Abstract Island biogeography has classically focused on abiotic drivers of species distributions. However, recent work has highlighted the importance of mutualistic biotic interactions in structuring island floras. The limited occurrence of specialist pollinators and mycorrhizal fungi have been found to restrict plant colonization on oceanic islands. Another important mutualistic association occurs between nearly 15,000 plant species and nitrogen-fixing (N-fixing) bacteria. Here, we look for evidence that N-fixing bacteria limit establishment of plants that associate with them. Globally, we find that plants associating with N-fixing bacteria are disproportionately underrepresented on islands, with a 22% decline. Further, the probability of N-fixing plants occurring on islands decreases with island isolation and, where present, the proportion of N-fixing plant species decreases with distance for large, but not small islands. These findings suggest that N-fixing bacteria serve as a filter to plant establishment on islands, altering global plant biogeography, with implications for ecosystem development and introduction risks.
more »
« less
Mycorrhizal types influence island biogeography of plants
Abstract Plant colonization of islands may be limited by the availability of symbionts, particularly arbuscular mycorrhizal (AM) fungi, which have limited dispersal ability compared to ectomycorrhizal and ericoid (EEM) as well as orchid mycorrhizal (ORC) fungi. We tested for such differential island colonization within contemporary angiosperm floras worldwide. We found evidence that AM plants experience a stronger mycorrhizal filter than other mycorrhizal or non-mycorrhizal (NM) plant species, with decreased proportions of native AM plant species on islands relative to mainlands. This effect intensified with island isolation, particularly for non-endemic plant species. The proportion of endemic AM plant species increased with island isolation, consistent with diversification filling niches left open by the mycorrhizal filter. We further found evidence of humans overcoming the initial mycorrhizal filter. Naturalized floras showed higher proportions of AM plant species than native floras, a pattern that increased with increasing isolation and land-use intensity. This work provides evidence that mycorrhizal fungal symbionts shape plant colonization of islands and subsequent diversification.
more »
« less
- Award ID(s):
- 1656006
- NSF-PAR ID:
- 10322355
- Date Published:
- Journal Name:
- Communications Biology
- Volume:
- 4
- Issue:
- 1
- ISSN:
- 2399-3642
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
more » « less
Abstract Arbuscular mycorrhizal (AM) fungi are root symbionts that can facilitate plant growth and influence plant communities by altering plant interactions with herbivores. Therefore, AM fungi could be critical for the conservation of certain rare plants and herbivores. For example, North American milkweed species are crucial hosts for monarch butterflies (
Danaus plexippus ). Understanding how mycorrhizal composition affects milkweeds will have direct impacts on the conservation and restoration of both increasingly threatened guilds. We present data from three studies on the effect of AM fungal composition on milkweed growth, latex production, and establishment. First, we grew seven milkweed species with and without a mixture of native mycorrhizal fungi. We assessed how important fungal composition is to milkweed growth and latex production by growing four milkweed species with seven fungal compositions, as single‐species inoculations with four native fungi, a mixture of native fungi, a single commercial fungus of presumably non‐native origin, and noninoculated controls. Finally, we assessed the field establishment of two milkweed species with and without native mycorrhizal inoculation. Milkweed species grew 98% larger and produced 82% more latex after inoculation with native mycorrhizae. Milkweeds were strongly affected by fungal composition; milkweeds were inhibited by commercial fungi (average of −14% growth) and showed variable but positive responses to native fungal species (average of +3% to +38% biomass). Finally, we found that restoration establishment was dependent on inoculation with native fungi and milkweed species. Overall, our findings indicate that some milkweed species (i.e.,Asclepias syriaca andA. incarnata ) are not responsive to mycorrhizal fungal presence or sensitive to mycorrhizal composition while others are, including endangered species (A. meadii ) and species of high conservation value (A. tuberosa ). We conclude that the reintroduction of native AM fungi could improve the establishment of desirable milkweed species and should be considered within strategies for plantings for monarch conservation. -
BACKGROUND The Republic of Madagascar is home to a unique assemblage of taxa and a diverse set of ecosystems. These high levels of diversity have arisen over millions of years through complex processes of speciation and extinction. Understanding this extraordinary diversity is crucial for highlighting its global importance and guiding urgent conservation efforts. However, despite the detailed knowledge that exists on some taxonomic groups, there are large knowledge gaps that remain to be filled. ADVANCES Our comprehensive analysis of major taxonomic groups in Madagascar summarizes information on the origin and evolution of terrestrial and freshwater biota, current species richness and endemism, and the utilization of this biodiversity by humans. The depth and breadth of Madagascar’s biodiversity—the product of millions of years of evolution in relative isolation —is still being uncovered. We report a recent acceleration in the scientific description of species but many remain relatively unknown, particularly fungi and most invertebrates. DIGITIZATION Digitization efforts are already increasing the resolution of species richness patterns and we highlight the crucial role of field- and collections-based research for advancing biodiversity knowledge in Madagascar. Phylogenetic diversity patterns mirror that of species richness and endemism in most of the analyzed groups. Among the new data presented, our update on plant numbers estimates 11,516 described vascular plant species native to Madagascar, of which 82% are endemic, in addition to 1215 bryophyte species, of which 28% are endemic. Humid forests are highlighted as centers of diversity because of their role as refugia and centers of recent and rapid radiations, but the distinct endemism of other areas such as the grassland-woodland mosaic of the Central Highlands and the spiny forest of the southwest is also important despite lower species richness. Endemism in Malagasy fungi remains poorly known given the lack of data on the total diversity and global distribution of species. However, our analysis has shown that ~75% of the fungal species detected by environmental sequencing have not been reported as occurring outside of Madagascar. Among the 1314 species of native terrestrial and freshwater vertebrates, levels of endemism are extremely high (90% overall)—all native nonflying terrestrial mammals and native amphibians are found nowhere else on Earth; further, 56% of the island’s birds, 81% of freshwater fishes, 95% of mammals, and 98% of reptile species are endemic. Little is known about endemism in insects, but data from the few well-studied groups on the island suggest that it is similarly high. The uses of Malagasy species are many, with much potential for the uncovering of useful traits for food, medicine, and climate mitigation. OUTLOOK Considerable work remains to be done to fully characterize Madagascar’s biodiversity and evolutionary history. The multitudes of known and potential uses of Malagasy species reported here, in conjunction with the inherent value of this unique and biodiverse region, reinforce the importance of conserving this unique biota in the face of major threats such as habitat loss and overexploitation. The gathering and analysis of data on Madagascar’s remarkable biota must continue and accelerate if we are to safeguard this unique and highly threatened subset of Earth’s biodiversity. Emergence and composition of Madagascar’s extraordinary biodiversity. Madagascar’s biota is the result of over 160 million years of evolution, mostly in geographic isolation, combined with sporadic long distance immigration events and local extinctions. (Left) We show the age of the oldest endemic Malagasy clade for major groups (from bottom to top): arthropods, bony fishes, reptiles, flatworms, birds, amphibians, flowering plants, mammals, non-flowering vascular plants, and mollusks). Humans arrived recently, some 10,000 to 2000 years (top right) and have directly or indirectly caused multiple extinctions (including hippopotamus, elephant birds, giant tortoises, and giant lemurs) and introduced many new species (such as dogs, zebu, rats, African bushpigs, goats, sheep, rice). Endemism is extremely high and unevenly distributed across the island (the heat map depicts Malagasy palm diversity, a group characteristic of the diverse humid forest). Human use of biodiversity is widespread, including 1916 plant species with reported uses. The scientific description of Malagasy biodiversity has accelerated greatly in recent years (bottom right), yet the diversity and evolution of many groups remain practically unknown, and many discoveries await.more » « less
-
There has been a surge in industries built on the production of arbuscular mycorrhizal (AM) fungal-based inoculants in the past few decades. This is not surprising, given the positive effects of AM fungi on plant growth and nutritional status. However, there is growing concern regarding the quality and efficacy of commercial inoculants. To assess the potential benefits and negative consequences of commercial AM fungal inoculants in grasslands, we conducted a controlled growth chamber study assessing the productivity and AM fungal root colonization of nine grassland plant species grown in grassland soil with or without one of six commercial AM fungal products. Our research showed no evidence of benefit; commercial inoculants never increased native plant biomass, although several inoculants decreased the growth of native species and increased the growth of invasive plant species. In addition, two commercial products contained excessive levels of phosphorus or nitrogen and consistently reduced AM fungal root colonization, indicating an unintentional de-coupling of the symbiosis. As there is little knowledge of the ecological consequences of inoculation with commercial AM fungal products, it is critical for restoration practitioners, scientists, and native plant growers to assess the presence of local AM fungal communities before investing in unnecessary, or possibly detrimental, AM fungal products.more » « less
-
more » « less
Abstract Plant–microbe interactions play an important role in structuring plant communities. Arbuscular mycorrhizal fungi (AMF) are particularly important. Nonetheless, increasing anthropogenic disturbance will lead to novel plant–AMF interactions, altering longstanding co‐evolutionary trajectories between plants and their associated AMF. Although emerging work shows that plant–AMF response can evolve over relatively short time scales due to anthropogenic change, little work has evaluated how plant AMF response
specificity may evolve due to novel plant–mycorrhizal interactions. Here, we examine changes in plant–AMF interactions in novel grassland systems by comparing the mycorrhizal response of plant populations from unplowed native prairies with populations from post‐agricultural grasslands to inoculation with both native prairie AMF and non‐native novel AMF. Across four plant species, we find support for evolution of differential responses to mycorrhizal inocula types, that is, mycorrhizal response specificity, consistent with expectations of local adaptation, with plants from native populations responding most to native AMF and plants from post‐agricultural populations responding most to non‐native AMF. We also find evidence of evolution of mycorrhizal response in two of the four plant species, as overall responsiveness to AMF changed from native to post‐agricultural populations. Finally, across all four plant species, roots from native prairie populations had lower levels of mycorrhizal colonization than those of post‐agricultural populations. Our results report on one of the first multispecies assessment of local adaptation to AMF. The consistency of the responses in our experiment among four species provides evidence that anthropogenic disturbance may have unintended impacts on native plant species' association with AMF, causing evolutionary change in the benefit native plant species gain from native symbioses.
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1038/s42003-021-02649-2
