Floral Biology and Visitors Behaviour of Caralluma Acutangula (Decne.) N.E.Br
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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 Caralluma 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 species of Asclepiadoideae(Apocynaceae) in the Tihama hill slopes of Jazan, Southwestern Saudi Arabia. The flowers of the plant 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 mimicry 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 (Danaus chrysippus – Nymphalidae) 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 genus 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 Asclepias, Calotropis, Reproduction success in higher plants and Ceropegia (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 shrubs. 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- Stapelia (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 pollen) 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.