Think biodiversity and a tropical rainforest might come to mind. Wet tropical forests, the most species-rich ecosystems on earth, are estimated to support nearly half of all known terrestrial species. Trees are a particularly diverse group of organisms in wet tropical forests and some regions like the Amazon can host over 1,000 different tree species in a single hectare of forest. Ecologists have long pondered the mechanisms underlying such astounding variety (Wright 2002). How do so many organisms of such similar, albeit simple, requirements coexist in such diversity in close proximity? It appears that the answer might partly lie in plant pathogens (Muller-Landau 2014).
How pathogens regulate the diversity of trees is a remarkable ecological tale. But, to better understand this story, we need to make a short trip down a path of scientific hypotheses. Many ideas have been posited to explain the conundrum of how multiple species coexist at relatively small spatial scales to generate diversity. Broadly, diversity can stem from mechanisms classified as stochastic or deterministic. Simply put, stochastic mechanisms are happenstance. Would a seed arrive at a spot? Would a seedling be accidentally killed by a falling branch or underfoot a roving deer? In contrast, deterministic mechanisms, as the term suggests, are processes that govern species’ survival in predictable ways, such as availability of necessary resources or susceptibility to pests, pathogens, and predators (Freckleton and Lewis 2006).
The interaction between plants and their consumers and plants and pathogens has been suggested previously as an important driver of plant diversity. Only recently, however, have the links between pathogens and plant diversity been demonstrated through empirical experiments.
The Natural History of Natural Enemies
Predators and pathogens regulating population numbers of their prey or host is a well-known concept in a variety of ecosystems. In rivers, lakes, seas, or forests, predators keep consumer numbers in check. As with larger animals, predators of seeds and seedlings also exert a top-down effect on plant populations, and wet tropical forests are home to a variety of insects and fungi that kill seeds and seedlings. The forest understory provides especially conducive settings for fungi. Thriving in the wet, dark forest floor, soil fungi infect seeds and seedlings, thus regulating their numbers. In a surprising twist, however, by keeping down the numbers of their hosts, plant predators allow other species to persist, thus promoting diversity of plant communities.
Pathogens act in a manner termed “negatively density dependent.” Negative density dependence just means that an individual plant is more likely to be infected by its pathogen when in the vicinity of its own kind, i.e., other individuals of the same or closely related plant species (Freckleton and Lewis 2006). Just as human diseases spread more when humans crowd together, increasing individuals of a single plant species cultivates the soil for the very pathogens that kill the plant’s seeds and seedlings. So, when a species becomes numerous, its individuals are more likely to die, allowing less competitive species to persist, leading to a more diverse community.
Back in 1971, negative density dependence as a mechanism for diversity in multispecies communities was proposed independently by Janzen and Connell, for tropical rainforests and coral reefs, respectively (Janzen 1971). The Janzen-Connell (J-C) hypothesis states that diversity of a community is maintained in part by the parasites and predators that cull young progeny, especially where host numbers are high. Specifically, mortality of seeds and seedlings of a species will be higher with increasing numbers of that species in a neighborhood (such as close to seed-producing adult trees), opening up these spaces for other species to occupy, thus promoting diversity.
A recent meta-analysis—an analysis of the net outcome from multiple studies conducted in different ecosystems—found that overall empirical evidence supported the J-C hypothesis (Comita et al. 2014). However, the J-C hypothesis was largely tested in the context of insects and mammalian seed predators, although evidence was mounting that fungal pathogens were also crucial agents of negative density dependence. Notably, no study had explicitly tested whether density-dependent culling by seed and seedling predators actually increased diversity of the plant community.
Then in 2014, in a seasonally wet forest in Belize, researchers demonstrated how the plant community changed if the action of insects and fungi was experimentally inhibited using insecticide and fungicide (Bagchi et al. 2014). Without insects, the community of recruiting seedlings was markedly different from the naturally regenerating community. Without fungi, the diversity of seedlings dropped sharply in relation to natural regeneration.
Clearly, pathogens drove diversity of the tree community in this neotropical forest. But would insects and fungi play the same role in other closed-canopy forests? Moreover, insect and fungal communities vary with factors like light and moisture—factors that also affect plants directly. How would pathogen impacts on plant diversity and composition change with different habitat conditions brought about from different light and moisture levels? Importantly, with environmental conditions changing rapidly because of human actions, how would maintenance of plant diversity via pathogens change in human-altered forests (Swinfield et al. 2012)?
What Happens When Humans Alter Forests?
We live today in a human-dominated planet. For food, fuel, and other natural resources, humans have deforested much of the earth, breaking once-large and contiguous forest into smaller parcels, a process known as forest fragmentation. One of the greatest threats to biodiversity, forest fragmentation sets in motion a range of ecological processes that alter the dynamics of species’ survival in the remnant forests.
Long-term research in experimentally and naturally fragmented forests have found that fragments often lose species in predictable ways (Laurence et al. 2011). Edge effects, or altered habitat conditions at forest edges, are strongly associated with changes in fragmented tree communities. At edges and in smaller fragments, slow-growing, dense-wooded, shade-tolerant tree species are lost over time, being replaced by fast-growing, light-loving species. However, while patterns of species’ losses are clear, the underlying mechanisms are less well understood (Didham et al. 2012).
Hitherto, edge effects have been primarily examined as changes to abiotic conditions—alteration in light, moisture, wind speed, etc., as we move from the forest edge to interior. Because species differ in their ability to survive in different levels of these resources, changes to light or moisture are assumed to alter species survival at different distances from edges. As a consequence, the plant community changes at edges compared to interior forest. Such changes in the tree community have important consequences for ecosystem functions such as carbon storage or nutrient cycling (Chapin et al. 2000). Hence, grasping the mechanisms driving community-wide changes to trees could improve management and inform restoration of fragmented forests for tree diversity and ecosystem function.
So why are edges dominated by light-wooded, early successional tree species? Let us suppose that edges behave like giant forest gaps. Light-loving, fast-growing species often colonize and dominate gaps by exploiting the high resource conditions. But, once the canopy is established in a gap, light availability reduces and more shade-tolerant species are able to come in. Without abundant light, the light-loving species do not have the resources to grow fast and are outcompeted by slower-growing species.
Events unfold differently in forest edges. Even after the canopy forms, shade-tolerant species seem unable to establish at edges. It is argued that high light at edges disadvantages slow-growing, shade-tolerant species, and fast-growing species outcompete them. As a consequence, edges and small fragments, which are subject to edge effects, remain dominated by light-loving species while shade-tolerant species are unable to regain a foothold. However, it is also possible that this “arrested succession” is happening because of changes to pathogen activity.
Light-loving species tend to be more susceptible to pathogens than shade-tolerant species, although there are exceptions. While light-loving species might initially increase in areas of high light, their numbers should start coming down when pathogens build up around them over time. Thus, in edges of older fragments, the seedlings of abundant light-loving species should suffer higher mortality from pathogens, opening up that space for shade-tolerant species. However, warmer, drier conditions at edges might reduce pathogen activity, thus diluting the mechanism that prevents one of few species from becoming super abundant. Alternatively, the benefits of high light per se help overcome losses to pathogens for all species. In this case, no species will be much affected by pathogens at edges and controlling pathogen activity would not improve survival of shade-tolerant versus shade-intolerant species.
Plant–Pathogen Interactions in Fragmented Forest
In a fragmented, human-altered forest, I examined whether and how the influence of pathogens during seedling recruitment (establishment and survival of seedlings) varied with distance to edges. The research site was within the Western Ghats Biodiversity Hotspot in Karnataka state, India. To test whether light alone or a combination of light and pathogens regulated seedling recruitment, I set up groups of seedling plots at increasing distances from the forest edge. Each group consisted of two seed traps and five seedling plots. In each group, one plot each was sprayed with fungicide, insecticide, fungicide plus insecticide, and water, and one plot was retained as control without any spraying. I set up 145 such groups at 15 locations, three groups each at distances of 0, 25, 50, and 100 meters (0, 82, 164, and 328 feet) from the edge, totaling 730 seedling plots. I applied pesticide treatments from November 2015 through November 2016. During this time, seeds falling into the seed traps were recorded twice a month. I conducted censuses for new recruits twice during the year: once at the end of the dry season and then at the end of the wet season after peak recruitment occurred.
/Preliminary results indicate that seedling diversity reduces when plots are sprayed with fungicide, but only as we move into interior forest. Similarly, turnover of species between seeds that arrive at a spot and seedlings that establish is lowered with fungicides, but only in interior forest. Importantly, the density-dependent effect of fungi and insects appears to be at play only in interior forest. Hence, it appears that the lower diversity of seedlings in plots with pesticides are likely due to a loss of pathogen-mediated mortality of seeds and young seedlings as we move towards the forest edge. Clearly, edge effects are changing some interactions between plants and their pathogens, which in turn appears to be affecting the diversity of the plant community.
The Future of Diversity
Uncovering the mechanisms driving diversity remains a fascinating quest. You know you have stumbled upon a rich question when every answer opens up more questions. But, as we slowly piece together bits of the diversity puzzle, we are also changing natural systems at an unprecedented scale. Labeling the “Anthropocene” as a valid geological epoch awaits scientific consensus, but few can miss the ubiquitous influence of humans on Earth (Corlett 2015). Human actions have wiped out entire species, introduced new plants and animals to places where they were unlikely to reach, changed species’ numbers in relation to one another, and altered biological communities in a blink of evolutionary time. Unless we apply some serious course correction, today’s biodiversity might stand a bleak chance for tomorrow. Even if we set aside areas of land and water for other species, much of Earth will likely continue to be occupied by Homo sapiens in the near future. One hopes that by understanding the subtle processes that generate diversity, we can better manage the spaces that we share with other species, both for biodiversity and its contribution to human needs.
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Meghna Krishnadas is a graduate student in the Yale School of Forestry and Environmental Studies and the 2016 recipient of the Arnold Arboretum’s Ashton Award for research in Asian tropical forest biology.