What makes the heart of Boa constrictor ( Squamata : Boidae ) beat faster ?

Body size is highly correlated with metabolism, which in turn influences physiological rates such as heart rate. In general, heart rate is negatively influenced by the size of animal's body, but there is insufficient data corroborating this pattern in snakes. This study evaluated how body size affects heart rate in captive Boa constrictor Linnaeus, 1758. We measured the heart rate of 30 snakes using digital palpation and evaluated how this rate is influenced by body mass and sex using Analysis of Covariance (ANCOVA). The heart rate of the snakes was 58.8 ± 6.7 bpm (beats per minute). Body size, estimated as log-transformed body mass, negatively influenced heart rate (F1,28 = 10.27, p = 0.003, slope = -0.00004, R2 = 0.27), but sex had no effect (F1,27 = 0.07, p = 0.80). In conclusion, this result corroborates the negative relationship between body size and heart rate for snakes and reinforces the influence of related metabolic characteristics, such as body size, on the physiological parameters of snakes.

The heart rate of snakes is influenced by diverse factors such as temperature (LILLYWHITE et al. 1999, KIK & MITCHELL 2005, RUTSKINA et al. 2009), the digestive process (WANG et al. 2001, ENOK et al. 2013), activity pattern (WANG et al. 2001), and pregnancy (BIRCHARD et al. 1984), among others.One particular trait of animals, body size, is strongly and negatively correlated with metabolic rates (CLARKE & JOHNSTON 1999, GILLOOLY et al. 2001).Metabolic rates influence heart rate and other physiological responses.Large vertebrates have slower heart rate when compared with smaller ones (LILLYWHITE et al. 1999, SCHMIDT-NIELSEN 2002), a pattern that has been confirmed for some Australian snakes (SEYMOUR 1987) and Burmese pythons (ENOK et al. 2014).In one study conducted on snake embryos (DU et al. 2013) the heart rate was higher in small species than in larger ones.However, general laws governing cardiovascular functions and body size may have exceptions, and for this reason it is important to evaluate whether or not they apply to different species (ENOK et al. 2014).This is particularly true for snakes, a group for which the relationship between heart rate and body size remains relatively unexplored.
Boa constrictor Linnaeus, 1758 (Boidae), popularly known as the common boa, occurs from Mexico to northern Argentina (VANZOLINI et al. 1980).This snake is commonly reared in captivity as a pet (PUORTO & FRANÇA 2009).Even though the heart rate of B. constrictor has already been documented, previous studies are based on small samples (CLARK & MARX 1960, VALENTINUZII et al. 1969a, b) that did not allow for a statistical evaluation of the relationship between heart rate and body size.One additional study, by WANG et al. (2001), evaluated the influence of diet and forced activity on the heart rate of this species.
According to RASKE et al. (2012), information about heart rate, respiratory rate, and body temperature may improve the clinical treatment of ectothermic vertebrates.This study aimed to investigate the heart rate of captive common boas and to evaluate whether it is influenced by body size, a characteristic that is associated with metabolism.
We kept 30 captive B. constrictor at the Núcleo Regional de Ofiologia da Universidade Federal do Ceará (NUROF-UFC) at a room temperature (29.1 ± 1.4°C) and humidity (62 ± 7%).Each snake was maintained in an individual wooden box and offered water ad libitum.The experimental group, composed of 19 females and 11 males, was kept without food for about 15 days before the experiment started.This fasting period is important to control for the influence of the digestion process on heart rate (ENOK et al. 2013).
We immobilized the animals using a herpetological hook and measured their heart rate (HR) by digital palpation.Heart

SHORT COMMUNICATION
What makes the heart of Boa constrictor (Squamata: Boidae) beat faster?-DEMERS et al. 2000).Since we measured the heart rate of active individuals using palpation, our results reflect the maximal or active, not resting, HR.The body mass of each snake was measured in grams (g) using a digital balance.
Initially, we employed Analysis of Covariance (ANCOVA) with log 10 (HR) as a dependent variable (response), and gender and mass as independent variables (explanatory), because there was an unequal ratio of males and females in the sample.ANCOVA assumptions (linearity and equal slopes) were valid.Next, we performed a simple linear regression to evaluate the effects of mass on HR.Residuals of the regressions were checked for normality and their relationship with fitted values, in order to confirm their validity.The level of significance used in these comparisons was 5% (p < 0.05).Descriptive statistics are presented as mean ± standard deviation.Analyses were performed in the software R ver.3.0.2(R CORE TEAM 2013).
Our results for B. constrictor corroborate the general pattern reported in the literature of a negative correlation between heart rate and body size (LILLYWHITE et al. 1999, SCHMIDT-NIELSEN 2002), demonstrating that metabolic related measurements are good predictors of vital rates in this species.Our data on the heart rate of B. constrictor, unlike previous studies, is based on a large sample, and for this reason it might be more relevant for veterinary use (RASKE et al. 2012).
A negative relationship between heart rate and body mass had been previously reported in reptiles, and more specifically snakes (SEYMOUR 1987, LILLYWHITE et al. 1999, ENOK et al. 2014).Seymour's results are restricted to Australian snakes and were obtained from a small sample size (only 13 individuals in nine different species).The heart rate of Burmese pythons, Python bivittatus Kuhl, 1820, is negatively related with body size (ENOK et al. 2014), but the HR values obtained for this species are lower than for B. constrictor.This may be due to differences in mass between the two species.P. bivittatus is heavier than B. constrictor, corroborating the pattern of a negative relationship between HR and body size reported by SEYMOUR (1987).However, the body mass of many individuals of P. bivittatus investigated by ENOK et al. (2014) was greater than the body size of B. constrictor used in our study.Also, the differences found between both studies could be due to the methodology used by ENOK et al. (2014): they kept the animals under minimum disturbance and measured their resting HR.
The heart rate values found in this study were similar to the values found by WANG et al. (2001) for B. constrictor in conditions of forced activity and similar temperature (28 ± 5°C).In their data the animals were encouraged to strike and bite (61.4 ± 1.5 bpm, where 1.5 is standard error).The HR of the snakes in our study was measured in the NUROF-UFC while the animals were active (most of them sibilating and constricting the hands of the researchers during the measurements).Therefore, the similarity between our results and WANG et al.'s (2001) was expected because animals in both studies were similarly active and were in equivalent environmental conditions.The heart rate of B. constrictor from the NUROF-UFC was higher than in the specimen evaluated by CLARK & MARX (1960).Differences in environmental temperature may explain this difference, because this variable is known to influence heart rate (LILLYWHITE et al. 1999, KIK & MITCHELL 2005, RUTSKINA et al. 2009).
The similarity in mean and standard error values obtained in similar environmental and activity situations in our study and in WANG et al.'s (2001) (mean = 58.8 and 61.4 bpm;and standard error = 1.50 and 1.49, respectively) indicates that the manual method of measuring HR seems to be useful for estimating patterns of heart rate in common boas.However, it was difficult to perform in large snakes with strong muscles and a deep body cavity.The manual method is valuable when it is not possible to use more sophisticated methods such as electrocardiogram (e.g., VALENTINUZII et al. 1969a, b, RUTSKINA et al. 2009, STUGINSKI et al. 2011), Doppler blood flow detector (e.g., RASKE et al. 2012), or pressure transducers (WANG et al. 2011, ENOK et al. 2014). According to RASKE et al. (2012), safe and inexpensive measurements of heart rate may be valuable for exotic animal medicine.STUGINSKI et al. (2011) also found no relationship between HR and sex in Crotalus durissus Linnaeus, 1758.Sexual changes in the HR of snakes may occur due to pregnancy, which increases heart rate (BIRCHARD et al. 1984).Common boas were maintained in individual cages in NUROF-UFC since their arrival and they exhibited no signs of pregnancy.
In conclusion, the heart rate of captive B. constrictor was negatively influenced by body size.This study, in addition to offering HR parameters of the model species for comparative purposes for veterinarians, also reinforces the influence of variables related to metabolism on physiological rates such as the heart rate of snakes.

Figure 1 .
Figure1.Relationship between body mass (g) and log 10 -transformed heart rate, measured as beats per minute in 30 individuals of Boa constrictor from Núcleo Regional de Ofiologia da Universidade Federal do Ceará.

João Fabrício Mota Rodrigues 1,2,3 , Roberta da Rocha Braga 2 , Thaís Helena Alencar Ferreira 2 , Estéfanni de Castro Pinheiro 2 , Géssica dos Santos Araújo 2 & Diva Maria Borges-Nojosa 2 rate
(RASKE et al. 2012 ENOK et al. 2014)per minute (bpm).Even though most modern studies have used another method to measure heart rate, which includes a surgically inserted catheter filled with heparinized saline connected to a pressure transducer(WANG et al. 2001, ENOK et al. 2014), we have found that our method produces similar results (see discussions below for more details).Furthermore, digital palpation is easier to perform, cheaper, and safer for the subjects.Safety is an important concern in the care of exotic animals(RASKE et al. 2012) such as B. constrictor.We measured the heart rate of active individuals because anesthesia may result in greater variations of this measurement (BLOUIN