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Notes on sexual dimorphism, diet and reproduction of the false coral snake Oxyrhopus rhombifer Duméril, Bibron & Duméril, 1854 (Dipsadidae: Pseudoboini) from coastal plains of Subtropical Brazil

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Acta Herpetologica 15(2): 143-148, 2020
ISSN 1827-9635 (print) © Firenze University Press
ISSN 1827-9643 (online) www.fupress.com/ah
DOI: 10.13128/a_h-7875
Notes on sexual dimorphism, diet and reproduction of the false
coral snake Oxyrhopus rhombifer Duméril, Bibron & Duméril, 1854
(Dipsadidae: Pseudoboini) from coastal plains of Subtropical Brazil
F M. Q*, F C, D L
Laboratório de Vertebrados, Instituto de Ciências Biológicas, Universidade Federal do Rio Grande, Avenida Itália s/n, Vila Carreiros,
Rio Grande, Rio Grande do Sul, Brazil
Fundação Aury Luiz Bodanese, Rua João Martins, 219D, São Cristovão, Chapecó, Santa Catarina, Brazil
*Corresponding author. E-mail: fmquintela@yahoo.com.br
Submitted on: 2020, 22nd January; revised on: 2020, 8th July; accepted on: 2020, 9th July
Editor: Stefano Scali
Abstract. Herein, we provide information on diet, sexual dimorphism and reproductive biology of the false coral
snake Oxyrhopus rhombifer from the southernmost Brazilian coast, Pampa Biome, a region under inuence of sub-
tropical climatic domains. e analysis of 142 specimens revealed a marked sexual dimorphism, with signicant dif-
ferences for all the characters analyzed. e diet of the species is composed by small rodents and squamate reptiles,
the latter consisting mainly of lizard tails, probably autotomized. Males reached sexual maturity at smaller sizes (SVL)
than females (354 mm vs 451 mm, respectively). Secondary follicles were found mainly in spring months and one sin-
gle female presented 3 oviductal eggs in January (summer). Our results add to the knowledge on biology of snakes in
the Pampa morphoclimatic domain.
Keywords. Feeding habits, reproductive biology, Pampa Biome, Squamata, Xenodontinae.
Investigating the natural history of species is essential
for understanding ecological processes at dierent levels
and provides crucial information for species conservation
(Greene, 1993; Gaiarsa et al., 2013). Regarding Neotropi-
cal snakes, the last decades have experienced an incre-
ment in the number of studies concerning diverse traits
of natural history and sexual dimorphism, but these are
still fragmented and incipient, considering the groups
high diversity (Barbo et al., 2011; Gaiarsa et al., 2013).
e Oxyrhopus genus comprises 14 species of medi-
um-sized pseudoboines distributed from southeast-
ern Mexico to central Argentina (Lynch, 2009; Uetz et
al., 2017). Most Oxyrhopus species exhibit a coral snake
mimetic pattern (Savage and Slowinski, 1992), respon-
sible for the popular name ‘false coral snakes’. Oxyrho-
pus rhombifer (Fig. 1) is the southernmost distributed
Oxyrhopus, ranging from southeastern Brazil to central
Argentina (province of Buenos Aires) (Giraudo, 2001).
ere are few scattered data available O. rhombifer diet
and reproductive biology (Vidal, 2002; Maschio et al.,
2003, 2004; Sawaya et al., 2003, 2008; Gaiarsa et al., 2013)
and no data on its sexual dimorphism. Herein, we exam-
ined size at sexual maturity, female reproductive cycle,
feeding habits and sexual dimorphism of O. rhombifer
from southernmost Brazilian coastal environments.
Specimens were collected along a stretch of ca. 470
km of the coastal plain of the Rio Grande do Sul state
(30°15’44”S, 50°28’03”W; 33°40’27”S, 53°30’52”W),
southern Brazil, between August 2008 and October 2017.
Sampling method consisted in active search performed
by two researchers in 77 field trips with an average
duration from two to 11 hours (average of four hours).
144 Fernando M. Quintela, Felipe Caseiro, Daniel Loebmann
Searches were conducted on foot and by car at low speed
(20-40 km/h) during day and night periods. is region
is inserted in the Pampa biome, under “subtemperate
humid” and “temperate humid” climatic domains accord-
ing to the regional classication by Maluf (2000). Seasons
are well-dened, with monthly average air temperature
ranging from 13 °C in the winter (July) to 22 °C in the
summer (January). Average rainfall is 1,271 mm and rain
is distributed mainly from June to October (Climate-
Data, 2019). Predominant vegetation types are shrub
grassland, and other phytophysiognomies with less cov-
erage include the coastal peat and sandy forests (restinga
forests) and psamophyte formations of coastal dunes.
Specimens were euthanized through intraperitoneal
injection of pentobarbital sodium 50 mg/ml, in accord-
ance with guidelines from international protocols. is
procedure had been authorized in our laboratory since
2006 and it is in accordance with the institutional com-
mittee for the use of animals in research (CEUA-FURG).
Collection was permitted by the Brazilian environmental
agency (ICMBio process nº 43658-1). e snakes had to
be euthanized for the analyses of the reproductive condi-
tion and digestive tract content and for the availability of
specimens and tissues for the projects “Taxonomic revi-
sion and systematics of Oxyrhopus rhombifer (Serpentes:
Dipsadidae)” and “Male reproductive cycle of Oxyrho-
pus rhombifer (Serpentes: Dipsadidae) in Southern Bra-
zil”. Oxyrhopus rhombifer is classied as Least Concern
by IUCN (Arzamendia et al., 2019). All specimens are
deposited in the herpetological collection of Universidade
Federal do Rio Grande (CHFURG) (Appendix).
Sex was determined through verification of the
presence or absence of hemipenes via subcaudal inci-
sion. e following measurements were taken from each
specimen, with a digital caliper to the nearest 0.01 mm:
snout-vent length (SVL), tail length (TL), head length
(HL), head width (HW), inter-ocular length (IOL), inter-
nostril length (INL). We examined the existence of sexual
dimorphism in the following characters: 1) SVL; 2) tail
proportion in relation to body length (ratio TL/SVL); 3)
number of ventral scales; 4) number of subcaudal scales;
5) head length in proportion to body length (ratio HL/
SVL); 6) head width in proportion to head length (ratio
HW/HL); 7) inter-ocular length in relation to head
length (ratio IOL/HL); 8) inter-nostril length in relation
to head length (ratio INL/HL). All database was checked
for normality through Shapiro-Wilk tests, which detected
normal distributions only for SVL, TL/SVL, and number
of subcaudal scales. For these characters, the existence of
signicance dierences between males and females was
examined with a Students t test. For the other charac-
ters (HL/SVL, HW/HL, IOL/HL, INL/HL and number of
ventral scales) we applied a Mann-Whitney test aiming
to verify signicant dierences between the sexes. Only
mature specimens were examined for sexual dimorphism
in SVL, TL/SVL, HL/SVL, HW/HL, IOL/HL and INL/
HL. Mature and immature specimens were pooled for the
analysis on sexual dimorphism in the number of ventral
and subcaudal scales. Statistical tests were performed in
soware PAST v.3.25 (signicance P < 0.05). (Hammer et
al., 2001).
A ventral incision was made from the esophageal
region to around 5 mm above the cloaca and the diges-
tive and reproductive tracts were externalized for analy-
sis. All stomach and gut contents were removed and
identified to the lowest possible taxonomic category.
Whenever possible, the direction of prey intake (head
first or tail first) was annotated. Numeric abundance
(N%) of all consumed taxa was determined as the ratio
between the absolute number of prey from one taxon and
the sum of prey of all identied taxa (Corrêa et al., 2016).
e following reproductive data were recorded from
females: total number of ovarian follicles; number of fol-
licles in secondary vitellogenesis (secondary follicles
are dened as enlarged follicles with yolk accumulation;
diameter ≥ 9 mm, based on the scatterplot of the larg-
est follicles of all females and on coloration [Almeida-
Santos et al., 2014]); diameter of the largest secondary
follicle; total number of eggs; occurrence of celomatic fat
storage; and largest diameter of the largest egg. Females
were considered mature when showing at least one of
the following characteristics: 1) secondary follicles; 2)
oviductal eggs; and 3) folded oviducts, indicating recent
oviposition. Males were considered mature when pre-
sented coiled and opaque ductus deferens, indicating the
presence of sperm. e female reproductive cycle was
evaluated by: 1) analysis of the distribution of females
Fig. 1. Oxyrhopus rhombifer (unvouchered) from Rio Grande, Rio
Grande do Sul state, southern Brazil.
145
Notes on sexual dimorphism, diet and reproduction of the false coral snake
carrying secondary follicles and oviductal eggs along
the months of the year; 2) analysis of the annual prole
resultant from the plot of the largest follicles and eggs
of each female (Mesquita et al., 2013; Almeida-Santos et
al., 2014). Fecundity was determined by the number of
eggs in the oviduct (real fecundity) and the number of
secondary follicles (potential fecundity) in the ovarium
(Mesquita et al., 2013). e correlation between female
SVL and potential fecundity was examined with a simple
linear regression analysis (Mesquita et al., 2013).
A total of 141 O. rhombifer specimens (89 males,
52 mature and 37 immature; 53 females, 22 mature, 31
immature) were analyzed. Females presented higher
mean values of SVL and number of ventral scales. Males
presented higher mean values for TL/SVL, HL/SVL, HW/
HL, IOL/HL, INL/HL, and number of subcaudal scales
(Table 1). Summary statistics for all the variables ana-
lyzed for sexual dimorphism are presented in Table 1.
Signicant dierences between sexes were found for all
the variables tested (Table 1).
Twenty-four specimens contained 24 prey item each.
Prey was comprised of rodents (N% = 50.0) and Squama-
ta reptiles (N% = 50.0) (Table 1). Eight out of nine prey
in which the direction of intake could be determined were
head-rst consumed (Table 2). Eleven out of 12 rodents
identified were consumed by mature individuals. Liz-
ards were consumed by both mature and immature indi-
viduals. e single snake identied was consumed by an
immature individual. Half of the squamate prey consisted
of tail fragments of Scincomorpha and Anguidae lizards.
The smallest female exhibiting secondary folli-
cles presented 451 mm of SVL, while the smallest male
exhibiting coiled/opaque ducti deferentes presented 354
mm of SVL. Secondary follicles were found mainly from
Table 1. Summary statics of the variables analyzed for sexual dimorphism in Oxyrhopus rhombifer from southern Brazilian coast (Rio
Grande do Sul state) and results of Student’t and Mann-Whitney tests performed on the variables. Analyses on SVL, TL/SVL, HL/SVL,
HW/HL, IOD/HL and IND/HL were performed in mature specimens. Analyses on number of ventral and subcaudal scales were performed
on both mature and immature specimens. See main text for abbreviations; n = number of specimens.
Vari a b l e Males Females test value P value
SVL 445 ± 59 (354-597) n = 52 616 ± 92 (451-758) n = 22 9.58 1.701E-14
TL/SVL 0.276 ± 0.023 (0.226-0.358) n = 52 0.189 ± 0.012 (0.161-0.215) n = 22 16.35 5.902E-26
HL/SVL 0.034 ± 0.003 (0.026-0.041) n = 49 0.032 ± 0.003 (0.027-0.039) n = 22 2.94 0.0032
HW/HL 0.557 ± 0.065 (0.478-0.779) n = 49 0.520 ± 0.061 (0.429-0.675) n = 22 2.38 0.017
IOD/HL 0.0346 ± 0.036 (0.296-0.455) n = 49 0.0317 ± 0.006 (0.246-0.368) n = 22 2.56 0.010
IND/HL 0.202 ± 0.028 (0.153-0.289) n=49 0.184 ± 0.022 (0.138-0.226) n = 22 2.40 0.016
Nº ventral scales 180 ± 6 (162-197) n = 78 192 ± 9 (160-212) n = 51 7.74 9.76E-15
Nº subcaudal scales 65 ± 3 (58-71) n = 81 57 ± 3 (50-63) n = 50 16.06 2.19E-22
Table 2. Absolute number (n) and numeric abundance (N%) of prey items found in digestive tracts of Oxyrhopus rhombifer from the south-
ern Brazilian coast (Rio Grande do Sul state), frequency and percentage (between parentheses) of prey intake directions of identied taxa,
namely: head rst (hf), tail rst (tf ) and not determined (ND).
Prey n N% hf tf ND
Sauropsida: Squamata
Ophiodes sp. (Anguidae) 2 8.3 2 (100)
Aspronema dorsivittatum (Scincidae) 1 4.2 1 (100)
Cercosaura schreibersii (Gymnophthalmidae) 7 29.2 3 (42.9) 1 (14.2) 3 (42.9)
Lizard not identied 1 4.2 1 (100)
Snake not identied 1 4.2 1 (100)
Mammalia: Rodentia
Deltamys kempi (Cricetidae: Akodontini) 1 4.2 1 (100)
Oligoryzomys avescens (Cricetidae:
Oryzomyini) 3 12.5 3 (100)
small rodent not identied 8 33.3 8 (100)
146 Fernando M. Quintela, Felipe Caseiro, Daniel Loebmann
September to November (spring). A single female pre-
sented secondary follicles in January (early summer) and
another one showed secondary follicles in May (middle
autumn) (Fig. 2). Potential fecundity varied from two to
13 (x = 7.9 ± 3.4 SD; n = 11). One single female, eutha-
nized in January, presented eggs in the oviduct (three
eggs). is same female also presented secondary and
primary follicles in the ovaries, indicating the possible
occurrence of more than one clutch during the cycle.
is female did not present expanded oviducts, which
indicates that there was no previous egg laying, and the
three oviductal eggs may correspond to a single oviposi-
tion event. A greater fat storage was observed in mature
females during initial and intermediate secondary vitel-
logenesis while low celomatic fat deposition was found
in females in advanced secondary vitellogenesis. We did
not nd any signicant, albeit positive, correlation (r =
0.07; P = 0.84) between female SVL and potential fecun-
dity. An aggregation of three similar-sized males and one
larger female, intertwined, but not involved in copulation,
was observed in October (early spring).
Our results indicated that sexual dimorphism is
very well marked in O. rhombifer from southern Bra-
zilian coastal plain, considering that all the variables
herein tested were signicantly dierent between sexes.
e dimorphism in body size (SVL) is noteworthy, with
females signicantly larger and showing higher num-
ber of ventral scales. Males, however, presented tail pro-
portionally longer, higher number of subcaudal scales,
head proportionally longer and wider and greater inter-
ocular and inter-nostril measurements. e larger body
in females and the tail proportionally longer in males
is a well-known aspect in dipsadid snakes (Aguiar and
Di-Bernardo, 2005; Balestrin and Di-Bernardo, 2005;
Mesquita et al., 2013; Quintela et al., 2017; Quintela and
Loebmann, 2019a, b), including the congener Oxyrhopus
trigeminus (Alencar et al., 2012). Mature females of Oxy-
rhopus guibei also showed SVL signicantly larger than
mature males (Pizzatto and Marques, 2002). e longer
body size in females in species without male-male com-
bat is associated with fecundity so that a larger body can
accommodate a larger ospring. us, females experience
the fertility selection, in which larger bodies take advan-
tage (Shine, 1994). In relation to head dimensions, stud-
ies have demonstrated that sexual dimorphism in head
traits of snakes are related to dierences in the maxi-
mum size of preys consumed by dierent sexes (Shine,
1989; Pearson et al., 2002; Shetty and Shine, 2002; Vin-
cent et al., 2004). A broader analysis of the feeding habits
of the species, based on a larger sample of preyed items,
could reveal if in fact males feed on larger prey. Anoth-
er hypothesis to be considered is the use of the head by
males for the immobilization of females during mating.
Oxyrhopus rhombifer feeds on small mammals and
squamate reptiles in the studied area, which is in agree-
ment with data from other regions where the species
occurs (Vidal, 2002; Maschio et al., 2003, 2004; Sawaya et
al., 2008; Gaiarsa et al., 2013) and from other Oxyrhopus
species (Alencar et al., 2012; Gaiarsa et al., 2013). How-
ever, the high occurrence of solely lizard tail fragments in
the analyzed digestive tracts (25% of all prey items, 50%
of Squamata items; Tab. 1), possibly autotomized to avoid
predation, is remarkable. Caudal autotomy is a very com-
mon defensive mechanism in lizards (Clause and Capaldi,
2006), considering that solely tail fragments have been
found in tracts of other xenodontine species such as Philo-
dryas aestiva and P. patagoniensis (Quintela, pers. comm.).
Females attained sexual maturity at much larger siz-
es than males, in agreement with O. guibei (Pizzatto and
Marques, 2002), O. trigeminus (Alencar et al., 2012) and
other xenodontine genera (Pizzato et al., 2008; Mesquita
et al., 2013; Rebelato et al., 2016; Quintela et al., 2017,
Quintela and Loebmann, 2019a, b). e small number
of mature females in our sample, however, did not allow
further analysis or conclusions about the reproductive
cycle and fecundity. e occurrence of females show-
ing secondary follicles in spring may indicate a seasonal
reproductive cycle, a pattern already recorded for other
xenodontines in the studied region (Oliveira et al., 2011;
Rebelato et al., 2016; Quintela et al., 2017; Quintela and
Loebmann, 2019a, b). A marked greater accumulation
of celomatic fat in females during initial and intermedi-
ate secondary vitellogenesis when compared to females
in advanced secondary vitellogenesis also indicates a
capital-breeding strategy (Bonnet et al., 1998), where
the consumption of lipidic energy sources occurs along
Fig. 2. Monthly variation in diameter (mm) of the largest follicles
(black circles) and egg (white circles) of Oxyrhopus rhombifer from
the southern Brazilian coast (Rio Grande do Sul state). e hori-
zontal line indicates size from which follicles were considered as
being in secondary vitellogenesis (secondary follicles).
147
Notes on sexual dimorphism, diet and reproduction of the false coral snake
the reproductive cycle (Almeida-Santos et al., 2014). e
only data on real fecundity (three oviductal eggs) showed
a clutch size smaller than those observed in O. rhombifer
from other regions (four to 17; Pontes and Di-Bernardo,
1988; Yanosky et al., 1996; Gallardo and Scrocchi, 2006;
Gaiarsa et al., 2013), but within the clutch size variation
found for O. guibei (three to 20; Pizzato and Marques,
2002) and O. trigeminus (one to 11; Alencar et al., 2012).
Sampling and examination on a greater number of
females and histological analyses of male gonads, already
in progress, will soon allow a more profound understand-
ing of O. rhombifer reproductive biology in the southern
Brazilian coast.
ACKNOWLEDGMENTS
We thank: CAPES (Coordenação de Aperfeiçoamen-
to de Pessoal de Nível Superior) for the postdoctoral fel-
lowship granted to the rst author; Samara Arsego, Omar
M. Entiauspe-Neto, Victor H. S. Teixeira, Ruth A. Regnet,
Melise L. Silveira, Rafael A. Porciuncula and Franck L.
Silveira for help in eldwork and laboratory procedures;
Rebecca Alves and Omar M. Entiauspe-Neto for language
review; and ICMBio/SISBio environmental agency for the
permission to transportation, collection and euthanasia
(proc. 43658). All procedures adopted are in accordance
with guidelines from institutional committee on ethics in
the use of animals for research (CEUA/FURG).
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APPENDIX
Specimens examined and deposited in the herpeto-
logical collection of Universidade Federal do Rio Grande
(CHFURG).
Oxyrhopus rhombifer: Brasil: Rio Grande do Sul: Pal-
mares do Sul (CHFURG 1267, 2548); Tavares (CHFURG
4320, 4321); Rio Grande, Quinta (CHFURG 2015),
Parque Marinha (CHFURG 833, 4580), Vila Carreiros
(CHFURG 2540, 2963), Distrito Industrial (CHFURG
1313, 1314, 1704, 1846, 1851, 1886, 1888, 1899, 1901,
1904, 1906, 1907, 1908, 1909, 1915, 1959, 1961, 1962,
2385, 3156, 3328, 4561, 5070, 5078, 5243), Senandes
(CHFURG 832), Área de Proteção Ambiental da Lagoa
Verde (CHFURG 1926, 1963, 1964, 1965, 2975, 3436),
Cassino (CHFURG 1120, 1900, 1902, 1905, 3239, 4570,
4582, 4583, 5169, 5170, 5171, 5172, 5174, 5175, 5176,
5177, 5178, 5276, 5404, 5957, 5958, 5959, 5960, 5961,
5962, 5963, 5964), Barra (CHFURG 1910, 3076, 3078,
3079, 3090, 3208, 3274, 3328, 3329, 4419, 4444, 4567,
4578, 4579, 4581, 4584, 4671, 4680, 4687, 4688, 4789,
4790, 4820, 4891, 4902, 4918, 4920, 4921, 5071, 5072,
5073, 5074, 5075, 5076, 5077, 5078, 5079, 5080, 5081,
5082, 5083, 5173, 5201, 5238, 5239, 5240, 5241, 5242,
5243, 5244, 5245, 5246, 5247, 5249, 5250, 5285, 5633,
5966), Estação Ecológica do Taim (CHFURG 1500); San-
ta Vitória do Palmar (CHFURG 5376).
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