Tag Archives: Grazing

Mystifying trophic cascades

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Within ecosystems, trophic cascades may occur when one species, usually a predator, has a negative effect on a second species (its prey), thereby having a positive effect on its prey’s prey. Today’s example considers the interaction between a group of predators (including several fish species, a sea snail and a sea star) their prey (the sea urchin Paracentrotus lividus) and sea urchin prey, which comprise numerous species of macroalgae that attach to the shallow ocean floor. These predators can negatively affect sea urchin populations either by eating them (consumptive effects), or by scaring them so they forage less efficiently (nonconsumptive effects). If sea urchins are less abundant or less aggressive foragers, the net indirect effect of a large population of fish, sea snails and sea stars will be an increase in macroalgal abundance.

Maldonado Halo

A large sea urchin grazing in a macroalgal community.  Notice the white halo surrounding the urchin, indicating that it has grazed all of the algae within that region. Credit: Albert Pessarrodona.

Many humans enjoy eating predatory fish, and we have overfished much of the ocean’s best fisheries including the shallow temperate rocky reefs (4 – 12 m deep) in the northwest Mediterranean Sea. Removing these predators has caused sea urchin populations to explode, overgrazing their favorite macroalgal food source, and ultimately leading to the formation of urchin barrens – large areas with little algal growth, low productivity and a small nondiverse assemblage of invertebrates and vertebrates.

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A sea urchin barrens whose macroalgae have been overgrazed by sea urchins. Credit: Albert Pessarrodona

Albert Pessarrodona became interested in this trophic cascade after years of diving in the Mediterranean. He noticed that in Marine Protected Areas, predatory fish abound and there are few visible urchins and lots of macroalgae. In nearby unprotected areas where fishing is permitted, urchins graze out in the open brazenly, and urchin barrens are common. He also wondered whether a second variable – sea urchin size – might play a role in this dynamic. Were large sea urchins relatively immune from predation by virtue of their large size and long spines, allowing them to forage out in the open even if predators were relatively common?

Urchinfig1

Interactions investigated in this study.  (a) Predators consume either small (left) or large (right) sea urchins (consumptive effects). (b) Sea urchins eat macroalgae. (c) Predators scare small or large sea urchins, reducing their foraging efficiency (nonconsumptive effects). (d) Predatory fish indirectly increase macroalgal abundance.

Pessarrodona and his research team used field and laboratory experiments to explore the relationship between sea urchin size and their survival and behavior in high-predator-risk and low-predator-risk conditions. High-risk was the Medes Islands Marine Reserve, which has had no fishing since 1983 and boasts a large, diverse assemblage of predatory fish, while low-risk was the nearby Montgri coast, which has a similar habitat structure, but allows fishing. The researchers tethered 40 urchins of varying sizes to the sea bottom (about 5m deep) in each of these regions, left them for 24 hours, and then collected the survivors to compare survival in relation to body size in high and low-risk conditions. They discovered that large urchins were much less likely to get eaten than were small urchins, and that the probability of getting eaten was substantially greater in the high-risk site.

UrchinFig3a

Probability of being eaten in relation to sea urchin size (cm) in high-risk (blue line) and low-risk (green line) habitats.

Pessarrodona and his colleagues followed this up by investigating whether the relatively predation-resistant large urchins were less fearful, and thus more likely to forage effectively, even in high-risk sites. Previous studies showed that sea urchins can evaluate risk using chemical cues given off by other urchins injured in a predatory attack, or given off by the actual predators. To explore the relationship between these cues and sea urchin behavior, the researchers put either large or small sea urchins into partitioned tanks with an injured sea urchin. Water flowed from one partition to the other, so the experimental sea urchins received chemical cues from the injured urchins. They also had a group of sea urchins placed in similar tanks without any injured sea urchins as controls. The experimental sea urchins were given seagrass to feed on, and the researchers calculated feeding rates based on how much food remained after seven days.

Small sea urchins were not deterred by the presence of an injured urchin (left graph below), while large sea urchins drastically reduced their feeding rates in response to the presence of an injured urchin (middle graph). This was startling as it flew in the face of the commonsense expectation that small sea urchins (most susceptible to predation) should be most fearful of predator cues. The researchers repeated the experiment (under slightly different conditions) placing an actual predator (a fearsome sea snail) on the other side of the partition. Again, large urchins showed drastically reduced foraging rates (right graph below).

UrchinFig4

Sea urchin responses to predation risk cues in the laboratory. When exposed to injured urchins – symbolized as having a triangle cut out – (A) small urchins did not reduce their grazing rate, while (B) large urchins drastically curtailed grazing. (C) When exposed to a predatory snail on the other side of a partition, large urchins sharply curtailed grazing. n.s = no significant difference, **P<0.01.

It turns out that large sea urchins are the critical players in this trophic cascade because they do much more damage to algal biomass than do the smaller urchins (we won’t go through the details of that research). The question then becomes how this plays out in natural ecosystems. Do consumptive and non-consumptive effects of predators in high-risk sites reduce sea urchin abundance and reduce the foraging levels of large sea urchins so that macroalgal cover is greatly enhanced? Pessarrodona and his colleagues surveyed high-risk and low-risk sites for sea urchin density and algal abundance. They set up 45 quadrats (40 X 40 cm) at each site, measured each sea urchin’s diameter, and estimated the abundance of each type of algae by harvesting a 20 X 20 cm subsample from each quadrat and drying and weighing the sample.

The findings were striking. Small and large sea urchins were much less abundant at high-risk sites than at low-risk sites (left graph below). At the same time, macroalgae were much more abundant at high-risk sites than at low-risk sites (right graph below).

UrchinFig5bc

(Left graph) Density of small and large sea urchins in high-risk and low-risk habitats. (Right graph) Biomass of macroalgae of different growth structures in high-risk and low-risk habitats. Canopy algae are taller than 10 cm, while turf algae are lower stature. Codium algae are generally not grazed by sea urchins. **P<0.01, ***P<0.001.

UrchinFig6a

Summary of interactions.  Arrow width indicates relative importance.

To summarize this system, predators reduce small sea urchin abundance by eating them (consumptive effects), and reduce large sea urchin foraging by intimidating them (nonconsumptive effects). The net indirect effect of predators on macroalgae is a function of these two effects. Large sea urchins are the major macroalgae consumers, but, of course, large sea urchins develop from small sea urchins.

The $64 question is why large sea urchins fear predators so much, while small (more vulnerable) urchins do not. The quick answer is that we don’t know. One possibility is that small sea urchins may be bolder in risky environments since they are more vulnerable to starvation (have fewer reserves), and also have lower reproductive potential since they are likely to die before they get large enough to reproduce. In contrast, large sea urchins can survive many days without food because of their large reserves. In addition, large urchins are close to sexual maturity, and thus may be unwilling to accept even a small risk to their well-being, which could interfere with them achieving reproductive success.

note: the paper that describes this research is from the journal Ecology. The reference is Pessarrodona, A.,  Boada, J.,  Pagès, J. F.,  Arthur, R., and  Alcoverro, T. 2019.  Consumptive and non‐consumptive effects of predators vary with the ontogeny of their prey. Ecology  100( 5):e02649. 10.1002/ecy.2649. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2019 by the Ecological Society of America. All rights reserved.

Mangroves partner with rats in China

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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.

zhangregenshoot

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).

Zhangfig2

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.

ZhangFig4

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.