Silk moths in Madagascar: Biology, uses and challenges related to




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Silk moths in Madagascar: Biology, uses and challenges related to Borocera cajani (Boisduval, 1833) (Lepidoptera – Lasiocampidae)

Abbreviated title: Silk moths in Madagascar



Tsiresy M. RAZAFIMANANTSOAI, Eric HAUBRUGEII, François J.VERHEGGENII

IDepartment of Animal Biology, Ecology and Conservation, Faculty of Sciences, BP 906, University of Antananarivo (Madagascar)

IIDepartment of Functional and Evolutionary Entomology, Gembloux Agro-Bio Tech, Liege University (Belgium)

Correspondence:

François J. Verheggen

Department of Functional and Evolutionary Entomology

Gembloux Agro-Bio Tech, Liege University

Passage des Déportés 2

5030 Gembloux (Belgique)

fverheggen@ulg.ac.be

081 62 22 80 (tel)

081 62 23 12 (fax)



ABSTRACT - Borocera cajani (Lepidoptera, Lasiocampidae), also named Landibe, is main wild silk moth currently used to produce silk textiles in Madagascar. Silk production involve many member of the local population, from the wild silk harvesters, to the spinners, traders, dyers, weavers and the artisans who transform the silk into clothing, accessories and decorative items. Uapaca bojeri (Tapia) forests are the last remnants of highland primary forest, which are threatened by human destruction through bush fires, firewood collection and charcoal production. Uapaca bojeri forest in the highland shelters wild Malagasy silkworms Borocera cajani and is the main host plant of this Lepidoptera species. Both this tree and Borocera cajani are endemic of Madagascar. Due to other-harvest of pupae and destruction of nature forest, wild silk production in those early sites has largely disappeared. Studing Borocera cajani’s biology and revitalize its silk constitute a way to conserve them. Key word: Borocera cajani, Landibe, silk, Uapaca bojeri, Madagascar, biodiversity

RÉSUMÉ - Borocera cajani (Lepidoptera, Lasiocampidae), également appelé Landibe, est le principal ver à soie sauvage actuellement utilisé pour produire la soie à Madagascar. La production de soie implique de nombreux membres de la population locale, les cueilleurs, les fileurs, les commerçants, les teinturiers, les tisserands et les artisans qui transforment la soie des vêtements, accessoires et objets décoratifs. Les forêts de Uapaca bojeri (Tapia) sont les derniers vestiges de forêt primaire des hauts plateaux, qui sont menacées par la destruction de l'Homme par les feux de brousse, la collecte de bois de chauffage et de production de charbon de bois. Ces forêts abritent les vers à soie sauvage Borocera cajani. Borocera cajani et sa plante hôte principale Uapaca bojeri sont endémiques de Madagascar. En raison de la récolte des pupes et de la destruction de la forêt, la production de soie sauvage a largement disparue. Étudier la biologie de Borocera cajani et revaloriser sa soie constituent des moyens de les conserver. Mots clefs : Borocera cajani, Landibe, soie, Uapaca bojeri, Madagascar, biodiversité

INTRODUCTION


Madagascar is one of the most important centers of world’s biodiversity with a high level of endemicity (around 90%) (Mittermeier et al., 2004) and many of its species are forest dwelling (Myers, 1998). This biodiversity affects all of the animal’s classes, including insects. Among these insects, moths are the most used in textile trades. Historically, Malagasy textile silk is not recent. Indeed, wild silk « landibe » was exploited before the introduced “Chinese silk”, exploited from another silk moth Bombyx mori during the 19th century (Rafidiarimala, 1974 ; Costa, 2004). Wild silk in Madagascar has many origins, and can be exploited from various moth species, the mostly known and used is Borocera cajani (ONU, 1991). The Malagasy population used Borocera cajani silk to make sumptuous shroud. This way f producing silk has persisted during the last fifty years until a gradual disappearance for this species (Paulian, 1953).

BIOLOGY


  1. Taxonomy

The genus Borocera was originally described by Boisduval (1833) and the species cajani by Vinson (1863). It has been confused with Borocera madagascariensis which often resides in the coastal part of the Island but can also be found in other places of Madagascar. Borocera cajani is a silk moth belonging to the Lasiocampidae family and the Gonometinae subfamily. This subfamily is endemic of Madagascar, and contains most of the Lasiocampidae species of this island (De Lajonquière, 1972 ; ONU, 1991). It is characterized by the vein 8 of the hindwings which is connected with the vein 7 only far or very far from its base, and then forms a secondary cell with a length nearly equal by to top of the median cell, both cells also having about the same width (Aurivillus, 1927).


  1. Morphology

The genus Borocera gathers all moths with fasciculate antennae which are uneven in the first third part from the base. They have a small head, proboscis missing and small eyes slightly prominent. Borocera cajani is the most widespread in Madagascar and without doubt one of the most abundant. It has many forms and landraces.

Both sexes show a very high dimorphism in size and color. But the genitalia remains constant whatever the origin of species examined (De Lajonquière, 1972). Borocera cajani is generally a large moth and the female presents a size about the triple of the male (De Lanjonquière, 1972). The wing is generally fuzzy dark for the male and grey uniform for the female (Paulian, 1950 ; Razafindraleva, 2001).

Males are smallish, hairy and thick-bodied moths. Their antennae are well-developed and are bipectinate with a blackish flagellum and dark yellow fasciculation. Their head, thorax and legs have the same color than that of forewing, but the abdomen is slightly lighter. Wingspan is about 38 – 52 mm (De Lanjonquière, 1972). Forewings are oblong, well developed in width, apex slightly sinuous or round. Their color is red ochracea to brown with predominantly brown mahogany tone, showing a sinuate submarginal line, a postmedial transverse line and a stigma grayish point in the discal cell (Paulian, 1951) and a little darker sooty fringe. Forwings’ form varies for one egg-laying (Paulian, 1953). Hindwings colour is quite similar to the forewings though often overshadowed in part or in whole. Cilia are clearer white. Dorsal wings are as in the front sometimes barred transversely by an apparent median reddish shadow, sometimes obsolete, but rather with the proximal part of wing darker (De Lanjonquière, 1972 ; Razafindraleva, 2001). The genitalia are formed by a membrane which leads to a thicker penis and serrated edges. The penis is crossed by a prominent ejaculatory duct. Two valves are located on both sides of the penis (De Lanjonquière, 1972 ; Razafindraleva, 2001).

Females are much larger. Their wingspan is about 70 - 75mm, with forewing length of 35mm. Antennal shaft is black with yellow pectination. These moths are hairy with thick bodied, grayish yellow tinted, bears thorax and legs of the same color as the forewings. Hairy legs are terminated by tarsi black. Abdomen is lighter than the thorax. Wings are dirty white to pale grey, silky and shiny (De Lanjonquière 1972 ; Razafindraleva, 2001). Forewings are crossed by two transverse lines that spilt the wing in different spaces (Razafindraleva, 2001). The sooty discal area is defined proximally by the apparent brownish sub-basal line and the sinuous postmedial line. There is a dark lunule dot at the end of the cell. The submarginal line is formed by a row of diffuse inter-nervurals chevron patches. The cilia are sooty. Hindwings color is as in the forewing, with cilia clearer. The back of the 4 wings is yellowish sepia consistent with very less apparent median gray shadows. The apex of the abdomen is characterizes by two well developed thick ridges with sensory hairs. The genital opening is formed by the superposition of two beads. This structure ensures coaptation during mating and ovoposition.


  1. Life cycle and habitat

Borocera cajani is bivoltine; it has two generations per year (Paulian 1953 ; Razafindraleva, 2001 ; Razafimanantsoa, 2008). The first generation, where eggs hatched in January (Razafimanantsoa, 2008), February and March (Razafindraleva, 2001) is obtained during the rainy season. The second generation is the population that comes from of the eggs having hatched in the end of April until November (Razafindraleva, 2001 ; Razafimanantsoa, 2008).

The life cycle of the moth silk includes four stages: egg, caterpillar or larva, chrysalis or pupa, and adult. After their emergence, females attract males by releasing a sexual pheromone. This chemical is carried on a plume downwind rather than disseminated in all directions. Males use their antennae to detect the pheromone and can orientate toward females location (Zborowski et al., 2007). For both sexes, the higher emergence hour is situated between 2 and 6 pm. Mating is observed between 1 and 7 pm. Then, it may take one hour without repetition. One male can mate with up to 3 females. The adult does not feed. Egg laying is done from 7 pm, at the same day of female emergence and mating. Unfertile female can lay eggs but they could not hatch. The number of eggs laid varies from 250 to 845 and are placed on graminaceae, on leaf or on the branch and the trunk surface (Razafimanantsoa, 2008). Females lay eggs in captivity even without their necessary host plant.


Borocera cajani eggs is fairly hemispherical, had a hard shell and a granular texture. The porcelain-like eggs are ornate by a grey greenish band. Their size is about 2 mm. The most fertile eggs hatched after about 10 days with a hatching rate of about 89%. Few remain as eggs in the following 4 days. No parthenogenetic character has been observed in Borocera cajani.
The higher mortality rate is observed in the first instar larvae (Paulian, 1953). In this stage, larvae disperse themselves by dropping from twigs on long silken thread (Piney, 1975) which can lead them on a wrong plant food. First instar larvae cannot survive a four days starvation (Paulian, 1953). Caterpillars, as they develop through four stages, change in size and shape. Second instar larvae begin to have four spiny bouquets which is a specific character for the genus Borocera. The spiny bouquets develop progressively between all larval stages. When alarmed, they expose four “pom – pom like” spiny bouquets, red in the base and black on the top. But some larvae show only the blackish bristle. Fifth instar caterpillar is very hairy in the lateral face and quiete long: over 12 mm long (Grangeon, 1906 ; Razafimanantsoa, 2008 ; Rakotoniaina, 2009). In nature, they are remarkably well camouflaged to mimic bark of their plant food. The color is grey – blue.
After about 12 days, a larva migrates for making a cocoon. Cocoon is grayish oval cocoon and projecting urticant hairs on it. The cocoon size is about 5 mm in length for the females, and about 2.5 mm in diameter. It is much smaller in males. It has 3 layers and weights 300 – 400 mg for the female; 90 – 200 mg for the male. Prepupa lasts for 3 to 5 days (Grangeon, 1906 ; Razafimanantsoa, 2008).
As many moth species, Borocera cajani is preyed by many predators and diseases and is attacked at any stage (Zborowski et al., 2007). Bird predators are Acridithores tristis, Cuculus rochii, Centropus toulou, Corvus alba, Hypsipetes madagascariensis). But other predators exist with e.g. bats, reptiles (Furcifer lateralis), praying mantises, ants, and spiders. The most destructive of all are the parasites, which are mostly wasps (Ichneumonidae: Pimpla, Xanthopimpla hova, Brachymeria borocera, Ophion sp, Braconidae: Apanteles borocerae and decaryi, Tachinidae: Synthesiomyia nudiseta) that attack larvae but may emerge in a subsequent stage (Grangeon, 1906 ; Grangeon, 1907 ; Paulian, 1953 ; Razafindraleva, 2001 ; Razafimanantsoa, 2008). There is also a wide range of fungal, bacterial and viral diseases as “pebrine, muscardine and flasherie” (Grangeon, 1907).
Borocera cajani spend 47 to 179 days (Razafindraleva, 2001 ; Razafimanantsoa, 2008) in order to complete its cycle life (Figure 1). So it needs almost more than one and half months to assure their successive generations. The major difference observed in days to pupal stage is due to diapauses during the dry season.

The species colonizes the Uapaca bojeri woodlands which are found in the central highland zones and the southwestern of Madagascar as Imamo, Itremo and Isalo zones (Gade, 1985). It is a human modified vegetation formation. They are found in small cluster around the central highland (Kull, 2003). The “Tapia” forest constitutes one of the natural formation forests more or less reduced in one species, Uapaca bojeri (Rakotoarivelo, 1993). This plant is one of the Borocera cajani’s plant foods. But silk moth is very polyphagious so it can be found in many habitats of the island as Diego Suerez, Montagne d’Ambre, Nosy Be, Anjozorobe, Analavory, Ankazobe region, Antananarivo, Manjakatompo, Ankarana’s massif, Ambohimahasoa, Andringitra's massif, Bekily, Majunga, Ankarafantsika's Region, Antsingy, Antsalova region, Morondava (De Lanjonquière, 1972). They feed also on Psydium guyava, Psidium cattleyanum, Aphloia theaformis, Dodonea madagascariensis, Cajanus indicus, Harungana madagascariensis, Acacia dealbata, Schefflera sp, Eucalyptus sp, Tamarindus indica, Avicennia officinali, Salís babylonica, Terminalia catappa, (Paulian, 1953 ; De Lanjoquière, 1972 ; Razafindraleva, 2001 ; Rakotoarivelo, 1993 ; Razafimanantsoa, 2008 ; Rakotoniaina, 2009).

The herbaceae stratum in the Uapaca woodland has an important role in the life cycle of Borocera cajani. It serves a place for nidificate the chrysalis especially in the dry season (Razafimanantsoa, 2008).

IMPORTANCE


The Gonometinae species are currently used for wild silk production in Madagascar, and in most cases the silk is spun by Borocera cajani (De Lanjonquière, 1972). The size of the harvest varies greatly from one year to the next, with averages reaching 10t to 30t for the whole island (Gade, 1985). Wild silk production is one important income for the adjacent communities (Kull, 2003). It provides alternative incomes to the poorest and most disadvantaged of the human population especially during the “lean period” (Kull, 2005 ; Ny Tanintsika, 2010). Villagers painstakingly gather cocoons and sell them. The chrysalis is removed and eaten; the empty cocoons are cooked, spun and woven into silk fabrics (Kull, 2003). 34% of households in Ambohimanjaka and 65% of household in Ilaka earn cash incomes from the harvest of Borocera cajani cocoons (Kull, 1998 ; Randriamboavonjy, 2000 ; Kull 2002). The larger rainy season silk harvest provides crucial cash income during the meager months before the rice harvest. Collecting Borocera cocoons, processing them, unraveling the filaments to spin into thread, and weaving that into a silk have been part-time activities of highland rice growing peasants for several hundred years (Gade, 1985).

Silk production involves many actors of the population, from the wild silk harvesters, to the spinners, dyers, weavers and artisans who transform the silk into clothing, accessories and decorative items (Ny Tanintsika, 2010). Borocera silk moths are the preferred delicacy. Beside animal protein, insects provide occasional variation of texture and taste to the daily regime which is heavy in primarily rice and manioc (Decary, 1937 ; Gade, 1985 ; Guigo, 1989 ; Kull, 2005). Borocera cajani silk processing, to produce ritual burial shrouds and for clothing item throughout the highlands, is part of the area’s culture. The Landibe shroud is inescapable for any respected dead person. To be wrapped by many “Lambamena” (red silk shroud) is a honor supreme sign according the Malagasy adage: “Izay sahy maty mifono lambamena” (The intrepid front the death wears one Landibe shroud). Indeed, wild silk is precious for this secular usage in ways and customs (Rakotoniaina, 2009). The stuff produced from the Borocera cajani cocoons is very remarkable by its glow, its tenacity, its elasticity and its solidity (Ch. Coquerel, 1854 ; Guigou, 1989) and silk stay the textile’s queen in the world (Krishnaswami, 1974).


PROBLEMS


We estimate that between 150,000 and 200,000 ha of the island forest is lost per year (Minten et al., 2003). As many species in Madagascar, Borocera cajani is critically endangered by the destruction of their native forest (Razafimanantsoa et al., 2006). It becomes to be rare. In 1933, the Uapaca bojeri forest in the West of Arivonimamo was important enough to allow in this locality cocoon collection. But after twenty years, it became a very clear forest (Paulian, 1953). The Imamo woodland has ceased to produce Landibe since 1960s (Razafintsalama et al., 1999 ; Kull 2003 ; Kull et al., 2005). The Isalo and Itremo zones remain the producing center of the wild silk in Madagascar (Paulian, 1953). In the island, the wild silk production becomes very low when the croissant request of the market exerts an important pressure on the population remaining. In the Itremo zone west of Ambatofinandrahana, cocoons are abundant in cycles of one year out of five. The sparse cocoon populations are not worth the harvest effort (Gade, 1985). This fact is caused by:

- the destruction of its habitat; the way that cocoon harvester gathers the cocoons in the forest, they break many branches (Grangeon, 1904)

- the proliferation of introduced species such as "Pinus sp": which harms the native plant with its heliophile characteristic, grows quickly and in addition, it can change the microhabitats including the soil quality so put at a disadvantage the Uapaca bojeri (Kull et al., 2005),

- and by the bush fire which kills Borocera cajani (Paulian, 1953). Even if the trees tolerate fire, repeated fires destroy shrubs (niche of Borocera cajani too) and kill the generation because ground fires also kill the Uapaca bojeri seedling and sprouts (Grangeon, 1910 ; Pierrier de la Bathie, 1921 ; Vigmal, 1963; Guigou, 1989 ; Gade, 1996 ; Kull, 2005).

The over harvesting of the pupae accompanied by the natural fluctuation of the insect’s population threaten the species (Paulian 1953, Kull 2005, Razafimanantsoa et al, 2006, Razafimanantsoa 2008).

In addition to human pressure, parasites, predators and the abundance of other Lepidoptera feeding and defoliate the “Tapia” leaves as Maltagorea fusicolor, Latoia albifrons, Parasa sp are also the cause of the decrease of the Landibe’s population (Grangeon, 1907).

The native silk manufacture becomes to be demise because of the non modernization of the manual process, and place the Landibe burial shroud as major expenditure. The domesticated Chinese silkworm Bombyx mori is produced with cheap labor and has an esthetically superior fabric for export, a market with which Borocera cajani could not compete (Rafidiarimalala, 1974 ; Gade 1985). Moreover, Borocera cajani produce less silk than Bombyx mori (Krishnaswami, 1974).

Management methods including GELOSE: “Gestion locale Sécurisée” (secure local management) and GCF: “Gestion Contractualisée des Forêts” (contractual management of forests) are now entrusted to local communities for large parts of the Tapia forest. Based local communities legally constituted are composed of residents of a hamlet, village or a group of villages. It groups volunteer peoples united by common interests and obeying the rules of common life, and become the natural resource management associations (GELOSE, 1999 ; Robsomanitrandrasana, 2008). They have a role to ensure through self - sustainable management of natural resources present on their territory including forest and fauna like silkworm (Razafindrakoto, 2005 ; Robsomanitrandrasana, 2008). Currently, due to community management, conservation and recovery of the forest proved a successful transfer of good management, charcoal production has stopped (Consortium RESOLVE - PCP - IRD, Final Report, inventory, 2005; Robsomanitrandrasana, 2008). But some villagers do not wish to join the association (based local community) to escape the rules to follow.

CONCLUSION and recommendations


Although sericulture still plays a minor role in Madagascar in the international level (Krishnaswami, 1974), it remains a considerable income source for local people who depend on it. Silk industry revitalization could be a factor to conserve Borocera cajani. The human pressures on Borocera cajani and its habitat have decreased when applying the method of management by local communities. But it remains to convince people who do not wish to join the associations, so everyone has the same conviction.

A comprehensive study on the biology and ecology of the insect and its habitat is necessary for its management. The permanent cessation of bush fires practice and logging, the reforestation of Uapaca bojeri and elimination of the introduced plants (Pinus) inside the Tapia forest are very important actions in the context of Borocera cajani s habitat maintaining (ONU, 1991 ; Razafimanantsoa, 2008). Restrictions on the way to collect cocoons avoiding breaking branches and time of cocoon’s gathering dates to ensure the next generation should be established.


A test breeding in the wild to repopulate “Landibe” and to have a good production is recommended by mastering the various enemies of this moth (Guigo, 1989). Environmental educations to the children in the region, where Borocera cajani are abundant, are also helpful. Then, they can understand the importance of Borocera Cajani as an endemic species of Madagascar, source of silk and protein, as well as its conservation.
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Figure 1: Borocera cajani life cycle in insectarium (Ambohimanjaka, 2006)

Figure 1: Cycle de vie de Borocera cajani élevé en insectarium (Ambohimanjaka, 2006)







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