Boa constrictor, Linnaeus, 1758

Gonzalez, Rodrigo Castellari, Lima, Lorena Corina Bezerra de, Passos, Paulo & Silva, Maria José J., 2024, The good, the bad and the boa: An unexpected new species of a true boa revealed by morphological and molecular evidence, PLoS ONE (e 0298159) 19 (4), pp. 1-29 : 11-20

Boa constrictor – Pontes & Rocha, 2008 (part.) [ 73]; Hynkovà et al. 2009 [ 30] (part.); Reynolds et al., 2014 [ 35] (part.); Wallach et al., 2014 [ 74] (part.); Card et al., 2016 [ 11] (part.); Boa constrictor constrictor –Reynolds & Henderson, 2018 [ 34] (part.); Boa constrictor – Nogueira et al., 2019 [ 9] (part.).

Holotype. Brazil: Rio de Janeiro, Fundação Osório, Rio Comprido, Rua Paula Ramos , 52 (22˚56’03.0"S 43˚12’36.9"W, datum WGS84 ; 93 m above sea level, hereafter asl), MNRJ 27242 ,

adult male, collected by Sergeant Marco Aurélio da Silva on 13 September 2019. The holotype was collected on a tree, while copulating with the paratype MNRJ 27243 .

Paratypes (n = 47). All from Brazil: Alagoas State: Passo do Camaragibe (9˚16’28.5"S, 35˚ 28’04.8"W), 44 m asl, MNRJ 3940 , female, collected by H. Silva at Passo on 18 January 1988; Bahia State: Ilhéus , CEPEC-CEPLAC (14˚45’21.6"S, 39˚13’53.4"W), 58 m asl, CZGB 4862 , female, collected by G.A. Costa on 10 July 1996; Salobrinho, Ilhéus (14˚47’S, 39˚10’W), 29 m asl, MNRJ 6362 , male, collected by S. Rangel in September 1987; Ituaçú (13˚48’S, 41˚18’W), 539.95 m asl, MNRJ 6361 , female, collected by U. Caramaschi & H. Niemeyer on 07 August 1997; Espírito Santo state: Cachoeiro do Itapemerim (20˚51’00.4"S, 41˚06’42.9"W), 35 m asl, IBSP 79063 , female, collector unknown, collected on 10 January 2011; Setiba, Guarapari (20˚ 37’S, 40˚26’W), 20 m asl, MNRJ 23361 , female, collected by T. S. Soares, date of collection unknown and MNRJ 24903 , male, collected by C.F.D. Rocha on 15 November 1999; Reserva Biológica de Comboios, Linhares (19˚33’S, 40˚03’W), 13 m asl, MNRJ 23879 , male, collected by A.P. Almeida on 31 August 2007; São Mateus, Campus CEUNES/ UFES (18˚40’S, 39˚51’W) , 8 m asl, MNRJ 23882 , male, collected by R. S. Bérnils on 15 March 2011; Vitória, Morro da Gamela (20˚17’50.1"S, 40˚18’05.5"W), 17 m asl, MNRJ 9565 , male, collected by J.L. Gasparini, & F. Campagnolli on 14 January 2002; Rio de Janeiro state: Cabo Frio (22˚50’S, 41˚59’W), 6 m asl, MNRJ 22936 , female, collected by R. R. Pinto et al on 03 May 2012; Carapebus, Parque Nacional da Restinga de Jurubatiba (22˚15’S, 41˚39’W), 8 m asl, MNRJ 26802 , male, collected by D.S. Fernandes et al. on the 8 March 2018; Guapimirim (22˚34’S, 43˚0’W) 23 m asl, MNRJ 14238 , female, collector unknown, collected in May 2001; Guapimirim (22˚34’S, 43˚0’W) 23 m asl, MNRJ 14250 , female, collector unknown, collected in May 2001; Iguaba Grande (22˚50’S, 42˚10’W), 37 m asl, MNRJ 17353 , female, date of collection and collector unknown; Itaboraí, Complexo Petroquímico do Rio de Janeiro (COMPERJ) (22˚39’S, 42˚51’W), 21 m asl, MNRJ 25057 , female, collected by J. Creusen on 03 June 2013 and MNRJ 26324 , male, collected on 28 July 2016; Itaboraí (22˚39’S, 42˚51’W), 134 m asl, MNRJ 25413 , female, date of collection and collector unknown; Maricá (22˚55’S, 42˚51’W), 12 m asl, MNRJ 13111 , female, collected by C. L. Prata on 12 May 2005; Itaipu, Niterói (22˚57’S, 43˚02’W), 7 m asl, MNRJ 11205 , female, collected by F. Vieira, J. V. Camargo, & M.A. Gonçalves in May 2004; Pendotiba, Niterói (22˚54’S, 43˚04’W), 111 m asl, MNRJ 23573 , female, collected by M.S.C. Mesquita on 19 January 2013; Niterói (22˚57’S, 43˚02’W), 2 m asl, MNRJ 16922 , female, collected on 17 July 2008, by R . W. Kisling; Nova Iguaçu (22˚42’S, 43˚28’W), 34 m asl, MNRJ 24860 , male, collected by A. Antunes on 13 June 2013; and MNRJ 26213 , female, collector unknown, collected in 2014; Porciúncula, Fazenda Vargem Alegre (20˚58’S, 42˚02’W), 231 m asl, MNRJ 14172 , female, collected by B. Pimenta on 08 March 2006; Rio das Ostras (22˚30’S, 41˚56’W), 31 m asl, MNRJ 10117 , female, collected by D.S. Fernandes et al. on 17 November 2003; Rio de Janeiro, Aeroporto Internacional Tom Jobim (22˚48’S, 43˚15’W), 7 m asl, MNRJ 25952 , female, collected by J. T. Baldine in November 2015 and MNRJ 26350 , female, collector unknown, collected on 9 May 2016; Água Santa (22˚54’19.0"S, 43˚18’26.1"W), 221 m asl, MNRJ 25950 , female, collected by D.S. Fernandes, B. Miranda, & P. Pinna 09 December 2015; Bairro Jardim Botânico, Horto Grotão (22˚57’S, 43˚14’W), 650 m asl, MNRJ 19740 , male, collected by L. Caetano on 13 July 2010; Cosme velho (22˚56’S, 43˚11’W), 18 m asl, MNRJ 19412 , male, collected by J.P. Pombal on 05 April 2010 and MNRJ 19564 , male, collected on 18 May 2010; Del Castilho (22˚52’S 43˚16’W), 22 m asl, MNRJ 25953 , female, collected by R. Baptista on 30 January 2016; Estrada do Rio Morto (23˚00’S, 43˚29’W), 3 m asl, MNRJ 23144 , female, by R. L. Santos, date of collection unknown; Estrada dos Mananciais (22˚55’S, 43˚22’W), 21 m asl, MNRJ 26589 , female, collected by D. B. Santos on 21 April 2017; Ilha do Governador (14˚47’52.6"S, 39˚10’35.3"W), 15 m asl, MNRJ 9449 , female, collector unknown, collected on 21 March 2001 and MNRJ 26585 , female, collected by A. Carneiro on 6 June 2017; Parque Nacional da Tijuca (22˚56’S, 43˚ 17’W), 360 m asl, MNRJ 26886 , female, collected by C. Bueno on 13 March 2018 and MNRJ 27262 , female, same collector, collected on 29 February 2019; Recreio dos Bandeirantes (23˚ 01’S, 43˚28’W), 14 m asl, MNRJ 14200 , female, collected on by J. R. Gomes 27 May 2006 and MNRJ 14201 , female, same collector, collected on 13 May 2006; Serra do Mendanha (22˚50’S, 43˚29’W), 190 m asl, MNRJ 17547 , female, collected by J.A.L. Pontes, date of collection unknown; Rio de Janeiro (22˚57’S, 43˚18’W), 10 m asl, MNRJ 10092 , male, collected by M. Mocelin, date of collection unknown and MNRJ 26796 , male, collector unknown, collected on 22 August 2017; São Francisco de Itabapoana (21˚14’03.0"S, 41˚07’19.0"W), 4 m asl, MBML 2097, male, collected by G.L. Forreque on 10 October 2006; Teresópolis , road BR- 116 km 86.5 (22˚24’S, 42˚58’W), 972 m asl, MNRJ 20700 , female, collector unknown, collected on 25 July 2011; Fundação Osório, Rio Comprido, Rua Paula Ramos , 52 (22˚56’03.0"S 43˚12’36.9"W, WGS84 ), 93 m asl, MNRJ 27243 , adult female, collected by Sgt. Marco Aurélio da Silva on 13 September 2019 [copulating with the holotype MNRJ 27242 ] .

Diagnosis. Boa atlantica sp. nov. can be distinguished from the other congeners by the following unique combination of characters: (i) ventrals 228–243; (ii) subcaudals 47–58 in males, and 31–56 in females; (iii) anterior dorsal scale rows 51–66; (iv) midbody dorsal scale rows 69–90; (v) posterior dorsal scale rows 42–54; (vi) dorsal body spots 17–23; (vii) tail spots 4–6 in males, 2–6 in females; (viii) longitudinal head stripe usually continuous; (ix) head stripe without lateral projections; (x) elliptical, circular or double-oval dorsal interspots; (xi) posterior dorsal interspots not blotched; (xii) no change in dorsal spots towards the tail; (xiii) lateral ocelli dark brown, black or faint reddish, white bordered; (xiv) belly cream with tones of orange, brown and black, scattered of black dots and large groups of black spots; (xv) belly with progressive darkening towards the tail; (xvi) black spots on ventral surface of tail.

Etymology. The species epithet atlantica is a Latin adjective that refers to the Atlantic coast but mainly the Atlantic Forest ecoregion, the homeland of several endemic species, including this new Boa . The preservation of this biome is crucial for conservation, nonetheless, it has been suffering deforestation since the colonial times and only 12% of it remains standing. This situation is under serious threat since the past Brazilian policies lack empathy for conservation issues and seem to foster deforestation even further.

Description of the holotype. MNRJ 27242 ( Figs 3 and 4 ), adult male, SVL 2016 mm, TL 294 mm, head width 27.5 mm, head length 77.9 mm, head height 27.5 mm, distance between eyes 22.9 mm, eye-rostral distance 26.3 mm, eye-mouth distance 8.2 mm, distance between nostrils 12.3 mm, cloacal spur length 7.3/ 6.8 mm, eye height 6.2 mm, eye length 6.5 mm, scales over the preocular stripe 9/7, circumorbitals 17/15, suboculars 1/2, supralabials 22/21, infralabials 26/26, scales between nostrils 6, intrasupraoculars 17, gulars 18/17, dorsal scale rows 64/ 90/50, tail dorsal scale rows 24, preventrals 2, ventrals 245, subcaudals 57. Dorsum of head light brown light brown with discrete dark grey speckles; longitudinal head stripe brown, bordered by dark brown and black, extending from internasal region, breaking in occipital region, and continued up to cervical region; lateral head surface light brown; preocular stripe faded brown; and subocular stripe brown marginally reaching supralabials; postocular stripe dark brown, connecting with first dorsal saddle; some supralabials with dark brown dots; head ventral surface cream, with grey and salmon speckles and black dots; black dots unite forming two larger pairs of infralabial spots, and another three pairs of gular spots; dorsal background light brown progressively darkens towards tail; saddle-shaped dorsal spots, 22, laterally connected to each other, delimiting oval spots, dark brown in 2/3 of body, closer to each other and brownish-red before tail; body, lateral surface 2/3 of body greyish cream with salmon speckles and dark brown ocelli, encircling creamish white spots; last body third cream, with black speckles and irregular black ocelli encircling brick-red spots; ventral body surface cream, with black speckles and larger black blotches united on the sides, almost in alternate way; salmon tones in the midline of belly; dorsal background of tail yellow with five brick-red spots, bor-

dered by black; first three spots with a pair of yellowish ocelli; ventral surface of tail cream,

with alternate black spots among lateral sides of subcaudals not contacting each other.

Hemipenis of the holotype: fully everted and maximally expanded hemipenis renders a

bilobed, non-capitate, and non-calyculated organ; lobes relatively short and sub-cylindrical

with rounded apices, similar size and oriented centrifugally; lobes covered by 6 transversal

flounces on its basal portion; lobes naked from median to apical region; sulcus spermaticus divides on distal portion of organ; sulcus spermaticus branches centrifugally oriented running to tip of lobes; margins of sulcus spermaticus bordered by flounces on basal to most of distal portion of lobes; sulcus spermaticus expanded at apices of lobes; hemipenial body subcylindrical; distal region of hemipenial body defined by transversal series of 4 transversal flounces connected to the sulcus spermaticus; proximal region of hemipenis naked ( Fig 5 ).

Variation. We refer to Tables 3 and S 1 for the synthesis of quantitative variation of Boa

atlantica. Dorsal ground colour from light to pinkish brown; flanks on the first two thirds of

body lighter than dorsum, usually with grey tones; flanks darker on last third of body, usually

with tones of blackish brown; longitudinal head stripe darker than background colouration,

usually with brown; head stripe usually continuous, with a brown blotch of the same colour as

the body; longitudinal head stripe without lateral projections, from internasal region, usually

extending to occipital region; preocular and subocular pigmented with tiny brown dots; last

two stripes lighter than postocular or with same colour; postocular stripe extends to quadrate-

mandibular articulation or connects to first dorsal saddle; usually no gular blotch; dorsal spots

17–23, elliptical, circular or double-oval, not blotched; dorsal spots (13–28 scales long, 8–17

scales wide) light brown to pinkish brown, bordered by brown; posterior dorsal spots do not

change in colour or form; saddles dark brown or black (4–13 scales long), bordered by light

brown to pinkish brown, usually connected to each other; dorsal saddles usually with brown

on last body third; lateral ocelli from dark red, brownish orange to blackish brown, bordered

by cream; belly cream with pinkish tones and black blotches; ventral black blotches progressively increase in number and size towards last body third (= posterior ventral darkening); dorsal tail colour light brown, with 3–6 dorsal brown or black spots, without tail interspots; ventral surface of tail cream with spots generally uniformly black or light brown, bordered by black; cloacal blotch, if present, brown or black.

Sexual secondary dimorphism. Despite the size of the lateral cloacal spurs, which is larger in males than in females, we found evidence of sexual dimorphism in Boa atlantica sp. nov., as confirmed by the MANOVA (F = 1038; p<0.03). The variables in which we found sexual differences were: number of subcaudal rows (F 1,28 = 6.49; p<0.02), number of tail spots (F 1,28 = 6.19; p<0.02), eye-mouth distance (F 1,28 = 4.88; p<0.04), head width (F 1,2 = 4.24; p<0.05). Comparing the central tendency measures and 95% confidence intervals ( Table 4 ), females have broader heads and have larger eye-mouth distance than males, and males have more subcaudals and more tail spots than females. The largest male is from São Fidelis , state of Rio de Janeiro ( IBSP 4620 ) 2114 mm SVL, 290 mm TL; largest female from Floresta da Tijuca , Rio de Janeiro, state of Rio de Janeiro ( MNRJ 26886 ) 1.808 mm SVL, 245 mm TL .

Comparison with South American mainland congeners. Boa atlantica sp. nov. differs from B. constrictor amarali (in parenthesis) by having belly cream with tones of orange, brown

and black, scattered of black dots and large groups of black spots (vs. heavily pigmented with black and brown); posterior dorsal spots not blotched (vs. blotched); and tail interspots absent (vs. fuzzy) ( Fig 6 ). Boa atlantica sp. nov. differs from B. c. constrictor (in parenthesis) by having posterior dorsal saddle spots shape similar to the anterior spots (vs. last dorsal saddles comprising large red polygons different from the anterior in B. c. constrictor ); last lateral ocelli dark brown, black or dark red (vs. blood-red in B. c. constrictor ) ( Fig 6 ); tail spots black (vs. blood-red in B. c. constrictor ) ( Fig 6 ). Boa atlantica sp. nov. differs from B. nebulosa (in parenthesis) by having 228–243 ventrals (vs. 256–269 in B. nebulosa ), 69–90 midbody dorsal scale rows (vs. 59–69 in B. nebulosa ), subocular stripe present (vs. absent in B. nebulosa ), posterior dorsal spots and saddles do not change shape (vs. posterior saddles fuse with lateral ocelli forming brown bands in B. nebulosa ), and belly with shades of brown and black with and randomly distributed black dots, and larger spots concentrated on the paraventral region (vs. belly heavily pigmented with black, brown dots and shades in B. nebulosa ). Boa atlantica sp. nov. differs from B. orophias (in parenthesis) by having 228–243 ventrals (vs. 262–280 in B. orophias ), 44– 59 subcaudals (vs. 63–69 in B. orophias ), 17–23 dorsal spots (vs. 25–30 in B. orophias ), 3–6 tail spots (vs. 6–9 in B. orophias ), longitudinal head stripe usually continuous with regular borders and no lateral projections (vs. longitudinal head stripe usually fragmented, with carved borders and none, two or multiple lateral projections in Boa orophias ). Boa atlantica sp. nov. differs from B. c. occidentalis (in parenthesis) by having 17–23 dorsal spots (vs. 23–29 in B. c. occidentalis ); general colour light to dark brown (vs. dark brown in B. c. occidentalis ); longitudinal head stripe with no lateral projections (vs. two or more projections in B. c. occidentalis ); lateral ocelli dark brown, black or faint reddish (vs. cream in B. c. occidentalis ); belly cream with tones of orange, brown and black, scattered of black dots and large groups of black spots (vs. heavily variegated with brown, yellow, black and white blotches in B. c. occidentalis ); belly progressively darker towards tail (vs. no changes in belly pattern in B. c. occidentalis ); Tail spots black (vs. cream in B. c. occidentalis ) ( Fig 6 ). Additionally, B. occidentalis was always recovered as monophyletic on the molecular analyses, although grouped either as the sister group to the South American representatives or as the sister group to the Mexico + Central America Clade, depending on the markers and the dataset used. We refer to S1–S4 Tables for the meristic and morphometric data on B. atlantica , B. occidentalis , B. orophias and B. nebulosa (respectively).

Hemipenial morphology of the sympatric congeners. The hemipenes of the sympatric Boas are similar in several aspects: organ bilobed, non-capitate, and non-calyculate; lobes relatively short and sub-cylindrical with rounded apices, similar in size and oriented centrifugally; sulcus spermaticus divides on distal portion of hemipenial body below sulk bifurcation; sulcus spermaticus branches centrifugally oriented running to tip of lobes; margins of sulcus spermaticus bordered by flounces on basal to most of distal portion of lobes; sulcus spermaticus expanded at apices of lobes; hemipenial body subcylindrical; proximal region of hemipenis naked.

Nevertheless, the hemipenes of Boa atlantica sp. nov. ( Fig 5 ) differ from those of B. c. constrictor and B. c. amarali (in parentheses) by having lobes bifurcated at about 70–74% of the total length (vs. at 54–79% in B. c. constrictor and 65–76% in B. c. amarali ), lobes covered by 4–6 transversal flounces on its basal portion (vs. 6–8 flounces in B. c. amarali ), lobes naked from median to apical region (vs. with shallow flounces in B. c. constrictor and B. c. amarali ); distal region of hemipenial body with 5–7 transversal flounces connected to the sulcus spermaticus (vs. 4–6 in B. c. constrictor and B. c. amarali ).

Distribution. Boa atlantica sp. nov. is found along the coastal Atlantic Forest along eastern Brazil from Caicó (6˚27’23.2"S 37˚06’05.8"W; Fig 7 and S 5 Table, point 1) in Rio Grande do Norte State to Ilha Grande (23˚08’48.4"S, 44˚13’40.3"W; Fig 7 and S 5 Table, point 156) in Rio de Janeiro State, which is also de westernmost point in the southern distribution. The westernmost point in the northern distribution is Ituaçú (13˚48’26.7"S 41˚18’39.5"W; Fig 7 and S 5 Table point 26) in Bahia State.

In this heterogeneous environment, B. atlantica sp. nov. is found from the sea level up to 906 m a.s.l. ( Fig 7 ).

Figures

Fig 3. Dorsal (A), ventral (B), and lateral (C) views of the head of the holotype of Boa atlantica sp. nov. (MNRJ 27242) from Rio de Janeiro, Atlantic coast of Brazil. https://doi.org/10.1371/journal.pone.0298159.g003

Fig 4. Dorsal (A) and ventral (B) views of the holotype of Boa atlantica sp. nov. (MNRJ 27242) from Rio de Janeiro, Atlantic coast of Brazil. https://doi.org/10.1371/journal.pone.0298159.g004

Fig 5. Sulcate (A) and asulcate (B) sides of hemipenis of the holotype of Boa atlantica sp. nov. (MNRJ 27242) from Rio de Janeiro, Atlantic coast of Brazil. https://doi.org/10.1371/journal.pone.0298159.g005

Fig 6. Pre-cloacal region and tails of mainland South-American boas. B. atlantica sp. nov. (MNRJ 27243): a) superior view, b) lateral view; B. constrictor (USNM 566533): c) superior view, d) lateral view; B. amarali (UFG 134): e) superior view, f) lateral view; B. occidentalis (FML28405): g) superior view, h) lateral view. https://doi.org/10.1371/journal.pone.0298159.g006

Fig 7. Distribution of Boa atlantica sp. nov. based on the examined vouchers and tissue samples. A) Detailment in Rio de Janeiro City, including type locality. B) records in northern Rio de Janeiro and Espírito Santo States, C) records in Rio de Janeiro State. See also S4 Table. https://doi.org/10.1371/journal.pone.0298159.g007

Tables

Table 4. Basic descriptive statistics for the sexual dimorphic characters of Boa atlantica. max = maximum; min = minimum; n = number of samples; SD = standard deviation.

	Sex	Min	max	Mean	SD	n
Head width (mm)	M	22.9	57.6	35.3	8.1	21
	F	29.8	52.7	39.7	6.6	26
Distance Eye-Mouth (mm)	M	3.5	7.4	5.3	1.3	20
	F	4.3	8.8	6.5	1.4	26
Number of subcaudal rows	M	47	58	52.9	2.8	26
	F	31	56	48.0	5.0	25
Number of tail spots	M	4	6	5.0	0.6	26
	F	2	6	4.3	0.8	25
Abbreviations: F = female; M = male.

https://doi.org/10.1371/journal.pone.0298159.t004