Biogeosciences, 11, 6657–6665, 2014 www.biogeosciences.net/11/6657/2014/ doi:10.5194/bg-11-6657-2014 © Author(s) 2014. CC Attribution 3.0 License. Colonization of an empty island: how does a plant with a plastic gender system respond? M. Philipp and H. Adsersen Department of Biology, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen Ø, Denmark Correspondence to: M. Philipp ([email protected]) Received: 10 April 2014 – Published in Biogeosciences Discuss.: 11 July 2014 Revised: 3 October 2014 – Accepted: 7 October 2014 – Published: 3 December 2014 Abstract. Honckenya peploides is the most common plant The barren volcanic surface of the island was soon colonized species on the island of Surtsey. It arrived in 1967 and af- by plants dispersed as seeds by sea water (Fridriksson, 1989). ter a juvenile period of 4 years it produced seeds and had The new environment was in many respects different from increased its number from below 100 to several millions. where the plants came from: the substrate was recent vol- Most populations had the individuals distributed in a regular canic tephra or lava with very low contents of C and N, and or random pattern, suggesting that intraspecific competition there were no or very few competitors, herbivores or pol- is important. H. peploides has a subdioecious reproductive linators. This would favour or constrain other phenotypes system consisting of pistillate plants producing capsules, and and genotypes than in the source population, and the isola- staminate plants delivering pollen. Some of the latter are in tion would reduce gene flux from the latter. The results may addition producing capsules and are denoted hermaphrodites. be differences in genetic diversity, morphology and/or repro- Populations at the south coast of Iceland had around equal ductive system as compared to the source populations. numbers of pistillate and staminate plants. At Surtsey we Plants that successfully colonize isolated localities are found more pistillate plants, probably due to their higher wa- supposed to possess reproductive systems able to function ter stress tolerance. We also found a tendency to a higher in spite of low density of mates or pollinators (Baker, 1955). frequency of hermaphrodite plants with a higher number of Many reproductive systems studied at oceanic islands have seeds per capsule compared to populations at the south coast turned out to be “mixed mating systems” able to produce of Iceland and the nearby island of Heimaey. We suggest that seeds after selfing as well as out-crossing (Barrett, 1989; this arises from the time right after the colonization of Surt- Bramow et al., 2013; Philipp et al., 2006). Such a system im- sey where population size was small and the small generalist plies reproductive assurance and maintains the potential for pollinators were not able to deposit sufficient pollen on pistil- generating individuals with different adaptive properties. late plants, causing the hermaphrodites to have an advantage In the present paper, we focus on the reproductive system by being able to set seed after selfing. The result of this ini- of Honckenya peploides (L.) Ehrh. (Caryophyllaceae) and tial advantage of the hermaphrodites in combination with the how it responded after establishment on Surtsey where, ini- inheritance of the sexes can still be seen due to the longevity tially, there were no or very few pollinators and few mates. of individuals. A generalized account of the colonization his- H. peploides has a circumpolar distribution and is fairly tory of H. peploides is given. common on sandy beaches throughout the distribution area. Populations occur on many beaches of Iceland where indi- viduals form large clumps by vegetative propagation. The immigration history of H. peploides on Surtsey is well 1 Introduction known. The first individuals were recorded in 1967 (Fridriks- son and Johnsen, 1968). In 1968, 103 individuals were ob- Surtsey is the youngest and southernmost island in the Vest- served and during 1968 to 1972 the number of recorded in- mannaeyjar Archipelago south of Iceland. It appeared as a dividuals was between 52 and 71 (Fridriksson, 1992). The result of volcanic eruptions during the years 1963 to 1967. Published by Copernicus Publications on behalf of the European Geosciences Union. Reproductive response of Honckenya peploides to colonization of Surtsey 6658 M. Philipp and H. Adsersen: Colonization of an empty island 6 individuals and with few pollinators, successful seed set may occur more frequently in hermaphrodites than in pistillate in- dividuals. 5 By comparing populations at Surtsey with populations on the Icelandic mainland and Heimaey, we address the follow- 4 ing questions: 1. Has the sexual reproductive system of H. peploides 3 changed from subdioecy towards hermaphroditism? Log population size 2. Has the ratio between pistillate and staminate individu- 2 als in populations influenced the male and female func- tion of the individuals? 1 66 68 70 72 74 76 78 80 82 3. Has population age or stability any influence on the ratio between pistillate and staminate individuals? 1 Year 4. Which mechanisms could be involved in such changes? 2 Fig 1. Figure 1. Increase in number of Honckenya peploides plants on 3 Surtsey between the years 1967 and 1981 (after Fridriksson, 1992). 2 The species 4 5 Sea sandwort, Honckenya peploides (L.) Ehrh. (Caryophyl- first capsule was observed in 1971 (Fridriksson, 1982), and in laceae) has been subdivided into four varieties, of which H. 6 1973 the number of recorded individuals increased to > 500. peploides var. diffusa (Horn.) Mattf. (Böcher et al., 1978) 7 This indicated that in the first years the population was build- is the arctic circumpolar variety that occurs in Iceland. H. ing up from immigrating seeds and that the founding pop- peploides is a perennial hemicryptophyte and shoots sprout ulation size was ∼ 100 individuals. The abrupt increase in each spring from buds on prostrate rhizomes forming dense 1973 must have been due to successful seed set and local clones. The leaves are opposite and succulent with short in- dispersal episodes in 1972. From then H. peploides spread ternodes. The clones are found on beaches as pioneers and rapidly all over the island from the coast to the top of the often become covered by sand. A unique feature of the H. two calderas (ca. 150 m a.s.l.) and it is at present the most peploides populations at Surtsey is that most of them have common plant species with probably millions of individuals established and developed without interspecific competition 29 (Fridriksson, 1992) (Figs. 1 and 2). Throughout the 1970s and disturbance by human activities. As a result of this most all colonizing individuals were marked with sticks on which individuals consist of rounded pillows or mats up to 6 m a number and the year of the first observation were noted. in diameter and consequently, we had no problem in iden- Most of the marker sticks are still extant so it is possible tifying single individuals. In mainland situations, individu- to age many individuals, and of course none are more than als tend to become fragmented due to disturbance, compe- 50 years old. tition and senescence, so it was harder to identify individu- In most populations of H. peploides two types of flow- als and avoid resampling of genets. The amplified fragment ers (pistillate or staminate) occur (see below and Fig. 3). length polymorphism (AFLP) analyses of the collected ma- Plants with pistillate flowers do not have functional stamens terial show, however, that no genetically identical individuals and most often develop copious capsules whereas the stami- were recorded in our samplings (K. Anamthawat-Jónsson, nate plants have stamens and no or in some cases few cap- personal communication, 2014). Flowers are white and soli- sules. The reproductive system may be characterized as sub- tary in leaf axils. Two types of flowers are found (Fig. 3). dioecious as the staminate plants function as males, mostly. On some individuals the flowers possess short petals, non- Crossing experiments in a Greenlandic population showed functional anthers and long styles (pistillate). These indi- that the staminate plants were self-compatible (Eithun, 2003) viduals are producing plenty of globular capsules with large as was also found in H:p: subsp. major from Japan (Tsukui seeds. On other individuals the petals are longer, anthers are and Sugawara, 1992). well-developed and the styles are short (staminate). These During the initial colonization in 1967–1972, H. peploides individuals function mainly as males but some, in addition, survived with very few and scattered individuals (Figs. 1 are able to produce a few capsules with seeds and are denoted and 2) (Fridriksson, 1992; Jakobsson et al., 2007). Given hermaphrodites (Eithun, 2003; Malling, 1957; Sánchez-Vilas that the staminate H. peploides individuals are able to set et al., 2010; Tsukui and Sugawara, 1992). seeds after selfing, we expected the reproductive system to have responded in the direction of a higher degree of hermaphroditism. In populations with large distances among Biogeosciences, 11, 6657–6665, 2014 www.biogeosciences.net/11/6657/2014/ M. Philipp and H. Adsersen: Colonization of an empty island 6659 Figure 2. During 1967 to 1997 Honckenya peploides dispersed to every part of Surtsey. The shaded areas indicate the shape of the island in theReproductive respective response years. of Honckenya The peploides intensity to colonization of green of reflectsSurtsey the abundance of the plant (Jakobsson et al., 2007). 1 2 the minimum distance from each individual to its neighbour 3 and from each individual to an individual of the same and 4 opposite morph respectively. 5 The collected flowers and capsules were stored in 50 % 6 ethanol for later inspection. In the lab one non-dehisced an- 7 ther from up to four individuals per population was placed in a b c glycerol on an object glass and finely subdivided.