Kelp consumption curtailed by señorita

Miranda Haggerty was diving through a kelp forest, and noticed that many kelp bore a large number of tiny limpets that were housed in small scars that they (or a fellow-limpet) had excavated on the kelp’s surface. This got her thinking about how these scars might affect the kelp, and equally relevant, whether there were any limpet predators that might lend the kelp a hand (or a mouth) by removing limpets.

Jerry Kirkhart

A limpet grazes on a kelp frond. Credit: Jerry Kirkhart

Feather boa kelp (Egregia menziesii) is a foundation species within the subtidal marine system off the California coast, providing food and habitat for many species that live on or among its fronds. The tiny seaweed limpet, Lottia insessa, specializes on feather boa kelp, grazing on its fronds and living within the scars. Many invertebrates and fish live within the kelp forest, but the most abundant fish is the señorita, Oxyjulis californica. Haggerty wondered whether the señorita might benefit the kelp (directly) by removing limpets, or (indirectly) by scaring limpets away – what ecologists call a trait-mediated indirect interaction.

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The señorita – a fearsome predator of limpets.  Credit: Miranda Haggerty

The first order of business was to determine whether the limpets were actually harming the kelp.  Haggerty and her colleagues approached this in two ways.  First they chose 94 kelp plants from kelp forests off the California coast.  From each individual they chose one grazed and one ungrazed frond (each 3 m long). Grazed fronds averaged 5-10 scars and at least 2 limpets per meter of length.  Every three weeks they visited their kelp to score for broken fronds. In 29 of 30 cases, the grazed frond broke before the ungrazed frond (in the remaining cases the entire plant was missing, or both fronds broke and the researchers could not tell which had broken first).

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Photo of feather boa kelp showing grazing scars, including one housing a limpet (left).  Diagram of feather boa kelp showing multiple fronds (right).

But the researchers were concerned that perhaps limpets chose to graze on weaker fronds, so the breakage was not caused by grazing scars, but by limpet choice.  To account for this concern, Haggerty and her colleagues chose 43 ungrazed kelp plants, placed three  limpets on one frond, and chose a second, equal-sized frond as an unmanipulated control. Once again, they visited their plants every three weeks, and discovered that grazed fronds broke first in all 20 pairs that the sequence of frond breakage could be determined.  Clearly, limpet grazing is bad news for feather boa kelp.

How does the señorita fit into this system? The researchers designed a laboratory experiment to address this question.  They used 10 large tanks (1700 L), and set up five different experimental treatments to compare direct effects of predation, and indirect effects of predator presence, on limpet grazing, and ultimately on kelp survival. To isolate the direct effects of predation from the indirect effects of predator cues on limpets, Haggerty and her colleagues placed four kelp fronds into fish exclosure cages, which were housed in the large tanks, and placed three limpets onto some of these fronds.  To mimic actual predation (CE treatment in Table below), they removed limpets by hand at a constant rate typical of señorita predation. For the NCE treatment (testing indirect effects of predator presence) they introduced señorita into the large tank so the limpets experienced the predator cues, but were not eaten. The different treatments are summarized in the table below. These experiments ran for one week and each treatment was replicated 10 times.

HaggertyTableFinalEach day the researchers monitored the number of limpets and grazing scars.  After one week, Haggerty and her colleagues counted the number of grazing scars, and measured the breaking strength of each frond by clamping the frond’s end to a table and pulling on the opposite end with a spring scale until it broke. They then recorded the amount of force needed to break the frond.

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Clamped kelp frond whose breaking strength has been tested.  Notice that the frond broke at a grazing scar (right). Credit Miranda Haggerty.

Not surprisingly, the predator control (PC) kelp (limpets present without señorita) had the most scars and lost the greatest amount of tissue.  Kelp receiving the consumptive predator effect treatment (CE) had fewer scars and lost less tissue than PC.  But interestingly, kelp receiving NCE and TPE treatments had significantly fewer scars than the CE kelp, and were statistically indistinguishable from each other.  Thus, in the laboratory, the presence of señorita cues (NCE treatment) was more important than actual predation (CE treatment) in reducing kelp scarring and tissue consumption (top and middle graph below).  As a result, the NCE treated kelp were stronger (had greater breaking strength) than were the CE treated kelp (bottom graph below).

HaggertyFig2

Mean (+ standard error) number of grazing scars (top), mass of tissue consumed (middle) and breaking strength (bottom) of kelp in response to five experimental treatments. CE = consumptive effect, NCE = non-consumptive effect, TPE = total predator effect, PC = predator control, LC = limpet control. Different letters above bars indicate significant differences between the means when comparing treatments.

Haggerty and her colleagues replicated this experiment, with a few experimental design modifications, in a field setting.  As with the laboratory experiment we’ve just discussed, the researchers found a very strong non-consumptive effect. The researchers suspect that these limpets respond to chemical cues emitted by their señorita predators. They could not respond to many types of sensory cues because they lack auditory organs, and the experimental design prevented fish from transmitting any shadows (visual cues) or vibrational cues. In addition previous studies have shown that some limpet species use chemoreception for predator avoidance, foraging and homing. However, the nature of this chemical cue is yet to be discovered for this predator-prey system.

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Schooling señorita. Credit: Miranda Haggerty

Trophic cascades occur when the effects of one species on another species cascade down through the ecosystem. In this case, señorita predators directly and indirectly reduce limpet density, which increases the survival of kelp – a foundation species for this ecosystem. The researchers point out that this trophic cascade only occurs in the southern feather boa kelp range, because señorita are absent further north.  We don’t know if limpets have other predators in the northern range, but we do know that the kelp are structurally more robust further north, so they (and the ecosystem) may be relatively immune to limpet-induced destruction.

note: the paper that describes this research is from the journal Ecology. The reference is Haggerty, M. B., Anderson, T. W. and Long, J. D. (2018), Fish predators reduce kelp frond loss via a trait‐mediated trophic cascade. Ecology, 99: 1574-1583. doi:10.1002/ecy.2380. 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.

Life and death in a diminutive ecosystem

Ecosystems are big things, as they encompass an entire community of organisms and the nonliving factors (such as nutrients and water) that interact with the community. So we’re accustomed to thinking about the Serengeti as an ecosystem, as it includes (among many things) the large animals, such as lions, wildebeest and buffalo that live there, the animals and plants they eat, and the soils and nutrients that feed these plants.

But ecosystems can also be tiny. Let’s think about an individual tank bromeliad, Quesnelia arvensis, which can hold up to 3 liters of water in tanks formed where individual leaves come together. Gustavo Romero has identified over 140 species of invertebrates that live within these natural tanks, including large predators such as damselfly and tabanid larvae, and many species of smaller predators (mesopredators) including a diverse group of chironomid midges. The larger predators eat the smaller predators, while predators of both sizes eat a very diverse group of detritivores – animals that feed on the remains of dead organisms. The terrestrial fauna in the immediate vicinity are spiders. Visitors from the surrounding forest ecosystem include 12 bird species and 6 frog species, which forage on larvae within the bromeliads.

Cantorchilus longirostris on bromeliad (Quesnelia arvensis) leaf

Long-billed marsh wren perches on the tip of bromeliad leaf.  This bird can use its long beak to probe for invertebrates living within the bromeliad tank. Credit: Crasso Paulo Bosco Breviglieri

Crasso Paulo Bosco Breviglieri and his colleagues had previously done research demonstrating how insectivorous birds hanging out near bromeliads inhibited dragonflies from ovipositing (laying eggs) within the bromeliad tank. As these birds were much larger than the animals living within the tanks, Breviglieri and Romero hypothesized that the birds would focus on eating the largest items offered to them by this ecosystem. By removing the largest items (the top predators), birds increase the biomass of the prey of these top predators, including detritivores. Thus bird predation should indirectly increase decomposition rate and nutrient availability.

Breviglieri food web

Effects of birds and frogs on bromeliad trophic cascades. Solid arrows are direct effects and dashed arrows are indirect effects (for example frogs eat top predators, thereby indirectly increasing mesopredators).  Wider arrows are stronger effects.

Trophic cascades, a process in which the effects of consumption within an ecosystem cascade down from higher to lower feeding levels, can be difficult to study. The problem is that one favorite approach is to remove predators (the top trophic level) and see if prey abundance increases while the food of these prey decreases, and so on. This is extremely challenging when top predators are lions or wolves and ecosystem area encompasses thousands of kilometers, but much easier when predators are birds or frogs, and each ecosystem is a tank bromeliad. Simply put a cage over a tank bromeliad and presto!, no birds or frogs can get in.

Dr. Crasso Paulo B. Breviglieri building the cages that isolated the bromeliads

Breviglieri with a caged bromeliad. Credit: Jennifer Tezuka

Breviglieri and Romero collected 30 tank bromeliads from the forest, and meticulously cleaned each plant to remove all organisms and organic matter. They filtered and homogenized the water from the bromeliads, and returned 1 liter of water to each plant so that each plant began the experiment with the same quantity of water and microorganisms. The researchers then added equal numbers of organisms to each bromeliad from all of the trophic levels, ranging from apex predators such as damselflies down to detritivores, such as shredders, which eat dead plant leaves and begin the break down process. They also added 10 leaves to each tank for detritivore consumption and further decomposition.

For their experiment, Breviglieri and Romero had three different treatments, with 10 bromeliads per treatment: (1) caged, with each bromeliad enclosed within a steel mesh that allowed insects through but restricted birds and frogs, (2) open-cage control, with each bromeliad only partially enclosed so predators had free access, (3) uncaged control. They returned these to the field at 40 meter intervals, and allowed 155 days to pass.

Larva of zygoptera on bromeliad (Quesnelia arvensis)leaf

Bromeliad with a damselfly larva (top predator) that for unknown reasons has climbed out of the tank onto a leaf.  A bird flew to a nearby perch, but the alert damselfly dove back down into the tank, earning a 9.6 from the judges. Credit: Crasso Paulo Bosco Breviglieri

After 155 days, Breviglieri and Romero collected all of the bromeliads, and identified, counted and weighed (dry weight) all of the organisms. They discovered that the dry mass of invertebrates was much greater in the caged treatments than either control (Figure A). The abundance of apex predators (damselflies and tabanids) did not increase; but the size of individuals increased dramatically (Figure B). Mesopredators increased in abundance (Figure C), while shredder abundance declined sharply (Figure D). Shredder larvae forage on sediment and are a favorite damselfly food item, so it is not surprising that shredders declined, given the sharp increase in damselfly size, and presumably appetite.

BreviglieriFig3ABCD

Lower shredder abundance in the caged bromeliads led to a sharp decline in decomposition rates (left graph below). In theory, this should make fewer nutrients available to the bromeliads and reduce bromeliad growth. In contrast to expectations, caged bromeliads actually grew more leaves (right graph below), despite the reduction in decomposition rates. Breviglieri and Romero remind us that the greater mass of larvae were producing a much greater mass of fecal matter and prey carcasses, both of which are very nutrient rich. Also, higher predation rates can cause some insects to mature and leave their tank at a smaller size, consuming fewer nutrients while in the larval form, and leaving more nutrients for each plant to use for its own growth.

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Decomposition rate measured as detrital mass lost (left graph), and growth rate measured as new leaves grown by the bromeliads (right graph), for caged, open-caged and uncaged controls.

Clearly, there are many unanswered questions about this trophic cascade. For example, why don’t the number of top predators increase in abundance when birds and frogs are excluded? When I asked him this question, Breviglieri suggested that two processes could explain this finding. First, top predators eat smaller larvae of their own species. Second, female insects can chemically sense the presence of predators in these bromeliads, and refrain from ovipositing in plants hosting large predators.

Perhaps most important, can we extend the conclusions from these small ecosystems to larger ecosystems? In nature there are many analogous ecosystems in which predators have strategies for crossing boundaries and influencing ecosystem processes. For example, many birds dive into lakes searching for fish and invertebrates. Moving in the opposite direction, banded-archerfish spit out water jets to dislodge invertebrates from adjacent vegetation into the water, and crocodiles leave rivers to grab and consume convenient gnus. In these systems, as in bromeliads, predators cross ecosystem borders to feed, and it is important for us to understand if there are any general patterns in how these visitors from the outside affect ecosystem functioning.

note: the paper that describes this research is from the journal Ecology. The reference is Breviglieri, Crasso Paulo Bosco, and Gustavo Q. Romero. 2017. Terrestrial vertebrate predators drive the structure and functioning of aquatic food webs. Ecology. doi:10.1002/ecy.1881.  It was published online on June 12, and should appear shortly in print. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2017 by the Ecological Society of America. All rights reserved.

Timely trophic cascades

While many of us appreciate oysters as delectable delights, we may underestimate the environmental benefits they also bring to the table. As filter feeders, they remove vast quantities of organic debris from the water, and as reef builders they protect our shorelines from violent wave action.

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Oyster reef. Credit: WFSU, Public Media

Of course, humans are not the only animals to enjoy eating oysters. For example, along portions of the Florida coast dominated by the reef-building oyster Crassostrea virganica, the mud crab, Panopeus herbstii, is a major consumer of juvenile oysters. In some locations, the average abundance of these voracious crabs can exceed 10 adults/m2 of reef. But all is not food and gravy for these crabs, as lurking in nearby burrows are equally voracious crab-eating toadfish, Opsanus tau. When toadfish are detected, the mud crabs will hide within the protective matrix of oyster shells and sediment that form the reef.

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A mud crab hiding among a cluster of oysters. Credit: WFSU, Public Media

By consuming mud crabs, toadfish are indirectly protecting oysters from being eaten. Ecologists call this a consumptive effect (CE). But David Kimbro and his colleagues have also shown than toadfish, by their mere presence, can also protect oysters by scaring the crabs into hiding. Since, in this case, they are not consuming the crabs, ecologists call this a non-consumptive effect (NCE). Together, CEs and NCEs should both increase oyster survival. More surviving oysters lead to higher overall feeding by oysters, which lead to more oyster poop, and more organic matter deposited into the sediment below. Ecologists call this type of relationship a trophic cascade, because the effects on one species cascades down through the ecosystem. In this case, increasing toadfish will decrease crabs, thereby increasing oysters and sediment organic matter. Conversely, decreasing toadfish should increase crabs, thereby decreasing oysters and sediment organic matter.

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Toadfish/mud crab/oyster/sediment organic matter (SOM) cascade. Dotted arrows are indirect effects

Kimbro and his colleagues wanted to explore this trophic cascade in more detail. They set up an experiment with 24 artificial reefs (made out of natural materials, except for the surrounding fence), which included 35 L of live oysters. They supplied each reef with 0, 2, 4, 6, 8 or 10 live crabs, and provided half of the reefs with a caged toadfish. They then measured oyster survivorship in relation to crab density in the presence or absence of predators.

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Setting up an artificial reef. Credit: WFSU, Public Media

The graphs below summarize their findings. The first thing to notice is that mud crabs were bad news for oysters, as survivorship plummeted when mud crabs were abundant. However, early in the experiment (graphs A and B) having a toadfish around helped out considerably. Oysters survived much better in the presence of toadfish (triangles and dotted curve) than they did without toadfish (circles and solid curve). But by the middle of the experiment (Graphs C and D), the toadfish no longer helped. Interestingly, by the end of the experiment (Graph E) the toadfish was once again helping the oyster’s cause, as survivorship was again greater in the presence of toadfish than in its absence. Realize that the difference between the dotted and solid curve is a measure of the NCE, as the toadfish are not eating the crabs (because they are caged). So we can conclude that there was a strong NCE early on, which waned in the middle of the experiment and then returned by the end of the experiment.

Kimbrograph

A second finding is that the reef grew (expanded) when there were no crabs present, but that even two crabs were enough to reduce reef growth to zero. In addition sediment organic matter was greatest when there were either none or only two crabs present in the reef. Four or more crabs in the reef reduced the deposition of sediment organic matter. These findings were not influenced by the presence or absence of toadfish.

This is a complicated system, but we (and toadfish, crabs and oysters) live in a complicated world. And there are several other complications that I have not even mentioned! We might argue that the crabs may habituate (get accustomed) to these toadfish, so that by the middle of the experiment, the toadfish NCE had worn off. That begs the question of why the NCE returned towards the end of the experiment. Kimbro suggests that at the beginning of the experiment, the novelty of the predator cue probably caused strong NCEs. But by the middle of the experiment, the crabs became hungry and chose to forage regardless of predator cue. Finally, towards the end of the experiment, the crabs, having filled up on juvenile oysters, opted to hide rather than forage when toadfish were present. Whatever the reason, these findings caution us that if we want to understand trophic cascades, we need to consider the dimensions of both space and time.

note: the paper that describes this research is from the journal Ecology. The reference is Kimbro, D. L., Grabowski, J. H., Hughes, A. R., Piehler, M. F., & White, J. W. (2017). Nonconsumptive effects of a predator weaken then rebound over time. Ecology 98(3): 656-667. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2017 by the Ecological Society of America. All rights reserved.