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Broad geographic distribution of roundscale spearfish (Tetrapturus georgii) (Teleostei, Istiophoridae) in the Atlantic revealed by DNA analysis: Implications for white marlin and roundscale spearfish management
Fisheries Research 139 (2013) 93–97
Contents lists available at SciVerse ScienceDirect
Fisheries Research journal homepage: www.elsevier.com/locate/fishres
Short communication
Broad geographic distribution of roundscale spearfish (Tetrapturus georgii) (Teleostei, Istiophoridae) in the Atlantic revealed by DNA analysis: Implications for white marlin and roundscale spearfish management Andrea M. Bernard a , Mahmood S. Shivji a,∗ , Rodrigo Rodrigues Domingues b,h , Fabio Hissa Vieira Hazin c , Alberto Ferreira de Amorim b , Andres Domingo d , Freddy Arocha e , Eric D. Prince f , John P. Hoolihan g , Alexandre Wagner Silva Hilsdorf h a
The Guy Harvey Research Institute, Oceanographic Center, Nova Southeastern University, 8000 N. Ocean Drive, Dania Beach, FL 33004, USA Agencia Paulista de Tecnologia dos Agronegócios, Instituto de Pesca, Av. Bartolomeu de Gusmão, 192, Santos, São Paulo 11030-906, Brazil c Departamento de Pesca e Aquicultura, Universidade Federal Rural de Pernambuco, Rua Dom Manoel de Medeiros, s/n, Dois Irmãos, Recife, PE 52171-032, Brazil d Laboratorio de Recursos Pelágicos, Dirección Nacional de Recursos Acuáticos. Constituyente 1497, CP 11200 Montevideo, Uruguay e Instituto Oceanográfico de Venezuela, Universidad de Oriente, Apartado de Correos, 204, Cumaná 6101, Venezuela f National Marine Fisheries Service, Southeast Fisheries Science Center, 75 Virginia Beach Drive, Miami, FL 33149, USA g Cooperative Institute for Marine and Atmospheric Studies, Rosenstiel School for Marine and Atmospheric Science, University of Miami, 4600 Rickenbacker Causeway, Miami, FL 33149, USA h Universidade de Mogi das Cruzes, Núcleo Integrado de Biotecnologia, PO Box 411, Mogi das Cruzes, São Paulo 08701-970, Brazil b
a r t i c l e
i n f o
Article history: Received 24 May 2012 Received in revised form 3 October 2012 Accepted 4 October 2012 Keywords: Fisheries management Species identification Kajikia albida Mitochondrial DNA Billfish
a b s t r a c t The recent validation of the roundscale spearfish (Tetrapturus georgii) within the western North Atlantic has introduced new complexities in the management of the overfished white marlin (Kajikia albida) in this region due to historical and contemporary misidentification between the two morphologically similar species. Compounding the management challenge for white marlin, which is currently assessed as a single Atlantic-wide stock, is an unclear picture of the extent of the roundscale spearfish’s overall Atlantic distribution. By using genetic tools (mitochondrial DNA ND4L-ND4 locus sequences) for species identification, we confirm that the roundscale spearfish has a much broader distribution than previously known, including the central North Atlantic and much of the western South Atlantic to at least 28◦ 52 S. This much wider Atlantic distribution of the roundscale spearfish sympatric with its morphologically similar congeners, the white marlin and longbill spearfish (Tetrapturus pfluegeri), raises further management complexities: it increases the geographic scale for species misidentification in catch records that form the basis for stock assessments and uncertainty in currently accepted white marlin biological parameters. Additional vigilance in obtaining accurate species identification by improved fishery onboard observer training and incorporation of genetic tools is recommended for informing management of white marlin, longbill spearfish and roundscale spearfish throughout the Atlantic. © 2012 Elsevier B.V. All rights reserved.
1. Introduction The existence of a potential sixth istiophorid billfish species in the eastern North Atlantic, the roundscale spearfish (Tetrapturus georgii), was first suggested by Lowe (1840) based on a cursory description of a single specimen captured near Madeira Island, Portugal, and subsequently by Robins (1974) based on a more detailed morphological examination in 1961 of four individuals caught in the Mediterranean Sea and the eastern North Atlantic. However, given this small sample set of examined animals and an
∗ Corresponding author. Tel.: +1 954 262 3653; fax: +1 954 262 4098. E-mail address: [email protected] (M.S. Shivji). 0165-7836/$ – see front matter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.fishres.2012.10.009
absence of further reports of this billfish since 1961, the validity of the roundscale spearfish remained uncertain until its existence was confirmed genetically and morphologically over four decades later (Shivji et al., 2006; Beerkircher et al., 2008). Despite the roundscale spearfish’s now realized large genetic divergence relative to other billfishes (Collette et al., 2006; Shivji et al., 2006; Hanner et al., 2011), its lack of recognition by fishers and managers until recently is attributed to its strong gross morphological resemblance to the white marlin, Kajikia albida (formerly Tetrapturus albidus), and overall similarity to its congener the longbill spearfish, Tetrapturus pfluegeri. Reliable morphological discrimination among these three species remains challenging, requiring close examination of lateral scale appearance and/or morphometric assessments.
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The roundscale spearfish remains enigmatic in all aspects of its biology, including distribution. Its presence in waters of the western North Atlantic is now unambiguously confirmed on the basis of genetic and morphological examination (Shivji et al., 2006; Beerkircher et al., 2008, 2009) and its occurrence has also been documented within the Caribbean Sea, although based on morphological assessments only (Arocha and Ortiz, 2006a). To date, however, only circumstantial or minimal information is available regarding the potential distribution of this species in other parts of the Atlantic. Arfelli et al. (1986) noted morphological differences among individuals identified as K. albida caught by the longline fleet along the southeastern coast of Brazil, which they attributed to a possible second billfish species. Following documentation of T. georgii in the western North Atlantic (Shivji et al., 2006), researchers are investigating its distribution in other areas. Seven putative roundscale spearfish were captured in the Uruguayan tuna fishery between 27◦ 01 S and 31◦ 58 S in the western South Atlantic (Domingo et al., 2009). However, identification of these individuals was based primarily on the position of the anal opening relative to the origin of the anal fin, which by itself is an imprecise criterion. Within the western North and western Central Atlantic, the historic mis-identification of roundscale spearfish as white marlin has raised important concerns about the accuracy of past white marlin stock assessments given its severely overfished status (Beerkircher et al., 2009). Furthermore, with substantial white marlin catches documented in the South Atlantic and concerns about its stock status in this region also (Anon., 2007), determining the Atlanticwide distribution of the roundscale spearfish is a necessary first step for clarifying the potential for misidentifications with white marlin, as well as longbill spearfish, which also occurs in offshore Atlantic fisheries (Ueyanagi et al., 1970; Arocha et al., 2007; Anon., 2011). Here, we show by DNA analysis that some specimens originally recorded in the multinational Atlantic offshore catch as white marlin or longbill spearfish are roundscale spearfish, and demonstrate that the distribution of roundscale spearfish extends into the central North Atlantic and much of the western South Atlantic up to at least 28◦ 52 S. We also comment on the implications of this larger distribution on issues related to white marlin and roundscale spearfish management in the latter region. 2. Materials and methods 2.1. Sampling and DNA sequencing As part of a separate, ongoing study aimed at checking identities of white marlin and longbill spearfish catch in commercial long-line fisheries outside the western North Atlantic, we discovered that some of the billfish samples possessed mitochondrial DNA sequences that did not correspond to either white marlin or longbill spearfish. We selected 14 of these samples captured across the broadest geographic range (Fig. 1 and Table 1) in our
Fig. 1. Map showing capture locations of genetically identified T. georgii specimens. Capture locations of 14 animals from this study are shown as symbols (() represents single individuals and (䊉) represents three individuals); () represents capture locations of animals from the western North Atlantic reported in Shivji et al. (2006).
sample set for further identification by sequencing their mitochondrial NADH 4L-4 (ND4L-ND4) subunit genes, as this locus unambiguously distinguishes all Atlantic billfish species with the exception of T. pfluegeri (longbill spearfish) from Tetrapturus belone (Mediterranean spearfish) (Shivji et al., 2006). Tissue samples were stored in 95% ethanol until DNA extraction. All laboratory procedures for DNA extraction, PCR, and sequencing and sequence assembly were those specified in Shivji et al. (2006). 2.2. Data analyses Species identification for the 14 samples was determined by maximum likelihood (ML) and neighbor joining (NJ) phylogenetic reconstructions that included previously published billfish species reference ND4L-4 sequences (1268 bp) from Shivji et al. (2006) (GenBank accession numbers in Fig. 2). The Akaike information criterion (AIC), as implemented in Modeltest 2.06 (Posada and Crandall, 1998) was utilized to identify the most appropriate model of DNA evolution for the ND4L-4 sequences. The ML and NJ phylogenetic reconstructions were performed using PAUP version 4.0b10 (Swofford, 1999) which employed the TrN + I model of sequence evolution from Modeltest. The estimated proportion of invariable
Table 1 T. georgii sample identification number (from Fig. 1), GenBank accession number, and capture coordinates. Sample identification number
GenBank accession number
Latitude
Longitude
1 2 3 4 5 6 7 8 9 10 11 12–14
DQ872424 JQ926729 DQ872425 JQ926732 DQ872424 JQ926731 JQ926728 DQ872425 JQ926733 JQ926730 JQ926727 DQ872424, DQ872425, DQ872424
37◦ 41 N 10◦ 57 N 4◦ 25 N 3◦ 48 S 7◦ 43 S 12◦ 23 S 13◦ 08 S 25◦ 46 S 27◦ 13 S 27◦ 11 S 28◦ 52 S 25◦ 30 S–26◦ 30 S
38◦ 52 W 56◦ 00 W 32◦ 08 W 28◦ 41 W 30◦ 45 W 28◦ 54 W 27◦ 58 W 29◦ 21 W 28◦ 41 W 32◦ 13 W 32◦ 59 W 45◦ 30 W–46◦ 30 W
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Fig. 2. Maximum likelihood phylogenetic tree depicting major billfish clades inferred from the mitochondrial ND4L-ND4 genes. The 14 specimens sequenced in this study are indicated in bold. Specimen numbers 1–14 correspond to Fig. 1. Bootstrap values at nodes correspond to maximum likelihood (top) and neighbor-joining (bottom) analyses. Bootstrap values ≥90% are shown for the major clades.
sites was 0.7835. GenBank sequence DQ872417 (Makaira nigricans) was defined as an outgroup for all phylogenetic analyses. The ML tree was constructed by implementing a heuristic search, which utilized random stepwise addition (10 replicates) to acquire the starting trees. Statistical support for branch nodes was determined via nonparametric bootstrap analyses (1000 replicates) using PAUP for both the ML and NJ trees. 3. Results and discussion The ND4L-4 sequences from the 14 specimens comprised nine haplotypes and formed a strongly supported, reciprocally monophyletic group with reference T. georgii sequences from western
North Atlantic animals (Fig. 2). Two of the nine haplotypes were previously published in Shivji et al. (2006). This result confirms the identity of the 14 specimens as roundscale spearfish and the independent evolutionary trajectory for this lineage. The capture locations for the 14 genetically confirmed roundscale spearfish ranged from latitudes 37◦ 41 N to 28◦ 52 S, and longitudes 56◦ 00 W to 27◦ 58 W (Fig. 1 and Table 1), confirming and broadly extending the previously documented range of this species to include the central North and western South Atlantic at the minimum. Based on these findings and the early description of this species in the eastern North Atlantic (Robins, 1974), it seems reasonable to assume that the roundscale spearfish is widely distributed throughout the North Atlantic basin at least
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up to 37◦ 41 N, and along the entire western Atlantic minimally to 28◦ 52 S. The extent of its distribution into the eastern South Atlantic remains undocumented. However, given the occurrence of roundscale spearfish in the far eastern North Atlantic, it is reasonable to assume its range may also extend close to the western African continental margins in the South Atlantic, where white marlin and longbill spearfish are also known to occur (Nakamura, 1985; Kerstetter et al., 2009; Garcia-Cortés et al., 2012). The broad extension of the documented Atlantic distribution of the roundscale spearfish, combined with known species misidentification issues, has ramifications for management and conservation of the species complex comprising white marlin (IUCN Red List Vulnerable status, Collette et al., 2011), longbill and roundscale spearfish throughout this range. 3.1. Implications for white marlin and roundscale spearfish Both white marlin and roundscale spearfish, as well as longbill spearfish, are endemic to the Atlantic Ocean and managed under the authority of the International Commission for the Conservation of Atlantic Tunas (ICCAT). The issue of the abundance and distribution of the roundscale spearfish has become an important factor for white marlin management given the likelihood of species misidentifications. It became apparent from fisheries observer data for this region that recent “white marlin” catches were in fact comprised of a combination of white marlin and roundscale spearfish, with the latter species comprising ∼27% of white marlin recorded catch (Beerkircher et al., 2009). The proportion of the two species may also vary spatially and temporally in specific areas of the Caribbean Sea (Arocha and Silva, 2011). However, the proportions of the two species in historical reported catch data used for ICCAT white marlin stock assessments is unknown, and will be difficult to determine (Anon., 2011). Beerkircher et al. (2009) simulated population assessments using variable hypothetical proportions of the two species over time and showed that varying the proportions had a large influence on the population assessment outcomes for both species in the western North Atlantic, casting considerable uncertainty on past white marlin stock assessments. The vastly extended distribution of the roundscale spearfish documented here to Atlantic regions not considered by Beerkircher et al. (2009) increases the potential for species misidentifications in catch records. In fact, a genetic assessment of 85 white marlin specimens sampled over 18 landings events in 2009 from the Sao Paulo, Brazil-based longline fishery, covering the area spanning 17–35◦ S and 27–52◦ W, revealed 10.6% of the specimens to be roundscale spearfish and 4.7% to be longbill spearfish (author AFA, unpublished). These identification errors occurring over a much larger region also subject to heavy commercial fishery bycatch of white marlin (Anon, 2011) exacerbates the uncertainties in both currently accepted white marlin biological parameters and Atlantic-wide stock assessments. The spatial distribution of the roundscale spearfish documented here indicates considerable overlap with the longbill spearfish in the western South Atlantic (Arocha and Ortiz, 2006b). The two species also share an overall morphological similarity (Nakamura, 1985), resulting in the potential for significant species misidentification errors in fisheries catch data. In fact in a genetic assessment of 100 fishery observer identified longbill spearfish captured in Brazilian longline fisheries between 4◦ 25 N–19◦ 46 S and 23◦ 52 W–39◦ 23 W between June 2006 and November 2007, 49% of the specimens were roundscale spearfish (authors MSS and FHVH, unpublished). The status of longbill spearfish populations is unknown (STECF, 2009). Given concerns that they might be experiencing the same overfishing problems as other billfish, monitoring catches of all spearfish species to aid in their management has been recommended (STECF, 2009). However, the potential for increased
incidence of species misidentification between longbill and roundscale spearfishes in catch data over a South Atlantic-wide region adds to the complexities of such species-level monitoring. The broad distribution of the roundscale spearfish documented here highlights the need for additional vigilance in obtaining accurate species identification for informing management of white marlin, longbill spearfish and roundscale spearfish throughout Atlantic multinational fisheries. Accurately resolving the spatial and temporal catch composition will be essential for improving the reliability of the science that supports the management of these morphologically similar species. Since it is not possible to append the historic catch records, ICCAT has recommended that the upcoming 2012 white marlin stock assessment be recognized as a mixed species assessment (Anon., 2011). However, such mixed species assessments are sub-optimal for conservation of biodiversity and preventing unrecognized declines of individual species that may have lower productivity. Improved species identification by better training of onboard observers as well as fishers (Beerkircher et al., 2008) and broader incorporation of genetic tools (Beerkircher et al., 2009) in the acquisition of billfish catch data is recommended to reduce species uncertainties and accomplish management and conservation goals. Acknowledgements This work was supported by funding from NOAA/NMFS SEFSC, a National Science and Engineering Research Council of Canada Graduate Fellowship (AMB), The Guy Harvey Ocean Foundation, The Brazilian Ministry of Fisheries and Aquaculture, Universidade de Mogi das Cruzes, Unidade de Biotecnologia, FAPESP (proc. 2009/54660-6), and Agencia Paulista de Tecnologia dos Agronegócios, Instituto de Pesca. We thank S. Teter for creating Fig. 1 map. This research was carried out in part under the auspices of the Cooperative Institute for Marine and Atmospheric Studies (CIMAS), a Cooperative Institute of the University of Miami and the National Oceanic and Atmospheric Administration, cooperative agreement #NA1RJ1266. The views expressed herein are those of the authors, and do not necessarily reflect the views of NOAA or any of its subagencies. References Anon., 2007. Report of the 2006 ICCAT Billfish Stock Assessment. Madrid, Spain, May 15–19, 2006. Col. Vol. Sci. Pap. ICCAT 60(5), 1431–1546. Anon., 2011. Report of the 2011 Blue Marlin Stock Assessment And White Marlin Data Preparatory Meeting. Madrid, Spain, April 25–29, 2011. ICCAT, 71 pp. Arfelli, C.A., Amorim, A.F., Galhardo-Amado, J.C., 1986. Analysis on Tetrapturus albidus Poey (1861), caught off south and southeast Brazil (1971–1984). Col. Vol. Sci. Pap. ICCAT 25, 202–217. Arocha, F., Ortiz, M., 2006. Roundscale spearfish. ICCAT Manual. Chapter 2.1.8.4. Available from: http://www.iccat.int/Documents/SCRS/Manual/ CH2/2 1 8 3 SPG ENG.pdf (accessed 04.12). Arocha, F., Ortiz, M., 2006. Longbill spearfish. ICCAT Manual. Chapter 2.1.8.3. Available from: http://www.iccat.int/Documents/SCRS/Manual/ CH2/2 1 8 2 SPF ENG.pdf (accessed 04.12). Arocha, F., Barrios, A., Lee, D.W., 2007. Spatial-temporal distribution, sex ratio at size and gonad index of white marlin (Tetrapturus albidus) and longbill spearfish (Tetrapturus pfluegeri) in the western central Atlantic during the period of 2002–2005. Col. Vol. Sci. Pap. ICCAT 60, 1746–1756. Arocha, F., Silva, J., 2011. Proportion of Tetrapturus georgii (SPG) with respect to T. albidus (WHM) in the Venezuelan pelagic longline catch in the western Caribbean Sea and adjacent Atlantic waters during 2002–2007. Col. Vol. Sci. Pap. ICCAT 66, 1787–1793. Beerkircher, L.R., Lee, D.W., Hinteregger, G.F., 2008. Roundscale spearfish Tetrapturus georgii: morphology, distribution, and relative abundance in the western north Atlantic. B. Mar. Sci. 82, 155–170. Beerkircher, L.R., Arocha, F., Barse, A., Prince, E.D., Restrepo, V., Serafy, J.E., Shivji, M.S., 2009. Effects of species misidentification on population assessment of overfished white marlin Tetrapturus albidus and roundscale spearfish T. georgii. Endanger. Species Res 9, 81–90. Collette, B.B., McDowell, J.R., Graves, J.E., 2006. Phylogeny of recent billfishes (Xiphioidei). B. Mar. Sci. 79, 455–468.
A.M. Bernard et al. / Fisheries Research 139 (2013) 93–97 Collette, B.B., Carpenter, K.E., Polidoro, B.A., Juan-Jordá, M.J., Boustany, A., Die, D.J., et al., 2011. High value and long life – double jeopardy for tunas and billfishes. Science 333, 291–292. Domingo, A., Pons, M., Rios, M., 2009. Analisis de la captura, distribucion y composicion de tallas de istioforidos en el atlantico sur observada en la flota de palangre uruguaya (1998–2007). Col. Vol. Sci. Pap. ICCAT 64, 1885–1902. Garcia-Cortés, B., Ramos-Cartelle, A., Mejuto, J., 2012. Observations of the white marlin (Tetrapturus albidus) carried out on board of the Spanish surface longline fleet targeting swordfish from 1993-2010. Col. Vol. Sci. Pap. ICCAT 68, 1432–1445. Hanner, R., Floyd, R., Bernard, A., Collette, B.B., Shivji, M., 2011. DNA barcoding of billfishes. Mitochondrial DNA 22, 27–36. Kerstetter, D.W., Orbesen, E.S., Snodgrass, D., Prince, E.D., 2009. Movements and habitat utilization of two longbill spearfish, Tetrapturus pfluegeri, in the eastern tropical South Atlantic Ocean. B. Mar. Sci. 85, 173–182. Lowe, R.T., 1840. On new species of fishes from Madiera. P. Zool. Soc. Lond. 8, 36–39. Nakamura, I., 1985. FAO species catalogue, vol. 5. Billfishes of the world. An annotated and illustrated catalogue of marlins, sailfishes, spearfishes and swordfishes known to date. FAO Fisheries Synopsis. Rome, Italy.
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Posada, D., Crandall, K.A., 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818. Robins, C.R., 1974. The validity and status of the roundscale spearfish, Tetrapturus georgei. In: Shomura, R.S., Williams, F. (Eds.), Proceedings of the 1st International Billfish Symposium. NOAA Technical Report. , pp. 61–64, NMFS SSRF-675. Shivji, M., Magnussen, J.E., Beerkircher, L.R., Hinteregger, G.F., Lee, D.W., Serafy, J.E., Prince, E.D., 2006. Validity, identification, and distribution of the roundscale spearfish, Tetrapturus georgii (Teleostei: Istiophoridae): morphological and molecular evidence. B. Mar. Sci. 79, 483–491. STECF, 2009. Review of scientific advice for 2010. Part 2. European Commission. Available from: https://stecf.jrc.ec.europa.eu/c/document library/ get file?p l id=53334&folderId=44863&name=DLFE-4716.pdf (accessed 12.11). Swofford, D.L., 1999. PAUP 4.0 Phylogenetic analysis using parsimony and other methods. Beta version 4. 0. 5. Sinauer Associates, Sunderland. Ueyanagi, S., Kikawa, S., Uto, M., Nishikawa, Y., 1970. Distribution, spawning, and relative abundance of billfishes in the Atlantic Ocean. Bull. Far Seas Fish. Res. Lab. 3, 15–55.
Contents lists available at SciVerse ScienceDirect
Fisheries Research journal homepage: www.elsevier.com/locate/fishres
Short communication
Broad geographic distribution of roundscale spearfish (Tetrapturus georgii) (Teleostei, Istiophoridae) in the Atlantic revealed by DNA analysis: Implications for white marlin and roundscale spearfish management Andrea M. Bernard a , Mahmood S. Shivji a,∗ , Rodrigo Rodrigues Domingues b,h , Fabio Hissa Vieira Hazin c , Alberto Ferreira de Amorim b , Andres Domingo d , Freddy Arocha e , Eric D. Prince f , John P. Hoolihan g , Alexandre Wagner Silva Hilsdorf h a
The Guy Harvey Research Institute, Oceanographic Center, Nova Southeastern University, 8000 N. Ocean Drive, Dania Beach, FL 33004, USA Agencia Paulista de Tecnologia dos Agronegócios, Instituto de Pesca, Av. Bartolomeu de Gusmão, 192, Santos, São Paulo 11030-906, Brazil c Departamento de Pesca e Aquicultura, Universidade Federal Rural de Pernambuco, Rua Dom Manoel de Medeiros, s/n, Dois Irmãos, Recife, PE 52171-032, Brazil d Laboratorio de Recursos Pelágicos, Dirección Nacional de Recursos Acuáticos. Constituyente 1497, CP 11200 Montevideo, Uruguay e Instituto Oceanográfico de Venezuela, Universidad de Oriente, Apartado de Correos, 204, Cumaná 6101, Venezuela f National Marine Fisheries Service, Southeast Fisheries Science Center, 75 Virginia Beach Drive, Miami, FL 33149, USA g Cooperative Institute for Marine and Atmospheric Studies, Rosenstiel School for Marine and Atmospheric Science, University of Miami, 4600 Rickenbacker Causeway, Miami, FL 33149, USA h Universidade de Mogi das Cruzes, Núcleo Integrado de Biotecnologia, PO Box 411, Mogi das Cruzes, São Paulo 08701-970, Brazil b
a r t i c l e
i n f o
Article history: Received 24 May 2012 Received in revised form 3 October 2012 Accepted 4 October 2012 Keywords: Fisheries management Species identification Kajikia albida Mitochondrial DNA Billfish
a b s t r a c t The recent validation of the roundscale spearfish (Tetrapturus georgii) within the western North Atlantic has introduced new complexities in the management of the overfished white marlin (Kajikia albida) in this region due to historical and contemporary misidentification between the two morphologically similar species. Compounding the management challenge for white marlin, which is currently assessed as a single Atlantic-wide stock, is an unclear picture of the extent of the roundscale spearfish’s overall Atlantic distribution. By using genetic tools (mitochondrial DNA ND4L-ND4 locus sequences) for species identification, we confirm that the roundscale spearfish has a much broader distribution than previously known, including the central North Atlantic and much of the western South Atlantic to at least 28◦ 52 S. This much wider Atlantic distribution of the roundscale spearfish sympatric with its morphologically similar congeners, the white marlin and longbill spearfish (Tetrapturus pfluegeri), raises further management complexities: it increases the geographic scale for species misidentification in catch records that form the basis for stock assessments and uncertainty in currently accepted white marlin biological parameters. Additional vigilance in obtaining accurate species identification by improved fishery onboard observer training and incorporation of genetic tools is recommended for informing management of white marlin, longbill spearfish and roundscale spearfish throughout the Atlantic. © 2012 Elsevier B.V. All rights reserved.
1. Introduction The existence of a potential sixth istiophorid billfish species in the eastern North Atlantic, the roundscale spearfish (Tetrapturus georgii), was first suggested by Lowe (1840) based on a cursory description of a single specimen captured near Madeira Island, Portugal, and subsequently by Robins (1974) based on a more detailed morphological examination in 1961 of four individuals caught in the Mediterranean Sea and the eastern North Atlantic. However, given this small sample set of examined animals and an
∗ Corresponding author. Tel.: +1 954 262 3653; fax: +1 954 262 4098. E-mail address: [email protected] (M.S. Shivji). 0165-7836/$ – see front matter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.fishres.2012.10.009
absence of further reports of this billfish since 1961, the validity of the roundscale spearfish remained uncertain until its existence was confirmed genetically and morphologically over four decades later (Shivji et al., 2006; Beerkircher et al., 2008). Despite the roundscale spearfish’s now realized large genetic divergence relative to other billfishes (Collette et al., 2006; Shivji et al., 2006; Hanner et al., 2011), its lack of recognition by fishers and managers until recently is attributed to its strong gross morphological resemblance to the white marlin, Kajikia albida (formerly Tetrapturus albidus), and overall similarity to its congener the longbill spearfish, Tetrapturus pfluegeri. Reliable morphological discrimination among these three species remains challenging, requiring close examination of lateral scale appearance and/or morphometric assessments.
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The roundscale spearfish remains enigmatic in all aspects of its biology, including distribution. Its presence in waters of the western North Atlantic is now unambiguously confirmed on the basis of genetic and morphological examination (Shivji et al., 2006; Beerkircher et al., 2008, 2009) and its occurrence has also been documented within the Caribbean Sea, although based on morphological assessments only (Arocha and Ortiz, 2006a). To date, however, only circumstantial or minimal information is available regarding the potential distribution of this species in other parts of the Atlantic. Arfelli et al. (1986) noted morphological differences among individuals identified as K. albida caught by the longline fleet along the southeastern coast of Brazil, which they attributed to a possible second billfish species. Following documentation of T. georgii in the western North Atlantic (Shivji et al., 2006), researchers are investigating its distribution in other areas. Seven putative roundscale spearfish were captured in the Uruguayan tuna fishery between 27◦ 01 S and 31◦ 58 S in the western South Atlantic (Domingo et al., 2009). However, identification of these individuals was based primarily on the position of the anal opening relative to the origin of the anal fin, which by itself is an imprecise criterion. Within the western North and western Central Atlantic, the historic mis-identification of roundscale spearfish as white marlin has raised important concerns about the accuracy of past white marlin stock assessments given its severely overfished status (Beerkircher et al., 2009). Furthermore, with substantial white marlin catches documented in the South Atlantic and concerns about its stock status in this region also (Anon., 2007), determining the Atlanticwide distribution of the roundscale spearfish is a necessary first step for clarifying the potential for misidentifications with white marlin, as well as longbill spearfish, which also occurs in offshore Atlantic fisheries (Ueyanagi et al., 1970; Arocha et al., 2007; Anon., 2011). Here, we show by DNA analysis that some specimens originally recorded in the multinational Atlantic offshore catch as white marlin or longbill spearfish are roundscale spearfish, and demonstrate that the distribution of roundscale spearfish extends into the central North Atlantic and much of the western South Atlantic up to at least 28◦ 52 S. We also comment on the implications of this larger distribution on issues related to white marlin and roundscale spearfish management in the latter region. 2. Materials and methods 2.1. Sampling and DNA sequencing As part of a separate, ongoing study aimed at checking identities of white marlin and longbill spearfish catch in commercial long-line fisheries outside the western North Atlantic, we discovered that some of the billfish samples possessed mitochondrial DNA sequences that did not correspond to either white marlin or longbill spearfish. We selected 14 of these samples captured across the broadest geographic range (Fig. 1 and Table 1) in our
Fig. 1. Map showing capture locations of genetically identified T. georgii specimens. Capture locations of 14 animals from this study are shown as symbols (() represents single individuals and (䊉) represents three individuals); () represents capture locations of animals from the western North Atlantic reported in Shivji et al. (2006).
sample set for further identification by sequencing their mitochondrial NADH 4L-4 (ND4L-ND4) subunit genes, as this locus unambiguously distinguishes all Atlantic billfish species with the exception of T. pfluegeri (longbill spearfish) from Tetrapturus belone (Mediterranean spearfish) (Shivji et al., 2006). Tissue samples were stored in 95% ethanol until DNA extraction. All laboratory procedures for DNA extraction, PCR, and sequencing and sequence assembly were those specified in Shivji et al. (2006). 2.2. Data analyses Species identification for the 14 samples was determined by maximum likelihood (ML) and neighbor joining (NJ) phylogenetic reconstructions that included previously published billfish species reference ND4L-4 sequences (1268 bp) from Shivji et al. (2006) (GenBank accession numbers in Fig. 2). The Akaike information criterion (AIC), as implemented in Modeltest 2.06 (Posada and Crandall, 1998) was utilized to identify the most appropriate model of DNA evolution for the ND4L-4 sequences. The ML and NJ phylogenetic reconstructions were performed using PAUP version 4.0b10 (Swofford, 1999) which employed the TrN + I model of sequence evolution from Modeltest. The estimated proportion of invariable
Table 1 T. georgii sample identification number (from Fig. 1), GenBank accession number, and capture coordinates. Sample identification number
GenBank accession number
Latitude
Longitude
1 2 3 4 5 6 7 8 9 10 11 12–14
DQ872424 JQ926729 DQ872425 JQ926732 DQ872424 JQ926731 JQ926728 DQ872425 JQ926733 JQ926730 JQ926727 DQ872424, DQ872425, DQ872424
37◦ 41 N 10◦ 57 N 4◦ 25 N 3◦ 48 S 7◦ 43 S 12◦ 23 S 13◦ 08 S 25◦ 46 S 27◦ 13 S 27◦ 11 S 28◦ 52 S 25◦ 30 S–26◦ 30 S
38◦ 52 W 56◦ 00 W 32◦ 08 W 28◦ 41 W 30◦ 45 W 28◦ 54 W 27◦ 58 W 29◦ 21 W 28◦ 41 W 32◦ 13 W 32◦ 59 W 45◦ 30 W–46◦ 30 W
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Fig. 2. Maximum likelihood phylogenetic tree depicting major billfish clades inferred from the mitochondrial ND4L-ND4 genes. The 14 specimens sequenced in this study are indicated in bold. Specimen numbers 1–14 correspond to Fig. 1. Bootstrap values at nodes correspond to maximum likelihood (top) and neighbor-joining (bottom) analyses. Bootstrap values ≥90% are shown for the major clades.
sites was 0.7835. GenBank sequence DQ872417 (Makaira nigricans) was defined as an outgroup for all phylogenetic analyses. The ML tree was constructed by implementing a heuristic search, which utilized random stepwise addition (10 replicates) to acquire the starting trees. Statistical support for branch nodes was determined via nonparametric bootstrap analyses (1000 replicates) using PAUP for both the ML and NJ trees. 3. Results and discussion The ND4L-4 sequences from the 14 specimens comprised nine haplotypes and formed a strongly supported, reciprocally monophyletic group with reference T. georgii sequences from western
North Atlantic animals (Fig. 2). Two of the nine haplotypes were previously published in Shivji et al. (2006). This result confirms the identity of the 14 specimens as roundscale spearfish and the independent evolutionary trajectory for this lineage. The capture locations for the 14 genetically confirmed roundscale spearfish ranged from latitudes 37◦ 41 N to 28◦ 52 S, and longitudes 56◦ 00 W to 27◦ 58 W (Fig. 1 and Table 1), confirming and broadly extending the previously documented range of this species to include the central North and western South Atlantic at the minimum. Based on these findings and the early description of this species in the eastern North Atlantic (Robins, 1974), it seems reasonable to assume that the roundscale spearfish is widely distributed throughout the North Atlantic basin at least
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up to 37◦ 41 N, and along the entire western Atlantic minimally to 28◦ 52 S. The extent of its distribution into the eastern South Atlantic remains undocumented. However, given the occurrence of roundscale spearfish in the far eastern North Atlantic, it is reasonable to assume its range may also extend close to the western African continental margins in the South Atlantic, where white marlin and longbill spearfish are also known to occur (Nakamura, 1985; Kerstetter et al., 2009; Garcia-Cortés et al., 2012). The broad extension of the documented Atlantic distribution of the roundscale spearfish, combined with known species misidentification issues, has ramifications for management and conservation of the species complex comprising white marlin (IUCN Red List Vulnerable status, Collette et al., 2011), longbill and roundscale spearfish throughout this range. 3.1. Implications for white marlin and roundscale spearfish Both white marlin and roundscale spearfish, as well as longbill spearfish, are endemic to the Atlantic Ocean and managed under the authority of the International Commission for the Conservation of Atlantic Tunas (ICCAT). The issue of the abundance and distribution of the roundscale spearfish has become an important factor for white marlin management given the likelihood of species misidentifications. It became apparent from fisheries observer data for this region that recent “white marlin” catches were in fact comprised of a combination of white marlin and roundscale spearfish, with the latter species comprising ∼27% of white marlin recorded catch (Beerkircher et al., 2009). The proportion of the two species may also vary spatially and temporally in specific areas of the Caribbean Sea (Arocha and Silva, 2011). However, the proportions of the two species in historical reported catch data used for ICCAT white marlin stock assessments is unknown, and will be difficult to determine (Anon., 2011). Beerkircher et al. (2009) simulated population assessments using variable hypothetical proportions of the two species over time and showed that varying the proportions had a large influence on the population assessment outcomes for both species in the western North Atlantic, casting considerable uncertainty on past white marlin stock assessments. The vastly extended distribution of the roundscale spearfish documented here to Atlantic regions not considered by Beerkircher et al. (2009) increases the potential for species misidentifications in catch records. In fact, a genetic assessment of 85 white marlin specimens sampled over 18 landings events in 2009 from the Sao Paulo, Brazil-based longline fishery, covering the area spanning 17–35◦ S and 27–52◦ W, revealed 10.6% of the specimens to be roundscale spearfish and 4.7% to be longbill spearfish (author AFA, unpublished). These identification errors occurring over a much larger region also subject to heavy commercial fishery bycatch of white marlin (Anon, 2011) exacerbates the uncertainties in both currently accepted white marlin biological parameters and Atlantic-wide stock assessments. The spatial distribution of the roundscale spearfish documented here indicates considerable overlap with the longbill spearfish in the western South Atlantic (Arocha and Ortiz, 2006b). The two species also share an overall morphological similarity (Nakamura, 1985), resulting in the potential for significant species misidentification errors in fisheries catch data. In fact in a genetic assessment of 100 fishery observer identified longbill spearfish captured in Brazilian longline fisheries between 4◦ 25 N–19◦ 46 S and 23◦ 52 W–39◦ 23 W between June 2006 and November 2007, 49% of the specimens were roundscale spearfish (authors MSS and FHVH, unpublished). The status of longbill spearfish populations is unknown (STECF, 2009). Given concerns that they might be experiencing the same overfishing problems as other billfish, monitoring catches of all spearfish species to aid in their management has been recommended (STECF, 2009). However, the potential for increased
incidence of species misidentification between longbill and roundscale spearfishes in catch data over a South Atlantic-wide region adds to the complexities of such species-level monitoring. The broad distribution of the roundscale spearfish documented here highlights the need for additional vigilance in obtaining accurate species identification for informing management of white marlin, longbill spearfish and roundscale spearfish throughout Atlantic multinational fisheries. Accurately resolving the spatial and temporal catch composition will be essential for improving the reliability of the science that supports the management of these morphologically similar species. Since it is not possible to append the historic catch records, ICCAT has recommended that the upcoming 2012 white marlin stock assessment be recognized as a mixed species assessment (Anon., 2011). However, such mixed species assessments are sub-optimal for conservation of biodiversity and preventing unrecognized declines of individual species that may have lower productivity. Improved species identification by better training of onboard observers as well as fishers (Beerkircher et al., 2008) and broader incorporation of genetic tools (Beerkircher et al., 2009) in the acquisition of billfish catch data is recommended to reduce species uncertainties and accomplish management and conservation goals. Acknowledgements This work was supported by funding from NOAA/NMFS SEFSC, a National Science and Engineering Research Council of Canada Graduate Fellowship (AMB), The Guy Harvey Ocean Foundation, The Brazilian Ministry of Fisheries and Aquaculture, Universidade de Mogi das Cruzes, Unidade de Biotecnologia, FAPESP (proc. 2009/54660-6), and Agencia Paulista de Tecnologia dos Agronegócios, Instituto de Pesca. We thank S. Teter for creating Fig. 1 map. This research was carried out in part under the auspices of the Cooperative Institute for Marine and Atmospheric Studies (CIMAS), a Cooperative Institute of the University of Miami and the National Oceanic and Atmospheric Administration, cooperative agreement #NA1RJ1266. The views expressed herein are those of the authors, and do not necessarily reflect the views of NOAA or any of its subagencies. References Anon., 2007. Report of the 2006 ICCAT Billfish Stock Assessment. Madrid, Spain, May 15–19, 2006. Col. Vol. Sci. Pap. ICCAT 60(5), 1431–1546. Anon., 2011. Report of the 2011 Blue Marlin Stock Assessment And White Marlin Data Preparatory Meeting. Madrid, Spain, April 25–29, 2011. ICCAT, 71 pp. Arfelli, C.A., Amorim, A.F., Galhardo-Amado, J.C., 1986. Analysis on Tetrapturus albidus Poey (1861), caught off south and southeast Brazil (1971–1984). Col. Vol. Sci. Pap. ICCAT 25, 202–217. Arocha, F., Ortiz, M., 2006. Roundscale spearfish. ICCAT Manual. Chapter 2.1.8.4. Available from: http://www.iccat.int/Documents/SCRS/Manual/ CH2/2 1 8 3 SPG ENG.pdf (accessed 04.12). Arocha, F., Ortiz, M., 2006. Longbill spearfish. ICCAT Manual. Chapter 2.1.8.3. Available from: http://www.iccat.int/Documents/SCRS/Manual/ CH2/2 1 8 2 SPF ENG.pdf (accessed 04.12). Arocha, F., Barrios, A., Lee, D.W., 2007. Spatial-temporal distribution, sex ratio at size and gonad index of white marlin (Tetrapturus albidus) and longbill spearfish (Tetrapturus pfluegeri) in the western central Atlantic during the period of 2002–2005. Col. Vol. Sci. Pap. ICCAT 60, 1746–1756. Arocha, F., Silva, J., 2011. Proportion of Tetrapturus georgii (SPG) with respect to T. albidus (WHM) in the Venezuelan pelagic longline catch in the western Caribbean Sea and adjacent Atlantic waters during 2002–2007. Col. Vol. Sci. Pap. ICCAT 66, 1787–1793. Beerkircher, L.R., Lee, D.W., Hinteregger, G.F., 2008. Roundscale spearfish Tetrapturus georgii: morphology, distribution, and relative abundance in the western north Atlantic. B. Mar. Sci. 82, 155–170. Beerkircher, L.R., Arocha, F., Barse, A., Prince, E.D., Restrepo, V., Serafy, J.E., Shivji, M.S., 2009. Effects of species misidentification on population assessment of overfished white marlin Tetrapturus albidus and roundscale spearfish T. georgii. Endanger. Species Res 9, 81–90. Collette, B.B., McDowell, J.R., Graves, J.E., 2006. Phylogeny of recent billfishes (Xiphioidei). B. Mar. Sci. 79, 455–468.
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