Stressed-out primates

The endangered black lion tamarin, (Leontopithecus chrysopygus), lives in mostly degraded and highly fragmented landscape in the state of Sao Paulo, Brazil.  Olivier Kaisin is a PhD student who wants to know whether declining environmental conditions are causing increased stress to the tamarins. Researchers often use glucocorticoid (GC) levels as a measure of physiological stress, as many animals, including primates, produce and release GCs in response to stress.  Many researchers have argued that prolonged elevation of GC levels has a negative impact on individual survival or reproduction, but it is not clear whether this is true for most primates. Given that 60% of primate species are currently threatened with extinction, it would be nice to know whether conservation biologists could use GC levels to identify populations that are at risk.

The black lion tamarin, Leontopithecus chrysopygus.

One of the unadvertised features of graduate programs is that students need to learn about their study system before doing research. In this spirit, before beginning his tamarin study, Kaisin (working with several other researchers) did a meta-analysis of all studies (published until 2020) that compared cortisol levels in primates from disturbed vs. undisturbed habitats to see if the type of disturbance influenced GC levels.  Disturbance types included hunting, tourism, habitat loss, ongoing logging, habitat degradation and other human activities.  Habitat loss was a reduction in forest fragment size to less than 500 hectares.  Habitat degradation resulted from logging in the past 20 years that led to changes in forest structure and diversity, but did not substantially reduce the size of the forest habitat.  Other human activities did not fit into the five disturbance types, and included activities such as mining, urbanization and access to rubbish.

The graph below shows the effects of the different disturbance types.  “Hedges g” is a test statistic used in meta-analyses to look for effects of different variables.  The midpoint of the bar (or the diamond in the case of the overall effect) is the mean value of Hedges g, while the endpoints of each bar (or diamond) indicate the 95% confidence interval.  If the entire interval does not overlap 0, then we can conclude that there is a statistically significant effect of that variable.  Based on this analysis, both hunting and habitat loss were associated with significant increases in glucocorticoid levels in primates, contributing to a significant overall increase in glucocorticoid levels in response to disturbance.

The influence of six types of disturbance on GC levels of 24 different primate species. * indicates statistically significant effects.

As Kaisin and his colleagues point out, six of the studies actually showed a significant decrease in GC levels in association with disturbance.  For example, howler monkeys had reduced GC levels in response to ongoing logging.  The researchers interpret this surprising GC decrease on the elimination of large predators from the logged forest, which substantially reduces howler monkey stress levels. As a second example, in Madagascar, an invasive tree species in the degraded site provided important fruits for red-bellied lemurs, leading to well-fed lemurs with reduced GC levels. Unfortunately, these confounding variables cannot be easily controlled, so researchers need to consider each study on a case-by-case basis. Some families of primates were more influenced by stress than others. In particular, hominids (great apes) and atelids (New World monkeys such as howler, spider and woolly monkeys) both showed significantly greater GC levels in association with stress.  Three families showed smaller increases while three other families of primates were basically unaffected.

The influences of disturbance on eight different primate families (as measured by Hedges g). CI (95%) is the 95 percent confidence interval. Weight is a measure of the contribution of each primate family to the overall effect. Families with more species/studies contribute more weight to the overall effect

The researchers emphasize that many more studies are needed in order to understand when we should expect stress to elevate GC levels in primates.  For example, only one of the studies looked at stress effects on Asian primates. Future studies in endocrinological primatology should relate how prolonged stress influences fitness – including survival, growth and development and reproductive success.  In turn, this would allow the conservation community to understand the relationship between stress and future population viability.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Kaisin, O., Fuzessy, L., Poncin, P., Brotcorne, F. and Culot, L., 2021. A meta‐analysis of anthropogenic impacts on physiological stress in wild primates. Conservation Biology35(1), pp.101-114. Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2021 by the Society for Conservation Biology. All rights reserved.

Tadpoles shun trout across time

At a young school child (so long ago I can’t recall exactly when) I was exposed to Ernst Haeckel’s dictum that “ontogeny recapitulates phylogeny.”  More interested in language than biology at the time, I thought “cool – three words that I’m clueless about.” Though biological thinking about ontogeny – the processes of growth and development – has changed since Haeckel’s time, interest has, if anything, grown more intense across disciplines. Tiffany Garcia has explored her lifelong fascination with ontogeny by focusing her research on amphibians, which are famous for their distinct stages of development, each with unique habitats and ecological requirements. Working with eggs and tadpoles of the Pacific chorus frog (Pseudacris regilla), Garcia and her colleagues investigated whether stress associated with the presence of predators during one developmental stage (for example an egg) would carry over to influence behavior or development of subsequent stages.

chorus frog

The Pacific chorus frog (Pseudacris regilla). Credit Brett Hanshew.

A tadpole’s anti-predator strategy can be influenced by other factors besides carry-over from earlier developmental stages.  For example, we might expect that tadpoles whose ancestors lived in association with predators for many generations might have evolved a different anti-predator strategy than did tadpoles whose ancestors lived in a less threatening environment (this would be an adaptive effect). Tadpoles may also show very short-term changes in behavior or development (this is termed plasticity) if exposed to a cue that indicated a possible predation threat.


Collecting newly laid eggs at Three Creeks Lake. Credit: Lindsey Thurman

These three processes operate over very different time scales (long term – adaptive; intermediate term – carry-over; short term – plastic).  Garcia and her colleagues designed an experiment to explore how these processes might interact to influence a tadpole’s anti-predator strategy.  To investigate long term adaptive effects, the researchers collected newly laid (fertilized) eggs from lakes with and without rainbow trout (Oncorhynchus mykiss). They investigated carry-over effects by conditioning these eggs with four different environments during development: (1) trout odor, (2) cues from injured tadpoles (alarm cues), (3) trout odor paired with alarm cues, and (4) a water control (no odors nor cues).  The researchers created alarm cues by grinding up four juvenile tadpoles in 150 ml of water, and trout odor by housing 30 juvenile rainbow trout in a 200 L tank filled with well water.  They then conducted behavioral and developmental assays on tadpoles to see how adaptive, carry-over and plastic effects influenced tadpole growth, development and behavior.


Overview of the experimental design.

Garcia and her colleagues discovered that early exposure to trout odor had very little effect on growth and development, with body size and stage of development equivalent to that of controls.  In contrast exposure of eggs to tadpole alarm cues or to alarm cues + trout odor resulted in smaller, less developed fish (see table below).  In addition there was no effect of evolutionary history – eggs from lakes with and without trout showed similar patterns of growth and development.


Tadpole size and development in response to the four conditioning  treatments.  Higher Gosner stage numbers indicated more developed tadpoles. A tadpole hatches at Gosner stage 21 and begins metamorphosis at Gosner stage 42.

The next question is how do tadpoles respond behaviorally from exposure to different environments over the long, intermediate and short time scale?  To test tadpole anti-predator behavior, the researchers placed an individual tadpole into a tub that had a 6 X 8 cm piece of corrugated black plastic, which the tadpole could use as a refuge.  The researchers added to each tub one of the following: water (as a control (C)), tadpole alarm cues (AC), trout odor (TO), or alarm cues + trout odor (AC+TO).  After an acclimation period, a researcher noted the position of the tadpole (under the refuge or out in the open) every 20 minutes over a 3-hour time period.

There were no effects of evolutionary history on refuge use.  Tadpoles from lakes with and without trout showed similar patterns of refuge use.  However, embryonic conditioning to alarm cues and trout odor had a large effect on refuge use.  The left graph below shows the response of tadpoles from all four conditioning groups (C, AC, TO and TO+AC) to the addition of water.  As you can see, tadpoles that hatched from eggs that were conditioned with AC+TO were most likely to use refuges, while tadpoles from AC only or TO only eggs were somewhat more likely to use refuges. The pattern repeats itself when tadpole alarm cues are added to the water (second graph from left).  However when trout odor is added to the water, the responses are much more extreme, but follow the same pattern (third graph).  Lastly, when confronted with alarm cues and trout odor, tadpoles increase refuge use dramatically, but again show the same pattern, with tadpoles from control eggs using refuges the least, and tadpoles from eggs conditioned with alarm cues and trout odor using refuges the most (right graph).


Refuge use by tadpoles in response to embryonic conditioning and experimental exposure. C = water control, AC = tadpole alarm cue, TO = trout odor, and AC+TO = tadpole alarm cue and trout odor. Blue bars are means and gray bars are 95% confidence intervals.

There are two processes going on here.  First, over the short term, tadpoles are more responsive to the strongest cues, increasing refuge use when exposed to both tadpole alarm cues and trout odor.  Second, over the intermediate term, there is solid evidence for carry over effects.  Tadpoles that hatched from eggs conditioned with alarm cues and/or trout odor showed markedly increased refuge use than did tadpoles that hatched from control eggs.

These predator-induced responses impose a cost to the tadpoles.  Tadpoles exposed to alarm cues and trout odor while still in the egg were smaller and less developed, and probably metamorphosed into smaller frogs.  Many studies have shown that smaller frogs have reduced reproductive success.  The researchers recommend further studies to explore these trade-offs between survivorship, growth rate, development rate and size at metamorphosis. These studies are particularly essential, because rainbow trout are a non-native predator to these lakes.  Studies such as these allow conservation ecologists to understand the evolution and development of predator-prey interactions when novel species are introduced into an ecosystem.

note: the paper that describes this research is from the journal Ecology. The reference is Garcia, T. S.,  Bredeweg, E. M.,  Urbina, J., and  Ferrari, M. C. O..  2019.  Evaluating adaptive, carry‐over, and plastic antipredator responses across a temporal gradient in Pacific chorus frogs. Ecology  100( 11):e02825. 10.1002/ecy.2825.  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.












Hot ants defend plants from elephants

I’ve lost a lot of sleep over ants.  As a spider researcher, I often placed ants on spiderwebs to lure my spiders out of their underground retreats and onto their webs. The problem was that these harvester ants (Pogonmyrmex species) were fierce, so to minimize damage to myself, I was forced to capture them in the very early morning, when they and (alas) I were very sluggish.

acacias_thorn copy

Swollen thorn (domatia) that serves as living quarters for acacia ants. Credit: T. Palmer.

Todd Palmer has worked with ants for many years, including research on ant-plant mutualisms in which acacia trees provide domatia (swollen thorns) as ant living quarters and extrafloral nectaries as ant food, while ants provide protection from herbivores such as elephants, kudus and steenboks.

Similar to my efforts with ants and spiders, Palmer wanted to reduce ant-induced damage to himself and his colleagues, so he often took advantage of early morning ant sluggishness for purposes of manipulating acacia trees. On the other hand, if he wanted to study aggressive responses, he learned that mid-day was best. Recognizing the daily patterns of ant activity got Palmer, Ryan Tamashiro (Palmer’s undergraduate research student) and Patrick Milligan (Palmer’s graduate student) thinking about how these different levels of activity would influence herbivores, many of which tend to be most active during dawn and dusk when temperatures are low and ants are relatively sluggish.

Elephant side

Elephants are major herbivores that can cause enormous damage to acacia trees. Credit: T. Palmer.

Four species of ants live in domatia on branches of Acacia drepanolobium, the dominant tree species at Mpala Research Centre in Laikipia, Kenya.

Acdr habitat

A grove of Acacia drepanolobium. Credit: T. Palmer.

In order of relative abundance, the ant species are Crematogaster mimosae (52%), C. sjostedti (18%), Tetraponera penzigi (16%) and C. nigriceps (15%).  Previous research showed that C. mimosae and C. nigriceps are the two most effective acacia defenders.

Cnigriceps copy

Crematogaster nigriceps on an acacia tree. Credit: T. Palmer.

Ants are poikilotherms, whose body temperature, and presumably their activity levels, fluctuate with environmental temperature.  As these ants live in acacia branches, the first order of business became to determine how branch temperature fluctuated with time of day during the 21 days of data collection.  Not surprisingly, branch temperature peaked at mid-day, and was lowest at dawn and dusk (temperatures were not measured during the night).

TamashiroFig S!

Variation in branch surface temperature with time of day. Horizontal bars are median values; boxes are first and third quartiles.

Tamashiro, Milligan and Palmer next asked how ant activity level related to branch temperature.  Different ant species don’t get along so well, so each tree hosted only one ant species.  For each tree surveyed, the researchers counted the number of ants that passed over a 5 cm branch segment during a 30 second time period (they did this twice for each tree),  The researchers discovered a strong correlation between branch surface temperature and baseline ant activity, with C. mimosae and C. nigriceps showing greatest activity levels at all temperatures, which increased sharply at higher temperatures.

TamashiroFig 1a

Ant activity levels in relation to branch surface temperature. Shaded areas are 95% confidence intervals for each species.

Do higher temperatures cause a stronger aggressive response to predators or other disturbances? Tamashiro and his colleagues tested this by rapidly sliding a gloved hand over a 15 cm segment of a branch three times and then resting the gloved hand on the branch for 30 s.  They then removed the glove and counted the number of ants that had swarmed onto the glove.  Again, C. mimosae and C. nigriceps showed the strongest aggressive response, which increased sharply with temperature

TamashiroFig 1b

Aggressive swarming by ants in relation to branch surface temperature. Shaded areas are 95% confidence intervals for each species.

While a gloved hand is a nice surrogate for predators, the researchers wanted to know how the ants would respond to a real predator, and whether the response was temperature dependent.  At the same time, they wanted to determine whether the predator would change its behavior in response to changes in ant defensive behavior at different temperatures.  They used eight somali goats (Capra aegagrus hircus) as their predators, and C. mimosae as the focal ant species for these trials.

Cpl. Paula M. Fitzgerald, USMC - United States Department of Defense

Somali goats in Ali Sabieh, Djibouti. Credit: Cpl. Paula M. Fitzgerald, USMC – United States Department of Defense.

The researchers chose eight trees of similar size for their experiment, and removed ants from four of the trees by spraying them with a short-lived insecticide, and preventing ant recolonization by spreading a layer of ultra-sticky solution (Tanglefoot) around the based of each treated tree.  Goats were allowed to feed for five minutes.


Number of bites (top graph) and time spent feeding (bottom graph) by goats in relation to branch surface temperature. Shaded area is 95% confidence interval.

Tamashiro and his colleagues measured the number of bites taken (top graph) and the amount of time spent feeding (bottom graph) at different branch temperatures.  Both measures of goat feeding were not influenced by branch temperature if there were no ants on the trees (blue lines and points).  But if ants were present (red lines and points), goat feeding decreased sharply with increasing branch temperature, presumably reflecting more aggressive ant defense of the plants.

These findings have important implications for acacia trees, which are a critical species in the sub-Saharan ecosystem.  Previous research has shown that elephant damage is strongly influenced by the number of swarming ants on a particular tree; a greater number of swarming ants are associated with less elephant damage. Many vertebrate browsers feed throughout the day, but may feed preferentially at dawn and dusk, when temperatures are cooler and ant-defense is weakest. Browsing is particularly problematic for acacia saplings, which are usually attacked by small-bodied vertebrates such as steenbok, which forage primarily at night when ants are least active.  Thus the effectiveness of ant defense may be compromised by mismatches between vertebrate activity periods and ant activity periods.

note: the paper that describes this research is from the journal Ecology. The reference is Tamashiro, R. A., P. D. Milligan, and T. M. Palmer. 2019. Left out in the cold: temperature-dependence of defense in an African ant–plant mutualism. Ecology 100(6): e02712. 10.1002/ecy.2712 . 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.



Sweltering ants seek salt

Like humans, ants need salt and sugar.  Salt is critical for a functioning nervous system and for maintaining muscle activity, while sugar is a ready energy source. In ectotherms such as ants, body temperature is influenced primarily by the external environment, with higher environmental temperatures leading to higher body temperatures.  When ants get hot their metabolic rates rise, so they can go out and do energetically demanding activities such as foraging for essential resources like salt and sugar. On the down side, hot ants excrete more salt and burn up more sugar.  In addition, like humans, very high body temperature can be lethal, so ants are forced to seek shelter during extreme heat.   As a beginning graduate student, Rebecca Prather wanted to know whether ants adjust their foraging rates on salt and sugar in response to the conflicting demands of elevated temperatures on ants’ physiological systems.

Prather at field site

Rebecca Prather at her field site in Oklahoma, USA. Credit: Rebecca Prather.

Prather and her colleagues studied two different field sites: Centennial Prairie is home to 16 ant species, while Pigtail Alley Prairie has nine species.  For their first experiment, the researchers established three transects with 100 stations baited with vials containing cotton balls and either 0.5% salt (NaCl) or 1% sucrose.  The bait stations were 1 meter apart.  After 1 hour, they collected the vials (with or without ants), and counted and identified each ant in each vial.  The researchers measured soil temperature at the surface and at a depth of 10 cm. The researchers repeated these experiments at 9 AM, 1 PM and 5 PM, April – October, 4 times each month.


Ants recruited to vials with 0.5% salt solution.  Credit: Rebecca Prather.

Sugar is easily stored in the body, so while sugar consumption increases with temperature, due to increased ant metabolic rate, sugar excretion is relatively stable with temperature.  In contrast, salt cannot be stored effectively, so salt excretion increases at high body temperature.  Consequently, Prather and her colleagues expected that ant salt-demand would increase with temperature more rapidly than would ant sugar-demand.


Ant behavior in response to vials with 0.5% salt (dark circles) and 1% sucrose (white circles) at varying soil temperatures at 9AM, 1 PM (13:00) and 5PM (17:00). The three left graphs show the number of vials discovered (containing at least one ant), while the three right graphs show the number of ants recruited per vial.  The Q10 value  = the rate of discovery or recruitment at 30 deg. C divided by the rate of discovery or recruitment at 20 deg. C. * indicates that the two curves have statistically significantly different slopes.

The researchers discovered that ants foraged more at high temperatures. However, when surface temperatures were too high (most commonly at 1 PM during summer months), ants could not forage and remained in their nests.  At all three times of day, ants discovered more salt vials at higher soil temperatures. Ants also discovered more sugar vials at higher temperatures in the morning and evening, but not during the 1 PM surveys. Most interesting, the slope of the curve was much steeper for salt discovery than it was for sugar discovery, indicating that higher temperature increased salt discovery rate more than it increased sugar discovery rate (three graphs on left).

When ants discover a high quality resource, they will recruit other nestmates to the resource to help with the harvest.  Ant recruitment rates increased with temperature to salt, but not sugar, indicating that ant demand for 0.5% salt increased more rapidly than ant demand for 1% sugar (three graphs above on right).

The researchers were concerned that the sugar concentrations were too low to excite much recruitment, so they replicated the experiments the following year using four different sugar concentrations.  Ant recruitment was substantially greater to higher sugar concentrations, but was still two to three times lower than it was to 0.5% salt.


Ant recruitment (y-axis) to different sugar concentrations at a range of soil temperatures (X-axis). Q10 values are to the left of each line of best fit.

Three of the four most common ant species showed the salt and sugar preferences that we described above, but the other common species, Formica pallidefulva, actually decreased foraging at higher temperatures.  The researchers suggest that this species is outcompeted by the other more dominant species at high temperatures, and are forced to forage at lower temperatures when fewer competitors are present.

In a warming world, ant performance will increase as temperatures increase up to ants’ thermal maximum, at which point ant performance will crash.  Ants are critical to ecosystems, playing important roles as consumers and as seed dispersers. Thus many ecosystems in which ants are common (and there are many such ecosystems!) may function more or less efficiently depending on how changing temperatures influence ants’ abilities to consume and conserve essential nutrients such as salt.

note: the paper that describes this research is from the journal Ecology. The reference is Prather, R. M., Roeder, K. A., Sanders, N. J. and Kaspari, M. (2018), Using metabolic and thermal ecology to predict temperature dependent ecosystem activity: a test with prairie ants. Ecology, 99: 2113-2121. doi:10.1002/ecy.2445Thanks 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.

Too much of a good thing is killing Monarch butterflies

There was a time in the mid-Pleisticine when a photo of an ecological event was an awesome novelty, and a movie of an ecological event even more so.  Dodderers of an ecological bent (myself included), can vividly recall viewing a series of photos or a movie, either in a seminar or in an ancient ecology text, of a blue jay consuming a monarch butterfly, Danaus plexippus.  Consumption is immediately followed by explosive vomiting, as the cardenolides within the monarch butterfly claim another victim.  The monarch sequesters these cardenolide toxins from its larval food (milkweed), and incorporates them into its tissues as a means of protecting itself from predators – presumably blue jays learn from this very aversive experience.  I should point out that the individual sacrificial butterfly enjoys no fitness from this learning event – which raises some evolutionary questions we will not explore at the present.

Karen Oberhauser

Five instars (stages of development) of monarch caterpillars on a milkweed leaf. Credit: Karen Oberhauser

Rather we turn our attention to the relationship between milkweed, monarchs, and climate change. In several places in this blog we’ve talked about how climate change has influenced the behavior or physiology of a single species. For example, my first blog (Jan 31, 2017) discusses how increasing temperatures create more females in a loggerhead turtle population. But there are fewer studies that explore how climate change influences the ecological landscape, ultimately affecting interactions between species.  Along these lines, Matt Faldyn wondered if increased air temperature would change the chemical constitution of milkweed in a way that might influence monarch populations.  As he describes, “With milkweed toxicity, there is a ‘goldilocks’ zone where monarchs prefer to feed on milkweed that produce enough toxins in order to sequester these (cardenolide) chemicals as an antipredator/antiparasite defense, while also avoiding reaching a tipping point of toxicity where feeding on very toxic milkweeds negatively impacts monarch fitness.” He expected that at higher temperatures, milkweed would become stressed, and be physiologically unable to sustain normal levels of cardenolide production.


Monarch butterfly feeds on a native milkweed, Asclepias incarnata. Credit: Teune at the English Language Wikipedia.

For their research, Faldyn and his colleagues worked with two milkweed species.  Asclepias incarnata is a common, native milkweed found throughout the monarch butterfly’s range in the eastern and southeastern United States.  Asclepias curassavica is an exotic species that has become established in the southern United States.  In contrast to A. incarnata, A. curassavica does not die back over the winter months; consequently some monarch populations are no longer migratory, relying on A. curassavicato provide them with a year round food supply.


The exotic milkweed, Asclepias curassavica. Credit: 2016 Jee & Rani Nature Photography (License: CC BY-SA 4.0)

To protect against herbivory, milkweeds have two primary chemical deterrants: (1) the already-mentioned cardenolides, which are toxic steroids that disrupt cell membrane function, and (2) release of sticky latex, which can gum up caterpillar mouthparts and actually trap young caterpillars.

field_noborderii.jpgThe researchers wanted to simulate climate change under field conditions, so they created open-top chambers with plexiglass plates that functioned much like mini-greenhouses, into which they placed one milkweed plant that was covered with butterfly netting.  This setup raised ambient temperatures by about 3°C during the day and 0.2°C at nighttime.  Control plots were single milkweed plants with butterfly netting. Half of the plants were native milkweed, and the other half were the exotic species.

For their experiments, Faldyn and his colleagues introduced 80 monarch caterpillars (one per plant) and allowed them to feed normally until they pupated.  Pupae were brought into the lab and allowed to metamorphose into adults.


Matt Faldyn holds two monarch butterflies in the laboratory. Credit Matt Faldyn.

At normal (ambient) temperatures, monarchs survived somewhat better on exotic milkweed.  But at warmer temperatures, there is a strikingly different picture. Monarch survival is unaffected by warmer temperatures on native milkweed, but is sharply reduced by warmer temperatures on exotic milkweed (top graph below). The few that managed to survive warm temperatures on exotic milkweed grew much smaller, based on their body mass and forewing length (middle and bottom graph below)


Survival (top), adult mass (middle) and forewing length (bottom) of monarch butterflies raised under normal (ambient) and warmed temperatures.  Error bars are 95% confidence intervals.

Both milkweed species increased production of both types of chemicals over the course of the experiment. But by the end of the experiment, the exotic species released 3-times the quantity of latex and 13-times the quantity of cardenolides than did the native milkweed species.


Average amount of latex released at the beginning and end of the experiment.  Error bars are 95% confidence intervals.


Average cardenolide concentration at the beginning and end of the experiment.

The researchers argue that the exotic milkweed, Asclepias curassavica, may become an ecological trap for monarch butterflies, in that it attracts monarchs to feed on it, but will, under future warmer conditions, result in dramatically reduced monarch survival. Interestingly, these results are not what Faldyn originally expected; recall that he anticipated that temperature-stressed plants would reduce cardenolide production. The tremendous increase in cardenolide production in exotic milkweed at warmer temperatures may simply be too much toxin for the monarchs to process. The researchers predict that as climate warms, milkweed ranges will expand further north into Canada, and lead to northward shifts of monarch populations as well.  They urge nurseries to emphasize the distribution of native rather than exotic milkweed, so that monarchs will be less likely to become victims of this ecological trap.

note: the paper that describes this research is from the journal Ecology. The reference is Faldyn, M. J., Hunter, M. D. and Elderd, B. D. (2018), Climate change and an invasive, tropical milkweed: an ecological trap for monarch butterflies. Ecology. doi:10.1002/ecy.2198. 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.

Parrotfish put on their big boy pants

While it would be awesome if parrotfish were named for their conversational abilities, it turns out that they earn their moniker for their specialized teeth that are fused together for scraping algae from coral, thus resembling a parrot’s beak. Despite lacking verbal skills these fish are incredible. Approximately 100 species occupy reefs, rocky coastlines and eelgrass meadows in tropical and subtropical waters. Many species are sequential hermaphrodites, beginning life as females and then changing into males after reaching a certain size. While female reproductive success is limited by the number of eggs she can produce, male reproductive success can be much higher if he can fertilize the eggs of many females.  So if a parrotfish transitions into a large male, and can control access to numerous females, he will enjoy greater reproductive success than if he had remained a female.

C. spilurusBrettTaylor

Two Chlorurus spilurus parrotfish show off their teeth and colors.  The large colorful fish on the right is a male, while the smaller darker fish to his left is a female. Credit: Brett Taylor.

Phenotypic plasticity describes the ability of an individual with a particular genetic makeup to vary in a variety of traits (such as what it looks like, or how it behaves) in response to different environmental conditions. About 15 years ago, Nick Gust’s PhD research on tropical reef fish revealed that tremendous variation in parrotfish traits existed over a distance of a few kilometers. But what causes this variation? When funding became available, Brett Taylor jumped at the opportunity to pinpoint the causes, focusing on the diverse parrotfish community in the Great Barrier Reef (GBR).


Eastern slope of the Great Barrier Reef hosts a diversity of fish and coral species. Credit: Brett Taylor.

Taylor and his colleagues surveyed 82 sites within 31 reefs across 6 degrees of latitude in the northern GBR. To standardize data collection, divers, armed with a multitude of cameras and GPS devices, swam at a standardized rate (about 20 meters/minute) for 40 minutes per survey, recording each parrotfish along a 5 m wide swath. They collected data about the habitat and the environment, about the physical traits of each individual parrotfish (such as size and sex), and about the type and abundance of parrotfish and their predators present at each site.


Researcher takes notes while conducting a dive.  Credit Kendra Taylor.

The researchers wanted to identify what factors influenced growth rate, maximum body size, and the size at sex change, and how these factors related to the parrotfish mating system. Four species of parrotfish were sufficiently abundant across the GBR to allow researchers to do this type of analysis.


Four parrotfish species  abundant along exposed outer shelf (yellow sites) and protected inner shelf (blue) regions of the Great Barrier Reef. Males are larger and more colorful.

The GBR varies structurally across a relatively small spatial scale of 40 – 100 km, with outer shelf regions (eastern) exposed to wave action, and inner shelf regions (western) relatively protected. All four species tended to change sex at a larger size in protected sites than they did at exposed sites. However, the differences are only compelling for two of the species: C. spilurus and S. frenatus. There were fewer data points for the other two species, so it is possible (but unknown) that they too would show a more pronounced trend if more data were available.


Proportion terminal phase (sex-changed males) in relation to body size (measured to the fork of the tail) in exposed (yellow) and sheltered (blue) sites.

Not surprisingly, parrotfish grew larger in protected areas. Presumably, less wave action provided a more benign environment for rapid growth, both of parrotfish and their preferred food items (algae growing on rocks and coral).


Standardized maximum size (Lmax) attained by parrotfish in sheltered vs. exposed sites.

The researchers were somewhat surprised that most other factors, such as latitude, coral cover, sea surface temperature, and predator abundance, had very little effect on the size at sex change. Rather, the size at sex change appears to be strongly influenced by the local size distribution. In protected habitats, parrotfish grow large and change sex at a large size, while in exposed habitats, parrotfish are smaller, and change sex at a smaller size.

But sex is never simple. Nick Gust’s PhD research showed that C. spilurus had different patterns of sexual allocation in protected vs. exposed areas. In protected areas, the mating system is haremic, with a large male defending a territory and servicing a harem of females. In exposed areas, the mating system is mixed; there still are large territorial males with their harems, but they compete with many more small males, and group spawning is much more prevalent. Theoretically, the presence of these small males may make it less worthwhile for a female to transition into a male, and may influence the optimal size for transitioning in exposed reefs. Given that we still don’t know the mating system details of the other parrotfish in this study, it will be fascinating to see if they too show similar patterns of haremic vs. mixed mating systems in relation to habitat structure.

note: the paper that describes this research is from the journal Ecology. The reference is Taylor, B. M., Brandl, S. J., Kapur, M., Robbins, W. D., Johnson, G., Huveneers, C., Renaud, P. and Choat, J. H. (2018), Bottom-up processes mediated by social systems drive demographic traits of coral-reef fishes. Ecology 99(3): 642-651. doi:10.1002/ecy.2127. 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.

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.

Climate change: to bee or not to bee

From the standpoint of how they regulate their body temperature, we can very crudely divide the animal world into ectotherms and endotherms. Ectotherm body temperature is influenced primarily by the external environment, while endotherms maintain a relatively constant body temperature by conserving the heat they generate from the many chemical reactions that occur within their body. This division is crude because there are many, many organisms, including the bee species that is the focus of this tale, that use both approaches.


The mason bee, Osmia iridis, with a color-marking on its thorax. Credit Jessica Forrest


For now, I’m going to make a generalization that it is very difficult to be a small ectotherm in cold climates. After all, small animals can’t have much insulation, and most of the cells belonging to small ectotherms are located near the surface, and subject to the chilling effects of the cold air. Cold cells can’t do much because most chemical reactions that power our small ectotherm need warmth for maximum efficiency.

Perhaps the most common small-ectotherm-in cold-climates approach is to be active only on warm sunny days. This works great, so long as there are sufficient warm sunny days to get on with the business of life (primarily food, sex and not becoming someone else’s dinner). Rumor has it that there was a huge celebration of small-ectotherms-in cold-climates, when they heard about Donald Trump’s election, as they reasoned that global warming was likely to continue, and they might be able to enjoy a more successful life.

Jessica Forrest and Sarah Chisolm wanted to know how rising temperatures would affect the success of the solitary mason bee, Osmia iridis, in cold climates. This bee survives by consuming nectar and pollen gathered from leguminous plants (bean and peas are common legumes), primarily Lathyrus lanszwertii, and Vicia americana. This bee can elevate its body temperature somewhat above air temperature, but its body temperature, and consequent activity levels are nonetheless greatly influenced by air temperature. The researchers reasoned that warmer temperatures would allow the bees to fly more often and gather more nectar and pollen, so they could grow more quickly, reach a larger size and produce more bee babies.

 Co-author Sarah Chisolm observes bees and wasps at the field site at Rocky Mountain Biological Laboratories in Crested Butte, Colorado. Credit Jessica Forrest.
Three Lathyrus lanszwertii flowers. Credit Jessica Forrest.


But there’s a fly in many ointments, or in this case a brood parasitic wasp, Sapyga pumila, which can lay its egg in a nest cell where the bee has just laid its egg. The wasp egg usually hatches first, kills and eats the bee baby, and, adding insult to injury, also eats the pollen that the bee mother has left to provision its (now dead) baby. So if warmer temperature helps the wasp, by giving it more flight time and faster development, perhaps warmer temperatures will actually decrease the bee’s reproductive output.


Sapyga wasp approaches a bee’s nest entrance. Credit Jessica Forrest



Larval Sapyga wasp (center) begins to eat a bee egg (bottom right). Credit Jessica Forrest













So how does this play out?

Forrest and Chisolm marked and released 109 bees over the course of three years, and discovered that these bees, on average, built more nest cells on warmer days. This could indicate that bee reproductive output increases with temperature. But only if all other factors influenced by air temperature are equal.


But all factors influenced by temperature are not equal. As it turns out, Sapygia wasps, the most significant parasite on these bees, are most active at high temperatures as well. So while bees can make more nest cells at high temperatures, they also need to deal with more parasitic wasps.


These bees make more babies when most of their nest cells are not parasitized. Very few offspring are produced when the parasitism rate climbs above 0.5 (50%).


Overall it’s pretty much a wash for the bees. Bees benefit directly from increased nest cell construction at high temperatures, but suffer from the increased rate of parasitism. In contrast, the parasites are more successful at high temperatures. Several other studies of hosts and parasites have shown that the parasites usually benefit from increased temperature more than the hosts, but there are some counterexamples. The authors caution us that forecasting the impact of future warming requires understanding all the factors that can affect population regulation – a daunting challenge. In the meantime our bees may want to cancel their “We love Donald Trump” party, as their enemies appear to be benefiting more than they are from a warmer climate.