As animal seed dispersers go the way of the dodo, forest plants are at risk

The few remaining rainforests on Mauritius whisper with the memory of former residents, now ghosts.

This once-lush Indian Ocean island remained mostly uninhabited by humans until 1598, when it became a Dutch port of call. By the time the French government took over some 150 years later and imported slaves to start sugar plantations, the ecological damage was already irreparable. The dodo disappeared, and in the years since would become an icon for extinction. Meanwhile, as jungles fell and humans and domestic animals streamed in, tortoises, parrots, pigeons, fruit bats and giant lizards also dwindled and vanished.

Other losses on the island were harder to notice: trees and other plants that relied on those vanished animal species to spread their nuts and seeds. Changes in the plant kingdom are not easily perceived because “we’re just not seeing the trees within the forest,” says Tammy Mildenstein, a wildlife biologist at Iowa’s Cornell College. But the absence of flora also reverberates, further reducing fauna that rely on those plants for food and homes.

In some woodlands, jungles, marshes and grasslands, “vegetation is relatively lush, but you hear only silence,” says Evan Fricke, an ecologist at Rice University. It’s a condition sometimes called empty forest syndrome. “If it doesn’t have birds and mammals, what happens to those forests?” Fricke asks.

In a recent study, his team reported that seed-disbursing creatures have “steeply declined” globally. Their findings wave a red flag, highlighting growing concern about the ability of plant communities to reproduce and survive long-term in a changing climate, on altered landscapes, with diminished wildlife.

Now, researchers are delving into the many unstudied mysteries of plant-animal relationships, to unravel the ways that flora and fauna mutually support each other. Conservationists are also beginning to incorporate seed dispersers into rewilding and forest regeneration projects to restore healthy ecosystems worldwide.

Spreading seeds

Some seeds, like dandelions and maples, fly on the breeze. Some fruits explode, forcibly ejecting seeds. But many plants and trees evolved relationships with wildlife that feed on their fruits, berries, seeds or gather their nuts — and help them reproduce.

It’s an effective strategy that’s been adopted by up to 90% of tree species in the tropics and half of those in temperate zones, says Haldre Rogers, a community ecologist at Iowa State University.

There are many, many animals that disperse seeds: birds, bats, rodents, primates, insects, and an army of small and large mammals. With some 73,000 known tree species and perhaps 435,000 plant species overall, wildlife has a lot of work to do.

Animals provide seeds with the legs or wings they need to survive, Rogers says. Plants’ future progeny travel inside mouths, beaks and stomachs; hitchhike on legs and fur; and are carried off, dropped, regurgitated or excreted some distance away from the parent plant. In new territory, there are better odds that the seeds won’t sprout in big, competitive clumps, be deprived of light, infected by pathogens or eaten by seed predators.

These natural systems are well designed: Digestion, for example, offers power-washing services, with acids stripping away pulp and neutralizing compounds that attract fungus and pathogens, a process that may improve germination. Animals then defecate seeds, depositing them within their own dung fertilizer packet.

But human activities are disrupting these systems: Hunting, logging, expanding agriculture, development, and now, climate change, are driving animal extinctions, with many species now in a precipitous worldwide decline. Wildlife losses ripple throughout ecosystems that have evolved in synchrony over millennia. When animals no longer distribute seeds, plant communities change and some species disappear. Then, with fewer fruiting trees and bushes, animal species from insects to elephants go hungry, sparking the next wave of declines or local extinctions.

This “trophic cascade,” or domino effect, is easily triggered in tropical forests, which are home to four-fifths of the world’s biodiversity, Rogers says. Ecuador’s Yasuní National Park offers an example, with 670 tree species found in just a single hectare (2.5 acres) of old-growth rainforest.

Rare plants living in small or specialized habitats face the highest risk when they lose their seed dispersers. Depending on the species, there may be a substantial time lag before they disappear entirely, since some trees live for hundreds of years — long after the demise of the animals that  helped them reproduce.

Naturalist John Muir described the process well. “When we try to pick out anything by itself, we find it hitched to everything else in the Universe.” When one domino falls, it takes down another, and another.

From bats and birds to lemurs and elephants

There’s a long history of species losses sparked by humans — losses we can learn from. The giant lemur was an ancient casualty. This Madagascar primate went extinct some 2,000 years ago after people arrived on that African island. The giant lemur once transported seeds in its belly and helped keep endemic forests healthy.

Now, amid Earth’s sixth mass extinction, there are many recent declines, including elephants poached for their ivory in Africa; birds decimated by the invasive brown tree snake in Guam; tapirs, monkeys and other mammals hunted out of Brazil’s Atlantic Forest; and the many species gone from Canada’s boreal forests, leveled for biomass energy, tar sands oil and sand mining.

Globally, thousands of species help keep flora alive. A single fleshy fruit may be a staple food for a particular animal. Other species have broad palates. Any bird that eats fruit plays a role: they are the workhorses of the seed-dispersing world. Bats may play a similar role, “bigger than I ever would have guessed,” says Mildenstein. She and colleagues tallied 1,072 plant species eaten by 75 species of fruit bat, an animal that reseeds a huge swath of the world.

Some seeds hitch rides with many creatures. But certain plants, such as Asia’s strangler fig, coevolved with a specific animal that may be crucial for its long-term survival. Mildenstein explained that birds, monkeys, wild pigs and others gorge on the figs, but it’s the flying foxes that best propagate this tree. The foxes soar high above the canopy, defecating seeds that fall onto top branches. Shadowed on the ground in dense tropical undergrowth, fig seeds fail, but in full sunlight, the stranglers sprout and extend their braided roots to the forest floor. Figs are an important community member, available year-round to feed animals when little other food is available.

For some plants, the distance carried is critical. Large bats travel long distances, up to 88 kilometers (55 miles) in a night, or hundreds when migrating. Hornbills — the so-called “farmers of the forest” in Africa and Asia — move more than 700 plant species up to 11 km (7 mi) in a day. Chimpanzees spread huge amounts of seed across miles in Senegal’s savannas and woodlands.

“But the king of all dispersers is the elephant,” says John Poulson, a tropical ecologist at Duke University’s Nicholas School of the Environment. At 3.5 tons, they’re the largest fruit-eating mammal in Central African forests, carrying vast numbers and types of seeds in their gut for up to 100 km (60 mi). They also ingest fruit too large for other animals to swallow.

But poaching has made it difficult for fruit-bearing trees and bushes to survive in places like Gabon’s Minkébé National Park, where more than 25,000 forest elephants were slaughtered for their ivory from 2004 to 2014.

Fricke highlighted the crux of the problem. “Unfortunately, the large animals that are most important for seed dispersal are the types of species that are often the first to disappear from our ecosystems.”

The need to move

Because plants are firmly rooted immobile organisms, they need to move their seeds to regenerate and spread, especially amid major environmental disturbances and increasing climate change impacts.

But that’s growing harder as animals decline and landscapes fragment into what conservation biologist George Powell dubbed “green measles” –– disconnected scraps of habitat, broken up by fences, cultivated fields, pastures, roads, and settlements.

Overall, deforestation is the greatest threat to both plants and animals, with land cleared for timber and industrial-scale agriculture: cattle, soy, rubber, palm oil and other commodities. From 2001 to 2020, the planet lost 4.1 million square kilometers (1.6 million square miles) of tree cover, according to the nonprofit Global Forest Watch.

Many of nature’s architects need large areas of habitat to survive. In patchy, subdivided landscapes, both plant and animal communities contract in size and diversity. Only a subset of creatures remain in scraps of habitat, severing interactions between former residents that helped keep all alive.

A changing climate

The need for mobility is rising alongside warming temperatures and more frequent extreme weather events. Transported elsewhere, plants may be able to “outrun” warming climate, says Beatriz Rumeu, an island ecologist at the University of Cádiz in Spain.

Some organisms will need to move upslope, toward the poles, or closer to water, says Fricke. But in flat areas, species may need to migrate tens of kilometers yearly to maintain constant environmental conditions. “That’s a super tall order [for plants], especially in places that don’t have animals to transport seeds over long distances,” Fricke adds.

He led a study showing that in habitats with reduced birds and mammals, the risk of plants being stranded in inhospitable environments rises to at least 60%. Trapped without their animal associates, they face wildfire, flood, heat, drought and more frequent disease outbreaks.

California’s huckleberry bush offers one example. It’s been a century since grizzly bears wandered the state, gorging on berries and reseeding this bush. Robins, foxes and others still eat huckleberries, but they distribute fewer seeds over much shorter distances that may not keep pace with climate change.

Researchers have identified similar cascading impacts linked to climate change in Gabon’s Lopé National Park. In 1993, ecologist Caroline Tutin discovered that some Gabon trees only flowered and produced fruit if nights cooled below 18° Celsius (66° Fahrenheit). Temperatures have since warmed, and now, there’s a fruit famine. In the 1980s, one of every 10 trees held ripe fruit. Now, it’s one in 50, with the physical health of the region’s remaining forest elephants visibly deteriorating as a result. Elephant poachers compound the trees’ seeding problems, says Poulson. Long-distance dispersal, once carried out by elephants, is now mostly left to guenons, mangabeys, chimps and gorillas that foray over shorter distances.

Unraveling the mysteries of plant-animal relationships

Much remains unknown about individual plant-animal disperser relationships, says Lilisbeth Rodríguez, a botanist at the Smithsonian Tropical Research Institute in Panama.

To reveal the hidden natural history of one of these unstudied plants, Zamia pseudoparasitica, Rodríguez clipped into climbing ropes and hoisted herself aloft  ––  sometimes up to 30 meters (100 feet) into trees –– to install camera traps. This rare epiphyte, a “living fossil” that appeared some 34 million years ago, lives attached to trees in Panama’s Atlantic lowland and cloud forests — but no one knew who came to eat its large, inch-long seeds.

The cameras were left in the forest for three months. Rodríguez and her biologist colleagues, Claudio Monteza-Moreno and Pedro Castillo-Caballero, retrieved them just as the world was locking down at the start of the COVID-19 pandemic, and so were forced to sleep in their car as they traveled between study sites.

The photos and video they captured revealed a hidden world, showing a bird (a toucanet) and seven mammals (including opossums, kinkajous, squirrels and monkeys) visiting the plant’s seed cones. But just one animal, the northern olingo, was captured actually taking and moving seeds.

This single study points out the challenges of such investigations. But even as science is exploring specific plant-animal relationships, many interactions are changing. Much of what we know about shifting relationships comes from studies on islands, which are exceptionally vulnerable to ecological change. With constrained boundaries, quick lifecycles, unique and diverse species, and sometimes intense human pressures, islands act as living laboratories.

The Galápagos Islands are among those laboratories, a place where fleshy-fruited plant species dominate. Beatriz Rumeu joined expeditions there that highlighted the archipelago’s precarious plant-seed disperser balance. The key fruit eaters are the San Cristóbal tortoise, two species of lava lizards, two mockingbirds, and a flycatcher. However, the loss of just one species, the Santa Cruz lava lizard, would prove disastrous, as it spreads more than half the community’s plant species. The giant tortoise also plays a unique role on these islands as the only creature big enough to eat large fruits. Meanwhile, invasive fire ants, parasitic nest flies, feral dogs, cats — and extreme weather events — put the entire system at risk.

Haldre Rogers shares an extreme scenario. On the island of Guam, the accidentally introduced exotic brown tree snake wiped out the island’s seed dispersers: its birds and most of the bats, too. A small number of bats remain, and feral pigs also munch on fallen fruit, but the ecosystem is irrevocably altered. The quick-growing “pioneer plant species” that need well-lit areas “just drop right out,” Rogers says. “I don’t think people recognize that animal dispersers are incredibly important for keeping our systems running.” Guam offers a dire warning, showing what happens when dispersers disappear, she says.

A world without seed dispersers

By disbursing seeds, animals help facilitate all the benefits plants provide for us: storing carbon, controlling floods, and providing water, food, timber, fiber, fuel and medicine, Fricke says. Without seed dispersers, humanity would face serious challenges.

But there are growing efforts to restore this critical ecological process. If successful, such projects could offer a bonanza of benefits: preventing extinctions, helping bringing back endangered plants and wildlife, recovering wild lands, and curbing climate change. Some of this work is being facilitated under the United Nations Decade on Ecosystem Restoration.

Protecting key animal species will help — especially toucans, elephants, apes and others that travel far or carry large seeds. Because bats are so important, there are global efforts to protect roosting sites.

Rewilding is another relatively low-cost solution, although difficult to implement due to the need for permits, quarantines and careful monitoring. One success story comes from Brazil’s Atlantic Forest, where most mammals were hunted out, threatening 45 types of native palm. Researchers, reserve managers and animal keepers reintroduced red-humped agoutis and brown howler monkeys to Tijuca National Park, near Rio de Janeiro.

These seed-dispersing animals filled an important ecological void, sparking a “disproportional effect on forest regeneration.” Reintroducing heavily-hunted giant tortoises to the Galápagos also proved successful, offering promise for other islands. Tropical forests can regrow relatively quickly after being burned or logged, especially if seed dispersers are available to aid regrowth.

In some areas, reforestation could restore destroyed habitat, but only if important native species are planted — not exotic monocultures, says Monteza-Moreno. Reconnecting fragmented habitat and protecting wild, intact landscapes is also critical. The Central African Forest Initiative is now paying countries to protect forests.

Poulson mentioned another important initiative happening in Gabon, a country that previously protected 13% of its land in national parks. President Ali Bongo Ondimba signed a policy in 2020 that takes effect this year, requiring logging concessions to operate sustainably. It’s an important model, one that needs similar versions for agriculture and other deforesting industries,

Positive things are happening, Poulson says. “The question is whether the positive things can outrace climate change, unsustainable hunting, poaching, industrial agriculture and deforestation.”

Banner image: A pair of great hornbills. Hornbills — the so-called “farmers of the forest” in Africa and Asia — move more than 700 plant species up to 11 km (7 mi) in a day. Image by chamnan phanthong via Adobe Stock.

Citations:

Redford, K. H. (1992). The Empty Forest: Many large animals are already ecologically extinct in vast areas of neotropical forest where the vegetation still appears intact. BioScience, 42(6), 412-422. doi:10.2307/1311860

Fricke, E. C., Ordonez, A., Rogers, H. S., & Svenning, J. (2022). The effects of defaunation on plants’ capacity to track climate change. Science, 375(6577), 210-214. doi:10.1126/science.abk3510

Caughlin, T. T., Ferguson, J. M., Lichstein, J. W., Zuidema, P. A., Bunyavejchewin, S., & Levey, D. J. (2015). Loss of animal seed dispersal increases extinction risk in a tropical tree species due to pervasive negative density dependence across life stages. Proceedings of the Royal Society B: Biological Sciences, 282(1798). doi:10.1098/rspb.2014.2095

Cazzolla Gatti, R., Reich, P. B., Gamarra, J. G., Crowther, T., Hui, C., Morera, A., … Liang, J. (n.d.). The number of tree species on Earth. Proceedings of the National Academy of Sciences, 119(6). doi:10.1073/pnas.2115329119

Enquist, B. J., Feng, X., Boyle, B., Maitner, B., Newman, E. A., Jørgensen, P. M., … McGill, B. J. (2019). The commonness of rarity: Global and future distribution of rarity across land plants. Science Advances, 5(11). doi:10.1126/sciadv.aaz0414

Ceballos, G., Ehrlich, P. R., & Raven, P. H. (2020). Vertebrates on the brink as indicators of biological annihilation and the sixth mass extinction. Proceedings of the National Academy of Sciences, 117(24), 13596-13602. doi:10.1073/pnas.1922686117

Hansen, D. M., Kaiser, C. N., & Müller, C. B. (2008). Seed dispersal and establishment of endangered plants on oceanic islands: The Janzen-Connell model, and the use of ecological analogues. PLOS ONE, 3(5), e2111. doi:10.1371/journal.pone.0002111

Silliman, B. R., & Angelini, C. (2012). Trophic cascades across diverse plant ecosystems. Nature Education Knowledge, 3(10), 44. Retrieved from https://www.nature.com/scitable/knowledge/library/trophic-cascades-across-diverse-plant-ecosystems-80060347/

Wells, J. V., Dawson, N., Culver, N., Reid, F. A., & Morgan Siegers, S. (2020). The state of conservation in North America’s boreal forest: Issues and opportunities. Frontiers in Forests and Global Change, 3. doi:10.3389/ffgc.2020.00090

Abdul Aziz, S., McConkey, K. R., Tanalgo, K., Sritongchuay, T., Low, M., Yong, J. Y., … Racey, P. A. (2021). The critical importance of Old World fruit bats for healthy ecosystems and economies. Frontiers in Ecology and Evolution, 6. doi:10.3389/fevo.2021.641411

Naniwadekar, R., Rathore, A., Shukla, U., Chaplod, S., & Datta, A. (2019). How far do Asian forest hornbills disperse seeds? Acta Oecologica, 101, 103482. doi:10.1016/j.actao.2019.103482

Aguado, W. D., Rogers, H. S., & Pruetz, J. D. (2022). Chimpanzees as ecosystem service providers: Seed dispersal of an economically important plant resource. Biotropica. doi:10.1111/btp.13080

White, L. J. T. (1994). Biomass of rain forest mammals in the Lopé Reserve, Gabon. The Journal of Animal Ecology, 63(3), 499-512. doi:10.2307/5217

White, L. J. T, Tutin, C. E. G., & Fernandez, M. (1993). Group composition and diet of forest elephants, Loxodonta Africana cyclotis Matschie 1900, in the Lopé Reserve, Gabon. African Journal of Ecology, 31(3), 181-199. doi:10.1111/j.1365-2028.1993.tb00532.x

Tutin, C. E. G., & Fernandez, M. (1993). Relationships between minimum temperature and fruit production in some tropical forest trees in Gabon. Journal of Tropical Ecology, 9(2), 241-248. Retrieved from https://www.jstor.org/stable/2559296

Bush, E. R., Jeffery, K., Bunnefeld, N., Tutin, C., Musgrave, R., Moussavou, G., … Abernethy, K. (2020). Rare ground data confirm significant warming and drying in western equatorial Africa. PeerJ, 8, e8732. doi:10.7717/peerj.8732

Bush, E. R., Whytock, R. C., Bahaa-el-din, L., Bourgeois, S., Bunnefeld, N., Cardoso, A. W., … Abernethy, K. (2020). Long-term collapse in fruit availability threatens Central African forest megafauna. Science, 370(6521), 1219-1222. doi:10.1126/science.abc7791

Erdei, B., Calonje, M., Hendy, A., & Espinosa, N. (2018). A review of the Cenozoic fossil record of the genus Zamia L. (Zamiaceae, Cycadales) with recognition of a new species from the late Eocene of Panama — evolution and biogeographic inferences. Bulletin of Geosciences, 93(2), 185-204. doi:10.3140/bull.geosci.1671

Monteza‐Moreno, C. M., Rodriguez‐Castro, L., Castillo‐Caballero, P. L., Toribio, E., & Saltonstall, K. (2022). Arboreal camera trapping sheds light on seed dispersal of the world’s only epiphytic gymnosperm: Zamia pseudoparasitica. Ecology and Evolution, 12(3). doi:10.1002/ece3.8769

Rumeu, B., Devoto, M., Traveset, A., Olesen, J. M., Vargas, P., Nogales, M., & Heleno, R. (2017). Predicting the consequences of disperser extinction: Richness matters the most when abundance is low. Functional Ecology, 31(10), 1910-1920. doi:10.1111/1365-2435.12897

Rodda, G. H., & Savidge, J. A. (2007). Biology and impacts of Pacific island invasive species. 2. Boiga irregularis, the brown tree snake (Reptilia: Colubridae). Pacific Science, 61(3), 307-324. doi:10.2984/1534-6188(2007)61[307:baiopi]2.0.co;2

Galetti, M., Donatti, C. I., Pires, A. S., Guimarães Jr., P. R., & Jordano, P. (2006). Seed survival and dispersal of an endemic Atlantic forest palm: The combined effects of defaunation and forest fragmentation. Botanical Journal of the Linnean Society, 151(1), 141-149. doi:10.1111/j.1095-8339.2006.00529.x

Cid, B., Figueira, L., De T. e Mello, A. F., Pires, A. S., & Fernandez, F. A. (2014). Short-term success in the reintroduction of the red-humped agouti Dasyprocta leporina, an important seed disperser, in a Brazilian Atlantic Forest reserve. Tropical Conservation Science, 7(4), 796-810. doi:10.1177/194008291400700415

Genes, L., Fernandez, F. A., Vaz-de-Mello, F. Z., Da Rosa, P., Fernandez, E., & Pires, A. S. (2019). Effects of howler monkey reintroduction on ecological interactions and processes. Conservation Biology, 33(1), 88-98. doi:10.1111/cobi.13188

Fernandez, F. A., Rheingantz, M. L., Genes, L., Kenup, C. F., Galliez, M., Cezimbra, T., … Pires, A. S. (2017). Rewilding the Atlantic Forest: Restoring the fauna and ecological interactions of a protected area. Perspectives in Ecology and Conservation, 15(4), 308-314. doi:10.1016/j.pecon.2017.09.004

Falcón, W., & Hansen, D. M. (2018). Island rewilding with giant tortoises in an era of climate change. Philosophical Transactions of the Royal Society B: Biological Sciences, 373(1761). doi:10.1098/rstb.2017.0442

Poorter, L., Craven, D., Jakovac, C. C., Van der Sande, M. T., Amissah, L., Bongers, F., … Hérault, B. (2021). Multidimensional tropical forest recovery. Science, 374(6573), 1370-1376. doi:10.1126/science.abh3629