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.


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.


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).


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.


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.

Plant communities bank against drought

Many plants shed their young embryos (seeds) into the soil where they may accumulate in a dormant (non-growth) state over years before germinating (resuming growth and development). Ecologists describe this collection of seeds as a seed bank.  Marina LaForgia describes how scientists were able to germinate and grow to maturity some 32,000 year old Silene stenophylla seeds that was stashed, probably by an ancient squirrel, in the permafrost! With increased climatic variation predicted by most climate models, she wanted to know how environmental variability might affect germination of particular groups of species within a community.  In addition, she and her colleagues recognized that most ecological studies investigate community responses to disturbances by looking at the aboveground species.  It stands to reason that we should consider the below-surface seed bank as a window to how a community might respond in the future.


Some seedlings coming up from the seed bank. Credit:Marina LaForgia.

Seed banks can be viewed as a bet-hedging strategy that spreads out germination over several (or many) years to reduce the probability of catastrophic population decline in response to one severe disturbance, such as drought, flood or fire. In some California annual grassland communities, species diversity is dominated by annual forbs – nonwoody flowering plants that are not grasses. Many forbs produce seeds that can lie dormant in the seed banks for several years. Though these forbs are the most diverse group, there are also about 15 species of exotic annual grasses that dominate the landscape in abundance and cover. These grasses dominate because they produce up to 60,000 seeds per m2, they grow very quickly, and they build up a layer of thatch that suppresses native forbs. However, seeds from these grasses cannot lie dormant in the seed bank for very long.



Area of field site dominated by Delphinium (purple flower) and Lasthenia (yellow flower).  Looking closely you can also see some tall grasses rising. Credit Marina LaForgia.

How is drought affecting these two major components of the plant community? LaForgia and her colleagues answered this question by collecting seeds from a northern California grassland at the University of California McLaughlin Natural Reserve in fall 2012 (beginning of the drought) and fall 2014 (near the end of the drought). They used a 5-cm diameter 10-cm deep cylindrical sampler  to collect soil and associated seeds from 80 different plots.  The researchers also used these same plots to estimate aboveground-cover, and to identify the aboveground species that were present. The research team germinated and identified more than 11,000 seeds.


Plants germinating in the greenhouse. Credit Marina LaForgia.

The researchers knew from previous work on aboveground vegetation that exotic annual grasses declined very sharply in response to drought.  In contrast, the native forbs did relatively well, in part depending on their specific leaf area (SLA) – a measure of relative leaf size, with low SLA plants conserving water more efficiently. It seemed reasonable that these same patterns would be reflected belowground. Recall that most grass seeds are incapable of extended dormancy, while many forbs can remain dormant for several years. Consequently, LaForgia and her colleagues expected that grass abundance in the seed bank would decline more sharply than would forb abundance. In addition, they expected that high SLA forbs would not do as well as low SLA forbs during drought.

The researchers discovered very sharp differences between the two groups over the course of the drought. Exotic annual grasses declined sharply in the seed bank, while native annual forb abundance tripled.  Aboveground cover of grasses declined considerably, while aboveground cover of forbs increased modestly.  Clearly the exotic grasses were suffering from the drought, while the forbs were doing quite well.


(a) Seed bank abundance of grasses (red circles) and forbs (blue triangles) at beginning of drought (2012) and near end of drought (2014). (b) Percent cover of grasses (red circles) and forbs (blue triangles) at beginning of drought (2012) and near end of drought (2014). Data are based on samples from 80 plots. Error bars indicate one standard error.

We can see these differences on an individual species basis, with most of the grasses declining modestly or sharply in abundance, while most of the forbs increased.


Mean change in seed bank abundance per species based on 15 exotic grass species and 81 native forb species.

It is not surprising that the grasses do so poorly during the drought.  Presumably, less water causes poorer germination, growth, survival and seed production.  In addition, because grass seeds have a low capacity for dormancy, grass abundance will tend to decrease in the seed bank very quickly with such a low infusion of new seeds.

But why are the forbs actually doing better with less water available to them?  One explanation is that grass abundance and cover declined sharply, causing the forbs to experience reduced competition with grasses that might otherwise inhibit their growth, development and reproductive success. The tripling of native forbs in the seed bank was much greater than the 14% increase in aboveground forb cover.  The researchers reason that the drought caused many of the forb seeds to remain dormant, leading to them building up in the seed bank. This was particularly the case for low SLA forbs, which increased much more than did high SLA forbs in the seed bank.

We can understand exotic grass behavior in the context of their place of origin – the Mediterranean basin, which tends to have wet winters.  In that environment, natural selection favored individuals that germinated quickly, grew fast and made lots of babies. Since their introduction to California in the mid 1800s, 2014 was the driest year on record.  It will be fascinating to see if these exotic grasses can recover when, and if, wetter conditions return.  Can we bank on it?

note: the paper that describes this research is from the journal Ecology. The reference is LaForgia, M.L., Spasojevic, M.J., Case, E.J., Latimer, A.M. and Harrison, S.P., 2018. Seed banks of native forbs, but not exotic grasses, increase during extreme drought. Ecology99 (4): 896-903. 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.