PISCIOTTA, Silvestro

SAJEVA, Maurizio

ZITO, Pietro

Archivio istituzionale della ricerca - Università di Palermo

Naturalista sicil., S. IV, XXXII (1-2), 2008, pp. 241-251SILVESTRO PISCIOTTA, PIETRO ZITO & MAURIZIO SAJEVADANAUS CHRYSIPPUS (LINNAEUS, 1758) (Lepidoptera Nymphalidae)LARVAE FEEDING ON CARALLUMA EUROPAEA (GUSS.)N.E.BR. (Asclepiadaceae) IN LAMPEDUSA ISLANDSUMMARYDanaus chrysippus (L.) is a wide-ranging migrant species; it has considerably increased andextended its range in the North African coastal regions in the past two decades, and from there hascolonised parts of the south coast of Spain, Corsica, Sardinia, Italy, Malta and Greece. Although itis a polyphagous species its larvae feed on plants which contain cardenolides, expecially Asclepi-adaceae, Apocynaceae and Moraceae. In this paper we report on a population found in LampedusaIsland which larvae feed on Caralluma europaea (Guss.) N.E.Br. (Asclepiadaceae).Observations were carried out from April 2006 to November 2007, during a multi-yearresearch project on the ecology of C. europaea in Lampedusa. The larvae of the population found inLampedusa Island feed on Caralluma europaea (Guss.) N.E.Br. (Asclepiadaceae). Larvae and eggshave been collected to observe development and feeding preferences under controlled conditions.The strict relation between Danaus chrysippus and Asclepiadaceae is confirmed and a strong prefer-ence for the follicles versus stems has been observed.RIASSUNTOLarve di Danaus chrysippus (Linnaeus, 1758) (Lepidoptera Nymphalidae) fitofaghe di Carallu-ma europaea (Guss.) N.E.Br. (Asclepiadaceae) nell’isola di Lampedusa. Danaus chrysippus (L.) è unaspecie ad ampio raggio di migrazione che nell’ultimo ventennio ha notevolmente aumentato la suadistribuzione. Dalle coste nordafricane ha colonizzato parte del sud della Spagna, la Corsica, la Sar-degna, l’Italia, Malta e la Grecia. È una specie polifaga, ma le sue larve si nutrono di piante che con-tengono cardenolidi, specialmente delle famiglie Aclepiadaceae, Apocynaceae e Moraceae. In que-sta nota gli autori riportano dati su una popolazione ritrovata nell’Isola di Lampedusa le cui larve sinutrono di Caralluma europaea (Guss.) N.E.Br. (Asclepiadaceae). Le osservazioni sono state con-dotte da aprile 2006 a novembre 2007, nell’ambito di un progetto di ricerca pluriennale sull’ecolo-gia di C. europaea a Lampedusa. Le larve e le uova di D. chrysippus sono state prelevate ed allevatein condizioni controllate per osservare lo sviluppo e le abitudini alimentari. La stretta relazione traDanaus chrysippus e le Asclepiadaceae è confermata dai nostri dati, che mostrano una spiccata pre-ferenza delle larve nei confronti dei follicoli rispetto ai fusti.INTRODUCTIONDanaus chrysippus is a wide-ranging migrant species belonging toDanainae, a subfamily of Nymphalidae, tropical butterflies with a complexpheromone biology (FRANCKE, 1989). D. chrysippus distribution rangesfrom Africa to southern Europe (Canary Islands, coastal Mediterraneanregions, Turkey), Saudi Arabia, tropical Asia; it is present in Australia andNew Zealand too. D. chrysippus is polyvoltine and prefers bushy, rockyplaces, and coastal gullies, usually near gardens and cultivated areas(PERKOVIC´, 2006).Warming trends at lower latitudes seem to be associated with move-ments of tropical species into more-temperate areas. In the past two decadesD. chrysippus has considerably increased and extended its range in the NorthAfrican coastal regions, and from there has colonised parts of the south coastof Spain, Corsica, Sardinia, Sicily, Italy, Malta and Greece (BURTON, 2001).The first European population established in southern Spain in 1980 and bythe 1990s had established multiple, large metapopulations (PARMESAN, 2006).The first record for D. chrysippus in Sicily dates back to 1983 (GATTO, 1985).The biology of this species is influenced by the availability of larval food-plants. Altough it is polyphagous, its larvae feed on plants which contain car-denolides, expecially Asclepiadaceae, Apocynaceae and Moraceae (ACKERY& VANE-WRIGHT, 1984). In this paper we report on a population found inLampedusa Island which larvae feed on Caralluma europaea (Guss.) N.E.Br.(Asclepiadaceae).NOTES ON THE STUDIED SPECIESDanaus chrysippus (Linnaeus 1758) (Nymphalidae).D. chrysippus adults reach a wingspan of 58 mm, the ground colour ofthe fore-wing and the hind-wing upper- side is light orange- brown to chest-nut brown, while fore-wing upper-side apex is dark brown with transversewhite spots (Fig. 1) (PERKOVIC´, 2006).The male scent-producing organs consist of abdominal hairbrushes andalar- or patch-like glands. Males and females are known to accumulatepyrrolizidine alkaloids from plants. The males metabolize these in parts to242 S. PISCIOTTA, P. ZITO & M. SAJEVAvolatile dihydropyrrolizines, some of which may play a specific role incourtship behaviour (FRANCKE, 1989).The caterpillar has five larval instars and is about 5 cm long just beforepupating. It has black and yellow bands and three pairs of fleshy filaments,one pair, the longest, just behind the head, the second near the start of theabdomen and the third near the end of the abdomen. The base of the fila-ments is red, and they function as sense organs. Caterpillars accumulate poi-sonous chemicals from the plants they feed on and are unpalatable to preda-tors. Their striking habitus therefore is a form of warning aposematiccoloration (Fig. 2) (BRANDES, 2005).The pupae are pale green with golden spots and hang head down froma silken pad (Fig. 3). The eggs are silvery white, shiny, bullet-shaped with anapical point and ribbed sides (Fig. 4). The shell is lined with a layer of wax,which helps keep the egg from drying out.Caralluma europaea (Guss.) N.E.Br. (Asclepiadaceae)C. europaea is a stem- succulent plant belonging to the family Asclepi-adaceae. Some authors suggest that Aclepiadaceae should be merged intoApocynaceae (SENNBLAD, 1996; OLMSTEAD et al., 1993). Even so most papers243Danaus chrysippus (Linnaeus, 1758) (Lepidoptera Nymphalidae)...Fig. 1 — Specimen of Danaus chrysippus from pupa reared in laboratory (Photo: P. Zito).244 S. PISCIOTTA, P. ZITO & M. SAJEVAFig. 2 — Larva of D. chrysippus feeding on stem of C. europaea under laboratory condition (Photo:P. Zito).dealing with the ecology and taxonomy of the family (e.g. ALBERS & MEVE,2002) still recognise and use Asclepiadaceae as a valid family. In this paperAsclepiadaceae are being treated as a family, in accordance with ALBERS &MEVE (2002), and OLLERTON (2003). C. europaea has quadrangular stems, theyounger ones are green and have small leaves that soon wither while the old-Fig. 3 — Pupa of D. chrysippus fromeggs collected in Lampedusa and rearedin laboratory (Photo: P. Zito).245Danaus chrysippus (Linnaeus, 1758) (Lepidoptera Nymphalidae)...Fig. 4 — Egg of D. chrysippuson the follicle of C. europaeaphotographed in the field(Photo: P. Zito).Fig. 5 — Flowers of C.europaea (Photo: P. Zito).est ones look greyish. It forms large clumps up to 15-20 cm in diameter. Flow-ers are red-brown with yellow stripes or streaks, 10-15 mm in diameter. Thecorona is normally purplish (Fig. 5) (SAJEVA & COSTANZO, 1994). Fruits arefollicles that at maturity dry out. Plants growing in rock crevices usually havea central erect stem and many smaller ones more or less procumbent, whilethose growing under bushes grow more chaotically (SAJEVA, 1984). The tax-onomy of C. europaea has been changed by several authors, as it often hap-pens in succulent plants groups; according to WHITE & SLOANE (1937) thespecies includes 5 varieties (var. marmaricensis, var. simonis, var. maroccana,var. affinis, and var. confusa), while more recently MEVE & HENEIDAK (2005)use the binomial Apteranthes europaea (Guss.) Plowes and recognize twovarieties (var. europaea and var. judaica).MATERIALS AND METHODSObservations were done during a multi-year research project on theecology of C. europaea in Lampedusa started in April 2006. Information inthe present paper is updated to November 2007. Lampedusa lies in theMediterranean sea and the studied sites are Isola dei Conigli, Albero Sole,Capo Grecale, Cala Galera (Fig. 6).246 S. PISCIOTTA, P. ZITO & M. SAJEVAFig. 6 — Map of the Mediterranean sea, showing the position of Lampedusa. The inset map of theisland shows the highest point (133 m) on the north coast and the localities where observations werecarried out.From May to September 2007 we found adults of D. chrysippus along thewhole island with Isola dei Conigli being the area with highest abundance. Lar-vae and eggs were present during May and June 2007 only at Albero Sole andIsola dei Conigli. Larvae were feeding on C. europaea which grows well cam-ouflaged in rock crevices or among Thymus capitatus (L.) Hoffmanns et Linkbushes (Fig. 7). We did not find pupae on C. europaea nor on any other plants.Five larvae and five eggs have been collected monthly to observe thefeeding behaviour. Eggs and larvae were reared in plastic boxes placed in athermostated room at 25 ± 2 °C illuminated with 100 µmol m–2 flux and aphotoperiod of 16/8 light/dark hours. To study food preference, as source offood they were supplied with stems, follicles or stem with follicles of C.europaea collected in Lampedusa and cultivated at the Botanical Garden ofPalermo. The process of complete metamorphosis of D. chrysippus has beenobserved in controlled conditions. After the emergence, the adults weremounted and stored in entomological boxes at the Dipartimento di ScienzeBotaniche.247Danaus chrysippus (Linnaeus, 1758) (Lepidoptera Nymphalidae)...Fig. 7 — C. europaea and T. capitatus in Lampedusa Island (Photo: P. Zito).RESULTS AND DISCUSSIONSince 1988, a remarkable increase in the distribution range of the D.chrysippus has occurred in Italy. It has been recorded in the whole Sicily, Cam-pania, Lampedusa, Sardinia, Isole Ponziane, and also in Emilia-Romagna andLiguria, the northernmost sightings in Europe (BORGO et al., 1992). The dif-fusion of the species was linked with the warm conditions occurred from1986-1990 (PERKOVIC´, 2006).Between 1988 and 1991 D. chrysippus has been found along the north-ern coast of Sicily, from Terrasini to the mouth of Imera river, in the south-western coast from Mazara del Vallo to Torre Salsa and in the eastern coastnear Aci S. Antonio, the mouth of Simeto river and Siracusa (ARNONE &ROMANO, 1991). The presence of adults of D. chrysippus in Lampedusa hasbeen reported for the first time on June 1988 in the area of vallone Imbriaco-la, and after that on April and July 1990 (ROMANO & ROMANO, 1995).In the studied period C. europaeawas the only food source for the larvae ofD. chrysippus. During the field observations the eggs have been found only on thesuture line of the follicle. The female perches on the follicles and, curling itsabdomen around the edge, lays an egg on the follicle. D. chrysippus usually laystheir eggs singly (ACKERY & VANE-WRIGHT, 1984). Eggs hatch about four daysafter laying.Each follicle hosted 1 to 6 eggs andon eachplant amaximumof threelarvae have been counted. Larvae were feeding primarly on follicles, and usedstems only after complete consumption of the follicles of the host plant (Fig. 8).Under our controlled conditions in the presence of stems with folliclesthe larvae fed on follicles first and ate the stems only when follicles were nomore available.The entire larval stage lasts from nine to fourteen days. In our conditionsthe time from laying to eclosion is 2-4 days. Larvae fed for about 10 days andreached a length of about 5 cm, in ten days growing from 4.5 to 50 mm. Onreachingmaturity, the caterpillars left the foodplants to search for suitable pupa-tion sites. Under laboratory condition the larvae silked a pad of silk and clingedhead downwards by means of the anal claspers on the lid of the boxes (Fig. 3).The pupal development period depends on conditions of light, temperature andhumidity (ACKERY & VANE WRIGHT, 1984); in our condition it took 8-10 days.Butterflies of the subfamily Danainae become unpalatable to predatorswhen their larvae feed on plant species containing cardiac glycosides (cardeno-lides) (MEBS et al., 2005). Danainae biological cycle is linked mainly to Asclepi-adaceae, Apocinaceae and Moraceae (ACKERY & VANE-WRIGHT, 1984).The larvae of D. chrysippus feed mainly on Asclepiadaceae, from whichthey store cardenolides. Other families involved, according to VANE-WRIGHT &DE JONG, (2003) are: Convolvulaceae, Euphorbiaceae, Sapindaceae, and248 S. PISCIOTTA, P. ZITO & M. SAJEVAPlumbaginaceae. Among Asclepiadaceae the following taxa have been report-ed as host plants for larvae of D. chrysippus: Asclepias, Aspidoglossum, Brachys-telma, Calotropis, Caralluma, Ceropegia, Cynanchum, Gomphocarpus, Huernia,Ischnostemma, Kanahia, Leichardtia, Leptadenia,Marsdenia,Metaplexis, Pachy-carpus, Pentarrhinum, Pentatropis, Pergularia, Periploca, Pleurostelma, Raphis-temma, Rhyncharrhena, Sarcostemma, Schizoglossum, Secamone, Stapelia, Stath-mostelma, Tylophora (ACKERY & VANE-WRIGHT, 1984; VANE-WRIGHT & DEJONG, 2003). Within the genus Caralluma, only C. burchardii (BRANDES, 2005)has been recorded at specific level as forage plant forD. chrysippus. Our recordis the first for the species C. europaea as fodder for D. chrysippus.The genus Periploca has been described as foodplant for D. chrysippus(VANE-WRIGHT & DE JONG, 2003) and it is represented in Lampedusa byPeriploca angustifolia. It is interesting to note that no larvae have been foundfeeding on it. This may be related to the different phenology of the two Ascle-apiadaceae species. According to PIGNATTI (1982) C. europaea blooms and setsfruits between April and July, while P. angustifolia blooms and set fruits betweenNovember and March. During our field researchC. europaea had the maximumfruit production in April and May, while P. angustifolia had follicles in Februaryand March. We found eggs and larvae in C. europaea only when follicles were249Danaus chrysippus (Linnaeus, 1758) (Lepidoptera Nymphalidae)...Fig. 8 — Caterpillars of D. chrysippus feeding on follicles of C. europaea. (Photo taken in labora-tory: P. Zito).present, that is from May to June 2007 (Tab. 1). It is possible that the first gen-eration ofD. chrysippus arrives from Africa helped by the strong winds from thesouth-east quadrant which are prevailing in April (data kindly supplied byENEA). On its arrival it lays eggs on the follicles present, those of C. europaea atthat time. Larvae feed on follicles and stems. At the end of pupate period there250 S. PISCIOTTA, P. ZITO & M. SAJEVATable 1Presence (•) of follicles of Caralluma europaea, of Periploca angustifolia,of adults and larvae of Danaus chrysippus in Lampeusa island during the observation period.All the larvae found were feeding on follicles of C. europaea.Year 2006 2007Month A M G L A S O N D G F M A M G L A S O NFolliclesC. europaea • • • • • • • •FolliclesP. angustifolia • • •LarvaeD. chrysippus • •AdultsD. chrysippus • • • • •is the emergence of second generation, and new eggs are laid on follicles. In thisway it seems that the biological cycle of D. chrysippus in Lampedusa is strictlylinked to C. europaea. From our observation and available data it seems that D.chrysippus is present in Lampedusa only as a migrant species; in fact its presenceis not constant through the years. Our data give a strong confirm to the relationbetween Danainae and Asclepiadaceae and increase the number of knownspecies on whichD. chrysippus larvae feed. P. angustifolia could be an alternativefood source in the event of a early migration of Danaus in Lampedusa.Acknowledgements. — We would like to thank the Director Giusi Nicolini and the staff of Ri-serva Naturale Orientata Isola di Lampedusa for the assistance and the logistic support. We alsothank Alcide Di Sarra of ENEA for kindly providing meteorological data on Lampedusa. Theresearch was supported by funding from Università di Palermo (Fondi di Ateneo)REFERENCESACKERY R.I. & VANE-WRIGHT R.I., 1984 — Milkweed butterflies, their cladistics and biology. —British Museum (Natural History), London.ALBERS F. & MEVE U., 2002 — Illustrated Handbook of Succulent Plants: Asclepiadaceae. —Springer-Verlag, Berlin, Heidelberg.ARNONE M. & ROMANO M., 1991 — Nuovi reperti di Danaus chrysippus (Linnaeus, 1758) in Sicilia(Lepidoptera Danaidae). — Naturalista sicil., 15: 161-166.BRANDES D., 2005 — Calotropis procera on Fuerteventura. — Technical University Braunschweig,Germany, pp. 7. http://www.biblio.tu-bs.de/geobot/fuerte.htm.BORGO E., CASSULO L., RAINIERI V. & ZILLI A., 1992 — On the expansion ofDanaus chrysippus (Lin-naeus, 1758) during the last decade in Italy. — Atalanta, 23: 407-410.BRUYNS P.V., 1987 — Miscellaneous notes on Stapelia (Asclepiadaceae). — Bradleya, 5: 77-90.BURTON J.F., 2003 — The apparent influence of climatic change on recent changes of range by Euro-pean insects (Lepidoptera, Orthoptera). — Proc. 13th Int. Coll. EIS, 13-21.COMPTON S. G., 1987 — Aganais speciosa and Danaus chrysippus (Lepidoptera) sabotage the latexdefences of their host plants. — Ecological Entomology, 12: 115-118.FRANCKE W., 1989 — Terpenoids from bark beetles, solitary bees and danaine butterflies. — Pureappl. Chem., 61: 539-542.GATTO A., 1985 — Ripresa di Danaus chrysippus L. in quel di Palermo (Sicilia) (Lepidoptera,Danaidae). — Giorn. ital. Ent., Cremona, 2: 369-370.MEBS D., REUSS E. & SCHNEIDER M., 2005 — Studies on the cardenolide sequestration in Africanmilkweed butterflies (Danaidae). — Toxicon, 45: 581-584MEVE U. & HENEIDAK S., 2005 — A morphological, karyological and chemical study of the Apter-anthes (Caralluma) europaea complex. — Biol. J. Linn. Soc., 149: 419-432.OLMSTEAD R.G., BREMER B., SCOTT K.M. & PALMER J.D., 1993 — A parsimony analysis of theAsteridae sunsu lato based on rbcL sequences. — Ann. Missouri Botan. Garden, 80:700-722.PARMESAN C., 2006 — Ecological and Evolutionary Responses to Recent Climate Change. — Annu.Rev. Ecol. Evol. Syst., 37: 637-669.PERKOVI D., 2006 — Danaus chrysippus (Linnaeus, 1758) (Lepidoptera, Nymphalidae, Danainae),a new species in the fauna of Croatia. —Nat. Croat. Zagreb., 15: 61-64.PIGNATTI S., 1982 — Flora d’Italia. — EdAgricole, Bologna.ROMANO F.P. & ROMANO M., 1995 — Lepidoptera. Pp. 693-722 in: Arthropoda di Lampedusa,Linosa e Pantelleria (Canale di Sicilia, Mar Mediterraneo). —Naturalista sicil., Paler-mo, 19 (suppl).SAJEVA M., 1984 — Caralluma europaea (Guss.) N. E. Br. and its Type Locality: Lampedusa Island.— British Cactus and Succulent Journal, 2: 40-42.SAJEVA M. & COSTANZO M., 1994 — Succulents. The Illustrated Dictionary. — Cassell plc, Lon-don UK.SENNBLAD B. & BREMER B., 1996 — The familial and subfamilial relationships of Apocynaceaeand Asclepiadaceae evaluated with rbcL data. — Plant Systematic Evolution, 202:153-175.WHITE A. & SLOANE B.L., 1937 — The Stapelieae. Vol. I. — Abbey San Encino Press, Pasadena.VANE-WRIGHT R.I. & DE JONG R., 2003 — The butterflies of Sulawesi: annotated checklist for a crit-ical island fauna. — Zool. Verh. Leiden, 343: 221-223.Authors’ address. — S. PISCIOTTA, P. ZITO, M. SAJEVA, Dipartimento di Scienze Botaniche del-l’Università di Palermo, Via Archirafi n. 38 - 90123 Palermo, Italy; correspondig author: M. Sajeva,email: sajeva@unipa.it251Danaus chrysippus (Linnaeus, 1758) (Lepidoptera Nymphalidae)...

Danaus chrysippus (Linnaeus, 1758) (Lepidoptera Nymphalidae) larvae feeding on Caralluma europaea (Guss.) N.E.Br. (Asclepiadaceae) in Lampedusa Island.

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Danaus chrysippus (Linnaeus, 1758) (Lepidoptera Nymphalidae) larvae feeding on Caralluma europaea (Guss.) N.E.Br. (Asclepiadaceae) in Lampedusa Island.

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