Pregnancy, growth and drought

We currently have transmitters implanted in six female rattlesnakes. We have been tracking Female 39 since 2014 and Females 41 and 53 since 2015 and all are currently pregnant and in their gestation shelters where they will likely thermoregulate for six weeks or more. Furthermore, they have all produced a brood during each season we have been following them, so this will be the third year in a row for Female 39 and the second in a row for 41 and 53. And we don’t know how many consecutive years they might have reproduced before that! Each has returned to the same gestation refuge each year, although 41 uses a different location than 39 and 53, who gestate together. We have also found pregnant unmarked females in both places in past seasons with these girls.

That’s not all. We have three new females this season, numbers 66, 75 and 80. These snakes do not appear to have settled into gestation shelters yet (and I don’t know where they were in previous years) but I just implanted a transmitter in Female 80 a few weeks ago and could feel six fetuses in her belly…it felt like she had swallowed six soft ping pong balls! I’m not sure about the reproductive status of 66 and 75, since their surgeries were earlier in the year and both had so much material in their intestines that it made identifying small embryos with confidence difficult.

Another opportunity to assess the health and growth of the rattlesnakes at Effie Yeaw Nature Center occurred day-before-yesterday (13 July) when Kelly came across an adult rattlesnake at the end of the Visitor Center building early in the morning. Per protocol, she expertly maneuvered it into the capture bag and deposited it in the holding barrel for me. It turned out to be Male 52, a rattlesnake previously captured, processed, and released without a transmitter early in May 2015. At that time, he was 30.7 inches in total length and weighed 11.6 ounces. He now measures 33.5 inches and weighs 18.9 ounces. While increasing 9% in length and 63% in mass in 14 months, he has shed three times (see photo below).

For those of you new to the blog, I inject acrylic paint into the first hollow segment of the rattle
For those of you new to the blog, I inject acrylic paint into the first hollow segment of the rattle, next to the black live segment at the end of the tail. With a different color combination for each snake, it allows me to visually identify them. As the snake grows and sheds the corneal layer of its skin periodically, it produces a new rattle segment with each shed. The segment with the paint is thus moved away from the tail until it eventually breaks off. When this seems imminent, as in Male 52 above, I inject paint into another segment to preserve the marking.

 

The constant growth of all the rattlesnakes being sampled and the annual reproduction of many of the females attests to the health of not just the rattlesnake population but the overall small animal community in the riparian habitat at Effie Yeaw Nature Center. While the region is undeniably in a severe long-term drought, enough local rainfall has occurred to keep the annual plants, shrubs, some trees, and the food web they support healthy.

Finally, I want to share with you a little bit about a presentation I made at the annual Joint Meeting of Ichthyologists and Herpetologists last week in New Orleans. I have reproduced the published abstract (summary) of my talk below. Please excuse the Latin names. Crotalus scutulatus is the scientific term for the Mohave rattlesnake and Crotalus oreganus is our own northern Pacific rattlesnake. While recent drought has not yet affected the rattlesnakes or their prey in the areas of northern California I have sampled, 2002 was a rainless year in the Mohave Desert, with no plant growth and a dramatic reduction in the availability of kangaroo rats and other small mammals that make up the great majority of the rattlesnakes’ diet there. During 2002, Mohave rattlesnakes changed their behavior very significantly, staying tightly coiled and avoiding wind and sun while moving very little and not courting or mating.

Cardwell abstract

The take-home message I delivered in New Orleans was that (1) these animals are used to hot dry summers and get most of their water from their prey; (2) regional drought does not necessarily equal local drought; (3) rattlesnake behavior is probably not affected by drought until prey availability is affected; (4) water-stressed rattlesnakes minimize exposed skin by remaining coiled most of the time; (5) when water-stressed, they don’t move more, they move a lot less than usual; and (6) there is no evidence that they leave their normal home range during a drought.

In other words, there is zero evidence to support the frequent news media claims that drought drives rattlesnakes into yards.

Emphasis now on hunting and shedding

Before I launch into what’s been going on with the Effie Yeaw rattlesnakes over the past few weeks, I want to pass on a link to a recent interview with Dr. Bree Putman. Bree was a grad student with Matt Holding (lead author of the journal article I linked to in my last post) in Emily Taylor’s lab at Cal Poly San Luis Obispo before she moved on to Rulon Clark’s lab at San Diego State to finish her Ph.D. In Bree’s interview (click here), she talks about ground squirrels and northern Pacific rattlesnakes and she describes some of the very intriguing behavioral questions many of us would love to answer.

Back to EYNC rattlesnakes –

This female California ground squirrel was clearly nursing pups on 26 April at Effie Yeaw Nature Center.
This female California ground squirrel was clearly nursing pups on 26 April in the Effie Yeaw Nature Center preserve.

I have not seen a courting pair of rattlesnakes since 28 April, when three rattlesnake pairs were found together in different locations. Male 37 was found with unmarked adults that were likely females on 11 and 14 May but no courtship was observed. But as the spring courtship season wound down, California ground squirrels began producing pups and the emphasis of both rattlesnake sexes turned to hunting.

After not finding a telemetered rattlesnake in or very near a ground squirrel burrow during the first 400+ observations this year, Male 46 was found in an ambush coil facing an active burrow a foot away on 9 May. In the five weeks since, several rattlesnakes have been found close to or inside squirrel burrows on several occasions.

At the same time, the snakes have also been hunting heavily in vole (aka: meadow mouse; Microtus californicus) tunnels in the grass.

Male 46 visible in a vole tunnel on the morning of 3 June 2016. Original RAW IMG_2192.CR2
Male 46 uncovered (arrow) in a vole tunnel in the grass on the morning of 3 June. Although you cannot see it here, voles construct a maze of above-ground tunnels in thick dry grass that protects them from most predators… but not rattlesnakes. I hope you can appreciate just how impossible it would be to learn about the habits of these snakes without radiotelemetry!

And since about the end of May, the rattlesnakes – especially males – have been shedding.

Pre-shed Male 38 on 14 June 2016 Original RAW IMG_2320.CR2
The rattle of pre-shed Male 38 under a log yesterday, 14 June. The new rattle segment forming in the base of the tail is whitish and covered by the last couple rows of scales. He is easily identified visually by red/green paint in his rattle.

Periodically shedding the corneal layer of the skin (called ecdysis; for more info, click here) takes snakes out of commission for a week or more and males seem to put it off during the spring mating season. It’s a bit like race car drivers waiting for a yellow caution flag to make a pit stop!

Even more interesting is that the rattlesnakes have favorite places where they go during this process and it is not uncommon to find several pre-shed individuals of both sexes together this time of year. Like hibernation, there seem to be many logs and burrows where they could shelter while waiting to shed but they congregate in just a few of them. Those of us who study rattlesnake behavior would love to know why. What is so special about certain locations? Or is it something else… like family ties or some other social interaction?

 

Male 36 finally recaptured!

If you have been following my rattlesnake study from the beginning, you know that we struggled through some faulty transmitters early in the project (search “failed transmitters” for previous info). The first six transmitters I implanted failed early. Several failed during hibernation (2014/15) and, because I knew where the snakes spent the winter, I was able to capture them when they began basking in the spring. Two, however, proved to be a bigger problem.

Male 36’s transmitter was first to fail in September 2014, with two months of activity remaining that season. Male 37’s transmitter lasted into the winter but he hibernated high on the bluff under a thick mat of vegetation, making his exact location very difficult to visit and impossible to pinpoint. Thus, both emerged in the spring of 2015 without functioning transmitters.

Both eluded recapture until October 2015, when I found Male 37 (details here) under the log I call “The Community Center” because everybody visits it from time to time. Males visit looking for girls, pregnant females hang out there to thermoregulate and give birth, and both sexes use it for shelter while waiting to shed (but nobody spends the winter there). I replaced Male 37’s transmitter then, leaving only Male 36 unaccounted for – until last week.

After twenty months, I had just about given up on finding Male 36 again. But when I checked around The Community Center one day last week, I was thrilled to spot his rattle with red/red paint! Like Male 37 last fall, Male 36 was also pre-shed and using The Community Center for shelter while he waited to complete the process.

Pre-shed Male 36, with failed transmitter, at Refuge 01, Effie Yeaw Nature Center, on 11 May 2016, moments before his recapture. Original RAW IMG_1531.CR2
Pre-shed Male 36, with failed transmitter, at The Community Center on 11 May 2016, moments before his recapture. If you look closely (partly obscured by grass), you can make out the new light-colored rattle segment forming under the skin at the rattle base.

 

Just like Male 37, I captured Male 36 and kept him several days until he shed. His transmitter was replaced and he was released yesterday.

Male 36 disappearing into
Male 36 disappearing into The Community Center yesterday with a new transmitter and re-marked rattle (his rattle is quite long and likely to break soon, potentially taking his original paint with it). Note how clean and crisp his pattern appears after shedding, compared to the photo above.

 

The return of Male 36 fills my permit quota of seven telemetered males. We currently have five females telemetered and I am holding out, hoping to get a couple of females radio-tagged farther out in the northeastern portion of the preserve where few of our current snakes venture. Interestingly, Male 38 was hanging around with two females out there last week, including last Saturday when I was hosting a video crew from UC Santa Cruz. While I would have loved to get a transmitter into one of them, they were too wary and repeatedly escaped when approached.

I wish more people could see just how hard these fascinating creatures try to avoid confrontations with people!

 

 

Missing Male 37 captured!

After being on the lam since December when his transmitter failed prematurely during hibernation, Male 37 was discovered getting ready to shed in one of his favorite hollow logs last Friday and recaptured. As soon as he sheds in a few days, his transmitter will be replaced and he will be released. Note in the photos below that this will be his 4th shed in 16 months (4 new rattle segments behind the paint); his new live segment is still covered by thin scales that will be lost with this shed. He has also lost five old segments from the end. He will be on display at our Living with Rattlesnakes booth at EYNC’s Nature Fest tomorrow, October 4th.

CROR's rattle on 3 October 2015
CROR 37’s rattle on 3 October 2015.
CROR37's rattle on 14 June 2014.
CROR 37’s rattle on 14 June 2014.

Rattle Growth, Shedding & Estimating Age

Now is the perfect time for this discussion because the Effie Yeaw rattlesnakes have been shedding like crazy. Since the end of spring courtship about two months ago, the pregnant females have hunkered down to thermoregulate at optimum gestation temperature while the males and non-reproductive females have been hunting with far less attention to temperature control. All have been shedding over the past few weeks.

If you haven’t yet read my description of the shedding process near the end of my last post, do so now; the following discussion will make much more sense with that background.

Because the corneal layer of the skin does not grow, shedding (or ecdysis) is a recurring process throughout a scaled reptile’s life. Like other animals, baby snakes grow rapidly, so they must replace the corneal layer frequently to accommodate rapidly expanding bodies. Since shedding frequency is highly correlated with growth rate, juveniles usually shed several times per year. Growth rate and shedding frequency slows with size and age, with large adult rattlesnakes sometimes shedding less than once per year.

Rattle growth is a fundamental part of the shedding process for rattlesnakes. The rattle is made of keratin, the same stuff as the acellular matrix of the corneal skin layer – and your fingernails. Each time the snake generates a new corneal layer and prepares to shed the old one, it also produces a new rattle segment. Thus the newest segment is always at the base of the tail and contains live tissue – much like the base of your fingernail. And because each new segment is the width of the tail, young rapidly-growing rattlesnakes produce a tapered rattle (photo below).

Male northern Pacific rattlesnake, Crotalus oreganus (CROR46), 09 March 2015 Original RAW IMG_5583.CR2
Our Male 46 on 09 March 2015, just before his rattle was marked with paint. All segments except the newest are hollow and dry.

The rattle is made up of loose, hollow, interlocking segments. Except for the first segment (or “birth button”), each segment consists of three lobes, yet only one is visible. The two hidden lobes fit loosely inside the older adjacent segments (photo, below). There is nothing loose inside that makes noise, the rattlesnake’s buzz comes from the loose segments vibrating together.

A single rattle segment from a mature rattlesnake, showing the three-lobed structure (left). On the right is a back-lit rattle from an old rattlesnake (note the lack of taper) showing how the segments interconnect. Older segments are at the top of the photo.
A single rattle segment from a mature rattlesnake, showing the three-lobed structure (left). On the right is a back-lit rattle from an old rattlesnake (note the lack of taper) showing how the segments interconnect. Older segments are at the top of the photo.

 

Rattlesnakes are born with a tiny hard cap on the end of the tail. I like to use the analogy of an eraser on a pencil – which is the approximate size of the newborn snake and the cap.  During the first ten days or so, the first rattle segment or “birth button” is produced, which is uncovered by the postpartum shed. This is the only time that a part of the rattle comes off with the shed “skin.”

Rattle cap of a neonatal Southern Pacific Rattlesnake (Crotalus oreganus helleri), about a minute old and still in its amniotic sac.
Rattle cap of a neonatal Southern Pacific Rattlesnake (Crotalus oreganus helleri), about a minute old and still in its amniotic sac.
Rattle of a one-week-old Southwestern Speckled Rattlesnake (Crotalus mitchelli pyrrhus) showing the newly-formed birth button inside the rattle cap, which will be lost with the post-partum shed in a few days.
Rattle of a one-week-old Southwestern Speckled Rattlesnake (Crotalus mitchelli pyrrhus) showing the newly-formed birth button inside the rattle cap, which will be lost with the postpartum shed in a few days.
"Skins" from post-partum sheds showing the neonatal rattle caps. The one on the right is in its natural condition (inside-out); the one on the left has been manually everted to expose the cap.
“Skins” from postpartum sheds showing the neonatal rattle caps. The one on the right is in its natural condition (inside-out, with the cap hidden inside); the one on the left has been manually everted to expose the cap.
Birth button of two-week-old Northern Pacific Rattlesnake after post-partum shed. This is the first rattle segment and will stay with this animal until it gets too dry and brittle, which will allow it to break off while being dragged through the brush in a few years.
Birth button of a two-week-old Northern Pacific Rattlesnake after its postpartum shed. This is the first rattle segment and will stay with this animal until it gets dry and brittle, which will allow it to break off while being dragged through the brush in a few years.

During every subsequent shed, the old corneal layer will simply be an open tube that slips over the rattle. When a shedding cycle begins, formation of the new rattle segment is usually noticeable before the eyes turn blue (photo, below).

On 24 June, the tail of Female 54 showed early tell-tale evidence of a shedding cycle beginning. The black segment is the live one but notice how the scales next to it look almost transparent and the tissue beneath is much lighter... that is a new segment beginning to form.
On 24 June, the tail of Female 54 showed early tell-tale evidence of a shedding cycle beginning. The black segment is the live one but notice how the scales next to it look almost transparent and the tissue beneath is much lighter… that is a new segment beginning to form.
A week or so further along in the shedding cycle than Female 54 (above), the tail and rattle of Male 46 last May illustrate the progression of growth of a new segment in the end of the tail. During the process,  live tissue receeds from the last new segment (next to the paint),  leaving it hollow and dry after the old corneal layer is shed.
A week or so further along in the shedding cycle than Female 54 (above), the tail and rattle of Male 46 last May illustrate the progression of growth of a new segment in the end of the tail. During the process, live tissue recedes from the last new segment (next to the paint), leaving it hollow and dry after the old corneal layer is shed.

Injecting acrylic paint into the first hollow segment allows me to identify rattlesnakes visually, with each animal receiving a unique color combination. The paint also allows me to record how often they shed.

This is the rattle of my Female 05 from El Dorado Hills in October 2013. The paint in the middle of the rattle is from her initial capture in June 2010. I marked her rattle with new paint in 2013 (next to the black live segment) because the older segments will eventually dry, crack, and break away, taking the original paint with them.
This is the rattle of my Female 05 from El Dorado Hills in October 2013. The paint in the middle of the rattle is from her initial capture in June 2010. I marked her rattle with new paint in 2013 (next to the black live segment) because the older segments will eventually dry, crack, and break away, taking the original paint with them.

In Female 05 (above), note that her birth button and the next two or three segments are already missing. The location of her original paint tells us that she has shed four times in the 40 months since she was first marked. The slight taper at the end of her rattle provides a hint of her age: considering the number of segments I think are missing and that snakes grow much faster and shed more frequently when young, I estimate that I originally captured her in her third or fourth year, making her about seven years old in this photo. Once all of the tapered segments at the end are lost, we have no way of estimating how old she is from the rattle.

You can also see that the rattle segments produced by Fem 05 (photo, above) as a young rattlesnake are noticeably larger than the more recent thin segments. This happens in the middle of rattles, too, with some segments being wide and robust while others are thin. I think rattle segments are a bit like tree rings in that good conditions with lots of  food produce wider thicker segments. In the case of adult females like 05 above, it likely reflects the shift in resource allocation (more below) when she became sexually mature. It is worth mentioning that this snake had reproduced three years in a row when this photo was made (and she produced the four recent thin rattle segments) and her body condition was very poor after three consecutive litters.

In almost all rattlesnake species, adult males are larger than adult females. Yet the growth rate of baby males and females is indistinguishable until they reach sexual maturity. Once they start reproducing, however, female growth slows. We believe this happens because females start diverting most nutritional resources to the production of offspring, leaving much less available for their own growth. Males, on the other hand, are free to continue devoting their resources to increased body size – which is advantageous for fending off predators while searching for females and for battling other males for access to receptive females (click here for video of males fighting).

Finally, can we tell a snake’s age from the rattle? The one sure thing is that each rattle segment does not represent one year. The addition of rattle segments is well correlated with growth rate which, in turn, depends on age and food intake. We can make a pretty good estimate of age from a complete unbroken rattle and even when a few segments are missing, so long as some significant taper remains at the end. But for older snakes with broken rattles having no taper, there is just no way to know how many segments are missing.

So how long can rattlesnakes live? Decades! I have personally kept some southern California species in captivity over twenty years. The Splash Education Center at Mather Field has a healthy Northern Pacific Rattlesnake that has been in captivity for a well-documented 32 years! But how long they survive in the wild is a much different question. Captive snakes do not have to contend with coyotes, hawks, owls, king snakes, temperature extremes, and all the other hazards of a natural existence – not to mention humans and their cars. While references like Robert Stebbins’ Field Guide to Western Reptiles and Amphibians (2003; Houghton Mifflin Co.) list the maximum size of our northern California species as over five feet, the fact is that three-footers are now uncommon. Large rattlesnakes have become very rare all over the United States, with individuals approaching old record lengths almost never found. Of course, in some remote wilderness where people rarely visit (if there is such a place today!), maybe there are still a few very large wild rattlesnakes…

 

 

Pregnant females, injuries, and shedding

First a quick general update: Spring courtship seems to be over; I have not seen a courting pair since 16 May. Since the end of May, the pregnant females have taken up refuge in ideal shelters where they can thermoregulate optimally. Females 39 and 41 are now in the same shelters where they gave birth last year (but not together) and Female 47 is with 39. Female 54 is by herself and has not moved since we implanted a transmitter and released her on 23 May. Neither 47 nor 54 were telemetered last year so I have no history for them. These soon-to-be mothers are all maintaining body temperatures within a couple of degrees of 30C (86F). The males and Female 53 (not pregnant?) have been hunting, mostly hanging around California ground squirrel burrows for the past month as the squirrels produce the first pups of the season (more on hunting ground squirrels) and the body temperatures of these foraging snakes has varied widely compared to the pregnant females (more on body temps).

In my last post, I showed you a photo of an unidentified rattlesnake in the refuge with Female 41 – the same refuge where Females 41 and 43 had babies last year. (You may remember that Female 43 was found dead at the refuge last October; click here for that account) While I could only see the new snake’s nose and a small area of flank at the first encounter, I saw her twice more over the next eight days. She was shades of dark brown, while Female 41 is quite pretty with chocolate brown dorsal blotches on a gray background. During the subsequent two sightings, I could also see the new animal’s rattle, which was long and unbroken (i.e., she still had her birth button). Then a week ago, I found Female 41 and the new rattlesnake basking next to each other and was able to capture the new animal (CROR55).

The first thing I noticed was that she was pre-shed. That is, her eyes and new rattle segment were milky white (more about shedding below). The next important discovery was that she is, indeed, a female – and quite heavy…maybe pregnant. A photo of her snout (bottom photo, below), when compared to the nose in the photos of the unidentified rattlesnake on 3 June (top photo, below) confirms that she is the same animal.

unidentified Crotalus oreganus under log at Refuge 03 on 03 June 2015, Effie Yeaw Nature Center Origonal RAW IMG_7382.CR2

I have numbered some landmark scales in these photos that you can compare but also compare the size and arrangement of surrounding unnumbered scales. And while the fine pigmentation of the individual scales is obscured in the pre-shed photo, I have circled some larger pigmented areas that are visible. Keep in mind that the photos were taken from slightly different angles, making some scales that are visible in one hard or impossible to see in the other. The size, number, and arrangement of nose and crown scales on these rattlesnakes are a bit like fingerprints on primates: they are individually unique, so far as we know. Also note the whitish eyes and how the scales on her nose appear a bit swollen in the pre-shed photo.

As I examined her further, I made another interesting discovery: she has sustained a serious injury to her abdomen sometime in the past. Although well healed now, her skin is scarred on the dorsal midline 575 mm (23 in) from her nose (her body length, excluding tail [snout-vent length or SVL] is 720 mm [28 in]). Furthermore, her body is noticeably narrowed at the scar (photo below) and her abdomen is hard and dense to the touch for several inches on both sides of the scar.

Female CROR 55 Original RAW IMG_7555.CR2

Nonetheless, she looks and acts healthy and might, indeed, be pregnant. I could feel two masses in her anterior abdomen that were consistent with fetuses but could not differentiate anything posteriorly where her abdomen is apparently scarred internally. She would normally be a great transmitter candidate but I elected to release her without one because of the suspected internal scarring where the transmitter would be implanted, plus I did not want to damage her skin as she prepares to shed.

This brings up the point that life is not easy for these snakes. In addition to this healed injury to Female 55 and the death of Female 43 last year, you may remember that I processed and released a small male (CROR44) early last December that had recently sustained some significant trauma from a predator, including a deep penetrating abdominal wound that I suspected would prove fatal over the winter (more details). While processing Male 52 early last month, I removed a “foxtail” (a seed from one of the non-native Bromus grasses that blanket the preserve) from his cloaca (cloaca defined). This little floral harpoon had not yet caused much damage but I don’t know what would have prevented it from burrowing into his abdomen and causing a potentially fatal injury. My point is that these rattlesnakes, despite their formidable reputation, are susceptible to constant hazards.

Shedding (the technical term is ecdysis) is the sloughing or molting of the outer epidermal layer (the stratum corneum) in scaled reptiles. This corneal layer is a matrix of keratin (the same material as your hair and fingernails – and the rattlesnake’s rattle!) infused with lipid (fat) molecules that greatly slows the passage of water through the skin. Because this matrix is acellular (contains no cells), it cannot grow. Thus, as the snake grows, this layer must be replaced periodically. When the time comes, the snake’s body produces a new corneal layer under the old one. This creates the blue or whitish tint, most notable in the eyes. In rattlesnakes, a new segment is produced at the base of the rattle during each shed, which is also whitish at this stage. Once the new corneal layer is ready, the snake’s body secretes fluid between the old and new layers, separating them and softening the old one. When this fluid is secreted, the whitish color disappears (the eyes clear) and the snake is ready to shed. They then rub their face on any available surface and start to peel back the old layer from around the nose and mouth (photo below). They continue rubbing, eventually crawling out of the old “skin,” leaving it inside-out, usually in one piece.

A 10-day-old Northern Pacific Rattlesnake beginning his post-partum shed while being processed during my El Dorado Hills field study.
A 10-day-old Northern Pacific Rattlesnake beginning her post-partum shed while being processed during my El Dorado Hills field study. (Also note the “birth button” at the end of her tail)

I’ll leave it there until next time, when I’ll explain rattle growth and trying to estimate age from the rattle.

Mike

Copulation & a malformed rattle

Just a quick entry regarding two very interesting recent observations:

First, just in case you were wondering what rattlesnakes do when they first warm up after a long winter’s nap… I came across this copulating pair early this afternoon. What you see in the photo (below) is almost all I could see. Most of their bodies were hidden in the deep grass. The elevated tail is the female’s and the male’s tail is wrapped under her cloaca. You’ll notice that neither rattle contains any paint; they were (and remain) unmarked snakes. I didn’t disturb them!Copulation 18Mar15

Also, the most recent animal to be processed and released at EYNC was a small (554 mm/22 inch) female with a deformed rattle (below). These are pretty rare. It looks like a congenital deformity rather than being the result of trauma. One additional segment clings to the terminal one and the snake can make a little buzz but I am sure she is incapable of accumulating a string of segments. The lesson here is that even in the rare event of a deformity or amputation, no rattlesnake has a long tapered tail like California’s harmless snakes.Rattle_CROR50 18Mar15