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NOAA Integrating DNA Barcoding of Fish Eggs Into Ichthyoplankton

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NOAA Integrating DNA Barcoding of Fish Eggs Into Ichthyoplankton 15 3 NOAA First U.S. Commissioner National Marine Fishery Bulletin established 1881 of Fisheries and founder Fisheries Service of Fishery Bulletin Abstract—The data collected through ichthyoplankton monitoring surveys Integrating DNA barcoding of fish eggs into provide valuable insight into the ichthyoplankton monitoring programs spawning dynamics of multiple spe- cies. Fish eggs, more than larvae, offer a more precise evaluation of Leah A. Lewis1 species-specific spawning character- David E. Richardson (contact author)1 istics; however, egg collections are 2 greatly underused because of the Evgeny V. Zakharov limitations associated with morphol- Robert Hanner2 ogy-based identifications. In recent years, a new means of molecular Email address for contact author: [email protected] identification, termed DNA barcod- ing, has made species identification 1 Northeast Fisheries Science Center readily available across a broad National Marine Fisheries Service, NOAA range of taxa. We used DNA bar- 28 Tarzwell Drive coding to identify ethanol-preserved Narragansett, Rhode Island 02882 fish eggs collected during 2002–2012 2 along the northeastern U.S. conti- Biodiversity Institute of Ontario nental shelf. A subsampling protocol University of Guelph was used to select 1603 unidentified Guelph, Ontario, Canada N1G 2W1 eggs for analysis. DNA sequences were successfully obtained from 1495 (93.26%) of these eggs, repre- senting 50 species—many of which have either never before been iden- Pelagic eggs and larvae, collec- obstacle for the use of fish eggs in tified to the species-level as eggs or tively referred to as ichthyoplank- long-term monitoring and manage- have been identified previously only ton, are the life-history stages of ment programs. to a higher taxonomic level or dur- ing specific developmental egg stag- fish that are most abundant within Historically, the identification of es. In comparison with past attempts the marine epipelagic zone. Be- fish eggs has been limited; illustra- at morphological identification, our cause of this prominence, a number tive guides often reference a small molecular identifications comprise a of long-term ichthyoplankton moni- subsample of eggs from known par- broader diversity of eggs and provide toring programs have been estab- ents or a small quantity of eggs col- a technique with high success rates lished worldwide. The data collected lected during surveys and reared of unambiguous identifications that through large-scale surveys provide through the larval and juvenile stag- is not sensitive to egg stage. Overall, fisheries-independent information on es (Colton and Marak1; Ahlstrom and this work shows that DNA barcoding the spawning locations, times, and Moser, 1980; Berrien and Sibunka2). of fish eggs is sufficiently advanced intensities of multiple species simul- On a broad scale, identifications tra- to be incorporated into long-term, regional-scale ichthyoplankton moni- taneously. Ichthyoplankton data have ditionally have been based on mor- toring programs. also been used to estimate spawning phological characteristics, including stock biomass (Zeldis, 1993) and to egg shape and diameter; number, develop long-term indices of abun- size, and position of oil globules; dance (Richardson et al., 2010a). In width of the perivitelline space; na- contrast to larvae, fish eggs provide ture of the egg yolk and chorion sur- a more precise means of evaluating face; and embryonic pigmentation. the distribution and abundance of spawning fish populations because of 1 Colton, J. B., Jr., and R. R. Marak. 1969. Manuscript submitted 6 April 2015. the reduced cumulative influence of Guide for identifying the common plank- Manuscript accepted: 20 January 2016. egg transport and mortality (Ouellet tonic fish eggs and larvae of continental Fish. Bull. 114:153–165 (2016). et al., 1997; Richardson et al., 2009). shelf waters, Cape Sable to Block Island. Bur. Commer. Fish., Biol. Lab. Ref. 69-9, Online publication date: 5 February 2016. However, the number of identifi- doi: 10.7755/FB.114.2.3 43 p. able egg characteristics is far fewer 2 Berrien, P. L., and J. D. Sibunka. 2006. than the number of morphological A laboratory guide to the identifica- The views and opinions expressed or features available for larval iden- tion of marine fish eggs collected on the implied in this article are those of the northeast coast of the United States, author (or authors) and do not necessarily tification. Consequently, the major 1977–1994. U.S. Dep. Commer., NOAA, reflect the position of the National prerequisite—accurate species-level Northeast Fish. Sci. Cent. Ref. Doc. 06- Marine Fisheries Service, NOAA. identification from eggs—remains an 21, 162 p. 15 4 Fishery Bulletin 114(2) Several of these features remain relatively constant Ocean (Zemlak et al., 2009). The method of DNA bar- throughout embryonic development; however, many coding has also been used to connect the egg and larval characteristics are stage specific. stages of marine species along the coastline of Yucatan, Overall, there are 4 significant limitations involved Mexico, to their adult counterparts (Valdez-Moreno et with morphological identifications. First, natural vari- al., 2010) and for a large-scale larval fish study in the ation in morphological features of fish eggs, within a Straits of Florida (Richardson et al., 2007; Richardson species, is common because of the effects of both mater- et al., 2010b). To date, the DNA barcoding database for nal (Chambers and Leggett, 1996; Marteinsdottir and fishes (Barcode of Life Data System [BOLD], website, Steinarsson, 1998; Marteinsdottir and Begg, 2002) and accessed March 2015) contains sequences of more than environmental (Chambers and Leggett, 1996; Kucera 175,000 specimens, representing more than 15,000 spe- et al., 2002) factors. Second, overlaps in morphological cies (Ratnasingham and Hebert, 2007). These advances, stages and similarities among the eggs of related and coupled with a simultaneous decrease in cost (Richard- unrelated cryptic taxa can lead to incorrect identifica- son et al., 2007), have made it possible to consider the tions (Hyde et al., 2005; Berrien and Sibunka2; Gleason use of DNA barcoding for identification of fish eggs and and Burton, 2012). Third, egg fixation in preservatives to incorporate this approach into ecosystem monitoring causes the loss of natural pigmentation and can obscure programs. the developmental stage of an embryo (Valdez-Moreno In our study, we used DNA barcoding for the large- et al., 2010). Finally, fixation can cause substantial egg scale identification of fish eggs. We sequenced DNA shrinkage, a phenomenon that varies with preservative from eggs that were selected from a 10-year, multisea- type and length of exposure (Hiemstra, 1962). In the sonal archive of 456 ethanol-preserved samples that Northwest Atlantic specifically, descriptions of eggs are exists within the Northeast Fisheries Science Center lacking for more than 50% of fish species, and for those (NEFSC), National Marine Fisheries Service, NOAA. species for which there are descriptions, characteristics Before 2000, fish eggs were identified by using morpho- used to confidently identify field-collected specimens logical criteria. Since 2000, fish eggs collected through may be lacking for some or all stages of egg develop- the NEFSC Ecosystem Monitoring (EcoMon) program ment (Kendall and Matarese, 1994). have been counted but not identified because of a lack Over the past decade, the use of molecular identi- of personnel. The goals of this study are 1) to compare fication techniques has increased in response to the the species identifications, those produced from mor- limitations associated with morphological identifica- phological versus molecular analyses of eggs, in terms tions. For ichthyoplankton, these methods most fre- of species diversity and taxonomic resolution and 2) to quently have involved the use of polymerase chain re- evaluate the feasibility of incorporation of DNA bar- action (PCR) with species-specific primers and probes coding into long-term, regional-scale ichthyoplankton (Shao et al., 2002; Fox et al., 2005; Hyde et al., 2005; monitoring programs. Carreon-Martinez et al., 2010) or the use of multiplex suspension bead arrays (Gleason and Burton, 2012); the former technique is even implemented onboard a Materials and methods research vessel (Hyde et al., 2005) and is used with formalin-preserved samples (Goodsir et al., 2008). Al- Sample collection and processing though these methods have been used successfully, the primary focus in these studies was to discriminate The NEFSC since 1971 has conducted ichthyoplank- among a limited number of species. As a result, these ton surveys multiple times annually along the north- methods rarely have proved versatile enough for use eastern U.S. continental shelf between Cape Hatteras, in fisheries monitoring programs or in large-scale egg North Carolina, and Nova Scotia, Canada (Richardson surveys for which the identification of a wide diversity et al., 2010a). During these surveys, ichthyoplankton of species is necessary. was sampled throughout the water column (to a depth Around 2005, a new means of molecular identifica- within 5 m of the seafloor or to a maximum depth of tion was proposed with the goal of providing a uni- 200 m) with paired bongo samplers that had diameters versal approach to species identification. This concept, of 61 cm and that were equipped with 333-µm mesh termed DNA barcoding, is based on the premise
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