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2 School of Biological Sciences, The University of Auckland, Private Bag 92019 Auckland, New Zealand; and 3 CSIRO Division of Plant Industry, GPO Box 1600, Canberra ACT 2601, Australia
Received for publication December 15, 1998. Accepted for publication December 14, 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Fixation Index] was consistently higher than Fm in all populations, indicating that selection may eliminate selfed offspring from populations prior to achieving reproductive maturity. Results suggest that increased selfing in mainland populations due to pollinator changes is not responsible for current patterns of poor regeneration of this species.
Key Words: birds • geitonogamy • inbreeding depression • Metrosideros • Myrtaceae • mixed mating • New Zealand • pollinator shift • selfing
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Barrett and Harder, 1996
; Hall, Walker, and Bawa, 1996
). Among the genetically determined parameters, life history, plant size, and floral design and display, as well as factors such as pre- or post-zygotic self-incompatibility and/or inbreeding depression, are important features influencing the mating system (Barrett and Harder, 1996
; Kennington and James, 1997
). Important ecological factors include population size, density, and pollinator numbers and behavior (Ellstrand, Torres, and Levin, 1978
; Watkins and Levin, 1990
; Karron et al., 1995
). The possible effects of changes in this second set of factors have recently become a particular point of concern regarding in situ conservation of plant species in the light of increasing destruction and fragmentation of populations due to habitat loss (Murawski, Gunatilleke, and Bawa, 1994
; Young, Boyle, and Brown, 1996
). Habitat fragmentation leading to small populations and loss of pollinators both will increase levels of inbreeding and pose a threat to population viability and species persistence (Barrett and Kohn, 1991
; Sampson, Hopper, and James, 1995
).
Metrosideros excelsa Sol. ex Gaertn. (pohutukawa) is a distinctive, multistemmed tree of rocky coastlines endemic to New Zealand. Individual trees reach a height of 25 m (Poole and Adams, 1990
) and flower profusely for a peak time of 
2 wk in summer (November–January). The showy red "brush" flowers are set in large inflorescences and produce 50 µL of nectar per flower per day (Schmidt-Adam, Gould, and Murray, 1999
).
A number of flower visitors have been shown to be effective pollinators, as they regularly forage on pohutukawa flowers, carry large pollen loads, and effect fruit set (Anderson, 1997
). These include the native New Zealand honeyeaters (Meliphagidae), a range of introduced birds and native and introduced bees (Donovan, 1980
; Salmon, 1980
; Anderson, 1997
). Geckos and bats also feed from pohutukawa flowers and have been suggested as pollinators (Whitaker, 1987
; Eifler, 1995
; Arkins, 1996
).
Pohutukawa originally occurred as a continuous band of forest along the seashores of the northern half of the North Island. Land clearing for settlement by European immigrants in the 19th century, subsequent extensive pastoral farming, and the need of timber for a growing ship-building industry (Dieffenbach, 1843; Colenso, 1868) have eliminated an estimated 90% of pohutukawa (Forest Research Institute, 1989
). The species is now largely reduced to isolated stands or individual trees, and its conservation status has been described as "declining" (de Lange and Norton, 1998
).
Among the factors that contribute to the species' decline is the browsing by introduced herbivores such as the brush-tailed possum (Trichosurus vulpecula), which eats vegetative buds and mature leaves (Hosking and Hutcheson, 1993
) and reduces flower production (Skeates, 1980
; Carlaw, 1997
). Natural regeneration of pohutukawa is limited and confined to safe germination sites free of leaf litter and competition from other vegetation (Wotherspoon, 1993
).
A dramatic shift in the suite of pollinators since the time of European immigration has accompanied the decline of pohutukawa populations and still has the potential to affect extant populations. On the mainland endemic birds, such as the three species of the New Zealand honeyeaters, have decreased in number or become locally extinct. At the same time, several bird species native to Europe and Asia have been introduced to New Zealand and have become established (Diamond and Veitch, 1981
). In the 1830s, honeybees were introduced (Donovan, 1990
), which now co-exist with the native short-tongued bees. On a few islands off the New Zealand mainland, however, there has been little change in the bird and insect fauna since the beginning of European settlement, and in these locations the original suite of pollinators remains intact.
Such a change in the suite of pollinators as seen on mainland New Zealand has considerable potential to affect the frequency and pattern of mating events, in particular the rate of cross- vs. self-fertilization. Previous work on the reproductive biology of pohutukawa using controlled pollinations has shown that individual pohutukawa trees differ considerably in their ability to produce seeds following self-pollination (Schmidt-Adam, Gould, and Murray, 1999
). Natural populations are likely, therefore, to consist of a mixture of self-incompatible and self-compatible individuals. Fragmentation and the shift from native to predominantly introduced pollinators may lead to increased selfing; harmful effects of selfing such as inbreeding depression may interfere with seedling establishment. Such a pollinator-induced shift to increased selfing could account for some of the poor regeneration described above.
The goal of this study was to examine the mating system of pohutukawa in natural populations. In particular, our aims were (1) to estimate the frequency of selfing and examine whether inbreeding depression acts as a selective force on the species and (2) to explore whether the shift in the pollinator fauna from native to predominantly introduced species had an effect on the mating system. To achieve this, we compared mainland populations with those on offshore islands that have experienced little change in the bird and insect fauna.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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120 ha of pohutukawa forest occurring mainly on coastal cliffs and as a fringing belt along the cliff bases (Hamilton, 1961
). Collections were made from a subpopulation of 200 trees at the southwest tip of the island (Te Maraeroa). Tiritiri Matangi (TTI, 220 ha), is 3.5 km off the Whangaparoa Peninsula. Here, an estimated 300–350 mature pohutukawa trees are found on exposed coastal cliffs and in inland bush remnants. On the mainland, seed capsules were collected from trees at Cooper's Beach (CB) at Doubtless Bay in the north, Tapapakanga Regional Park (TP) southeast of Auckland, and Whites Beach (WB) on Auckland's west coast. The estimated size of these three populations was 150–200 trees.
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). Although little is known about the occurrence of insects in the studied populations, honey bees were reported from TTI (Anderson, 1997
), and native bees and honey bees presumably coexist in the coastal mainland habitats.
To obtain a relative measure of pollinator numbers at peak flowering in the five populations, bird and insect species were identified and their relative abundance was assessed. Stationary standard 5-min bird counts (Dawson and Bull, 1975
) were made on five trees per population from late November to late December 1997. In each pohutukawa stand, a total of 40–52 counts were made with two daily morning counts per tree for at least 4 d. All birds heard or seen within a 100-m range from the observed tree were recorded, and only those bird species that were observed feeding at least once from flowers were reported.
Insects were counted in the two island populations and at WB on the mainland. All insects landing on flowers within an observation area of 0.2 m2 (50 inflorescences) per tree were recorded for durations of 10 min each. In total, 18–20 counts per population were made on 2–3 trees per population for at least 3 d. All observations were restricted to still or near to still conditions with no rainfall and insect counts were only made in full sun. The overall mean abundance of all bird or insect species per population was given by the mean of all counts made in that population.
Allozyme analysis of outcrossing rates
Within each population, 15 "open-pollinated" seeds from a bulked sample of capsules from five random positions within a tree were sampled from each of 15 maternal trees in April 1996. Seeds were germinated in a growth cabinet under 12 h of 15°C dark and 12 h of 25°C light, and 3-wk-old seedlings with fully emerged cotyledons were ground in one drop of chilled 0.05 mol/L borate extraction buffer (pH 7.0) containing 1 mg/mL dithiothreitol and 20 mg/mL polyvinylpyrrolidine (PVP 40). The tissue extract was absorbed by 6 x 4 mm wicks (Whatman Number 3 filter paper) and starch gels (9% w/v, 6 mm thick) were run at constant current at 4°C.
Thirteen out of 16 enzyme systems initially screened showed either poor resolution or were monomorphic. Five polymorphic loci for three enzymes were resolved clearly and consistently on a histidine gel and electrode buffer system at pH 8.0 (Brewer and Sing, 1970
): glucose-phosphate-isomerase (Gpi) E.C. 5.3.1.9 (one locus), phosphoglucomutase (Pgm) E.C. 5.4.2.2 (two loci), and glucose-1-phosphate-uridilyl-transferase (Gpt) E.C. 2.7.7.9 (two loci). The banding pattern of putative heterozygotes and homozygotes suggested Mendelian inheritance of these loci based on expectations from known enzyme subunit structures (Kephart, 1990
).
Maternal genotypes were inferred from the genotypes in progeny arrays (Brown and Allard, 1970
). Maximum likelihood estimates of single-locus and multilocus outcrossing rates (t) were made using the program developed by Ritland and Jain (1981)
. Standard errors of the estimates were based on 500 bootstraps with resampling among mothers. Wright's fixation index (F) (Wright, 1965
) was calculated for maternal trees and seedlings using maternal and progeny genotypic frequencies for polymorphic loci.
Seed germination and seedling growth
Seed capsules of pohutukwa contain a mixture of filled seeds with a fully developed embryo and empty seeds. To assess the effect of selfing on germination and seedling fitness, a total of 240 filled seeds originating from hand self- or cross-pollinations from a diallel cross using four trees (Schmidt-Adam, Gould, and Murray, 1999
) were germinated in potting mix, and seedling height was measured at 2-mo intervals up to 1 yr of age.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Allozyme analysis of outcrossing rates
The frequency of self-fertilization was high in all five pohutukawa populations, with estimates of multilocus outcrossing rates ranging from as low as tm = 0.22 up to a maximum of tm = 0.53. There was little variation in the outcrossing rates of four of the populations (tm > 0.4), but TP was much lower (tm = 0.22) (Table 2). No significant differences between single (ts) and multilocus (tm) outcrossing rates were found. Wright's Fixation Index (Wright, 1965
) was consistently higher for progeny (Fs) than for the maternal parents (Fm). Allelic richness (A) was high in all populations providing good power for the estimates of tm (Table 2).
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= 0.05; SAS, 1989
), and all seedlings survived up to 1 yr. However, after 6 mo of growth, plants originating from cross-pollination were significantly taller than those from self-pollination (Tukey's studentized range test; significant at = 0.05; SAS, 1989
), and this effect became more pronounced up to 12 mo (Fig. 4).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), and the low outcrossing rates reported here show that 60% of seeds originated from selfing. However, the very small differences between single and multilocus outcrossing rate estimates suggest that biparental inbreeding is negligible.
The estimated outcrossing rates of 40–50% are intermediate between predominant selfers and predominant outcrossers in comparison to other animal-pollinated species. Only very few other woody perennials, however, have lower outcrossing rates than pohutukawa, and selfing is therefore unusually high for a long-lived species (Barrett and Eckert, 1990
; Barrett, Harder, and Worley, 1996
).
The outcrossing rates reported here are the first for a member of the genus Metrosideros and are among the lowest that have been observed within the Myrtaceae. Mass-flowering Myrtaceae, such as many species of Eucalyptus, generally show high outcrossing rates in the range of tm = 0.70–0.86 (Moran and Bell, 1983
; Peters, Lonie, and Moran, 1990
), and Melaleuca alternifolia has an extremely high outcrossing rate of tm = 0.93 (Butcher, Bell, and Moran, 1992
).
The high levels of selfing observed for pohutukawa result in the production of large numbers of inbred progeny, as evidenced by the high seedling fixation indices of up to Fs = 0.37. However, the consistenly lower levels of gene fixation in mothers (mean Fm = 0.07) in all five populations suggest that adult fitness may be maintained by strong selection against homozygotes prior to reproductive maturity.
The germination rate of seeds in potting mix averaged 44% and was not significantly different for seeds from selfing and crossing. Whereas in a previous study, seed germination on filter paper under controlled conditions was found to be much higher (98.4%; Schmidt-Adam, Gould, and Murray, 1999
), again no differences in germination rate for "selfed" or "crossed" seeds were found. These results indicate that inbreeding depression is not acting at this early stage of the life cycle.
However, inbreeding depression was expressed in lower rates of shoot growth of selfed seedlings relative to outcrossed seedlings after a six month growth period. Although the genetic basis of inbreeding depression is not fully understood (Damgaard and Loeschcke, 1994
), it is probable that such late-acting inbreeding depression is due to small effects at many gene loci, rather than major effects at a few loci, which is more commonly expressed as early-acting lethals (Barrett and Harder, 1996
; Husband and Schemske, 1996
). Late-acting inbreeding depression has been observed in other myrtaceous species. In E. globulus ssp. globulus, inbreeding depression for height first occurred between germination and 8 mo after planting and in E. gunnii both survival and height of seedlings from selfing were depressed after one year's growth in comparison to wide intraspecific crosses (Potts, Potts, and Cauvin, 1987
; Hardner and Potts, 1995
). In E. regnans, the major phase of post-dispersal selection occurred after 4 yr and was coincident with canopy closure and onset of strong competition for resources. Inbreeding depression in survival at 15 yr was 67% for selfs and was one of the highest reported for a tree species (Hardner and Potts, 1997
).
There was no significant difference in outcrossing rates between island and mainland populations. Accepting that the number of populations sampled in this study was small and that caution has to be applied with regard to conclusions, we found marked differences in the abundance and make-up of pollinators of island and mainland populations. Both island populations sustain a large number of native birds, whereas the three mainland sites were almost exclusively populated by introduced birds. Thus, if native bird species were more efficient than introduced species in promoting outcrossing in pohutukawa, lower selfing rates would be expected in the island populations. In addition, there was no support for the notion that birds per se promote outcrossing, because there was no link in the total number of birds per population to the outcrossing rates in the five populations.
There is wide support for the notion of birds promoting outcrossing in the Myrtaceae (e.g., Ford, Paton, and Forde, 1979
; Hopper and Moran, 1981
; Sampson, Hopper, and James, 1995
), and in Metrosideros in particular (Carpenter, 1976
; Anderson, 1997
), but there are also exceptions. Outcrossing rates of the bird-pollinated E. rhodantha, for example, were at the lower end of the range found in eucalypts (tm = 0.59–0.67; Sampson and Hopper, 1989
), and this has been attributed to a mixed-mating system with a significant proportion of selfing and inbreeding within small neighbourhoods.
There was no correlation between outcrossing rates and insect abundance, either. Observations showed that high numbers of native, solitary bees were visiting pohutukawa flowers on LBI. Although solitary bees stay predominantly on one tree rather than moving between trees (Frankie, Opler, and Bawa, 1976
) and therefore are more likely to effect self- rather than cross-pollination, this was not expressed in the outcrossing rates in this study. It was difficult to estimate the relative contributions of both birds and insects to pollination and outcrossing rates, as these could not be considered separately in the present study.
Quite apart from pollinator abundance, factors such as foraging patterns, flight distances, body size and social hierarchy of pollinators may influence the mating system (Waser, 1982
; Craig, 1985
; Stewart and Craig, 1989
; Karron et al., 1995
). In some insect-pollinated plants, for example, the high interpopulation variation in outcrossing rates can be largely attributed to the behavior of pollinators (Schemske and Lande, 1985
). Tuis, the most nectarivorous of the New Zealand honeyeaters, occupy higher feeding levels in the canopy than bellbirds and stitchbirds (Atkinson and Millener, 1991
). In addition, the two smaller honeyeater species are regularly chased by tuis (Rasch and Craig, 1988
), and thus could enhance outcrossing. These examples show that specific pollinator characteristics may determine plant-pollinator relationships in pohutukawa. This also suggests that a detailed study on pollination ecology would help to elucidate the complex interactions underlying the lack of correlation of outcrossing rates and pollinator abundance reported here.
However, outcrossing rates are not only a consequence of pollinator activity, but are a complex response to a range of demographic and genetic factors. Forest fragmentation reduces the size and increases the spatial isolation of plant populations. Although this may result in a decrease in heterozygosity due to higher levels of inbreeding (Barrett and Kohn, 1991
; Young, Boyle, and Brown, 1996
), there are exceptions. In Eucalyptus pulverulenta and E. argutifolia (Peters, Lonie, and Moran, 1990
; Kennington and James, 1997
), small population size was not linked to higher levels of selfing. Outcrossing rates in the pohutukawa populations we studied were low, and the largest population by far, on Little Barrier Island, showed similar levels of outcrossing to the remaining populations.
The frequency of outcrossing is the most important determinant of the distribution of genetic diversity within and among populations (Hamrick and Godt, 1990
; Barrett and Harder, 1996
). The mating system of Metrosideros polymorpha, the dominant tree species endemic of the Hawaiian islands, has been broadly characterized as allogamous, and pollination is accomplished by birds, insects, and wind. The distribution of allozyme variation in this common species indicated that genetic diversity is comparable, if not higher, than found in other allogamous tree species and that there is very little interpopulation differentiation along altitudinal gradients (Aradhya, Mueller-Dombois, and Ranker, 1993
). A comparative study of the genetic differentiation in Metrosideros polymorpha and M. excelsa would be interesting, as their contrasting demographic characteristics may relate to their respective breeding system.
An important genetic factor with the potential to strongly influence the mating system of plants is self-fertility. Controlled pollination experiments on pohutukawa have shown that the ability of trees to produce seeds upon self-pollination is variable, and the species may be composed of self-compatible and incompatible individuals (Schmidt-Adam, Gould, and Murray, 1999
). Low estimates of multilocus outcrossing rates in some populations, such as TP (tm = 0.22), could therefore be a reflection of a high proportion of self-compatible trees in those populations. This illustrates that self-incompatibility could be an important factor influencing outcrossing rates for species with a variable degree of self-compatibility.
Conclusions and implications for conservation
The results of this study show the contribution of the mating system of pohutukawa to the survival of the species in the wild. Overall, the reproductive strategy of the species could be labelled "wasteful but sufficient". The species is primarily a selfer, as mass-flowering allows a substantial amount of geitonogamous selfing. There is a large overall output of selfed seeds in each tree per season, although self-incompatiblity of individual trees may reduce this number considerably. Selection eliminates a large proportion of the selfed progeny from populations and ensures highly heterozygous adult populations. Furthermore, despite high rates of selfing, the absolute number of outcrossed seeds per tree is very large and sufficient to ensure the survival of the species.
The finding that the shift from native to predominantly introduced pollinators did not have a measurable impact on outcrossing rates shows the limited influence of pollinators on the mating system in pohutukawa. This apparent ability of the species to use a wide range of pollinators renders the species largely resistant to shifts in the suite of local pollinators that are often associated with habitat degradation. From a conservation perspective this also means that increased selfing cannot explain the poor regeneration of pohutukawa on the mainland, and we must look elsewhere for the underlying causes of the continued decline of the species on the mainland.
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FOOTNOTES |
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4 Author for correspondence (e-mail: g.schmidt-adam{at}massey.ac.nz
).
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