwestern Saudi Arabia.

(*)E-mail: [email protected] ISSN: 6050-1658 Journal of Jazan University - Applied Sciences Branch Vol.1 No.1 December 2011 (Muharram1433 H) 69 Y.S.Masrahi

2. MATERIALS and METHODS dent’s t-test. Study species and sites Caralluma acutangula is a perennial erect 3. RESULTS stem succulent, 0.4-1m tall. Flowers are Flower morphology crowded in terminal dark globose heads Flowers of Caralluma acutangu- on stems. Flowers bloom after summer la are arranged in dark large globose rain,from July- October. Field observations heads,pseudumbles inflorescence (fig.1,A). were conducted in rocky habitats (Tihama Flowers emit fetid scents,resembling rotten hill and slopes), 3 km east of Abu-Arish meat or decaying organic matter. The single city,Jazan district,southwestern Saudi Ara- flower consists of five petals(corolla lobes). bia, between 100-400 m a.s.l. Plant distribu- The surface of the corolla lobe is wrinkled. tion is patchy in these areas, where the plant The corona (the centre of the flower) -in grows in microhabitats between rocks and cludes white coloured stigma head sur- beneath . Average annual tempera- rounded by five staminal coronas. Five pol- ture is 32.3°C , whereas annual rainfall is lination units, the pollinia,are located on the between 186-328 mm . The study was car- margins of the stigma head, just above guide ried out in the flowering stage of summer rails. Guide rails represent narrow slits (to r a i n f a l l ( J u l y - O c t o b e r 2 0 1 0 ) . received pollinia)(fig.1,E). These guide rails Flower morphology produce droplets of nectar as seen under the Flower morphology was described based microscope. The droplets drop and accumu- on concepts of Asclepiadoideae (Liede and late in the nectar cavity below the guide rail Kunze,1993; Meve and Liede,1994). Flow- (fig.1,C). ers were collected from the field and imme- Pollination and visitors behavior diately transferred to the laboratory to be C. acutangula flowers were visited mainly examined under stereomicroscope. by insects in orders Diptera and Lepidoptera Flower visitors and their behaviour as well as Arachnoidae (Thomosidae-crab Sampling (in total 104 flowers) was under- spiders). taken in the period (07:00 a.m. – 16:00 p.m.). Diptera were the most frequent visitors At the same times, the behavior and move- to flowers (table 1.) followed by Plain- Ti ment of the visitors were observed closely. ger butterfly (as observed by larval stage The frequency of visitors were recorded as feeding on flowers), and finally crab spiders (very frequent, frequent, infrequent) (Taroda (Thomisidae). and Gibbs,1982). Specimens collected were Diptera visitors belonged to three fami- killed in chloroform tubes (insects bearing lies: Muscidae, Sarcophagidae, and Calli- pollinia) and examined immediately under phoridae. Female were more frequent than stereomicroscope or preserved in 70% etha- males (P<0.001) except Chrysomya margi- nol for subsequent examination. Samples nalis which male and female were equall in were identified by Amoudi(1997) in the case p e r c e n t a g e o f v i s i t i n g ( fi g . 2 . ) . of flies ; Larsen(1984) in case of butterflies; The behavior of all fly species was al- Taher and Faragalla (1990); Hawkeswood most similar whereby the fly lands on the (2003) in case of spiders (at family level). flower attracted to the corona at the center Statistical Analysis of the flower. In order to reach the nectar Data of visitors are represented as mean ± cavities inside,the fly then extends its pro- SE (visitors to N of flowers = 104). Statis- boscis and probe the surface of these narrow tical significance was evaluated using Stu- chambers which are wide enough only for 70 Journal of Jazan University - Applied Sciences Branch Vol.1 No.1 December 2011 (Muharram 1433 H) Floral Biology and Visitors Behaviour the proboscis (fig. 1,B). This activity leads decaying organic matter. Attraction in sap- to attachment of the pollinia to the probos- romyophilous flowers is by deceit, with flies cis (fig.1,D). In all cases,pollinia were found confusing the flowers for decaying organic attached only to the proboscis. Upon repeat- matter as a suitable brood and food site ing this process with the nectar cavity of (Faegri and Van der Pijl,1979; Dafni,1984; another flower, the pollinia enter the slit of Jürgens et al.,2006). Typical examples of guide rail and hence the flower ensures pol- sapromyophily are found in the genera lination (fig1, F). No pollinia were ever de- (Apocynaceae-Asclepiadoideae), tected adhering to the bodies of other groups Arum (Araceae), Rafflesia (Rafflesiaceae), of visitors. and some Orchids (Kevan and Baker,1983; Other visitors to the flowers of C. acutan- Beaman et al.,1988; Albre et al.,2003). gula were the Plain Tiger butterfly (Danaus On the basis of the above concepts,the chrysippus-Nymphalidae) and crab spiders flowers of Caralluma acutangula belong to (Thomisidae)(fig.3). Larvae of D. chrysip- sapromyophily syndrome since they have pus were frequently found on flowers and dark colour, pollination units not exposed, feed on corolla lobes (fig.3,A). The duration and odour resembling that of decaying or- of feeding behavior is not included in this ganic matter. study. On reaching maturity,the larvae left In entomophillous flowers,structures vary the flowers to search for suitable pupation and are adapted to fit the structure and be- sites (usually part of the stem just below the havior of insect pollinators. By analogy, flowers-fig.3,B,C). flower-visiting insects have many -modifi Thomisidae spiders were infrequently cations to get flower attractants (nectar and found on the flowers. They hide between ) especially in the mouthparts (Krenn flowers in inflorescence, waiting for Diptera et al.,2005). Flowers of C. acutangula prey (fig.3,D,E). don’t have easy access to nectar and pol- 4. DISCUSSION linia, so they must have many adaptations in Faegri and Van der Pijl (1979) have distin- shape,colour and odour to attract pollinators. guished two types of pollination syndrome Pollinators of C. acutangula are flies from for fly-pollinated flowers: myophily and families Muscidae,Calliphoridae, and Sar- sapromyophily. General features of myoph- cophagidae. These flies have a short probos- ily are simple structures ,light colours, im- cis. Most flower-visiting Diptera with a short perceptible odour,easy access to nectar and proboscis take nectar from flowers with open exposed sexual organs (anthers and stigma). and easily accessible nectarines (Bracken- Sapromyophily is characterized by dark bury,1995; Krenn et al.,2005). On the other or brown-purple colour (or blotched dark hand,flies of Muscidae,Calliphoridae, and spots), pollination units frequently have Sarcophagidae,especially species visiting C. great depth, and odour resembling that of acutangula flowers, common in slaughter-

Table.1. Frequencies of visitors for flowers of C. acutangula

Visitors Frequency Flies Very frequent Plain tiger butterfly Frequent Crab spiders Infrequent Journal of Jazan University - Applied Sciences Branch Vol.1 No.1 December 2011 (Muharram1433 H) 71 Y.S.Masrahi

Fig.1. A. Caralluma acutangula in its natural habitat. B. Musca domestica on a flower. C. L.S. in the flower.D. Pollinia attached to Musca domestica proboscis. E. guide rail. F. Guide rail after entrance of pollinium (L.S) (arrows indicate germination tubes). (abbreviations in C. cl. Corolla lobe, gr. guide rail, sh. stigma head, nc. nectar cavity, sc. staminal corona, o. ovary, s. sepal). 72 Journal of Jazan University - Applied Sciences Branch Vol.1 No.1 December 2011 (Muharram 1433 H) Floral Biology and Visitors Behaviour houses and garbage dumps, being share in to the proboscis. On repeating this process attracted to meat in which the eggs are de- with another cavity, the chance is suitable to posited (Buttiker et al.,1979; Gadallah and entrance of pollinium into the guide rail, and Bosly, 2006). Flowers of C. acutangula with thus the flower ensures pollination. The de- odour resembling rotten meat (or carcasses), pendence on flies for pollination seems to be and appearance with dark colour and wrin- an adaptive strategy, because these insects kled surfaces, mimic brood and food sites of are widespread, prefer high temperatures, t h e s e fl i e s . and are present at all times of the year (Büt- After the attraction and landing on the tiker et al.,1979; Faegri et al.,1979). flowers, the fly may try to search for a suit- Another visitor to the flowers of C. acu- able location to lay eggs(most of flies visit- tangula is the Plain Tiger butterfly (Danaus ing are females). In the behaviour of laying chrysippus-Nymphalidae). It is well known eggs in females, choosing a site correlates that butterflies of Danaus spp. feed - exclu to two stimulators: general stimulator to sively on poisonous plants of Apocynaceae site (odour) and special stimulator to spe- (especially Asclepiadoideae) which contain cific location (particular concentrations of cardiac glycosides (cardenolides) (Lars- cations in excretion decaying matter sensed en,1984; Zalucki and Brower,1992; Mebs by receptors on ovipositor of the flies) et al.,2005). The larvae sequester these poi- (Rice,1977; Byrd and Castner, 2001; Amendt sons and pass them to the adults in concen- et al.,2004). Therefore, fly females -can trated form. Small mammals and birds re- not lay eggs on dry decaying matter ( Byrd act with vomiting when they attempt to eat and Castner,2001; Amendt et al.,2004). In them (Mebs et al.,2005). The female of D. our field observations,we did not observed chrysippus lays eggs on the flowers. After eggs on the flowers, which may confirm the hatching, larvae feed on corolla lobes. It is above mentioned. Flowers of C. acutangula not known if the flowers of C. acutangula seem to mimic general stimulator to brood contain cardenolides or not. Some samples site (odour), whereas the dry appearance of of D. chrysippus feeding on Apocynaceae corolla lobes surfaces does not motivate the plants do not contain cardenolides (Mebs et special stimulator to lay eggs. al.,2005) indicating a lack of them in eaten Nectar in most succulents of Asclepiad- plant parts. On the other hand,some chemi- oideae is found in the guide rail and flows cals (like flavonol glycosides) in Apocyna- to the bottom of the nectar cavity(Meve and ceae plants act as oviposition stimulants for Liede,1994; Bruyns,2000a). Nectar cavities Danaus spp.,which means that recognition of C. acutangula are narrow,and nectar is not of host plants by these butterflies depends easily accessible. In this case, the presence on the unique chemistry of these plants of nectar may be detected by taste sensory (Haribal and Renwick,1998). Existence of organs on the fly’s labellae, maxillary palps the larvae on the flowers of C. acutangula, and tarsi. Touching of these organs, espe- not on any plant species in the same habitat, cially tarsi, with flowing nectar stimulates c o n fi r m t h e a b o v e m e n t i o n e d . the proboscis to extend and probe (Chap- Crab spiders (Thomisidae) are infre- man,1971; Daly et al.,1978; Vogel,1983). quently found on flowers (as compared with On searching for nectar in the nectar cavity, other visitors). This observation may be the fly must extend its proboscis in this nar- misleading, because these spiders hide in row chamber and probe cavity surfaces. This flowers (below petals), especially light co- behavior leads to attachment of pollinium lour species (Hawkeswood,2003). They sit Journal of Jazan University - Applied Sciences Branch Vol.1 No.1 December 2011 (Muharram1433 H) 73 Y.S.Masrahi

Fig. 3. A. Larva of Danaus chrysippus feeds on a flower of C. acutangula . B. Pupa on a stem of C. acutangula. C. The adult butterfly is shown minutes after it emerged from the pupa. D,E. Thomisidae spiders on the flowers (in E spider has caught and is feeding on Musca domestica). 74 Journal of Jazan University - Applied Sciences Branch Vol.1 No.1 December 2011 (Muharram 1433 H) Floral Biology and Visitors Behaviour

Fig.2. Percentage of sex in Diptera visiting to flowers ofC. acutangula motionless to wait for landing insects, and Handbook of Succulent Plants- Asclepiada- then seize them by strong front legs,bite and ceae”, Springer-Verlag,Berlin. inject a rapidly acting poison (Foelix,1996). Crab spiders represent most frequent am- Albre, J., Quilichini,A. and Gibernau,M., bush predators that sit on or near the flowers (2003), “Pollination ecology of Arum ita- (Dukas,2004). Crab spiders respond to the licum (Araceae)”, Bot. J. Linn. Soc., 141:205-214. floral signals in the same manner as polli- nators, including olfactory signals (Aldrich Aldrich, J. R. and Barros,T. M., (1995), and Barros,1995; Heiling et al.,2004). “Chemical attraction of male crab Flowers of C. acutangula represent three spiders(Araneae,Thomisidae) and klep- types of plant-visitors interactions : toparasitic flies(Diptera,Milichiidae, and 1-Seduction and deception of Diptera for Chloropidae)”, J. Arachnol., 23:212-214. pollination, 2-Predation of flowers (larvae of D. chrysip- Amendt, J., Krettek,R. and Zehner, R., pus), (2004), “Forensic entomology”, Naturwis- 3- Act as an attractive microhabitat to insect senschaften, 91:51-65. predators (Thomisidae spiders). Amoudi, M. A., (1997), “Diptera of Saudi These three types of interactions seem to Arabia.,Economic and Medical share in the same manner of visitors attrac- Importance.” Published by Author. tants: olfactory and chemical signals, and w e e m p h a s i z e t h a t f u r t h e r w o r k i s r e q u i r e d . Beaman, R.S., Decker,P. J. and Beaman, J. References: H., (1988), “Pollination of Rafflesia (Raffle- siaceae)”, Am. J. Bot., 75, 8:1148-1162. Albers, F. and Meve,U., (2002), “Illustrated Journal of Jazan University - Applied Sciences Branch Vol.1 No.1 December 2011 (Muharram1433 H) 75 Y.S.Masrahi Brackenbury, J., (1995), “Insects and Flow- dah region,western Saudi Arabia”, Fauna of ers, a biological partnership”, Blandford, Arabia, 21:339-350. London. Gilbert,M. G., (2003), “Carallu- Bruyns, P. V., (2000), “Phylogeny and Bio- ma” In:Hedberg,I., Edwards,S. and geography of Stapeliads, 1.Phylogeny”, Nemomissa,S.(eds.): Flora of Ethiopia and Plant Syst. Evol., 221:199-226. Eritrea. National herbarium, Addis Ababa University, 4, 1: 170-176. Bruyns, P. V., (2000), “Phylogeny and Bio- geography of Stapeliads. 2. Biogeography”, Haribal,M. and Renwick,J.A.A., (1998), Plant Syst. Evol., 221:227-244. “Identification and distribution of ovipisi- tion stimulants for monarch butterflies in Byrd, J. H. and Castner, J. L., (2001), “In- hosts and nonhosts”, J. Chem. Ecol., 24, sects of Forensic Importance” In:Byrd, J. H. 5:891-904. and Castner, J. L. (eds.): Forensic Entomol- ogy. CRC Press. Boca Raton,Florida, pp 43- Hawkeswood,T.J., (2003), “Spiders of Aus- 79. tralia”, Pensoft,Moscow.

Büttiker, W.;Attia,M.D. and Pont,A.C., Heiling,A.M., Cheng,K. and Herber- (1979), “Insects of Saudi Arabia. Diptera: stein, M.E., (2004), “Exploitation of flo- synanthropic flies”, Fauna of Saudi Arabia, ral signals by crab spiders(Thomisus 1:352-367. spectabilis,Thomisidae)”, Behav. Ecol., 15, 2:321-326. Chapman, R.F., (1971), “Insects: Structure and Function”, Edward Arnold, London. Jürgens,A. , Dotterl,S. and Meve,U., (2006), “The chemical nature of fetid floral odours Dafni, A., (1984), “Mimicry and decep- in Stapeliads (Apocynaceae-Asclepiadoide- tion in pollination”, Ann. Rev. Ecol. Syst., ae-Ceropegieae)”, New Phytol., 172, 3:452- 15:259-278. 468.

Daly,H.V., Doyen,J.T. and Ehrlich,P.R., Kevan, P. G. and Baker, H. G., (1983), “In- (1978), “Introduction to Insect Biology and sects as flower visitors and pollinators”, Diversity”, McGraw Hill Kogakusha ltd., Ann. Rev. Entomol., 28:407-453. Tokyo. Krenn, H. W., Plant, J. D. and Szucsich, N. Dukas,R., (2004), ”Effects of predation risk U., (2005), “Mouthparts of flower-visiting on pollinators and plants.” In:Chittka,L. and insects”, Arthropod Struc. Develop., 34:1- Thomson,J.D.(eds.): Cognitive Ecology of 40. Pollination. Cambridge University Press, Cambridge. pp 214-236. Kunze,H., (1991), “Structure and function in Asclepiad pollination”, Plant Syst. Evol., Foelix,R.F., (1996), “Biology of Spiders”. 176:227-253. Oxford University Press, New York. Larsen,T.B., (1984), “Butterflies of Saudi Fægri, K. and van der Pijl, L., (1979), “The Arabia and its Neighbours”, Transworld Principles of Pollination Ecology”, 3rd ed, Arabian Library and Stacey International, Pergamon Press, Oxford. London.

Gadallah,N.S. and Bosly,H.A., (2006), Liede, S. and Kunze, H., (1993), “A descrip- “Diptera associated with camels in the Jed- tive system for corona analysis in Ascle- 76 Journal of Jazan University - Applied Sciences Branch Vol.1 No.1 December 2011 (Muharram 1433 H) Floral Biology and Visitors Behaviour piadaceae and Periplocaceae”, Plant Syst. Encyclopedia of Physiology, Physiological Evol., 185:275-284. Plant Ecology III, vol. 12C . Springer-Ver- lag, Berlin, pp. 559-624. Masinde, P. S., (2004), “Trap-flower fly pollination in East African Ceropegia L. Zalucki,M. P. and Brower,L.P., (1992), (Apocynaceae)”, Int. J. Tropical Insect Sci., “Survival of first instar larvae of Danaus 24, 1:55-72. plexippus(Lepidoptera:Danainae)in rela- tion to cardiac glycoside and latex content Masrahi,Y.S., (2011), Illustrated guide to of ”, Chemoecology, the Wild Plants of Jazan. (in press). 3:81-93. Mebs,D., Reuss,E. and Schneider,M., (2005), “Studies on the cardenolide sequestration in African milkweed butterflies(Danaidae)”, Toxicon, 45:581-584.

Meve,U. and Liede,S., (1994), “Floral bi- ology and pollination in stapeliads – new results and a literature review.”, Pl. Syst. Evol.,192:99-116.

Müller,B. and Albers,F., (2002), “Caral- luma.” In: Albers,F. and Meve,U.(eds.): Il- lustrated Handbook of Succulent Plants, Asclepiadaceae, Springer-Verlag, Berlin, pp.46-63.

Rice, M. J., (1977), “Blowfly ovipositor re- ceptor neurone sensitive to monovalent cat- ion concentration” ,Nature , 268:747-749.

Sakai,S., (2002), “A review of brood-site pollination mutualism:plants providing breeding sites for their pollinators”. J. Plant Res., 115:161-168.

Taher,M.O., Faragalla,A.A., (1990), “A pic- torial key of some families of true spiders (Araneomorphae) recovered in the western region of Saudi Arabia”, J.K.A.U,Sci., 2:63- 78.

Taroda,N. and Gibbs.,P.E., (1982), “Floral biology and breeding system of Sterculia chichi St. Hil.(Sterculiaceae)”, New Phytol., 90:735-743.

Vogel, S., (1983), “Ecophysiology of Zoo- philic Pollination” In: Lange, O. L., Nobel, P. S., Osmond, C. B. and Ziegler, H. (eds.): Journal of Jazan University - Applied Sciences Branch Vol.1 No.1 December 2011 (Muharram1433 H) 77 Y.S.Masrahi بيولوجيا الأزهار و�سلوك الزائرات لنبات الغلفي يف منطقة جازان،جنوب غرب اململكة العربية ال�سعودية

يحيى �سليمان م�سرحي ، حنان �أبو القا�سم ُب�صلي ق�سم الأحياء ، كلية العلوم ، جامعة جازان

Q

يعترب نبات الغلفي �أحد �أكرث ع�صاريات حتت الف�صيلة الع�شارية ً تواجدايف منحدرات �سهول تهامة جازان،جنوب غرب اململكة العربية ال�سعودية. جتذب �أزهار النبات العديد من �أنواع الذباب، خ�صو�ص ًا �ضمن ف�صائل الذباب املنزيل،ذباب اللحم، والذباب املعدين. جلذب ّامللقحات ت�سلك الأزهار �سلوك اخلداع واملحاكاة لأماكن و�ضع البي�ض والغذاء؛ ولذا ف�إن �إناث الذباب هي �أكرث الزائرات ًترددا. ت�ؤثر املحاكاة التي تبديها الأزهار على �سلوك الذباب م�ؤدية �إىل الت�صاق الكتل اللقاحية بخرطوم احل�شرة ونقلها �إىل امل�ستقبل املي�سمي)ال�شق ّاملوجه(. من الزائرات الأخرى للأزهار الفرا�شات، وتتمثل بنوع وحيد هو فرا�شة منر ال�سهول؛ حيث تتغذى يرقاتها على الأزهار. بع�ض �أنواع العناكب)من ف�صيلة عناكب ال�سرطان( تنجذب �أي�ض ًا للأزهار؛ حيث تختبئ بني الأزهار لقتنا�ص الفرائ�س من الذباب الزائر. تلقي هذه الدرا�سة بع�ض ال�ضوء على العلقة املعقدة بني الأزهار وزائراتها يف البيئات اجلافة.

كلمات مفتاحية: نبات الغلفي - الأزهار - الذباب املنزيل - ذباب اللحم - الذباب املعدين - جازان - اململكة العربية ال�سعودية.

الربيد الإلكرتوين : ISSN: 6050-1658 [email protected]