Conservation genetics and ecology of Angiopteris chauliodonta Copel. (Marattiaceae), a critically endangered fern from Pitcairn Island, South Central Pacific Ocean

Abstract

Angiopteris chauliodonta, endemic to remote Pitcairn Island, was until recently thought to occur in only two small populations. Survey work carried out on the island in 1997 increased the number of populations to six, but as the total number of plants found was 774 (of which only 147 were mature adults) the species should be regarded as critically endangered. The species occurred in native fern-rich Homalium taypau and Metrosideros collina forest that was in many areas heavily invaded by Syzygium jambos and Lantana camara. RAPD analysis identified related populations but there was no correlation between genetic and geographical distance. The highest levels of genetic diversity was partitioned within populations (H_S=0.154; D_ST=0.116), although the larger populations were not necessarily the most diverse. Threats are primarily due to forest clearance, invasive species and erosion. Conservation management for this species will be through reinforcement of existing populations to maximise their genetic diversity and translocation of new populations to suitable habitats.

Introduction

Island biota and ecosystems are highly vulnerable to disturbances associated with human activities, the most serious of which are the introduction and release of grazing mammals and alien plants Given, 1981, Mueller-Dombois & Loope, 1990, Paulay, 1994, Wright & Lees, 1996. Currently one in three of all known threatened plant species are island endemics (Whittaker, 1998). The reason for the susceptibility of island populations to extinction is controversial, but once the taxon's numbers have been depleted, the coup de grâce is usually delivered by stochastic factors, whether anthropogenic, demographic, environmental, catastrophic or genetic (Rosenweig, 1995, Frankham, 1997). Four genetic factors that can contribute to higher extinction rates in island populations are: inbreeding depression, loss of genetic variation, accumulations of mildly deleterious mutations and genetic adaptations to island environments (Frankham, 1997). Thus genetic studies of species which occur in fragmented island populations are likely to benefit conservation management programmes.

The ultimate goal of conservation biology is to maintain the evolutionary potential of species by maintaining natural levels of diversity, as this genetic diversity is essential for species and populations to respond to long and short term environmental change and thus overcome stochastic factors which could otherwise result in extinction (Frankel & Soule, 1981, Lande & Barrowclaugh, 1987, Rossetto et al., 1995). In addition, genetic diversity has been shown to be positively and significantly correlated with population fitness (Reed and Frankham, 2003). The use of molecular analysis as an integral component in the conservation of rare and endangered species is still in its infancy, but is becoming more widely used as the techniques become more accessible and less expensive. Knowledge of the genetic structure and relationships within and between populations leads to more appropriate population management from the beginning of conservation efforts, when options may be the most flexible (Haig, 1998). In addition, genetic surveys are a more accurate means of inferring demographic fragmentation, and the resulting level of risk of local extinction (Templeton et al., 1990). This information can also be used to select appropriate genotypes to maximise genetic diversity when formulating long term conservation strategies (Haig, 1998, Rossetto et al., 1995). The primary conservation goal should be to establish self-sustaining populations whenever possible, if necessary using ecological manipulations to minimise inbreeding and maximise genetic variability within populations (Holsinger & Gottlieb, 1991, Lande, 1988). Genetically effective management varies between species, and so for any plan to be drawn up there must also be a detailed knowledge of the species' natural history (e.g. ecology, breeding system, life-history), and in the case of pteridophytes spore dispersal may allow much more interpopulation gene flow than in most seed plants (Soltis and Soltis, 1990). It has been suggested that a recovery or management plan drawn up without considering this information may be subject to error (Hamrick et al., 1991).

A commonly used PCR technique for the detection of genetic variability is Randomly Amplified Polymorphic DNA (RAPD) (Williams et al., 1991). The RAPD technique is particularly useful for population studies (Parker et al., 1998, Williams et al., 1991), as it surveys the entire genome, rather then selected fragments, as with minisatellites and allozyme markers. RAPDs therefore provide unbiased estimates of genetic and clonal identity, making them useful in the development of breeding programmes and recovery strategies (Stewart and Porter, 1995). RAPD technology is also thought to be more liable to detect variation in inbred species (Williams et al., 1993, Dow et al., 1997), and consistently find more polymorphism than AFLP or ISSR (Lu et al., 1996, Parker et al., 1998). It has major advantages in molecular ecology because of its wide applications and the fact that it requires the least in technology, labour and cost, without the necessity of radioactivity and requiring only small amounts of DNA (Hadrys et al., 1992, Dawson et al., 1993, Fischer et al., 2000).

Angiopteris Hoffmann (Marattiaceae) is a widespread genus of giant ferns with bipinnate fronds up to 4 m in length which arise from a rosette. The genus occurs from Madagascar across South East Asia and Polynesia, and north to Japan. The taxonomy of the genus is debated with some authorities retaining only one species, A. evecta, in the genus while others allowing up to 200 (Verdoorn, 1938, Copeland, 1947). Angiopteris is distinguished from the morphologically similar genus Marattia as having rounded sporangia arranged in two rows (normally of 5–7 sporangia), while in Marattia the sporangia are fused into a single linear synangium (Copeland, 1947). Angiopteris is distinguished from Archangeopteris by being bipinnate and large in size (Copeland, 1947).

Little is known about the breeding biology of Angiopteris species, or about the life cycle of individuals within the genus. In addition no literature was found relating to the population dynamics of species within the genus or in closely related genera. Angiopteris species, however, reproduce both sexually by spores and vegetatively by means of the large fleshy globular rhizomes found at the base of the frond (known as ‘stipules’). The gametophytes are large and long lived; they are thought to be obligate mycorrhizal (Hepden, 1960), although not necessarily to a specific mycorrhiza (Cooper, 1976), but were successfully germinated on sterilised compost in Trinity College Dublin.

Angiopteris chauliodonta Copel., endemic to Pitcairn Island, was first described by Copeland in 1938 based on collections made by during the Mangarevan expedition in 1934. The fronds are bipinnate, with the pinnules slightly toothed and the sori formed by two rows of sporangia. The rachis is densely covered in scales when young. Closely related species include A. longifolia Grev. & Hook. from the Cook, Austral and Society Islands, from which it differs in having broad, sterile apices of the pinnules, with sharp, narrow, incurved teeth at their bases (Copeland, 1938). Pitcairn material was assigned by Brown and Brown (1931) to A. longifolia, and the type specimen for A. longifolia is also attributed to Pitcairn (Copeland, 1938). A. longifolia is, however, confined to the Society Islands, the Cook Islands and Rapa, and the species was probably described from Tahitian material, mistakenly labelled as having been collected from Pitcairn (Copeland, 1938; the type specimen is labelled as collected in 1830, but as it was published by Hooker in 1830, it was probably actually collected in 1825 on Captain Beechey's voyage to the Pacific). The local name on Pitcairn is nehe, and the plant is used for bedding and as an ornamental.

Angiopteris chauliodonta is a biogeographically significant component of the genus as it represents the most south-easterly species in the genus. In addition it is almost certainly one of the rarest Angiopteris species both in terms of its distribution on only a single island and its reduced population size.

The aim of this study was to gather information on the ecology and population structure of Angiopteris chauliodonta in order to understand the reasons for the species' limited distribution and population size on Pitcairn Island, and to use this information to develop scientifically sound conservation management for the species.