Mechanisms controlling venom expulsion in the western diamondback rattlesnake, Crotalus atrox

Abstract

Although many studies have documented variation in the amount of venom expended during bites of venomous snakes, the mechanistic source of this variation remains uncertain. This study used experimental techniques to examine how two different features of the venom delivery system, the muscle surrounding the venom gland (the Compressor Glandulae in the rattlesnake) and the fang sheath, could influence venom flow in the western diamondback rattlesnake, Crotalus atrox. Differential contraction of the Compressor Glandulae explained only approximately 30% of the variation in venom flow. Lifting (compression) of the fang sheath as occurs during a normal strike produced marked increases in venom flow; these changes were closely correlated and exceed in magnitude by almost 10 Â those recorded from the Compressor Glandulae alone. These results suggest that variation in these two aspects of the venom delivery system-both in terms of magnitude and temporal patterning-explain most of the observed variation in venom injection. The lack of functional or mechanical links between the Compressor Glandulae and the fang sheath, and the lack of skeletal or smooth muscle within the fang sheath, make it unlikely that variation in venom flow is under direct neural control. Instead, differential venom injection results from differences in the pressurization by the Compressor Glandulae, the gate keeping effects of the fang sheath and enclosed soft-tissue chambers, and by differences in the pressure returned by peripheral resistance of the target tissue.

Spitting versus Biting: Differential Venom Gland Contraction Regulates Venom Expenditure in the Black-Necked Spitting Cobra, Naja nigricollis nigricollis

“…Indeed, our analyses of venom flow duration in four other viperid species support this view (Herbert, 1998(Herbert, , 2007Hayes, 2008). Recently, Young and Kardong (2007) evaluated this possibility experimentally in the Western Diamondback (C. atrox). They reported that fang sheath compression resulted in 10-fold greater increases in venom flow (peak pressure) compared to differential contraction of the compressor glandulae muscles acting on the venom gland.…”

“…In both groups, individual pulses are associated with jaw contractions that, in viperids, also involve fang retraction. Thus, venom delivery characteristics are similar for the two snake families despite well-documented differences in their venom delivery systems (Jackson, 2003;Young and Kardong, 2007) and prey capture behavior (Kardong et al, 1997).…”

“…Rattlesnakes and other viperids, in contrast, lack muscular control of the venom sheath, which is compressed passively during contact with a target as the fangs penetrate the target (Young and Kardong, 2007). Even so, in both taxa, venom expulsion results from an additive effect of gland compression and fang sheath deformation and is executed by precise (although error-prone) coordination between various muscles controlling the jaws, fangs (in viperids), and venom gland (Kardong, 1986;Young and Zahn, 2001;Young et al, 2004;Young and Kardong, 2007). Accordingly, Young and Kardong (2007) concluded that there was a high degree of functional convergence between viperids and elapids within this system.…”

Spitting versus Biting: Differential Venom Gland Contraction Regulates Venom Expenditure in the Black-Necked Spitting Cobra, Naja nigricollis nigricollis

“…Indeed, our analyses of venom flow duration in four other viperid species support this view (Herbert, 1998(Herbert, , 2007Hayes, 2008). Recently, Young and Kardong (2007) evaluated this possibility experimentally in the Western Diamondback (C. atrox). They reported that fang sheath compression resulted in 10-fold greater increases in venom flow (peak pressure) compared to differential contraction of the compressor glandulae muscles acting on the venom gland.…”

“…In both groups, individual pulses are associated with jaw contractions that, in viperids, also involve fang retraction. Thus, venom delivery characteristics are similar for the two snake families despite well-documented differences in their venom delivery systems (Jackson, 2003;Young and Kardong, 2007) and prey capture behavior (Kardong et al, 1997).…”

“…Rattlesnakes and other viperids, in contrast, lack muscular control of the venom sheath, which is compressed passively during contact with a target as the fangs penetrate the target (Young and Kardong, 2007). Even so, in both taxa, venom expulsion results from an additive effect of gland compression and fang sheath deformation and is executed by precise (although error-prone) coordination between various muscles controlling the jaws, fangs (in viperids), and venom gland (Kardong, 1986;Young and Zahn, 2001;Young et al, 2004;Young and Kardong, 2007). Accordingly, Young and Kardong (2007) concluded that there was a high degree of functional convergence between viperids and elapids within this system.…”

Viper Fangs: Functional Limitations of Extreme Teeth

“…Young and Zahn (2001) recorded venom flow in the venom duct both when the ipsilateral fang penetrated and when it did not. Surprisingly, in the latter cases, no venom emerged from the fang, suggesting that flow through the fang is regulated independently of flow from the venom gland, supporting the hypothesis of a critical intermediate reservoir (Young and Kardong 2007) and the role of peripheral resistance in venom flow (Young et al 2002. Further, the fact that venom is typically not ejected from an unembedded fang when the contralateral fang is embedded shows that although all events through early mouth closing are likely to be feed-forward ones, unilateral regulation of venom expulsion may not be a function of gland constrictor muscles but of peripheral regulators of venom flow lying somewhere between the duct and the discharge orifice of the fang.…”

“…Combining the critical flow data from Young and Zahn (2001) with all the other morphological and kinematic data produced by Young and colleagues (Young et al 2000(Young et al , 2001a(Young et al , 2001b(Young et al , 2002Young and Kardong 2007) provides compelling support for the hypothesis that venom expulsion results from the fang sheath sliding upward (unplugging the discharge orifice) combined with entry of the discharge orifice into prey tissues having hydrostatic pressures lower than those in the venom duct and venom canal. The possible dependence of venom injection on sensory feedback may underlie the relatively long duration of the bite phase.…”

Spitting versus Biting: Differential Venom Gland Contraction Regulates Venom Expenditure in the Black-Necked Spitting Cobra, Naja nigricollis nigricollis

“…Indeed, our analyses of venom flow duration in four other viperid species support this view (Herbert, 1998(Herbert, , 2007Hayes, 2008). Recently, Young and Kardong (2007) evaluated this possibility experimentally in the Western Diamondback (C. atrox). They reported that fang sheath compression resulted in 10-fold greater increases in venom flow (peak pressure) compared to differential contraction of the compressor glandulae muscles acting on the venom gland.…”

“…In both groups, individual pulses are associated with jaw contractions that, in viperids, also involve fang retraction. Thus, venom delivery characteristics are similar for the two snake families despite well-documented differences in their venom delivery systems (Jackson, 2003;Young and Kardong, 2007) and prey capture behavior (Kardong et al, 1997).…”

“…Rattlesnakes and other viperids, in contrast, lack muscular control of the venom sheath, which is compressed passively during contact with a target as the fangs penetrate the target (Young and Kardong, 2007). Even so, in both taxa, venom expulsion results from an additive effect of gland compression and fang sheath deformation and is executed by precise (although error-prone) coordination between various muscles controlling the jaws, fangs (in viperids), and venom gland (Kardong, 1986;Young and Zahn, 2001;Young et al, 2004;Young and Kardong, 2007). Accordingly, Young and Kardong (2007) concluded that there was a high degree of functional convergence between viperids and elapids within this system.…”

Viper Fangs: Functional Limitations of Extreme Teeth

“…Young and Zahn (2001) recorded venom flow in the venom duct both when the ipsilateral fang penetrated and when it did not. Surprisingly, in the latter cases, no venom emerged from the fang, suggesting that flow through the fang is regulated independently of flow from the venom gland, supporting the hypothesis of a critical intermediate reservoir (Young and Kardong 2007) and the role of peripheral resistance in venom flow (Young et al 2002. Further, the fact that venom is typically not ejected from an unembedded fang when the contralateral fang is embedded shows that although all events through early mouth closing are likely to be feed-forward ones, unilateral regulation of venom expulsion may not be a function of gland constrictor muscles but of peripheral regulators of venom flow lying somewhere between the duct and the discharge orifice of the fang.…”

“…Combining the critical flow data from Young and Zahn (2001) with all the other morphological and kinematic data produced by Young and colleagues (Young et al 2000(Young et al , 2001a(Young et al , 2001b(Young et al , 2002Young and Kardong 2007) provides compelling support for the hypothesis that venom expulsion results from the fang sheath sliding upward (unplugging the discharge orifice) combined with entry of the discharge orifice into prey tissues having hydrostatic pressures lower than those in the venom duct and venom canal. The possible dependence of venom injection on sensory feedback may underlie the relatively long duration of the bite phase.…”

Spitting versus Biting: Differential Venom Gland Contraction Regulates Venom Expenditure in the Black-Necked Spitting Cobra, Naja nigricollis nigricollis

“…Indeed, our analyses of venom flow duration in four other viperid species support this view (Herbert, 1998(Herbert, , 2007Hayes, 2008). Recently, Young and Kardong (2007) evaluated this possibility experimentally in the Western Diamondback (C. atrox). They reported that fang sheath compression resulted in 10-fold greater increases in venom flow (peak pressure) compared to differential contraction of the compressor glandulae muscles acting on the venom gland.…”

“…In both groups, individual pulses are associated with jaw contractions that, in viperids, also involve fang retraction. Thus, venom delivery characteristics are similar for the two snake families despite well-documented differences in their venom delivery systems (Jackson, 2003;Young and Kardong, 2007) and prey capture behavior (Kardong et al, 1997).…”

“…Rattlesnakes and other viperids, in contrast, lack muscular control of the venom sheath, which is compressed passively during contact with a target as the fangs penetrate the target (Young and Kardong, 2007). Even so, in both taxa, venom expulsion results from an additive effect of gland compression and fang sheath deformation and is executed by precise (although error-prone) coordination between various muscles controlling the jaws, fangs (in viperids), and venom gland (Kardong, 1986;Young and Zahn, 2001;Young et al, 2004;Young and Kardong, 2007). Accordingly, Young and Kardong (2007) concluded that there was a high degree of functional convergence between viperids and elapids within this system.…”

Viper Fangs: Functional Limitations of Extreme Teeth

“…Young and Zahn (2001) recorded venom flow in the venom duct both when the ipsilateral fang penetrated and when it did not. Surprisingly, in the latter cases, no venom emerged from the fang, suggesting that flow through the fang is regulated independently of flow from the venom gland, supporting the hypothesis of a critical intermediate reservoir (Young and Kardong 2007) and the role of peripheral resistance in venom flow (Young et al 2002. Further, the fact that venom is typically not ejected from an unembedded fang when the contralateral fang is embedded shows that although all events through early mouth closing are likely to be feed-forward ones, unilateral regulation of venom expulsion may not be a function of gland constrictor muscles but of peripheral regulators of venom flow lying somewhere between the duct and the discharge orifice of the fang.…”

“…Combining the critical flow data from Young and Zahn (2001) with all the other morphological and kinematic data produced by Young and colleagues (Young et al 2000(Young et al , 2001a(Young et al , 2001b(Young et al , 2002Young and Kardong 2007) provides compelling support for the hypothesis that venom expulsion results from the fang sheath sliding upward (unplugging the discharge orifice) combined with entry of the discharge orifice into prey tissues having hydrostatic pressures lower than those in the venom duct and venom canal. The possible dependence of venom injection on sensory feedback may underlie the relatively long duration of the bite phase.…”