PLoS ONEplosplosonePLoS ONE1932-6203Public Library of ScienceSan Francisco, USA09-PONE-RA-14285R110.1371/journal.pone.0010676Research ArticleEvolutionary BiologyEcology/Community Ecology and BiodiversityEcology/Marine and Freshwater EcologyMarine and Aquatic Sciences/EcologyBiodiversity Assessment of the Fishes of Saba Bank Atoll, Netherlands AntillesFishes of Saba BankWilliamsJeffrey T.1*CarpenterKent E.2Van TassellJames L.3HoetjesPaul4TollerWes5¤aEtnoyerPeter6¤bSmithMichael7Fish Division, Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Suitland, Maryland, United States of AmericaDepartment of Biological Sciences, Old Dominion University, Norfolk, Virginia, United States of AmericaDepartment of Ichthyology, American Museum of Natural History, New York, New York, United States of AmericaDepartment of Environment and Nature, Ministry of Public Health and Social Development, Curaçao, Netherlands AntillesSaba Conservation Foundation, Fort Bay, Saba, Netherlands AntillesHarte Research Institute, Texas A&M University-Corpus Christi, Corpus Christi, Texas, United States of AmericaCenter for Applied Biodiversity Science, Conservation International, Arlington, Virginia, United States of AmericaGratwickeBrianEditorSmithsonian's National Zoological Park, United States of America* E-mail: williamsjt@si.edu
Conceived and designed the experiments: MS. Performed the experiments: JTW KEC JLVT PCH WWT PJE MS. Analyzed the data: JTW KEC JLVT PCH PJE. Wrote the paper: JTW. Wrote portions of the paper: KEC PCH PJE. Helped prepare tables and check species identifications: JLVT. Prepared Fig. 1: PCH.
Current address: MSC Accreditation Program, Accreditation Services International GmbH, Bonn, Germany
Current address: Center for Coastal Environmental Health and Biomolecular Research, National Oceanic and Atmospheric Administration, Charleston, South Carolina, United States of America
Dr. Peter Etnoyer co-authored the Deep Sea News blog with PLoS One editor Dr. Craig McClain 2005–2009. Dr. McClain has recused himself from the Saba Bank Biodiversity Assessment volume for this reason.
2010215201055e106761311200921120102010This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose.
Biodiversity surveys were conducted on Saba Bank, Netherlands Antilles, to assess ichthyofaunal richness and to compare with published surveys of other Caribbean localities. The primary objective was to estimate the total species richness of the Saba Bank ichthyofauna. A variety of sampling techniques was utilized to survey the fish species of both the visually accessible megafauna and the camouflaged and small-sized species comprising the cryptic ichthyofauna.
Based on results presented herein, the number of species known on Saba Bank is increased from 42 previously known species to 270 species. Expected species-accumulation curves demonstrate that the current estimate of species richness of fishes for Saba Bank under represents the actual richness, and our knowledge of the ichthyofauna has not plateaued. The total expected fish-species richness may be somewhere between 320 and 411 species.
The Saba Bank ichthyofaunal assemblage is compared to fish assemblages found elsewhere in the Caribbean. Despite the absence of shallow or emergent shore habitats like mangroves, Saba Bank ranks as having the eighth highest ichthyofaunal richness of surveyed localities in the Greater Caribbean. Some degree of habitat heterogeneity was evident. Fore-reef, patch-reef, and lagoonal habitats were sampled. Fish assemblages were significantly different between habitats. Species richness was highest on the fore reef, but 11 species were found only at lagoonal sites.
A comprehensive, annotated list of the fishes currently known to occur on Saba Bank, Netherland Antilles, is provided and color photographs of freshly collected specimens are presented for 165 of the listed species of Saba Bank fishes to facilitate identification and taxonomic comparison with similar taxa at other localities. Coloration of some species is shown for the first time. Preliminary analysis indicates that at least six undescribed new species were collected during the survey and these are indicated in the annotated list.
The Department of Environment and Nature of the Netherlands Antilles and Conservation International provided funding for this project. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.Introduction
Saba Bank is the largest atoll in the Atlantic Ocean Basin and one of the three largest atolls on earth [1]. Located in the Dutch Windward Islands about 250 km east of Puerto Rico, it is a flat-topped seamount rising 1800 m from the surrounding sea floor. Except for the fact that it does not break the water surface, Saba Bank is a classic atoll consisting of a submerged mountain crowned at the summit with a ring of actively growing coral reefs [2]. Saba Bank is relatively free of the problems that are degrading many Caribbean reef systems, and the few problems it faces include anchoring and abrasion by oil tankers maneuvering off the petroleum transshipment facilities on St. Eustatius, potential petroleum spillage and subsequent use of dispersants, general vessel passage in a zone of high maritime traffic, possible overfishing for certain species, and exploration for petroleum reserves (so far unsuccessful). Saba Bank's fisheries and dive operations are economically significant to the small community on Saba Island (about 1500 residents) that has direct responsibility for its management.
The known fish fauna of Saba Bank prior to our survey consisted of 42 fish species. Most of these species were taken during fishery bottom-trawl surveys on Saba Bank, including two M/V Oregon stations in 1958 and nine stations in 1959, and two trawl hauls taken in 1969 by the R/V Pillsbury. Although four of these trawls were taken on or near the top of Saba Bank, nine were on the deep outer slopes. The habitats sampled during these surveys were restricted to relatively soft-bottom habitats due to the exclusive use of trawling techniques. These trawl samples provided valuable records of fishes living on soft bottoms and on the outer slopes of Saba Bank.
A biodiversity-assessment survey was carried out on Saba Bank during 2006 and 2007, with a major goal being to improve knowledge of the biodiversity on one of the world's most significant, though poorly known, coral-capped seamounts. In an effort to record as many fish species as possible in the short period of time available for the survey, we utilized a variety of fish sampling techniques. These techniques included visual surveys by divers, use of SCUBA to apply ichthyocide (a natural fish toxicant consisting of dried and powdered Derris root - assayed at 7.5% rotenone), hand-line fishing, by-catch from lobster and fish traps taken by local fishermen, and port sampling observations of fish landings. During the surveys, an attempt was made to obtain a photograph documenting the fresh colors of as many species as possible, a tissue sample of each species, and preserved specimen vouchers that have been archived in the National fish collection (USNM) of the National Museum of Natural History (NMNH), Smithsonian Institution (SI). Specimens representing six or more undescribed species and two rare gobies, Pycnomma roosevelti and Psilotris boehlkei, were collected.
The habitats surveyed on the Saba Bank “atoll” during this study are classified as: fore reef, patch reef, lagoonal and Small Bank. Fore-reef areas are located around the outer rim of the submerged atoll. Patch reef is an isolated portion of “reef” situated on the lagoonal (interior) side of the fore reef. Lagoonal is the central portion of the atoll interior to the fore-reefs around the atoll rim and may have a variety of bottom types. Small Bank is a small, independent “seamount-like” structure located off the northwest corner of Saba Bank with its shallowest depth at about 11 m. Depth categories were arbitrarily assigned as shallow (11–24 m), mid-depth (25–34 m), and deep (35–38 m).
The primary goals of the overall biodiversity survey were to provide data and analysis to support designation of Saba Bank as a marine protected area, to support the development of a management plan, and to contribute to a petition to the International Maritime Organization to designate appropriate parts of Saba Bank as a Particularly Sensitive Sea Area.
Results
We occupied fish stations at 25 locations during a rapid assessment (RAP) survey, 2–16 January 2006; including: 20 ichthyocide stations, 12 roving visual surveys, two hook & line stations, and five by-catch stations from lobster traps; two fish-ichthyocide stations were occupied at two additional locations on 20 June 2007 (Figure 1). In 2007, Toller assessed the benthic communities and fish assemblages based in part on 40 visual surveys of the fish fauna at an area on the eastern side of Saba Bank.
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Bathymetric map of Saba Bank with fish stations marked.
Specimens collected during the RAP survey were preserved as vouchers and processed into the fish collection (available online at http://vertebrates.si.edu/fishes/fishes_collections.html) at the NMNH (as many species as possible were also tissue sampled and photographed in the field). Toller collected and preserved vouchers from fishery landings when possible and photographed specimens representing new records. Toller's vouchers were processed into the fish collection at the NMNH and are also available in the online database.
Some species were only taken during fishery bottom trawl surveys by the M/V Oregon (1958, 1959) and the R/V Pillsbury (1969) on Saba Bank. Species represented by voucher specimens in museum collections are included in our comprehensive species list.
A non-metric multidimensional-scaling (MDS) ordination of the 12 rotenone and roving stations based on a Bray-Curtis similarity matrix of incidence data was used to illustrate similarities and differences of fish assemblages found on the four atoll habitat types: fore reef, patch reef, lagoonal, Small Bank (Figure 2). There were significant differences among habitat types (ANOSIM Global R = 0.96, P = 0.001). Differences between fore-reef stations and patch-reef stations were most pronounced (ANOSIM, Pairwise R = 0.92, P = 0.002). Fore-reef assemblages ranged from 39 to 60 species per station while the patch-reef stations had 26 and 32 species. Fore-reef stations were 50% similar to each other, and patch-reef stations were up to 60% similar. Fore-reef assemblages were not significantly different than Small Bank, or the lagoonal habitat (ANOSIM, Pairwise R = 0.973, P = 0.11). Low sample size (one station with 39 species) in the lagoonal habitat limits this comparison.
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MDS ordination of fish-survey stations illustrates high similarity of assemblages within fore-reef sites and significant differences (ANOSIM, P<0.05) among habitats.
There were significant differences in the fish assemblages when classified by depth - shallow, middle, and deep (ANOSIM Global test, R = 0.618, P = 0.006). Differences in species composition were most evident between mid-depth and deep sites (ANOSIM Pairwise test, R = 0.829, P = 0.008). Fore-reef sites were typically at mid to shallow depths (20 to 34 m) whereas the patch-reef sites were typically deep (35 to 38 m). There is some evidence of habitat heterogeneity and vertical zonation for fish assemblages on Saba Bank, but more sampling is necessary to discern whether habitat or depth best explains the differences among groups.
The horizontal axis in the MDS plot represents a gradient in species richness with patch-reef and lagoonal sites having lowest richness ( Figure 2). The vertical axis in the MDS plot illustrates differences related to depth with deepest station (Small Bank) higher in the vertical axis, and shallower sites lower in the vertical axis. The two-dimensional stress value was low in the MDS (stress = 0.1) indicating a slight chance of misrepresentation.
A principal components analysis (PCA) was used to understand which species assemblages were responsible for differences among stations. The first three components explained 43.9% of the variation. The first component (18.6% of variation explained) was dominated by ubiquitous species and most common species. Strongest loadings (negative) on the first principal component (PC1) included the four species found at all stations (Halichoeres garnoti, Serranus tigrinus, Stegastes partitus, and Thalassoma bifasciatum) and 13 species found at all but one to four of the stations. These 13 common species are rarely found at the small bank, patch-reef, and lagoonal stations and, therefore, PC1 also serves to define the fore-reef sites. For example, Acanthurus bahianus, Coryphopterus glaucofraenum, Coryphopterus dicrus, and Scarus taeniopterus were found at all fore-reef sites but rarely at the Small Bank, lagoonal and at least one of the patch-reef sites. The strongest positive loadings on PC1 are from 11 species only found at the lagoonal site. Principal components 2 and 3 correspond strongly to the horizontal or species richness component on the MDS with strongest positive loadings on species typically found at the low to medium species richness stations 3, 5, 6 and 8–12 (e.g. Cryptotomus roseus, Haemulon melanurum, Halichoeres bivittatus, Astrapogon puncticulatus, and Serranus baldwini). Strongest negative scores were on species that were frequently found at high to medium species richness stations 1, 2, 4, 7 and 8 (e.g. Hypoplectrus puella, Lythrypnus elasson, Prognathodes aculeatus, Neoniphon marianus, and Gramma loreto).
An annotated list of the fishes of Saba Bank is provided below. In the list, we include the family, genus and species, author and English common name (as common names are not standardized internationally, we strove to apply the most widely used English common name based on FishBase (http://www.fishbase.org) listings). The use of “cf” before a species name indicates that the specimen photographed is similar to that species, but probably represents an undescribed species. Voucher specimens are archived at the National Museum of Natural History (USNM) and the Florida Museum of Natural History (UF) and each species with vouchers is annotated with the museum's acronym where the specimens are housed. The basis of each species record is indicated by: I – ichthyocide station, F – caught by a local fisherman and photographed, T – bottom trawl, O – visual sighting during Toller survey, V – visual sighting during RAP survey at roving and rotenone station. Lengths of specimens are recorded in mm for either standard length (SL), total length (TL), or fork length (FL). Photographs showing the color pattern of freshly collected specimens are included for as many of the species as possible. Images illustrating observed sexual and developmental (juvenile to adult) variability in color pattern are included where possible.
Antennarius pauciradiatus, 24.9 mm SL, photo by JT Williams.
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Antennarius pauciradiatus, 24.9 mm SL, close-up of head, photo by JT Williams.
Antennarius multiocellatus (Valenciennes, 1837) —longlure frogfish; USNM, I
A single juvenile specimen was collected in 2007. Although adults of this species have a very long first spine, our juvenile specimen has the first dorsal spine about the same length as the second. Böhlke and Chaplin [3] mention this allometric growth pattern in which the first spine is short in young specimens, but increases in length with growth. The juvenile exhibits the typical adult color pattern.
Chaunacidae—sea toads
Chaunax suttkusi Caruso, 1989—Suttkus sea toad; USNM, T
Ogcocephalidae—batfishes
All of the batfish records from Saba Bank are based on trawl collections with vouchered museum specimens.
Dibranchus atlanticus Peters, 1876—Atlantic batfish; UF, T
Halieutichthys aculeatus (Mitchill, 1818)—pancake batfish; UF, T
Ogcocephalus pumilus Bradbury, 1980—dwarf batfish; USNM, T
Rypticus saponaceus, 44.1 mm SL, photo by JT Williams.
Rypticus new species; USNM, I
This new species of soapfish is very similar in appearance to Rypticus subbifrenatus. The new species is being described by C Baldwin and DG Smith (pers. comm.).
Apogon cf quadrisquamatus, 21.1 mm SL, photo by JT Williams (this specimen represents a new undescribed species.
The specimens identified here as A.cf quadrisquamatus have been found to represent a new undescribed species closely related to A. quadrisquamatus (C. Baldwin & D.G. Smith, pers. comm. 2009).
Caulolatilus cyanops, 288 mm SL, photo by W Toller.
Malacanthus plumieri (Bloch, 1786)—sand tilefish; UF, O, V
Coryphaenidae-dolphinfishes
Coryphaena hippurus Linnaeus, 1758—common dolphinfish; F
Rachycentridae-cobias
Rachycentron canadum (Linnaeus, 1766)—cobia
Our record for this species is based on an underwater video recently filmed by Yap Films Inc (Toronto, Canada) at the shipwreck on Saba Bank. The video clearly shows a cobia swimming along the side of the shipwreck.
Mulloidichthys martinicus, 105 mm SL, photo by JT Williams.
Pseudupeneus maculatus (Bloch, 1793)—spotted goatfish; USNM, I, O, V; Figure 98
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Pseudupeneus maculatus, 218.8 mm SL, photo by JT Williams.
Chaetodontidae—butterflyfishes
Chaetodon capistratus Linnaeus, 1758—foureye butterflyfish; USNM, I, O, V; Figure 99
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Chaetodon capistratus, 99.4 mm SL; when younger, the specimen was apparently injured in the region of the fourth dorsal-fin spine (missing) and the area healed leaving a gap in the fin; photo by JT Williams.
Chaetodon ocellatus Bloch, 1787—spotfin butterflyfish; USNM, F, O, V
Chaetodon sedentarius Poey, 1860—reef butterflyfish; UF, O, V
Chaetodon striatus Linnaeus, 1758—banded butterflyfish; USNM, I, O, V; Figure 100
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Chaetodon striatus, 111.3 mm SL, photo by JT Williams.
Prognathodes aculeatus (Poey, 1860)—longsnout butterflyfish; USNM, I, O, V; Figure 101
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Prognathodes aculeatus, 62.9 mm SL, photo by JT Williams.
Pomacanthidae—angelfishes
Centropyge argi Woods & Kanazawa, 1951—cherubfish; USNM, I, O, V; Figure 102
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Centropyge argi, 33.8 mm SL, photo by JT Williams.
Holacanthus ciliaris (Linnaeus, 1758)—queen angelfish; USNM, F, I, O, V
Holacanthus tricolor (Bloch, 1795)—rock beauty; USNM, I, O, V; Figures 103, 104
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Holacanthus tricolor, 19.3 mm SL, juvenile color pattern, photo by JT Williams.
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Holacanthus tricolor, 40.1 mm SL, intermediate color pattern, photo by JT Williams.
Pomacanthus arcuatus (Linnaeus, 1758)—gray angelfish; V
Pomacanthus paru (Bloch, 1787)—French angelfish; O, V
Kyphosidae—sea chub
Kyphosus incisor (Cuvier, 1831)—yellow chub; V
Kyphosus sectatrix (Linnaeus, 1766)—Bermuda chub; O, V
Cirrhitidae—hawkfishes
Amblycirrhitus pinos (Mowbray, 1927)—redspotted hawkfish; USNM, I, O; Figure 105
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Amblycirrhitus pinos, 22.6 mm SL, photo by JT Williams.
Pomacentridae-damselfishes
Chromis cyanea (Poey, 1860)—blue chromis; USNM, I, O, V; Figure 106
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Chromis cyanea, 67.5 mm SL, iridescent blue colors on body faded immediately after death, photo by JT Williams.
Chromis multilineata (Guichenot, 1853)—brown chromis; USNM, I, O, V; Figure 107
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Chromis multilineata, 56.3 mm SL, photo by JT Williams.
Microspathodon chrysurus (Cuvier, 1830)—yellowtail damselfish; O, V
Stegastes adustus (Troschel, 1865) —dusky damselfish; O
Stegastes leucostictus (Müller & Troschel, 1848) —beaugregory; O
Stegastes partitus (Poey, 1868)—bicolor damselfish; USNM, I, O, V; Figures 108, 109
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Stegastes partitus, 58.6 mm SL, black-tailed color morph, photo by JT Williams.
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Stegastes partitus, 58.6 mm SL, yellow-tailed color morph, photo by JT Williams.
This species has a variable color pattern throughout its range. Two color morphs were found at Saba Bank. Both morphs have a yellow pectoral fin and a reduced yellowish white area covering the caudal peduncle. One morph has a black caudal fin (Figure 108) and the other morph has a pale yellowish caudal fin with a dusky brown area in the middle of the upper and lower lobes (Figure 109).
Stegastes planifrons (Cuvier, 1830)—threespot damselfish; USNM, I, O; Figure 110
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Stegastes planifrons, 82.7 mm SL, photo by JT Williams.
Labridae—wrasses
Bodianus rufus (Linnaeus, 1758)—Spanish hogfish; O, V
Clepticus parrae (Bloch & Schneider, 1801)—creole wrasse; USNM, I, O, V; Figure 111
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Clepticus parrae, 59.8 mm SL, photo by JT Williams.
Doratonotus megalepis Günther, 1862—dwarf wrasse; USNM, I, V; Figure 112
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Doratonotus megalepis, 44.1 mm SL, photo by JT Williams.
Halichoeres bivittatus (Bloch, 1791)—slippery dick; USNM, I, O, V; Figures 113, 114
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Halichoeres bivittatus, 37.9 mm SL, juvenile/initial color phase, showing the black spot in the dorsal fin and a somewhat unusual orangish anal fin, photo by JT Williams.
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Halichoeres bivittatus, 103.0 mm SL, terminal male color phase, with a distinctive red blotch on the side of the body above the pectoral fin, photo by JT Williams.
Halichoeres cyanocephalus (Bloch, 1791)—yellowcheek wrasse; O, V
Halichoeres garnoti (Valenciennes, 1839)—yellowhead wrasse; UF, USNM, I, O, V; Figures 115, 116, 117
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Halichoeres garnoti, 46.4 mm SL, juvenile color phase, showing the characteristic blue stripe on a yellow body, photo by JT Williams.
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Halichoeres garnoti, 118.1 mm SL, initial/terminal color phase, this specimen has almost completed the transition from the female initial phase into a terminal male, photo by JT Williams.
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Halichoeres garnoti, 125.3 mm SL, terminal male color phase, this specimen has completed the transition from the female initial phase into a terminal male and shows the characteristic black bar and dark area over the caudal peduncle, photo by JT Williams.
These figures show portions of the transitional color phases as individuals transform from juveniles (Figure 115) into initial phase females (Figure 116) and finally into terminal phase males (Figure 117).
Halichoeres maculipinna (Müller & Troschel, 1848)—clown wrasse; USNM, I, O
Starksia atlantica, 9.5 mm SL, juvenile, photo by JT Williams.
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Starksia atlantica, 15.1 mm SL, adult male, photo by JT Williams.
The Saba Bank population may be a distinct species in the species complex currently referred to as Starksia atlantica. This complex requires additional taxonomic study.
Starksia lepicoelia, 20.2 mm SL, adult female, photo by JT Williams.
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Starksia lepicoelia, 19.8 mm SL, adult male, photo by JT Williams.
Females (Figure 151) lack the black spot on the cheek that is characteristic of mature males (Figure 152). The Saba Bank population may be a distinct species in the species complex currently referred to as Starksia lepicoelia. This complex requires additional taxonomic study.
Starksia melasma Williams & Mounts, 2003—black spot blenny; USNM, I
Starksia nanodes, 10.6 mm SL, adult male, photo by JT Williams.
The Saba Bank population may be a distinct species in the species complex currently referred to as Starksia nanodes. This complex requires additional taxonomic study.
Acanthemblemaria aspera, 14.0 mm SL, juvenile/female, photo by JT Williams.
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Acanthemblemaria aspera, 19.7 mm SL, adult male, photo by JT Williams.
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Acanthemblemaria aspera, 20.4 mm SL, yellow color morph (female?), photo by JT Williams.
Three different color patterns were observed at Saba Bank: juvenile/female (Figure 154), adult male (Figure 155), and a distinctive yellow, probably female, color morph (Figure 156). The adult male and the yellow morph were taken together at the same collecting station.
Emblemariopsis cf signifer, 16.2 mm SL, adult male, this specimen represents an undescribed species in the signifer species complex, photo by JT Williams.
The signifer species complex ranges from Brazil throughout the Caribbean and includes a number of undescribed species in the Caribbean region. Additional taxonomic study is required to resolve the taxa.
Psilotris boehlkei, 26.5 mm SL, adult, photo by JT Williams.
The fresh colors of P. boehlkei are presented (Figure 179) for the first time. This very rare species was previously known from only five specimens taken at St. Barthelemey in 1965. The single specimen we collected extends the known distribution of P. boehlkei to Saba Bank. We have named this species the yellowspot goby in reference to the yellow spots on the head and body.
Pycnomma roosevelti, 14.6 mm SL, adult, photo by JT Williams.
Although P. roosevelti has previously been taken from a several scattered localities around the Caribbean (Isla Providencia, Guadeloupe, Belize and Puerto Rico), there are fewer than 10 specimens known and its fresh colors (Figure 180) have not been published previously.
Chilomycterus antillarum, 180.0 mm SL, photo by JT Williams.
Diodon holocanthus Linnaeus, 1758—balloonfish; USNM, I, V; Figure 200
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Diodon holocanthus, 104.9 mm SL, photo by JT Williams.
Diodon hystrix Linnaeus, 1758—porcupinefish; O
Discussion
We document the occurrence of 270 species of fishes at Saba Bank. The diversity of fishes at Saba Bank is comparable (Table 1) to that of the oceanic atolls of Colombia (273 species), the islands in the Mona Passage of Puerto Rico (261 species) and Buck Island Reef National Monument (BIRNM; 262 species). The relatively high diversity of fishes at Saba Bank exists despite the lack of emergent land at the bank. There is no shallow-water shore-fish fauna represented on the bank due to the absence of a high-energy shoreline. These habitats typically add significantly to the fish diversity of Caribbean habitats. For example, the tube blennies (family Chaenopsidae) are a group of shorefishes typically found in fairly shallow coastal waters. According to Williams [4], there are approximately 22 recognized species of tube blennies known to occur in the central Caribbean, but only three of these species were found on Saba Bank. In addition, the absence of mangrove vegetation and apparent lack of sea-grass beds also limits the fish fauna of Saba Bank. In their quantitative study of a number of Saba Bank habitats, Toller et al. [5] attribute the apparent lack or rarity of a number of fish species found on Saba Bank to the absence of those habitats as nurseries for the juvenile stages of these fish species. Nevertheless, diverse habitat types exist on Saba Bank ranging from coral reefs and algal flats to soft-bottom lagoon areas and scoured hard, flat, pavement-like zones. These diverse habitats support a highly diverse, fish fauna and include a number of undescribed, new species along with species rarely encountered elsewhere in the Caribbean.
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Number of fishes recorded at well sampled sites in the Greater Caribbean.
Site
No. fish species
Source
Alligator Reef, FL
517
Starck [12]
Dry Tortugas, FL
442
Longley & Hildebrand [13]
Bermuda
433
Smith-Vaniz et al [14]
St. Croix
400
Clavijo et al [15]
Barrier Reef, Belize
339
C.L. Smith et al [9]
Offshore Banks, Belize
293
C.L. Smith et al [9]
Oceanic Atolls, Colombia
273
Mejia et al [16]
Saba Bank
270
This paper
Buck Island Reef
262
Smith-Vaniz et al [8]
Mona Passage Islands, Puerto Rico
261
Dennis et al [7]
Flower Garden Bank Nat. Mar. Sanctuary, Texas, USA
240
E. Hickerson, NOAA, pers. comm., Dec. 2009
Navassa Island, USA
237
Collette et al [6]
Rhomboidal Cays, Belize
193
C.L. Smith et al [9]
Core Pelican Cays, Belize
168
C.L. Smith et al [9]
Peripheral Rhomboidal Cays, Belize
123
C.L. Smith et al [9]
The highly diverse, fish fauna so far reported appears to substantially under represent the species richness of fishes for Saba Bank. The actual species-accumulation curve of rotenone collections and visual surveys combined do not reach an asymptote (Figure 201). The expected species-accumulation curves (Chao2 and Jack1 estimators in EstimateS) predict total fish-species richness somewhere between 320 and 411 species.
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Actual species-accrual curve (black dots) for 38 dives collecting and identifying fish species on Saba Bank.
Sobs (Mao Tau) 95% confidence intervals [8] are shown as light blue dashed lines.
Of the 270 species we report (Table 1) from Saba Bank, 132 (49%) were observed during visual surveys. This result is comparable to the findings for Navassa Island where 41% of the fish species were detected by visual surveys [6], for the Mona Passage islands with 43% of the fish species detected visually [7], and for BIRNM with 44% of the fish species detected visually [8]. A higher percentage of fish species was detected visually at Saba Bank than at Navassa, Mona, or BIRNM. This could possibly be a result of the higher number of visual surveys carried out at Saba Bank than at Navassa or Mona. Although the BIRNM results are based on a higher number of visual surveys (70), a comparable percentage of the fauna was detected visually at BIRNM. BIRNM ichthyocide surveys (58) appear to demonstrate the ability of ichthyocide collections to more thoroughly sample the fauna (see below). Visual censuses have numerous biases as discussed in the methods for the Pelican Cays study [9]. Despite the slight differences in methods and sampling designs between the published fish species-richness studies in different parts of the Caribbean, the methods utilized produce consistent and comparable results.
Ichthyocide collections at Saba Bank yielded specimens representing 155 fish species (57% of the total fish fauna). At Navassa Island where there were fewer visual surveys than at Saba Bank, over 70% of the fish species were collected with ichthyocide [6], at the Mona Passage islands, 61% of the fish species were collected with ichthyocide [7], and at BIRNM, 87% of the fish species were collected with ichthyocide despite their being more visual surveys in the BIRNM study [8]. By occupying 58 (27 at Saba Bank) ichthyocide stations covering a broader diversity of ecological habitats, the BIRNM study appears to have obtained a more thorough sampling of the resident species. The lower number of species taken at Saba Bank with ichthyocide is at least partially due to the absence of shallow habitat. Shallow habitat is required by many of the small cryptic fish species that are normally detected only with the use of ichthyocide and these species have not been found at Saba Bank. The prevalence of strong currents across Saba Bank further limits the effectiveness of ichthyocide, which is only effective when relatively high concentrations of ichthyocide remain in one place (preferably in a confined area) for more than 15 to 20 minutes. The ichthyocide-collecting methods employed at Saba Bank were the same as those used at Navassa Island and Belize. The BIRNM ichthyocide collecting methods differed from ours only in that the BIRNM study used a block net in addition to collecting outside the net. Nevertheless, the BIRNM methods were comparable to ours because the BIRNM study included those species collected outside the block nets in their results. There are inherent biases in ichthyocide collecting due to unpredictability of environmental parameters, such as currents, temperature, degree of confinement of the sampling area, ability of larger species to swim away, and variable assays of active rotenone in the powdered Derris root (batches often vary from 5% to over 11% active rotenone due to natural variation in rotenone concentration among the roots of different plants). Despite these biases, ichthyocide collections yield comparable results as described above.
Neither visual surveying nor ichthyocide collecting alone are capable of providing a comprehensive survey of coastal (or submerged atoll in the case of Saba Bank) fish species. A combination of visual surveys, ichthyocide sampling using SCUBA, and various fishing techniques must be employed to effectively assess fish-species richness in marine habitats shallow enough to be accessible to SCUBA divers.
The number of fish species living on Saba Bank is undoubtedly higher than 270 as indicated by Chao2 and Jack1 estimators. As most parts of Saba Bank are deeper than 25 m, sampling with ichthyocides using SCUBA is limited by the reduced bottom time at these depths. As a result we focused primarily on the rim (shallowest parts) of the submerged atoll to maximize bottom time for collecting. Future sampling with ichthyocides applied by divers utilizing rebreathers, supplemented with trawl and dredge sampling would allow collecting from the outer slopes and would certainly yield additional new and interesting species of fishes from this submerged atoll.
Methods
The NMNH/SI Animal Care and Use Committee approved the methods and procedures utilized during the course of this biodiversity assessment project. All Saba Bank projects had collecting permits through the Convention on Trade in Endangered Species (CITES, where necessary) and the Saba Conservation Foundation (where CITES was not required).
Roving surveys were completed using SCUBA and lasted 60 minutes, bottom time permitting. All species encountered were listed on a slate while swimming in a haphazard pattern covering all bottom depths possible down to a maximum of 38 m. Other visual surveys are described in Toller et al [5]. Collecting methods follow Collette et al [6]. Species were photographed in aquaria after the fins were pinned out and brushed with formaldehyde solution. Tissue samples were taken from fresh specimens and the voucher specimens were preserved in a formaldehyde solution diluted with water to 3.75% formaldehyde. Large specimens were also injected with 37.5% formaldehyde before being soaked in the 3.75% formaldehyde solution.
After arrival at the Museum Support Center (MSC), National Museum of Natural History, specimens were transferred sequentially through water-diluted solutions of 25% ethanol, 50% ethanol, and finally into 75% ethanol for permanent archival storage. Specimens were then processed and cataloged into the USNM at the MSC in Suitland, MD.
To generate species-accumulation curves, a data matrix of presence/absence was constructed from 38 combined roving surveys, rotenone collections, and fish-habitat transects using species as variables and dives as observations (Table 2 provides details for each survey and collecting station). The matrix was employed for actual and expected species-accumulation curves (Mao Tau) in EstimateS v.8.0 software [10]. Total expected richness was estimated using Chao2 and Jack1 estimators.
10.1371/journal.pone.0010676.t002
Collecting stations occupied on Saba Bank, 2006-2007.
Station number
Roving & Rotenone
Coordinates
Date
Depth (m)
Local name
Description of habitat
Saba-06-01
RR01
17o28.778N; 63o13.663W
04 Jan 2006
30
North East Reef
N.E. reefs, just S of Poison Bank. Spur and groove reef, low relief, many algae (Dictyota)-rotenoned a groove in reef with sand at bottom, walls of groove with low corals
Saba-06-02
RR02
17o26.883N; 63o54.055W
05 Jan 2006
38
Small Bank South
Small Bank South. Scattered corals, many Xestospongia. Nassau grouper, yellowfin grouper, and black grouper sighted. Nurse shark-rotenoned area with encrusting corals
Saba-06-03
RR03
17o25.778N; 63o41.037W
05 Jan 2006
35
Rhodolith Reef
Western patch reef, many rodoliths-rotenoned a flat area with sponges and rubble bottom
Saba-06-04
17o18.557N; 63o22.019W
05 Jan 2006
35
Fish Trap- Local Fishermen
Saba-06-05
RR04
17o24.602N; 63o11.748W
06 Jan 2006
27
Redman Bulge
Eastern reef, spur and groove, medium height, many algae (dictyota)
Saba-06-06
RR05
17o26.028N; 63o16.536W
06 Jan 2006
22
Seaweed city
pavement covered with ca. 10 cm sand layer, Pseudopterogorgia, many algae species
Saba-06-07
17o33.697N; 63o46.949W
0-1
Caught on hook and line while trolling over Saba Bank
Saba-06-08
RR06
17o33.092N; 63o28.758W
07 Jan 2006
37
Grouper Bank
bare pavement, occasional solution holes, Manicinias, many conch (old)
Saba-06-09
RR07
17o34.893N; 63o24.400W
07 Jan 2006
30
Rendezvous Hill
pavement with corals, low relief-rotenoned a low-relief coral reef with soft and hard corals, and sponges
Saba-06-10
17o25.883N; 63o21.874W
08 Jan 2006
0-1
Caught on hook and line while trolling over Saba Bank
Saba-06-11
RR08
17o14.070N; 63o26.915W
08 Jan 2006
25
Butterfly Reef
Southern outer reef. Spur and groove, medium height (2-3 ft)
Saba-06-12
RR09
17o14.380N; 63o26.915W
08 Jan 2006
18
Brain coral reef
Southern inner reef, rock pavement, scattered corals
Saba-06-13
RR10
17o33.801N; 63o17.806W
09 Jan 2006
32
Fishpot surprise
sloping pavement with ledges, sand patches and large rubble, algae, scattered corals-rotenoned an area with sand and loose rock at base of rocky slope with brown algae abundant.
Saba-06-14
17o33.970N; 63o17.227W
09 Jan 2006
40
Fish Trap
Saba-06-15
17o33.897N; 63o17.730W
09 Jan 2006
40
Fish Trap
Saba-06-16
17o33.878N; 63o17.168W
10 Jan 2006
40
Fish Trap
Saba-06-17
RR11
17o33.849N; 63o17.872W
10 Jan 2006
26
Lost anchor
Sloping pavement, patches of large rubble, algae, scattered corals; red hind spawning area
Saba-06-18
17o33.837N; 63o17.962W
10 Jan 2006
30
Fish Trap
Saba-06-19
RR12
17o33.686N; 63o17.629W
10 Jan 2006
26
Moonfish Bank
Sloping pavement, sand patches, large rubble, algae, scattered corals; red hind spawning area
Saba-06-20
17o30.751N; 63o13.632W
12 Jan 2006
29
Poison Bank
Rotenone
Saba-06-21
17o28.046N; 63o14.978W
12 Jan 2006
19
Rotenone-northeastern shallow flats
Saba-06-22
17o26.390N; 63o27.776W
13 Jan 2006
26
Rotenone-flat bottom in central area of bank
Saba-06-23
17o30.580N; 63o27.595W
13 Jan 2006
28
Rotenone-flat bottom in central area of bank
Saba-06-24
17o20.766N; 63o15.008W
14 Jan 2006
31
Coral Garden
Rotenone-coral groove at top of steep outer dropoff on SE side of Saba Bank, rock, coral, and sponges, sand at bottom of groove.
Saba-06-25
17o21.162N; 63o15.138W
14 Jan 2006
18
Rotenone-near Coral Garden at SE edge of Saba Bank, small ledge on edge of sand and rubble flat, gorgonians, coral and rock
Saba-06-26
No label with these-specimens taken at one or more of the other stations, but their locality labels were lost
Saba 2007-01
17.51206 N; 63.2332 W
20 Jun 2007
29-38
Poison Bank- rotenone-dead and live coral channel with rubble on deep reef.
Saba 2007-02
17.46028 N; 63.2517 W
20 Jun 2007
15-19
Twin Peaks- rotenone-algae covering rock and some sand on a low ridge
A Bray-Curtis resemblance matrix was generated from a matrix of presence/absence data from 12 combined roving surveys and rotenone collections in order to produce a non-metric multidimensional scaling (MDS) ordination and group averaged hierarchical clustering dendrogram in PRIMER v. 6.1 software [11]. The ANOSIM statistic was employed to test for a priori differences between habitat types and depth classes. A dendrogram based on group averaged hierarchical cluster techniques was used to illustrate the differences among depth classes (Figure 202). Color codes are derived from the similarity profile (SIMPROF) statistic in Primer 6.1. SIMPROF is less powerful than ANOSIM, intended for a posteriori tests of structure in the data. The test was employed here for representational purposes. A second data matrix of species presence and absence was introduced for an a posteriori test of genuine data structure among Caribbean localities, using the Bray-Curtis resemblance measure to determine the level of similarity among localities. Principal Components Analysis (PCA) was also conducted in PRIMER 6.1 in order to determine the fish species primarily responsible for differences among habitats.
10.1371/journal.pone.0010676.g202
Hierarchical clustering dendrogram of stations showing significant differences (black bars) among fish assemblages at deep stations versus middle-depth and shallow stations (SIMPROF, P<0.05).
This program was a joint initiative of the Department of Environment and Nature of the Netherlands Antilles and Conservation International. We are especially grateful to the many people who made the biodiversity survey possible, including Andy Caballero of Nature Foundation St. Maarten; David Kooistra, Stanley Peterson, and Jan Den Dulk of Saba Conservation Foundation; Shelley Lundvall, Saba Bank project manager; fishermen Leroy Peterson, Nicky Johnson and Armand Simmons. We thank Jerome Finan, Kris Murphy, and David G. Smith, National Museum of Natural History, Smithsonian Institution, for their help with this project. We thank Menno Van der Velde and Wim Schutten for collecting fishes at several ichthyocide stations. Jill Leger, Yap Films Inc, provided a video clip of fishes filmed at the shipwreck on Saba Bank. Emma L. Hickerson, Flower Garden Banks National Marine Sanctuary (FGBNMS), NOAA, kindly provided information on the number of fish species known to occur at the FGBNMS. Dr. JA Sanchez, University de los Andes, allowed us to use his photograph for Figure 3.
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