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Marine Biology (2020) 167:85 https://doi.org/10.1007/s00227-020-03698-7 ORIGINAL PAPER Bacterial communities on the gills of bonefsh (Albula vulpes) in the Florida Keys and The Bahamas show spatial structure and diferential abundance of disease‑associated bacteria Christopher D. Dunn1 · Lewis J. Campbell1 · Elizabeth M. Wallace2 · Andy J. Danylchuk3 · Steven J. Cooke4 · Aaron D. Shultz5 · Brooke D. Black6 · Jacob W. Brownscombe3,7 · Lucas P. Grifn3 · David P. Philipp5 · Aaron J. Adams6,8 · Tony L. Goldberg1,9 Received: 21 September 2019 / Accepted: 28 April 2020 / Published online: 30 May 2020 © Springer-Verlag GmbH Germany, part of Springer Nature 2020 Abstract The Caribbean bonefsh species Albula vulpes is an economically important nearshore marine sport fsh that has notably declined in the Florida Keys over the past 20–30 years. The reasons for this decline are unclear, although habitat loss, water quality reductions, climate change, and other environmental drivers likely play a role. Infectious disease can also cause precipitous species-specifc declines in wildlife populations, but virtually nothing is known about infection in bonefsh. We analyzed communities of bacteria on the gills of bonefsh from the Florida Keys, where declines are pronounced, and the islands of Eleuthera and Inagua in The Bahamas, where no such declines have been recorded. Bacterial community composi- tion varied signifcantly among island location (Keys, Eleuthera, Inagua) and among sites within island locations (e.g., tidal creeks, coves, inlets). Seventeen times more bacterial taxa were over-represented in the Florida Keys than in The Bahamas, and several bacterial genera over-represented in the Florida Keys have been linked to environmental contamination and disease (e.g., Corynebacterium; Acholeplasma; Staphylococcus; and Streptococcus). These results show that gill bacterial community signatures may prove useful for investigating bonefsh spatial ecology and that communities of microbes on bonefsh gills contain diferentially abundant and potentially pathogenic bacteria that covary with the overall “health” of the population. Introduction Bonefsh are highly prized as sport fsh and represent a rare example of a recreational fshery that is predominantly Bonefsh (Albula spp.) are a circum-tropically distributed catch-and-release, although they are harvested for con- assemblage of genetically related species with a morphol- sumption in some areas (Danylchuk et al. 2007b; Adams ogy and physiology adapted for benthivory and high-speed and Cooke 2015; Filous et al. 2019). Much of the economic burst swimming (Colborn et al. 1997; Murchie et al. 2011). value of bonefsh is tied to angling and eco-tourism, which can provide sustained revenue for communities close to the nearshore, shallow marine habitats (“fats”) that bonefsh Reviewed by Z. Pratte and M. Reverter. inhabit (Adams et al. 2014). Bonefsh also play important ecological roles in coastal marine food webs (Haak et al. Communicated by K. Clements. 2019; Murchie et al. 2019). Sustainable management of Christopher D. Dunn and Lewis J. Campbell contributed equally bonefsh populations is therefore a priority in both the trop- to this work. ics and sub-tropics (Adams and Cooke 2015). Unfortunately, bonefsh populations in certain locations Electronic supplementary material The online version of this are declining precipitously (Adams et al. 2014). In the Flor- article (https ://doi.org/10.1007/s0022 7-020-03698 -7) contains ida Keys, for example, anglers and guides have reported supplementary material, which is available to authorized users. substantial reductions in catch rates and fsh sizes over the * Tony L. Goldberg last several decades (Brownscombe et al. 2018; Kroloft et al. [email protected] 2019). Given the economic importance of fats fshing to Extended author information available on the last page of the article Florida’s economy (estimated at over $465 million in 2012, Vol.:(0123456789)1 3 85 Page 2 of 11 Marine Biology (2020) 167:85 much of this distributed locally; Fedler 2013), determin- and Rodiles 2015; Pratte et al. 2018), even serving as reser- ing the causes of bonefsh declines is paramount. Proposed voirs of bacterial diversity for complex ecosystems such as factors include habitat loss, water quality declines, weather coral reefs (Reverter et al. 2017). Fish gill microbiomes also and hydrological events, reductions in forage, chemical/toxic refect disease states, such as developmental abnormalities inputs, overexploitation, and interactions among these fac- (Hess et al. 2015) and chronic gastroenteritis (Legrand et al. tors (Brownscombe et al. 2018; Kroloft et al. 2019). Direct 2017). In bonefsh, gills develop during the post-larval life evidence for specifc factors is scant, however, and other stage, such that bonefsh must acquire their gill microbial “fats” species that are also targeted by recreational anglers communities as they metamorphose between 41 and 71 days (e.g., permit, Trachinotus falcatus, and Atlantic tarpon, after fertilization (Mojica et al. 1995; Miller and Tsukamoto Megalops atlanticus) have shown no evidence of similar 2004; Diaz-Viloria et al. 2017). Gill microbiomes should declines. therefore ofer insights that are specifc for the bonefsh juve- Infectious disease can reduce or cause the extinction nile and adult life stages. of wildlife populations, either alone or in synergy with other factors (McCallum 2012; Cunningham et al. 2017). Such diseases include those caused by viruses (e.g., Ebola Methods virus disease in gorillas; Bermejo et al. 2006), bacteria (e.g., hemorrhagic septicemia in antelopes; Robinson et al. Sampling bonefsh 2019) fungi (e.g., white-nose syndrome in bats; Frick et al. 2010), eukaryotic parasites (e.g., trichomonosis in fnches; Bonefsh were sampled by angling (using spinning and Lawson et al. 2012), and even transmissible cancers (e.g., fy-fshing tackle) from nearshore environments in the facial tumor disease in Tasmanian devils; McCallum 2008). Florida Keys and the islands of Eleuthera and Inagua in Infectious diseases are emerging at accelerated rates glob- The Bahamas (Fig. 1; Table S1). Within each of these ally, driven by forces such as pollution, habitat degradation, three locations, fsh were sampled from multiple sites that species invasions, and climate change (Cunningham et al. included tidal creeks, islets, coves, saltwater ponds, and 2017; Young et al. 2017; Ogden et al. 2019), including in similar features. To avoid physiological exhaustion and fsh (e.g., Chen et al. 2018; Combe and Gozlan 2018; Reid to maximize post-release survival, fsh were angled for et al. 2019). Southern Florida is noteworthy as an epicenter minimal duration (Danylchuk et al. 2007a). Once a fsh of invasive species, including their pathogens, due to high was captured, it was briefy removed from the water and a rates of introduction of exotic species and ecological condi- sterile polyester swab with a Dacron tip (Fisher Scientifc, tions favorable for their persistence (Simberlof et al. 1997; Waltham, MA) was inserted briefy between the gill fla- Farrell et al. 2019). Furthermore, certain infectious agents ments and gently rotated approximately fve times. Swabs have narrow host ranges or are pathogenic to only one or were then immediately placed tip-down into a 1.2-ml cryo- a few species within ecological assemblages (McCallum vial (Fisher Scientifc, Waltham, MA) containing 0.25 ml 2012). Infectious disease has not, to our knowledge, previ- RNAlater nucleic acid stabilization solution (Qiagen, ously been considered among the panoply of factors contrib- uting to bonefsh declines. The purpose of this study was to provide a provisional 0 100 200 300 Florida km assessment of the hypothesis that microbes are contributing N to the decline of bonefsh in the Florida Keys (Goldberg WE 2019). We examined diferences in bacterial communities S on the gills of bonefsh from several sites in the Florida 2 Keys, where marked declines have occurred, and in The 1 Bahamas, which are latitudinally and ecologically similar The Bahamas but where bonefsh declines have not been observed. We then identifed bacterial taxa that difered most signifcantly in abundance between the Florida Keys and The Bahamas, and we examined whether those taxa might be associated with disease. We chose to analyze gill bacterial communi- 3 ties because gills are immunologically active organs that are entry points for bacterial pathogens of teleost fshes (Secombes and Wang 2012). Previous studies have shown Fig. 1 Map of sampling locations. The Florida Keys are highlighted the gill microbial communities of fshes to be diverse and in red, the Bahamian island of Eleuthera in dark blue, and the Baha- distinct from those of other body compartments (Merrifeld mian island of Inagua in light blue 1 3 Marine Biology (2020) 167:85 Page 3 of 11 85 Hilden, Germany) and swab shafts were cut fush with Sequence processing the tube opening using sterile scissors, after which tubes were capped and labeled. An approximately 1 × 1 cm fn We used the R (R Core Team 2019) package DADA2 (Cal- clip was then removed from the fsh for genetic analysis lahan et al. 2016) to quality-screen and trim sequence reads. using sterile scissors and placed immediately into a sepa- We trimmed reads at the frst appearance of a base with a rate 1.2-ml cryovial containing 0.5 ml RNAlater. Tubes quality score of two or lower. We then truncated forward containing swab tips and fn clips were stored at − 20 °C reads at 240 bases in length and reverse reads at 160 bases within 6 h of sampling, shipped at ambient temperature to in length to account for diferences in the rate of per base the laboratory, and stored at − 80 °C thereafter. quality degradation between forward and reverse reads. We also removed reads with non-assigned bases (N) and reads mapping to the PhiX sequencing standard. We then applied Molecular analyses DADA2 to detect sequence variants (SVs) and merged paired reads into single consensus reads, after which we In addition to A. vulpes, two other species of bonefsh, A.

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