Phycodurus Research Articles

What the genome of the leafy seadragon teaches us about rapid evolution of camouflage and adaptations to life in the kelp forest.

What the genome of the leafy seadragon teaches us about rapid evolution of camouflage and adaptations to life in the kelp forest.

The genetic basis of the leafy seadragon's unique camouflage morphology and avenues for its efficient conservation derived from habitat modeling.

The leafy seadragon certainly is among evolution's most "beautiful and wonderful" species aptly named for its extraordinary camouflage mimicking its coastal seaweed habitat. However, limited information is known about the genetic basis of its phenotypes and conspicuous camouflage. Here, we revealed genomic signatures of rapid evolution and positive selection in core genes related to its camouflage, which allowed us to predict population dynamics for this species. Comparative genomic analysis revealed that seadragons have the smallest olfactory repertoires among all ray-finned fishes, suggesting adaptations to the highly specialized habitat. Other positively selected and rapidly evolving genes that serve in bone development and coloration are highly expressed in the leaf-like appendages, supporting a recent adaptive shift in camouflage appendage formation. Knock-out of bmp6 results in dysplastic intermuscular bones with a significantly reduced number in zebrafish, implying its important function in bone formation. Global climate change-induced loss of seagrass beds now severely threatens the continued existence of this enigmatic species. The leafy seadragon has a historically small population size likely due to its specific habitat requirements that further exacerbate its vulnerability to climate change. Therefore, taking climate change-induced range shifts into account while developing future protection strategies.

Length–Weight Relationships and Growth Parameters of Common and Leafy Seadragons (Syngnathidae) from a Public Aquarium

The length–weight relationships (LWR) of the common seadragon Phyllopteryx taeniolatus (Lacepède, 1804) and the leafy seadragon Phycodurus eques (Günther, 1865), Syngnathidae, are presented in this paper, based on specimens raised in the Birch Aquarium at Scripps, La Jolla, California. Furthermore, we used the length at known age of 40 specimens of common and 15 leafy seadragons to estimate the parameter of the von Bertalanffy growth function (VBGF) for these species. Some of the pros and cons of the newly proposed length type used, ‘scalene length’ are presented. The parameters of the LWR and the VBGF parameters are discussed, with an emphasis on the rearing conditions, the peculiar anatomy of seadragons, especially of P. eques, and on the Gill-Oxygen Limitation Theory (GOLT).

Editorial 2022

Editorial 2022

Cover Image

Molecular EcologyVolume 30, Issue 6 p. i-iv ISSUE INFORMATION Cover Image First published: 16 March 2021 https://doi.org/10.1111/mec.15887AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat Abstract Cover Illustrations: A leafy seadragon (Phycodurus eques) in its habitat in southern Australia. Photo Credit:Greg W. Rouse Volume30, Issue6March 2021Pages i-iv RelatedInformation

The hidden landscape: Evidence that sea-level change shaped the present population genomic patterns of marginal marine species.

Oftentimes, to understand the genetic relatedness and diversity of today's populations requires considering the ancient landscape on which those populations evolved. Nowhere is this clearer than along Earth's coastline, which has been in its present-day configuration for only about 6.5% of the past 800,000years (Dolby et al., 2020; Miller et al., 2005). During ice ages when glaciers expanded in the Northern Hemisphere, they stored enough of the planet's water to drop global sea level by ~120m below present levels ("lowstand", Figure 1a), and there have been at least eight of these 100,000-year cycles preceding today. When glaciers melted, ocean water reflooded shorelines, shifting and re-forming marginal marine habitats globally and shaping the relatedness of populations (Dolby et al., 2016). In a From the Cover article in this issue of Molecular Ecology, Stiller et al. (2020) integrate population genomic analysis of leafy seadragons in southern Australia with estimates of available seabed area to reveal that the expansion of habitat that accompanied this reflooding led to strong demographic expansions. With statistical models, they also show that western populations were eliminated and then recolonized because the continental shelf there is narrow, leaving little available habitat when sea level was low (Figure 1b). Their results document the dynamic and interrelated nature of a hidden, changing landscape and the evolution of species inhabiting it.

Using ultraconserved elements to track the influence of sea-level change on leafy seadragon populations.

During the Last Glacial Maximum (LGM), global sea levels were 120-130m lower than today, resulting in the emergence of most continental shelves and extirpation of subtidal organisms from these areas. During the interglacial periods, rapid inundation of shelf regions created a dynamic environment for coastal organisms, such as the charismatic leafy seadragon (Phycodurus eques, Syngnathidae), a brooder with low dispersal ability inhabiting kelp beds in temperate Australia. Reconstructions of the palaeoshoreline revealed that the increase of shallow areas since the LGM was not uniform across the species' range and we investigated the effects of these asymmetries on genetic diversity and structuring. Using targeted capture of 857 variable ultraconserved elements (UCEs, 2,845 single nucleotide polymorphisms) in 68 individuals, we found that the regionally different shelf topographies were paralleled by contrasting population genetic patterns. In the west, populations may not have persisted through sea-level lows because shallow seabed was very limited. Shallow genetic structure, weak expansion signals and a westward cline in genetic diversity indicate a postglacial recolonization of the western part of the range from a more eastern location following sea-level rise. In the east, shallow seabed persisted during the LGM and increased considerably after the flooding of large bays, which resulted in strong demographic expansions, deeper genetic structure and higher genetic diversity. This study suggests that postglacial flooding with rising sea levels produced locally variable signatures in colonizing populations.

Complete mitochondrial genome characterization of the alligator pipefish Syngnathoides biaculeatus and phylogenetic analysis of family Syngnathidae

The alligator pipefish Syngnathoides biaculeatus (Bloch, 1785) is one of the heavily traded and expensive ingredient in traditional Chinese medicine. In this study, the complete mitogenome of S. biaculeatus was determined. The mitochondrial genome of S. biaculeatus was 16,480 bp in length. It contains 13 protein coding genes (PCGs), 2 rRNAs (12S rRNA and 16S rRNA), 22 tRNA genes, one origin of replication (OL) and a non-coding control region (D-loop). The overall base composition is 29.71, 28.39, 26.53 and 15.37% for A, T, C and G, respectively. Phylogenetic tree analysis suggests S. biaculeatus was placed as a sister relationship to the the leafy seadragon Phycodurus eques with high statistical support. This work provides fundamental molecular data of S. biaculeatus, which will be beneficial to species identification, genetic differentiation and further management and conservation in this species.

First live records of the ruby seadragon (Phyllopteryx dewysea, Syngnathidae)

Until recently, only two species of seadragon were known, Phycodurus eques (the leafy seadragon) and Phyllopteryx taeniolatus (the common seadragon), both from Australia. In 2015, we described a new species of seadragon, Phyllopteryx dewysea (the ruby seadragon). Although the leafy and common seadragons are well known and commonly seen in aquarium exhibits world-wide, the ruby seadragon was known only from four preserved specimens, leaving many aspects of its biology unknown. Based on specimen records, it was speculated that the ruby seadragon normally lives at depths beyond recreational SCUBA diving limits, which may also explain why it went undiscovered for so long. The ruby seadragon also bears a superficial resemblance to the common seadragon, with a number of specimens misidentified in museum collections. The only recent live-collected specimen was trawled from the Recherche Archipelago, a cluster of over 100 islands in Western Australia. We took a small remotely operated vehicle (miniROV) to this locality to obtain the first images of live ruby seadragons. We made observations on the seadragon habitat and behavior, including feeding. We also provide new key observations on their morphology, notably that they lack dermal appendages and have a prehensile tail. We recommend that the ruby seadragon be protected as soon as practicable.

The Leafy Seadragon, Phycodurus eques, a Flagship Species with Low But Structured Genetic Variability.

The leafy seadragon (Phycodurus eques, Syngnathidae), is a charismatic endemic of Australia’s temperate coast. The species exhibits remarkable camouflage in its kelp and seagrass habitat. These habitats have been retreating throughout the range of the species, leading to concerns about the persistence of leafy seadragons. Despite being a popular aquarium display and a flagship for coastal conservation, little is known about leafy seadragon biology. We used 7 microsatellite markers and 2 mitochondrial DNA fragments to investigate the population structuring and genetic diversity of 71 individuals. Bayesian cluster analysis identified 2 main genetic partitions, one in Western Australia and the other in South Australia. Shallower, yet significant, differentiation of mitochondrial DNA (φST) and microsatellites (FST, F′ST, D) was found on the smaller geographic scales in South Australia. Distinct groups were supported in Encounter Bay, on both shores of Gulf St Vincent, and in Spencer Gulf. Sample sizes were too small in the eastern Great Australian Bight and in the westernmost locality to address genetic differentiation in these regions. Overall genetic diversity was moderate to low, but particularly low levels were found in the Western Australian cluster. This latter point needs confirmation at other sites in Western Australia. In South Australia, signatures of demographic changes were detected, which may have been caused by a population expansion due to post-glacial reflooding of the gulfs. The Western Australian and South Australian clusters appeared as demographically independent units. Conservation actions should focus on preserving genetic diversity at local scales and maintaining habitat connectivity.

A spectacular new species of seadragon (Syngnathidae).

The exploration of Earth's biodiversity is an exciting and ongoing endeavour. Here, we report a new species of seadragon from Western Australia with substantial morphological and genetic differences to the only two other known species. We describe it as Phyllopteryx dewysea n. sp. Although the leafy seadragon (Phycodurus eques) and the common seadragon (Phyllopteryx taeniolatus) occur along Australia's southern coast, generally among relatively shallow macroalgal reefs, the new species was found more offshore in slightly deeper waters. The holotype was trawled east of the remote Recherche Archipelago in 51 m; additional specimens extend the distribution west to Perth in 72 m. Molecular sequence data show clear divergence from the other seadragons (7.4–13.1% uncorrected divergence in mitochondrial DNA) and support a placement as the sister-species to the common seadragon. Radiographs and micro-computed tomography were used on the holotype of the new species and revealed unique features, in addition to its unusual red coloration. The discovery provides a spectacular example of the surprises still hidden in our oceans, even in relatively shallow waters.

Novel Microsatellite Loci Variation and Population Genetics within Leafy Seadragons, Phycodurus eques

Novel leafy seadragon (Phycodurus eques) microsatellite loci were developed via standard cloning techniques and tested for use in population genetics studies. Six out of a total of twelve microsatellites tested were usable for population analysis. Seadragon samples from Western Australia (N = 6), Southern Australia (N = 11), and a captive group (N = 11) were analyzed. Here, we present leafy seadragon microsatellite primer sequences for all 12 loci and population genetics statistics for the six loci that amplified consistently and displayed adequate variability to estimate population parameters, such as diversity, population differences, and relatedness. Observed heterozygosities ranged from 0.225 to 0.926 and expected heterozygosities ranged from 0.278 to 0.650. Pairwise differences among populations (FST estimates) from samples collected off the southern coast of Western and South Australia, and captive animals ranged from a low of 0.188 between Southern Australia and captive animals, to a high of 0.212 between Western Australia and captive animals. Statistical assignment analyses suggested between one and three populations. Percent first order relatives among individuals was high and ranged from 40 within Western Australia to 55 within captive animals. These loci were tested on other species including weedy seadragons (Phyllopteryx taeniolatus), as well as assorted seahorses (Hippocampus reidi, H. erectus) and pipefish (Doryrhamphus dactyliophorus, D. pessuliferus, Corythoichthys intestinalis, Syngnathus leptorhynchus) with no success.

Pathologic Findings in Weedy (Phyllopteryx taeniolatus) and Leafy (Phycodurus eques) Seadragons

A retrospective study of the pathologic findings in weedy (Phyllopteryx taeniolatus) and leafy (Phycodurus eques) seadragons was performed on specimens submitted to 2 reference laboratories from 1994 to 2012 to determine the range and occurrence of diseases affecting aquarium-held populations. One hundred two and 94 total diagnoses were recorded in weedy and leafy seadragons, respectively. Two of the more common etiologic diagnoses in both species were mycobacteriosis and scuticociliatosis, whereas myxozoanosis was common in weedy seadragons. Metazoan parasite infections were less common etiologic diagnoses. There were no correlations between mycobacteriosis and ciliate protozoan infections in either species. Myxozoanosis was usually found in combination with other diseases and, except for 1 case, was restricted to weedy seadragons. Phaeohyphomycosis, nonmycobacterial bacterial infections, and trauma were also important but less frequent diagnoses. Intestinal coccidiosis was found in weedy but not leafy seadragons. Mineralization of the swim bladder was detected in 26 of 197 leafy seadragons and only 2 of 257 weedy seadragons. Although weedy and leafy seadragons share certain diseases of significance to exhibit populations, there are diseases unique to each species about which the veterinary pathologist, clinician, or diagnostician should be aware.

Disseminated Phaeohyphomycosis in Weedy Seadragons (Phyllopteryx Taeniolatus) and Leafy Seadragons (Phycodurus Eques) Caused by Species of Exophiala, Including a Novel Species

During the period from January 2002 to March 2007, infections by melanized fungi were identified with greater frequency in aquarium-maintained leafy seadragons (Phycodurus eques) and weedy seadragons (Phyllopteryx taeniolatus), pivotal species to the educational and environmental concerns of the aquarium industry and conservation groups. The objective of this study was to characterize the pathology and identify fungi associated with phaeohyphomycotic lesions in these species. Samples from 14 weedy and 6 leafy seadragons were received from 2 institutions and included fresh, frozen, and formalin-fixed tissues from necropsy and biopsy specimens. Fresh and frozen tissues were cultured for fungi on Sabouraud dextrose agar only or both Sabouraud dextrose agar and inhibitory mold agar with gentamicin and chloramphenicol at 30 degrees C. Isolates were processed for morphologic identification and molecular sequence analysis of the internal transcribed spacer region and D1/D2 domains of the large subunit ribosomal RNA gene. Lesions were extensive and consisted of parenchymal and vascular necrosis with fungal invasion of gill (11/20), kidney (14/20), and other coelomic viscera with or without cutaneous ulceration (13/20). Exophiala sp. isolates were obtained from 4 weedy and 3 leafy seadragons and were identified to species level in 6 of 7 instances, namely Exophiala angulospora (1) and a novel species of Exophiala (5), based on nucleotide sequence comparisons and phylogenetic analyses. Disseminated phaeohyphomycosis represents an important pathologic condition of both weedy and leafy seadragons for which 2 species of Exophiala, 1 a novel species, have been isolated.

Severe Scuticociliate (Philasterides dicentrarchi) Infection in a Population of Sea Dragons (Phycodurus eques and Phyllopteryx taeniolatus)

Scuticociliatosis is a disease of fish induced by ciliated parasites of the genus Scuticociliatida. It has been described in sea horses (Hippocampus sp.), flounders (Paralichthys olivaceus), and turbots (Scophthalmus maximus). Here we present a case study of a population of sea dragons chronically infected with scuticociliates identified as Philasterides dicentrarchi by histopathology and PCR. Beginning in 2004, over a period of 19 months, 10 sea dragons (Phycodurus eques and Phyllopteryx taeniolatus) were found dead in an aquarium of the Zoological Garden Basle, Switzerland. Clinically, the animals showed only faint symptoms of disease over a short period of time. At necropsy, macroscopic lesions were confined to the skin with multiple, often hemorrhagic, ulcerations. Histologically, epidermal ulcers were associated with necrosis and inflammation of the underlying dermis and musculature. Numerous ciliates, with a morphology consistent with scuticociliates, were present in these lesions. In several animals these ciliates had invaded blood vessels and were detected in gills and internal organs including kidney, thyroid gland, and central nervous system (CNS). In these organs, mild degenerative lesions and inflammatory reactions were evident. The ciliates were identified as Philasterides dicentrarchi based on small-subunit ribosomal RNA (SSUrRNA) gene sequences obtained by polymerase chain reaction (PCR) on DNA extracted from paraffin-embedded tissue sections. Our report shows that scuticociliate infections of sea dragons can develop into a systemic infection and that both species of sea dragons can be affected.

Molecular Evidence for Association of Chlamydiales Bacteria with Epitheliocystis in Leafy Seadragon ( Phycodurus eques ), Silver Perch ( Bidyanus bidyanus ), and Barramundi ( Lates calcarifer )

Epitheliocystis in leafy seadragon (Phycodurus eques), silver perch (Bidyanus bidyanus), and barramundi (Lates calcarifer), previously associated with chlamydial bacterial infection using ultrastructural analysis, was further investigated by using molecular and immunocytochemical methods. Morphologically, all three species showed epitheliocystis cysts in the gills, and barramundi also showed lymphocystis cysts in the skin. From gill cysts of all three species and from skin cysts of barramundi 16S rRNA gene fragments were amplified by PCR and sequenced, which clustered by phylogenetic analysis together with other chlamydia-like organisms in the order Chlamydiales in a lineage separate from the family Chlamydiaceae. By using in situ RNA hybridization, 16S rRNA Chlamydiales-specific sequences were detected in gill cysts of silver perch and in gill and skin cysts of barramundi. By applying immunocytochemistry, chlamydial antigens (lipopolysaccharide and/or membrane protein) were detected in gill cysts of leafy seadragon and in gill and skin cysts of barramundi, but not in gill cysts of silver perch. In conclusion, this is the first time epitheliocystis agents of leafy seadragon, silver perch and barramundi have been undoubtedly identified as belonging to bacteria of the order Chlamydiales by molecular methods. In addition, the results suggested that lymphocystis cysts, known to be caused by iridovirus infection, could be coinfected with the epitheliocystis agent.

Patterns of movement and habitat use by leafy seadragons tracked ultrasonically

Nine adult leafy seadragons Phycodurus eques were tracked using ultrasonic telemetry for between 2‐10 days around West Island, Australia. All fish except one moved within well‐defined home ranges of up to 5 ha (using minimum convex polygon method). Short bursts of movement (at average velocities of 2‐17 m h−1) punctuated long periods (up to 68 h) without movement. The exceptional fish moved almost in a straight line away from its tagging location near the end of the tracking period, at a maximum velocity of 146 m h−1. There was no constant diel pattern in movements; some fish moved more at night, others during the day. The time leafy seadragons spent over particular habitats compared to the area of those habitats available at the study site was greater for Posidonia seagrass, about as expected for kelp‐covered reefs and bare sand patches, and less than expected for Amphibolis seagrass and boulders covered with brown algae. In searching for tagging effects, a comparison of movement immediately after tagging showed no difference with subsequent movements for most fish. The lack of tagging effect may be because the transmitter can be attached to the bony appendages away from the body of the fish. There was no sign of damage to fish upon removal of transmitters after tracking.

Patterns of movement and habitat use by leafy seadragons tracked ultrasonically

Nine adult leafy seadragons Phycodurus eques were tracked using ultrasonic telemetry for between 2-10 days around West Island, Australia. All fish except one moved within well-defined home ranges of up to 5 ha (using minimum convex polygon method). Short bursts of movement (at average velocities of 2-17 m h−1) punctuated long periods (up to 68 h) without movement. The exceptional fish moved almost in a straight line away from its tagging location near the end of the tracking period, at a maximum velocity of 146 m h−1. There was no constant diel pattern in movements; some fish moved more at night, others during the day. The time leafy seadragons spent over particular habitats compared to the area of those habitats available at the study site was greater for Posidonia seagrass, about as expected for kelp-covered reefs and bare sand patches, and less than expected for Amphibolis seagrass and boulders covered with brown algae. In searching for tagging effects, a comparison of movement immediately after tagging showed no difference with subsequent movements for most fish. The lack of tagging effect may be because the transmitter can be attached to the bony appendages away from the body of the fish. There was no sign of damage to fish upon removal of transmitters after tracking.

Abundance, movement and individual identification of leafy seadragons, Phycodurus eques (Pisces: Syngnathidae)

The aim of this study was to estimate, for the first time, abundance and degree of movement of leafy seadragons, Phycodurus eques, at one location in southern Australia. The pattern of wear and damage to the leafy appendages was found to vary among individuals but was not a reliable method of identification of individual fish over long periods. Photographic evidence of individual facial markings was more reliable and full-grown individuals could be recognised by their facial markings for at least 11 months. We made 45 sightings in 47 dives over 14 months. Sightings were made in depths of 3-11 m over brown algae, seagrass, and sand covered with drift macroalgae. Nine individual fish were sighted and all except one were sighted at least twice (mean of five sightings, s.e. 1.2, range 1-12). Capture and recapture calculations (moment estimator algorithm) estimated 9.2 (±0.3) seadragons in the study area (density 57 fish ha-1). Resightings were made months apart, suggesting that the fish are remaining within a home range (range of 35-82 m, maximum distance between sightings for fish sighted >5 times). Information about patterns of movement of seadragons is directly relevant to management plans for this species and for marine protected areas designed to aid in their protection.

Epitheliocystis in the leafy sea‐dragon

Australian Veterinary JournalVolume 68, Issue 7 p. 244-244 Epitheliocystis in the leafy sea-dragon JS LANGDON, JS LANGDON Fish Health Section, Departments of Agriculture and Fisheries, South Perth, Western Australia 6151Search for more papers by this authorK. ELLIOTT, K. ELLIOTT Fish Health Section, Departments of Agriculture and Fisheries, South Perth, Western Australia 6151Search for more papers by this authorB. MACKAY, B. MACKAY Underwater World, Hillarys, Western Australia 6025Search for more papers by this author JS LANGDON, JS LANGDON Fish Health Section, Departments of Agriculture and Fisheries, South Perth, Western Australia 6151Search for more papers by this authorK. ELLIOTT, K. ELLIOTT Fish Health Section, Departments of Agriculture and Fisheries, South Perth, Western Australia 6151Search for more papers by this authorB. MACKAY, B. MACKAY Underwater World, Hillarys, Western Australia 6025Search for more papers by this author First published: July 1991 https://doi.org/10.1111/j.1751-0813.1991.tb03219.xCitations: 12AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat No abstract is available for this article.Citing Literature Volume68, Issue7July 1991Pages 244-244 RelatedInformation