Introduction

Materials and methods

Study Site

Madagascar Reef is part of a cluster of three reefs named Sisal Reefs. These reefs are located in the Campeche Bank, a large carbonate platform of gentle slope (Fig. 1) that presents a low topographic complexity that is only increased sporadically by the presence of scattered reefs. Madagascar Reef is located 40 km from the fishing port of Sisal, whose inhabitants exploit its marine resources; however, fishermen from nearby ports, such as Celestun and Progreso, also visit the reef. Its morphology is peculiarly elongated, extending 2.5 km East-West and 130 m North-South in its widest point. The reef rises from sandy plains at 14m of depth to the reef crest at 4 m depth, where the illumination is high and the water current stronger (Zarco-Perelló et al. 2013).

Figure 1.

Madagascar Reef, part of the Sisal Reefs (upper-right magnifying glass), and other reefs and reef systems of the Mexican Atlantic (Modified from Jordán-Dahlgren (2002)).

Data collection

Fish species occurrence was registered during two different surveys. During the first campaign (2007), seven transects of 50 m were deployed and all fishes on sight were photographed along the way for later identification (Fig. 2). The second campaign (2010) focused on cryptic species, which historically have received less attention (MacNeil et al. 2008). In this campaign, six transects of 50 m were deployed and species were counted visually and/or collected using clove oil (eugenol) diluted to 10% with 70% ethanol and sea water (Cunha and Rosa 2006). Collected fishes were preserved in 70% ethanol for later identification in the laboratory. The surveys included areas from the shallow reef crest (5 m) to the deep sandy plains around the reefs (25 m). The taxonomic identification of the species was based on Robins and Ray (1999), Böhlke and Chaplin (1993), McEachran and Fechhelm (1998), McEachran and Fechhelm (2006), Humann and DeLoach (2008). The nomenclature was revised using the Catalog of Fishes (Eschmeyer and Fricke 2013). The order of the species in the list was arranged following Nelson (2006) for the suprageneric categories, while the genera and species were ordered alphabetically. Information about the general geographic distribution of the species was based on Felder and Camp (2009), Carpenter (2002a), Carpenter (2002b) and Colin (2010) for the species of the genus Elacatinus. All the species collected and photographed were registered in the Ichthyology Collection (YUC-PEC-239-01-11) of the Unidad Multidiciplinaria de Docencia e Investigacion Sisal (UMDI-Sisal), a research station of the National Autonomous University of Mexico (UNAM). The list of species found in our field work was complemented with species documented in the M.Sc. thesis work of Martínez de la Portilla (2008) who surveyed Madagascar Reef in 2005.

Figure 2.

Sampling locations on Madagascar Reef. Coordinates in UTM 15N, WGS84.

Discussion

Our study found that the fish fauna of Madagascar Reef consists of 8 orders, 30 families, 43 genera and 54 species. The families with the highest representation were: Serranidae (7), Gobiidae (5), Scaridae (4), Lutjanidae (3), Haemulidae (3) and Pomacanthidae (3) (Table 1). Almost all the species found at Madagascar Reef are distributed generally within the Gulf of Mexico (Felder and Camp 2009). However, Hypoplectrus ecosur was recorded here for the first time in the Gulf of Mexico, although it is possible that previous studies in the region have callected this species and identified as other species within the same genus (Victor 2012). Elacatinus xanthiprora was recorded here for the second time in Mexico, expanding its distribution westwards from Alacaranes Reef (González-Gandara and Arias-González 2001). Sanopus reticulatus, which is endemic to the Yucatan state, was recorded here for the first time at a reef, expanding its distribution westwards from Puerto Progreso (Collette 1983). Additionally, Mycteroperca microlepis, Equetus lanceolatus and Chaetodipterus faber are new species records for the CB reefs.

Table 1. Download as CSV 

Fish species of Madagascar Reef and its distribution on other reefs of the Gulf of Mexico. ID abbreviations: C: collected, Ph: Photograph, Vc: Visual census. Reef abbreviations: TRS: Tuxpan Reef System, Bl: Blanquilla, Me: Medio, Lo: Lobos, Ta: Tanhuijo, En: Enmedio, Tx: Tuxpan; VRS: Veracruz Reef System: dEn: De Enmedio; CB: Campeche Bank: Al: Alacranes, Ac: Arcas, Ar: Arenas, To: Triangulo Oeste, Ma: Madagascar; Mx Carib: Mexican Caribbean. The symbol • means present with no reef specified in the bibliography. References: (1) González-Gándara et al. 2013; (2) Del Moral Flores et al. 2013; (3) Tunnell Jr et al. 2007; (4) González-Gandara and Arias-González 2001; (5) Tuz-Sulub et al. 2006; (6) Taylor and Bright 1973; (7) Martínez de la Portilla 2008; (8) Schmitter-Soto et al. 2000; (9) This work.

Family	Genus and species	Authority	ID	TRS	VRS	CB	Mx Carib	References
Urotrygonidae	Urobatis jamaicensis	(Cuvier, 1816)	Ph	Tx	dEn	Al, Ma	•	1, 2, 4, 8, 9
Muraenidae	Gymnothorax funebris	Ranzani, 1839	Ph	Lo	dEn	Al, To, Ma	•	1, 2, 3, 4, 8, 9
Synodontidae	Synodus sp.		Vc	Lo, Ta, En, Tx	•	Al, Ma	•	1, 2, 4, 7, 8
Batrachoididae	Sanopus reticulatus	Collette, 1983	C			Ma		9
Holocentridae	Holocentrus adscensionis	(Osbeck, 1765)	Ph	Bl, Me, Lo, Ta, En, Tx	dEn	Al, To, Ma	•	1, 2, 3, 4, 8, 9
Scorpaenidae	Scorpaena plumieri	Bloch, 1789	C	Lo, Ta	dEn	Al, To, Ma	•	1, 2, 3, 4, 8, 9
Serranidae	Epinephelus adscensionis	(Osbeck, 1765)	Ph	Bl, Me, Lo, Ta, En, Tx	dEn	Al, Ac, Ar, To, Ma	•	1, 2, 3, 4, 6, 8, 9
	Epinephelus morio	(Valenciennes, 1828)	Ph		•	Al, Ma	•	2, 4, 8, 9
	Hypoplectrus ecosur	(Cuvier, 1828)	Ph			Ma		1, 2, 4, 8, 9
	Mycteroperca bonaci	(Poey, 1860)	Vc	En, Tx	dEn	Al, Ma	•	1, 2, 4, 7, 8
	Mycteroperca microlepis	(Goode & Bean, 1879)	Vc	Ta, En	•	Ma		1, 2, 9
	Mycteroperca venenosa	(Linnaeus, 1758)	Vc		dEn	Al, Ar, Ma	•	2, 3, 4, 5, 6, 7, 8
	Serranus subligarius	(Cope, 1870)	Vc	Ta, En, Tx	dEn	Al, Ma		1, 2, 4, 7
Opistognathidae	Opistognathus aurifrons	(Jordan & Thompson, 1905)	C		dEn	Al, Ma	•	2, 4, 8, 9
Apogonidae	Astrapogon stellatus	(Cope, 1867)	C			Al, Ma	•	4, 8, 9
Echeneidae	Echeneis sp.		Ph	Lo	dEn	Al, Ma	•	1, 2, 4, 8, 9
Carangidae	Carangoides ruber Syn. Caranx ruber	(Bloch, 1793) (Bloch, 1793)	Ph	Bl, Lo, Ta, En, Tx	dEn	Al, Ac, Ar, Ma	•	1, 2, 3, 4, 8, 9
Lutjanidae	Lutjanus apodus	(Walbaum, 1792)	Vc	Bl, Me, Lo, En, Tx	dEn	Al, Ac, Ar, Ma	•	1,2, 3, 4, 7, 8
Haemulidae	Lutjanus griseus	(Linnaeus, 1758)	Ph	Bl, Me, Lo, Ta, En, Tx	dEn	Al, To, Ma	•	1, 2, 3, 4. 8, 9
	Ocyurus chrysurus	(Bloch, 1791)	Ph	Bl, Me, Lo, Ta, En, Tx	dEn	Al, Ac, Ar, Ma	•	1, 2, 3, 4, 8, 9
	Anisotremus virginicus	(Linnaeus, 1758)	Ph	Bl, Me, Lo, Ta, En, Tx	dEn	Al, Ac, Ar, Ma	•	1, 2, 3, 4, 8, 9
	Haemulon aurolineatum	Cuvier, 1830	Ph	Bl, Me, Lo, Ta, En, Tx	dEn	Al, Ac, Ar, Ma	•	1, 2, 3, 4, 8, 9
	Haemulon plumierii	(Lacepède, 1801)	Ph	Bl, Me, Lo, Ta, En, Tx	•	Al, Ac, Ar, Ma	•	1, 2, 3, 4, 7, 8, 9
Sparidae	Calamus sp.		Ph	Bl, Me, Lo, Ta, En, Tx	dEn	Al, Ma	•	1, 2, 4, 8, 9
Scianidae	Equetus lanceolatus	(Linnaeus, 1758)	Ph	Lo, Tx	dEn	Ma	•	1, 2, 4, 8, 9
	Pareques umbrosus	(Jordan & Eigenmann, 1889)	Ph	En	•	Al, Ma	•	1, 2, 4, 8, 9
Chaetodontidae	Chaetodon ocellatus	Bloch, 1787	Ph	Bl, Me, Lo, Ta, En, Tx	dEn	Al, To, Ma	•	1, 2, 3, 4, 7, 8, 9
Pomacanthidae	Holacanthus bermudensis	Goode, 1876	Ph	Bl, Me, Lo, En, Tx	•	Al, Ma	•	1, 2, 4, 8, 9
	Holacanthus ciliaris	(Linnaeus, 1758)	Vc	Bl, Me, Lo, Tx	dEn	Al, Ma	•	1, 2, 4, 7, 8
	Pomacanthus arcuatus	(Linnaeus, 1758)	Ph		dEn	Al, Ma	•	2, 4, 8, 9
Pomacentridae	Abudefduf saxatilis	(Linnaeus 1758)	Ph	Bl, Me, Lo, Ta, En, Tx	dEn	Al, Ac, Ar, To, Ma	•	1, 2, 3, 4, 8, 9
	Stegastes variabilis	(Castelnau, 1855)	Ph	Bl, Me, Lo, Ta, En, Tx	dEn	Al, Ac, Ar, To, Ma	•	1, 2, 3, 4, 8, 9
Kyphosidae	Kyphosus sectatrix	(Linnaeus 1758)	Vc	Bl, Lo, Ta, Tx	dEn	Al, To, Ma	•	1, 2, 3, 4, 7, 8
Labridae	Halichoeres sp.		Vc	Bl, Me, Lo, Ta, En, Tx	dEn	Al, Ac, Ar, To, Ma	•	1, 2, 3, 4, 7, 8
	Lachnolaimus maximus	(Walbaum, 1792)	Ph	Bl, Lo, Tx	dEn	Al, Ma	•	1, 2, 4, 8, 9
	Thalassoma bifasciatum	(Bloch, 1791)	Vc	Bl, Me, Lo, Ta, En, Tx	dEn	Al, Ac, Ar, To, Ma	•	1, 2, 3, 4, 7, 8
Scaridae	Scarus coeruleus	(Edwards, 1771)	Ph	Me, Lo, Ta	dEn	Al, Ac, Ar, Ma	•	1, 2, 3, 4, 8, 9
	Sparisoma aurofrenatum	(Valenciennes, 1840)	Ph	Bl, Me, Lo, Ta, En, Tx	•	Al, Ma	•	1, 2, 4, 8, 9
	Sparisoma rubripinne	(Valenciennes, 1840)	Ph	Bl, Me, Lo, Ta, En, Tx	dEn	Al, To, Ma	•	1, 2, 3, 4, 8, 9
	Sparisoma viride	(Bonnaterre, 1788)	Ph	Bl, Me, Lo, Ta, En, Tx	dEn	Al, Ac, Ar, To, Ma	•	1, 2, 3, 4, 8, 9
Labrisomidae	Malacoctenus triangulatus	Springer, 1959	C	Bl, Me, Lo, Ta, En, Tx	•	Al, Ma	•	1, 2, 4, 8, 9
Blennidae	Parablennius marmoreus	(Poey, 1876)	C	Bl, Me, Lo, En, Tx	dEn	Al, Ma		1, 2, 4, 9
Gobiidae	Coryphopterus dicrus	Böhlke & Robins, 1960	C	Lo	•	Al, Ma	•	1, 2, 4, 8, 9
	Coryphopterus glaucofraenum	Gill, 1863	C	Bl, Me, Lo, Ta, En, Tx	•	Al, Ma	•	1, 2, 4, 8, 9
	Elacatinus oceanops	Jordan, 1904	C, Ph	Me, Lo, Ta, En, Tx	•	Al, Ma	•	1, 2, 4, 8, 9
	Elacatinus xanthiprora	(Böhlke & Robins, 1968)	C			Al, Ma		4, 9
	Tigrigobius macrodon Syn. Elacatinus macrodon Gobiosoma macrodon	(Beebe & Tee-Van, 1928) (Beebe & Tee-Van, 1928) Beebe & Tee-Van, 1928	Vc	Lo		Ma		1, 9
Microdesmidae	Ptereleotris calliura	(Jordan & Gilbert, 1882)	Ph	Tx		Al, Ma		1, 4, 9
Ephippidae	Chaetodipterus faber	(Broussonet, 1782)	Vc	Lo, Ta, Tx	•	Ma	•	1, 2, 7, 8
Acanthuridae	Acanthurus tractus Syn. Acanthurus bahianus	Poey, 1860 Castelnau, 1855	Vc	Bl, Me, Lo, Ta, En, Tx	dEn	Al, Ac, Ar, To, Ma	•	1,2, 3, 4, 7, 8
	Acanthurus coeruleus	Bloch & Schneider, 1801	Ph	Bl, Me, Lo, Ta, En, Tx	dEn	Al, Ac, Ar, To, Ma	•	1, 2, 3, 4, 8, 9
Sphyraenidae	Sphyraena barracuda	(Edwards, 1771)	Ph	Bl, Lo, Ta, En, Tx	dEn	Al, Ma	•	1, 2, 4, 8, 9
Scombridae	Scomberomorus maculatus	(Mitchill, 1815)	Ph		dEn	Al, Ma		2, 4, 9
Monacanthidae	Aluterus scriptus	(Osbeck, 1765)	Ph	Lo, Tx	dEn	Al, Ma	•	1, 2, 4, 8, 9

The species composition found at Madagascar Reef was a mixture of species from other reef systems within the Mexican Atlantic (Figs 3, 4, 5). Among the species found at Madagascar Reef, 40 (74%) are registered for all of the reef systems of the Mexican Atlantic. The remaining 14 species (26%) are absent in at least one reef system. Madagascar Reef shared 45 (83%) species with TRS (González-Gándara et al. 2013), 48 (89%) with VRS (Del Moral Flores et al. 2013), 50 (91%) with Alacranes Reef (González-Gandara and Arias-González 2001), 24 (46%) with Arcas, Arenas and Triangulo Oeste reefs in the CB (Tunnell Jr et al. 2007) and 45 (85%) species with the Mexican Caribbean reefs (Schmitter-Soto et al. 2000) (Table 1, Fig. 6). Mycteroperca microlepis is shared only with the TRS and VRS and Astrapogon stellatus and Hypoplectrus ecosur are only shared with the Caribbean. Finally, Elacatinus xanthiprora is registered only in the CB and Sanopus reticulatus only in Madagascar reef (Table 1).

a

b

c

d

e

f

Figure 3.

Images of some fish species recorded from Madagascar Reef.

a: Aluterus scriptus
b: Lachnolaimus maximus
c: Pomacanthus arcuatus
d: Epinephelus morio
e: Scarus coeruleus
f: Anisotremus virginicus

a

b

c

d

e

f

Figure 4.

Images of some fish species recorded from Madagascar Reef.

a: Scomberomorus maculatus
b: Sphyraena barracuda
c: Gymnothorax funebris
d: Epinephelus adscensionis
e: Holocentrus adscensionis
f: Sparisoma viride and Echeneis sp.

a

b

c

d

e

f

Figure 5.

Images of some fish species recorded from Madagascar Reef.

a: Hypoplectrus ecosur
b: Equetus lanceolatus
c: Chaetodon ocellatus
d: Stegastes variabilis
e: Scorpaena plumieri
f: Haemulon plumierii

Figure 6.

Number of species shared between Madagascar Reef and the reef systems of the Mexican Atlantic. TRS: Tuxpan Reef System; VRS: Veracruz Reef System; CB: Campeche Bank; Mx Carib: Mexican Caribbean. (Suppl. material 1).

The species richness at Madagascar Reef is similar to other reefs in the CB, but lower than richness values reported for reefs in the VRS and TRS (Fig. 7). Of the four reefs in the CB with ichthyological information, three present lower species richness than Madagascar Reef. Cayos Arcas and Arenas have 37 species registered, whereas Triangulos Oeste has 52 (Tunnell Jr et al. 2007). Only Alacranes reef surpasses these numbers with 294 species (González-Gandara and Arias-González 2001). All the reefs in the TRS present higher richness. For example, Medio Reef has the lowest with 83 and Lobos Reef has the highest with 248 species, while each of the remaining reefs have approximately 100 species (González-Gándara et al. 2013). Similarly, Enmedio Reef in the SAV has 145 species (Tunnell Jr et al. 2007).

Figure 7.

Species richness of coral reefs of the Gulf of Mexico and Mexican Caribbean (Mx Carib). Species number by individual reefs (bars) and reef systems (circles). Reef abbreviations: TRS: Tuxpan Reef System, Bl: Blanquilla, Me: Medio, Lo: Lobos, Ta: Tanhuijo, En: Enmedio, Tx: Tuxpan; VRS: Veracruz Reef System: deEn: De Enmedio; CB: Campeche Bank, Mada: Madagascar, Ac: Arcas, An: Arenas, To: Triangulo Oeste, Al: Alacranes. References: TRS: González-Gándara et al. 2013. VRS: Del Moral Flores et al. 2013; Tunnell Jr et al. 2007. CB: Tunnell Jr et al. 2007; Martínez de la Portilla 2008; and this work. Mexican Caribbean: Schmitter-Soto et al. 2000. (Suppl. material 2).

The estimation of the species richness through the species accumulation curve clearly shows that the list of species presented here is not an exhaustive compendium of the species inhabiting this reef and that more species remain undiscovered (Fig. 8). With only three sampling campaigns comprising about 15 surveys (including Martínez de la Portilla (2008)) Madagascar Reef presented about 1/7 of the reef fish species in the Gulf of Mexico (376 species) (Withers and Tunnell Jr 2007). This numbers are lower than other better studied reefs but still quite significant given the low coral cover in the reef (Zarco-Perelló et al. 2013). The implementation of more studies at Madagascar Reef and other reefs in the CB not only would probably increase its species richness, reflecting the fish biodiversity of nearby hotspots such as Alacranes Reef (González-Gandara and Arias-González 2001) and the Caribbean (Schmitter-Soto et al. 2000) but also has the potential to extend distribution ranges of species from the Gulf of Mexico and Caribbean by finding new species records in this region, as was the case in the present study.

Figure 8.

Fish species accumulation curve for Madagascar Reef. Calculated using sample-based incidence data with the software EstimateS v9 (http://purl.oclc.org/estimates) using Eq. 5 in Colwell et al. (2004) and Eq. 17 in Colwell et al. (2012) for rarefaction and Eq. 18 in Colwell et al. 2012Colwell et al. (2012) for extrapolation. Bars represent 95% confidence intervals calculated using Eq. 6 in Colwell et al. (2004) for rarefaction and Eq. 19 in Colwell et al. (2012) for extrapolation. For a full output of the analysis see Suppl. material 3.

Acknowledgements

Author contributions

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