The Lizard Log

The Langkilde Lab in Action


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Lizard in PA

So, here’s a song about being a lizard in the cold, cold, northeast US.

And for those who may not notice, it is specifically

about a male Sceloporus undulatus in Pennsylvania.

 

 

Lizard in PA  (click here if the link above is not functional)

It’s cold outside

and I can’t move my muscles

cause my physiology won’t bring the heat,

but I’ll be fine.

 

My parietal eye will tell my future

by and by

and by the sun

I will move on,

when the winter’s gone.

 

I’m a lizard in PA

and I’m coming out today

to heat my bones

and eat a bug.

 

Heat my bones

Heat my bones

 

I’m a lizard in PA

and I’m coming out today

to heat my bones

and eat a bug.

 

I hope I find my mates

and set my territory straight

before I see a flash of blue

that comes to call,

I’ll fight um all.

 

Their push ups

don’t scare me

I’m sure they’re all one hemipene

shy of a clutch,

I’d bet my lunch.

 

Heat my bones

Heat my bones

 

I’m a lizard in PA

and I’m coming out today

to heat my bones

and eat a bug.

 

Heat my bones

Heat my bones

.Heat

……….my

……………….bones

and eat bug.

 

(c) 2014

Music, lyrics, vocals, and harmonica by Travis R. Robbins

Music, vocals, and guitar by Kristan Robbins

Produced at Gwendolyn’s Sleeping Studio (TM)

 

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Do fence lizards take a chance and eat stinging ants when exotics advance? Indeed they do!

Part 2 of 2 in the fence lizard fire ant saga: Rapid evolution of fence lizards (Sceloporus undulatus) in response to selective pressures imposed by red imported fire ants (Solenopsis invicta).

I’m a postdoctoral research fellow in the Langkilde Lab who studies the ecological mechanisms that result in evolution. My interests range from the evolution of life histories in response to climate change to behavioral evolution in response to invasive species to the evolutionary significance of culture.  Most of my research, however, is on Sceloporus lizards (AKA Spiny lizards or Swifts), focusing on their genetic and plastic responses to environmental change and the underlying interactions between physiological (e.g. hormonal), behavioral (e.g. resource use and niche construction), and epigenetic mechanisms. My research endeavors have brought me to Costa Rica, Panama, Mexico, the subtropics of Florida, and inside Biosphere 2 in the Arizona desert, but I am currently focusing on lizard evolution in the southeastern US, which brings us to the current continued blog post.

So, in the first chapter of the Saga we found out that fence lizards are adapting to habitats where they coexist with fire ants, which quickly find and attack lizards when on the ground. Some fence lizards dance and run away from fire ants when attacked, and the number of lizards that exhibit this behavior increases the longer a population has experienced fire ants. See the first chapter of the Saga here.

Fire ants attacking lizards is interesting, but what is even more interesting is that this interaction can be turned on its head!  Ants are a normal part of a fence lizard’s diet, so why wouldn’t fire ants be susceptible to being eaten by a fence lizard? Fire ants are susceptible! We’ve noticed while in the field that fence lizards do occasionally eat fire ants during encounters.  Not surprising, until you pick up a little insider information about a strange twist.  One of Tracy Langkilde’s studies revealed that eating fire ants can decrease lizard survival!

If it is bad for lizards to eat fire ants, why do they do it?  In light of what appears to be evolution with regard to the dance and run behaviors, we hypothesized that fire ant-eating behavior of fence lizards should be less frequent in populations that have experienced fire ants for a longer time (i.e. more generations). We tested this by recording fire ant consumption during staged encounters between fire ants and fence lizards from both fire ant invaded (experienced) and uninvaded (naïve) lizard populations. We also tested both juveniles and adults because we knew that they have a tendency to respond to fire ants differently.

We found a complex relationship that somehow supports both what we already knew from previous experiments (adults in fence lizard populations are adapting to the presence of fire ants) and our newer hypotheses about juvenile lizards adapting to the fact that eating fire ants can be toxic!  It seems that adult fence lizards from populations that have been coexisting with fire ants for a long time eat fire ants much MORE frequently than lizards that have never experienced fire ants.  What!?

AntInsideMouth - T. Langkilde, T.R. Robbins

Photo credit: T. Langkilde, T.R. Robbins

Figure 2 - Robbins Langkilde 2012 - JEB

Fire ant consumption by lizards. The proportion of field-caught (a) and laboratory-reared (b) adult (open squares) and juvenile (solid squares) fence lizards, Sceloporus undulatus, from a fire ant-invaded and uninvaded site that consumed fire ants during fire ant attack. Points represent mean values ± 1 standard error.
Figure – Robbins and Langkilde 2012 J Evol Biol 25(10):1937-46

We also found, as we hypothesized, that juvenile fence lizards from populations that have been coexisting with fire ants for a long time eat fire ants much LESS frequently than their inexperienced counterparts.  So we see changes in feeding behavior in fence lizards after fire ants invade their habitat, just like we saw with the dance and run anti-predator behaviors. What is more fascinating, however, is that our results with regard to feeding behavior suggest what is called an ontogenetic shift in selection pressures.  That is, it is more adaptive to behave one way while young and then behave the opposite way when older!  Fire ant invaded habitats select (via natural selection) juveniles that do not eat fire ants, but can learn to eat fire ants once they grow up!

Next, obviously, we wanted to test if and how well juvenile lizards learn to eat fire ants.  Our hypothesis for this experiment was actually that the lizards would learn NOT to eat fire ants because they get stung in the mouth when they eat them. At some time during their life with fire ants they seem to learn to eat fire ants, but we thought it would be after they were adults because fewer juveniles from the invaded site had eaten fire ants when on the mound and under attack (see above).

lizfirenear

Photo credit: T. Langkilde, T.R. Robbins

We were wrong!  When it comes to eating fire ants, the longer lizards are exposed to fire ants the more lizards eat them!

Figure 2 - Robbins et al 2013 - Biol Inv

Proportion of lizards from invaded (open circles and broken line) and uninvaded (solid circles and solid line) populations that ate a fire ant over a 6-day period. During this period lizards were fed 1 fire ant followed later by 2 crickets each day, representing a subsistence diet. Points show proportions ± 1 standard error.
Figure – Robbins et al 2012 Biol Inv 15: 407-415

We even found that more juvenile lizards from the invaded site ate fire ants during the experiment than those from the uninvaded site (lizards naïve to fire ants).  So, juvenile lizards appear to learn to eat stinging ants pretty quickly when they are not on a mound being attacked!  It changed from 50% to 80% of lizards eating fire ants within 6 days.  Maybe fire ants are addictive like hot sauce is for us! Endorphins can be powerful rewards.

I know, it’s a little confusing.  Juveniles from invaded sites (i.e. that have experience with fire ants) eat fire ants less often when on the mound being attacked (first graph), but more often when fed one ant each day over a 6 day period (second graph)?  Well, the two scenarios are a little different with a lizard being under attack by many fire ants in the first and in the other only being exposed to one lonely fire ant.  And that may have something to do with the it.

The effects of envenomation are mass dependent, so the fact that juvenile lizards are small means that they can be overcome by fire ant venom faster than adults. When a juvenile lizard is on a fire ant mound and notices many potentially stinging ants, it doesn’t think to eat them as much as it thinks to dance and run away.  However, away from fire ant mounds fire ants are often an abundant potential food source.  When fire ants invade habitats they pretty much take over and push out many of the other arthropods that otherwise serve as food for lizards.  Although eating fire ants can increase the chances of a lizard’s early demise, eating a few fire ants here and there will not overtly harm all juvenile lizards.  Even in the study that found an increase in mortality after eating fire ants there was still a 66% survival rate.  So, because venom effects are mass dependent, it’s possible that juvenile lizards that survive and grow up (and thus get bigger) can eat more fire ants (and get stung) without feeling the negative effects of fire ant venom.

Although natural selection appears to select juvenile lizards that do not eat fire ants when being attacked, it seems they like to get stung in the tongue as they become less young!  But this tale has yet to be completely sung! We only fed the lizards 1 fire ant per day, which may not be enough to make them learn to avoid eating them.  They may easily forget what they had for breakfast yesterday and thus need to experience eating and getting stung on the tongue a few times a day to learn to avoid eating fire ants.  Or not.  We are analyzing experiments we designed to test just that right now!

So the saga continues . . .


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If lizards had pants the pants would have ants and the lizards would dance. Indeed they do!

Part 1 of 2 in the fence lizard fire ant saga: Rapid evolution of fence lizards (Sceloporus undulatus) in response to selective pressures imposed by red imported fire ants (Solenopsis invicta).

Dr. Travis R. Robbins is a postdoctoral research fellow in the Langkilde Lab who studies the ecological mechanisms that result in evolution. His interests range from the evolution of life histories in response to climate change to behavioral evolution in response to invasive species to the evolutionary significance of culture.  Most of his research, however, is on Sceloporus lizards (AKA Spiny lizards or Swifts), focusing on their genetic and plastic responses to environmental change and the underlying interactions between physiological (e.g. hormonal), behavioral (e.g. resource use and niche construction), and epigenetic mechanisms. His research endeavors have brought him to Costa Rica, Panama, Mexico, the subtropics of Florida, and inside Biosphere 2 in the Arizona desert, but he is currently focusing on lizard evolution in the Southeastern US, which brings us to the current blog post.

Dude

Photo credit: T.R. Robbins

For the past three years I have been studying how fence lizards change their behavior and morphology after red imported fire ants invade the fence lizard habitat. This amazing study system that Dr. Tracy Langkilde fostered almost a decade ago reveals more exciting ecology with every research project!  Tracy found an interesting trend across fence lizard populations that were invaded by fire ants at varying times in the past.  The longer fence lizard populations coexist with fire ants, the more fence lizards in each population begin to respond to agonistic encounters with fire ants.

Change in use of (a, d) body twitch (solid symbols) and (b, e) flee (solid symbols) defensive behavior, and (c, f ) the relative hind limb length (shown as hind limb length/snout–vent length, SVL); of adult vs. juvenile fence lizards (Sceloporus undulatus) across sites with different histories of fire ant invasion. Open symbols represent behavior exhibited during control trials conducted in the absence of fire ants. Sexes are pooled for all panels. In all panels, values for adults represent mean 6 SE for 20 male and 20 female lizards from each site; values for juveniles represent mean 6 SE for 157 juveniles born to 16 females from Site 1, and 128 juveniles born to 18 females from Site 4. Figure  – Langkilde 2009 Ecology 90(1): 208-217

Change in use of (a, d) body twitch (solid symbols) and (b, e) flee (solid symbols) defensive behavior, and (c, f ) the relative hind limb length (shown as hind limb length/snout–vent length, SVL); of adult vs. juvenile fence lizards (Sceloporus undulatus) across sites with different histories of fire ant invasion. Open symbols represent behavior exhibited during control trials conducted in the absence of fire ants. Sexes are pooled for all panels. In all panels, values for adults represent mean 6 SE for 20 male and 20 female lizards from each site; values for juveniles represent mean 6 SE for 157 juveniles born to 16 females from Site 1, and 128 juveniles born to 18 females from Site 4.
Figure – Langkilde 2009 Ecology 90(1): 208-217

Usually this lizard species uses crypsis to avoid predation, so it is not prone to moving when something, that is usually harmless (i.e. not a fire ant), crawls over it. The lizards respond to fire ants, however, by dancing (twitching) and running away! And they evolve longer hind limbs so they can be really efficient at it!

Most of our data collection has been about how fence lizards respond to fire ants when they find themselves being attacked on top of a fire ant mound.  Fire ants are quite aggressive when they find someone knocking on their door. Unfortunately, especially for those of you that live with fire ants in your yard, fire ants spend a lot of time away from the mound ubiquitously foraging and roaming around the habitats they invade. Lizards surely encounter fire ants when they have the displeasure of accidentally knocking, but most of the time lizards are basking in the sun or foraging for food somewhere other than fire ant mounds. Thus, we wondered how often a fence lizard would encounter a fire ant away from a fire ant mound, so we conducted an experiment.  We placed lizards 4 meters away from a fire ant mound (and fire ant mounds are approximately 10 meters apart where abundant, so this almost as far as you can get from one!) and observed them to measure how long it would take for a fire ant to find the lizard.  We also measured the behavioral response of the lizard and its effectiveness in avoiding an attack.

Fence lizards were found by fire ants within 105 seconds on average!

We call the first fire ant to find a lizard a “scout”, and this single ant is not much of a threat to a fence lizard.  However, that scout tells his buddies where to find the lizard, and a bunch of ants start heading toward the lizard to attack.  We call this “recruitment”, and this higher number of ants attacking is potentially dangerous.  It only takes 12 ants to immobilize an adult fence lizard in 60 seconds.  But, don’t worry, we never let this happen during our trials. We hypothesized that fence lizards that grew up with fire ants would enact their dance and run technique (twitch and flee behavior) whereas naïve fence lizards would not.  We also hypothesized that the dance and run would be effective at curtailing the recruitment.  If fence lizards responded to the scout before the scout could bring back recruits, the recruits would come to an empty spot, and the lizard in its new spot would no longer be threatened by an attack.

Our results suggested that this was indeed the case!  Experienced lizards (those caught in the field at the invaded site) danced and ran when they encountered the scout.

Figure 1 - Freidenfelds et al 2012 - Behav Ecol

The proportion of field-caught (gray bars; n = 40 from each site) and laboratory-raised (white bars; n = 22 from each site) adult fence lizards from an invaded and uninvaded site that behaviorally responded to attack by red imported fire ants on a fire ant mound. Bars represent mean values ± 1 SE. Different letters above the bars denote significantly different groups.
Figures – Freidenfelds et al 2012 Behav Ecol 23: 659-664

We found that experience with fire ants (lizards from the invaded site) affected only adults, however, because juvenile lizards from all populations were scaredy-cats, running away quickly. We also found that dancing and running in response to a scout was an effective strategy to escape the danger of an attack by recruits.

Figure 2 - Freidenfelds et al 2012 - Behav Ecol

The proportion of fence lizards that had red imported fire antsrecruit to attack them after being located by a fire ant scout, comparing responder (lizards that behaviorally responded to fire ants, n = 13) and nonresponder (lizards that did not respond to fire ants, n = 7) adults. Bars represent mean values 6 1 SE. Different letters above the bars denote significantly different groups.

Our results suggest that when lizards grow up with fire ants they change their behavior in an adaptive way that likely increases their biological fitness by avoiding attacks by stinging fire ants (likely keeping them alive and in better moods). Overall, we have found that the longer a population has coexisted with fire ants, the more fence lizards in the population exhibit the changes, suggesting that these behaviors and morphologies are evolving to help fence lizards adapt to deal with the pesky, painful, and potentially portentous fire ants.  We are currently examining whether or not these behaviors are inherited by comparing behaviors of mothers to their offspring once they become adults.

Stay tuned . . .