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The Enigmatic Seagrass

The Complex and Emerging Story of Johnson’s Seagrass

By: Dr. Mark S. Fonseca, Vice President of Science at CSA Ocean Sciences, Inc. and
Dr. Jeanine L. Olsen, Professor of Marine Biology at Groningen Institute for Evolutionary Life Sciences, University of Groningen, The Netherlands

Johnson’s seagrass, (Halophila johnsonii) is native to the Indian River Lagoon System (IRLS) and southeastern Florida coast, where it carries the formal status of a Threatened Species under the Endangered Species Act (ESA). This legally binding label protects it and, by proximity, other seagrasses throughout the entire IRLS. As long as Johnson’s seagrass is listed under the ESA, many forms of coastal development are limited or prohibited and mitigation for its disturbance is not an option.


Image 1.  An individual Halophila decipiens collected from 2m below MLLW in Bocas del Toro, Panama. For scale, the longest leaves shown are 1.5cm in length. Photo credit: Kyle Glenn.

It has been suggested that Johnson’s seagrass may have been misidentified and that it is actually another species within the genus (i.e., Halophila ovalis). H. ovalis is native to the Indo-West Pacific and was unknown in the greater Caribbean area until its discovery on Antigua in 2009 as a presumably human-mediated introduction. If Johnson’s seagrass is equated with H. ovalis, then Johnson’s seagrass could also be considered an introduced species. Reclassification would lead to delisting Johnson’s seagrass from its ESA Threatened status and (as seen for other non-native seagrass species in the U.S.) a possible call for its eradication. A change from “protected” to “intruder” would open the door to stakeholder conflicts with potentially negative ecological consequences for other seagrasses and the IRLS more generally.

Here we provide a perspective on controversies surrounding Johnson’s seagrass with respect to species identification, its ecological status as a possible introduction, the consequences of a decision to delist, and some reflections on what listing achieves. We conclude that continued listing as “Threatened” remains warranted based on the scientific evidence.

An Overlooked Foundation
In the estuaries and lagoons of southeast Florida exists a small marine plant with unique status: it is the first and only marine plant to be listed as Threatened under the Endangered Species Act (ESA). This plant is Johnson’s seagrass (Halophila johnsonii) named after one of the patrons of Harbor Branch Oceanographic Institution where much of the early work on this species occurred. H. johnsonii was described as a species in 1980 (Eiseman and McMillan, 1980). The decision to list the seagrass in 1998 (Federal Register 98-24357) was based on meeting criteria defined in the ESA. Restricted distribution (plants occur only along ~125 miles of Florida coast from Miami to just south of Cape Canaveral (Eiseman and McMillan, 1980; Kenworthy, 1993; Virnstein et al., 1997; Virnstein and Morris, 2007), unusual asexual reproduction evidenced by a lack of male plants, and its vulnerable habitat in the Indian River Lagoon System (IRLS) supported its formal listing as ‘Critical Habitat’ in 2000 (Federal Register 65 FR 17786; Box 1).


Box 1 - Critical Habitat
Federal Register 65 FR 17786: Critical Habitat can be designated within the geographical areas occupied by the species at the time of listing if they contain physical or biological features essential to conservation, and those features require special management; or outside the geographical areas occupied by the species if the agency determines that the area itself is essential for conservation. Critical habitat designations must be based on the best scientific information available, in an open public process, within specific timeframes. A critical habitat designation does not set up a preserve or refuge; it applies only when Federal funding, permits, or projects are involved. Under Section 7 of EST, all Federal agencies must ensure that any actions they authorize, fund, or carry out are not likely to jeopardize the continued existence of a listed species, or destroy or adversely modify its designated critical habitat.


Seagrasses are marine flowering plants that pollinate, set seed, and exist almost entirely underwater. Approximately 12 seagrass species are found in North America (six in the IRLS) and >70 worldwide. It must be said “approximately” as the definition of what is and is not a species looms large in attempts to understand the status of this plant in Florida waters.

Seagrasses, including the diminutive Halophila genus (Image 1), are among the most productive plant communities in the world. They provide critical ecosystem services, including sediment stabilization, water column filtration, carbon burial, and—in particular—refuge, feeding, and nursery habitat for a tremendous number of juvenile fish, shrimp, and crabs. Charismatic grazing animals, including manatees, dugongs, and sea turtles, feed directly on seagrasses for much of their nutrition. Seagrasses are, thus, a critical part of the foundation for the lagoon ecosystem. More than 15,000 papers have been published in scientific journals (Web of Science, keyword seagrass) that establish the importance of seagrasses to coastal ecosystems (see reviews by Larkum et al., 2006; Duffy et al., 2014).

There is worldwide concern for seagrasses, which are being lost a an alarming rate (Orth et al., 2006; Waycott, 2009) and almost entirely from human impacts, including destruction from dredging, filling, algal blooms/overgrowth associated with coastal pollution (arising from nutrient loading), sediment runoff, and vessel impacts (moorings, groundings, prop scarring) (Grech et al., 2012). In Florida, seagrasses are protected by both state and federal laws. A formal economic valuation of seagrass ecosystem services (Costanza et al., 1997, 2014) ranked their value per unit area as second only to estuaries overall.

Florida enjoys the greatest seagrass acreage in the contiguous U.S., conservatively mapped at approximately 2.1 million acres of nearshore (Yarbro and Carlson, 2011) and several million more acres offshore (Iverson and Bittaker, 1986; Continental Shelf Associates, Inc., 1989). Those millions of acres of offshore seagrass beds are composed almost exclusively of Halophila beds, both paddle grass (H. decipiens; Image 2) and star grass (H. engelmannii; Image 3), stretching along the entire west coast of Florida in waters between ~30 and 100 ft in depth. Unlike the other Florida seagrasses, Halophila species are all very small with leaves rarely exceeding an inch in overall length and with stems and leaves together no more than 1 to 3 inches in height overall. In contrast, Florida’s large seagrasses such as turtle grass (Thalassia testudinum) and shoal grass (Halodule wrightii) have strap-like leaves exceeding a foot in length; manatee grass (Syringodium filiforme) can sometimes exceed 2 ft in length. Small size tends to mean overlooked, but small does not translate to unimportant. The areal coverage and rapid turnover of Halophila species is enormous, more than compensating for its small size by the mobilization (as well as sequestration) of carbon and nitrogen up the food chain (Burke et al., 2003; Fourqurean et al., 2012).

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Image 2. Paddle grass (Halophila decipiens) on a shallow sand bar inside Palm Beach Inlet, Florida. The typical paddle-shaped leaves are intermixed with the narrower leafed (arrows) Johnson’s seagrass (Halophila johnsonii). Photo credit: Mark Fonseca.

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Image 3. Star grass (Halophila engelmannii) showing its characteristic floret of multiple leaves per shoot. Photo credit: Txmarspecies.tamug.edu.


Much of the Halophila resource in Florida (except for H. johnsonii) is highly seasonal, often relying on seed set to overwinter with new recruitment in the spring (e.g., most of the seagrasses on the west Florida shelf) (Fonseca et al., 2008; Bell et al., 2008). Growth is rapid with individual leaves being shed after 6 to 10 weeks, whereas during their growing season they are continuously generated from the apical meristems (growing points) of a horizontal rhizome (underground stem and root system) similar to a strawberry runner (Image 1). Such high productivity (i.e., photosynthesis and generation of new biomass), along with associated seafloor microalgae comprise the primary production base of the nearshore food web of the eastern Gulf of Mexico (Burke et al., 2003). Like the Serengeti grasslands of Africa with its many large and small animal grazers, seagrass meadows have a similar structure. In seagrass ecosystems, this includes grazing marine mammals (manatees), turtles, and some fish as well as hundreds of species of tiny animals and juveniles stages of larger animals that graze on epiphytes (algae and other organisms that grow on seagrass leaves) to form intermediate linkages of the food web.

Vulnerability And The Downward Spiral
When seagrasses are lost, habitat quality diminishes precipitously and associated organisms disappear leading to a steep loss in biodiversity that may be almost impossible to regain. Ecosystem changes are almost never caused by a single factor but rather several factors that interact in complex, non-linear ways. Thus, shifts in the community structure and function are typically abrupt rather than gradual. Such shifts are called tipping points or regime shifts. Scientists are beginning to understand the fragile dynamics of stability, resilience, and what combinations of factors (also called cumulative effects) are most likely to produce tipping points (e.g., Nystrom et al., 2012; Dakos et al., 2015). However, this understanding has only recently begun to be applied to seagrass ecosystems (Koch et al., 2009; Brown et al., 2014).

Seagrass-based systems are especially vulnerable to the downward spiral of degradation and are difficult to restore once lost (Van Katwijk et al., 2015). The vulnerability of seagrasses in general and Johnson’s seagrass in particular is why further action was taken in 2000 to protect its Critical Habitat, with follow-up reports recommending continued listing as Threatened from the National Marine Fisheries Sanctuary (NMFS) in 2002 and 2007.

An Ounce of Protection is Worth a Pound of Cure
While all seagrasses are protected by government regulations, Johnson’s seagrass receives added protection as a Threatened Species under the ESA. This means that not only is disturbance of the seagrass prohibited, but compensatory, mitigative options to offset any impacts are also prohibited (e.g., creation of new habitat and acreage elsewhere). This “no-disturbance status” directly limits private development options as well as public projects—particularly those involving dredging.

Unlike options with crop plants on land or restoration of freshwater wetlands where there are various site-engineering options available, seagrass restoration must frequently be undertaken at sites that have already been disturbed by humans and not re-engineered for seagrass needs (see www.csaocean.com/press-releases/csa-completes-sea grass-mitigation-for-miami-harbor). In general, seagrass restoration involves overcoming factors that limit recruitment of plants to an area that may involve poor sediment, poor water clarity, changed hydrodynamics, animal disturbance, storms, or combinations of these and other environmental factors. Selection of suitable sites for restoration of seagrass (where they are currently absent) is questionable because the limiting factors are typically unknown or not addressed. The governing question is, “If there is no seagrass there now what makes you think you can make it grow there?” (Fredette et al., 1985). In short, reliable, long-term restoration absolutely depends on careful attention to understanding limiting factors and site selection.

The effectiveness of mitigation through transplantation of mature plants and/or seeding has been most extensively investigated in the seagrass Zostera marina. Bays in southern California and parts of Chesapeake Bay, Virginia have met with good success in many cases, whereas many efforts elsewhere have failed. As of the last U.S. national study (Fonseca et al., 1998), the restoration success rate for all seagrass projects was about 50%. In a recent worldwide analysis of 1,786 restoration trials, Van Katwijk et al. (2015) found that overall survival rate after 36 months was 37% and that the low rate was largely attributable to the small scale of the trials (i.e., 55% involved <1,000 specimens planted); whereas a 42% survival rate after 36 months was found for large-scale trials (>100,000 specimens planted). Transplant efforts are also expensive at up to ∼20,000 USD/acre for just the planting alone.

Although natural seeding techniques show promise in eelgrass (Z. marina) (Marion et al., 2010), current restoration techniques still mainly rely on transplantation of mature plants or portions thereof. Restoration techniques for Halophila species including Johnson’s seagrass remain experimental and very small scale (Baca et al., 2006; Heidelbaugh et al., 2007). Further complicating the potential for mitigation of Halophila is its ability to shift locations (Morris et al., 2007). Management strategies for shifting patchiness, which is far less frequent for larger seagrasses, are not well defined and thus pose a significant challenge for regulatory agencies, the key question being, “Is the change in observed areal cover due to natural fluctuations or human-induced disturbance and over what timescale?” Restoration of Halophila habitats, with their extreme temporal and spatial dynamism, would represent a tectonic shift in the way regulatory agencies currently approach seagrass management.

The reasons for poor restoration success of seagrasses are related to the sensitive biological and physical dynamics of the system, especially where there is degradation of the habitat at the outset of the restoration effort (and the beginnings of a downward spiral in ecosystem function). Planting seagrass is not the same as replanting grass in your backyard. Further, the very existence of mitigative options for seagrasses opens the legal door to permitted disruption of seagrass beds, which despite federal and state habitat protection, continue to decline in many areas. In the specific case of H. johnsonii, poorly understood seasonal dynamics and exclusive asexual reproduction further limit mitigative options and lead to the provisional conclusion that continued protection remains the best option.

Species - Still At The Frontier Of Science
It is necessary to delve into the biology of Johnson’s seagrass, particularly its method of reproduction because this weighed heavily in the decision to classify Johnson’s seagrass as a Threatened species.

Missing Sex And Clonality
Flowering plants come with one of two general reproductive strategies; they have either both male and female flowers on the same plant (monoecious/hermaphroditic) or each sex and flower type on a separate plant (dioecious). Examples of plants that are monoecious include oaks, fir trees, walnuts and figs, to name a few, as well as some seagrasses (Zostera species). Well-known examples of dioecious plants include hollies, asparagus, dates, mulberry, spinach, and most seagrasses. Species in the genus Halophila are dioecious. Interestingly, no male plants of Johnson’s seagrass have ever been found (Eiseman and McMillan, 1980; York et al., 2008)—only female plants. A common compensatory mechanism in plants for loss of males is apomixis (called agamospermy) and this was hypothesized for H. johnsonii (York et al., 2008). It involves the absence of meiosis during formation of the egg cell and subsequent direct development of an unfertilized female “seed”; meiosis being the reductive cell division process in which chromosomal DNA is halved. However, York and colleagues found normal meiosis in female embryos of H. johnsonii and that unfertilized female embryo “seeds” did not germinate; they simply needed pollen (i.e., males).

Another common mechanism leading to loss of sexuality in plants involves various types of polyploidy (i.e., extra sets of chromosomes that can arise in various ways) (Box 2) and sexual incompatibilities arising through mating with relatives or closely related sister species (hybridization). The key point is that a natural loss of sexuality in plants, including the loss of one sex in a dioecious species, is common and can be caused by a variety of environmental and genetic mechanisms, especially in geographically isolated populations, as fits the case with H. johnsonii (reviewed in Barrett [2015]).


Box 2 - Plant Propensities
Polyploidy (extra sets of chromosomes that can arise in various ways) and hybridization (mating with relatives or closely related sister species) are common and can produce mixed gene sequences due to the presence of paralogues (different version of a sequence due to the duplications). Polyploidy has not been extensively studied in seagrasses, but polypoid events have been documented in Halophila, specifically in the H. ovalis complex (York, 2005).

Hybridization has been documented between some Zostera species (Coyer et al., 2008; Olsen et al., 2014). However, this has not been studied in Halophila, the observation that the genus has many described species as compared with other seagrass genera. Moreover, existing phylogenies show evidence of genes products arising from a common ancestor (parology) and paraphyly (a group is paraphyletic if it consists of the group's last common ancestor and all descendants of that ancestor; Short et al., 2010), suggesting that one or both of these mechanisms could be at work.


Aside from sexual anomalies, asexual reproduction via vegetative propagation is also extremely important in seagrasses and is the primary means of propagation for Johnson’s seagrass (Hall et al., 2006). This involves rhizome extension, fragmentation, and colonization of those fragments in the sediment. Many plants reproduce in this manner including other Halophila species. Thus, although absence of males and asexuality are often associated with introduced and invasive species, there are many other reasons why a plant can be asexual and why one sex may be missing.

The deeper question is whether a species can exist over the longer term without sexual reproduction and whether asexual species are recognized. The answer is yes. While the absence of sex reduces genetic variation (because there is no opportunity for mixing new combinations of chromosomes through a process called recombination), it is also true that asexual species can exist pretty much indefinitely as long as environmental conditions remain favorable (Birky and Barraclough, 2009). Physiological integration, mutations arising from cell division, and large clone size have been shown to enhance resistance, thus shielding long-lived individuals from environmental changes (up to a point; discussed in Barrett [2015]). Examples of ancient clonal plants include aspen trees (Populus spp.) up to 80,000 years old, the Mediterranean seagrass Posidonia oceanica whose clones may extend back 100,000 years (Arnaud-Haond et al., 2012), and thousand-year-old giant clones of the seagrass Zostera marina in the Baltic (Reusch et al., 1999). The key point is that the absence of male plants of Johnson’s seagrass and the presence of long-term asexual reproduction do not equate with evolutionary doom, but it does establish a distinct population segment and greater vulnerability due to reduced genetic variation.

Identity Crisis
As early as 2002, it was suggested that H. johnsonii was possibly H. ovalis based on a phylogenetic comparison using nuclear rDNA-ITS sequence (Waycott et al., 2002). Although the results were inconclusive, Green and Short (2003) described a range extension of H. ovalis to include the Florida coast in their World Atlas of Seagrasses. York (2005), who was investigating polyploidy in Halophila, also constructed a phylogeny for the H. ovalis cluster/complex based on the chloroplast DNA trnL gene, which placed H. johnsonii in a sub-clade with H. ovalis from Zanzibar. York also provided evidence for polyploidy in Halophila, determining that three such events have occurred in the genus with the most recent one in H. ovalis species complex. At the time, not much attention was paid to these various results, in part because the taxonomic difficulties of the H. ovalis cluster/complex were well known and the confirmation of polyploidy just added more confusion.

The issue of species identity of Johnson’s seagrass was not considered again until 2009. Short et al. (2010) reported H. ovalis in Antigua (Caribbean), a surprising finding as the species is Indo-West Pacific in its distribution. The Antigua specimen was sequenced and compared against the same samples of H. johnsonii and a subset of H. ovalis individuals used by Waycott et al. (2002). It confirmed that the Antigua specimen belonged to the H. ovalis cluster/complex and that the sample was identical in its ITS sequence with the H. johnsonii sequence. However, there were also other species mixed in the cluster/complex differing by only one or a few nucleotides (i.e., H. euphlebia, H. australis, H. hawaiiania, H. johnsonii, H. nipponica, and H. minor), including many biogeographic isolates of H. ovalis from distant locations. This raised a number of questions: Had H. johnsonii naturally dispersed from the IRLS or been introduced to Antigua? Had H. ovalis been introduced or was H. ovalis a rare species in Caribbean that had been missed by seagrass scientists? We will return to these questions, but first let us return to species concepts versus an operational definition of species.

Defining Species Operationally
The ESA is mute on the definition of a species (Box 3) in the common biological sense and relies implicitly on scientific expertise to determine what is and is not a species (Gleaves et al., 1992). The operational definition of what constitutes a species is not fixed and this often comes as a surprise to non-biologists. Thus, there is a collision of sorts between scientists who embrace evolving information and that of public law, which typically does not.


Box 3 - ESA’s Use of the Term “ Species”
“ The term species includes any subspecies of fish, wildlife or plants, and any distinct population segment of any species of vertebrate fish or wildlife, which interbreeds when mature".

No further elaboration of “ species” is given in the ESA. “ Subspecies” or “ distinct population segment” is recognized but not defined. Further, ESA states, “ Deference is given to scientific assessment in combination with discretion of ESA… many cases involve scientific uncertainty and disagreement. ESA has latitude in its judgement.

Even IUCN (International Union for Conservation of Nature) does not define a species. They use population / subpopulation. Population is defined as “ the total number of individuals of a taxon.” Subpopulations are defined as “ geographically or otherwise distinct groups in the population between which there is little exchange.” www.iucnredlist.org/static/categories_criteria_2_3#definitions

In this case, it is worth mentioning that these definitions were developed with an eye towards fish stocks.


The standard definition of a species taught in introductory college courses is the biological species concept, which relies exclusively on reproductive isolation. Under this definition, if an individual can, through mating, produce another fertile individual (i.e., itself capable of producing offspring) then that individual and its mate are considered to be of the same species. If not, then the individuals are said to be reproductively isolated from one another and, thus, different species. Many animals that we see as individual species can mate and produce young (e.g., donkey and horse that produce mules) but those hybrid offspring are most often sterile and so cannot transmit their genes to another generation a reproductive and evolutionary dead-end, reinforcing recognition of donkeys and horses as different species. Plants, however, do not fit neatly into the classic species definition that dates back to the 1940s and was originally based on studies of birds. Plants are often promiscuous (self-fertilizing and outcrossing [mixing strains]) and/or utilize both sexual and asexual forms of reproduction. Reproductive isolation is thus not a hard criterion and speciation can be rapid (almost instant) through polyploidy and related mechanisms. See Box 4 for a discussion about how species arise.

Using an organism’s physical appearance (shape, size, and morphology, referred to as the phenotype) by itself to define a species also lost credibility as researchers recognize the great variation that occurs in nature. Early taxonomists thought about species as static entities based on “types” (i.e., a standard set of morphological/anatomical features). Slight deviations in morphology were considered adequate for describing a new species. Taxonomists taking this to the extreme were known as “splitters.” In contrast, those who accepted a lot of morphological variation were known as “lumpers.” These differing philosophies have played havoc with the taxonomy (i.e., biodiversity estimates) of many groups, including seagrasses—especially Halophila. What we now know is that most organisms are morphologically “plastic” (i.e., capable of dramatically changing their shape and size in response to environmental conditions). Some species do so more than others. For example, when a common seagrass (eelgrass; Zostera marina) that dominates most of the temperate zone of North America was transplanted among depth zones, the plants took on the physical shape of those already at that depth. Shallow plants became longer when moved to a greater depth and vice versa (Phillips, 1976).

Conversely, there are also cases in which species are morphologically identical but are actually different species. These are called cryptic species. This discovery of cryptic species was one of the rude awakenings of the 1980s and 1990s as DNA sequencing and genotyping data became widely available. The important point is that the fact that two entities look alike is no guarantee that they are the same species—and likewise the fact that two entities look different is no guarantee that that are indeed different species. Here, it’s DNA to the rescue—at least in most cases.

Comparative DNA sequencing is the most common method for identifying, separating, and determining species relationships with one another. This is because DNA carries the evolutionary history of organisms that allows scientists to construct the “family tree” back through thousands and even millions of generations. While the principles are simple enough to understand, as usual, the devil is in the details.

Selection of the pieces of DNA to be sequenced (i.e., reading the order of the nucleotides A, T, C and G; the letters of the genetic code) from the genome have to be appropriate for the period of interest (i.e., ancient event or recent event). If the DNA chosen is evolving slowly, it will be good for sorting out older species and deeper lineage relationships that have been separated for a long time, but not for recently evolved species because there will be no observed variation in the DNA. The more different two DNA sequences are, the longer ago they diverged. Rapidly evolving DNA sequences are needed to detect recently evolved species and can be difficult to find if the species are really, really recently diverged.

A phylogenetic analysis at the species level assumes that the compared differences are “fixed” (i.e., not variable among individuals sequenced). In contrast, a phylogenetic analysis at the population level, as is the case when populations of a species are diverging through genetic drift (Box 4), are not fixed but variable. In most cases, DNA sequences of a few genes (sometimes one) can provide unequivocal evidence of species identity as compared with other species in the genus. However, in other cases, single sequence comparisons may not be definitive.


Box 4 - Thinking Deeper About How Species Form
Geographic isolation (also called allopatry) is an important driver of speciation and may lead to eventual reproductive isolation. This works as follows: as populations of individuals become physically separated and isolated, their gene pools will initially be the same but little by little, they will begin to diverge. This occurs through the process of genetic drift (i.e., random changes in gene frequencies that occur by chance and that are affected by the size of the population; small populations experience drift more strongly and can lose variation relatively quickly). Over time, the populations diverge and may become reproductively isolated.

A second process affecting speciation is natural selection by the environment (sometimes called ecological speciation). Within a population, different combinations of genes are shuffled and reshuffled through sexual reproduction. Some of the gene combinations are ecologically advantageous (e.g., produce individuals that can withstand higher temperatures) and the individuals possessing these successful combinations (called genotypes) contribute more offspring to the next generation (i.e., “ survival of the fittest” ). Little by little, over many generations, the populations adapt in this way to their respective environments and may become reproductively isolated. In the case of plants, even if sexual reproduction is lost, genotypes/clones that are well adapted to their environment will continue to survive through asexual/clonal reproduction as long as the environmental conditions do not change beyond the capacity of the individuals living there. Clonal species form persistent and remarkably resistant habitats (see above section on Missing Sex and Clonality).

The processes of genetic drift and natural selection are not either/or. The two occur together with the relative importance of each dependent on the size of the population and the environmental regime being experienced. Two other processes (i.e., dispersal/ gene flow and mutation) also play a role. Speciation is thus a dynamic process with a highly variable time frame. Exactly when speciation can be said to be complete (e.g. reproductively isolated) is seldom known and can be hard to determine in practice. Moreover, many species are never reproductively isolated. The fact is, if reproductive isolation were the only criterion, then the vast majority of “ species” on Earth would no longer be species. However, let us not get carried away. Most scientists take the conceptual view that morphological and genetic distinctness will lead to eventual reproductive isolation.


There is no agreement about how divergent two entities have to be in order to be designated separate species. If sequence divergence is strong (e.g., many nucleotide differences based on multiple genes [typically three to five]) and the taxa form a single group (called a monophyletic group or clade), then there is seldom an argument. In contrast, when species or lineages are very, very recently diverged and only a few nucleotide differences are present, interpretation becomes problematic (see Box 2). In short, when divergence is minimal and different genes give different divergences (or lack thereof), then it becomes a judgement call. In its way, this issue is similar to the “splitting” and “lumping” mentality encountered with morphological data discussed earlier. Applying a fixed operational definition of “when is a species a species” fails, as there is “no one size fits all.”

Many Halophila species are both morphologically distinct and genetically divergent to the extent that no one is in doubt as to them being different species. The exception is H. ovalis, which is highly morphologically plastic (leading to much taxonomic confusion at the morphological level), as well as molecularly polymorphic at the DNA level. This is why researchers refer to these taxa as members of the “ovalis cluster/complex.” Over the past 80 years, every specialist in taxonomy has been confronted with this problem and only now are the theory and methods becoming available to sort out these issues. In fact, the very nature of the speciation process is being reinvestigated in our new genomics era.

H. johnsonii is certainly morphologically distinct (the basis for its original taxonomic description) as well as strongly divergent from H. engelmannii and H. decipiens (its two Florida congeners) and others based on DNA sequence data. However, more recent morphological comparisons of H. johnsonii with H. ovalis suggest that H. johnsonii is within the range of morphological variation found in H. ovalis and DNA sequence comparisons also place H. johnsonii in the “ovalis cluster/complex” (Short et al., 2010). Note, however, that at the ITS sequence level, there is also considerable divergence within and among taxa found in the “ovalis cluster/complex.” As mentioned earlier (see Identity Crisis), this involves not only H. johnsonii, but also H. hawaiiana, H. euphlebia, H. nipponica, and H. minor). There are also disparate, biogeographic isolates of entities recognized as H. ovalis. This state of affairs is classic in cases of nascent or incomplete speciation.

The Problem Of Weak Direct Evidence
Is H. johnsonii really H. ovalis? The verdict is not likely to be in any time soon. (See companion article, Molecular Approaches to Johnson's Seagrass). What can be said is that the two taxa are very closely related based on DNA sequence data. If one wishes to take a “lumpers” approach, then several currently recognized Halophila species (mentioned above) would be merged into H. ovalis, including H. johnsonii. Conversely, one could apply a “splitters” approach maintaining that the two taxa are separate. Reproductive isolation is already a weak criterion in plants and combined with the asexuality prevalent in seagrasses, and H. johnsonii, in particular, offers little help. Likewise, the morphological variation expressed in seagrasses and in the Halophila ovalis “cluster/complex” also provides little help for H. johnsonii.

On a positive note, there is no doubt that H. johnsonii is a distinctive, asexual form characterized by a “unique population segment” in the IRLS and is a possible sub-species/species closely related to H. ovalis “cluster/complex.” This concept fits well into the ESA definition of Threatened—but there is still the issue of introductions.

Introductions Revisited
Over the past 30 years, scientists have come to realize that, as seen for terrestrial species, marine species not only disperse/migrate but are also moved around the planet by humans (Carleton & Geller, 1993). Seagrasses are no exception. Here, too, it has been suggested that Johnson’s seagrass may be nothing more than a range extension or introduction of the circumtropical H. ovalis cluster/complex and therefore not Threatened, where being listed as Threatened has created an onerous regulatory framework in the midst of highly valuable real estate. This is a very thorny supposition.

Range Extensions
Species have natural biogeographic distributions (Box 5). Some species are widespread and others restricted. Many factors affect the range of a species but the most important ones are “ecological envelops” governed chiefly by temperature in combination with long-distance dispersal ability (or lack thereof). Within these envelopes, additional factors and interactions can also play a role, including species interactions with respect to competition and predation. A species may arrive in a new location only to find incompatible physiological conditions or to be competed away.


Box 5 - Coming to Terms - Range Extensions, Introductions, and Invasive Species

Range expansion refers to the natural dispersal of a species into a wider geographic area. This is often brought about by changing climate, current patterns, or species interactions. Under current climate warming, many species are shifting their ranges north into cooler waters. This does not make them, per se, invasive.

Native species are those that naturally occur and are limited to a particular geographic area. They are also called endemic species. The area occupied can be extremely limited as is the case with Halophila johnsonii or extremely broad as is the case with H. ovalis.

Non-native species (also referred to as aliens or exotics) have been introduced either accidentally or intentionally by humans. They may be assimilated into the ecosystem at the new location with few effects on the ecosystem/environment or in, some cases, can become invasive.

Invasive species are introductions that produce negative effects on the environment, the economy, or human health. Note that "introduced" is not automatically equivalent to "invasive." Many introductions are not ultimately invasive.


With climate warming, biogeographers observe that many species are shifting ranges, mostly to the north or to higher altitudes (in the northern hemisphere) as conditions warm. This phenomenon has also been observed in seagrasses: the loss of Z. marina in southern Portugal but gains in cooler, northern latitudes (or to deeper water if water clarity is good); shifts of Thalassia testudinum in the western Caribbean, and potentially gradual northward movement of H. johnsonii along the eastern Florida coast. Historically, environmental change has been a catalyst for dramatic and sometimes perplexing rapid changes in plant community expansion (e.g., Reid’s Paradox—how oaks spread over hundreds of miles in northern Britain following the last ice age, far beyond the understood ability of the species to colonize space). A range extension of a species is a natural phenomenon and should not be confused with an introduction (which is a human-mediated range extension event) and then regarded as a “nonnative.” Semantics are important.

As species shift their ranges, the associations among resident and newly shifted species may change. In the specific case of an introduction that turns out to be invasive, competitive interactions are likely to result in a new community assembly. This appears to be the case for H. stipulacea (Willette et al., 2014) as it is comparatively aggressive in its colonization of the seafloor (Fonseca, M., personal observation). Arrival of H. stipulacea in south Florida could create another ecological dilemma if again found to be a competitor with other seagrasses. In contrast, there is no evidence that H. johnsonii is likely to become invasive elsewhere in the Caribbean as it is not a strongly competitive species (National Marine Fisheries Report, 2007).

Johnson’s niche in the IRLS typically occurs in areas where other seagrass species are unable to grow although it is also found mixed with other seagrass residents (Image. 2). In addition, its shifting patchiness and geographic distribution are its natural dynamic (Virnstein et al., 2009). The important point is that without a very long-term study to understand how a species naturally disperses, successfully colonizes, and vacates space over time (especially in light of climate warming), short term changes in distribution (simultaneous with changing levels of effort at detection of range changes) are meaningless in support of a timeline of introduction or invasiveness.

Human-mediated transport takes three principle forms for seagrasses. The first is via boats and entanglement of seagrass plants on anchors, nets, and other gear. There are literally tens of thousands of yachts and fishing vessels plying the waters of the Greater Caribbean and Florida as well as from around the world to these destinations. The Red Sea/Mediterranean seagrass Halophila stipulacea was discovered in Grenada, Caribbean in 2002 and has since spread to 19 islands throughout the Eastern Caribbean (Ruiz & Ballantine, 2004; Willette et al., 2014). Boating-related vectors are the most likely culprit but no pathway has yet been proven.

The second means of introduction is via aquarium shop and/or Internet sales (Walters et al., 2006) that may lead to eventual aquarium escapes, as documented for seaweeds (e.g., Caulerpa taxifolia in the Mediterranean and the tropical Indo-West Pacific lionfish in the Caribbean). “Seagrass aquarium gardens” featuring Halophila and other species can be purchased over the Internet. As far as we know, there are no documented cases of introductions of seagrass species by this means although the potential has not been rigorously examined.

Last is the case of piggybacking associated with shellfish aquaculture. The Japanese seagrass Zostera japonica has spread through parts of the Pacific Northwest (coast and Puget Sound), apparently having arrived ~50 years ago as packing material with live oysters imported for both food and aquaculture into the region from Japan. Stakeholder conflicts that have developed (seagrass preservation versus eradication) in combination with confusing science-to-policy links provide a cautionary tale (reviewed in Shafer et al., 2012) that we hope won’t be replayed in Florida. Rarity has also been proposed as an explanation for new reports of species range extensions. Even though seagrass scientists have worked for many decades in the region, it is still possible that a species will have been missed due to scarceness and low frequency of observation. For example, the lead author (Fonseca) recently identified what appears to be the seagrass Halodule beaudettei in south Florida southeastern Caribbean (Image 4). However, once pointed out to other seagrass scientists, some felt that they had occasionally seen the species through the years. Similarly, a lack of observations could be the case for the reporting of Halophila ovalis in Antigua in 2009 as a newcomer. The point is that, in most cases, distinguishing among range extensions, human transport, or rarity is not possible and leads to the chronic problem of circumstantial evidence but no proof of origin.

 fig 4web

Image 4. A sample of what may be Halodule beaudettei taken from Biscayne Bay, Florida.
Photo credit: Mark Fonseca.


Species, Range Expansions, Development and ESA
Regardless of the name applied, Johnson’s seagrass remains threatened in the context of ESA guidelines as (a) a distinct population segment, (b) having a limited range within the IRLS, (c) characterized by low diversity, (d) absence of males, asexuality, and consequently (e) the need for continuing Critical Habitat protection. Its naturally patchy dynamics and expansion in the north of the IRLS is also consistent with climate warming not necessarily invasiveness. It seems to us that even if Johnson’s were shown to be present in Antigua, the probability of it becoming invasive in other parts of the Caribbean is also minimal based on its performance at home. Finally, adopting the view that Johnson’s seagrass should not continue to be merited with Threatened status because of its potential global distribution (under the name of H. ovalis) seems unwarranted because, even in that case, the Florida plants comprise a genetically distinct population segment of a very large and poorly resolved/diffuse collection of entities.

 seagrass Johnsons Anne McCarthyweb

Johnson’s seagrass in Intracoastal waters near Jupiter Inlet, Florida. Photo credit: Anne McCarthy.


Delisting H. johnsonii on the grounds that it is another species and an introduction would certainly provoke debates and stakeholder conflicts in Florida. At worst, delisting could lead to a call for eradication—similar to those in Washington State (Shafer et al., 2014). However, the reality of any attempted eradication in Florida would be very different from what has been done with other seagrass species. Johnson’s seagrass moves about within the IRLS through asexual fragmentation. Plants float or tumble away from a location when disturbed (e.g., from wave action, propeller scarring, dredging, and simple biological disturbance from rays and other animals) and may then become lodged and root elsewhere. Thus, any effort to eradicate the plant would likely just antagonize this process and sustain the spreading process (not to mention the enormous costs—and for what end). Barring any monumental environmental regime shift that could render the estuaries inhospitable to seagrass, Johnson’s seagrass is a permanent Florida resident.

At best, delisting would still provide minimal protection under existing Critical Habitat regulations for seagrasses more generally (i.e., threatened with destruction, modification, or curtailment within its already limited range). Unfortunately, regulatory protection—which is a challenge for all seagrass species—remains inadequate as seagrasses acreage continues to be lost worldwide (Waycott et al., 2009). Moreover, there is as-yet no demonstrated, reliable means of restoring a spatially and temporally dynamic species because its existence will depend on the availability of space beyond that of any given project area, which is not a management strategy yet employed for plant communities. Finally, as currently practiced, State of Florida impact assessment methods rely on one-point-in-time assessments of habitat presence, a practice clearly inadequate for the management of Halophila spp.

Troubled Waters Or Smooth Sailing?
What is needed now is rethinking and retooling of the science-interface with other sectors. • Resource managers need better impact assessment, monitoring, and mitigation strategies that will protect both small and large seagrass species throughout Florida. At present, they are skewed towards the larger, comparatively (temporally and spatially) stable seagrasses.

• Social-economic valuation (Barbier et al., 2011) of seagrass ecosystem services (and especially Johnson’s seagrass and the other small seagrasses) needs to be included in IRLS developmental planning, as recently illustrated with Tampa Bay, Florida (Russell and Greening, 2015).

• Public outreach that demonstrates the value of the environment not found in the market place can be achieved through using animated video-scenarios and “dashboard indicators,” as has been successful in the Puget Sound Partnership (PSP, 2013). Citizens were surveyed to order to get an intuitive feel for different effects that certain types of development were likely to have on the coastal ecosystem. As a result, seagrasses were included among more than 20 conventional ecosystem indicators, including fish, birds, marine mammals, water quality, overhead structures, urban density, commute time, and real estate values, to name a few. The combination of scientific and socio-economic data translated into visuals was key to enabling the public to identify social preferences while simultaneously building a greater scientific and economic understanding of the risks and trade-offs. If something similar could be achieved for Johnson’s seagrass and the IRLS community, potential polarization could be reduced. Communication is needed among stakeholders who see “this little seagrass” as an annoying impediment to development projects and stakeholders who see “this little seagrass” as a sentinel guarding against possibly uncorrectable ecological damage in the downward spiral to a tipping point.

No matter how good the science, if it doesn’t connect with the other use sectors to inform policy and help to develop a shared vision for the IRLS, then a real solution to Johnson’s seagrass management will not be forthcoming (sensu Laurance et al., 2010; Russell-Smith et al., 2015).

Stakeholder perceptions of Johnson’s seagrass and its role in the IRLS need updating to avoid a devolved set of arguments based on incorrect or unlikely assertions that have led to Johnson’s seagrass being seen as an intruder rather than a sentinel. For these authors, the larger challenge is to reflect on what is to be achieved (or lost) in the scheme of sustainable use of the IRLS if a delisting decision is made. We conclude that for now, continued listing of Johnson’s seagrass as “Threatened,” based on the factors established by the ESA, remains warranted.

Thanks are given to early readers of this article, including Dr. Christopher Kelly and Amy Uhrin.

About The Authors
Mark Fonseca is Vice President of Science at CSA Ocean Sciences Inc. (CSA) He has conducted numerous studies in basic and applied marine/estuarine ecology with a focus on seagrass ecosystem restoration and management. He joined CSA after more than 30 years with the National Oceanic and Atmospheric Administration (NOAA) where he served as a research scientist and research branch chief. He has published over 80 papers on seagrasses, including the authoritative “Guidelines for the conservation and restoration of seagrasses in the United States and adjacent waters” (Fonseca et al., 1998), which remains one of the core documents for seagrass restoration both domestically and overseas.

Jeanine Olsen is Professor of Marine Biology at the Groningen Institute for Evolutionary Life Sciences, University of Groningen, The Netherlands. Her interests are in population genetics/genomics, phylogeography, and conservation of marine plants and algae. She has published more than 150 peer-reviewed papers, some 30 of which pertain to seagrasses. Her interests also extend to algal invasion biology, where she was part of the core group that investigated the “killer alga,” Caulpera taxifolia in the Mediterranean.

Both authors received their Ph.Ds. from the Department of Integrative Biology, University of California, Berkeley.

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