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Differential Herbivory on Disk and Ray Flowers

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Biological Journal of the Linnean Society, 2010, 101, 544–552. With 1 figure Differential herbivory on disk and ray flowers of gynomonoecious asters and goldenrods (Asteraceae) ROBERT I. BERTIN*, DANIEL B. CONNORS and HOLLY M. KLEINMAN Department of Biology, College of the Holy Cross, Worcester, Massachusetts 01610, USA Received 5 February 2010; revised 20 May 2010; accepted for publication 21 May 2010bij_1508 544..552 The selective advantage of gynomonoecy, the sexual system wherein plants produce a mixture of female and bisexual flowers, is poorly understood. One hypothesis for the evolution of this system is that the absence of androecia from female flowers reduces herbivore damage to the gynoecia of these flowers. Here, we examined patterns of herbivore damage in 53 collections representing 25 species of asters and goldenrods from Massachu- setts, USA. In these taxa flowers are crowded into compact capitula, with bisexual flowers occupying the centre and female flowers situated on the periphery. Damage to gynoecia of bisexual flowers was significantly greater than damage to gynoecia of female flowers overall, and in about half of the individual populations. We also compared damage to central and peripheral flowers in the heads of 16 collections of other Asteraceae that produce only bisexual flowers to see whether the location of flowers rather than their sex might determine the patterns of herbivory. In only one of these 16 collections did we find a significant difference in herbivory between flower positions. We conclude that herbivore damage is influenced by flower type in asters and goldenrods, a pattern consistent with a role for herbivory in the evolution and maintenance of gynomonoecy. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101, 544–552. ADDITIONAL KEYWORDS: capitulum – florivory – gynomonoecy – sexual system – Solidago – Symphyotrichum. INTRODUCTION damage than female plants (summarized in Boecklen & Hoffman, 1993; Ågren et al., 1999; but see Strauss, Herbivory is a major selection pressure in flowering 1990). Differential herbivory of male and female indi- plants, acting on many plant attributes, including viduals may be directed towards flowers (Bawa & reproductive biology. Several studies suggest that Opler, 1978; Cox, 1982; Boecklen, Price & Mopper, herbivory on flowers (florivory) can be an important 1990; Krischik & Denno, 1990; Muenchow & Delesalle, selective force in the evolution of sexual systems, 1992; Wolfe, 1997), or it may involve other plant parts, including the evolution of dioecy from cosexua- such as foliage, stems, or seeds (Danell et al., 1985; lity (Bawa & Opler, 1978; Cox, 1982; Muenchow & Ågren, 1987; Elmqvist & Gardfjell, 1988; Boecklen Delesalle, 1992; Ashman, 2002), and the maintenance et al., 1990; Krischik & Denno, 1990; Boecklen & of females in gynodioecious species (Marshall & Hoffman, 1993; Wolfe, 1997; Marshall & Ganders, Ganders, 2001) and males in andromonoecious species 2001). (Muenchow, 1998). The impact of herbivory on sexual Differential herbivory of flowers or inflorescences systems arises when the extent of damage differs that differ in sex expression within a single plant has between flowers, inflorescences, or plants that differ in been reported less often. Herbivory on male flowers sex expression. Such morph-specific herbivory has exceeded that on female flowers in monoecious Psig- been documented in numerous dioecious or gynodioe- uria warscewiczii and Sagittaria latifolia (Murawski, cious species, with male plants usually receiving more 1987; Muenchow & Delesalle, 1992). However, damage to female flowers exceeded damage to male flowers in Pinus edulis (Cobb, Trotter & Whitham, *Corresponding author. E-mail: [email protected] 2002). Damage to female flowers in Freycinetia 544 © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101, 544–552 GYNOMONOECY AND HERBIVORY IN COMPOSITES 545 reineckei was greater if they occurred in bisexual around 42.27°N, 71.81°W) during the late summer inflorescences than if they occurred in female and autumn of 2002, six in 2003, and 34 in 2007. inflorescences (Cox, 1982). Sixteen collections of composites with exclusively Whereas patterns of herbivory in relation to sexual bisexual flowers were made during the same period. system have been examined in dioecious, monoecious, The typical procedure was to walk through a popu- and gynodioecious species, the relevance of herbivory lation, collecting from the closest plant every 1–2 m to gynomonoecy remains unexplored. Gynomonoecy is (depending on the species) along the way. We col- a sexual system in which individual plants produce lected from up to 20 plants if sufficient indivi- both female and bisexual flowers. This system is duals were available. Multiple heads were collected widespread in the Asteroideae, the largest subfamily from scattered locations on each plant and pre- in the Asteraceae, and several surveys report its served in alcohol. To control for developmental occurrence in 2.8–7.0% of angiosperms (Yampolsky & stage, heads were selected only if they were old Yampolsky, 1922; Carlquist, 1974; Bernadello et al., enough that every flower in the head had opened, 2001; Lu & Huang, 2006). but not so old that perianths had detached or pappi Several possible adaptive advantages have been were conspicuous. suggested for gynomonoecy (Willson, 1983; Bertin & In addition to the 53 collections of asters and gold- Kerwin, 1998; Bertin & Gwisc, 2002). One hypothesis enrods, we collected heads from 16 populations rep- states that gynomonoecy is beneficial because it resenting ten species of composites that produce removes some gynoecia from the vicinity of androecia, exclusively bisexual flowers. These collections were and thereby reduces herbivore damage to pistils. made to evaluate the effect of position of flower within Such a pattern might occur, for example, if herbivores the head. Position is a potentially confounding vari- were attracted to pollen but additionally caused able in this study because ray flowers are always damage to pistils if these were present in the same peripheral and disk flowers are always central in flower. Under these conditions, plants producing some asters and goldenrods. Collected species containing of their gynoecia in female flowers (gynomonoecious only bisexual flowers included members of the genera individuals) would have higher maternal fitness than Eupatorium and Eutrochium in the tribe Eupatoriae plants that produced all of their gynoecia in bisexual of the subfamily Asteroideae, and Hieracium, Lactuca, flowers. A prediction of this hypothesis is that gyno- Scorzoneroides, Taraxacum, and Tragopogon in the ecial damage is greater in bisexual flowers than in tribe Cichorieae of the subfamily Cichorioideae female flowers. In this study we evaluate this expec- (Table 1). tation by comparing the frequencies of gynoecial We examined between one and five heads per damage in ray and disk flowers in 25 species of plant under a dissecting microscope. The number gynomonoecious asters and goldenrods. was constant for plants in a given population, and was influenced by the number of heads of a suitable developmental stage at the time of collection. For gynomonoecious species, we recorded the numbers of MATERIAL AND METHODS ray and disk flowers with ovary damage, and the STUDY SPECIES AND FIELD COLLECTIONS numbers with either stigma or style damage. A The terms aster and goldenrod refer here to taxa that stigma was scored as damaged if at least half of it at one time were assigned to the genera Aster and was missing. Styles scored as damaged were typi- Solidago, respectively. Taxonomic studies have since cally severed. For species with bisexual flowers we split each taxon into multiple genera. Asters used in removed the outermost ring of flowers from each this study are currently assigned to the genera Doel- head and treated these as ‘outer’ flowers, in contrast lingeria, Eurybia, Ionactis and Symphyotrichum. to the remaining ‘inner’ flowers. Ovary damage in Goldenrods now belong to the genera Euthamia and each group was recorded separately. We did not Solidago. All asters and goldenrods are in tribe record stigma damage for members of the tribe Astereae of the subfamily Asteroideae. Asters and Cichorieae because most of the stigmas had sepa- goldenrods produce numerous small flowers aggre- rated from the ovaries by the time of counting, ren- gated into heads, or capitula. Within a capitulum, an dering it impossible to distinguish the stigmas of outer ring of female flowers surrounds an inner group inner and outer flowers. Stigma/style damage was of bisexual disk flowers. In most taxa, each female tallied for the remaining two species with bisexual (ray) flower bears a single conspicuous petal, or ray. flowers (genera Eupatorium and Eutrochium). In The entire capitulum resembles a single large flower total, we examined 3654 heads and over 117 000 (Leppik, 1977). flowers from gynomonoecious species, and 805 heads We made 13 collections of gynomonoecious species and over 22 000 flowers from species with bisexual within 25 km of Worcester, Massachusetts (centred flowers only. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101, 544–552 546 R. I. BERTIN ET AL. Table 1. Collection information for composites examined in this study. Numbers after species names denote different populations. The collection no. is used for reference in Figure 1. Plants and heads refer to the numbers of sampled plants and numbers of heads per plant, respectively Gynomonoecious asters and goldenrods Collection no. Year Plants Heads Doellingeria umbellata (P. Mill.) Nees 1 1 2002 20 2 Doellingeria umbellata (P. Mill.) Nees 2 2 2002 15 2 Doellingeria umbellata (P. Mill.) Nees 3 3 2007 20 3 Doellingeria umbellata (P. Mill.) Nees 4 4 2007 20 3 Eurybia divaricata (L.) Nesom 1 5 2002 20 2 Eurybia divaricata (L.) Nesom 2 6 2007 20 3 Eurybia divaricata (L.) Nesom 3 7 2007 20 3 Euthamia graminifolia (L.) Nutt. 1 8 2007 20 5 Euthamia graminifolia (L.) Nutt. 2 9 2007 19 5 Ionactis linariifolius (L.) Greene 1 10 2002 20 1 Ionactis linariifolius (L.) Greene 2 11 2007 20 3 Solidago altissima L. 1 12 2002 20 3 Solidago altissima L.
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