First record of the seagrassHalophila stipulacea(Forskkal) Ascherson in the waters of the continental United States (Key Biscayne, Florida)

First record of the seagrass Halophila stipulacea (Forskkal) Ascherson in the waters of the continental United States (Key Biscayne, Florida) | bioRxiv /* */ /* */ <!-- <!-- /*! * yepnope1.5.4 * (c) WTFPL, GPLv2 */ (function(a,b,c){function d(a){return"[object Function]"==o.call(a)}function e(a){return"string"==typeof a}function f(){}function g(a){return!a||"loaded"==a||"complete"==a||"uninitialized"==a}function h(){var a=p.shift();q=1,a?a.t?m(function(){("c"==a.t?B.injectCss:B.injectJs)(a.s,0,a.a,a.x,a.e,1)},0):(a(),h()):q=0}function i(a,c,d,e,f,i,j){function k(b){if(!o&&g(l.readyState)&&(u.r=o=1,!q&&h(),l.onload=l.onreadystatechange=null,b)){"img"!=a&&m(function(){t.removeChild(l)},50);for(var d in y[c])y[c].hasOwnProperty(d)&&y[c][d].onload()}}var j=j||B.errorTimeout,l=b.createElement(a),o=0,r=0,u={t:d,s:c,e:f,a:i,x:j};1===y[c]&&(r=1,y[c]=[]),"object"==a?l.data=c:(l.src=c,l.type=a),l.width=l.height="0",l.onerror=l.onload=l.onreadystatechange=function(){k.call(this,r)},p.splice(e,0,u),"img"!=a&&(r||2===y[c]?(t.insertBefore(l,s?null:n),m(k,j)):y[c].push(l))}function j(a,b,c,d,f){return q=0,b=b||"j",e(a)?i("c"==b?v:u,a,b,this.i++,c,d,f):(p.splice(this.i++,0,a),1==p.length&&h()),this}function k(){var a=B;return a.loader={load:j,i:0},a}var l=b.documentElement,m=a.setTimeout,n=b.getElementsByTagName("script")[0],o={}.toString,p=[],q=0,r="MozAppearance"in l.style,s=r&&!!b.createRange().compareNode,t=s?l:n.parentNode,l=a.opera&&"[object Opera]"==o.call(a.opera),l=!!b.attachEvent&&!l,u=r?"object":l?"script":"img",v=l?"script":u,w=Array.isArray||function(a){return"[object Array]"==o.call(a)},x=[],y={},z={timeout:function(a,b){return b.length&&(a.timeout=b[0]),a}},A,B;B=function(a){function b(a){var a=a.split("!"),b=x.length,c=a.pop(),d=a.length,c={url:c,origUrl:c,prefixes:a},e,f,g;for(f=0;f<d;f++)g=a[f].split("="),(e=z[g.shift()])&&(c=e(c,g));for(f=0;f<b;f++)c=x[f](c);return c}function g(a,e,f,g,h){var i=b(a),j=i.autoCallback;i.url.split(".").pop().split("?").shift(),i.bypass||(e&&(e=d(e)?e:e[a]||e[g]||e[a.split("/").pop().split("?")[0]]),i.instead?i.instead(a,e,f,g,h):(y[i.url]?i.noexec=!0:y[i.url]=1,f.load(i.url,i.forceCSS||!i.forceJS&&"css"==i.url.split(".").pop().split("?").shift()?"c":c,i.noexec,i.attrs,i.timeout),(d(e)||d(j))&&f.load(function(){k(),e&&e(i.origUrl,h,g),j&&j(i.origUrl,h,g),y[i.url]=2})))}function h(a,b){function c(a,c){if(a){if(e(a))c||(j=function(){var a=[].slice.call(arguments);k.apply(this,a),l()}),g(a,j,b,0,h);else if(Object(a)===a)for(n in m=function(){var b=0,c;for(c in a)a.hasOwnProperty(c)&&b++;return b}(),a)a.hasOwnProperty(n)&&(!c&&!--m&&(d(j)?j=function(){var a=[].slice.call(arguments);k.apply(this,a),l()}:j[n]=function(a){return function(){var b=[].slice.call(arguments);a&&a.apply(this,b),l()}}(k[n])),g(a[n],j,b,n,h))}else!c&&l()}var h=!!a.test,i=a.load||a.both,j=a.callback||f,k=j,l=a.complete||f,m,n;c(h?a.yep:a.nope,!!i),i&&c(i)}var i,j,l=this.yepnope.loader;if(e(a))g(a,0,l,0);else if(w(a))for(i=0;i (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0];var j=d.createElement(s);var dl=l!='dataLayer'?'&l='+l:'';j.src='//www.googletagmanager.com/gtm.js?id='+i+dl;j.type='text/javascript';j.async=true;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-M677548'); Skip to main content Home About Submit ALERTS / RSS Search for this keyword Advanced Search New Results First record of the seagrass Halophila stipulacea (Forskkal) Ascherson in the waters of the continental United States (Key Biscayne, Florida) Justin E. Campbell , Aarin-Conrad Allen , Danielle C. Sattelberger , Matthew D. White , James Fourqurean doi: https://doi.org/10.1101/2024.09.02.610701 Justin E. Campbell 1 Florida International University, Institute of Environment, Department of Biological Sciences , 3000 NE 151st Street, North Miami, FL 33181, USA Find this author on Google Scholar Find this author on PubMed Search for this author on this site For correspondence: jcampbel{at}fiu.edu Aarin-Conrad Allen 1 Florida International University, Institute of Environment, Department of Biological Sciences , 3000 NE 151st Street, North Miami, FL 33181, USA Find this author on Google Scholar Find this author on PubMed Search for this author on this site Danielle C. Sattelberger 2 Florida Department of Environmental Protection , Southeast District, 3301 Gun Club Road, MSC 7210-1, West Palm Beach, FL 33406, USA Find this author on Google Scholar Find this author on PubMed Search for this author on this site Matthew D. White 3 Smart-Sciences, Inc. , 15500 New Barn Road, Suite 105, Miami Lakes, FL 33014, USA 4 Unity Environmental University , 70 Farm View Drive, Suite 200, New Gloucester, ME 04260, USA Find this author on Google Scholar Find this author on PubMed Search for this author on this site James Fourqurean 1 Florida International University, Institute of Environment, Department of Biological Sciences , 3000 NE 151st Street, North Miami, FL 33181, USA Find this author on Google Scholar Find this author on PubMed Search for this author on this site Abstract Full Text Info/History Metrics Preview PDF Abstract The first record of Halophila stipulacea is reported for the continental waters of the United States. In August 2024, a small meadow was identified inside Crandon Marina on Key Biscayne, Florida, USA. Following surveys have revealed that H. stipulacea has spread to adjacent areas immediately outside of the marina, often growing either in close proximity to, or interspersed with, the native seagrasses Thalassia testudinum, Syringodium filiforme , and Halodule wrightii . This serves as an initial report and extends the geographic scope of this introduced species in the Western Atlantic basin. Introduction Halophila stipulacea , is a dioecious, euryhaline seagrass native to the waters of the Red Sea, Persian Gulf, and western Indian Ocean. This species of seagrass has drawn attention in recent years as it has expanded its range into nonnative territories. Initially, H. stipulacea crossed through opening of the Suez Canal ( den Hartog, 1972 ; Lipkin 1975a , 1975b ) and has since spread west throughout the Mediterranean Sea (Van der Velte & den Hartog, 1989; Bianchi & Morri, 2004; Gambi et al., 2009 ; Sghaier et al., 2011 ). In recent decades, H. stipulacea has begun an invasive spread for the second time, with new reports of the species across the Caribbean. Here, we report that H. stipulacea is now within the continental waters of the United States (Key Biscayne, Florida), thereby extending its northernmost extent in the Western Atlantic basin. The first report of H. stipulacea in the tropical Western Atlantic occurred in 2001-2002 on the island of Grenada ( Ruiz & Ballantine, 2004 ). Ruiz and Ballantine (2004) hypothesized that this spread occurred from a recreational, luxury yacht departing the Mediterranean. Since this initial report, H. stipulacea has spread northward to St. Lucia and Dominica ( Willette & Ambrose, 2009 ; Steiner & Willette, 2015). In 2014, H. stipulacea was reported off Venezuela ( Vera et al., 2014 ). Since 2017, its spread has been documented throughout the Lesser Antilles, as far north as the U.S. Virgin Islands ( Olinger et al., 2017 ), Puerto Rico and British Virgin Islands ( Ruiz et al., 2017 ). Until recently, reports of H. stipulacea have been restricted to the islands southwest of Hispaniola. H. stipulacea is a fast-growing, pioneering seagrass species, that tolerates a wide range of salinities, temperatures, and light levels, and can withstand various disturbance regimes ( Willette & Ambrose, 2009 ; Short et al., 2010). These factors may have contributed to its rapid expansion across the Caribbean ( Ruiz & Ballantine, 2004 ; Olinger et al., 2017 ; Ruiz et al., 2017 ; Scheibling et al., 2018 ). Within its expanded range, some reports suggest that H. stipulacea can outcompete and replace native seagrasses like Halodule wrightii and Syringodium filiforme ( Winters et al., 2020 ), thus fueling concern over its continued spread. Methods Halophila stipulacea was first sighted inside Crandon Marina (25.72586 N, 80.15594 W) on Key Biscayne, FL in August 2024. Multiple small patches were initially observed along the shallow (∼2m depth) western margins of the interior seawall. Initial samples were immediately collected by hand and returned to the lab for identification. In late August 2024, the largest meadow inside the marina was surveyed for overall dimensions, seagrass percent cover, and total biomass. Ten small quadrats (0.0625m 2 ) were haphazardly tossed within the meadow and seagrass species and percent cover were recorded. Ten seagrass cores (above- and belowground biomass, 0.0625m 2 ) were also haphazardly collected by hand for total biomass. These cores were immediately placed in coolers, returned to the lab, rinsed free of sediment and processed for wet mass (g). Haphazard surveys were also conducted outside of the marina, both along the external margin of the marina entrance and the adjacent shallow seagrass flats and mangrove fringe ( Fig. 1 ). Approximate patch dimensions and seagrass community composition were recorded. Download figure Open in new tab Fig 1. Maps showing the location of Crandon Marina (Key Biscayne, FL). Red shapes indicate the location of H. stipulacea (not to scale). Results Morphological description Collected seagrass samples displayed paired elongated ellipsoid leaves (2.3 – 5.4cm long,0.5 – 0.8cm wide) with obtuse apices and serrulate margins ( Fig. 2 ). Cross veins were present at approx. 45º angles off the midrib vein and petioles (0.9 – 1.7cm long) were ensheathed in translucent scale leaves. Rhizome thickness was approx. 2mm and root length ranged from 2.8 –10.6 cm. Internode length varied and ranged from 1.1 – 2.0 cm. Flowers were not observed in any of our collected samples. Download figure Open in new tab Fig 2. Field photographs of H. Stipulacea inside Crandon Marina (Key Biscayne, Florida) (a,b). Close-up detail of samples collected inside the marina, structure and leaf cross veins (c,d). Photo credits: Matthew White (a,b) and Justin Campbell (c,d). Download figure Open in new tab Fig 3. Photographs of H. Stipulacea outside of the marina, along the mangrove fringe. Many patches were of mixed composition with the native seagrasses, T. testudinum, S. filiforme , and H. wrightii . Photo credits, Justin Campbell. Survey results Nine distinct occurrences of H. stipulacea were located during our surveys, one large meadow within Crandon Marina and eight smaller patches outside of the marina (see Fig. 1 and Table 1 for characteristics). Inside the marina, the meadow consisted of an irregular mosaic of dense H. stipulacea patches, separated by bare silty sediment. No other seagrasses were present; however, some patches did contain several individuals of calcareous green algae ( Halimeda spp). Averaged across the entire marina meadow, H. stipulacea percent cover was 60 ± 12.8% (mean ± SE) and total above-belowground biomass was 360.0 ± 79.2g wet mass / m 2 . Outside of the marina, patches were relatively small (0.8 – 17.4 m 2 ), shallow (∼1m depth), and strictly located along the mangrove fringe to the east of the boat anchorage ( Fig. 1 ). Often these meadows were mixed with the native species Thalassia testudinum, Syringodium filiforme , and Halodule wrightii . View this table: View inline View popup Download powerpoint Table 1. Halophila stipulacea characteristics at surveyed sites at Crandon Marina, Key Biscayne, FL. HS= H. stipulacea ; TT = T. testudinum ; SF = S. filiforme ; HW = H. wrightii . Discussion Our report is comparable to others from the Caribbean documenting the first sightings of H. stipulacea in disturbed habitats such as marinas, ports, or anchorages ( Willette et al. 2014 ).Crandon Marina has ∼250 boats, with the capacity to harbor medium-large sized sailboats (up to 25m in length). These vessels are likely capable of travel to and from areas where H. stipulacea is well-established (Puerto Rico, Virgin Islands), thus serving as a potential mechanism for introduction here in south Florida. Our observations are also consistent with others regarding the overall appearance, dense patches approaching 100% substrate cover. The marina meadow was largest and consisted of dense monospecific patches separated by bare substrate. The meadow did not seem to extend towards the deeper central portions of the marina; however, more thorough surveys are required. Outside of the marina, patches were restricted to the shallow sand halo surrounding the mangrove fringe ( Fig. 1 ). While these patches were predominantly comprised of H. stipulacea , some were interspersed with lower abundances of native seagrasses ( Table 1 ). It is possible that fragments were transported to the external anchorage by sailboats, and those fragments drifted over the native seagrass flat to the mangrove fringe where they settled in the sand halo and became established. It appears that these patches are now expanding both eastward towards the mangroves and westward toward the flat. The native seagrass flat between the anchorage and the mangrove fringe consists of dense T. testudinum and S. filiforme , and we did not locate any H. stipulacea patches inside this area, only along the mangrove fringe. We assert that it will be important to monitor these fringe patches as they begin to approach the dense flat. It is difficult to know exactly how long H. Stipulacea has been at this marina and the surrounding area. However, if we apply mean lateral patch expansion rates (∼0.5 cm/day along one axis) from other observational studies in the Caribbean ( Willette & Ambrose, 2009 ), we estimate that some of the smaller patches (∼1m diameter) outside the marina may be approximately 200 days old, while the medium patches (∼4m diameter) may be approximately 800 days (2.2 years) old. It is likely that the larger meadow inside the marina has also been there for at least several years. While these calculations don”t necessarily account for non-linear rates of expansion, they may provide a first-order estimate of patch age. There are also several other large marinas (e.g. Dinner Key Marina, Miami, FL) and anchorages in the Biscayne Bay area that could serve as additional points of introduction, highlighting further concern and warranting expanded surveys. Biscayne Bay harbors extensive seagrass meadows, some of which have been subjected to multiple ecological disturbances ( Santos et al. 2020 , Santos et al. 2016 ). Furthermore, the broader Florida Keys National Marine Sanctuary contains some of the most expansive (∼16,000 km 2 ) and protected seagrass meadows in the western hemisphere ( Fourqurean & Rutten, 2003 ). Evaluating the potential impacts of this invasive is of paramount importance. Future work is needed to (1) better understand the current extent of this new introduction, and (2) discern under what environmental conditions H. stipulacea can displace native seagrasses (as reviewed in Winters et al. 2020 ). Will this introduction continue to expand, or will it be restricted to disturbed environments such marinas, ports and anchorages? References Bianchi , C. N. , and Morri , C. , 2003 . Global sea warming and “tropicalization” of the Mediterranean sea: biogeographic and ecological aspects . Biogeographia 24 , 319 – 329 . 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A. , Chalifour , J. , Debrot , A. D. , Engel , M. S. , Miller , J. , Oxenford , H.A. , et al. , 2014 . Continued expansion of the trans-Atlantic invasive marine angiosperm Halophila stipulacea in the Eastern Caribbean . Aquat. Bot . 112 , 98 – 102 . OpenUrl ↵ Winters , G. , Beer , S. , Willette , D.A. , Viana , I.G. , Chiquillo , K.L. , BecaCarretero , P. , Villamayor , B. , Azcárate-García , T. , Shem-Tov , R. , Mwabvu , B. (…) Migliore L. , Rotini A. , Oscar M.A. , Belmaker J. , Gamliel I. , Alexandre A. , Engelen A.H. , Procaccini G. & Rilov G. , 2020 . The Tropical Seagrass Halophila stipulacea: Reviewing What We Know from Its Native and Invasive Habitats, along side Identifying Knowledge Gaps . Frontiers in Marine Science , 7 , 1 – 28 OpenUrl View the discussion thread. Back to top Previous Next Posted September 02, 2024. Download PDF Email Thank you for your interest in spreading the word about bioRxiv. 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