Zootaxa, A shallow water population of Pronotogrammus

Zootaxa 2228: 29–42 (2009)
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ISSN 1175-5326 (print edition)
Article
Copyright © 2009 · Magnolia Press
ZOOTAXA
ISSN 1175-5334 (online edition)
A shallow water population of Pronotogrammus martinicensis (Guichenot, 1868)
(Teleostei: Serranidae: Anthiinae) from South-western Atlantic, Brazil
ALFREDO CARVALHO-FILHO1,4, CARLOS E. L.FERREIRA2 & MATTHEW CRAIG3
1
Fish Bizz Ltda, R. D. Maria Garcez, 39, Pinheiros, São Paulo, SP, Brazil, 05424-070
Lab. de Ecologia e Conservação de Ambientes Recifais, Universidade Federal Fluminense (UFF) Departamento de Biologia
Marinha. C.P. 100644, Niterói-RJ, Brazil, 24001-970
3
Department of Marine Sciences, University of Puerto Rico, Mayagüez, P.O. 9000, Mayagüez, PR 00683
4
Corresponding author. E-mail: [email protected]
2
Abstract
A population of Pronotogrammus martinicensis (Guichenot, 1868) is described and recognized as a unique shallowwater variation of the species from the Brazilian South-Eastern coast, based on genetic, morphologic and ecological data.
It is distinguished from the deep water population by its smaller eye, longer snout, shorter pectoral-fin, color of the
adults, and habitat depth.
Key words: Habitat depth, coloration, speciation, genomic DNA, Anthias duplicidentatus
Resumo
Uma população de águas rasas da costa Sudeste do Brasil de Pronotogrammus martinicensis (Guichenot, 1868) é
descrita e reconhecida como sendo uma variação única da espécie, baseada em dados genéticos, morfológicos e
ecológicos. Distingue-se da população de águas profundas pelo tamanho menor do olho e do nono raio superior da
nadadeira peitoral, pelo maior focinho, pela coloração dos adultos e profundidade de habitat.
Introduction
The groupers and seabasses are an ecologically and economically important part of tropical and sub-tropical
reef fish communities. While they have long been thought to share close phylogenetic affinities, it has been
recently proposed to split the family Serranidae (which included both groupers and seabasses) into two
families: the Serranidae (seabasses and basslets) and Epinephelidae (groupers) (Craig & Hastings, 2007;
Smith & Craig, 2007). The serranid sub-family Anthiinae is composed of marine fishes from tropical,
subtropical, and temperate waters, with about 25 genera and 200 species, several of them recently described
and other species awaiting description (W. D. Anderson, Jr., per. com.). The Atlantic and eastern Pacific
members of this sub-family are currently under study by Anderson & Heemstra (manuscript in preparation).
In Brazilian waters there are at least six species of Anthiinae in three genera: Anthias (4 species), Hemanthias
(1) and Pronotogrammus (1) (Moura & Menezes, 2003); the latter genus being represented by
Pronotogrammus martinicensis (Guichenot, 1868), which inhabits depths bellow 65 meters (Anderson &
Heesmtra, 1980).
While scuba-diving off Ilha Rasa in 2002, at the entrance of Guanabara Bay, Rio de Janeiro, Brazil, the
first author noticed a loose aggregation of an anthiine species in shallow water (18 to 22 meters deep). Some
Accepted by L. Rocha: 18 Aug. 2009; published: 11 Sept. 2009
29
12 fishes were swimming among the rocks, alone or in pairs, two of them much smaller than the others; the
larger individuals were about 15 to 18 cm long, the smaller two were roughly half that length. When asked,
local fishermen and scuba-divers reported that the fish were often observed off the island, sometimes feeding
in the water column at depths between 3 and 5 meters. Photographed underwater (FIG 1), this form resembled
very much Pronotogrammus martinicensis in all aspects, but two: the color of the adult and the shallow water
habitat.
FIGURE 1. The shallow-water morph of Pronotogrammus martinicensis at Ilha Rasa, Rio de Janeiro, about 120 mm, 12
m deep. By A. Carvalho-Filho.
With aroused curiosity because of those differences, the first author searched for more information about
the “língua-de-lixa” (“sand-paper tongue”, as called by local fishermen), not only in the literature and on the
internet, but also in museums and through the Brazilian ichthyology brotherhood. Soon, the second author
reported that he often observed the same anthiine off Arraial do Cabo, and Cabo Frio (both beach-towns in
Rio de Janeiro - 23°S; 42°W); from the same place Ary Amarante and Osmar Luiz Jr. took fine pictures of it
(FIG. 2–3); João Luiz Gasparini reported sightings from Escalvada Island (a small island 10 kilometers off
Guarapari, Espírito Santo state - 20°40S; 40°22W); and Osmar Luiz Jr. also reported it from the Laje de
Santos (24º15´S; 46º10´W), a small egg-shaped island, 36 km off the city of Santos, São Paulo State. Finally,
a preserved specimen was located in the Museu de Zoologia da Universidade de São Paulo (MZUSP 47132)
collected in less than 10 meters depth, on June 1994 at Alcatrazes Island. All of the above specimens were
collected or observed in less than 40 meters depth and, as a rule, had a saddle-like dark brown to reddish
blotch under the dorsal fin. The map in FIG.4 shows the localities where the shallow-water morph has been
observed, collected, or photographed.
Given the uncertainty of the specific status of this unique eco-morph of P. martinicensis, we employed
both traditional morphological comparisons of museum specimens and genetic comparison of freshly
collected tissues. While no diagnostic differences were noted in the genetic analysis, morphological
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CARVALHO-FILHO ET AL.
comparisons of specimens collected from shallow and deep water (FIG. 5), showed some morphometric and
color differences that are herein reported as distinguishing a unique shallow-water population of the species.
FIGURE 2. Shallow-water morph of Pronotogrammus martinicensis, male displaying breeding colors. Arraial do Cabo,
Rio de Janeiro, about 120 mm, 25 m deep. By A. Amarante.
FIGURE 3. Shallow-water morph of Pronotogrammus martinicensis, small mixed group. Arraial do Cabo, Rio de
Janeiro, about 70–100 mm, 25 m deep. By A. Amarante.
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FIGURE 4. Map of the sites where the shallow- water morph of Pronotogrammus martinicensis, was observed,
collected or photographed: 1, Laje de Santos; 2, Ilha de Alcatrazes; 3, Ilha Rasa; 4, Arraial do Cabo; and 5, Ilha
Escalvada.
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FIGURE 5. Shallow-water morph (above) and deep-water morph (below) of Pronotogrammus martinicensis. Both
preserved in MZUSP (47132 and 11768). Note the smaller eye and the saddle-like blotch of the shallow-water morph.
Materials and methods
Genetic analysis
Tissue samples were dried and stored at ambient temperature. Total genomic DNA was isolated with the
DNEasy isolation kit (Qiagen Inc.) following manufacturer’s protocols. Extracted DNA was frozen in TE
buffer and archived at -20°C. An approximately 700 base pair fragment of mitochondrial cytochrome b was
amplified using the primers 5’-GTGACTTGAAAAACCACCGTTG-3’ and 5’AATAGGAAGTATCATTCGGGTTTGATG-3’, designed by Song et al. (1998) and Taberlet et al. (1992),
respectively. A 450bp fragment of the mitochondrial 12S rRNA gene was also amplified using the primers 5’AAACTGGGATTAGATACCCCACTAT-3’ and 5’-GAGGGTGACGGGCGGTGTGT-3’ designed by
Palumbi (1996).
Polymerase chain reaction (PCR) amplification mix consisted of BioMixRed (Bioline, USA) with the
addition of 10pmol of each primer and 10-100ng DNA template. PCR reactions utilized the following cycling
parameters: an initial denaturing step at 94°C for 2 min, then 35 cycles of amplification (30s of denaturation
at 94°C, 30s of annealing at 50°C, and 45s extension at 72°C), and a final hold at room temperature. Excess
oligonucleotide primers were removed through incubation of PCR product with exonuclease I and calf
intestine alkaline phosphatase (ExoCIAP). Sequencing reactions with fluorescently-labeled dideoxy
terminators were performed according to manufacturer’s recommendations, and analyzed with an ABI 3100
Genetic Analyzer (Applied Biosystems, Inc., Foster City CA) at the Hawaii Institute of Marine Biology
Sequencing Core Facility.
Morphological analysis
Counts and measurements were made following Anderson & Heemstra (1980), except as noted below.
Measurements were made with digital calipers to nearest 0.1 mm. Length of base of anal-fin was measured
from the insertion of the first spine to the insertion of the last soft ray.
The following abbreviations are used: MNRJ (Museu Nacional do Rio de Janeiro, Rio de Janeiro, Brazil);
MZUSP (Museu de Zoologia da Universidade de São Paulo, São Paulo, Brazil); ZUEC (Museu de História
Natural de Universidades Estadual de Campinas – UNICAMP); UFF (Universidade Federal Fluminense).
Of the 22 shallow-water specimens, 21 were recently collected (2005–2007) and of those 10 were fixed
with formalin and stored in ethyl alcohol, and 11 fixed with ethyl alcohol for genetic comparisons. Samples
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for genetic analysis of the deep-water population were taken from preserved specimens deposited in MZUSP
(61) and MNRJ (1), of which we examined 30 specimens, listed below. The preserved specimens were
examined at the following institutions:
Deep-water morph
MZUSP 13877 (1: 114.2 mm SL), oceanographic research vessel W. Besnard, Station 2218 (24o06’S,
43o41’W), 143–154 m, 23 February 1975; MZUSP 11770 (1: 100.2 mm SL), oceanographic research vessel
W. Besnard, Station 368 (31o22’S, 49o 42’W), 300 m, 20 August 1968; MZUSP 11768 (1: 98.3 mm SL)
oceanographic research vessel W. Besnard, Station 293 (30o06’S, 48o56’W), 133 m, 21 June 1968; MZUSP
11779 (1: 77.2 mm SL) oceanographic research vessel W. Besnard, Station 1006 (22o46’S, 41o15’W),67 m, 24
May 1970; MZUSP 11787 (1: 130.9 mm SL) oceanographic research vessel W. Besnard, Station 1156
(24o00’S, 43o52’W), 131 m, 10 August 1970, coll. J.L. Figueiredo & A.V. Boffi; MZUSP 11788 (1: 68.4 mm
SL) oceanographic research vessel W. Besnard, Station 1721 (31o14’S, 49o35’W), 177 m, 10 April 1972, coll.
G.Q. Benvegnú; MZUSP 86632 (1: 115.3 mm SL) oceanographic research vessel Atlântico Sul, launch 138
(32o02’13”S, 50o11’08”W), 158 m, 23 August 2002, coll. Projeto Revizee Score Sul; MZUSP 86437 (9: 94.6
– 112.3 mm SL) oceanographic research vessel Soloncy Moura, Station 1244 (23o53’41”S, 43o11’58”W), 25
April 2002, coll. Projeto Revizee Score Sul; MZUSP 80762 (2: 172.4 and 180.0 mm SL) oceanographic
research vessel Atlântico Sul, Station 218 (30o45’24”S, 48o46’05”W), 983 m, 04 May 1997, coll. Projeto
Revizee Score Sul; MZUSP 11771-11778 (8: 77.4–126.6 mm SL) oceanographic research vessel W. Besnard,
Station 1005 (22o59’S, 41o06’W), 87–92 m, 24 May 1970; MZUSP 13884 (1: 119.8 mm SL) oceanographic
research vessel W. Besnard, Station 547 (30o48’S, 49o18’W), 153–155 m, 07 March 1969; MZUSP 1389113892 (2: 108.2–111.1 mm SL) oceanographic research vessel W. Besnard, Station 547 (30o48’S, 49o18’W),
153–155 m, 07 March 1969; MNRJ 3029 (1: 118.3 mm SL) no data of collecting site, 14 December 1911,
coll. Companhia de Pesca.
Shallow-water morph
MZUSP 47132 (1: 95.3 mm SL) Arquipélago dos Alcatrazes, 24o06´S; 45 o42´W, São Sebastião, São
Paulo, 10–12 June 1994, coll. R.L. Moura; ZUEC 6333 (3: 96.3–123.4 mm SL) Ilha de Cabo Frio, Arraial do
Cabo, 23°S; 42°W, Rio de Janeiro, 20 December 2005, coll. C.E.L. Ferreira; MZUSP 100154(4: 76.3–120.2
mm SL) Ilha de Cabo Frio, Arraial do Cabo, 23°S; 42°W, Rio de Janeiro, 20 December 2005, coll. C.E.L.
Ferreira; UFF – LBRP 170 (4: 88.2–121.3 mm SL) Ilha de Cabo Frio, Arraial do Cabo, 23°S; 42°W, Rio de
Janeiro, 10–14 January 2006, coll. C.E.L. Ferreira; MNRJ 2233 (3: 80.1–134.2 mm SL) Ilha de Cabo Frio,
Arraial do Cabo, 23°S; 42°W, Rio de Janeiro, 10–14 January 2006, coll. C.E.L. Ferreira.
Results and discussion
Comparisons between the two morphs
Genetics: The sequences for the 12S gene were invariant between the deep and shallow water morph.
The cytocrhome b sequences showed some variation (~0.5%) but the variation did not correlate with
collection depth. These results indicate that the samples are from color morphs of a single species.
Morphometric characters: The analysis of the data presented in Table 1 show that the shallow-water
form differs in several morphometric characters from the deep-water morph. The highlights of these
differences, in rounded percentages, are:
1. The horizontal diameter of the eye is consistently smaller in the shallow-water morph, within the range
of 83% to 122% of the snout length, compared with 163% to 200% of deep-water morph; 22% to 32%
(mean=25.5%) of head length in shallow-water morph against 31% to 40% (mean=34.4%) in deep-water
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morph; 7% to 10% in standard length (mean=8.6%) in shallow-water morph, compared to10% to 13%
(mean=11.4%) in deep-water morph.
2. The snout is longer in the shallow-water morph when compared with the deep-water morph, as follows:
21 to 27% in head length (mean= 24.4%), against 18% to 23% (mean=19.7%); 7 to 9% (mean=8.2%) in
standard length, compared with 6 to 7% (mean=6.5%).
3. The pectoral-fin is usually shorter in the shallow-water morph than in the deep-water morph: often it
does not reach a vertical through the base of the third dorsal-fin ray (only 3 specimens of 22) nor the first analfin spine (4 of 22); in the deep-water morph it usually reaches to or beyond a vertical through the base of the
third dorsal-fin ray (only 3 of 21 specimens just to the base of the second dorsal fin ray) and the first anal-fin
spine (all but one of 21 specimens). Also, when compared to standard length and head, it is consistently
shorter: 26 to 33% of standard length (mean = 29.3%) in the shallow-water morph, against 30 to 36% (mean =
32.8%) in the deep-water morph; 74 to 100% of head length (mean = 87.2%) in the shallow-water morph,
compared with 85 to 120% (mean = 99.0%) in the deep-water morph.
TABLE 1. Selected counts and measurements of Pronotogrammus martinicensis. (TS), five Type-specimens from
Anderson & Heemstra (1980); SW(A), 21 shallow-water morph specimens recently collected (2005–2007) in Arraial do
Cabo, Rio de Janeiro; SW(B), one shallow-water morph preserved specimen (MZUSP 47132) collected in Alcatrazes
Island, São Paulo,1994; DW(A), 30 deep-water morph preserved specimens of MZUSP (see list below); DW(B), one
deep-water morph preserved specimen (MNRJ 3029) of unknown locality,1911; DW(C), 73 deep-water morph
specimens from the western Atlantic examined by Anderson & Heemstra (1980). Some of the data for DW(C) provided
by W. D. Anderson, Jr., August 2008. Standard lengths are in mm and the other measurements in thousandths of standard
length. N.D. = no data.
Character
TS
SW(A)
SW(B)
DW(A)
DW(B)
DW(C)
Dorsal fin
X,15
X-XI*,15
X,15
X,15–16
X,15
X,13–16
Anal fin
III,7
III,7–8
III,7
III,7
III,7
III,7–8
Pectoral fin
17
15*–17
16
16–18
16
16–18
Upper gillrakers
11
11–13
12
11–13
12
09–13
Lower gillrakers
27
22*–26
24
22*–25
24
24–29
Total gillrakers
36–38
33*–39
36
33*–38
36
34–41
Lateral line pores
37–40
37–41
38
36–40
38
35–41
Caudal peduncle scales
19–21
18–20
17*
17*–19
18
18–22
SL Range (mm)
65–97
67–134
95
78–121
118
16–128
Head length
332–352
319–358
347
297–358
331
312–426
Snout length
54–67
71–91
95*
61–73
59
53–93
Eye (orbit) diameter
107–123
73*–104
95
103–129
102
86–155
Body depth
331–366
395–439*
421
359–409
407
327–423
Predorsal length
324–344
299–345
326
310–365
339
N.D.
Preanal length
632–678
609–703
674
628–709
661
N.D.
Dorsal fin base length
N.D.
592–667
653
570–664
585
N.D.
Anal fin base length
N.D.
171–205
189
175–218
186
N.D.
Pelvic fin length
N.D.
263*–317
263*
273–323
288
250–351
Pectoral fin length
N.D.
257*–330
326
296–356
322
305–396
a
* Counts or proportions recorded for the first time. Concerning the dorsal fin spines one specimen of the shallow-water
morph had 11. The frequencies of other counts are presented in Tables 2 to 4.
(a) Only one specimen of the shallow-water morph, an immature (67 mm SL), had orbit diameter over 100 thousandths
of SL, the remaining between 73–96 thousandths of SL.
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TABLE 2. Frequency of pectoral fin rays.
15
16
17
18
SW (A+B = 22 )
02
16
04
--
DW (A+B = 31 )
--
12
17
02
TABLE 3. Frequency of lower gillrakers, including rudiments.
22
23
24
25
26
SW (A+B = 22 )
03
05
08
04
02
DW (A+B = 31)
06
09
12
04
--
TABLE 4. Frequency of caudal peduncle scales.
17
18
19
20
SW (A+B = 22 )
01
11
09
01
DW (A+B = 31 )
16
07
08
--
Data for 73 specimens from the western Atlantic examined by Anderson and Heemstra (W. D. Anderson,
Jr., pers. comm.) are as follows: horizontal diameter of orbit: 8.6 to 15.5 % SL; length of snout: 5.3 to 9.3 %
SL; pectoral fin length: 30.5 to 39.6% SL. These measurements show some differences when compared to the
data of the examined deep-water morph specimens from Brazil, and overlap most of the measurements taken
of the shallow-water morph Brazilian specimens.
Coloration: Adult specimens from shallow-water usually display a conspicuous large saddle-like blotch
under the base of the spinous dorsal fin from the 4th to the 8th or 9th spines that reaches the center of the body,
its lower end usually hidden by the pectoral fin. This blotch varies from blackish to bright red, and may be
greenish, reddish, brown or even a mix of these colors. The young also have the same blotch, but usually
darker, brown to black. In the larger individuals, the blotch does not have its borders very well defined, where
some green-yellowish cast is noted. The bright red phase might be related to reproductive behavior of males,
when the anal and pelvic fins, as well as the belly, are bright pale blue (Paul Thurman, pers. com.). According
to Colin (1974) and Michael (1998), the deep-water morph also has the saddle-like blotch, usually brown, but
only in the young (< 50 mm SL).
A color character of the deep-water population is the conspicuous, irregular, bright golden-yellowish lines
on anterior part of the body, upper head and dorsum, sometimes forming a square blotch in mid-body, partially
hidden by the pectoral fin rays (FIG. 6). The shallow-water morph usually lacks these lines: of all specimens
observed underwater and all photographs studied, only one showed a similar, even if faded, pattern. On the
other hand, the deep-water morph apparently does not show the magenta coloration, as observed by William
D. Anderson, Jr, in a personal comment after examining some shallow-water specimens: “I do not recall ever
seeing on any specimens of P. martinicensis the magenta (reddish purple) that is prominent on the head,
predorsal area, and dorsal fin of the specimens that you sent”.
Depth and habitat: Habitat segregation by morphotype varies not only in Brazil, but throughout its
range. The deep water morph has been reported at depths of 65 to 610 meters (Colin, 1974; Anderson &
Heemstra, 1980; Figueiredo & Menezes, 1980; Parker & Ross, 1986; Robins & Ray, 1986; Dennis & Bright,
1988; Bullock & Smith, 1991; Cervigón, 1991; Cervigón et al., 1993; Hoese & Moore, 1998; Michael, 1998;
Smith-Vaniz, Collette & Luckhurst, 1999; Figueiredo et al., 2002; Heemstra, Anderson & Lobel, 2003). On
the other hand, no shallow-water specimen has been reported from waters deeper than 40 meters, but they are
often observed between 8 and 30 meters (Table 5).
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TABLE 5. Depth of sightings, photographing or collecting of shallow-water specimens. Small group: 2 to 5 specimens;
Large group: more than 6 specimens.
Observer
Site
Depth
Date
Remark 1
Remark 2
Carvalho- Filho
Ilha Rasa, RJ
12 to 15 meters
March 2002
Photographed
Large group
Carvalho- Filho
Ilha Rasa, RJ
8 to 12 meters
July 2004
Photographed
Small group
C. E. L. Ferreira
Arraial do Cabo, RJ
10 to 35 meters
Several times
Observed
Large group
C. E. L. Ferreira
Arraial do Cabo, RJ
15 to 30 meters
September 2004
Collected
Large group
J. L. Gasparini
Escalvada Island, ES
25 meters
Several times
Observed
One specimen
Carvalho- Filho
Escalvada Island, ES
26 meters
October 2002
Observed
One specimen
Osmar J. Luis Jr.
Laje de Santos, SP
25 to 40 meters
Several times
Observed
Small group
C. E. L. Ferreira
Arraial do Cabo, RJ
12 to 30 meters
December 2005/
Jan. 2006
Collected
Large group
Carlos Rangel
Arraial do Cabo
12 to 30 meters
December 2005
Photographed
Large group
Rodrigo Moura
Ilha de Alcatrazes, SP
8 to 10 meters
June 1994
Collected
One Specimen
Ary Amarante
Arraial do Cabo
25 meters
Several Times
Photographed
Large group
These fishes were observed close to rocky outcrops or walls, as well as in shipwrecks.
FIGURE 6. Deep-water morph of Pronotogrammus martinicensis, from Southern Florida, collected between 200 and
250 m deep. By Scott W. Michael.
At the MZUSP and MNRJ, 61 Pronotogrammus specimens were examined and all but the shallow-water
collected off Alcatrazes Island came from waters deeper than 60 meters and were identified as the deep-water
morph. Several of the specimens were caught in the 1960s and 1970s but many others were collected in the
2000s.
It is noteworthy that no shallow-water specimen has been collected in Brazilian waters in depths greater
than 40 meters, despite the huge effort made by several oceanographic surveys during the last 10 years
(REVIZEE Program). The single specimen from Alcatrazes Island is the only one deposited in Brazilian
museums other than those herein examined.
Biology and behavioral notes: The shallow-water population is often observed in groups, small (2–5) to
large (6–20); occasionally a solitary adult is sighted. This morph feeds close to the substrate or in the water
column, no more than a meter away, when plankton is abundant. On only three occasions did we observe them
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far from the bottom (at least 3 meters), picking zooplankton in the water column. Most of the groups seen
were composed of both adults and young, but on some occasions only young were present. Individuals were
not shy and let the observer come within close range, sometimes to within a few centimeters. Curious, they
inspected any stone or debris turned by us and only looked for shelter if abrupt movements were made; they
responded to quick movements by attempting to hide in rock crevices or by just swimming away for deeper
water.
Water temperature preferences for the SW range from 13º to 20ºC; if the water warms, we observed that
they move to greater depths. We never observed P. martinicensis associated with any other fish species when
close to the substrate, but when foraging in the water column it might be joined by other plankton-feeders like
Clepticus brasiliensis and Chromis multilineata. On one occasion, related by J.L. Gasparini, a pair was
observed with a huge loose school of Chromis multilineata in open water.
Underwater observations revealed that the shallow-water morph is a planktivore, mostly acting as a
picker. Analysis of stomach contents of 18 specimens showed that adult males (8) ingested fish larvae and
eggs, copepods, decapod larvae and other planktonic crustaceans; in six of the adult females, the diet also
included fish scales, some apparently of their own species (FIG. 7); to our knowledge, this is the first time that
fish scales have been reported as part of the diet of Pronotogrammus martinicensis.
FIGURE 7. Scales in stomach content of six females of the shallow-water morph of Pronotogrammus martinicensis,
from Arraial do Cabo, Rio de Janeiro.
Protogynous hermaphroditism has been reported for this species by Coleman (1981). Data from the
present study agree with that report: 8 specimens less than 100 mm SL were females, one a transitional (96
mm SL) and all over 100 mm SL were males (12). The spawning period seems to begin in early spring in the
southern hemisphere (September) and end around March; none of the females collected after March were ripe,
but seven collected between October and March had tumescent bellies, with eggs being exuded with very little
pressure.
Miranda-Ribeiro´s Anthias duplicidentatus:
When we started to work with the shallow-water population, our first impression was that it could be an
undescribed species, but the color and the apparently much smaller eye lead us to conclude that we were
dealing with Miranda-Ribeiro´s Anthias duplicidentatus (FIG. 8). This species was described from the same
locality where we first photographed the shallow-water morph (Ilha Rasa, Rio de Janeiro) and even though the
data are scarce and the holotype missing, the picture of it in Miranda-Ribeiro´s work is remarkably similar to
ours´. Years ago, Anthias duplicidentatus was placed in the synonymy of P. martinicensis by Anderson &
Heemstra (1980), because:
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1. Of the absence of a type to examine, Miranda-Ribeiro’s holotype was apparently lost.
2. Of the four anthiine species known to occur in Brazilian waters, three could be eliminated from
consideration; the only species fitting the original description of Anthias duplicidentatus (Miranda Ribeiro,
1903) was Pronotogrammus martinicensis.
Thus, we agree with Anderson & Heemstra in their assertion. Only after their study was published did the
shallow-water morph turn up in the MZUSP collection. If a shallow-water specimen had been available at the
time Anderson & Heemstra wrote their paper, it would have cast doubts on their synonymy and, at least, have
been noted as a different morph, if not redescribed under Miranda-Ribeiro´s specific name. Moura (2003)
followed Anderson & Heemstra and identified MZUSP 47132, the only specimen of the shallow-water morph
ever deposited in a Zoological Museum until now, as P. martinicensis.
FIGURE 8. The main reason for Miranda-Ribeiro´s name for the shallow-water morph: duplicidentatus, “doubletoothed”.
Conclusions
Several fish species have been described or revalidated in the last 10 years from Brazilian marine waters
(Moura et al., 2001; Rocha & Rosa, 2001; Rocha, 2004; Sampaio et al., 2004; Santos et al., 2004; Guimarães
& Bacelar, 2002; Gasparini et al., 2003; Burgess, 2001; Feitoza, 2002; Heemstra, 2008; Luis-Jr. et al., 2009);
for a complete update from 1999 to 2009, see Carvalho-Filho et al. (in press).
The western North Atlantic and the western South Atlantic, once thought to have many of the same
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39
shallow water reef species, are now known to have more distinct and separate ichthyofaunal assemblages than
previously thought (Floeter et al., 2008). The Amazon plume is the main filter driving these patterns (Rocha,
2003).
Several authors reported that Pronotogrammus martinicensis lives in rocky and coralline environments
from 55 to 230 meters deep (Colin, 1974; Anderson & Heemstra, 1980; Figueiredo & Menezes, 1980; Parker
& Ross, 1986; Dennis & Bright, 1988; Bullock & Smith, 1991; Cervigón, 1991; Figueiredo et al., 2002;
McEachran & Fechhelm, 2005; Bernardes et al., 2005). We found no information in the literature concerning
the temperature of those depths, but assume it is not more than 20° C.
The southeastern Brazilian Atlantic shallow-waters offer, among other habitats, rocky reefs, often with
hard and soft coral, and usually subtropical temperatures ranging from 16º to 27ºC (Castro & Miranda, 1998);
in our observations we reported the shallow-water only between 14º to 19ºC, even close to the surface. Thus,
it is possible that, given the adequate conditions of temperature and habitat, the shallow-water population
thrives in this unique region, and is slowly adapting to clear waters, as the smaller eye and the contrasting
brown saddle-like blotch on back suggests.
In this paper we report a case of probable ongoing (incipient) speciation of a deep-water reef fish into a
different shallow-water reef population. To date, the genetic analyses do not support describing the shallowwater population as a new species, even if it could be done based on the morphological and color differences
between the two morphs.
If further studies show stronger evidence of genetic differences, the shallow-water morph should be
revalidated with Miranda-Ribeiro´s name (duplicidentatus). Even if the type is no longer available, the
published photograph, description and capture site of the specimen on which Miranda-Ribeiro based his work,
agree in all aspects with the fresh fishes we collected for this study.
The habitat preference of “duplicidentatus”, compared to that of martinicensis, suggests possible ongoing
ecological speciation, as stated by Wellenreuther et al. (2007) concerning the family Tripterygiidae from New
Zealand waters, and several other similar examples reported by Rocha and Bowen (2008). And this
suggestion leads to another question: What is the role played by the Falkland’s Current upwelling zone in the
speciation of fishes?
Floeter et al. (2008) presented several explanations for the diversity buildup observed in Atlantic reef
fishes, such as diversification within each province; stochastic accretion by means of dispersal between
provinces; and isolation as a result of biogeographical barriers. However, other barriers could also contribute
to speciation, such as water temperature and currents. Recent studies have revealed profound genetic
divergences between populations of the sciaenid Macrodon ancylodon, suggesting the existence of two
distinct species located to the north and south of a zone somewhere between 12º and 20º S, across which there
is no gene flow (Santos et al., 2003, 2006). These authors argue that the two species are adapted to distinct
patterns of water temperature and currents, which have reinforced their genetic differentiation.
We hypothesize that another important factor for speciation in the SW Atlantic could be the influence of
the cold Falklands Current, when depth is evaluated. Flowing from the Southern Convergence, it has its
upwelling zone in the Brazilian coast between northern São Paulo and southern Espírito Santo states (Castro
and Miranda, 1998). This happens in the very same area where the only shallow-water population of P.
martinicensis is reported to date. Thus, adapted to the cold from deeper waters and finding a suitable niche in
the shallows, the morph could be considered a recent “invader” from the deep. Several other deep, cold-water
fish species thrive in the same region: Pinguipes brasilianus, Scorpaena dispar and Acanthistius brasilianus,
to name a few (Luiz-Jr. et al. 2008). Further studies may bring new light to this hypothesis.
Acknowledgments
We are deep in debt with William D. Anderson, Jr., for his review of the manuscript, suggestions, support,
data, advice and help in analyzing specimens, comparing the two morphs, and describing some aspects of the
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shallow-water morph color pattern; also, we are grateful to Sergio Floeter, João Luiz Gasparini, Phil
Heemstra, Carlos Rangel, Robert H. Robins, Luiz Rocha, Ivan Sazima, and Paul Thurman, for their
suggestions and valuable help; to José Lima de Figueiredo, the very first to note the eye differences between
the two morphs, and Naércio Aquino Menezes, for their support and advice; to Ary Amarante and Osmar J.
Luiz-Jr for the fine pictures and suggestions; we also thank the editor and anonymous referees for their
suggestions and critical comments on the manuscript and, finally, to Eliane Morais Pinto buddy for life and at
Rasa and Escalvada islands dives.
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