reproduction – Page 2 – EYNC Rattlesnake Study

Missing males and waiting for kids

As birthing season approaches, I have been watching intently for signs of baby rattlesnakes. While postpartum mothers usually stay inside their shelters, the neonates are typically active and easily spotted. Although they do not leave their shelters before shedding the first time, babies can usually be seen crawling or basking at the entrance. And when we introduce the BurrowCam into the shelter, the kids can be seen exploring their new surroundings and crawling around on their mother. So far, there’s been no evidence of babies yet this year. This would be a bit early but quick warming last spring has me wondering about the potential for early births this year.

Remember that pregnant female rattlesnakes in our area hangout in carefully selected thermal shelters where they can maintain consistently warm body temperatures around the clock until they give birth. This period of thermoregulation lasts several months, during which the pregnant moms do not forage for food.

All five of our telemetered females are apparently pregnant, plus Female 55, who was processed and released without a transmitter in June (no transmitter surgery due to some old but significant trauma to her abdomen; click here for details). These females settled into their gestation shelters between 8 June and 1 July and have maintained body temperatures between 28ºC and 32ºC (82º–90ºF), almost without exception, ever since.

In fact, at dawn on a recent cool morning (16 August) when the ground temperature just before sunrise was in the mid-50s F, these girls still had body temps in the high 80s F. They maintain similar body temps during hot afternoons when the ground temperature (much hotter in the sun than air temp) outside is 120ºF and more. They thermoregulate like this by selecting logs or large rocks that have just the right thickness and sun exposure to stay warm at night but not get too hot in the afternoon sun. Such places are apparently scarce because three of our telemetered females are together in one shelter, while Female 41 is with non-telemetered Female 55 in another. Female 54 is in a third location, possibly by herself, but there could be others in there without radios. Females 39 and 41, both of whom produced broods in 2014, are in the same shelters as last year.

Flash photo of Female 41, tucked into her gestation refuge at sunrise on 16 August 2015. Note in the inset how her scales are pulled apart by her developing brood. Female 55 is also in this shelter but not visible on this morning.

On 27 August, the BurrowCam revealed Female 39’s abdomen to be greatly distended, extending all the way to the cloaca. So maybe delivery of her 2015 brood is not far off? The frame grab (below) from the BurrowCam video shows her abdominal scales pulled far apart. In the 50-second video (watch here), you’ll see what I see when we thread the BurrowCam into a passage. Female 39 is identified by red/blue (red-over-blue) paint in her rattle and the edge of another dark gray rattlesnake appears to be visible under 39’s coils. Known to be behind her in the passage (because of their radio signals) are Females 47 and 53, as well as Male 46. Additionally, in recent days, I have seen non-telemetered (and non-pregnant) Female 48 (green/green) and Male 36 (red/red; carrying a failed transmitter) in this log. It’s a popular place this time of year!

Frame grab from a 27 August BurrowCam video of the distended abdomen of telemetered Female 39, deep in her gestation refuge. — Frame grab from a 27 August BurrowCam video showing the distended abdomen of telemetered Female 39, deep in her gestation refuge.

As you may recall, Males 36 and 37 have been missing for months since their transmitters failed prematurely in September and December, respectively. Until last week, Male 36 had been last seen on the BurrowCam in a hollow log courting postpartum Female 41 on 2 October 2014, and I last saw Male 37 as his tail disappeared down a hole on 7 March 2015. There had been no sign of either of them since until a fellow photographer and herpetologist I encounter frequently at Effie Yeaw showed me a photo of Male 37 (IDed by his yellow/red rattle marking) crossing a trail on 20 August! Then, just 5 days later, while checking for babies in the shelter with Females 39, 47 and 54, and Male 46, I was surprised to see Male 36’s red/red rattle. (See photos below) So both are alive and well… but both still elude recapture.

Male36 (red/red paint in rattle) deep inside a hollow log with Female 41 on 02 October 2014.

Male 36 inside another hollow log on 25 August 2015 with at least three pregnant females and a smaller male. Compared to the 2 October photo (above), note that he has two additional rattle segments between the paint and the live black segment, indicating he has shed twice in the past ten months.

Earlier today, 29 August, I found Male 46 coiled in poison oak dozens of meters away from the log where he has been hanging out with the three pregnant girls continuously for the past two weeks. It is likely he has been chased off by a larger male, so maybe Male 36 is still in there. This refuge has a narrow deep passage that is nearly impossible to thread the BurrowCam into and, even when successful, I can usually only see whichever rattlesnake is closest to the top (for example, the 50-second video of Female 39, with the link earlier in this post).

So Baby Watch continues and I still hope to recapture missing Males 36 and 37.

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.

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.

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

The effect of drought on rattlesnakes

Field studies of rattlesnakes indicate that they cease most movement when water stressed and remain in their established home ranges, rather than migrating into developed areas in search of water, despite frequent claims to the contrary.

In my last post, I mentioned witnessing Females 41 and 47 feeding, as well as finding new Female 53, who was very heavy and likely pregnant. Since then, I have come across Female 41 eating another vole, found another new female (#54) that is heavy and definitely pregnant, and come across a fat but unidentified rattlesnake in the refuge where Females 41 and 43 had babies last year. I could only see the face and a bit of a flank of the unidentified animal (photo below) so I couldn’t even determine sex.

It could be a male that has just eaten a ground squirrel pup – but it is more likely another pregnant female. We now have five telemetered females (39, 41, 47, 53 and 54) and all are in great shape, with three either confirmed or likely pregnant and the others in good shape to reproduce although I have not yet had my hands on them this year to palpate for fetuses.

This brings up a timely point: This will obviously be a good year for rattlesnake reproduction in our area, despite being in the midst of an historic drought. Since the news media often quotes “experts” claiming drought “drives rattlesnakes out of the hills and into yards looking for water,” this is a great opportunity to set the record straight about how drought affects rattlesnake movement.

We live in a Mediterranean climate, historically characterized by warm dry summers and cool wet winters. Even during years with “normal” precipitation, vast tracks of mountains, foothills and many valley areas have no surface water between late spring and the return of winter rains in November or December – yet they support healthy populations of rattlesnakes. Herbivores (insects, rodents, etc.) get most of their water from the plants they eat and rattlesnakes get water from eating the herbivores. The bodies of terrestrial vertebrates are usually composed of 65–75% water, so eating a 100 gram (3.5 ounce) rodent is like drinking about 70 grams (2.5 ounces) of water for a rattlesnake (plus the nutrients and energy gained). Make no mistake, rattlesnakes suck droplets from various surfaces, including their own skin, deposited by rain and dew (photo, below) and they will certainly drink from standing water when it’s available. But especially during summer and fall, these other sources are not available and virtually all of the water a rattlesnake needs is obtained from its prey.

adult Crotalus s. scutulatus (Mohave Rattlesnake) drinking rain water near Apple Valley, San Bernardino County, California, USA [wild animal, in situ] — Mohave Rattlesnake drinking rain water from its own body. [Cardwell, M. D. 2006. Rain-harvesting in a wild population of *Crotalus s. scutulatus* (Serpentes: Viperidae). *Herpetological Review* 37:142-144.]

Rattlesnakes are models of low energy physiology. As ambush predators, they move comparatively little and rely largely on anaerobic metabolism. Their sedentary lifestyle combined with the corneal layer of their skin (full of water-blocking lipids) dramatically lowers the amount of water that passes into and out of their bodies – known as “water flux.” Nonetheless, multiple studies have shown that the most significant mechanism for water loss in terrestrial snakes is evaporation, with about 75% being lost through the skin and the remainder via exhaled breath.

During my four-year field study (2001–2004) of Mohave Rattlesnakes in southern California, I was able to compare behavior, including average daily movement and reproductive effort, between the severe drought year 2002 and 2003–2004, when rainfall returned to average or above average. I found that average daily movement during 2002 was less than one third of 2003–2004 averages. And while I encountered dozens of courting pairs during the two non-drought years, I observed a male courting a female on only one occasion in 2002. Yet these rattlesnakes continued to eat at a rate indistinguishable from the non-drought years, based on scats deposited in holding containers and later analyzed. These snakes were reducing exposed surface area (and, therefore, evaporative water loss) by remaining coiled and immobile, covering much of their skin within their coils. They even buried their coils partially in loose soil at times, covering additional skin area. Remaining stationary eliminated their ability to find and court mates but, as sit-and-wait ambush predators, it allowed them to continue to hunt – and obtain the body water of their herbivorous prey. They also positioned themselves behind vegetation and ground contours in 2002 to avoid wind and sun, both of which increase evaporation rates. You can find more details in my MS thesis.

We have seen similar behavior in Northern Pacific Rattlesnakes in recent years at my El Dorado Hills study site, where the rattlesnakes remained tightly coiled and stationary in deep chaparral on north-facing slopes during particularly hot dry summer weather. At Effie Yeaw, all of the rattlesnakes caught by staff around the ponds during the past year, as well as the telemetered rattlesnakes I have found there, have been males found during the courtship season. The females have remained in the woods, away from water sources. While the snakes will drink when they find the ponds (or other water sources), that’s not why the males are there… they’re wandering around looking for females! And, yet, the females are now fat and pregnant.

Drought probably does not affect rattlesnake movement until it becomes locally severe, as it did at my Mohave Rattlesnake study site in 2002. When the snakes start to become water stressed, they don’t set out into uncharted territory looking for surface water. Rather, they stop moving and hunker down where they can best reduce evaporative water loss while still striking any prey that wanders by. Currently, if the preserve at Effie Yeaw Nature Center is any indication, there is lots of annual plant growth and the vole and ground squirrel populations are thriving – and so are the rattlesnakes.

So when people find a rattlesnake in their yard during a drought, the most likely explanation is that it is a male looking for receptive females and the drought is not severe enough locally to stress the rattlesnakes. When they are truly water stressed, rattlesnakes move less – not more – than usual. Unlike most large mammals that have much higher metabolic and water flux rates and require standing water to drink, there is no evidence that rattlesnakes leave their established home ranges looking for water, despite the popular belief to the contrary. They do just the opposite.

More feeding, courting, and a new female

The first thing I encountered early in the afternoon of 13 May was a dead adult rattlesnake in the grass behind the Visitor Center. The carcass had completely putrefied and had been eviscerated by insects. It was an average-sized adult and had no paint in its rattle (i.e., it was not one of our study animals). I could not determine the sex. The head and rattle were intact, indicating it was unlikely a human had killed it. There was no obvious evidence of trauma elsewhere, either, but it was in such bad shape that it was difficult to tell. People often ask about the life expectancy of rattlesnakes and the answer is that, in captivity, they have been known to live more than 30 years. But in the wild, if they make it to adulthood (which few do), they are constantly threatened by raptors, coyotes, kingsnakes, people and their cars, temperature extremes, and other hazards. My guess is that few make it to ten years.

About 3 PM on the same day (13 May), I found the radio signal from Female 41 coming from dry grass on the hillside near the stairs on the trail behind the amphitheater. When I refined her location and parted the grass, I found her swallowing a small rodent – which she immediately spit out (this is common defensive behavior, as rattlesnakes are defenseless when swallowing prey). I had to remain completely still for five minutes or more before she decided it was safe to eat again. Because she was so deep in the grass and I had only a small opening through which to view her (photo below), I could not tell exactly what kind of mammal she was eating. It was uniformly gray with very fine fur, a gray belly, and was about mouse-sized. It was too large for a shrew and the lack of a light-colored belly ruled out most native mice. The dorsal fur looked too fine for a vole and I could not see the tail. What I could see looked like a house mouse, Mus musculus, but we will never know for sure as I did not want to bother her further and be the cause of her abandoning her kill.

When I next visited her two days later, she had moved only a few feet and was coiled next to a California Ground Squirrel burrow, which she retreated into when I arrived. This was the first time this season I have found a rattlesnake close to or in a ground squirrel burrow. I haven’t seen ground squirrel pups yet but I saw a pregnant female on 11 May, so I suspect there are pups in burrows by now and the rattlesnakes hunt the pups heavily in spring and early summer. (Click here and scroll to the bottom of the first page for more info on the fascinating interaction between Northern Pacific Rattlesnakes and California Ground Squirrels)

With all of our telemetered rattlesnakes alone and apparently hunting (and not having found a courting pair since 20 April), I was beginning to wonder if courtship might have concluded early this spring. But on 16 May, I found Male 38 on top of an unmarked female next to the large log in the meadow. She was heavy, healthy, and had no paint in her rattle – a beautiful rattlesnake, but she was also quick! As so often happens, the courting male was far less afraid of me (too much testosterone?!?!) than the female, who fled immediately and made it under the log before I could capture her.

I wish that people who fear rattlesnakes and think they are so malevolent could see how these animals really react to being approached by a person. If I had been able to catch all the unmarked rattlesnakes that have escaped from me this spring, our quota of seven males and seven females with transmitters would be full… but they are shy and very quick to flee into the grass, wanting nothing to do with something as big as a person. Remember, in their tiny primitive brains, rattlesnakes react to encounters based on three criteria: Can it eat me? Can I eat it? Can I mate with it? Clearly, we fall into the first category!

On 19 May, I found Female 47 in the meadow a little after 10 AM, crawling slowly through the grass, carefully tongue-flicking as she moved. I took a few photos and she crawled out of sight while I recorded my standard data. But when I started to depart, I came across her a couple of meters away with an alligator lizard, Elgaria multicarinata, in her mouth. She retreated a short distance to a small shrub with the lizard still in her mouth and, after I stood motionless once again for several minutes, she began to swallowed it (photo below).

Two days later, while searching for Male 35 on 21 May, his signal led me to a large and very dense thicket of armpit-high Milk Thistle (Silybum marianum) in the meadow. I have avoided penetrating this thicket when various males have occasionally visited it this spring because the spines go right through all clothing and there is just no way to avoid them. But on this cool morning, when I peered over the thistle into a little clearing in the thicket, I saw a nice unmarked rattlesnake laying in the grass, probably hoping the clouds would clear and allow some sun to shine through (photo below).

Hoping that she was a “she” and probably the reason that Male 35 was also in the thicket, I carefully retreated without spooking her and dropped all my gear in the grass except a cloth bag and snake hook. Stepping into the sea of spines, I slipped the snake hook under her and began to gently lift her before she reacted. I almost got her clear of the thistles before she wriggled off the hook but I was able to quickly catch her again before she completed her escape. Once clear of the thistles and in the dry yellow grass, she could no longer hide and I had her in the bag shortly thereafter.

Her sex was later confirmed and she became CROR53. (Click here for an explanation of CROR). She was very heavy for her length and full of shiny white abdominal fat when I implanted the transmitter. I could not be sure of her reproductive condition because of so much material in her bowel; she clearly had been feeding very successfully. Reproductive condition is determined by palpating her belly through her belly scales, feeling for yolk masses and, later in the season, for embryos. Because the transmitter incision is less than 3/4 of an inch long and made on the side, two scale rows up from the end of the belly scutes, it doesn’t help in determining reproductive condition. When she was released the morning after her surgery, she became our fourth telemetered female, along with four telemetered males (plus two additional males with failed transmitters I am still hoping to recapture). I am up to 413 recorded encounters with EYNC rattlesnakes this year… we are off to a great start!

Soon to come: an explanation of shedding and rattle growth.

Early home ranges and other news

Good news: On 25 April, I came across our Female 39, who’s transmitter had failed prematurely 19 days before. She was captured, her transmitter was surgically replaced, and she was released the next day. At her initial capture last July, she weighed 365 grams (12.9 oz) and she produced a litter of kids a couple of months later. When recaptured last weekend, she weighed 404 grams! She clearly has been hunting successfully and is in great shape to reproduce again this year. While tropical pit vipers often reproduce annually, pit vipers in temperate climates like ours often require a year or two to replenish body fat before they can sustain another pregnancy.

But annual births are not unheard of this far north. In fact, we had a female rattlesnake produce litters three years in a row in El Dorado County a few years ago. After her third litter, however, she was skin and bones and we didn’t think she would survive the winter. But she did and might have pulled through if she had not been nailed by a raptor the following spring.

One day we found her radio signal to be weak and coming from far down a canyon, well outside her typical home range. Because thick manzanita and chamise made getting to her signal very difficult, I didn’t investigate right away. Eventually, when her signal didn’t change, we burrowed through the chaparral until we got to a large live oak that stood by itself on a hillside. The snake’s transmitter was laying in the leaves under the tree, completely clean and undamaged – as if it had been surgically removed and washed! I have had telemetered rattlesnakes eaten by coyotes before but coyotes chew the transmitters. The undamaged transmitter under a lone large tree far from the snake’s last location just screamed raptor. The area was full of red-tailed hawks and there were certainly owls at night.

Back to our current study, just two males, 36 and 37, remain loose with failed transmitters. I recently shipped the other five faulty transmitters back to the manufacturer for evaluation and repair.

Last week I found one of the hollow logs frequently used by our telemetered rattlesnakes freshly ripped apart (photo below).

I’m not sure what kind of animal, besides a person or a black bear, might have ripped a log apart like that. While it is certainly not impossible for a bear to stray this far downstream, it would also be attracting attention in more obvious ways. Having encountered a visitor with a snake hook off-trail a few weeks ago, I thought this might be a good time to reiterate why I am no longer publishing plots of the study animals’ travels (as I did last year) or providing more details about where they are hanging out. Too many rattlesnake researchers have had study animals captured or killed after they disclosed their locations.

But I do want to share how far the telemetered rattlesnakes have been roaming during the first six weeks of the season. The illustration below shows the home ranges used by the seven rattlesnakes with working transmitters so far this year. The solid lines are the males and dashed lines are the females. The Effie Yeaw visitor center is in the top center and the EYNC parking lot is in the top left corner of the Google Earth photo.

The most interesting finding to me is that Females 41 and 47 have been moving as much as any of the males and much farther than some. Also remember that we lost almost three weeks’ movement on Female 39 when her transmitter failed. Male 35 had a small home range last year, primarily because he hung around in the elderberry and redbud thicket next to the bike rack for so much of the summer. He spent most of the rest of his time in the meadow – and that’s where he is again. Male 40 was the last to leave his winter shelter this spring, has not moved as frequently as the other males, and I have not found him courting any females. He has always been quite under weight for his length. He is an old guy, based on his untapered rattle and an impressive collection of scars, but he seems to be getting by.

Courtship seems to have slowed a bit in the past week, with most animals by themselves and apparently hunting, at least when I have visited. Nonetheless, there should be another month or so of courtship before the summer hiatus.