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Life-History Characters and Phylogeny Are Correlated with Extinction Risk In Journal of Biogeography (J. Biogeogr.) (2006) 33, 271–290 ORIGINAL Life-history characters and phylogeny are ARTICLE correlated with extinction risk in the Australian angiosperms A. Sjo¨stro¨m1 and C. L. Gross2* 1School of Mathematics, Statistics and ABSTRACT Computing Science and 2Ecosystem Aim To determine whether life-history characters that affect population Management, School of Environmental Sciences and Natural Resources Management, persistence (e.g. habit and life span) and those that influence reproductive University of New England, Armidale, NSW, success (e.g. sexual system and fruit type) are non-randomly correlated with Australia extinction risk (i.e. threat category) in the Australian flora (c. 19,000 species, of which c. 14% is threatened). To identify patterns that present useful conservation directions. To understand patterns of extinction risk in the Australian flora at a broad scale. Location Continental Australia. Methods A country-wide exploration of four life-history characters in the Australian flora (n ¼ 18,822 species) was undertaken using reference texts, expert opinion, herbarium records and field work. For each character and threat- category combination, a G-test (using a log-linear model) was performed to test the null hypothesis that the two factors were independent in their effects on count. A generalized linear model (GLM) with a logit link and binomial error distribution was constructed with the proportion of taxa in each extinction risk category as the response variable and the habit, sex and fruit-type characters as explanatory terms. In a separate approach, we investigated patterns across the threat categories of non-endangered extant, endangered, and extinct using a multinomial model. We examined whether or not species-poor genera were more likely to contain threatened or extinct species than species-rich genera. A GLM with a binomial error distribution and logit link function was constructed to obtain a weighted regression on the proportion of species listed as extinct or endangered within a genus versus the log of the size of the genus. We also used a supertree analysis and character tracing to investigate the role of phylogeny on extinction risk. Results We found that the Australian flora is primarily composed of bisexual shrubs with dry-dehiscent fruits. Dioecious breeding systems (separate female and male flowers on separate plants) in many floras are the predominant unisexual system, but in Australia there are unexpectedly high levels of monoecy (separate female and male flowers on the same plant). Within the extinct data set of 31 species we detected a significant departure from that expected for habit but not for life span, sexual system or fruit type. There are significantly fewer trees on the extinct list than expected. This may reflect the greater resilience of trees than of *Correspondence: C.L. Gross, Ecosystem Management, School of Environmental Sciences other growth habits to extinction processes as well as the observation time-frame. and Natural Resources Management, University Within the endangered data set of 450 species we found significant differences in of New England, Armidale, NSW, 2351, the representation of the observed characters from that expected within sex Australia. systems and fruit types. We show that, depending on the life form, unisexual E-mail: [email protected] breeding systems can be significantly and positively associated with endangered These authors contributed equally to this work. species compared with non-threatened species. For example, there are more ª 2006 The Authors www.blackwellpublishing.com/jbi 271 Journal compilation ª 2006 Blackwell Publishing Ltd doi:10.1111/j.1365-2699.2005.01393.x A. Sjo¨ stro¨ m and C. L. Gross monoecious species than expected by chance among the tree species listed as endangered but fewer among the herbaceous life forms. Threat category was found to be non-randomly clustered in some clades. Main conclusions Life-history characters in certain combinations are predictive of extinction risk. Phylogeny is also an important component of extinction risk. We suggest that specific life-history characters could be used for conservation planning and as an early warning sign for detecting vulnerability in lists of species. Keywords Australia, correlated evolution, extinction risk, flora, fruit types, genus size, life- history characters, phylogenetic analyses, sex systems. vascular species yet the abundance and distribution of INTRODUCTION fundamental life-history characters, such as those that affect There are many different types of events that can increase population persistence (e.g. habit and life span) and those that extinction risks in species; for example, fragmentation has influence reproductive success (e.g. sexual system and fruit multiple effects on ecosystems (Laurance et al., 2002) and is a type), are poorly known on a continental basis. Such data, if key factor worldwide that can prematurely halt population available, could be used to examine the general occurrence of persistence. However, it is not always that a species was just in patterns of rarity in the flora. There is certainly a need for a the wrong place at the wrong time – even related species in the broad approach as the estimate for the number of threatened same landscape can differ in their resilience to perturbations vascular plants in Australia is alarmingly high at 14.4% (Walter (e.g. Bertya ingramii versus B. rosmarinifolia, Scott & Gross, & Gillett, 1998). 2004). Are there inherent properties in species that predispose Establishing the abundance and distribution of life-history them to vulnerability or resilience? A broad approach to characters for an entire flora is a challenge, yet knowledge of address this question is to determine whether or not there are these properties at such a broad and inclusive scale could be a specific traits clustered with the state of extinction risk. powerful tool for conservation planning. As a starting point we Increasingly this approach is being used to evaluate the undertook a study of the distribution of four life-history properties of rarity and speciosity geographically or within characters that we consider fundamental to all species. These lineages (e.g. Hegde & Ellstrand, 1999; Rey Benayas et al., characters were habit, life span, sex system and fruit type, and 1999; Edwards & Westoby, 2000; Murray et al., 2002a,b; they were examined for Australian recently extinct and Golding & Hurter, 2003) in an attempt to forecast the types of endangered angiosperms and for the Australian flora as a species that may be vulnerable to extinction. The evolutionary whole. Habit (i.e. life form) has been linked to increased significance of trait clustering can also be examined using extinction risk in several floras (Robinson et al., 1994; Turner correlation tests of life-history characters against ecological et al., 1996; Hegde & Ellstrand, 1999; Rogers & Walker, 2002) parameters (e.g. Chazdon et al., 2003). However, seldom is and it is intricately linked with life span (Garcia, 2003). Sex there a comprehensive data set that covers whole continents system can also be associated with elevated extinction risks, (see later). Consequently an overall appraisal of extinction risk particularly for unisexual species. For example, Vamosi & is mostly lacking at continental scales. In most floras, for Vamosi (2005) found that dioecious species experience higher example, so little is known about the distribution of life- extinction rates and (or) lower speciation rates compared with history characters on a continental scale that partial data sets non-dioecious sister groups. They also found that the woody (e.g. a clade, Murray et al., 2002a) are used instead, with the growth habit is probably a contributing factor to the higher added power of phylogenetic analyses in some cases (e.g. incidence of dioecious species being at risk of extinction but Murray et al., 2002b; Murray & Lepschi, 2004). Biogeographi- that the character was not solely responsible for the pattern. cal attributes such as habitat type may also be important Certain fruit types can be non-randomly associated with rare predictors of increased extinction risk; however, our initial species (Hegde & Ellstrand, 1999) too, and as fruit type can be focus is at the Australia-wide scale and on whether or not there correlated with sex system and habit (reviewed in Gross, 2005) are life-history attributes correlated with increased extinction fundamental life-history characters such as habit, life span, sex risks. system and fruit type should not be examined in isolation from Perhaps the predominance of a life-history character (e.g. each other. habit) is skewed in abundance in both threatened species and We use the information on life-history characters to describe the greater population – it is difficult to resolve when data on first the composition of the Australian flora and then patterns the greater population are unavailable. The Australian vascular in trait distribution. Next we determine the utility of flora presents a challenge in this area: there are at least 19,000 taxon richness as a predictor of extinction (see Schwartz & 272 Journal of Biogeography 33, 271–290 ª 2006 The Authors. Journal compilation ª 2006 Blackwell Publishing Ltd Life-history characters in the Australian flora Simberloff, 2001). Finally we compare our results for the No additional checking was performed on the validity of Australian continent with other regions and provide informa- membership on the endangered list except
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