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Mutualism Disruption Threatens Global Plant Biodiversity: A Systematic Review.

Aslan CE, Zavaleta ES, Tershy B, Croll D - PLoS ONE (2013)

Bottom Line: Extinctions of mutualist partners can create "widow" species, which may face reduced ecological fitness.Hypothetically, such mutualism disruptions could have cascading effects on biodiversity by causing additional species coextinctions.Although uncertainty is high, there is evidence that mutualism disruption directly threatens significant biodiversity in some geographic regions.

View Article: PubMed Central - PubMed

Affiliation: Department of Environmental Studies, University of California Santa Cruz, Santa Cruz, California, United States of America.

ABSTRACT

Background: As global environmental change accelerates, biodiversity losses can disrupt interspecific interactions. Extinctions of mutualist partners can create "widow" species, which may face reduced ecological fitness. Hypothetically, such mutualism disruptions could have cascading effects on biodiversity by causing additional species coextinctions. However, the scope of this problem - the magnitude of biodiversity that may lose mutualist partners and the consequences of these losses - remains unknown.

Methodology/principal findings: We conducted a systematic review and synthesis of data from a broad range of sources to estimate the threat posed by vertebrate extinctions to the global biodiversity of vertebrate-dispersed and -pollinated plants. Though enormous research gaps persist, our analysis identified Africa, Asia, the Caribbean, and global oceanic islands as geographic regions at particular risk of disruption of these mutualisms; within these regions, percentages of plant species likely affected range from 2.1-4.5%. Widowed plants are likely to experience reproductive declines of 40-58%, potentially threatening their persistence in the context of other global change stresses.

Conclusions: Our systematic approach demonstrates that thousands of species may be impacted by disruption in one class of mutualisms, but extinctions will likely disrupt other mutualisms, as well. Although uncertainty is high, there is evidence that mutualism disruption directly threatens significant biodiversity in some geographic regions. Conservation measures with explicit focus on mutualistic functions could be necessary to bolster populations of widowed species and maintain ecosystem functions.

No MeSH data available.


Existing widow plants demonstrate reduced reproduction, while threatened vertebrates suggest that many more species may become widowed, especially on islands.a) The extinction of honeycreepers including (i) Hawaii's black mamo (Drepanis funerea) resulted in widowhood for lobelioids including (ii) Cyanea stictophylla[29]. The near extinction of (iii) New Zealand's greater short-tailed bat (Mystacina robusta) widowed (iv) Freycinetia baueriana[30]. The island-scale extinction of (v) the lizard Podarcis lilfordi in the Balearic Islands disrupted the pollination of (vi) Euphorbia dendroides[31]. b) IUCN conservation status rankings for vertebrate pollinators and dispersers reveal that island endemic species (red bars) are more vulnerable by percent threatened than are vertebrate mutualists globally (green bars). Photo/image credits: F. W. Frowahk (Drepanis funerea); C. Aslan (Cyanea stictophylla); B. Duperron (Mystacina robusta); Armchair Travel and Kew Gardens (Freycinetia baueriana); D. André (Podarcis lilfordi); K. Kozminski (Euphorbia dendroides).
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pone-0066993-g004: Existing widow plants demonstrate reduced reproduction, while threatened vertebrates suggest that many more species may become widowed, especially on islands.a) The extinction of honeycreepers including (i) Hawaii's black mamo (Drepanis funerea) resulted in widowhood for lobelioids including (ii) Cyanea stictophylla[29]. The near extinction of (iii) New Zealand's greater short-tailed bat (Mystacina robusta) widowed (iv) Freycinetia baueriana[30]. The island-scale extinction of (v) the lizard Podarcis lilfordi in the Balearic Islands disrupted the pollination of (vi) Euphorbia dendroides[31]. b) IUCN conservation status rankings for vertebrate pollinators and dispersers reveal that island endemic species (red bars) are more vulnerable by percent threatened than are vertebrate mutualists globally (green bars). Photo/image credits: F. W. Frowahk (Drepanis funerea); C. Aslan (Cyanea stictophylla); B. Duperron (Mystacina robusta); Armchair Travel and Kew Gardens (Freycinetia baueriana); D. André (Podarcis lilfordi); K. Kozminski (Euphorbia dendroides).

Mentions: Mutualism disruption has been documented in certain systems, providing a glimpse of its likely implications. Ongoing declines in animal-pollinated or -dispersed plants have been linked to concurrent loss of mutualist animals in Central Africa [72], Tonga [73], and Australia [74], among other locations. These impacts are evident in spite of the higher number of partners per plant that can be expected in continental systems, providing further evidence that mutualism disruption is of global concern. Indeed, the existing data available for our analysis, though limited, imply that the eastern hemisphere (Asia, Africa, and Oceania) as a whole faces particularly high risk of mutualism disruption. Perhaps more intuitively, the “extinction debt” on oceanic islands in particular may be considerable: declines resulting from lost mutualisms, even when leading inevitably to extinction, are likely to be slow because plants are long-lived and many self-pollinate to some degree [75]. A wave of widowhood-induced plant species extinctions appears increasingly likely following the animal extinction pulse driven by European colonization of the world's islands [75], [76]. Recorded reductions in vertebrate-pollinated plant populations on islands are consistent with this hypothesis (Fig. 4) [77], [78].


Mutualism Disruption Threatens Global Plant Biodiversity: A Systematic Review.

Aslan CE, Zavaleta ES, Tershy B, Croll D - PLoS ONE (2013)

Existing widow plants demonstrate reduced reproduction, while threatened vertebrates suggest that many more species may become widowed, especially on islands.a) The extinction of honeycreepers including (i) Hawaii's black mamo (Drepanis funerea) resulted in widowhood for lobelioids including (ii) Cyanea stictophylla[29]. The near extinction of (iii) New Zealand's greater short-tailed bat (Mystacina robusta) widowed (iv) Freycinetia baueriana[30]. The island-scale extinction of (v) the lizard Podarcis lilfordi in the Balearic Islands disrupted the pollination of (vi) Euphorbia dendroides[31]. b) IUCN conservation status rankings for vertebrate pollinators and dispersers reveal that island endemic species (red bars) are more vulnerable by percent threatened than are vertebrate mutualists globally (green bars). Photo/image credits: F. W. Frowahk (Drepanis funerea); C. Aslan (Cyanea stictophylla); B. Duperron (Mystacina robusta); Armchair Travel and Kew Gardens (Freycinetia baueriana); D. André (Podarcis lilfordi); K. Kozminski (Euphorbia dendroides).
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3686776&req=5

pone-0066993-g004: Existing widow plants demonstrate reduced reproduction, while threatened vertebrates suggest that many more species may become widowed, especially on islands.a) The extinction of honeycreepers including (i) Hawaii's black mamo (Drepanis funerea) resulted in widowhood for lobelioids including (ii) Cyanea stictophylla[29]. The near extinction of (iii) New Zealand's greater short-tailed bat (Mystacina robusta) widowed (iv) Freycinetia baueriana[30]. The island-scale extinction of (v) the lizard Podarcis lilfordi in the Balearic Islands disrupted the pollination of (vi) Euphorbia dendroides[31]. b) IUCN conservation status rankings for vertebrate pollinators and dispersers reveal that island endemic species (red bars) are more vulnerable by percent threatened than are vertebrate mutualists globally (green bars). Photo/image credits: F. W. Frowahk (Drepanis funerea); C. Aslan (Cyanea stictophylla); B. Duperron (Mystacina robusta); Armchair Travel and Kew Gardens (Freycinetia baueriana); D. André (Podarcis lilfordi); K. Kozminski (Euphorbia dendroides).
Mentions: Mutualism disruption has been documented in certain systems, providing a glimpse of its likely implications. Ongoing declines in animal-pollinated or -dispersed plants have been linked to concurrent loss of mutualist animals in Central Africa [72], Tonga [73], and Australia [74], among other locations. These impacts are evident in spite of the higher number of partners per plant that can be expected in continental systems, providing further evidence that mutualism disruption is of global concern. Indeed, the existing data available for our analysis, though limited, imply that the eastern hemisphere (Asia, Africa, and Oceania) as a whole faces particularly high risk of mutualism disruption. Perhaps more intuitively, the “extinction debt” on oceanic islands in particular may be considerable: declines resulting from lost mutualisms, even when leading inevitably to extinction, are likely to be slow because plants are long-lived and many self-pollinate to some degree [75]. A wave of widowhood-induced plant species extinctions appears increasingly likely following the animal extinction pulse driven by European colonization of the world's islands [75], [76]. Recorded reductions in vertebrate-pollinated plant populations on islands are consistent with this hypothesis (Fig. 4) [77], [78].

Bottom Line: Extinctions of mutualist partners can create "widow" species, which may face reduced ecological fitness.Hypothetically, such mutualism disruptions could have cascading effects on biodiversity by causing additional species coextinctions.Although uncertainty is high, there is evidence that mutualism disruption directly threatens significant biodiversity in some geographic regions.

View Article: PubMed Central - PubMed

Affiliation: Department of Environmental Studies, University of California Santa Cruz, Santa Cruz, California, United States of America.

ABSTRACT

Background: As global environmental change accelerates, biodiversity losses can disrupt interspecific interactions. Extinctions of mutualist partners can create "widow" species, which may face reduced ecological fitness. Hypothetically, such mutualism disruptions could have cascading effects on biodiversity by causing additional species coextinctions. However, the scope of this problem - the magnitude of biodiversity that may lose mutualist partners and the consequences of these losses - remains unknown.

Methodology/principal findings: We conducted a systematic review and synthesis of data from a broad range of sources to estimate the threat posed by vertebrate extinctions to the global biodiversity of vertebrate-dispersed and -pollinated plants. Though enormous research gaps persist, our analysis identified Africa, Asia, the Caribbean, and global oceanic islands as geographic regions at particular risk of disruption of these mutualisms; within these regions, percentages of plant species likely affected range from 2.1-4.5%. Widowed plants are likely to experience reproductive declines of 40-58%, potentially threatening their persistence in the context of other global change stresses.

Conclusions: Our systematic approach demonstrates that thousands of species may be impacted by disruption in one class of mutualisms, but extinctions will likely disrupt other mutualisms, as well. Although uncertainty is high, there is evidence that mutualism disruption directly threatens significant biodiversity in some geographic regions. Conservation measures with explicit focus on mutualistic functions could be necessary to bolster populations of widowed species and maintain ecosystem functions.

No MeSH data available.