Tuesday, January 14, 2014

Capitalism: A Rattlesnake Love Story

Griffin Capehart

It has long been accepted that heavy-bodied snakes like rattlesnakes and other pitvipers are what scientists call capital breeders. This means that they keep some energy in savings for things like reproduction (Jonsson 1997), much like us humans put money into savings for things like new cars, houses or less important items like our kids' college fund. Just like humans, snakes will budget their energy depending on the "economic" climate and some will not even place energy into yolk production unless they have enough savings (Lourdais & Bonnet 2002; Nalleau & Bonnet 1996). There are several possible factors that may affect how a female budgets her energy such as temperature, rainfall, stress, prey availability and even whether or not she reproduced the previous year. Most of these factors are intertwined, making it extremely difficult to tease apart the ultimate determinant of whether a female decides to roll the dice and attempt to put out in a given year. Males don't really have the same issue. They put most of their energy into things like muscle so that when they encounter another male, they can lay the smack-down on him (Bonnet et. al 1998). 

First of all, let's talk a little bit about rattlesnake reproduction as far as females are concerned. Female rattlesnakes have several stages for breeding preparation. Primary vitellogenesis (or production of yolk) is the first in which microscopic follicles increase in size to about 4-6 mm. Most females have these follicles present year-round. Secondary vitellogenesis occurs after primary (certain conditions being met, i.e. capital) and consists of increase in water content and addition of nutrients (Aldridge 1979). Then fertilization occurs and yolk production continues until a size-threshold is met (depending on species). The fertilized eggs are then ovulated where they will develop into fully-functioning miniature versions of their parents and will be born LIVE! This means that rattlesnakes DO NOT lay hard-shelled eggs. The young exit mama's cloaca in an amniotic sac and burst out into the world ready to be badasses. This is called viviparity. Very little post-partum care is given by the mother. The neonates may stay close to mom for a couple days but then they move out faster than a rebellious teenager. 

Mom's face says it all.
Breaking the Dogma

Sperm production is cheap, baby production not so much. Personally, I have always been befuddled about the idea that females don't feed during their pregnancy. This is the most energy-consuming process they will face in their lives and they make no attempts to maintain a healthy reserve to ensure the survival of their young? It just doesn't add up. The only theory that makes a bit of sense is the Space-constraint theory. The burden of fetuses PLUS food makes it difficult for the snakes to move (reviewed in Schuett et. al 2013), but females don't really move that much anyway so why would that matter? Until recently, that has been the consensus. Two papers recently busted the capital breeding theory by providing evidence for female foraging during pregnancy (Schuett et. al 2013; Webber et. al 2012).  Schuett et. al (2013) described Western Diamondback Rattlesnake (Crotalus atrox) females consuming prey during late pregnancy! This is almost unheard of in large-bodied vipers. Webber et. al (2012) found that Sidewinders (Crotalus cerastes) also fed during pregnancy. This is not as surprising being that Sidewinders are smaller and thus might lean toward a more income-based reproductive style. Going back to the D-backs, we see a total one-eighty in our former understanding of breeding strategies in rattlesnakes. What is going on with these snakes that causes them to continue feeding during pregnancy? Or maybe a better question, why were scientists so firm in believing that heavy-bodied vipers were capital breeders?
Pregnancy is not this glorious. Let's be real.

A possible answer to this question is the broad application of one researcher's findings because of his popularity and credibility (I don't want to point any fingers here, but if you look in the right places his papers will SHINE). In a quick literature search for capital breeding on Google Scholar, 7 of the 10 results on the first page are written by said herpetologist or a fellow scientist whom with he commonly co-authors papers. Bonnet et. al (1998) cite 3 papers and 1 book that claim rattlesnakes are capital breeders. Of the two papers I could access online, neither of them mentioned capital breeding and did not examine whether females were feeding during pregnancy or not (Brown 1991; Diller & Wallace 1984). They simply hand-wave ideas based on old postulates. An older study did provide real evidence for capital breeding in snakes and a more recent study on garter snakes (another viviparous species)also provided evidence for capital breeding (Gregory 1999; Keenlyne 1972). So why so much conflicting evidence!?!?!?

I'm so confused right now. http://gifsoup.com/view/2419676/confused.html

What's Going on

Nothing in science is black and white, and the question of income or capital breeding in rattlesnakes is no exception. There are a few things that immediately come to mind that could help explain the inconsistencies in the literature. 
1. Capital breeding does not mean the snake WILL NOT eat during pregnancy
Pitvipers are opportunistic, sit-and-wait, ambush foragers. This means that they sit-and-wait to ambush their prey (why can't everything in science be that easy). They do not constrict but rather rely on their toxic cocktail of venom to subdue their prey at which point the snake will use it's super-sense of smell to locate its prey for consumption. The process of venom production is expensive, as is baby-making. To me, it makes a whole lot of sense that if a gravid female rattlesnake were to have a nice and tasty mouse stumble right in front of her, that the mouse would be toast. Why not add a little bit of wood to the fire if you have space for it? Schuett et. al (2013) found that pregnant female rattlers fed MORE frequently during LATE pregnancy! Yes, this is only one study and there is potential for many confounding variables, but if there ever was a time and a place for a red flag, this is it. 
2. Allostatic Load
A relatively recent concept in biology is that of allostasis. This concept is defined basically as the processes involved with achieving homeostasis. An allostatic load is the sum of energy demands. Female rattlesnakes have basically two energy demands when pregnant: 1) Stay alive (maintain basal bodily functions) and 2) make babies. The little movement they may do is to find a better basking spot. Other than that, their allostatic load is pretty straightforward. Romero et. al (2009) describe a new model for predicting how an animal will react with regard to allostatic adjustments called the Reactive Scope Model. It mentions four ranges in which an animal may be at any given time period. The first is predictive homeostasis which includes basic life functions that are "predictable." The second is reactive homeostasis which accounts for unpredictable and potentially threatening changes in the environment. Third is homeostatic overload where an animal has exceeded its physiological capacity to react and begins using reserves. Finally, there is homeostatic failure where an animal can no longer support functions in the predictive homeostasis range. Pregnancy for a rattlesnake should fall into the predictive category. A female rattlesnake should never be surprised that they are pregnant. This isn't high school drama, this is real life. These things are planned. Evolutionarily it makes sense that a female would plan for the worst if the opportunity presents itself in the form of a meal IF consumption of that meal outweighs any potential costs of letting it continue it's pathetic existence. The snakes in Schuett's study seemed to think so. Was this just a special case or is something really friggin' cool going on here?
3. Fewer, but stronger babies
Maybe these snakes are not able to store enough capital in order to produce large clutches and smaller litters are better off. This allows females to continue to feed during pregnancy (Schuett et. al 2013). Sure, lots of baby snakes seems like a good idea, but divvying up resources to all those follicles evenly is most likely a daunting task. Some babies may get more yolk than they need and others get the shaft (what the layperson refers to as a "runt"). But, if mom produces only a few MASSIVE follicles, those babes will come out larger and potentially more fit to survive to a sexually mature life stage. So what's better - more weaklings or a few super-babies? 

He-man agrees. What's going on? Just watch it. 

In conclusion

So what's the final word? Income and capital breeding exists as a continuum. There are snakes on the far left (not liberal) and snakes on the far right (not conservative either!). However, most snakes fall somewhere in between. As a herpetologist, I want to know what factors influence snakes the most and what that means for their energy requirements during pregnancy. 

Literature Cited

Aldridge, R. 1979. Seasonal spermatogenesis in sympatric Crotalus viridis and Arizona elegans in New Mexico. Journal of Herpetology 13:187–192.

Bonnet, X., R. Shine, G. Naulleau, and M. Vacher-Vallas. 1998. Sexual dimorphism in snakes: different reproductive roles favour different body plans. Proceedings of the Royal Society B: Biological Sciences 265:179–183. 

Brown, W. 1991. Female reproductive ecology in a northern population of the timber rattlesnake, Crotalus horridus. Herpetologica 47:101–115. 

Diller, L., and R. Wallace. 1984. Reproductive biology of the Northern Pacific Rattlesnake (Crotalus viridis oreganus) in northern Idaho. Herpetologica 40:182–193.

Gregory, P., L. Crampton, and K. Skebo. 1999. Conflicts and interactions among reproduction, thermoregulation and feeding in viviparous reptiles: are gravid snakes anorexic? Journal of Zoology 248:231–241. 

Jönsson, K. 1997. Capital and income breeding as alternative tactics of resource use in reproduction. Oikos 78:57–66. 

Keenlyne, K. 1972. Sexual differences in feeding habits of Crotalus horridus horridus. Journal of Herpetology 6:234–237. 

Lourdais, O., and X. Bonnet. 2002. Capital breeding and reproductive effort in a variable environment: a longitudinal study of a viviparous snake. Journal of Animal Ecology 71:470–479. 

Naulleau, G., and X. Bonnet. 1996. Body condition threshold for breeding in a viviparous snake. Oecologia 107:301–306. 

Romero, L. M., M. J. Dickens, and N. E. Cyr. 2009. The Reactive Scope Model - a new model integrating homeostasis, allostasis, and stress. Hormones and Behavior 55:375–89. 

Schuett, G. W., R. a. Repp, M. Amarello, and C. F. Smith. 2013. Unlike most vipers, female rattlesnakes (Crotalus atrox) continue to hunt and feed throughout pregnancy. Journal of Zoology 289:101–110. 

Webber, M.M., X. Glaudas, and J.A. Rodríguez-Robles. 2012. Do Sidewinder rattlesnakes (Crotalus cerastes, Viperidae) cease feeding during the breeding season? Copeia 2012:100–105. 

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