Mystifying trophic cascades

October 2, 2019 by fredsingerecology

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.

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.

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?

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.

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).

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).

(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.

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.

The complex life of the pea

April 15, 2019 by fredsingerecology

As a behavioral ecologist, I’m spending a surprising amount of time reading and writing about plants these days. It turns out that plants are amazingly complex and interactive; you just need to know where and how to look. Today we will discuss the humble pea plant, how it is infected with a virus that is carried by an aphid that sucks its xylem, and how a herbivorous weevil fits into the whole system. The virus is the pea enation mosaic virus (PEMV), which causes pea leaves to yellow and wither, and also creates enations (scaly tissue) to develop on a leaf’s undersides. The aphid vector (a vector is the organism that carries a disease) is Acrythosiphon pisum, while the herbivorous weevil is Sitona lineatus.

Pea plant infected with pea enation mosaic virus. Credit Paul Chisholm.

David Crowder has been studying plant/insect interactions for many years, and knew that most researchers who studied interactions between plants and insect vectors focused their attention on the plants, insects and the disease, but did not consider how other species in the community might affect this relationship. Paul Chisholm was a PhD student in Crowder’s lab; and working with two other researchers, they explored whether S. lineatus, an abundant herbivore of peas, influenced viral transmission. They expected that if the pea was first attacked by the weevil, it might be more susceptible to subsequent viral infection. Conversely, if the pea was infected by the virus, it might be less able to chemically defend itself against subsequent herbivory by the weevil.

(Left) Pea aphids. Credit: Shipher Wu under a Creative Commons Attribution 4.0 International Public License. (Right) Very adult pea leaf weevils, Sitona lineatus. Credit: Gail Hampshire under a Creative Commons Attribution 4.0 International Public License

It is easy to visually distinguish between PEMV-infected and uninfected plants, so the researchers could assess whether infected plants tended to suffer more defoliation by weevils than did uninfected plants. They visited 12 different fields in northern Washington and western Idaho, USA, and measured defoliation by counting the number of feeding notches left by the weevils after feeding on 3 – 10 infected pea plants and an equal number of nearby uninfected plants on each field (more feeding notches = more defoliation). They discovered that PEMV-infected plants tended to suffer substantially higher herbivory than did uninfected plants

Herbivory (as measured by number of feeding notches) caused by weevils on paired uninfected (black bars) and PEMV-infected (blue bars) pea plants sampled from 12 different fields. Error bars for all figures represent 1 SE.

Given the correlation between herbivory and infection, Chisholm and his colleagues then explored whether (1) the weevil preferred to feed on infected plants, and/or whether (2) infective aphids preferred to feed on plants that had been damaged by herbivorous weevils. Both questions were answered with behavioral choice assays done in a greenhouse. First, the researchers created two groups of pea plants. The first group, sham infected, were fed on by aphids not carrying PEMV for 48 hours, while the second group of plants were fed on by PEMV-infected aphids for the same duration. Aphids were removed and PEMV infection developed within 15 days in the PEMV infected plants. The researchers then set up one sham infected and one PEMV-infected plant in a test cage, and released two weevils equidistant from the plants, allowing them to feed for six days. They discovered that aphids fed much more voraciously on the PEMV-infected plants.

Mean leaf area removed from sham infected and PEMV-infected pea plants.

For the second experiment, the researchers again created two types of plants: undamaged – no herbivory, and damaged – 48 hours of weevil herbivory. Weevils were then removed, and one leaf from each plant was connected to each end of a tube, while still attached to each plant.

Experimental setup with tube attached to one leaf of each experimental plant. Aphids were introduced into the central tube. Credit Paul Chisholm.

The researchers added either 25 infectious or 25 non-infectious aphids, and allowed them 3 hours to choose a leaf. PEMV-infected aphids preferred damaged leaves, while uninfected aphids showed no preference.

PEMV-infected aphid preference for undamaged (no herbivory) or damaged (weevil herbivory) leaves.

Chisholm and his colleagues then turned their attention to whether weevil herbivory made pea plants more susceptible to PEMV infection. In one experiment they allowed PEMV-infected aphids to feed on plants for 3 days, and then introduced 0, 1 or 3 weevils who fed on the plants for another 6 days. They used a protein assay to estimate the PEMV-titer (concentration) of each plant and discovered that the plants that were exposed to greatest herbivory had the highest PEMV titer (see graph below). In a second experiment the researchers allowed weevil herbivory before adding the aphids, and found no effect of prior herbivory on PEMV titer.

Relative PEMV-titer of infected leaves after they were subjected to herbivory by zero, one or three weevils for six days. different letters above bars indicate significant differences between treatments.

What causes these plant responses to challenges by PEMV and weevils? The researchers discovered that levels of three important plant hormones increased either in response to PEMV infection, weevil herbivory or both. At this point it is not clear how these different hormone levels interact to bring about the changes we’ve described.

The researchers conclude that weevil behavior has a profound influence on the interactions between aphids, the viruses they carry and the pea plants they feed on (and infect). The weevil is not a vector for the virus, yet it affects the virus directly by altering plant behavior and physiology and indirectly by altering the behavior of the vector (the aphids). PEMV outbreaks are more likely when weevils are abundant, as aphids prefer damaged plants, and feeding by weevils increased the PEMV titer in infected plants. Crowder argues that interactions in which a non-vector species influences the relationship between a host and its vector (and the pathogen it carries) are probably extraordinarily common in crop systems. So if we want to understand crop susceptibility to pathogens we need to cast a broad net and consider both the direct and indirect effects of a community of species that can influence how the crop responds to infection.

note: the paper that describes this research is from the journal Ecology. The reference is Chisholm, P. J., Sertsuvalkul, N. , Casteel, C. L. and Crowder, D. W. (2018), Reciprocal plant‐mediated interactions between a virus and a non‐vector herbivore. Ecology, 99: 2139-2144. doi:10.1002/ecy.2449. 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.

Kelp consumption curtailed by señorita

July 10, 2018 by fredsingerecology

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.

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.

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).

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.

HaggertyTableFinal Each 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.

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).

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.

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.

Indirect effects of the lionfish invasion

May 28, 2018 by fredsingerecology

I’m old enough to remember when ecological studies of invasive species were uncommon. Early on, there was a debate within the ecological community whether they should be called “invasive” (which conveyed to some people an aggressive image akin to a military invasion) or more dispassionately “exotic” or “introduced.” Lionfish (Pterois volitans), however, fit this more aggressive moniker. Native to the south Pacific and Indian Oceans, lionfish were first sighted in south Florida in 1985, and became established along the east Atlantic coast and Caribbean Islands by the early 2000s. They are active and voracious predators, consuming over 50 different species of prey in their newly-adopted habitat. Many population ecologists study the direct consumptive effects of invasive species such as lionfish. In some cases they find that an invasive species may deplete its prey population to very low levels, and even drive it to extinction.

A lionfish swims in a reef. Credit: Tye Kindinger

But things are not always that simple. Tye Kindinger realized that lionfish (or any predator that feeds on more than one species) could influence prey populations in several different ways. For the present study, Kindinger considered two different prey species – the fairy basslet (Gramma loreto) and the blackcap basslet (Gramma melacara). Both species feed primarily on zooplankton, with larger individuals monopolizing prime feeding locations at the front of reef ledges, while smaller individuals are forced to feed at the back of ledges where plankton are less abundant, and predators are more common. Thus there is intense competition both within and between these two species for food and habitat. Kindinger reasoned that if lionfish depleted one of these competing species more than the other, they could be indirectly benefiting the second species by releasing it from competition.

Fairy basslet (top) and blackcap basslet (bottom). Credit Tye Kindinger.

For her PhD research, Kindinger set up an experiment in which she manipulated both lionfish abundance and the abundance of each basslet species. She created high density and low density lionfish reefs by capturing most of the lionfish from one reef and transferring them to another (a total of three reefs of each density). She manipulated basslet density on each reef by removing either fairy or blackcap basslets from an isolated reef ledge within a particular reef. This experimental design allowed her to separate out the effects of predation by lionfish from the effects of competition between the two basslet species. Most of her results pertained to juveniles, which were about 2 cm long and favored by the lionfish.

KindingerTable

Alex Davis captures and removes basslets beneath a ledge. Credit Tye Kindinger.

Kindinger measured basslet abundance in grams of basslet biomass per m² of ledge area. When lionfish were abundant, juvenile fairy basslet abundance decreased over the eight weeks of the experiment (dashed line) but did not change when lionfish were rare (solid line). In contrast, juvenile blackcap basslet populations remained steady over the course of the study, whether lionfish were abundant or rare. Kindinger concluded that lionfish were eating more fairy basslets.

Abundance of juvenile fairy basslets (left) and blackcap basslets (right) as measured as change in overall biomass. Triangles represent high lionfish reefs and circles are low lionfish reefs.

Competition is intense between the two basslet species, and can affect feeding position and growth rate. Kindinger’s manipulations of lionfish density and basslet density demonstrate that fairy basslet foraging and growth depend primarily on the abundance of their blackcap competitors. When competitor blackcap basslets are common (approach a biomass value of 1.0 on the x-axis on the two graphs below), fairy basslets tend to move towards the back of the ledge, and grow more slowly. This occurs at both high and low lionfish densities.

Change in feeding position (top) and growth rate (bottom) of fairy basslets in relation to competitor (blackcap basslet) abundance (x-axis) and lionfish abundance (triangles = high, circles = low)

In contrast, blackcap basslets had an interactive response to fairy basslet and lionfish abundance. Let’s look first at low lionfish densities (circles in the graphs below). You can see that blackcap basslets tend to move towards the back of the ledge (poor feeding position) at high competitor (fairy basslet) biomass, and also grow very slowly. But when lionfish are common (triangles in the graphs below), blackcap basslets retain a favorable feeding position and grow quickly, even at high fairy basslet abundance.

Change in feeding position (top) and growth rate (bottom) of blackcap basslets in relation to competitor (fairy basslet) abundance (x-axis) and lionfish abundance (triangles = high, circles = low)

By preying primarily on fairy basslets, lionfish are changing the dynamics of competition between the two species. The diagram below nicely summarizes the process. Larger fish of both species forage near the front of the ledge, while smaller fish forage further back. But there is an even distribution of both species. Focusing on juveniles, they are relatively evenly distributed in the rear portion of the ledge (Figure B). When fairy basslets are removed experimentally, the juvenile blackcap basslets move to the front of the rear portion of the ledge, as they are released from competition with fairy basslets (Figure D). Finally, when lionfish are abundant, fairy basslets are eaten more frequently, and juvenile blackcaps benefit from the lack of competition (Figure F)

KindingerFig3

Kindinger was very surprised with the results of this study because she knew the lionfish were generalist predators that eat both basslet species, so she expected lionfish to have similar effects on both prey species. But they didn’t, and she does not know why. Do lionfish prefer to eat fairy basslets due to increased conspicuousness or higher activity levels, or are blackcap basslets better at escaping lionfish predators? Whatever the mechanism, this study highlights that indirect effects of predation by invasive species can influence prey populations in unexpected ways.

note: the paper that describes this research is from the journal Ecology. The reference is Kindinger, T. L. (2018). Invasive predator tips the balance of symmetrical competition between native coral‐reef fishes. Ecology, 99(4), 792-800. 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.

Mangroves partner with rats in China

May 13, 2018 by fredsingerecology

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.

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 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.

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.

Cottonwood genes and spider hostels

March 22, 2017 by fredsingerecology

Back in my working days, people that I met would sometimes ask me what I did for my research. I usually told them that I studied spider sex, which, while true, was a bit misleading, as my interests were actually slightly broader. But studying spider sex was a good fit for my disposition, because, more than anybody I know, I can stare at something for a very long time and not get bored. And when spiders have sex, there can be very long periods, when, to our eyes, nothing is going on. As it turns out there is a great deal of pheromonal communication going on, and considerable vibrational activity as well, but it is not that easy for humans (even abnormally patient ones) to detect.

A spider and her three egg cases within a web she has built in a Taphrina blister. Credit Matt Barbour

The point is that I have a very soft spot in my heart for spiders, and was delighted to learn about an indirect process that provided a comfortable home for needy spiders. Heather Slinn got interested in her project while an undergraduate summer intern. Her colleague, Matt Barbour, pointed out that when he flipped over blistered black cottonwood leaves (Populus trichocarpa) he often found a spider hanging out in there. This observation led to her to study the relationship between cottonwood trees, cottonwood genetics, pathogens that make leaf blisters and spider occupancy rates.

Taphrina fungi form cup-like blisters in the leaves of Populous trees. But these trees vary in how susceptible they are to leaf blisters. The researchers wanted to answer three questions about this relationship. First, do spiders prefer to live in leaf-blisters as opposed to unblistered leaves? Second, are differences in tree susceptibility to Taphrina a result of genetic differences between the trees? And third can differences in Taphrina-resistance account for differences in spider density?

One of the keys to the experiment was establishing a garden with distinct clones of trees of known genetic makeup (genotypes). Slinn and her colleagues studied five different genotypes, with approximately 40 trees per genotype. They dutifully watered them throughout the summer, and then sampled up to 30 leaves from each tree for blister density, blister size, and spider residency, using a modified shop vac to suck up all of the spiders.

Black Cottonwood garden. Credit Matt Barbour

The researchers discovered that blistered leaves were 35 times more likely to have a spider and/or spider web than were unblistered leaves. Clearly spiders found blistered leaves to be highly attractive homes.

But there were pronounced differences among the five genotypes in blister density, blister size, spider density and the probability that a spider was occupying a blister. Graph A shows that genotypes 1 and 3 (G1 and G3) had the lowest mean density of blisters (about 2 or 3 per meter of plant), while G4 averaged about 20 blisters per meter. Although G3 had relatively few blisters, it did boast the largest blisters (see graph B). The researchers concluded that blister density and size were both under genetic control, but not linked to each other.

Mean (A) blister density (number per meter of plant) and (B) blister size, for the five tree genotypes.

But how did blister density and size influence spider residency? G4, the genotype with the greatest number of blisters per plant, also had the greatest number of spiders (graph C). But on a per blister basis, we can see that the two genotypes with the largest blisters (G2 and G3 – see graph B) also had the highest probability of housing a spider in their blisters (graph D). So when spiders make decisions about where to live, both size and number are important.

Mean (C) spider density and (D) probability a blister hosts a spider, for the five tree genotypes.

It is unclear why the spiders are attracted to blisters. Some spider species have been shown to be attracted to structural complexity, because that provides more or better attachment points for web strands and egg cases. Depressed blisters may also give protection from abiotic factors such as wind and precipitation.

Like most good studies, this research raises a host of related questions. Why is there so much genetic variation in Taphrina-resistance within this tree species? Slinn suggests that there may be tradeoff whereby investment into Taphrina-resistance might compromise a plant’s ability to invest in other functions such as cold-resistance, or rapid growth and/or high reproductive rates. A second question is how does spider presence influence other species – for example does hosting a spider reduce the number of herbivorous insects that might attack the tree? A third issue raised by the authors is that plants infected with Taphrina may be weaker and more susceptible to herbivores. In that case, the spiders may be present in blisters because they are attracted to the herbivores that are eating the leaves. And finally, herbivores eating the leaves may transmit other diseases affecting our forests, such as dutch elm disease, chestnut blight and white pine blister rust. Unraveling this complex chain of events will keep researchers busy for many years.

note: the paper that describes this research is from the journal Ecology. The reference is Slinn, H. L., Barbour, M. A., Crawford, K. M., Rodriguez‐Cabal, M. A., & Crutsinger, G. M. (2016). Genetic variation in resistance to leaf fungus indirectly affects spider density. Ecology 98(3): 875-881. 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

March 8, 2017 by fredsingerecology

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.

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.

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.

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.

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.

Chironomids: the great Icelandic farmers

February 7, 2017 by fredsingerecology

Ecologists describe plants and algae as producers because, with the help of solar energy, they produce sugar and other complex carbohydrates from carbon dioxide in the process we call photosynthesis. Consumers, such as horses, chironomids and lions, eat producers or other consumers, using the chemical energy in their food’s complex molecules to fuel their own metabolic processes. Without photosynthesis there would be almost no life, as consumers would need to scavenge the organic molecules that happened to be lurking about in the environment.

You’ll notice I slipped in chironomids as consumers, because they are the diminutive heroes of this tale. There are actually more than 10,000 chironomid species, but the ones we are discussing lay their fertilized eggs into lake water where they sink into the sediment and hatch out as larvae. These larvae go through several growth stages, building tubes which serve as their houses during growth and development. Larvae then transform into pupae, which after a few days swim to the surface and metamorphose into winged adults, which mate and produce more fertilized eggs.

Chironomid Larvae. Credit Michael Drake

Larval tubes in sediment. Credit Cristina Herren

We usually think about consumers as having a negative effect on their food and/or prey. If we introduce a herd of sheep into a small pasture, we are confident that the grass will quickly disappear inside of sheep bellies. Similarly, if we introduce a few lions into a pen of sheep, we can be fairly confident that the sheep population will decline. But consumer effects on populations can act in strange and wonderful ways.

The subarctic Lake Mývatn in Iceland is host to an amazingly huge number of chironomid larvae; over 100,000 of these insects can squeeze into 1 m² of lake bottom!

Lake Myvatn. Credit Michael Drake

Swarming adult chironomids. Credit Michael Drake

As Cristina Herren describes, Lake Mývatn has long been studied because of the dramatic changes in chironomid densities. Chironomid populations can increase 10-fold in each of four or five consecutive generations during the subarctic spring and summer. So if you began with a density of 10 chironomids/m² in April, you might find 100/m² in May, 1000/m² in June, 10,000/m² in July and 100,000/m² in August. Herren was intrigued by this exponential growth, as it suggested that somehow chironomid food resources (primarily algae) were keeping pace with the exploding chironomid population, despite being eaten by this ever-expanding population. How could the algae keep pace with the furious chironomid growth rate? Herren wondered whether the chironomids were acting as farmers and somehow stimulating algal production.

Herren worked with several other researchers to figure out the answer to this puzzle. First, they wondered whether the larval tubes provided an awesome place for algae to live. Second, perhaps chironomids were pooping-out vast quantities of nutrient-rich waste products, which algae used to build their bodies. Either or both of these positive effects could more than compensate for the direct negative effect from chironomids eating the algae.

To investigate both hypotheses, the researchers set up 1-liter clear plastic containers with lake sediment and either 0, 50, 100, 200, 400, 600, 800 or 1200 chironomids (that must have been fun to count!). They placed six or seven containers with each population size into racks at the bottom of the lake.

The first task was to discover whether production actually increased with chironomid abundance. Oxygen is a waste product of photosynthesis, so scientists use oxygen production to measure photosynthetic rate, and also to infer algal abundance. They found that oxygen production actually increased with chironomid abundance. Note that chironomids (and the algae too) actually consume oxygen (just like you and I do) in the process of respiration, so this is a truly remarkable result. It indicates that production increased so much that it more than compensated for the oxygen used up by the chironomids and algae from respiration.

oxygenvslarvae

The algae use chlorophyll a in their cells as the molecule for photosynthesis, so algal abundance can be estimated by measuring how much chlorophyll a is present in each bottle. Again, they found more chlorophyll a in the bottles with more chironomids, despite the fact that chironomids were eating all the algae they could find.

chlorphyllvslarvae

In addition, the chironomids from more crowded conditions weighed more than those from sparsely-populated bottles. The researchers concluded that by eating algae, the chironomids were actually increasing algal abundance, thereby creating more food for themselves.

These findings fly in the face of our usual assumptions about consumers reducing the population size of the species they are consuming. The researchers confirmed two important indirect effects of chironomids on algae. First, the chironomid larvae do excrete vast quantities of concentrated nutrients (nitrogen and phosphorus) that are consumed by the algae. In addition, the chironomids tubes are indeed ideal surfaces for algae to hang-out on, as evidenced by finding much more chlorophyll a on the tubes than in the nearby sediment.

We citizens need to recognize that both direct and indirect effects operate within ecosystems. In this case, algae are clearly directly benefitting chironomids by providing them with food. Less obvious, the chironomid effects on algae are in two directions. Chironomids have a direct negative effect on algal populations by consuming vast quantities of algae. However, they have a stronger indirect positive effect on algal populations, by providing algae with high quality housing and abundant resources, so that the algal population grows dramatically over the year. The net effect of chironomids on algal populations (dashed arrow) is positive.

chironfigblog

Most ecosystems have many different direct and indirect effects operating between a large number of species. It’s a real challenge to identify and understand these diverse interactions, which is why we need to be cautious about changing ecosystems in significant ways. For example, when we dump our waste products into waterways or soils, the added nutrients can have pronounced direct and indirect effects on the species that live there. In many cases, we won’t be able to identify the unintended consequences of our actions on an ecosystem until the native species have gone extinct.

note: the paper that describes this research is from the journal Ecology. The reference is Herren, Cristina M., et al. “Positive feedback between chironomids and algae creates net mutualism between benthic primary consumers and producers.” Ecology 98.2 (2017): 447-455. 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.

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