Fragmented ecosystems: where top-down meets bottom-up

Biological diversity is one part of “ecosystem structure”.  Other components of ecosystem structure include which species are present, how abundant they are, whether some species are particularly important for the ecosystem to function, and how all the species interact with each other and the environment.  So ecosystem structure is a pretty loaded concept, and figuring out what controls ecosystem structure has captured the intellect and imagination of many ecologists for a long time.  

Two mutually non-exclusive theories have emerged in discussion of control of ecosystem structure.  The bottom-up control hypothesis argues that the producers (primarily plants) are key, so factors influencing plants (such as sun, water and soils), are paramount for understanding ecosystem structure.  The top-down control hypothesis argues that carnivores eat herbivores and herbivores eat plants, so we should focus our attention on the carnivores who directly influence herbivore abundance, and indirectly (by virtue of their effects on herbivores) influence plant abundance and diversity. 

Rong Wang, his research advisor Xiao-Yong Chen, and several other researchers recognized that Thousand Island Lake would be a perfect place to explore these hypotheses about control of ecosystem structure. Construction of the Xin’an River Dam in 1959 created the lake of 573 km2 that is dotted with more than 1000 islands of varying size.  This creates a natural laboratory for ecologists interested in understanding how island size influences ecosystem structure and specifically to explore the relative importance of bottom-up vs. top-down effects.  In addition, these islands are actually forest fragments surrounded by a matrix that is inhospitable to terrestrial species.  Ecologists are very interested in how fragmentation influences ecosystem structure, because development projects (residential, commercial, public works, etc.) invariably produce fragments of habitat of varying size. Lastly, when establishing nature preserves or conservancies, conservation ecologists need to know how large their reserves should be in order to optimize biological diversity and ecosystem functioning.

The Thousand Island Lake showing a few of its thousand+ islands. Credit: Xiao-Yong Chen.

The major producer in this ecosystem is the evergreen tree, Castanopsis sclerophylla

Two Castanopsis sclerophylla trees. Credit: Xiao-Yong Chen.

Their seeds are eaten by two species of rodents, which in turn are eaten by carnivores – primarily snakes, cats and weasels. The researchers knew about these interactions before beginning the study, but they wanted to understand precisely how each player affected ecosystem structure, and how the size of the ecosystem influenced these different levels. They also wanted to explore possible bottom-up effects; for example how does environmental quality affect ecosystem structure.

Hypothesized top-down (orange arrows) and bottom up (green arrows) processes within the ecosystem.

For their study, Wang and his colleagues established research sites on habitats of three different size classes: four small islands (0.6 – 3.2 ha), three medium islands (13-51 ha) and six large habitats (three on the only large island of 875 ha and three on the mainland forest).  Initially the researchers conducted surveys of Castanopsis sclerophylla seedling density, rodent density and environmental conditions.  They discovered that seedlings were much more abundant on the mainland and large island (graph a below), while rodents were much more abundant on medium islands (graph b).  However, small islands were more subject to drought due to lower soil moisture content and higher temperatures – a result of greater surface area exposed to the sun along the perimeter of each small island (graph c and d).   Ecologists call this the edge effect. If you refer back to the first photo in this blog, you will note that the small island in the foreground has a great deal of exposed edge.

Over several years, the researchers systematically placed 12,500 seeds of Castanopsis sclerophylla on the surface across all of the sites, and tracked seed predation and seed dispersal.  Seeds on medium islands survived much more poorly than did seeds on the other habitats (top graph below). Wang and his colleagues also planted 2,750 seeds of Castanopsis sclerophylla in transects across all four sites.  In this case seedling emergence and survival was much lower on small islands than any of the other three habitats (bottom graph).

Top Graph. Survival rates of Castanopsis sclerophylla seeds after being moved away by rodents to a new location (left graph) and overall survival rates until the next spring (right graph). Bottom graph. Emergence rate of 2750 planted seeds (bottom left), and survival through summer (middle) and over the following winter (right).

Piecing together these data, we can see both top-down and bottom-up forces influencing ecosystem structure depending on the size of the habitat. On the mainland and on large islands there are several different types of predators which feed on rodents.  But medium and small islands are just too small to support viable populations of predators.  Thus rodents are super-abundant on medium islands, and eat the seeds that are on the surface.  This is an example of top-down effects causing a trophic cascade, with predators eating rodents, which leads to high seed survival on large habitats. However on medium islands,  predators are absent causing rodents to increase sharply and consume most of the seeds.

But bottom-up effects prevail on small islands, which are so small that that they support only a few rodents.  Seeds that are broadcast on the surface survive predation from the small rodent population relatively well, but seeds that are planted have poor survival because of low soil moisture and high temperature (the edge effect).  I asked Chen whether he thought we could generalize that top-down effects might be more important on large scales and bottom-up effects on small scales.  He responded that both types of regulation are likely to be scale-dependent in many different ecosystems, but that species composition and resource availability would determine how top-down vs. bottom-up control ultimately influences ecosystem structure.

note: the paper that describes this research is from the journal Ecology. The reference is Wang, R.,  Zhang, X.,  Shi, Y.‐S.,  Li, Y.‐Y.,  Wu, J.,  He, F., and  Chen, X.‐Y..  2020.  Habitat fragmentation changes top‐down and bottom‐up controls of food webs. Ecology  101( 8):e03062. 10.1002/ecy.3062.  Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2020 by the Ecological Society of America. All rights reserved.

Mangroves partner with rats in China

Many of us have seen firsthand the havoc that invasive plants can wreak on ecosystems.  We are accustomed to think of native plants as unable to defend themselves, much like a skinny little kid surrounded by a group of playground bullies. ‘Not so fast’ says Yihui Zhang.  As it turns out, many native plants can defend themselves against invasions, and they do so with the help of unlikely allies.

In southern China, mangrove marshes are being invaded by the salt marsh cordgrass, Spartina alterniflora, which is native to the eastern USA coastline. Cordgrass seeds can float into light gaps among the mangroves, and then germinate and choke out mangrove seedlings.  However, intact mangrove forests can resist cordgrass invasion.  Zhang and his colleagues wanted to know how they resist.

mangrove-Spartina ecotone

Cordgrass (pale green) meets mangrove (bright green) as viewed from space. Credit: Yihui Zhang.

Cordgrass was introduced into China in 1979 to reduce coastal erosion.  It proved up to the task, quickly transforming mudflats into dense cordgrass stands, and choking out much of the native plant community.  Dense mangrove forests grow near river channels that enter the ocean, and are considerably taller than their cordgrass competitors.  The last player in this interaction is a native rat, Rattus losea, which often nests on mangrove canopies above the high tide level. At the research site (Yunxiao), many rat nests were built on mangroves, using cordgrass leaves and stems as the building material.

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Rat nest constructed from cordgrass shoots rests upon a mangrove tree.  Credit Yihui Zhang.

Zhang and his colleagues suspected that cordgrass invasion into the mangrove forest was prevented by both competition from mangroves and herbivory by rats on cordgrass.

Baby rat in the nest

Baby rats in their nest. Credit Yihui Zhang.

 

To test this hypothesis, they built cages to exclude rats from three different habitats: open mudflats (primarily pure stands of cordgrass), the forest edge, and the mangrove forest understory, (with almost no cordgrass). They set up control plots that also had cages, but that still allowed rats to enter.

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Arrow points to resprouting cordgrass. Credit Yihui Zhang.

The researchers planted 6 cordgrass ramets (genetically identical pieces of live plant) in each plot and then monitored rodent grazing, resprouting of original shoots following grazing, and shoot survival over the next 70 days.

They discovered that the cages worked; no rats grazed inside the cages.  But in the control plots, grazing was highest in the forest understory and lowest in the mudflats (Top figure below).  Most important, both habitat type and exposure to grazing influenced cordgrass survival.  In the understory, rodent grazing was very important; only one ramet survived in the control plots, while 46.7% of ramets survived if rats were excluded.  In the other two habitats, grazing did not affect ramet survival, which was very high with or without grazing (Middle figure). Rodent grazing effectively eliminated resprouting of ramets in the understory, but not in the other two habitats (Bottom figure).

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Impact of rat grazing on cordgrass in the field study in three different habitats.  Top figure is % of stems grazed, middle figure is transplant survival, and bottom figure is resprouting after grazing (there was no grazing in the rodent exclusion plots). Error bars are 1 standard error. Different letters above bars indicate significant differences between treatments.

The researchers suspected that low light levels in the understory were preventing cordgrass from resprouting after rat grazing. This was most easily tested in the greenhouse, where light conditions could be effectively controlled.  High light was 80% the intensity of outdoor sunlight, medium light was 33% (about what strikes the forest edge) and low light was 10% the intensity of outdoor sunlight (similar to mangrove understory light).  Rat grazing was simulated by cutting semi-circles on the stembase, pealing back the leaf sheath, and digging out the leaf tissue. Cordgrass ramets were planted in large pots, exposed to different light and grazing treatments, and monitored for survival, growth and resprouting following grazing.

Greenhouse setup

Cordgrass growing in greenhouse under different light treatments. Credit: Yihui Zhang.

Zhang and his colleagues found that simulated grazing sharply reduced cordgrass survival from 85% to 7% at low light intensity, but had no impact on survival at medium or high light intensities.  Cordgrass did not resprout after simulated grazing at low light intensity, in contrast to approximately 50% resprouting at medium and high light intensity.

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Survival (top) and resprouting (bottom) of cordgrass following simulated grazing in the greenhouse experiment.

The researchers conclude that grazing by rats and shading by mangroves are two critical factors that make mangroves resistant to cordgrass invasion. Rats tend to build their nests near the mangrove forest edge, so it is not clear how far into the forest the rat effect extends. Rats do prefer to forage in the understory (rather than right along the edge), presumably because the understory helps to protect them from predators.  In essence, mangroves compete directly with cordgrass by shading them out, and also indirectly by attracting cordgrass-eating rats. Conservation biologists need to be aware of both direct and indirect effects when designing management programs for protecting endangered ecosystems such as mangrove forests.

note: the paper that describes this research is from the journal Ecology. The reference is Zhang, Y. , Meng, H. , Wang, Y. and He, Q. (2018), Herbivory enhances the resistance of mangrove forest to cordgrass invasion. Ecology. Accepted Author Manuscript. doi:10.1002/ecy.2233. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.