Polydora Hoplura Research Articles

A twin of Polydora hoplura (Annelida: Spionidae) from the Arabian (Persian) Gulf, with review of primers used for barcoding of Spionidae

A twin of Polydora hoplura (Annelida: Spionidae) from the Arabian (Persian) Gulf, with review of primers used for barcoding of Spionidae

Heterogeneous microbiomes associate with shell-boring Polydora hoplura (Polychaeta, Spionidae) affecting the flat oyster Ostrea edulis

Shell-boring polychaetes belonging to the genus Polydora (Spionidae) infect commercially harvested bivalve molluscs worldwide, reducing their economic value. Due to their limited intraspecific variability, taxonomic identification becomes challenging without molecular approaches. In this study, we identified Polydora hoplura worms infecting flat oysters (Ostrea edulis) in the Gulf of Naples (Italy), providing the first DNA barcode data on the cytochrome c oxidase subunit 1 mitochondrial gene (COI) from its type locality. Three haplotypes with up to ten mutational step differences were detected, suggesting recent introductions from distant populations, including South Africa. The characterization of Polydora associated prokaryotic communities revealed a diverse and fluctuating microbiome linked to these worms, deviating from the usual species-specific pattern observed in other invertebrates. Core and some non-core bacteria could be playing symbiotic roles in nutrient provision, removal of waste products, and antioxidant and detoxifying processes to allow endolithic lifestyle within the borrowed valve chambers. The majority of these microbes though, seem to be acquired horizontally, from an interconnection between the environment and the flat oyster cavity. Indeed, there was a notable detection of opportunistic and potentially pathogenic taxa clusters, including Mycobacterium, Vibrio, Aliiroseovarius and Halarcobacter spp., which in concomitance with the prevalent polydorid infections may prompt implications for the health of the flat oyster host, and for its commercial market, including human consumption. Our study is novel in characterizing bacterial communities associated with shell-boring polychaetes, and sets the bases to propose these parasitic worms as vectors of alterable microbial exchange between oyster hosts and the environment.

First insight on the genetic base of the heritable variation of Pacific abalone (Haliotis discus hannai) resistance to Polydora hoplura infestation

Polydora hoplura is an invasive species and a harmful pest in commercial shellfish aquaculture, particularly for farmed abalone species. Different lines of treatment for Polydora affecting abalone have been explored, but with limited success. Using selective breeding to increase abalone resistance to and reduce shell damage from Polydora infestation could be a promising alternative. However, in abalone there is currently no information on the genetic variability for resistance to Polydora infestation. In the present study, heritability (h2) of traits associated with Pacific abalone resistance to P. hoplura were estimated after challenging abalone juveniles with trojan abalones heavily infested, using a nested experimental design, with 1 male crossed with 2–4 females. The heritability values were low but significant for some of those traits: survival h2=0.09; Infestation Intensity at Q50h2 = 0.16 ± 0.11; and the proportion of the shell area occupied by blisters caused by the mud-worms h2 = 0.29 ± 0.14. These results suggest a significant potential for improving resistance or tolerance to P. hoplura infestation through selective breeding in Pacific abalone.

Searching for a Home Port in a Polyvectic World: Molecular Analysis and Global Biogeography of the Marine Worm Polydora hoplura (Annelida: Spionidae).

The spionid polychaete Polydora hoplura Claparède, 1868 is a shell borer widely occurring across the world and considered introduced in many areas. It was originally described in the Gulf of Naples, Italy. Adult diagnostic features are the palps with black bands, prostomium weakly incised anteriorly, caruncle extending to the end of chaetiger 3, short occipital antenna, and heavy sickle-shaped spines in the posterior notopodia. The Bayesian inference analysis of sequence data of four gene fragments (2369 bp in total) of the mitochondrial 16S rDNA, nuclear 18S, 28S rDNA and Histone 3 has shown that worms with these morphological features from the Mediterranean, northern Europe, Brazil, South Africa, Australia, Republic of Korea, Japan and California are genetically identical, form a well-supported clade, and can be considered conspecific. The genetic analysis of a 16S dataset detected 15 haplotypes of this species, 10 of which occur only in South Africa. Despite the high genetic diversity of P. hoplura in South Africa, we tentatively propose the Northwest Pacific, or at the most the Indo-West Pacific, as its home region, not the Atlantic Ocean or the Eastern Pacific Ocean. The history of the discovery of P. hoplura around the world appears to be intimately linked to global shipping commencing in the mid-19th century, followed by the advent of the global movement of commercial shellfish (especially the Pacific oyster Magallana gigas) in the 20th century, interlaced with continued, complex dispersal by vessels and aquaculture. Given that P. hoplura has been detected in only a few of the 17 countries where Pacific oysters have been established, we predict that it may already be present in many more regions. As global connectivity through world trade continues to increase, it is likely that novel populations of P. hoplura will continue to emerge.

Polydorid species (Annelida: Spionidae) associated with commercially important oyster shells and their shell infestation along the coast of Normandy, in the English Channel, France

Polydorid species (Annelida, Spionidae), which inhabit the shells of the commercially important oyster Crassostrea gigas, were investigated along the coast of Normandy, France. Eight species, including five new records for Normandy (Polydora onagawaensis, Polydora websteri, Boccardia pseudonatrix, Boccardia proboscidea, and Boccardiella hamata) and two first records in European waters (P. onagawaensis and B. pseudonatrix), were identified based on morphological, molecular biological, and ecological characteristics. Polydora onagawaensis, which belongs to the Polydora ciliata/websteri complex, was discovered in the shells of wild and suspended cultured oysters, as well as in limestone substrates. In the phylogenetic analysis of mitochondrial COI gene sequences, specimens of P. onagawaensis collected from Normandy were grouped together with specimens from the USA into a single clade and were distinguished from the other three lineages that comprised Japanese and USA specimens. Polydora websteri inhabited shells of suspended cultured oysters. Polydora hoplura, Dipolydora giardi, and Dipolydora sp. were observed in shells from the sandy oyster culture grounds. Boccardiella hamata has been found in wild oyster shells from muddy oyster culture grounds. Boccardia pseudonatrix was observed in the shells of both the wild and cultured oysters. Adult and juvenile Boccardia proboscidea were observed in coralline algae, as well as in suspended cultured oysters. Mud tubes were observed to protrude from the outer surface of the shells, and abnormal black and calcareous deposits were secreted on the inner surface of the shells against polydorid penetration.

Identification of the shell-boring parasite Polydora hoplura (Annelida: Spionidae) on wild stocks of Pecten maximus in Galician waters, NW Spain

Infestations by shell-boring polychaetes have been gaining attention in recent years due to the harmful effects that their presence can pose to the growth and production of marine bivalves worldwide. The Galician region, located in the north-western corner of the Iberian Peninsula, is one of the major producers of marine bivalves in the word and therefore highly dependent on this industry. The recent finding of an unknown polychaete boring into the shells of the king scallop, Pecten maximus, has raised the attention of producers and authorities due to its potential harm to exploitable populations and the economical losses that could entail. The results from the morphological examination revealed the spionid Polydora hoplura as the only species present. DNA of a specimen was extracted and the mitochondrial 16S rRNA gene was partially sequenced for comparison with published sequences and confirmation of the morphological identification. Consequently, we report for the first time in the area the infestation of wild harvested populations of P. maximus by the mud worm Polydora hoplura. The presence of this shell-boring cosmopolitan invader could pose a threat to king scallop exploitation in Galicia; potential economic impacts need to be evaluated.

Complete mitochondrial genome of the abalone shell-boring Polydora hoplura (Polychaeta, Spionidae)

Polydora hoplura Claparede 1868 (Polychaeta, Spionidae) is a mollusk shell-boring species which has been reported as a harmful species. In the present study, we sequenced and reported the mitochondrial genome (mitogenome) of P. hoplura from Korea. Its mitogenome was determined by long range PCR and primer walking. The mitogenome was found to be 17,707 bp in length and contained two ribosomal RNAs (rRNAs), 23 transfer RNAs (tRNAs), and 12 protein-coding genes which showed different gene arrangement with that in related mitogenomes of species of Sedentaria (Annelida). Interestingly, the atp8 gene was not found in the mitogenome of P. hoplura, whereas it is present in the mitogenomes of related species P. brevipalpa and P. websteri. Moreover, nad2 (3’ end) and cox1 (5’ end) genes overlapped in 23 bases. The mitogenome structure and gene contents of P. hoplura provide useful information on the evolution and phylogenetic relationship among polychaete species.

Polychaetes collected from floats of oyster-farming rafts in Kure, the Seto Inland Sea, Japan, with notes on the pest species Polydora hoplura (Annelida: Spionidae)

Polychaetes collected from floats of oyster-farming rafts in Kure, the Seto Inland Sea, Japan, with notes on the pest species Polydora hoplura (Annelida: Spionidae)

Morphology and biology of Polydora hoplura Claparède, 1868 (Annelida: Spionidae)

Polydora hoplura Claparède, 1868 is one of the largest species among congeners, attaining 6 cm in length and 2 mm in width for more than 200 chaetigers. It is a harmful shell-borer unintentionally transported with objects of aquaculture across the world. Brief original description and absence of type material resulted in confusion with the identification of this species. Herein, we review previous records, establish a neotype and redescribe P. hoplura based on newly collected material from the type locality, the Gulf of Naples. We also describe worms from other localities in Italy, illustrate adult morphology and report gradual development of taxonomic features of this species in ontogenesis based on material from South Korea.

Dispersal and genetic structure of Boccardia polybranchia and Polydora hoplura (Annelida: Spionidae) in South Africa and their implications for aquaculture

Dispersal and observed genetic structure of sessile marine invertebrates such as the alien polydorid polychaete, Polydora hoplura, which is associated with cultured molluscs, may be influenced by biogeographic barriers and human-mediated dispersal. To test this hypothesis, we compared the population genetic structure of P. hoplura to that of Boccardia polybranchia since both species have similar larval developmental modes (and consequently natural dispersal potential) and distribution ranges in southern Africa. However, since B. polybranchia is not a pest, its population structure should reflect the effects of only biogeographic barriers on natural dispersal. Boccardia polybranchia was collected from five wild sites along the South African coast, and P. hoplura from seven wild sites and four oyster farms; two each were on-shore and off-shore. Analyses of mtDNA Cyt b sequence data indicate two distinct lineages for B. polybranchia, supporting Cape Point as a biogeographic barrier to the dispersal of larvae. In contrast, no distinct geographic lineages were identified for P. hoplura occurring in the wild, and haplotype sharing suggest possible cross infestation between farm and nearby wild sites. At farms the genetic diversity of P. hoplura is lower but also more structured, suggesting separate anthropogenic introductions at each site possibly from genetically distinct source populations. Furthermore, more limited genetic sharing was detected between worms from on-shore and nearby wild sites, whereas the opposite was observed for off-shore farms and associated wild sites. This suggests that populations in on-shore farms are more contained with most of the individuals carrying parasites corresponding to the source of introduction while those on off-shore farms display much more genetic exchange with wild populations. Thus oysters in off-shore facilities are probably more vulnerable to infestation by polydorid pests than are those in on-shore facilities. Statement of relevanceMovement of oysters spreads associated pests

And then there was one:Polydora uncinataandPolydora hoplura(Annelida: Spionidae), the problematic polydorid pest species represent a single species

It is necessary to monitor shell-associated polydorid worms owing to the risk that they pose to commercially important molluscs. This requires accurate identification, but is often hampered by morphological similarities among species, insufficient type specimens, and abridged species descriptions. Thus morphological characteristics and molecular sequences of the most harmful polydorid species,Polydora uncinatafrom Japan and Australia andPolydora hoplurafrom South Africa were compared to determine whether they represent two morphologically similar, but genetically distinct species, or a single species. A wide range of morphological variation (with respect to size, length of caruncle and pigmentation patterns) was observed in each species and population, and their variations largely overlapped and revealed them to be at the intraspecific level of a single species. This was confirmed by gene sequences of nuclear 18S and 28S rRNA that were completely identical forP. uncinataandP. hoplura. The mitochondrial 16S rRNA andcyt bgene analyses also showed no genetic differences between these two species. The tree topology of the mitochondrialcyt bgene did not reflect geographic differences but instead suggests artificial transportation of the species. We recommend the synonymization ofP. uncinatawithP. hoplura.

First report of the polychaete Polydora hoplura (Annelida: Spionidae) from North and South America and Asian Pacific

The spionid polychaete Polydora hoplura Claparede, 1868, is a harmful shell-borer accidentally transported with objects of aquaculture across the world. It was originally described from the Gulf of Naples, Italy, and later widely reported from European waters, South Africa, the Arabian Gulf, New Zealand, Australia and Tasmania. Here, for the first time, we describe adults and larvae of P. hoplura from Atlantic South America (Brazil), and report this species from Pacific North America (California, USA). We also examined material from Italy, New Zealand, Australia, Chile and Japan, and treat Polydora uncinata Sato-Okoshi, 1998, from Japan, as a junior synonym of P. hoplura. Consequently, we report P. hoplura for the first time in the Asian Pacific, Japan and South Korea, and in Pacific South America (Chile). The new records of P. hoplura from the American continents are cause for concern. The spread of this non-indigenous species may have negative impacts on the farm cultivation of oysters and abalone.

Predicting the Dispersal Potential of an Invasive Polychaete Pest along a Complex Coastal Biome.

Boccardia proboscidea is a recently introduced polychaete in South Africa where it is a notorious pest of commercially reared abalone. Populations were originally restricted to abalone farms but a recent exodus into the wild at some localities has raised conservation concerns due to the species' invasive status in other parts of the world. Here, we assessed the dispersal potential of B. proboscidea by using a population genetic and oceanographic modeling approach. Since the worm is in its incipient stages of a potential invasion, we used the closely related Polydora hoplura as a proxy due its similar reproductive strategy and its status as a pest of commercially reared oysters in the country. Populations of P. hoplura were sampled from seven different localities and a section of the mtDNA gene, Cyt b and the intron ATPSa was amplified. A high resolution model of the coastal waters around southern Africa was constructed using the Regional Ocean Modeling System. Larvae were represented by passive drifters that were deployed at specific points along the coast and dispersal was quantified after a 12-month integration period. Our results showed discordance between the genetic and modeling data. There was low genetic structure (Φ = 0.04 for both markers) and no geographic patterning of mtDNA and nDNA haplotypes. However, the dispersal model found limited connectivity around Cape Point-a major phylogeographic barrier on the southern African coast. This discordance was attributed to anthropogenic movement of larvae and adult worms due to vectors such as aquaculture and shipping. As such, we hypothesized that cryptic dispersal could be overestimating genetic connectivity. Though wild populations of B. proboscidea could become isolated due to the Cape Point barrier, anthropogenic movement may play the critical role in facilitating the dispersal and spread of this species on the southern African coast.

Observations on the composition and larval developmental modes of polydorid pests of farmed oysters (Crassostrea gigas) and abalone (Haliotis midae) in South Africa

This study provides preliminary insights into how the culture method of molluscs and the larval developmental mode of pest polydorids may determine which species become pests. A total of 10 species were identified on oysters and abalone in offshore and oysters in onshore culture on the west coast of South Africa. One-factor PERMANOVA showed that abalone and oysters cultured offshore housed similar communities of worms, but that they differed significantly from the communities housed by oysters cultured onshore. Oysters from onshore were infested mainly by Polydora hoplura, but also by Polydora cf. websteri and Boccardia pseudonatrix. All these species produce adelphophagic larvae or a mixture of these and planktotrophic larvae. Adelphophagic larvae usually only emerge soon before they settle, which would probably enhance their ability to recruit locally and establish local populations. By contrast, worms from molluscs grown offshore were infested by high abundances of P. hoplura and lower abundances of up to five more species per individual host. All hatched broods observed with these female P. hoplura contained planktotrophic larvae which have a long planktonic phase before settling. This would presumably enhance their ability to reach hosts in the offshore.

The effect of temperature on larval development of two non-indigenous poecilogonous polychaetes (Annelida: Spionidae) with implications for life history theory, establishment and range expansion

Marine invasions are recognized as an important threat to global biodiversity and predicting the establishment and spread of an introduced species can aid in management efforts to mitigate the damage incurred by these species. In South Africa, the recently introduced polychaete Boccardia proboscidea has been recorded at the outflow of abalone farms where they are known to infest the shells of these mollusks. To determine if B. proboscidea can become established along the South African coast and subsequently expand its range, we assessed brood size, larval size at hatching, larval survivorship and developmental time and rate of this species under temperature regimes reflective of those found along the coast. We also investigated similar temperature dependent development in the well-established non-indigenous shell borer Polydora hoplura which can serve as a proxy for our predictions. Worms were cultured in glass capillary tubes at five different temperature treatments (12°C, 17°C, 21°C, 24°C, 28°C) and planktotrophic and adelphophagic larvae were tracked from oviposition to settlement. We found that in P. hoplura, females producing adelphophagic larvae had smaller broods at the highest temperature treatment and higher temperatures resulted in significantly larger sizes at hatching. Survivorship of planktotrophic and adelphophagic larvae was highest at the intermediate to high temperature treatments (21°C and 24°C) and was generally lower at the lower temperatures (12°C and 17°C). Temperature had no significant effect on brood size of B. proboscidea whereas higher temperatures resulted in larger hatching sizes for planktotrophic and adelphophagic larvae. In B. proboscidea, larval types showed differences in survival optima with planktotrophic larvae exhibiting its highest survivorship at the colder temperatures and lowest at the warmer temperatures while adelphophagic larvae had its highest survivorship at 21°C and its lowest at the extreme temperatures. There was a positive relationship between temperature and developmental rate for both species. The difference in larval sizes of the non-feeding planktotrophic larvae of B. proboscidea was attributed to a growth window that allowed for variability in reproductive traits based on exogenous factors such as temperature. More importantly, the results indicate that B. proboscidea will be capable of producing viable populations at different localities along the South African coast including those where P. hoplura has already been established.

Polydorid polychaetes (Spionidae) on farmed and wild abalone (Haliotis midae) in South Africa: an epidemiological survey

Although there has been an increase in our understanding of the shell-boring polydorids that infest abalone Haliotis midae in South Africa, abalone from a limited number of farms, and wild populations from east of Cape Agulhas only, have been examined. To gain further knowledge and a more complete understanding of the local distribution of polydorids, we examined up to 30 abalone from each of 14 farms in the Northern, Western and Eastern Cape provinces, and five wild sites in the Western Cape, west of Cape Agulhas. Farm and wild communities were significantly different from each other (ANOSIM, r = 0.632, p < 0.002) and Bray–Curtis cluster analysis showed that most farms clustered separately from wild sites. Boccardia proboscidea was present on all but one of the infested farms, whereas some were also infested by Dipolydora capensis. By contrast, D. capensis was present at all wild sites sampled, whereas B. proboscidea was absent from these sites. Polydora hoplura, a common shell-boring pest, was present at only two farms and two wild sites. There appeared to be some exchange of polydorids among farms and between farms and wild abalone. The farm on the East Coast did not cluster with any other sites, indicating a unique composition of polydorids on that coast. No new, potentially problematic, species was encountered, although four species showed an increase in their known distribution.

Poecilogony in Polydora hoplura (Polychaeta: Spionidae) from commercially important molluscs in South Africa

Females of the polychaete Polydora hoplura (Claparede 1869) that produced planktotrophic and adelphophagic larvae were compared genetically to determine whether the different reproductive morphs represented sibling species or poecilogony. Worms were collected from Saldanha Bay, South Africa (33°0′37.71S, 17°56′59.74E), and cultured in a laboratory setting from November 2012 to April 2013. The results based on mitochondrial and nuclear DNA (Cyt b and ATPSα, respectively) showed shared haplotypes between reproductive morphs for both markers. Additionally, variation in mtDNA sequences was significantly higher within morphs than between morphs (95.8 and 4.2 %, respectively). A comparison of developmental modes found that broods of planktotrophic larvae were larger than broods of adelphophagic larvae, while the latter had larger eggs and larvae at hatching. Developmental time from oviposition to settlement for planktotrophic and adelphophagic larvae was 40.2 and 16.6 days, respectively. Polydora hoplura represents the fifth confirmed case of poecilogony in the Spionidae.

Control of Shell-Boring Polychaetes inHaliotis Tuberculata Coccinea(Reeve 1846) Aquaculture: Species Identification and Effectiveness of Mebendazole

The experimental culture of Haliotis tuberculata coccinea is carried out at the Institute of Marine Science of Canary Islands (Gran Canaria, Spain) based on specimens captured in their natural habitat and conditioned as broodstock. In 2008, an outbreak of shell-boring polychaetes affected the culture. This study aims to identify some of the species of shell-boring polychaetes that affect H. tuberculata coccinea and, second, to assess the effectiveness of multiple mebendazole applications for the control of these pests. Mebendazole was applied as baths of Lomper (Esteve Laboratory, Barcelona, Spain) using the concentrations 6 mL/L, 8 mL/L, and 10 mL/L, with 0 mL/L as a control measure. Abalone were exposed to 3 mebendazole baths over a 3-day period (1× 3-h bath applied for 3 consecutive days), as recommended in the drug directions for human use. After each bath, the abalone were returned to their original culture tanks until the following day. After these 3 days, the abalone were kept in their original culture tanks for a term of 1 mo. Each month, as a result of the effect of mebendazole, moribund and/or dead polychaetes became detached from the burrows and were found at the bottom of the tank during the first 15 days after the baths of mebendazole were applied. The polychaetes expelled from the shells were counted, collected, and fixed in 10% buffered formaldehyde for subsequent identification. This process was repeated month after month until no moribund and/or dead shell-boring polychaetes were found after the application of the baths of mebendazole. The shell-boring polychaete species was identified as Polydora hoplura (Claparède 1870). The efficacy rate of Lomper was around 99% in all the concentrations tested when it was applied during a 7-mo term (each month, 1 bath was applied for 3 consecutive days), and abalone mortality was limited to highly infested animals only. Monitoring of abalone weight gain suggested that the mebendazole treatments did not affect growth significantly during the study period.

Population structure and growth of polydorid polychaetes that infest cultured abalone Haliotis midae

Polydorid polychaetes can infest cultured abalone thereby reducing productivity. In order to effectively control these pests, their reproductive biology must be understood. The population dynamics and reproduction of polydorids infesting abalone Haliotis midae from two farms in South Africa is described using a length-based, age-structured model. Shells were infested mainly by introduced Boccardia proboscidea. Polydora hoplura and Dipolydora capensis were also present but in numbers too few to identify factors influencing infestation. At both farms, B. proboscidea lived for a minimum of 12 months. Growth rate, size at maturity, maximum size, infestation intensity, recruitment, percentage of the population brooding and mortality appear to be affected by abalone feeding regime and water temperature, and these factors need to be considered in controlling infestation. Brooders and recruits were present throughout the year, but increased significantly during mid- to late winter/early spring when water temperature and day length increased. Treatment measures should therefore be implemented throughout the year but with increased effort when water temperature increases.

CHIRURGIE de la main

Marine invasions are recognized as an important threat to global biodiversity and predicting the establishment and spread of an introduced species can aid in management efforts to mitigate the damage incurred by these species. In South Africa, the recently introduced polychaete Boccardia proboscidea has been recorded at the outflow of abalone farms where they are known to infest the shells of these mollusks. To determine if B. proboscidea can become established along the South African coast and subsequently expand its range, we assessed brood size, larval size at hatching, larval survivorship and developmental time and rate of this species under temperature regimes reflective of those found along the coast. We also investigated similar temperature dependent development in the well-established non-indigenous shell borer Polydora hoplura which can serve as a proxy for our predictions. Worms were cultured in glass capillary tubes at five different temperature treatments (12 °C, 17 °C, 21 °C, 24 °C, 28 °C) and planktotrophic and adelphophagic larvae were tracked from oviposition to settlement. We found that in P. hoplura, females producing adelphophagic larvae had smaller broods at the highest temperature treatment and higher temperatures resulted in significantly larger sizes at hatching. Survivorship of planktotrophic and adelphophagic larvae was highest at the intermediate to high temperature treatments (21 °C and 24 °C) and was generally lower at the lower temperatures (12 °C and 17 °C). Temperature had no significant effect on brood size of B. proboscidea whereas higher temperatures resulted in larger hatching sizes for planktotrophic and adelphophagic larvae. In B. proboscidea, larval types showed differences in survival optima with planktotrophic larvae exhibiting its highest survivorship at the colder temperatures and lowest at the warmer temperatures while adelphophagic larvae had its highest survivorship at 21 °C and its lowest at the extreme temperatures. There was a positive relationship between temperature and developmental rate for both species. The difference in larval sizes of the non-feeding planktotrophic larvae of B. proboscidea was attributed to a growth window that allowed for variability in reproductive traits based on exogenous factors such as temperature. More importantly, the results indicate that B. proboscidea will be capable of producing viable populations at different localities along the South African coast including those where P. hoplura has already been established.