Lost world

Researchers ventured to the world’s most remote island to study how fungi in soils could help to revive damaged ecosystems.

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Legions of seabirds squawked overhead as Toby Kiers bent down and grabbed a fistful of dark crumbly soil. She squeezed it between her fingers and brought some to her nose. “It smells really fresh. Vegetal, like vegetables. Like carrots or celery,” she said with a quick smile.

Kiers, an evolutionary biologist at the Free University of Amsterdam in the Netherlands, had travelled around the globe to hunt for fungi on the North Pacific atoll of Palmyra, one of the most remote islands on the planet. She was looking at tree roots to find symbiotic microorganisms called mycorrhizae, which form networks of filaments that help plants to absorb nutrients and water from the soil. They might also be a key part of the process that breaks down coral rubble on land into the peaty soil she found in some locations on Palmyra.

Kiers has sampled soil microbes worldwide, but her trip to Palmyra in November 2022 was the first time she had taken her search to an island. She is one of several researchers exploring whether below-ground microorganisms such as mycorrhizae could be a key to restoring heavily degraded ecosystems on these and other islands.

Palmyra’s 42 low-lying islets are home to some of the most pristine coral reefs in the world, but the above-water ecosystem has been radically altered — first by nineteenth-century coconut plantations that introduced invasive palm trees, and then by the US military, which dredged areas to create airstrips during the Second World War.

Now the atoll is uninhabited, except for a rotating cast of researchers testing how to repair degraded ecosystems. The non-profit global environmental organization The Nature Conservancy (TNC) bought Palmyra for US$30 million in 2000 and later sold part to the US government. The atoll is co-managed by TNC and the US Fish and Wildlife Service. The two organizations, along with Island Conservation, a California-based non-profit organization, have spent $4 million to eradicate rats in the past decade and are now in the middle of a $3.5-million effort to regenerate the atoll’s rainforest.

Palmyra could be a test case for restoring atolls and island ecosystems more broadly. Islands are some of the most imperilled, highly disturbed ecosystems in the world, and are home to roughly 20% of Earth’s biodiversity — endemic species that evolved in isolation and exist nowhere else.

Most efforts to restore island ecosystems, including on Palmyra, have focused on removing invasive species; TNC has done that by eradicating rats. But since 2020, the organization has been replanting native plant species in the hope that a healthier forest could help to make Palmyra’s coral reefs resilient to rising sea temperatures and increasingly acidic waters.

Native trees are part of a complex web that connects life on land and in the water. Pisonia grandis, or bird-catcher trees, are one of the native species that lure seabirds to the atoll. As bird guano collects around the gnarled roots and fills the soil with nutrients, soil microbes regulate their flow from the land to the sea, nourishing the reefs over time, says Kiers. The plan is to replant P. grandis to restore the island’s health, but those efforts have so far met with limited success.

A similar story is playing out elsewhere: many restoration efforts around the world have faltered in their attempts to re-establish native species. Holly Jones, a restoration ecologist at Northern Illinois University in DeKalb, and her colleagues conducted a meta-analysis of 400 restoration projects worldwide and found that, although the studied ecosystems are recovering, they rarely do so completely¹. And many projects do no better than letting ecosystems recover on their own.

That’s where the fungi might come in, says Kiers, who is also executive director of the Society for the Protection of Underground Networks, an initiative to map fungal networks. They might be crucial for the health of P. grandis and a native shrub, Heliotropium foertherianum, both of which provide a dense canopy that birds prefer to nest in. Kiers is convinced that the mycorrhizae play a pivotal part in the cycling of the bird guano’s nitrogen, phosphorous and potassium on land. With birds and mycorrhizae, “the trees are making their own soils”, she says.

Working out how to improve success rates for ecological repair is a high priority, particularly during the United Nations Decade on Ecosystem Restoration. This initiative, running from 2021 to 2030, calls on nations to deliver on their commitments to restore a total of more than one billion hectares, an area the size of China. The cost of global terrestrial restoration — excluding marine ecosystems — is estimated to be at least $200 billion per year by 2030, according to a 2021 analysis by the UN Environment Programme.

Because many restoration efforts so far have had lacklustre results, a growing number of researchers think the soil microbiota could be a missing piece of the puzzle. Many think that adding soil microorganisms to degraded ecosystems could help native plant species to thrive and bring regions back to health. But some researchers, including Jones, urge caution because manipulating species, particularly on islands, has a long history of unintended consequences.

Those are some of the considerations that brought Kiers to Palmyra last year, to conduct the first studies on mycorrhizae in this remote atoll. Other researchers are watching closely to see what such studies have to offer, both for islands and ecosystems across the planet.

“If we can get restoration right on islands, we have this great capacity to have an outsized impact on reversing the world’s biodiversity crisis,” says Jones.

Kiers and her colleagues spent 17 days on Palmyra in November 2022 to conduct the first survey of mycorrhizae and soil microbial DNA on 26 of the largest islets that have been cleared of Second World War munitions. The researchers recorded tree locations, dug through coral rubble to explore and collect tree roots, and took core samples of soil. The aim was to understand whether symbiotic fungi were present, and what role they might have in supporting the island’s ecosystem. Eventually, these data could help TNC with its restoration efforts on Palmyra.

“Islands are a global conservation priority, but we lack data on what successful restoration looks like,” says Alex Wegmann, director of science for TNC’s Palmyra programme. The soil microbiome, he says, “is one of the last frontiers that we absolutely should explore to be able to effectively restore and protect these systems”.

Palymra presents a big test for restoration efforts. When TNC purchased the atoll, about 45% of it was covered with coconut palms; P. grandis comprised just 13%. And coconut-palm seedlings exploded after the successful 2011 eradication of rats, which previously ate the seedlings as well as seabird eggs and chicks.

Since 2019, Palmyra land managers have painstakingly removed more than one million coconut palms. (The goal is to remove two million.) They have cleared palms from nearly 150 hectares and have so far replanted 18 hectares with native trees. For Wegmann, there is one overarching question: are the soils under the invasive palms able to host native P. grandis when the palms have been removed?

That’s where mycorrhizae could be key. Of the four types of mycorrhiza, two are most common. One kind, called arbuscular mycorrhizal fungi, infiltrates the roots of an estimated 72% of most vascular plant species, notably agricultural crops. Another, known as ectomycorrhizae, forms a sheath surrounding the roots of roughly 2% of plant species², largely trees, including Pisonia. Both types of fungi produce threadlike filaments called hyphae that extend the roots’ reach through the soil, improving the odds of securing often-scarce nutrients and water. These mats of hyphae not only serve as nutrient conduits, but also bind soil particles together to prevent erosion.

There are many tree-planting campaigns worldwide, but not all are successful, says Sofia Gomes, a postdoctoral researcher studying plant and soil microbial communities at Leiden University in the Netherlands. Even in abandoned crop fields, says Gomes, “it is surprisingly difficult to just go plant a tree”. Trees that rely on mycorrhizae often need their specific below-ground partners to survive drought, disease or any other stresses when they arrive in a new environment, she says.

Studies in forestry and agriculture have repeatedly shown a drastic increase in tree or crop productivity when mycorrhizae are added, either by introducing commercial fungal spores or native soil to the planting mix. Mycorrhizal additions are also showing promise in efforts seeking to restore ecosystems. Reintroducing arbuscular mycorrhizae to abandoned agricultural fields in the US Midwest, for instance, consistently improved the success of tallgrass prairie restoration efforts³. A 2019 meta-analysis of 26 field-based studies⁴ found that adding mycorrhizae to restored plant communities increased the number of species by 30%.

But land managers in the United States haven’t yet taken advantage of these findings. A study published this year examined 130 management plans for forests and grasslands and found that only 8% mentioned mycorrhizal fungi, with only one plan noting that mycorrhizae could boost regeneration⁵.

Beyond mycorrhizae and their partnership with plants, researchers think there are millions of other soil microorganisms that have crucial supporting roles in ecosystems. A 2022 analysis of 80 experiments showed that adding a small scoop of soil from intact ecosystems helps to boost plant biomass production by 64% on average, across ecosystems⁶. Researchers suspect the added microbes deserve the credit.

“Introducing a healthy soil microbiome from a native ecosystem tends to improve biodiversity even in the most degraded places, and speeds regeneration,” says study co-author Thomas Crowther, an ecologist at the Swiss Federal Institute of Technology in Zurich who created Restor, an online platform for restoration project managers to efficiently share insights about successes and failures.

Focus on fungi

The part that mycorrhizae play is starting to come into focus in many ecosystems. On islands, it’s clear that mycorrhizae shaped which plants initially colonized those areas. And on each of these isolated landmasses, the relationships between plants and fungi further influenced plant evolution⁷.

But humans have moved plants around the world for centuries, unwittingly introducing root-hitchhiking mycorrhizae into island ecosystems. The pace of this activity has picked up in the past few decades.

“We don’t know a lot about the native mycorrhizal communities in a lot of these islands,” says Kabir Peay, who studies plant microbes at Stanford University in California and is extracting the soil DNA from Palmyra with his team. There are an estimated 40,000–50,000 fungal species that form mycorrhizal associations with plants⁸, but it’s a difficult number to estimate because so many habitats have yet to be sampled, he adds. As a result, there are very few situations where researchers can say whether a mycorrhizal fungus is introduced or native, says Nicole Hynson, a fungal ecologist at the University of Hawaii at Manoa.

Before arriving on Palmyra, Kiers found hints in the literature that P. grandis⁹ and H. foertherianum on other islands might associate with mycorrhizae. And after Kiers sampled soils on Palmyra, she sent root material to Hynson, who confirmed that mycorrhizae are present on the roots of most of the P. grandis and H. foertherianum so far inspected. But the degree of colonization varies, and because the samples are blinded, Hynson doesn’t yet know whether the roots with greater colonization are from native forest or restoration areas.

In separate work in Hawaii, Hynson is exploring whether adding locally sourced fungi from the historical range of an endemic mint (Phyllostegia kaalaensis) that had been completely eradicated from the wild can help to restore populations. Previous attempts to reintroduce the mint had consistently failed because of disease. An initial study¹⁰ found that after applying a slurry of fungi to the leaves of mint plants, they survived longer in the wild than ever previously recorded.

“Mycorrhizal fungi are like plant immune boosters,” she says. Hynson is heartened by the results. But, she adds, “it’s going to take more experimentation to find the right recipe for long-term success”. It can take years, for example, to culture a mycorrhizal fungus.

There are some indications that these relationships could help restoration efforts on Palymra. In an unpublished pilot study started in 2019, researchers found that Pisonia cuttings planted in Pisonia-rich soil had a 50% survival rate, compared with only 37% survival for cuttings planted into soils collected from areas with no Pisonia trees. This suggests that soil gathered underneath a Pisonia grove contains beneficial microorganisms, says Wegmann.

With so few studies of plant-mycorrhizae dependency on islands, it is often unclear which, if any, below-ground species are crucial to plant success. Yet without interventions, some of the rarest, most endangered island plants could go extinct.

There are some hopeful signs. A 2020 study in Sulawesi in Indonesia found that mycorrhizae isolated from the roots of a tree in the same family as the endangered endemic tree, Kalappia celebica, significantly increased its growth on former gold-mining lands¹¹.

But some scientists are concerned about the unintended consequences of boosting mycorrhizal populations on islands. “We don’t know if the reintroduction of mycorrhizae will benefit native plants more than non-natives,” says James Bever, an ecological and evolutionary biologist at the University of Kansas in Lawrence. The fear is that adding mycorrhizae could give invasive plants an edge.

It’s a particular risk on islands because many have battled costly invasions of introduced species. Shallow-rooted miconia (Miconia calvescens), for example, is a non-native tree that was introduced in Hawaii; it accelerates erosion¹² and causes other types of damage estimated at $672 million annually.

There are hints that boosting mycorrhizae can backfire. This can be seen in initial work in the Galapagos Islands, conducted by Bever’s former graduate student, Jessica Duchicela, a restoration ecologist at the University of the Armed Forces in Sangolquí, Ecuador. Duchicela found that the non-native plant species benefited more from soil containing mycorrhizae than did native Galapagos plants¹³.

“We want to restore the Galapagos to increase the density of natives, not the exotics,” she says. Researchers need more information about what is in the soil and how the plants are responding before any attempts to alter the soil microbiota to restore endemic plants, she cautions.

“We have to ask these questions if we want to get it right,” says Kiers.

But it’s difficult to conduct some of these studies, especially in areas such as the Galapagos and Hawaii, which have strict protocols to protect native flora. Duchicela has spent the past few years trying to get permits to take soils from the Galapagos Islands to her laboratory to continue her mycorrhizae research.

Crab transport

While studying the Pisonia forests on Palmyra, Kiers and her colleagues marvelled at the clusters of crabs churning the soil by digging holes in and among the roots of trees — potentially spreading the mycorrhizal spores. She eagerly awaits the results of DNA sequencing on soil from crab holes to see whether there is evidence of the crustaceans moving fungi.

In her expedition last year, Kiers explored life both above and below the waves. As she was wading through shallow water one day, she shrieked after a curious reef shark bumped into her. The prowling sharks, captured in a video taken during the trip, are a sign of vibrant reefs, nourished in part by the one million birds that call Palmyra home — including massive colonies of sooty terns (Onychoprion fuscatus) and red-footed boobies (Sula sula). “We could hardly hear ourselves talk because the birds were so loud,” she says of the islets dominated by P. grandis. It was a sharp contrast to the relative quiet of the islets covered by coconut palms. Of Palmyra’s 12 breeding seabird species, only 2 will regularly nest in coconut palms, says Wegmann.

In the past five years, scientists have shown that islands with more seabirds — and therefore more nutrients — have more-resilient coral reefs. A 2018 study compared islands rife with seabirds to rat-infested islands that contained fewer seabirds. The coral reefs and fish that live around them grew faster near islands with more seabird nutrients¹⁴. “Before this paper, no one had connected the potential benefits of restoring natural nutrient flows to reefs,” says Casey Benkwitt, a research fellow at Lancaster University, UK, who is tracing how seabird nutrients reach reefs.

Although seabirds are the source of nutrients, Kiers thinks the soil microorganisms are the subterranean transport system that keeps nutrients flowing steadily on and off the island. In areas colonized by P. grandis and ectomycorrhizae, the soil is moist brown peat, entirely composed of organic matter, the kind that smelled like vegetables to Kiers. By contrast, the islets covered in coconuts were often just pure sand, unable to hold onto nutrients, she says.

Peay hopes researchers can race to document the below-ground biodiversity on islands — before further changes above ground make it even more difficult to disentangle native soil microorganisms from ones that humans introduced. “It’s critical to get a baseline understanding of which species are present and probably native,” says Peay, “because people are moving things around more and more.”

“We might be erasing the soil’s bio-geographic signature, which could have consequences for restoration,” he adds.

If, Kiers stresses, they find that the ectomycorrhizae were lost as palms took over the islands, it might be necessary to transplant soil from Palmyra’s remaining Pisonia forests to reintroduce the fungus onto islets that have been cleared of palms. “There is no other way P. grandis will be established without its fungal symbiont,” she says.

If trees can be restored to protect the corals, healthy reefs will return the favour. As sea levels rise, resilient coral reefs will provide the natural barriers that buffer waves and allow islands to persist, says Kiers. “Survival of the coral reef is fundamental to the survival of the atoll.”

• Author: Virginia Gewin
• Media editor: Agnese Abrusci
• Subeditor: Anne Haggart
• Art editor: Chris Ryan
• Editor: Richard Monastersky

Photos, video and drone footage from Palmyra: SPUN and The Nature Conservancy

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