Importance of seep primary production to Lophelia pertusa and associated fauna in the Gulf of Mexico

To investigate the importance of seep primary production to the nutrition of Lophelia pertusa and associated communities and examine local trophic interactions, we analyzed stable carbon, nitrogen, and sulfur compositions in seven quantitative L. pertusa community collections. A significant seep signature was only detected in one of the 35 species tested (Provanna sculpta, a common seep gastropod) despite the presence of seep fauna at the three sample sites. A potential predator of L. pertusa was identified (Coralliophila sp.), and a variety of other trophic interactions among the fauna occupying the coral framework were suggested by the data, including the galatheid crab Munidopsis sp. 2 feeding upon hydroids and the polychaete Eunice sp. feeding upon the sabellid polychaete Euratella sp. Stable carbon abundances were also determined for different sections of L. pertusa skeleton representing different stages in the growth and life of the aggregation. There was no temporal trend detected in the skeleton isotope values, suggesting that L. pertusa settles in these areas only after seepage has largely subsided. Isotope values of individual taxa that were collected from both L. pertusa and vestimentiferan habitats showed decreasing reliance upon seep primary production with average age of the vestimentiferan aggregation, and finally, no seep signature was detected in the coral collections. Together our data suggest that it is the presence of authigenic carbonate substrata, a product of past seep microbial activity, as well as hydrodynamic processes that drive L. pertusa occurrence at seep sites in the Gulf of Mexico, not nutritional dependence upon primary production by seep microbes.     

Depth-related structure and ecological significance of cold-seep communities—a case study from the Sea of Okhotsk

We discovered and investigated several cold-seep sites in four depth zones of the Sea of Okhotsk off Northeast Sakhalin: outer shelf (160–250 m), upper slope (250–450 m), intermediate slope (450–800 m), and Derugin Basin (1450–1600 m). Active seepage of free methane or methane-rich fluids was detected in each zone. However, seabed photography and sampling revealed that the number of chemoautotrophic species decreases dramatically with decreasing water depth. At greatest depths in the Derugin Basin, the seeps were inhabited by bacterial mats and bivalves of the families Vesicomyidae (Calyptogena aff. pacifica, C. rectimargo, Archivesica sp.), Solemyidae (Acharax sp.) and Thyasiridae (Conchocele bisecta). In addition, pogonophoran tubeworms of the family Sclerolinidae were found in barite edifices. At the shallowest sites, on the shelf at 160 m, the seeps lack chemoautotrophic macrofauna; their locations were indicated only by the patchy occurrence of bacterial mats.Typical seep-endemic metazoans with chemosynthetic symbionts were confined to seep sites at depths below 370 m. A comparative analysis of the structure of seep and background communities suggests that differences in predation pressure may be an important determinant of this pattern. The abundance of predators such as carnivorous brachyurans and asteroids, which can invade seeps from adjacent habitats and efficiently prey on sessile seep bivalves, decreased very pronouncedly with depth. We conclude from the obvious correlation with the conspicuous pattern in the distribution of seep assemblages that, on the shelf and at the upper slope, predator pressure may be high enough to effectively impede any successful settlement of viable populations of seep-endemic metazoans. However, there was also evidence that other depth-related factors, such as bottom-water current, sedimentary regimes, oxygen concentrations and the supply of suitable settling substrates, may additionally regulate the distribution of seep fauna in the area.As a consequence of the pronounced pattern in the distribution of seep communities, their ecological significance as food sources of surrounding background fauna increased with water depth. Isotopic analyses suggest that in the Derugin Basin seep colonists feed on chemoautotrophic seep organisms, either directly or by preying on metazoans with chemosynthetic symbionts. In contrast, seep organisms apparently do not contribute to the nutrition of the adjacent background fauna on the shelf and at the slope. In this area, elevated epifaunal abundances at seep sites were caused primarily by the availability of suitable settling substrates rather than by an enrichment of food supply.     

Monterey Bay cold-seep biota: Assemblages,abundance, and ultrastructure of living foraminifera

Although there is a growing body of evidence indicating benthic foraminifera inhabit hydrocarbon and cold seep environments, biochemical and ultrastructural data on seep foraminiferal communities are not available. Therefore, sediments collected from cold seeps in Monterey Bay, CA (900–1000 m), were examined for the presence of live benthic foraminifera. Results from three independent methods (ATP assay, ultrastructural analysis, rose Bengal staining) indicate that certain species inhabit the Clam Flat and Clam Field seeps. Abundances in our seep samples were lower than in comparable non-seep sites, although not atypical for these bathyal depths. Of 38 species represented at these two seep sites by cytoplasm-containing specimens, only Spiroplectammina biformis was restricted to the seep environment. However, because S. biformis is also known from non-seep sites in other areas, it should not be considered as endemic to seeps. Ultrastructural studies show abundant peroxisomes in seep specimens, which may allow inhabitation of such environments. One specimen of Uvigerina peregrina had prokaryotes nestled in test pores, suggesting that bacteria may play a role in the survival of foraminifera in this seep environment.     

Cold seeps of the deep Gulf of Mexico: Community structure and biogeographic comparisons to Atlantic equatorial belt seep communities

Quantitative collections of tubeworm- and mussel-associated communities were obtained from 3 cold seep sites in the deep Gulf of Mexico: in Atwater Valley at 1890 m depth, in Alaminos Canyon at 2200 m depth, and from the Florida Escarpment at 3300 m depth. A total of 50 taxa of macro- and megafauna were collected including 2 species of siboglinid tubeworms and 3 species of bathymodiolin mussels. In general, the highest degree of similarity was between communities collected from the same site. Most of the dominant families at the well-characterized upper Louisiana slope seep sites of the Gulf of Mexico were present at the deep sites as well; however, there was little overlap at the species level between the upper and lower slope communities. One major difference in community structure between the upper and lower slope seeps was the dominance of the ophiuroid Ophioctenella acies in the deeper communities. The transition between upper and lower slope communities appears to occur between 1300 and 1700 m based on the number of shared species with the Barbados seeps at either end of this depth range. Seep communities of the deep Gulf of Mexico were more similar to the Barbados Accretionary Prism seep communities than they were to either the upper slope Gulf of Mexico or Blake Ridge communities based on numbers of shared species and Bray–Curtis similarity values among sites. The presence of shared species among these sites suggests that there is ongoing or recent exchange among these areas. An analysis of bathymodioline mussel phylogeography that includes new collections from the west coast of Africa is presented. This analysis also suggests recent exchange across the Atlantic equatorial belt from the Gulf of Mexico to the seeps of the West Nigerian margin.     

Biologic and geologic characteristics of cold seeps in Monterey Bay, California

Cold seep communities discovered at three previously unknown sites between 600 and 1000 m in Monterey Bay, California, are dominated by chemoautotrophic bacteria (Beggiatoa sp.) and vesicomyid clams (5 sp.). Other seep-associated fauna included galatheid crabs (Munidopsis sp.), vestimentiferan worms (Lamellibrachia barhami?), solemyid clams (Solemya sp.), columbellid snails (Mitrella permodesta, Amphissa sp.), and pyropeltid limpets (Pyropelta sp.). More than 50 species of regional (i.e. non-seep) benthic fauna were also observed at seeps. Ratios of stable carbon isotopes (δ¹³C) in clam tissues near 36‰ indicate sulfur-oxidizing chemosynthetic production, rather than non-seep food sources, as their principal trophic pathway. The “Mt Crushmore” cold seep site is located in a vertically faulted and fractured region of the Pliocene Purisima Formation along the walls of Monterey Canyon ( 635 m), where seepage appears to derive from sulfide-rich fluids within the Purisima Formation. The “Clam Field” cold seep site, also in Monterey Canyon ( 900 m) is located near outcrops in the hydrocarbon-bearing Monterey Formation. Chemosynthetic communities were also found at an accretionary-like prism on the continental slope near 1000 m depth (Clam Flat site). Fluid flow at the “Clam Flat” site is thought to represent dewatering of accretionary sediments by tectonic compression, or hydrocarbon formation at depth, or both. Sulfide levels in pore waters were low at Mt Crushmore (ca 0.2 mM), and high at the two deeper sites (ca 7.011.0 mM). Methane was not detected at the Mt Crushmore site, but ranged from 0.06 to 2.0 mM at the other sites.     

Discovery of prolific natural methane seeps at Gullfaks, northern North Sea

The Gullfaks and Kvitebjørn fields are located on the North Sea Plateau (135 m water depth), and on an ancient beach (135–190 m) deposited during the sea-level lowstand during the Last Glacial Maximum (LGM). There are several continuous seeps of mainly methane gas, where large patches of Beggiatoa bacterial mats occur. The ‘Heincke’ seep area, which is named after the German research vessel Heincke, has been targeted by scientists studying seep-associated processes and microbiology. The Gullfaks area has a long history of shallow gas and seepage. In 1980, well no. 34/10–10 had a blowout from a reservoir located 230 m below seafloor. The active Heincke seep location has no topographic expression, probably because the seabed consists of dense sand and gravel. Extensive bacterial mats (Beggiatoa sp.) are found on the seafloor at this seep site. Organisms such as hermit crabs were seen ingesting pieces of such mat, indicating ‘trophic bypass,’ where carbon derived directly from seeping methane is evidently feeding directly into higher trophic organisms. Ongoing and future research at this seep location in the North Sea can answer some important questions on the environmental impact of natural methane seeps on continental shelves.     

Community structure and nutrition of deep methane-seep macrobenthos from the North Pacific (Aleutian) Margin and the Gulf of Mexico (Florida Escarpment)

Methane seeps occur at depths extending to over 7000 m along the world's continental margins, but there is little information about the infaunal communities inhabiting sediments of seeps deeper than 3000 m. Biological sampling was carried out off Unimak Island (3200–3300 m) and Kodiak Island (4500 m) on the Aleutian margin, Pacific Ocean and along the Florida Escarpment (3300 m) in the Gulf of Mexico to investigate the community structure and nutrition of macrofauna at these sites. We addressed whether there are characteristic infaunal communities common to the deep‐water seeps or to the specific habitats (clam beds, pogonophoran fields, and microbial mats) studied here, and ask how these differ from background communities or from shallow‐seep settings sampled previously. We also investigated, using stable isotopic signatures, the utilization of chemosynthetically fixed and methane‐derived organic matter by macrofauna from different regions and habitats. Within seep sites, macrofaunal densities were the greatest in the Florida microbial mats (20,961 ± 11,618 ind·m⁻²), the lowest in the Florida pogonophoran fields (926 ± 132 ind·m⁻²), and intermediate in the Unimak and Kodiak seep habitats. Seep macrofaunal densities differed from those in nearby non‐seep sediments only in Florida mat habitats, where a single, abundant species of hesionid polychaete comprised 70% of the macrofauna. Annelids were the dominant taxon (>60%) at all sites and habitats except in Florida background sediments (33%) and Unimak pogonophoran fields (27%). Macrofaunal diversity (H′) was lower at the Florida than the Alaska seeps, with a trend toward reduced richness in clam bed relative to pogonophoran field or non‐seep sediments. Community composition differences between seep and non‐seep sediments were evident in each region except for the Unimak margin, but pogonophoran and clam bed macrofaunal communities did not differ from one another in Alaska. Seep δ¹³C and δ¹⁵N signatures were lighter for seep than non‐seep macrofauna in all regions, indicating use of chemosynthetically derived carbon. The lightest δ¹³C values (average of species’ means) were observed at the Florida escarpment (−42.8‰). We estimated that on average animal tissues had up to 55% methane‐derived carbon in Florida mats, 31–44% in Florida clam beds and Kodiak clam beds and pogonophoran fields, and 9–23% in Unimak seep habitats. However, some taxa such as hesionid and capitellid polychaetes exhibited tremendous intraspecific δ¹³C variation (>30‰) between patch types. Overall we found few characteristic communities or features common to the three deep‐water seeps (>3000 m), but common properties across habitats (mat, clam bed, pogonophorans), independent of location or water depth. In general, macrofaunal densities were lower (except at Florida microbial mats), community structure was similar, and reliance on chemosynthesis was greater than observed in shallower seeps off California and Oregon.     

Phylogenetic position and systematics of the wood‐associate limpet genus Caymanabyssia and implications for ecological radiation into deep‐sea organic substrates by lepetelloid gastropods

The gastropod superfamily Lepetelloidea represents an extremely diverse lineage in terms of their utilization of different deep‐sea organic substrates that include sunken wood, leaves, whale and fish bones, egg cases of sharks and rays, annelid tubes and detrital cephalopod beaks among others. They also inhabit cold seeps and hydrothermal vents, thus presenting an interesting case for the evaluation of such organic substrates as ‘stepping stones’ into these chemosynthetically nourished environments. Here we show the first molecular phylogeny of the Pseudococculinidae, a primarily wood‐dwelling family and the most speciose in Lepetelloidea. Special emphasis is placed on the genus Caymanabyssia, for which the only subfamily Caymanabyssiinae has been established, and a new species Caymanabyssia solis is described herein and compared with previously known taxa in order to reconsider the morphological characteristics of lepetelloids on wood. Bayesian and likelihood trees reconstructed using four‐gene sequences reveal that Pseudococculinidae sensu auctt. is a polyphyletic taxon that is grouped by shared plesiomorphic conditions of characters including the radula, a digestive organ, the morphology of which is often governed strongly by diet and feeding ecology. The newly reinterpreted families Pseudococculinidae and Caymanabyssiidae represent reciprocal sister clades as a basal radiation in Lepetelloidea. Sunken wood might thus have served as an ancestral habitat from which species on other substrates and vent and seep taxa were derived.     

东山湾底栖介形类一新种(介形纲:壮肢目:海萤超科)

本文记录采自福建省东山湾的底栖介形类真喜萤属一新种:多刺真喜萤Euphilomedes spinulosasp.nov对其进行绘图和详细的描述,并与它的相似种非洲真喜萤Euphilomedes africanus(Klie,1940)进行特征比较,确定其新种地位。多刺真喜萤Euphilomedes spinulosasp.nov鉴别特征:(1)左壳腹缘内侧中部具13束短刺毛束;(2)第1、2、4、6对尾叉爪为主爪且细长,第3、5和7~11对尾叉爪为副爪,其中,第3和第5对爪夹于主爪之间;(3)第7附肢末端的开口下缘仅具1弯刺。     

软体动物腹足纲分类学研究进展——从近海到深海

随着科学技术的不断进步和研究的不断深入,我国关于海洋的研究已由浅海逐步向深海发展,不断取得新的发现和认知。自2014年4月起,中国科学院海洋研究所依托先进的"科学"号海洋科学综合考察船,搭载"发现"号水下机器人（remotelyoperated vehicle,ROV）,先后对冲绳海槽热液区、南海冷泉区、雅浦海山区以及马努斯热液区等深海区域进行了综合性科学考查,采集到了大量深海腹足纲（Gastropoda）标本,其中有一些为未经发现和描述的新种,极大地推动了我国关于深海软体动物物种多样性研究,实现了深海环境和软体动物资源的新认知。本文对近年来从深海采集到的腹足类标本进行了整理分类,对其中的11属13种进行描述,并对深海特殊环境中腹足纲物种多样性进行了总结,对中国软体动物腹足纲从近海至深海的分类现状进行研究论述。     

The discovery of a natural whale fall in the Antarctic deep sea

Large cetacean carcasses at the deep-sea floor, known as ‘whale falls’, provide a resource for generalist-scavenging species, chemosynthetic fauna related to those from hydrothermal vents and cold seeps, and remarkable bone-specialist species such as Osedax worms. Here we report the serendipitous discovery of a late-stage natural whale fall at a depth of 1444 m in the South Sandwich Arc. This discovery represents the first natural whale fall to be encountered in the Southern Ocean, where cetaceans are abundant. The skeleton was situated within a seafloor caldera, in close proximity (<250 m) to active hydrothermal vents. We used a DNA barcoding approach to identify the skeleton as that of an Antarctic minke whale (Balaenoptera bonaerensis). The carcass was in an advanced state of decomposition, and its exposed bones were occupied by a diverse assemblage of fauna including nine undescribed species. These bone fauna included an undescribed species of Lepetodrilus limpet that was also present at the nearby hydrothermal vents, suggesting the use of whale-fall habitats as stepping stones between chemosynthetic ecosystems. Using Remotely Operated Vehicle (ROV) videography, we have quantified the composition and abundance of fauna on the whale bones, and tested a hypothesis that varying concentrations of lipids in the bones of whales may influence the microdistribution of sulfophilic whale-fall fauna. Our data supported the hypothesis that more lipid-rich bones support a greater abundance of sulfophilic bacterial mats, which are also correlated with the abundance of grazing limpets (Pyropelta sp.). The abundance of Osedax sp. on bones however, showed a negative correlation with the bacterial-mat percentage cover, and hence greatest abundance on bones predicted to have lowest lipid content.     

Parasitic barnacles (Cirripedia: Rhizocephala) from New Zealand off‐shore waters

Nine genera and species of rhizocephalans were recorded from the off‐shore waters around New Zealand. Mitochondrial and nuclear gene sequences were used to examine base differences between the European and New Zealand species of Parthenopea. Serial sections to study the internal structures of the reproductive organs were made for the genera Thylacoplethus and Thompsonia. Two species, Parthenopea australis n. sp. and Thylacoplethus novaezealandiae n. sp. are new to science and described in detail. Parthenopea australis n. sp. is the first rhizocephalan species recorded from the vicinity of active cold seeps. Three rhizocephalans could not be identified as they were parasitised by hyperparasitic cryptoniscine isopods. The decapodhost species comprised the taxa Paguridae, Lithodidae, Galatheidae, Chirostylidae, and Callianassidae.     

Macrobenthic infaunal communities associated with deep‐sea hydrocarbon seeps in the northern Gulf of Mexico

There are thousands of seeps in the deep ocean worldwide; however, many questions remain about their contributions to global biodiversity and the surrounding deep‐sea environment. In addition to being globally distributed, seeps provide several benefits to humans such as unique habitats, organisms with novel genes, and carbon regulation. The purpose of this study is to determine whether there are unique seep macrobenthic assemblages, by comparing seep and nonseep environments, different seep habitats, and seeps at different depths and locations. Infaunal community composition, diversity, and abundance were examined between seep and nonseep background environments and among three seep habitats (i.e., microbial mats, tubeworms, and soft‐bottom seeps). Abundances were higher at seep sites compared to background areas. Abundance and diversity also differed among microbial mat, tubeworm, and soft‐bottom seep habitats. Although seeps contained different macrobenthic assemblages than nonseep areas, infaunal communities were also generally unique for each seep. Variability was 75% greater within communities near seeps compared to communities in background areas. Thus, high variability in community structure characterized seep communities rather than specific taxa. The lack of similarity among seep sites supports the idea that there are no specific infauna that can be used as indicators of seepage throughout the northern Gulf of Mexico, at least at higher taxonomic levels.     

中国南海中南部花水母亚纲一新属四新种记述

本文描述了采自中国南海中南部花水母亚纲一新属四新种：南海宽管水母,新属、新种Laticanna nanhaiensis gen.nov. et sp.nov.,芽拟原帽水母,新种Protiaropsis gemmifera sp.nov.,南海潜水母,新种Merga nanhaiensis sp.nov.和顶室无球水母,新种Rhabdoon apiciloculus sp.nov.。编制了深帽水母科已知属分属检索表和拟帽水母属、潜水母属以及无球水母属已知种分种检索表。模式标本保存于中国水产科学研究院南海水产研究所。     

Improved detection and mapping of deepwater hydrocarbon seeps: optimizing multibeam echosounder seafloor backscatter acquisition and processing techniques

Marine seep hunting surveys are a current focus of hydrocarbon exploration surveys due to recent advances in offshore geophysical surveying, geochemical sampling, and analytical technologies. Hydrocarbon seeps are ephemeral, small, discrete, and therefore difficult to sample on the deep seafloor. Multibeam echosounders are an efficient seafloor exploration tool to remotely locate and map seep features. Geophysical signatures from hydrocarbon seeps are acoustically-evident in bathymetric, seafloor backscatter, midwater backscatter datasets. Interpretation of these signatures in backscatter datasets is a fundamental component of commercial seep hunting campaigns. Degradation of backscatter datasets resulting from environmental, geometric, and system noise can interfere with the detection and delineation of seeps. We present a relative backscatter intensity normalization method and an oversampling acquisition technique that can improve the geological resolvability of hydrocarbon seeps. We use Green Canyon (GC) Block 600 in the Northern Gulf of Mexico as a seep calibration site for a Kongsberg EM302 30 kHz MBES prior to the start of the Gigante seep hunting program to analyze these techniques. At GC600, we evaluate the results of a backscatter intensity normalization, assess the effectiveness of 2X seafloor coverage in resolving seep-related features in backscatter data, and determine the off-nadir detection limits of bubble plumes using the EM302. Incorporating these techniques into seep hunting surveys can improve the detectability and sampling of seafloor seeps.     

Sidescan backscatter variations of cold seeps on the Hikurangi Margin (New Zealand): indications for different stages in seep development

Cold seeps on the Hikurangi Margin off New Zealand exhibit various seabed morphologies producing different intensity patterns in sidescan backscatter images. Acoustic backscatter characteristics of 25 investigated seep sites fall into four distinct types characterised by variations in backscatter intensity, distribution and inferred structural heights. The types reflect different carbonate morphologies including up to 20-m-high structures (type 1), low-relief crusts (type 2), scattered blocks (type 3) and carbonate-free sites (type 4). Each seep corresponds to a single type; intermediates were not observed. This correlates well with published data on seep fauna at each site, with the four types representing three different faunal habitats of successive stages of seep development. Backscatter signatures in sidescan sonar images of cold seeps may therefore serve as a convenient proxy for variations in faunal habitats.     

Seep mounds on the Southern Vøring Plateau (offshore Norway)

Multidisciplinary study of seep-related structures on Southern Vøring Plateau has been performed during several UNESCO/IOC TTR cruises on R/V Professor Logachev. High-resolution sidescan sonar and subbottom profiler data suggest that most of the studied fluid discharge structures have a positive relief at their central part surrounded by depression. Our data shows that the present day fluid activity is concentrated on the top of these “seep mounds”. Number of high hydrocarbon (HC) gas saturated sediment cores and 5 cores with gas hydrate presence have been recovered from these structures. δ¹³C of methane (between −68 and −94.6‰ VPDB) and dry composition of the gas points to its biogenic origin. The sulfate depletion generally occurs within the upper 30–200 cm bsf and usually coincides with an increase of methane concentration. Pore water δ¹⁸O ranges from 0.29 to 1.14‰ showing an overall gradual increase from bottom water values (δ¹⁸O ∼ 0.35‰). Although no obvious evidence of fluid seepage was observed during the TV surveys, coring data revealed a broad distribution of living Pogonophora and bacterial colonies on sea bottom inside seep structures. These evidences point to ongoing fluid activity (continuous seepage of methane) through these structures. From other side, considerable number and variety of chemosynthetic macro fauna with complete absence of living species suggest that present day level of fluid activity is significantly lower than it was in past. Dead and subfossil fauna recovered from various seep sites consist of solemyid (Acharax sp.), thyasirid and vesicomyid (cf. Calyptogena sp.) bivalves belonging to chemosymbiotic families. Significant variations in δ¹³C (−31.6‰ to −59.2‰) and δ¹⁸O (0.42‰ and 6.4‰) of methane-derived carbonates collected from these structures most probably related to changes in gas composition and bottom water temperature between periods of their precipitation. This led us to ideas that: (1) seep activity on the Southern Vøring Plateau was started with large input of the deep thermogenic gas and gradually decries in time with increasing of biogenic constituent; (2) authigenic carbonate precipitation started at the near normal deep sea environments with bottom water temperature around +5 °C and continues with gradual cooling up to negative temperatures recording at present time.     

Similar reproductive cycles and life-history traits in congeneric limid bivalves with different modes of nutrition

We have studied two congeneric limid bivalves, Acesta species novum and Acesta excavata (Bivalvia: Limidae), that live in similar physical conditions but use different food sources. Acesta sp. nov. live on the giant siboglinid tubeworm Lamellibrachia luymesi at cold seeps and feed on their eggs, a continuous food source that ultimately is derived from chemosynthesis, whereas A. excavata relies on planktonic food of photosynthetic origin, which varies seasonally. We hypothesized that these two species might show differences in the periodicity of reproduction; specifically, we predicted that A. sp. nov. would breed continuously and that A. excavata would demonstrate an annual reproductive cycle. Our hypothesis was refuted, as both species have a semi‐continuous reproductive cycle. Food quality, quantity or seasonality had no clear effect. Reproductive adults are functionally gonochoristic. Females broadcast buoyant eggs with an average size of 179 μm in A. sp. nov. and 160 μm in A. excavata. Both the size of the larval shell and the size of the spawned eggs are suggestive of pelagic lecithotrophic development. Both species also appear to be protandric hermaphrodites, changing from male to female at approximately 77 and 90 mm shell height, respectively, although not all individuals change sex. In the material investigated in this study there was a biased sex ratio favouring males.