Abstract
An understanding of rarity can provide important insights into evolutionary processes, as well as valuable information for the conservation management of rare and threatened species. In this research, my main objective was to gain an understanding of the biology of rarity by investigating colonization and extinction processes from an ecological and evolutionary perspective. I have focused on the genus Persoonia (family Proteaceae), because these plants are prominent components of the Australian flora and the distributional patterns of species vary dramatically, including several that are listed as threatened. The approach I have taken was first to define the level of commonness/rarity for all species and subspecies in the genus across Australia, in order to identify potential patterns in the traits of common and rare taxa (all termed species herein). From this set of species, the subsequent research was based on two pairs (one common and one rare species in each pair) of closely related, obligate seeding Persoonia species: P. mollis subspecies nectens (common pair 1) and P. mollis subspecies maxima (rare pair 1) and P. lanceolata (common pair 2) and P. glaucescens (rare pair 2). In this research, I investigated population genetics, pollination and seed dispersal to identify consistent differences between the common and rare species in the ecological processes influencing colonization and extinction. Few robust definitions of rarity enable unambiguous comparative investigations of these processes. I defined rarity using three different methods, and classified Persoonia species into three levels of rarity (common, intermediate, rare). There was no association between rarity and either taxonomic status or geographical distribution, but several environmental (rainfall, temperature and elevation) and life-history (resprouting ability and plant size) traits differed significantly between common and rare species. These results suggest that the common species have a greater ability to persist in often harsh landscapes, being able to resprout after disturbance and tolerate severe environmental conditions. Of the taxa examined in detail, local abundance was related to distribution patterns, as the rare species tended to have fewer plants within a patch than more common species. The current distribution of Persoonia species in the Sydney region appears to reflect historical patterns rather than recent effects of fragmentation. Theory predicts that genetic variation is important for long-term persistence of populations, and that the abundance and distribution of variation is strongly dependent on genetic drift and gene flow. Small, isolated populations are therefore expected to be less diverse and more differentiated than large, inter-connected populations. Thus, rare species may be more at risk from inbreeding depression, leading to extinction. I used 389 putative AFLP loci to compare genetic variation and structuring in the two common-rare pairs of closely related species. I genotyped 15-22 adult plants, from each of the four populations, covering the geographic range of each species. Although genetic variation was low for all four species (compared to the average for long-lived outcrossing perennials), I found significantly more variation within populations of the rare species than the common species (percentage polymorphism = 61.3, 61.0 cf. 54.5, 53.2; expected heterozygosity = 0.170, 0.148 cf. 0.124, 0.128; Shannon's I = 0.239, 0.216 cf. 0.182, 0.186). My AMOVA revealed significant levels of structure both among species (21percent) and populations (15percentage), although the proportion of inter-population variation within species did not vary consistently with rarity (Pair 1 - rare 21.1 percentage cf. common 16.5 percentage; Pair 2 - rare 15.8 percentage cf. common 20.6 percentage). I detected more differentiation between populations of the rare species than the common species (controlled for the level of geographic separation), suggesting greater gene flow between populations of the common species. Even relatively small populations of rare species were more diverse than large populations of common Persoonia species. Understanding the interactions between breeding systems and pollination ecology may enable some prediction of the consequences of rarity. Using a comparative approach, I tested whether rarity is associated with aspects of reproductive biology in the two species pairs. This study focused on natural ecosystems in Australia, which have been recently affected by changes in fire regimes, especially over the past 200 years of European settlement, and by the introduction of European honeybees (Apis mellifera). In populations of the common species, more than 35% of flowers matured fruits compared to less than 20% of flowers in the rare species. All species were obligate outcrossers in each of the study populations, but only the two rare species were pollen-limited (lack of compatible pollen), with significantly lower fruit-set on open-pollinated flowers than on those cross-pollinated by hand (mean plus or equal to SE; 0.18 plus or equal to 0.02 vs. 0.42 plus or equal to 0.05; P less than 0.001). Native bees (mostly Leioproctus species) and introduced honeybees (Apis mellifera) visited flowers of all species. The native bees visited fewer flowers within a plant and moved greater distances between plants than honeybees, so the native bees are expected to be more effective in promoting outcrossing. While honeybees were the most frequent visitors to flowers of all species, native bees made more visits to the common than the rare species (number of visits/10min; 0.65 plus or equal to 0.20 vs. 0.20 plus or equal to 0.09). These results suggest that the poorer reproductive success in the rare Persoonia species was associated with lower pollinator effectiveness. If seed dispersal and seed predation influence distribution and abundance, rare species may be expected to have lower rates of seed removal and/or higher levels of seed predation than common congeners. I compared post-dispersal seed removal and seed predation in the two species pairs in two populations of each species. Population size differs between common and rare species, so I also compared seed removal and predation in both small and large populations of the common P. lanceolata. Seed removal over a four-week period by macropods was significantly greater in populations of the two common species (greater than 50% seeds/plant) than in their rare congeners (less than 25%). There was no overall effect of rarity on seed predation by rodents, but significantly more seeds of the rare P. mollis subspecies maxima were eaten than those of the other three species. There was a significant effect of rarity on seed removal. High levels of seed removal were sustained in both small and large populations of the common P. lanceolata, suggesting that population size may not be contributing to the differences between these common and rare species. Therefore, limited seed dispersal could be a potential cause of rarity in Persoonia. In this research, I identified some important similarities and differences between common and rare Persoonia species, which provide insights into the processes currently shaping their distribution and abundance. I found that the ability of plants to resprout after fire is associated with commonness/rarity, with rare species generally reliant on seeds to re-establish. Some common species are also unable to resprout, but they appear to have a greater ability to disperse pollen and seed. Rare species harbour greater levels of genetic variation within populations than common congeners. Despite these consistent differences detected between closely related common and rare species, it is difficult to distinguish whether they are causes and/or consequences of rarity. In fact, the current processes influencing the ability of plants to persist and disperse are likely to differ from those operating in historic times due to anthropogenic disturbances, including habitat fragmentation and the introduction of honeybees. While herbarium records and genetic markers give some indication that rare species are likely to have historically restricted distributions and common species appear to have rapidly colonized the landscape since the last glacial maximum, a detailed phylogeographic investigation is required to fully unravel the historic patterns. These findings have important implications for the management of rare and threatened species. Firstly, the species identified here as rare should all be assessed for risk of extinction and considered for listing under national and state legislation, as they may be susceptible to the negative effects of stochastic demographic and genetic processes. Secondly, most of the species currently listed as threatened are unable to resprout after fire, and therefore may be less persistent in the landscape and susceptible to localized extinction from frequent fire events. The ability to resprout after fire should be determined for all Persoonia I classified as rare. Thirdly, rare obligate seeders may have a reduced ability to colonize surrounding available habitat than common species, but existing populations appear to have maintained genetic variation. Therefore, all populations of rare obligate seeding Persoonia species should be of high conservation priority and efforts should focus on preserving these populations in the wild.
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Claims 20
Claim · model-written summary
Rarity was unrelated to taxonomic status or geographical distribution.
Not reportedTaxon
Verbatim
e0“There was no association between rarity and either taxonomic status or geographical distribution”
Claim · model-written summary
Rainfall, temperature and elevation differed significantly between common and rare species.
Not reportedTaxon
Verbatim
e0“several environmental (rainfall, temperature and elevation) and life-history (resprouting ability and plant size) traits differed significantly between common and rare species”
Claim · model-written summary
Resprouting ability and plant size differed significantly between common and rare species.
Not reportedTaxon
Verbatim
e0“life-history (resprouting ability and plant size) traits differed significantly between common and rare species”
Claim · model-written summary
Rare species tended to have fewer plants per patch than common species.
Verbatim
e0“the rare species tended to have fewer plants within a patch than more common species”
Claim · model-written summary
Current Sydney region distributions appear to reflect historical patterns more than recent fragmentation.
- Outcome
- current distributione0
- Qualifier
- appears to reflect historical patterns rather than recent effects of fragmentatione0
- Setting
- Sydney regione0
PersooniaOrganisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“The current distribution of Persoonia species in the Sydney region appears to reflect historical patterns rather than recent effects of fragmentation.”
Claim · model-written summary
Genetic variation was low in all four species.
Verbatim
e0“genetic variation was low for all four species (compared to the average for long-lived outcrossing perennials)”
Claim · model-written summary
Rare species had significantly greater within-population genetic variation than common species.
Verbatim
e0“significantly more variation within populations of the rare species than the common species (percentage polymorphism = 61.3, 61.0 cf. 54.5, 53.2; expected heterozygosity = 0.170, 0.148 cf. 0.124, 0.128; Shannon's I = 0.239, 0.216 cf. 0.182, 0.186)”
Claim · model-written summary
Genetic structure was significant among species at 21percent.
Verbatim
e0“significant levels of structure both among species (21percent) and populations (15percentage)”
Claim · model-written summary
Genetic structure was significant among populations at 15percentage.
Verbatim
e0“significant levels of structure both among species (21percent) and populations (15percentage)”
Claim · model-written summary
Interpopulation variation did not vary consistently with rarity across the two species pairs.
Verbatim
e0“the proportion of inter-population variation within species did not vary consistently with rarity (Pair 1 - rare 21.1 percentage cf. common 16.5 percentage; Pair 2 - rare 15.8 percentage cf. common 20.6 percentage)”
Claim · model-written summary
Rare species showed greater differentiation between populations than common species after accounting for geographic separation.
Verbatim
e0“more differentiation between populations of the rare species than the common species (controlled for the level of geographic separation)”
Claim · model-written summary
Common species had fruit maturation above 35%, versus below 20% in rare species.
Verbatim
e0“In populations of the common species, more than 35% of flowers matured fruits compared to less than 20% of flowers in the rare species.”
Claim · model-written summary
All studied species were obligate outcrossers.
Verbatim
e0“All species were obligate outcrossers in each of the study populations”
Claim · model-written summary
Only rare species were pollen-limited, with lower open-pollinated fruit set than hand-crossed fruit set.
Verbatim
e0“only the two rare species were pollen-limited (lack of compatible pollen), with significantly lower fruit-set on open-pollinated flowers than on those cross-pollinated by hand (mean plus or equal to SE; 0.18 plus or equal to 0.02 vs. 0.42 plus or equal to 0.05; P less than 0.001)”
Claim · model-written summary
Native bees and introduced honeybees visited flowers of all species.
- Taxon
- speciese0
- Interactor
- Native beese0pollinator
- Second interactor
- honeybees
_Apis_mellifera_(female)_-_on_viburnum_tinus_flowers.jpg?width=60)
Apis melliferae0pollinator - Outcome
- visited flowerse0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
_Apis_mellifera_(female)_-_on_viburnum_tinus_flowers.jpg?width=500)
Verbatim
e0“Native bees (mostly Leioproctus species) and introduced honeybees (Apis mellifera) visited flowers of all species.”
Claim · model-written summary
Native bees visited fewer flowers per plant and moved farther between plants than honeybees.
- Interactor
- native beese0pollinator
- Outcome
- flowers within a plant and moved greater distances between plantse0
- Direction
- fewere0
- Comparator
- honeybeese0
Not reportedTaxon
Verbatim
e0“The native bees visited fewer flowers within a plant and moved greater distances between plants than honeybees”
Claim · model-written summary
Native bees visited common species more often than rare species.
Verbatim
e0“native bees made more visits to the common than the rare species (number of visits/10min; 0.65 plus or equal to 0.20 vs. 0.20 plus or equal to 0.09)”
Claim · model-written summary
Macropod seed removal exceeded 50% in common species and was below 25% in rare congeners.
Verbatim
e0“Seed removal over a four-week period by macropods was significantly greater in populations of the two common species (greater than 50% seeds/plant) than in their rare congeners (less than 25%).”
Claim · model-written summary
Rodent seed predation had no overall rarity effect, but rare P. mollis maxima seeds were eaten more than seeds of the other three species.
- Taxon
- P. mollis subspecies maxima
Persoonia mollise0 - Outcome
- seedse0
- Direction
- moree0
- Comparator
- other three speciese0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“There was no overall effect of rarity on seed predation by rodents, but significantly more seeds of the rare P. mollis subspecies maxima were eaten than those of the other three species.”
Claim · model-written summary
Authors recommend prioritizing conservation of all rare obligate-seeding Persoonia populations in the wild.
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“all populations of rare obligate seeding Persoonia species should be of high conservation priority and efforts should focus on preserving these populations in the wild”