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Topographical anatomy of the blunthead treesnake, imantodes cenchoa (Linnaeus, 1758) (colubridae: xenodontinae) / Anatomia topografica de la serpiente bejucillo cabezona, imantodes cenchoa (Linnaeus, 1758) (colubridae: xenodontinae).

AVEIRO-LINS, G.; ROCHA-BARBOSA, O.; SALOMAO, M. G.; PUORTO, G. & LOGUERCIO, M. F. C. Topographical anatomy of the blunthead treesnake, Imantodes cenchoa (Linnaeus, 1758) (Colubridae: Xenodontinae). Int. J. Morphol., 24(1):43-48, 2006.

SUMMARY: Imantodes cenchoa (Dumeril, 1853) is an arboreal, nocturnal and oviparous xenodontine snake, which feeds on amphibians and lizards. It is found in Central and South America, including northern and central Brazil. In this work, we investigated the relationship between topographic anatomy and habitat in I. cenchoa. Twenty specimens (13 non pregnant females and 7 males) were examined. The topographic anatomy study was realized through observations of the internal anatomy, particularly the position and size of lung, heart, liver, left and right gonads and left and right kidneys. Results showed that all the organs are located in a posterior position in relation to the snout vent length (SVL). The centre of gravity is found at about 74% of SVL in both males and females. In males, no positive allometry was observed among the positions of the organs. Negative allometry in females was observed regarding the position of the anterior tip of the left kidney, the anterior and posterior tips of the right kidney and in both ovaries. In males, negative allometry is present in the position of all the or gans. The distance between the last follicle and the cloaca was 8.78% of SVL. Our data corroborate the idea that the posterior position of all internal organs is linked to a habitat specialization of a snake, linking the arboreal species I. cenchoa with a relatively posterior internal topography.

KEY WORDS: Snakes; Ecomorphology; Anatomy; Allometry; Arboreality.

AVEIRO-LINS, G.; ROCHA-BARBOSA, O.; SALOMAO, M. G.; PUORTO, G. & LOGUERCIO, M. F. C. Anatomia topografica de la serpiente bejucillo cabezona, Imantodes cenchoa (Linnaeus, 1758) (Colubridae: Xenodontinae). Int. J. Morphol., 24(1):43-48, 2006.

RESUMEN: Imantodes cenchoa (Dumeril, 1853) es una serpiente xenodontinea, arborea, noctura y ovipara, que se alimenta de anfibios y largartos. Se encuenta en America Central y del Sur, incluyendo las partes Norte y Central de Brasil. En este trabajo, investigamos la relaciones entre la Anatomia Topografica y habitat en I. cenchoa. Fueron examinados 20 especimenes (13 hembras no prenadas y 7 machos). El estudio de la Anatomia Topografica fue realizada a traves de observaciones de la anatomia interna, particularmente la posicion y tamano del pulmon, corazon, higado, gonadas y rinones derechos e izquierdos. Los resultados mostraron que todos los organos estan localizados en una posicion posterior, en relacion a la entrada de la longitud del hocico(SVL). El centro de gravedad se encuentra a 74% de SVL en machos y hembras. En los machos, no fue observada alometria positiva entre la posicion de los organos. Fue observada alometria negativa en las hembras, considerando la posicion del extremo anterior del rinon izquierdo, los extremos anterior y posterior del rinon derecho y ambos ovarios. En machos, se presento alometria negativa en la posicion de todos los organos. La distancia entre el ultimo foliculo y la cloaca fue 8.78% de SVL. Nuestros datos corroboran la idea que la posicion posterior de todos los organos internos esta marcada por una especializacion al habitat de una serpiente, marcando la especie arborea I. cenchoa con una especial topografia interna posterior.

PALABRAS CLAVE: Serpientes; Ecomorfologia; Anatomia; Alometria; Arboreal.

INTRODUCTION

Snakes represent one of the more varied taxa concerning specializations for habitat and niche occupation (Lillywhite, 1988). Such specializations include differences in body size, habits, feeding behaviour and reproduction, and have determined the wide geographic distribution, as well as the evolutionary success of this group (Greene, 1997; Pough et al., 1998). Habitat characteristics mean a pool of biotic and abiotic levels of complexity that influence and might direct natural selection on morphology and physiology of snake populations (Vitt & Vangilder, 1983; Guyer & Donnelly, 1990; Cadle & Greene, 1993; Lillywhite & Henderson, 1993).

The study on topographic anatomy usually search for relations between the position and morphology of internal organs and external measurements or structures such as ventral scales, helping in the location of these organs and at the same time working as habitat use indicators in snakes. Several authors have reported the existence of anatomical variation in arboreal, terrestrial and aquatic snakes (Lillywhite, 1988; Rocha-Barbosa et al., 1999; Rocha-Barbosa et al., 2000), particularly heart position and size of vascular lung (Lillywhite, 1987b), which reflect strategies to adapt to gravitational variations in those habitats. The heart lies nearer to the head to guarantee blood supply to the brain both in typical arboreal species (Lillywhite, 1985b; Lillywhite, 1985a; Lillywhite, 1987a; Lillywhite, 1988; Lillywhite & Smits, 1992; Lillywhite, 1993; Lillywhite & Henderson; Badeer, 1998), as well as in those which exhibit incipient arboreality, as is the case of Bothrops insularis.

Therefore, since morphological differences express ecological shifts, it would be logical to expect anatomical changes in other parts of the body other than the heart.

However, little is known about the position, shape or volume of internal organs and its correlation to snake life history, particularly in tropical herpetofauna.

Imantodes cenchoa (Linnaeus, 1758) is a neotropical colubrid commonly known as blunt headed tree snake, and shows a special ability of moving quickly among branches (Greene). It is oviparous and during the night feeds on amphibians and lizards, especially anoles (Genus Anolis); (Robinson, 1977; Zug et al., 1979), whereas during the day it may be found hidden in bromeliads (Henderson & Nickerson, 1976), where it may feed on lizard eggs (Landry et al., 1966). Imantodes cenchoa occurs from the Isthmus of Tehuantepec, region of Mexico through Central and South America, reaching Paraguay and Bolivia (Peters & Orejas-Miranda, 1970).

This study aims to describe the topographic anatomy of I. cenchoa in an attempt to locate internal organs, as well as to define the position of the clutch in relation to the snout-vent length (SVL) and the ventral scales.

MATERIAL AND METHOD

Twenty adult specimens of Imantodes cenchoa (Linnaeus, 1758) (13 non-pregnant females and 7 males) were analyzed. All of them consisted of museum specimens from the collections Alphonse Richard Hoge, Instituto Butantan (IB) and Museu Nacional do Rio de Janeiro (MNRJ/UFRJ), Brazil.

To determine the centre of gravity of each specimen, the snakes are put on an aluminium tray. The straightness of the specimens is maintained by fine strings. A thread suspends the aluminium tray and slides gently till the point of equilibrium is reached. Such point (noted as the centre of gravity) is marked on the snake body. Later, this measure is converted into a proportion (%) of SVL.

Dissections were made following the methodology described previously by (Gomes et al., 1989) and (Gomes & Puorto, 1993). This technique allows the observation, location and measurement of internal organs, both as absolute measurements and in relation to position and length along the SVL. The position and length of organs were also recorded relative to the ventral scale count, by numbering the ventral scales and recording the number of the ventral scale at both the anterior and posterior ends of the organ. Lung, heart, liver, gonads and kidneys were longitudinally measured.

In females, the stage of vitellogenesis and the distance between the last ovarian or oviductal follicle and the cloaca were taken and transformed into a SVL proportion for comparisons with data of terrestrial and aquatic snakes obtained in the literature. (See Shine (1988) for details).

The biometrical measurements of both males and females were analyzed separately and compared subsequently to test for sexual dimorphism. Data were fitted using the power equation Y=a[X.sup.b] (Huxley, 1932), where dependent variable y represents the linear measurement and the independent variable x was the SVL. The problem of biased estimates of slopes of Y on X when both variables are subject to measurement error, was overcome using the slope of the principal axis of the standardized variables (reduced major axis, RMA) (Teissier, 1948; Sokal & Rohlf, 1995). A t-test was used to test for significance of departure from a predicted slope examined with residual analysis (Wittink, 1988). Each regression slope was checked for departure from isometry (Gould, 1966).

Equations were determined considering males and females separately. The equality of two population regression coefficients was tested for males and females allometric coefficients (sexual dimorphism). This involves the use of Student's t (p<0.05) in a fashion analogous to that of testing for differences between two population means. When the slopes of the males and females were not significantly different, then just one regression line was determined.

RESULTS

Biometrical data and regression analysis are presented in Tables I and II, respectively. Positive allometry was obtained for females regarding the following relationships: the end of the liver and left kidney, beginning and end of the heart and lung. In males, no positive allometry was verified. Negative allometry in females was observed for the beginning of the left kidney, beginning and end of right kidney and both ovaries. In males, negative allometry was obtained for all internal organs.

Band occurrence and band superposition of each organ (indicating the beginning and the end of each organ) takes into consideration ventral scales and SVL and are presented in Table III. In Imantodes cenchoa, the heart occupies a very anterior position, followed by other visceral organs (Fig.1). The centre of gravity was determined to be located in the medial position of the snake when total length is concerned. However, when SVL is taken into consideration, the centre of gravity is found posteriorly in both sexes (73.83% SVL).

[FIGURE 1 OMITTED]

All females analyzed were in primary vitellogenesis condition, with follicles reaching a maximum diameter 1.0 cm and did not present signs of vitello deposition. Despite the wide range of months included in the specimen sample (February, May, August and December), it was not possible to detect the period of secondary vitellogenesis and ovulation. The average distance between the last follicle and the cloaca was 64.79 [+ or -] 8.16 mm (n=6) which means 8.78% SVL at the ventral scale number 220.

DISCUSSION

Imantodes cenchoa is a snake whose body architecture shows almost all viscerae located in a posterior position relative to SVL, and a considerable space between the clutch and the cloaca, conditions which could facilitate locomotion on an arboreal habitat (Manzani, 1995). The weight of the animal, concentrated in the posterior part of the body, would serve as the main support for the snake, allowing the projection of the head and anterior part of the body without loss of equilibrium. This could speed up locomotion from branch to branch, and would enable the snake to strike agile prey more precisely, particularly lizards and amphibians (Young, 1982), the usual food items of the blunt headed tree snake.

In the field, we observed I. cenchoa supporting itself having only the last third of the body in contact with a branch, exactly the portion where the internal organs are concentrated. In this position the snake can easily project the head and the anterior part of the body forward very fast when capturing prey or escaping from predators.

Heart position may be constrained, due to the limited haemostatic control, lying in a more anterior position to ensure an adequate blood supply to the brain when the snake is tilted into a head-up position especially when climbing (Lillywhite & Smits, 1992; Lillywhite, 1993; Lillywhite & Henderson, 1993). Imantodes cenchoa assumes extreme vertical postures. However, our data show that its heart is located very posteriorly, about 36% SVL, opposed to the prediction of the authors mentioned above. Our findings agree with those of Manzani in which the heart is located between 11 and 42% SVL in arboreal snake representatives. Imantodes cenchoa is a member of the subfamily Xenodontinae, tribe Dipsadini, which includes other snakes with hearts in a posterior position (e.g., Leptodeira--Manzani), indicating that environmental pressures play a role as important as phylogeny in the determination of body structure.

Regarding the distance between the last follicle and the cloaca, our study indicates a wide space left over in the distal portion of the body, which suggests, according to (Shine), that locomotion may be prioritized over reproductive investment. The same pattern was observed in Philodryas olfersii, one arboreal representative of this genus, in which follicles are smaller than in other species of the same genus that also includes terrestrial members, probably due to the increased importance of body balance in trees compared to reproduction (Fowler & Salomao, 1994).

Tropical ophidian faunas show great morphological variety, probably owing to the adaptations presented in the occupation of diverse microhabitats (Guyer & Donnelly) as well as the variability of ecological niches, foraging strategies and diet (Kauffman & Gibbons, 1975). However, available data in the literature on ecomorphology take into consideration just some of the corporal variables, besides mentioning only the position of the heart and not any of other internal organs. The results here presented on I. cenchoa reinforce the importance of investigating the greatest possible number of internal corporeal variables, so that we can infer from physiological, ecological and behavioral aspects of a certain species or a group of serpents.

In general, the posterior position of all internal organs is linked to a habitat specialization of a snake (Martinez et al., 1985). Our data corroborate this idea, linking the arboreal species I. cenchoa with a relatively posterior internal topography.

Acknowledgements

We would like to thank FAPERJ (Proc. No E-26/ 171.310/2001; No E-26/170.654/04), Programa PROCIENCIA/UERJ, CNPq and CAPES for the financial support, Prof. Dr. Heitor Evangelista (UERJ), Prof. Dr. Ronaldo Fernandes (MNRJ) and Valdir Jose Germano (Instituto Butantan) for technical support. CR-BIO 02085.

Received: 29-09-2005 Accepted: 13-12-2005

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Lillywhite, H. B. Postural edema and blood pooling in snakes. Physiol. Zool., 58(6):159-65, 1985b.

Lillywhite, H. B. Circulatory adaptation of snakes to gravity. Am. Zool., 27:81-95, 1987a.

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Lillywhite, H. B. Snake, blood circulation and gravity. Sci. Am. 259:92-8, 1988.

Lillywhite, H. B. Orthostatic intolerance of viperid snakes. Physiol. Zool., 66(6):1000-14, 1993.

Lillywhite, H. B. & Henderson, R. W. Behavioral and functional ecology of arboreal snakes. In Snakes: ecology and behavior. Seigel, R. A. and Collins, J. T. (Eds.). New York, McGraw-Hill, 1993. pp 1-48.

Lillywhite, H. B. & Smits, A. W. The cardiovascular adaptations of viperid snakes. In Biology of pitvipers, 1992. pp 143-53,

Manzani, P. R. Acao da gravidade e sistema cardiovascular em serpentes: Habito ou Filogenia? Rio Claro, Sao Paulo, Universidade Estadual Paulista, 1995.

Martinez, D. R.; Lucio, J. A. & Schwartz, A. Topografia interna de las culebras del genero Uromacer (Colubridae). Caribaea, 1:48-59, 1985.

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Rocha-Barbosa, O.; Salomao, M. G.; Puorto, G.; Laporta-Ferreira, I. L. & Mandarim-de-Lacerda, C. A. Allometry and morphology of the heart in Oxyrhopus guibei Hoge & Romano, 1977 (Serpentes: Colubridae). Biomed. Res., 10:35-40, 1999.

Rocha-Barbosa, O., Salomao, M. G., Puorto, G., Laporta-Ferreira, I. L. and Mandarim-de-Lacerda, C. A. Allometry and ecology of the Oxyrhopus guibei Hoge & Romano, 1977 (Serpentes: Colubridae). Biomed. Res., 11:259-64, 2000.

Shine, R. Constraints on reproductive investiment: a comparison between aquatic and terrestrial snakes. Evolution, 42:17-27, 1988.

Sokal, R. R. & Rohlf, F. J. Biometry: the principles and practice of statistics in biological research. W.H. Freeman and Company, 1995.

Teissier, G. La relation d'allometrie: sa signification statistique et biologique. Biometrics, 4:14-48, 1948.

Vitt, L. J. & Vangilder, L. D. Ecology of a snake community in northeastern Brazil. Amphib. Reptil., 4:273-96, 1983.

Wittink, D. R. The Application of regression analysis. Boston, Allyn and Bacon Inc., 1988.

Young, A. M. Lizard eggs and snake (Imantodes) occupy "artificial bromeliads" in Costa Rican cacao plantations. Brenesia 19/20:393-6, 1982.

Zug, G. R.; Hedges, S. B. & Sukel, S. Variation in reproductive parameters of three metropical snakes, Coniophanes fissidens, Dipsas catesbyi, and Imantodes cenchoa. Smithsonian Contribution Zoology, 300:1-20, 1979.

* Gustavo Aveiro-Lins; * Oscar Rocha-Barbosa; ** Maria da Graca Salomao; *** Giuseppe Puorto & * Mariana Fiuza de Castro Loguercio

* Laboratorio de Zoologia de Vertebrados (Tetrapoda), Departamento de Zoologia/UERJ, IBRAG, Universidade do Estado do Rio de Janeiro, Rua Sao Francisco Xavier, 524, Maracana, 20550-013, Rio de Janeiro, RJ--Brasil.

** Laboratorio de Herpetologia, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, RJ--Brasil. obarbosa@uerj.br;

*** Museu Biologico do Instituto Butantan, Av. Vital Brazil, 1500, 05503-900, Sao Paulo, Brasil. mgsalomao@butantan.gov.br.

Correspondence to:

Oscar Rocha-Barbosa, PhD

Universidade do Estado do Rio de Janeiro

Laboratorio de Zoologia de Vertebrados

(Tetrapoda),

Departamento de Zoologia/UERJ, PHLC sls.

513b/515b, IBRAG

Rua Sao Francisco Xavier, 524, Maracana,

20550-013, Rio de Janeiro, RJ--Brasil

e-mail: obarbosa@uerj.br
Table I. Biometry of internal anatomy in Imantodes cenchoa, n=20. (SD -
standard deviation, X - mean, t - Student's t, p - probability.

Variable                             Males (X [+ or -] SD)

Heart                 Initial        276.28 [+ or -] 47.64
                      End            286.71 [+ or -] 49.14

Lung                  Initial        286.71 [+ or -] 49.14
                      End            338.30 [+ or -] 55.14

Liver                 Initial        311.00 [+ or -] 82.89
                      End            519.85 [+ or -] 92.81

Right ovary/testis    Initial        614.85 [+ or -] 129.71
                      End            624.28 [+ or -] 134.97

Left ovary/testis     Initial        632.00 [+ or -] 131.95
                      End            645.14 [+ or -] 138.97

Right kidney          Initial        635.57 [+ or -] 131.01
                      End            657.00 [+ or -] 131.19

Left kidney           Initial        645.14 [+ or -] 132.10
                      End            666.28 [+ or -] 134.38

Variable              Females (X [+ or -] SD)      t        p

Initial               272.15 [+ or -] 40.91      -0.28     0.79
End                   286.84 [+ or -] 40.76       0.01     0.99

Initial               279.38 [+ or -] 42.51      -0.48     0.64
End                   338.20 [+ or -] 39.23       0.00     1.00

Initial               323.77 [+ or -] 52.71       0.58     0.57
End                   497.84 [+ or -] 59.47      -0.89     0.39

Initial               633.00 [+ or -] 103.41      0.47     0.65
End                   657.15 [+ or -] 111.71      0.80     0.44

Initial               636.84 [+ or -] 95.87       0.13     0.90
End                   660.23 [+ or -] 101.33      0.38     0.71

Initial               663.62 [+ or -] 91.58       0.77     0.45
End                   688.23 [+ or -] 93.32       0.85     0.41

Initial               671.08 [+ or -] 93.18       0.70     0.73
End                   693.62 [+ or -] 93.81       0.49     0.48

Table II. Regression lines using the equation y=a[x.sup.b], is the SVL
and Y is one of the internal organs, n=20. (SVL - snout-vent length).
p - probability, r - coefficient of correlation.

  x          y                             Sex       [r.sup.2]

                                          males      0,86
                            Initial      females     0,82
SVL        Liver                          males      0,84
                              End        females     0,87

                                          males      0,80
SVL        Left kidney      Initial      females     0,73
                                          males      0,81
                              End        females     0,73

                                          males      0,80
SVL        Right kidney     Initial      females     0,77
                                          males      0,82
                              End        females     0,77

                                          males      0,80
SVL        Left ovary/
           testis           Initial      females     0,68
                                          males      0,81
                              End        females     0,73

                                          males      0,76
SVL        Right ovary/
           testis          Initial I     females     0,71
                                          males      0,77
                              End        females     0,75
                                          males      0,98
SVL        Heart            Initial      females     0,70
                                          males      0,98
                              End        females     0,66

                                          males      0,98
SVL        Lung             Initial      females     0,54
                                          males      0,99
                              End        females     0,87

  Sex      a            b            [P.sub.(0.05)]

 males     0,69         -189,29      0,002
females    0,54          -78,98      0,000
 males     0,76          -31,40      0,004
females    0,63           29,11      0,000
 males     1,06         -123,53      0,006
females    0,91           -0,75      0,000
 males     1,08          -11,878     0,006
females    0,92           16,90      0,000
 males     1,05         -127,65      0,006
females    0,92          -17,815     0,000
 males     1,06          -11,518     0,005
females    0,94           -6,07      0,000
 males     1,05         -132,83      0,007
females    0,91          -33,19      0,000
 males     1,11          -16,542     0,006
females    0,99          -71,49      0,000
 males     1,01         -117,39      0,011
females    1,00         -104,00      0,000
 males     1,06         -146,96      0,009
females    1,11         -160,98      0,000
 males     0,42          -29,39      0,000
females    0,37            2,46      0,000
 males     0,43          -29,32      0,000
females    0,38            4,97      0,000
 males     0,43          -29,32      0,000
females    0,36           16,29      0,000
 males     0,49          -18,69      0,000
females    0,42           29,50      0,004

Table III. Band Occurrence. (SVL - snout-vent length). n=20.

                                      Band occurrence

                                   SVL (%)    Ventral scale

Heart                 Initial      36-38         98-100
                      End          38-40         98-104

Lung                  Initial      37-40         98-104
                      End          45-47        115-121

Liver                 Initial      41-45        106-116
                      End          67-70        164-177

Right ovary/testis    Initial      82-88        208-220
                      End          84-91        214-226

Left ovary/testis     Initial      83-89        215-224
                      End          85-92        222-231

Right kidney          Initial      86-92        222-230
                      End          78-106       232-240

Left kidney           Initial      87-93        222-234
                      End          90-96        232-242

                          Band superposition

                     SVL (%)      Ventral scale

Initial               38              98-100
End

Initial
End

Initial
End

Initial               84-89          213-220
End

Initial               85-90          222-224
End

Initial               77-92          230-231
End

Initial               89-93          232-234
End
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Author:Aveiro-Lins, Gustavo; Rocha-Barbosa, Oscar; Salomao, Maria da Graca; Puorto, Giuseppe; Loguercio, Ma
Publication:International Journal of Morphology
Date:Mar 1, 2006
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