Mutualism Disruption Threatens Global Plant Biodiversity: A Systematic Review

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.

Figure 1. IUCN Red List threat levels by geographic region.

a) Threat levels for vertebrate seed dispersers. b) Threat levels for vertebrate pollinators. Geographic regions are as provided in the IUCN Red List (www.iucnredlist.org). DD  =  Data Deficient. EW  =  Extinct in the Wild. CR  =  Critically Endangered. EN  =  Endangered. VU  =  Vulnerable. NT  =  Near Threatened. LC  =  Least Concern.

Figure 2. PRISMA flowchart providing the steps of data collection for this systematic review.

Figure 3. A review of pollinator exclusion studies yielded weighted mean seed set reductions for widows previously pollinated by different vertebrate classes.

a) Seed set reductions after bat exclusion for bat-pollinated plants. b) Seed set reductions after nonvolant mammal exclusion for nonvolant mammal-pollinated plants. c) Seed set reductions after bird exclusion for bird-pollinated plants. d) Seed set reductions after lizard exclusion for lizard-pollinated plants. Bars depict weighted means. Vertical lines represent standard error. The minimum seed set observed in any exclusion study is indicated with an asterisk (*); this is the minimum predicted effect of loss of vertebrate pollinators for a given plant species. Bold numbers at the top of each bar provide the number of independent publications used to calculate each weighted mean.

Figure 4. 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 . The near extinction of (iii) New Zealand's greater short-tailed bat (Mystacina robusta) widowed (iv) Freycinetia baueriana . The island-scale extinction of (v) the lizard Podarcis lilfordi in the Balearic Islands disrupted the pollination of (vi) Euphorbia dendroides . 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).