Convergent Evolution of Carrion and Faecal Scent Mimicry in Fly-Pollinated Angiosperm Flowers and a Stinkhorn Fungus ⁎ S.D
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South African Journal of Botany 76 (2010) 796–807 www.elsevier.com/locate/sajb Convergent evolution of carrion and faecal scent mimicry in fly-pollinated angiosperm flowers and a stinkhorn fungus ⁎ S.D. Johnson , A. Jürgens School of Biological and Conservation Sciences, University of KwaZulu-Natal Pietermaritzburg, Private Bag X01, Scottsville 3209, South Africa Received 1 June 2010; received in revised form 24 July 2010; accepted 26 July 2010 Abstract Flowers of many angiosperms attract fly pollinators through mimicry of animal carrion and faeces. This phenomenon of “sapromyiophily” is also evident in the sporophytes of some mosses and fruiting bodies of “stinkhorn” fungi, both of which use flies as agents of spore dispersal. We studied the scent chemistry of a stinkhorn fungus (Clathrus archeri) and seven fly-pollinated plant species with foetid odours to determine the degree to which these organisms mimic the scent of carrion and faeces (reference scent samples were collected from rotting meat, a rat carcass and horse and dog faeces), as well as the degree of convergent evolution between the fungus and angiosperm flowers. We found that scents of both the fungus and angiosperms tended to contain compounds typical of carrion, such as oligosulphides, and of faeces, such as phenol, indole and p- cresol. This study provides compelling new evidence for mimicry of carrion and faeces, as well as a striking pattern of convergence in the putrid scents of the fungus and the angiosperms, relative to those of confamilial species. The syndrome of sapromyiophily thus encompasses at least two kingdoms (Plantae and Fungi) and provides an effective means of exploiting flies as agents of pollen and spore dispersal. © 2010 SAAB. Published by Elsevier B.V. All rights reserved. Keywords: Brood-site mimicry; Calliphoridae; Clathrus archeri; Diptera; Flower scent; GC-MS; Intraspecific variation; Sapromyiophilous; Stapeliads 1. Introduction pollinators (Jürgens et al., 2006; Knudsen and Tollsten, 1993, 1995). Floral “pollination syndromes” (sensu Faegri and Van der Pijl, “Sapromyiophilous” flowers – those which attract carrion 1979) provide classical examples of convergent evolution — and dung flies through mimicry of their food and brood sites – similarity of traits in unrelated organisms that have adapted to have evolved in many angiosperm families (Banziger and Pape, similar environmental factors. These syndromes, which arise when 2004; Burger et al., 1988; Johnson, 1997; Kite et al., 1998; unrelated plants adapt to the same functional pollinator group Ollerton and Raguso, 2006; Stensmyr et al., 2002; Shuttleworth (Fenster et al., 2004), are usually described using qualitative and Johnson, 2010a, 2010b). These species have foul-smelling characteristics of the morphology, colour and scent of flowers flowers which are typically brown with purple or reddish (Ollerton et al., 2009). However, general descriptors of floral scent blotches and often unusually large, as exemplified by Stapelia such as “sweet”, “pungent” etc. are inadequate to describe the gigantea (Apocynaceae) (this study) and Rafflesia arnoldii chemical complexity of this phenotypic trait (Raguso, 2008). An (Rafflesiaceae) (Barkman et al., 2008). There is now good increasing number of studies thus use coupled gas chromatogra- evidence that the attraction of flies to these flowers depends phy-mass spectrometry (GC-MS) for quantitative investigations of heavily on the emission of volatiles that are used by flies as cues floral scents (Knudsen et al., 2006), but there are still comparatively to locate carrion, faeces and even urine (Shuttleworth and few of these that explicitly consider the hypothesis of convergent Johnson, 2010a, 2010b; Stensmyr et al., 2002). Stensmyr et al. evolution in scent chemistry among unrelated plants that share (2002) showed that oligosulphides emitted by the Mediterra- nean ‘dead-horse’ Arum were identical to those emitted by ⁎ Corresponding author. animal carrion and triggered the same electrophysiological E-mail address: [email protected] (S.D. Johnson). response in fly antennae. More recently, Shuttleworth and 0254-6299/$ - see front matter © 2010 SAAB. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.sajb.2010.07.012 S.D. Johnson, A. Jürgens / South African Journal of Botany 76 (2010) 796–807 797 Johnson (2010a, 2010b) demonstrated that a shift to pollination particularly among succulent stapeliads (Bruyns, 2005; Meve by carrion flies could be induced in wasp-pollinated Eucomis and Liede, 1994), provides ideal opportunities for this purpose. species (Hyacinthaceae) simply by experimental addition of Attraction of flies through mimicry of their food and brood sites oligosulphides to inflorescences. Investigations of the chemical is not confined to angiosperms. There is now good evidence that composition of the scent of sapromyiophilous flowers by Kite sapromyiophily occurs among both mosses and fungi (Fischer and and Hetterscheid (1997) and Jürgens, et al. (2006) indicate that Vicha, 2003; Marino et al., 2009), although the function of fly there may be a number of different strategies in operation, attraction in these cases is for subsequent dispersal of spores rather including mimicry of carrion (characterized by oligosulphide than gametes. In mosses, sticky spores are usually transported on emission), mimicry of faeces (characterized by emission of p- the bodies of flies (Marino et al., 2009), while in fungi spores are cresol, phenol and skatole) and mimicry of urine (various acids). often consumed along with an exudate (the “gleba”)andgerminate However, the patterns are not yet clear and sampling of more once they have passed through the digestive system of flies (Tuno, species and manipulative experiments are required to gain 1998). Stinkhorn fungi belonging to the Phallaceae have foul- increased understanding of the significance of particular volatile smelling fruiting bodies that are known to attract flies (Fischer and blends. South Africa with its rich diversity of carrion flowers, Vicha, 2003; Sleeman et al., 1997; Tuno, 1998). This study Fig. 1. Sapromyiophilous species included in the scent analysis: (a) Fruiting body of the stinkhorn fungus Clathrus archeri; (b) Muscid fly feeding on the gleba of C. archeri; (c). Stapelia gigantea and visiting calliphorid flies; (d). Gynostegium of S. gigantea with eggs freshly deposited by a calliphorid fly; (e) Orbea variegata; (f) Orbea verrucosa; (g) Huernia hystrix; (h) Stapelia leendertziae; (i) Ferraria crispa with visiting sarcophagid fly; (j) Aristolochia cymbifera. 798 S.D. Johnson, A. Jürgens / South African Journal of Botany 76 (2010) 796–807 includes an investigation of the scent of Clathrus archeri, a species this specimen were taken in the field using the methods native to Africa and Australasia (Dring, 1980) which is commonly described in Section 2.2. known as the octopus or cuttlefish stinkhorn (Fig. 1a). Our In addition to the stinkhorn, we studied the floral scent of preliminary observations indicate that the foul-smelling fruiting seven angiosperm species with foul-smelling flowers typical of bodies of this species are visited by numerous flies, including the sapromyiophilous syndrome (Table 1; Fig. 1c–j). We also blowflies (Calliphoridae), flesh flies (Sarcophagidae) and house- included Euphorbia grandicornis Goebel ex N.E. Br. (Euphor- flies (Muscidae) (Fig. 1b). The scent of this species has not been biaceae) for comparison because its cyathial glands are sweet- investigated previously, but oligosulphides typical of carrion have smelling, yet its flowers are often visited by blowflies along been shown to be emitted from fruiting bodies of another stinkhorn, with a wide diversity of other insects (S.D. Johnson, the European species Phallus impudicus (Borg-Karlson et al., unpublished observations). The sapromyiophilous species 1994). Although the gleba of stinkhorns has some nutrient value, included five South African stapeliads in the genera Stapelia, investigations of the North American species Mutinus caninus Orbea and Huernia, a South African iris (Ferraria crispa) and a show that this is far less than that which flies obtain from dung or South American vine, Aristolochia cymbifera (Table 1). faeces (Stoffolano et al., 1990). We are also not aware of any Flowering plants of these species were all sampled in the evidence to suggest that the short-lived fruiting bodies of stinkhorn botanical garden of the University of KwaZulu-Natal, apart fungi are used as a brood place for the larvae of necrophagous flies. from Orbea verrucosa and A. cymbifera, which were sampled in The system can thus be described as one of deception. private gardens, and F. crispa, which was sampled in a In this study we investigated the scent of the stinkhorn C. population growing at Noordhoek on the Cape Peninsula. Some archeri and several angiosperm species that have flowers which of the study species have been reported to be pollinated by are known or suspected to be pollinated by carrion flies. We carrion flies (Table 1). In addition, we made observations of fly hypothesized that these species would show general conver- visits to flowers of S. gigantea, S. variegata, Stapelia gence in scent chemistry on account of mimicry of animal leendertziae, H. hystrix, and F. crispa. Identifications of the carrion and faeces. fungus and plant taxa were based primarily on the publications of de Vos (1979), Dring (1980) and Bruyns (2005). Vouchers of the plant species are deposited in the Bews Herbarium