Tag Archives: Predation

The buzz on trophic cascades

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Herbivores, by their nature, damage plants in natural ecosystems and in agricultural systems.  And predators, by their nature, do a lot of damage to herbivores, either by eating them, or by harassing them in ways that cause them to change their behavior, or in some cases change their morphology or physiology (these are called nonconsumptive effects).  The indirect effect of a trophic cascade in which predators damage herbivores which damage plants, is that predators can benefit plants by their detrimental effect on herbivores.

Much of the research on nonconsumptive effects has focused on aquatic systems because the predator cues are easy to manipulate in the laboratory.  Simply let a predator hang out in a water tank for a while, and then add the predator tank water to a tank with a possible prey item, and study the prey’s response. But there has been little work on nonconsumptive effects in terrestrial systems.  While there has been some research on how auditory cues emitted by terrestrial predators affect vertebrate herbivores, there has been almost no work on how auditory cues affect invertebrate herbivores.  This is surprising, because invertebrates cause enormous damage to agricultural systems. Evan Preisser and his students wondered whether the beet armyworm caterpillar, Spodoptera exigua, a voracious herbivore on many commercially important crops, responded to buzzing emitted by an important predator, the caterpillar-hunting paper wasp (Mischocyttarus sp.). More important, they tested whether the response was substantial enough to have an impact on caterpillar mortality, and subsequent plant development.

Four Spodoptera caterpillars chomp on a soybean leaf. Credit: Michasia Dowdy, University of Georgia, Bugwood.org

Perhaps the biggest challenge was technical.  The researchers needed to come up with a mechanism for delivering an auditory cue to one group of caterpillars that would not be detected by any other nearby group.  They tried various conformations, including separating the cages with soundproofing foam, which, unfortunately, was not soundproof to wasp buzzes.

One of the failed attempts at auditory isolation. Unfortunately, the auditory stimulus was detectable up to two boxes away from the source. Credit: Zachary Lee.

Nothing worked until one of the students suggested using boxes that dry ice was shipped in, reasoning correctly that it should have good insulating properties.  The decibel meter failed to detect any sound from adjacent boxes.

This worked! Credit: Zachary Lee.

Having solved the soundproofing problem, the researchers raised 36 groups of five caterpillars in small cups filled with 25 grams of caterpillar diet. Each cup was placed in a box and subjected to one of three treatments: no-sound control, recorded buzzing of a non-predatory mosquito, or recorded buzzing of a predatory wasp.  The volume was the same for both sound treatments. Each tape went for 12 hours per day, with 2 seconds on, followed by 6 seconds off.  The researchers found that survival was substantially lower for caterpillars that received the wasp treatment (top graph below).  Also, caterpillars that survived the wasp treatment took, on average, longer to develop (bottom graph below), though that difference was not statistically significant.

Survival (top graph ), weight (middle) and time to pupation (bottom) of Spodoptera caterpillars subjected to no sound (green bar), mosquito buzz (yellow) and wasp buzz (red). Different letters above bars indicated statistically significant differences between treatments.

Preisser’s graduate student, Zachary Lee, took the lead in organizing the field experiment.  The researchers wanted to know whether the negative effect of wasp buzzes that they detected in the laboratory had real consequences for agricultural systems.  They surrounded each tomato plant (72  in all) with a mesh bag (to keep the caterpillars in and other insects out), and placed an average of 96 newborn caterpillars on each plant.  Each group of four plants surrounded a speaker that emitted either no sound (control), mosquito buzzing, or wasp buzzing, which were broadcast at levels that caterpillars would experience when an insect was 5 cm away from them.  Each sound was played in a loop of 1 minute on, followed by 10 minutes off, for 12 hours per day.  Lee and his colleagues let the experiment run for 3 weeks, by which time all caterpillars had either pupated or died. They harvested each plant, and calculated the percentage of leaves that were damaged by caterpillars.  Then they dried each plant, including the roots, and weighed them.

Field experiment with four tomato plants positioned equidistant from one central speaker. Each group of four received one of the experimental treatments. Credit: Zachary Lee.

Plant leaves associated with wasp buzzing received the least damage, leaves on control plants received the most damage, and leaves on plants with mosquito buzzing received intermediate damage. Aboveground mass was greater in wasp treated plants than in controls, so the sound of wasp buzzing helps to protect the tomato plants against voracious caterpillar herbivores.

Indirect effects of no sound (green bar), mosquito buzz (yellow) and wasp buzz (red) on tomato plants, via the effects of these treatments on Spodoptera herbivory. Different letters above bars indicated statistically significant differences between treatments.

The researchers did not study caterpillar behavioral changes because these caterpillars are easily disturbed, either freezing or dropping off of plants when approached.  Lee and his colleagues point out that we know very little about how invertebrates, in general, respond to sound cues, as their survey of the literature on prey response to sound cues showed that 181/183 experiments used vertebrate prey.  Given how widespread invertebrates are in agricultural systems, and in ecosystems in general, we need more studies to get a better handle on how invertebrates respond to sound, and most important, how their response influences agricultural systems and ecosystem structure and functioning.

note: the paper that describes this research is from the journal Ecology. The reference is Lee, Z.A., Cohen, C.B., Baranowski, A.K., Berry, K.N., McGuire, M.R., Pelletier, T.S., Peck, B.P., Blundell, J.J. and Preisser, E.L., 2023. Auditory predator cues decrease herbivore survival and plant damage. Ecology, p.e4007. https://doi.org/10.1002/ecy.4007. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2023 by the Ecological Society of America. All rights reserved.

Introduced quolls quell melomys

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The cane toad has the distinction of being the world’s largest toad.  It was introduced to Australia in 1935 to control cane beetles that were eating sugarcane (see A toxic brew: toad vs. quoll).  Since their introduction, cane toads have expanded their range by over 2000 km from their release sites, which would be fine if all they did was eat cane beetles.  As it turns out, they are worthless at eating cane beetles, but are very good at being eaten by many predators, including the northern quoll (Dasyurus hallucatus).  This turns out poorly for the quolls, as cane toads are loaded with toxins, which quickly convert a cane-toad-fed quoll into a quoll corpse. Consequently, quoll populations are collapsing across much of Australia.

A northern quoll sports a radio collar. Credit: Chris Jolly

For his PhD work, Chris Jolly was hoping to explore whether he could use behavioral conditioning techniques to train quolls to avoid cane toads before he released them back into the environment.  Unfortunately, while in captivity, the quolls lost their fear of predators, and became easy prey for dingoes, which resulted in a failed reintroduction to Kakadu National Park. In an interesting twist, another graduate student was releasing quolls onto Indian Island for a different purpose, and Jolly decided to regroup and focus his attention on how the prey population responded to a novel predator. In 2017, 54 quolls were released on the northern part of the island, which set up a natural experiment in which quolls were present in the north, and absent in central and southern Indian Island

Ben Phillips and John Moreen release the first batch of northern quolls on Indian Island (Kabarl), Northern Territory, Australia. Credit: Chris Jolly

Working with several researchers, Jolly established four research sites in the north and three in the south.  At each one-hectare site, the researchers set up a 10 X 10 grid of live-traps which they baited with balls of peanut butter, rolled oats and honey (100 traps at each site). The target species was the grain-eating rodent, Melomys burtonia. Over the course of the study, 439 individual melomys were captured, weighed, sexed and implanted with a microchip for identification purposes. The researchers wanted to know how the presence of predaceous quolls influenced melomys abundance, and whether melomys adjusted behaviorally to quoll presence.  

Research sites on Indian Island. Quolls were introduced to the northern part of the island in 2017.

They discovered that the three southern sites (without quolls) maintained relatively steady numbers of melomys throughout the study.  In contrast, the four northern sites (with quolls) showed a sharp decrease in melomys abundance. Complicating the issue, a wildfire broke out in August 2017, affecting only the northern part of the island.  The researchers believe this fire did not affect the melomys in any significant way, as wildfires are common in the area, and several previous studies have shown no effect of wildfires on melomys abundance.

Melomys population estimates at three southern sites (left graph) and four northern sites (right graph). The dashed orange line denotes quoll introduction, while the dashed red line indicates the wildfire in 2017. Error bars are 95% confidence intervals.

Shyness can be an adaptive behavior if predators are in your environment.  Jolly and his colleagues wanted to know if there was any difference in the shyness (or conversely – the boldness) of melomys from the north (with quolls) and south (without quolls). They set up arenas that were baited with the aforementioned peanut butter balls, and placed a live-trap with a melomys at the door to the arena.  The researchers then opened up the trap door and recorded whether the melomys entered the arena within 10 minutes. 

Experimental setup testing melomys responses to open-field tests. Credit: Chris Jolly.

After 10 minutes, each melomys was rounded up and placed back in its trap, and a red plastic bowl was put into the arena.  The trap was then reopened and the researchers recorded whether the melomys interacted with the red bowl.

Looking at the left graph, you can see that in 2017, north island melomys were much shyer than melomys from the predator-free south island. But by 2019, this difference was mostly gone.  But when it comes to exploring a novel object (right graph), the northern melomys still retained some of their fear in comparison to southern melomys.

Figure 4

Left graph.Proportion (+ 95% confidence intervals) of melomys that emerged from live traps within 10 minutes in the open-field test. Right graph. Proportion of melomys that interacted with the novel object in the experiment that tested for neophobia (fear of novel objects).

Lastly, Jolly and his colleagues tested the effect of living with quolls on melomys foraging behavior.  At nightfall, the researchers placed one wheat seed at 81 locations in each site. Control (unmanipulated) seeds were set out at 40 locations while seeds that had been stored with quoll fur (and presumably smelled like quoll) were set out at 41 locations. At daybreak, the researchers counted the number of remaining seeds, so they could calculate seed removal. In the first session conducted shortly after quoll release, they found no evidence of discrimination based on predator scent in either melomys population. But over time, the northern melomys began to discriminate based on quoll scent, while southern quolls continued to forage at the same rate on control and quoll-scented seeds.

Figure 5B

Mean seed take bias (the number of scented seeds – the number of control seeds) taken by north and south island melomys. Error bars are 95% confidence intervals.

The researchers conclude that introduction of quolls as a novel predator influenced melomys in two distinct ways.  First, quolls preyed on them and reduced melomys abundance.  But equally important, quolls changed melomys behavior. Soon after quoll introduction, invaded melomys populations were substantially shyer than the non-invaded populations.  But this changed over the next two years, with a reduction in general shyness in the invaded populations, and an increase in predator-scent aversion. In effect, melomys were fine-tuning their behavioral response to quoll invasion.

Unfortunately, the researchers can’t evaluate whether these behavioral changes result from learning, or from natural selection.  Melomys has a short generation time, so natural selection could be strong, even over a short timespan.  Unfortunately, because of low survival from one year to the next, there were not enough melomys to test for whether individual behavior changed over time as a result of learning.  It is certainly plausible that natural selection and learning operate together to change melomys behavior following quoll introduction.  

note: the paper that describes this research is from the journal Ecology. The reference is Jolly, C. J., A. S. Smart, J. Moreen, J. K. Webb, G. R. Gillespie, and B. L. Phillips. 2021. Trophic cascade driven by behavioral fine-tuning as naıve prey rapidly adjust to a novel predator. Ecology 102(7): e03363. 10.1002/ecy.3363. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2021 by the Ecological Society of America. All rights reserved.

Turkey mullein trichomes gobble up protective pollen

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I’m always amazed at how brilliant plants can be.  For example Billy Krimmel and Ian Pearse showed in 2013 that many plant species exude sticky substances that entrap small arthropods, thereby attracting predators, which then rid these plants of many herbivores that might otherwise consume their leaves or reproductive structures. Jennifer Van Wyk joined this research group (which included Laure Crova) in graduate school. They were hunting for predatory hemipterans (true bugs) for a different experiment, which involved looking for them on turkey mullein (Croton setiger). They found plenty of predators, but almost no prey.  This was puzzling; what were these predators eating?  Intrigued, the researchers swabbed the turkey mullein leaves for pollen and found relatively vast quantities of pollen trapped in the trichomes (hairlike protuberances) of the leaves. Much of the pollen was from other species, and the researchers suspected that the trichomes were removing pollen from pollinators (primarily bees) that came to visit. Presumably the predators, which included spiders, hemipterans and ants, were attracted to this highly nutritious pollen.

VanWykTurkeyMullein

Turkey mullein with predaceous hemipteran on lower right leaf. Credit: Billy Krimmel – http://www.miridae.com/our-team

Van Wyk and her colleagues wondered whether pollen capture benefitted turkey mullein. If turkey mullein used pollen to attract predators, and predators ate herbivores, pollen extraction by trichomes would be an adaptation that formed part of turkey mullein’s defense strategy.  If this is true, supplementing turkey mullein with additional pollen should increase visitation by predators, and decrease herbivore abundance.  With fewer herbivores, the researchers predicted less leaf damage.

Wykdamagedturkeymullein

Turkey mullein with herbivore-damaged leaves

Supplementing turkey mullein with additional pollen presents its own set of problems – most importantly coming up with enough pollen – in particular pollen that predators want to eat (Van Wyk and her colleagues collected a pound of oak pollen, only to find that predacious bugs were not interested in it).  The researchers grew sunflowers in greenhouses, secured squash pollen from friends’ gardens and used tuning forks to vibrate pollen from tarweed flowers.

The researchers then set up experiments using 60 turkey mullein plants from one population in 2013 and 80 plants from another population in 2014. Nearby plants were paired up, with one member of the pair receiving 150 mg of supplemental pollen each week from mid-August to mid-September.  They surveyed all arthropods visible to the naked eye, and categorized each species as predator or herbivore based on its primary diet (many of the arthropods were actually omnivorous).

In accordance with expectations, predator abundance was substantially greater in the supplemented populations in both years of the study. Spiders showed the most consistent increase, while Orius (the minute pirate bug) increased significantly in the 2014 population. The 2014 population had fewer arthropods of all species, possibly because it was immediately adjacent to an agricultural field.

WykFig1

Mean predator abundance per plant in 2013 (top) and 2014 (bottom). Geocoris is a Genus of big-eyed bugs, while Orius is the minute pirate bug. ** p < 0.01, † p < 0.1. Error bars are 1 standard error.

The results are less clear-cut with herbivore abundance.  Fleahoppers were 18% less abundant on supplemented plants in 2014, and slightly (not significantly) less abundant in supplemented plants in 2013.  Plants with a greater number of spiders had fewer fleahoppers, suggesting that spiders were eating them (or scaring them away). The researchers were unable to measure the abundance of an important herbivore, the grey hairstreak caterpillar, which forages primarily at night, and retreats into the soil during the heat of the day.

WykFig2b

Mean number of fleahoppers  per plant in 2013 (left graph) and 2014 (right graph).  Blue bars indicated plants with supplemented pollen. * p < 0.05.

Lastly, supplemented plants suffered much less leaf damage than did unsupplemented plants.

WykFig2A

Mean number of damaged leaves per plant in 2013 (left graph) and 2014 (right graph).  Blue bars indicated plants with supplemented pollen. ** p < 0.01.

Taken together, these experiments indicate that turkey mullein uses its trichomes to capture pollen and attract a diverse army of predators, which reduce herbivore abundance and reduce damage to the plant.  It is possible that pollen supplementation could be used on a larger scale to reduce herbivore loads on agricultural crops.  More generally, it will be interesting to see whether other plants with sticky trichomes, such as the marijuana plant Cannabis sativa, also use their trichomes to attract predators and reduce herbivore abundance.

note: the paper that describes this research is from the journal Ecology. The reference is Van Wyk, J. I.,  Krimmel, B. A.,  Crova, L., and  Pearse, I. S..  2019.  Plants trap pollen to feed predatory arthropods as an indirect resistance against herbivory. Ecology  100( 11):e02867. 10.1002/ecy.2867. 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.

Spiders eat spiders sometimes

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In human society, a guild is an association of craftsmen or merchants that work together to achieve a common goal. For example, 14thcentury Paris boasted over 350 different guilds, including drapiers (cloth makers), knife-makers, locksmiths, helmet-makers and harness-polishers. Ecological guilds are similar to human guilds, in that members of the same guild depend on the same resources for survival. But members of the same ecological guild are  different species, each of which uses a similar resource, or group of resources.  As we shall now discover, as in human guilds, members of ecological guilds don’t always get along very well.

A guild is part of a food web, which is a summary of the feeding relationships within a community.  Israel Leinbach, Kevin McCluney and John Sabo were interested in one particular part of a food web – the relationship between a large wolf spider (Hogna antelucana), a small wolf spider (Pardosa species) and a cricket (Gryllus alogus).  Both spiders are in the same guild, because they obtain their energy from similar sources – insect prey.  This cricket specializes on willow and cottonwood leaves that fall to the ground in the semi-arid floodplain of the San Pedro River in southeast Arizona. Under natural conditions, the researchers observed the large spiders eating both the small spiders and crickets.  However, they never observed the small spider eating the relatively large cricket (which averages 20 times its mass), though small spiders are delighted to eat many other (smaller) insect species.

spideeatscricket.jpg

A large wolf spider subdues and begins to consume a cricket.  Credit: Kevin McCluney.

The researchers argue that even though guild members specialize on similar resources, it is important to consider how other resources might influence the relationships among the species.  During the dry season, water is a critical limiting resource.  As it turns out, large spiders, crickets and small spiders are very different in how much energy and water they contain. From the table below you can see that the small Pardosa spiders are very low in water content, but pack a huge amount of energy into their tiny bodies.  Crickets of both sexes have a high water content, but contain a relatively small amount of energy in their large bodies. Thus small spiders have a much higher energy/water ratio than crickets or large spiders.

SpiderTable2

Mean (+/- 1 standard error) dry mass, energy, water and energy/water ratio of the three species discussed in this report.

When water is limiting, the large spiders might devote themselves to eating crickets to take advantage of their very high water content. But when water is not limiting, the large spiders would be expected to turn their attention to eating small wolf spiders, which are much dryer, but much higher in energy per unit body mass. The researchers reasoned that providing water to large spiders should increase the rate of intraguild predation (in this case large spiders eating small spiders).

SpiderFig1

Interactions among the three species when water is limiting (Control – left) and abundant (Experimental – right).  Black arrows are direct effects, while gray arrows show the direction of energy flux).

Leinbach and his colleagues set up a mesocosm experiment using 2 X 2 X 2 meter cages in which they experimentally manipulated community composition and water availability.

spidercages.jpg

Network of cages set up in the San Pedro River floodplain. Credit: Kevin McCluney.

All cages, except controls, received either one large male or female spider, two small spiders (sex unknown) and two crickets (again either male or female). Controls received no large spiders, and were used to establish a baseline survival rate for the two potential prey items (small spiders and crickets). To test for the effects of water availability on predation by large spiders the researchers placed water pillows that held approximately 30 ml of water into half of the enclosures. They predicted that large spiders would primarily eat energy-rich small spiders in cages with water pillows, but prefer water-rich crickets in cages without water pillows. The water pillows had minimal impact on cricket water levels as they got plenty of water from their food (green water-rich leaves)

spiderwaterpillow.jpg

A large wolf spider sucks water from the water pillow.  Credit: Kevin McCluney.

Leinbach and his colleagues used per capita interaction strength as their quantitative measure of predation effects.  If prey survival was lower in the experimental cages than  in the control, there was a negative interaction strength – indicating that large spiders were eating a particular prey type.  When the researchers provided them with water, large spiders of both sexes ate significantly more small spiders than they did  without water supplements.

SpiderFig4

Interaction strength (effect of predation) of large spider (Hogna antelucana) on the small spider (Pardosa species).  Both male and female large spiders have significant negative effects on small spiders when water is supplemented (blue bars), but have minimal effects without water supplements (gray bars).

But the story was very different with crickets.  The researchers expected that when supplemented with water, large spiders would bypass the water-rich crickets in favor of the energy-rich small spiders. Surprisingly, instead of crickets in cages with pillows surviving as well as controls, they actually survived better – at least male crickets did. One possible explanation is that spiders may emit odor (or other types of) cues that affect cricket behavior in a negative way, for example by causing them to feed more cautiously and inefficiently. Once the large spiders have killed the small spiders, there may be fewer spiders around to smell up the place, and crickets may feed more efficiently, and thus survive better.

spidermccluney.jpg

Israel Leinbach searches for spiders and crickets within a cage. Credit Kevin McCluney.

I asked Kevin McCluney if there were any other surprising findings, and he pointed out that large male and female spiders showed very similar consumption patterns.  He expected that females would need more energy because egg production is very energy demanding.  One explanation for this lack of difference is that large male spiders may expend considerable energy wandering around in search of sexually receptive females, and their overall energy needs may be similar to those of females. Balancing the demands of energy, water and sex may be equally demanding for both sexes of large spiders, and may lead to adaptive feeding on different levels of the food chain as environmental conditions shift.

note: the paper that describes this research is from the journal Ecology. The reference is Leinbach, I.,  McCluney, K. E., and Sabo, J. L. 2019. Predator water balance alters intraguild predation in a streamside food web. Ecology 100(4):e02635. 10.1002/ecy.2635. 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.

Kelp consumption curtailed by señorita

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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.

bigsenorita.jpg

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).

HaggertyFigS1

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.

brokenkelp.jpg

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.

senoritaschool.jpg

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

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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.

Lionfish

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.

Basslets

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

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.

KindingerFig12A

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.

KindingerFig1BC

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.

KindingerFig2BC

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.

Prey populations: the only thing to fear is fear itself

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In reference to the Great Depression, Franklin Delano Roosevelt is famously quoted as stating during his 1933 inaugural speech “the only thing we have to fear is fear itself.” Roosevelt was no biologist, but his words could equally apply to a different type of depression – the decline of animal populations that can be caused by fear.

FDR

Roosevelt’s inauguration in 1933. Credit: Architect of the Capitol.

Ecologists have long known that predators can depress prey populations by killing substantial numbers of their prey. But only in the past two decades or so have they realized that predators can, simply by their presence, cause prey populations to go into decline. There are many different ways this can happen, but, in general, a predation threat sensed by a prey organism can interfere with its feeding behavior, causing it to grow more slowly, or to starve to death. As one example, elk populations declined after wolves were introduced to Yellowstone National Park. There are many factors associated with this decline, but one factor is fear of predators causes elk to spend more time scanning and less time foraging. Also, elk tend to stay away from wolf hotspots, which are often places with good elk forage.

Liana Zanette recognized that ecologists had not considered whether predator presence can cause bird or mammal parents to reduce the amount of provisioning they provide to dependent offspring, thereby reducing offspring growth and survival, and slowing down population growth. For many years, she and her colleagues have studied the Song Sparrow, Melospiza melodia, on several small Gulf Islands in British Columbia, Canada. In an early study, she showed that playbacks of predator calls reduced parental provisioning by 26%, resulting in a 40% reduction in the estimated number of nestlings that fledged (left the nest). But, as she points out, Song Sparrow parents provision their offspring for many days after fledging; she wondered whether continued perception of a predation threat during this later time period further decreased offspring survival and ultimately population growth.

Song sparrow

The Song Sparrow, Melospiza melodia. Credit: Free Software Foundation.

Zanette’s student, Blair Dudeck, did much of the fieldwork for this study. The researchers captured nestlings six days after hatching , weighed and banded them, and fit them with tiny radio collars. They then recaptured and weighed the nestlings within a few hours of fledging (at about 12 days post-hatching) to assess nestling growth rates.

sparrowbaby

Banded sparrow nestling with radio antenna trailing from below its wing. Credit: Marek C. Allen.

Three days after the birds fledged, Dudeck radio-tracked them, and surrounded them with three speakers approximately 8 meters from where they perched. For one hour, each youngster listened to recordings of calls made by predators such as ravens or hawks, followed, after a brief rest period, by one hour of calls made by non-predators such as geese or woodpeckers (or vice-versa). During the playbacks, Dudeck observed the birds to record how often the parents visited and fed their offspring, and whether offspring behavior changed in association with predator calls. This included recording all of the offspring begging calls.

BlairRadio

Blair Dudeck simultaneously uses a tracking device to locate Song Sparrows and a recorder mounted to his head to record their begging calls. Credit: Marek C. Allen.

Fear had a major impact on parental behavior. Parents reduced food provisioning vists by 37% when predator calls were played in comparison to when non-predator calls were played. They also fed offspring fewer times per visit, which resulted in 44% fewer meals in association with predator calls.

DudeckFig1

Mean number of parental provisioning visits (in one hour) in relation to whether predator (red) or non-predator (blue) calls were played. Error bars are 1 SE.

Hearing predator calls had no effect on offspring behavior – they continued to beg for food at a high rate, and did not attempt to hide.

Some parents were much more scared than others – in fact, some parents were not scared at all. The researchers measured parental fearfulness by subtracting the number of provisioning visits by parents during predator calls from the number of visits during non-predator calls. A more positive number indicated a more fearful parent (a negative number represents a parent who fed more in the presence of predator calls). The researchers discovered that more fearful parents tended to have offspring that were in poorer condition at day 6 and at fledging.

DudeckFig2

Offspring weight on day 6 (open circles) and at fledging (solid circles) in relation to parental fearfulness.  Higher positive numbers on x-axis indicate increasingly fearful parents.

Importantly, more fearful parents tended to have offspring that died at an earlier age. Based on this finding, the researchers created a statistical model that compared survival of offspring that heard predator playbacks throughout late-development with survival of offspring that heard non-predator playbacks during the same time period. They estimated a 24% reduction in survival. Combined with their previous study on playbacks during early development, the researchers estimate that hearing predator playbacks throughout early and late development would reduce offspring survival by an amazing 53%.

This “fear itself” phenomenon can extend to other trophic levels in a food web. For example recent research by Zanette and a different group of researchers showed that playbacks of large carnivore vocalizations dramatically reduced foraging by raccoons on their major prey, red rock crabs. When these carnivore playbacks were continued for a month, red rock crab populations increased sharply. This increase in crab population size was followed by a decline of the crab’s major competitor – the staghorn sculpin, and the crab’s favorite food, a Littorina periwinkle. Thus “fear itself” can cascade through the food web, affecting multiple trophic levels in important ways that ecologists are now beginning to understand.

note: the paper that describes this research is from the journal Ecology. The reference is Dudeck, B. P., Clinchy, M., Allen, M. C. and Zanette, L. Y. (2018), Fear affects parental care, which predicts juvenile survival and exacerbates the total cost of fear on demography. Ecology, 99: 127–135. 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.

Changing climate promotes prolific plants and satiated consumers

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Plants in Sweden can have a difficult life, but climate change has provided a more benign environment for some of them, including the white swallow-wort, Vincetoxicum hirundinaria. This perennial herb grows in patches in sun-exposed rocky areas, in forests located below cliffs, and along the edges of wooded areas. The plant forms clumps that are heavily laden with flowers in June and July, and creates pod-like fruits in July and August

Solbreck1AB

Vincetoxicum hirundinaria growing in rocky outcrop (top photo). Vincetoxicum pods releasing their wind-dispersed seeds (bottom photo).

Christer Solbreck has had a lifelong interest in insect populations, and he has been following the insects that eat Vincetoxicum’s seeds for the past 40 years. As he described to me, surprisingly few population ecologists actually measure the amount of food available to insects. I should add that very few people have the resilience to study the same population of insects for 40 years, either. And interestingly, though this paper discusses the effect of a changing climate on seed production and seed predation, it was not Solbreck’s intent to consider climate change as a variable when he began, as climate change was not a concern of most scientists in the 1970s.

But climate change has happened in southeastern Sweden (and elsewhere), and has affected ecosystems in many different ways. Ecologists can quantify climate change by describing its effect on the vegetation period, or growing season (days above 5°C), which has increased by about 20 days since the mid 1990s.

Solbreck2B

Length of growing season (vegetation period) in southern Sweden.

During the same time period the abundance of Vincetoxicum has increased sharply.

Solbreck2Ayes

Vincetoxicum abundance, measured as area of the research site covered, during the study.

You will note that “Vincetoxicum” has the word “toxic” in its midst; the seeds are toxic to most consumers, and are important food sources for only two insect species. Euphranta connexa females lay eggs in developing fruits of the host plant, with the emerging larva boring through the seeds and killing most of them. Lygaeus equestris is an all-purpose seed predator; both larvae and adults suck on flowers, on developing seeds within the fruits, and on dry seeds they find on the ground up to a year later.

solbreck1c.png

Euphranta connexa female lays eggs in an immature seed pod.

Solbreck1D

Lygaeus equestra larva feeds on a fallen seed.

Solbreck teamed up with biostatistician Jonas Knape to analyze his data. From the beginning of the study, Solbreck suspected that annual variation in weather – particularly rainfall – might influence Vincetoxicum seed production, and consequent population growth of the two insect species. They discovered something quite unexpected; the dynamics of seed production shifted dramatically in the second half of the study, alternating annually from very high to very low production over that period. This dynamic shift coincides with the extension of the growth season as a result of climate change.

Solbreck2Cyes

Seed pod abundance by year.

The researchers argue that there is a non-linear negative feedback relationship of the previous year’s seed production on the current year’s seed production. Negative feedback occurs when an increase in one factor or event causes a subsequent decrease in that same factor or event. In this case, an increase in seed production uses up plant resources, leading to a decrease in seed production the following year. But the effect is non-linear, and does not come into play unless Vincetoxicum produces a huge number of seeds, as shown by the graph below,

Solbreck3yes

Seed production in the current year in relation to seed production in the previous year. Note that both axes are logarithmic. The curve represents the expected seed pod density generated by the statistical model, with the shaded area representing the 95% credible intervals. Open circles are data for 1977-1996, while closed circles are data for 1997-2016.

The researchers also found that high rainfall in June and July increased seed production.

So how do these wild fluctuations in seed production affect insects and the plant itself? One important finding is that in high seed production years, the proportion of seeds attacked by insects plummets because the sheer number of seeds overwhelms the seed-eating abilities of the insect consumers. Ecologists describe this phenomenon as predator satiation.

Solbreck4yes

Seed predation rates in relation to seed pod density.  Note that both axes are logarithmic. The curve represents the expected predation rate generated by the statistical model, with the shaded area representing the 95% credible intervals. Points are E. connexa predation rates while triangles are combined predation by both insect species.

As a result of predator satiation, there were, on average, seven times as many healthy (unattacked) seed pods in 1997-2016 than there were in 1977-1996. Presumably, this increased number of healthy seeds translates to an increase in new plants becoming established in the area. An important takehome message is that the entire dynamics of an ecosystem can change as a result of changes to the environment, in this case, climate change. More long-term studies are needed to evaluate how common these shifting dynamics are likely to become in the novel environmental conditions we humans are creating.

note: the paper that describes this research is from the journal Ecology. The reference is Solbreck, Christer and Knape, Jonas (2017), Seed production and predation in a changing climate: new roles for resource and seed predator feedback?. Ecology, 98: 2301–2311. doi:10.1002/ecy.1941. 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.

Life and death in a diminutive ecosystem

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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.

BreviglieriFig3EF

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.