Snails grow large to fight fear

In a recent post (Jan 12), I discussed research showing that song sparrow parents reduce provisioning to their offspring when threatened by predators, ultimately reducing offspring survival rates.  But in a turnabout that highlights the natural world’s dazzling diversity, a recent study by Sarah Donelan and Geoffrey Trussell revealed a very different impact of fear on the development of snail offspring. Donelan had worked as Trussell’s laboratory technician for two years and became fascinated by the egg capsules laid by the carnivorous snail Nucella lapillus, an ecologically important species in rocky intertidal communities. Earlier work had shown that predator-induced fear reduced snail feeding and growth rates, so Donelan decided that for her PhD work she would see how predator-induced fear influenced offspring development.


Adult Nucella alongside ca. 100 egg capsules. Credit: Sarah Donelan.

The researchers recognized that the fear environment experienced by parents before or during reproduction, and by the embryos during early development, could influence growth and development of those embryos. At their research site along the Massachusetts, USA coast, the predatory green crab, Carcinus maenas, can be a source of fear for these adult and embryonic snails. Donelan and Trussell exposed snails to fear by housing separately one male and one female snail in adjacent protected perforated containers (with six blue mussels in each container to feed them) that were set within a large plastic bucket. This bucket also had a somewhat larger perforated container (the risk chamber) containing the dreaded green crab (and two snails to feed it). The control risk chamber had two snails, but no crab.


Experimental setup with buckets containing egg capsules in perforated cages experiencing different exposure to fear. Credit: Sarah Donelan.

In late spring of 2015 and 2016, field-collected female and male snails were matched to create a total of 80 parental pairs. Donelan and Trussell set up experiments to explore the effects of parental experience with predation risk, embryonic experience with predation risk, and duration of embryonic experience.

Parent snails were exposed to a risk chamber (with a crab in the experimental group, and without a crab in the control group) for three days, and then placed together for four days (without risk) to mate. If an egg capsule was laid, the researchers removed it, and immediately exposed it to an experimental or control risk chamber for a week. Embryonic risk duration was further manipulated by continuing to expose half of the egg capsules to risk for a total of six weeks. The table below summarizes the treatments received by parents and offspring.



Mean (+ standard error) shell length (top graph) and tissue mass (bottom graph) of snail embryos exposed to predation risk. Parents were either exposed (solid circles) or not exposed (open circles) to risk before mating.


When parents were not exposed to risk, but their offspring were exposed, these offspring had shorter shells and reduced tissue mass compared to all other groups. When both parents and offspring were exposed to risk, offspring shell length increased by 8% and offspring mass increased by a whopping 40% over risk-exposed offspring whose parents were not exposed to risk (left data points in figures a and b). If embryos were not exposed to risk, parental exposure had no significant impact on embryonic development (right data points on figures a and b). Embryonic risk duration had no impact on development.


In addition, risk-exposed offspring of risk-exposed parents emerged from their egg capsules an average of 4.1 days sooner than other offspring.


Mean (+standard error) number of days until emergence of snail offspring that experienced the presence or absence of predation risk during early development.  Their parents were exposed to risk (solid circle) or no risk (open circle) before mating.

What could be causing these differences in size and rate of development? Donelan and Trussell hypothesized that embryonic snails could grow larger and more quickly if they were somehow able to reduce their metabolic rate. With a reduction in metabolic rate, more energy could be diverted to growth and development, resulting in larger and faster-growing snails. The researchers used an oxygen meter to measure oxygen consumption rates of individual egg capsules (from the eight different treatments in the first experiment) six weeks after deposition, about a week before embryos would begin to emerge. They exposed some of the capsules to predation risk during the experiment (current risk graph below), and left other capsules unexposed. When tested under risky conditions, capsules from parents who were exposed to risk, and that experienced risk as embryos during early development, had 56% lower metabolic rates than the other three groups (left graph), and similarly low metabolic rates as capsules tested without risk (right graph).


Mean (+ standard error) respiration rate of egg capsules that were (left graph) or were not (right graph) exposed to current predation risk.  During early development, the embryos in these capsules experienced risk or no risk, and were produced by parents exposed to risk (solid circles) or no risk (open circles) before mating.

Overall, parental experience with predation risk enhances offspring growth and development in the presence of risk. If the parents lack this exposure, risk-exposed offspring suffer the costs associated with small size and slower development. Currently Donelan and Trussell are trying to figure out what these costs are. Smaller snails have less energy reserves, may feed on a less diverse group of prey, and are less likely to remain in safer habitats than are larger juveniles. But we still don’t know whether these effects on early stages of life have lasting impacts as a snail gets older and larger. More generally, we don’t know whether there are similar types of interactions between parental and embryonic experiences of other stressors, most notably environmental stresses that are already being imposed by climate change.

note: the paper that describes this research is from the journal Ecology. The reference is Donelan, S. C. and Trussell, G. C. (2018), Synergistic effects of parental and embryonic exposure to predation risk on prey offspring size at emergence. Ecology, 99: 68–78. doi:10.1002/ecy.2067. 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

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.


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.


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.


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.


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.


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.