The Ecology of Plant Extinction: Rates, Traits and Island Comparisons

The ecology of plant extinction: rates, traits and island comparisons

A LAN G RAY

Abstract Although there is increasing evidence for a sixth it uses rigorously applied and standardized criteria. IUCN mass extinction, relatively few plants have been officially de- defines the category Extinct as when ‘there is no reasonable clared extinct (, are categorized as Extinct on the IUCN doubt that the last individual has died’ (IUCN, ). There Red List). The Red List, although the data are neither perfect is uncertainty surrounding documented plant extinctions nor comprehensive, is perhaps the most reliable indicator of (Vellend et al., ) and there can be costs associated extinction and extinction threat. Here, data collated from with misclassifying extinct species (Akçakaya et al., ). the Red List, of Extinct plant species and of Critically Akçakaya et al. () and Keith et al. () suggest setting Endangered plant species with populations in decline, are thresholds for the probability of extinction and to classify examined to address three questions: () How do back- species as extinct, possibly extinct, and extant. The Red ground, continental, and island plant extinction rates com- List data are therefore neither perfect nor comprehensive pare? () Are biological and physical island parameters (many taxa have not been assessed) but the List is neverthe- associated with plant extinction? () Are any plant traits less widely regarded as the best indicator of the degree of associated with extinction and if so do these differ between extinction of individual species. Here, data collated from islands and continents? The background rate for plant the publicly available Red List, of Extinct plant species and extinction is estimated to be .–. E/MSY (extinctions of Critically Endangered plant species with populations in per million species-years) and the Red List data are above decline, are examined to address three questions: ()How these background rates and also above a higher extinction do background, continental, and island plant extinction rate of . E/MSY. The data indicate that plant extinctions rates compare? () Are biological and physical island para- are dominated by insular species. The Red List extinction meters associated with plant extinction? () Are any plant data are associated with lower competitive ability and traits associated with extinction and if so do these differ lower climate change velocities, and anthropogenic factors. between islands and continents? Analyses using only Critically Endangered species whose Data for extinct species were retrieved from the Red List populations are in decline (arguably the species most at (IUCN, ). A Critically Endangered subset of species was risk of extinction in the near future) largely mirrors this pat- also selected, including only those with a population trend tern and suggests that drivers of plant extinction may have categorized as declining. These latter data were used as in- an inertia that could last well into the future. dicators of species that potentially could become extinct in the near future and are therefore likely to be indicative of Keywords Botany, climate change, conservation, endemic ongoing extinction processes. Extinction date can be diffi- species, extinctions, islands, plants, red list cult to determine. We therefore used the date last seen, re- The supplementary material for this article is available at trieved from the Red List and spanning –, for our https://doi.org/./S analysis. If a date was absent from the Red List, floras, herb- aria databases, specimens and other sources were checked. Evidence is growing for a sixth mass extinction in the These sources were also used to compile plant traits. The Anthropocene (Ceballos et al., ) but for plants relatively number of extinctions were summed per year, plotted as few species have been officially declared extinct, with ,  the cumulative proportion of all species assessed against on the IUCN Red List of Threatened Species (IUCN, ). time (cf. Ceballos et al., ), and compared with an esti- More than , plants are estimated to be under threat mated background rate for plant extinction of .–. E/ (Kew, ) but it can take many years for a plant species MSY (i.e. . extinctions per million species-years; Levin & to become extinct even when populations are functionally Wilson, ; Stanley, ; De Vos et al., ; Vellend et al., extinct (Cronk, ), suggesting a massive extinction debt ) and a high background rate of . E/MSY (Pimm (Hanski, ; Kuussaari et al., ; Gilbert & Levine, et al., ). ). The Red List (IUCN, ) is perhaps the most reli- Islands are often considered discrete crucibles of evolu- able indicator of extinction and extinction threat because tion, and can form useful case studies because of their dis- tinct boundaries. To determine whether abiotic and/or biotic parameters are associated with extinction a number ALAN GRAY NERC Centre for Ecology and Hydrology, Bush Estate, Penicuik, Midlothian EH26 0QB, UK. E-mail [email protected] of islands datasets were combined and analysed (UNEP,    Received  September . Revision requested  November . ; Weigelt & Kreft, ; Gray & Cavers, ; Weigelt Accepted  February . First published online  May . et al., ). These data were collated to test for differences

Oryx, 2019, 53(3), 424–428 © 2018 Fauna & Flora International doi:10.1017/S0030605318000315 Downloaded from https://www.cambridge.org/core. IP address: 170.106.35.234, on 29 Sep 2021 at 23:57:45, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318000315 Ecology of plant extinction 425

TABLE 1 Parameters potentially associated with extinction of plant species on islands (data from the IUCN Red List, ), with median values for islands where species extinction has occurred and for islands where no extinction has been recorded, and separately for the subset of plant species that are categorized as Critically Endangered and have declining populations, with results of the asymptotic Kruskal-Wallis test for islands with and without extinctions and for islands on which Critically Endangered species are present or absent.

Parameter All species Critically Endangered species Extinction No extinction P Present Absent P Invasive species index1,a 32 0.001 320.01 Human impact2,a 10.0 4.0 0.01 8.5 4.0 0.02 Human population density (per km)a 43.8 3.5 0.02 54.1 3.2 0.02 Growth rate3,a 1.2 1.6 . 0.05 1.2 1.5 . 0.05 % of population in agriculture4,a 20.0 17.0 . 0.05 19.5 17.0 . 0.05 Gross Domestic Product5,a 1,600 630 . 0.05 843 629 . 0.05 Area (km2)b 439 46 ,0.001 1.77 5.80 ,0.001 6,b ,0.001 . Climate change velocity in temperature (m/yr; log10) 2.04 5.65 1501.60 4.06 0.05 Elevation (m)b 768 323 ,0.001 1394 13 . 0.05 Isolation distance (km)7,b 1,868.0 50.5 ,0.001 550.7 50.5 . 0.05 Total annual precipitation (mm)b 2,361 1,374 ,0.001 1721 1191 . 0.05 Coefficient of variation of total annual precipitationb 28 36 0.02 36.5 40 . 0.05 Surrounding landmass proportion8,b 0.11 0.02 0.01 0.51 1.17 . 0.05 No. of species per km2,b 0.46 2.54 ,0.001 0.39 2.74 . 0.05 Mean annual temperature (°C)b 24.0 23.3 0.02 23.8 11.0 . 0.05 Mean annual temperature range (°C)b 11.6 13.1 0.04 12.4 19.6 . 0.05

 Numerical indicator based on the number and threat of invasive species (UNEP, ); , few or no introductions; , some introductions (e.g. rats, common weeds); , common domestic introductions (e.g. dogs, cats, pigs); , some problems with invasive species; , major problems with invasive species; , deva- stated by invasive species.  Human Impact Indicator calculated according to island population density, growth rate and level of tourism.  Annual population growth rate: ,, decreasing; –%, stable; –%, increasing slowly; –%, increasing; .%, increasing rapidly.  Percent of the population occupied in agriculture.  Gross Domestic Product per capita (USD).  An index of temperature change derived from spatial temperature gradients and multimodel forecasts of temperature increase rates for the st century, representing the instantaneous local velocity along Earth’s surface needed to maintain constant temperatures (Loarie et al., ).  Shortest distance from an island to the nearest mainland.  The proportion of landmass surrounding each island in distance classes up to , km radius, multiplied by –. aUNEP (). bWeigelt et al. (), Weigelt & Kreft ().

between islands where extinction has occurred and those (Vellend et al., ), these findings are of concern because where it has not been recorded (Table ). As the data did estimated single island endemic speciation rates (Gray & not satisfy the assumptions of parametric statistical methods Cavers, ) are only slightly above a background extinction a non-parametric approach was adopted for examining dif- rate of . E/MSY. The data for extinct species and island ferences in these parameters between islands where extinc- physical and biological datasets suggest that lower competi- tion or Critically Endangered species occur and islands tive ability and climate change velocities, and anthropogenic where extinctions or Critically Endangered species are factors, may be associated with extinction events (Table ). absent, using asymptotic Kruskal-Wallis tests in Rv... Islands with known plant extinctions have higher human (R Development Core Team, ) using the package coin population densities, greater anthropogenic impacts and a (Hothorn et al., ). higher invasive species index (Table ). Where plant extinc- Extinction rates for plants are above both a background tions have occurred, islands appear to have higher mean rate of .–. E/MSY and above a higher background temperatures but less temperature variability, higher precipi- rate of . E/MSY (Fig. ). This pattern is evident using ei- tation but less variability, higher elevation, are more isolated, ther the full list of extinct plant species (including species as- and are larger in area, but have a lower surrounding land- sessed using versions of the IUCN Red List prior to the mass proportion and lower climate change velocities adoption of the current v. . Red List categories; IUCN, (Table ). Although these data need to be interpreted cau- ) and only those species assessed using the v. . criteria. tiously as the overlap between the UNEP () island data- The data also indicate that plant extinctions are dominated base and those islands on the Red List is low (e.g. only  by species loss from islands (Fig. ). Although speciation islands of the  listed on the UNEP list have extinction could potentially increase during the Anthropocene events for human impact), the results are as expected.

FIG. 1 Plant extinction rates for global, island and continental areas during –  compared to a high background rate of . extinctions per , species per  years (. E/MSY) for: (a) all species in the Red List (IUCN, ), including those categorized prior to v. . of the Red List criteria (IUCN, ), and (b) only those species categorized using v. . of the Red List criteria.

Repeating these analyses for Critically Endangered spe- plant list is dominated by trees, and thus the traits for extinc- cies whose populations are in decline largely mirrors this tion are also biased towards trees. That the majority (%) of pattern, suggesting that drivers of plant extinctions may Critically Endangered plants that have declining popula- have an inertia that could last well into the future tions largely mirror these patterns and that most are from (Table ). Islands where Critically Endangered species forests should still be a concern despite this bias with declining populations occur also seem to be associated (Supplementary Table ). However, the domination of the with lower climate change velocities (Table ). This may be list by forest species also suggests a significant gap in our un- an intrinsic vulnerability of species that have evolved in eco- derstanding of plant extinction. Lastly, irregular floral sym- systems buffered from climate variability, and when climate metry appears to be more associated with Critically does change (even at low velocity), these species could be Endangered plants that have declining populations, in con- particularly maladapted. In addition, low velocity anthropo- trast to extinct species. genic climate change may still be high velocity with respect If we assume that Fig.  is indicative of the extinction pro- to natural climate change because anthropogenic climate cesses happening to all plants globally, this increases the evi- change is additional to natural change. Where extinction dence for a sixth mass extinction. Additionally, we know has occurred on islands, overall species richness also ap- these are underestimates and there may be extinction debt pears to be lower, suggesting that insular species may have and lag periods to extinction (Hanski, ; Kuussaari evolved in less competitive environments, perhaps leading et al., ; Gilbert & Levine, ; Cronk, ). Our ac- to a predisposition to be vulnerable to invasive species. tions are resulting in non-random extinction patterns at That climate variables can be associated with island extinc- an increasing rate, are affecting islands disproportionately, tions is potentially of concern. and are likely to be exacerbated by climate change. A number of characteristics or traits, such as an epiphytic The main drivers of plant extinction are known (habitat lifestyle, floral symmetry, biotic pollination, breeding system loss, invasive species and climate change) but nevertheless type, flowering period, seed production and ploidy level, extinctions continue. There are many initiatives to conserve have been linked to an elevated risk of plant extinction plant biodiversity, including the Global Strategy for Plant (Kew, ). However, it is unclear whether these patterns Conservation (CBD, ), and, although deforestation are universal, as data for most species traits have yet to be rates are high, they are decreasing (MacDicken et al., combined on a global scale. The trait data for the Red List ). If the data presented here are indicative, environ- are of a broadly similar pattern for islands and continents, ments that are species poor and have low climate change vel- and indicate that most plant extinctions have been of woody ocity may indicate increased likelihood of extinction. On perennials that relied on biotic pollination and dispersal, islands and where populations are small and comprise spe- produced fruit with few seeds, and possessed symmetrical cies with small and decreasing gene pools, techniques such flowers (Supplementary Table ). Perhaps the clearest find- as genetic rescue are likely to be required to address pro- ing is that the majority of extinct plants are associated with blems such as inbreeding depression (Cronk, ; Gray forest habitats. Given deforestation rates throughout the et al., ). Accordingly, it is going to be increasingly im- modern era (considered here as post ) this may not be portant to find effective ways of identifying and conserving surprising. However, the Red List is not exhaustive and may plant genetic diversity. The genomes of rare plants could be be taxonomically and/or geographically biased, and the sequenced to understand and address the genetic problems

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