Martin Thiel

Disentangling Ribbon Worm Relationships: Multi-Locus Analysis Supports Traditional Classification of the Phylum Nemertea

The phylogenetic relationships of selected members of the phylum Nemertea are explored by means of six markers amplified from the genomic DNA of freshly collected specimens (the nuclear 18S rRNA and 28S rRNA genes, histones H3 and H4, and the mitochondrial genes 16S rRNA and cytochrome c oxidase subunit I). These include all previous markers and regions used in earlier phylogenetic analyses of nemerteans, therefore acting as a scaffold to which one could pinpoint any previously published study. Our results, based on analyses of static and dynamic homology concepts under probabilistic and parsimony frameworks, agree in the non‐monophyly of Palaeonemertea and in the monophyly of Heteronemerta and Hoplonemertea. The position of Hubrechtella and the Pilidiophora hypothesis are, however, sensitive to analytical method, as is the monophyly of the non‐hubrechtiid palaeonemerteans. Our results are, however, consistent with the main division of Hoplonemertea into Polystilifera and Monostilifera, the last named being divided into Cratenemertea and Distromatonemertea, as well as into the main division of Heteronemertea into Baseodiscus and the remaining species. The study also continues to highlight the deficient taxonomy at the family and generic level within Nemertea and sheds light on the areas of the tree that require further refinement.

Marine Litter as Habitat and Dispersal Vector

Floating anthropogenic litter provides habitat for a diverse community of marine organisms. A total of 387 taxa, including pro- and eukaryotic micro-organisms, seaweeds and invertebrates, have been found rafting on floating litter in all major oceanic regions. Among the invertebrates, species of bryozoans, crustaceans, molluscs and cnidarians are most frequently reported as rafters on marine litter. Micro-organisms are also ubiquitous on marine litter although the composition of the microbial community seems to depend on specific substratum characteristics such as the polymer type of floating plastic items. Sessile suspension feeders are particularly well-adapted to the limited autochthonous food resources on artificial floating substrata and an extended planktonic larval development seems to facilitate colonization of floating litter at sea. Properties of floating litter, such as size and surface rugosity, are crucial for colonization by marine organisms and the subsequent succession of the rafting community. The rafters themselves affect substratum characteristics such as floating stability, buoyancy, and degradation. Under the influence of currents and winds marine litter can transport associated organisms over extensive distances. Because of the great persistence (especially of plastics) and the vast quantities of litter in the world’s oceans, rafting dispersal has become more prevalent in the marine environment, potentially facilitating the spread of invasive species.

Reproductive biology of Limnoria chilensis: another boring peracarid species with extended parental care

Several boring peracarid species engage in extended parental care with parents tolerating small juveniles in their burrows, but only anecdotal observations have been reported from boring isopods of the genus Limnoria. The isopod Limnoria chilensis Menzies is frequently found in holdfasts of the macroalgae Macrocystis pyrifera (L.) C. Agardh and Durvillea antarctica (Chamisso) Hariot. In the present study, holdfasts of D. antarctica that harboured L. chilensis were carefully dissected in order to examine the association pattern of reproductive females and small juveniles. In most infested holdfasts, L. chilensis reached very high densities of 43.7 ± 3.9 (mean ± SE) individuals cm−2 (range: 0–90 individuals cm−2). The overall sex ratio (females:males) was close to unity (1.2). Male size varied between 1.5 and 2.6 mm body length (BL) and female size between 1.5 and 3.6mm BL. The percentage of reproductive females was low (19.7% of all females), and only the largest females (>2.6 mm BL) were reproductive. Embryo numbers ranged between six and 19 per female and a significant correlation between female BL and the number of embryos was found. Several females were found with small juveniles (0.8–1.2 mm BL) in the terminal end of their burrows. On several occasions, aggregations of similar-sized juveniles (1.0–1.5 mm BL) in their own burrows were found near a female burrow, indicating that these juveniles initiated their first individual burrows from within the maternal burrows. Some females with small juveniles in the terminal end of their burrows were either accompanied by males or they were ovigerous, indicating that they may have been in the process of producing a second brood. The fact that juveniles build their first burrows in the protection of female burrows suggests that such small juveniles have not yet developed full boring capacity. Extended parental care in this (and other boring) peracarid species represents a mechanism facilitating high juvenile survival rates. Given the highly local recruitment, it is suggested that the reproductive biology of this isopod has strong implications for Its population biology.

Floating Seaweeds and Their Communities

A wide diversity of floating seaweeds is found in temperate and subpolar regions of the world’s oceans where sea surface currents and winds determine their traveling velocities and directions. The importance of floating seaweeds as dispersal agents for associated organisms and for the algae themselves varies depending on the supply from benthic source populations and on their persistence at the sea surface. Persistence of floating algae depends on water temperature, grazing activity, epifaunal load, and, to a lesser extent, on prevailing irradiance conditions. In temperate regions, persistence of floating algae is primarily limited by warm sea surface temperatures and high densities of motile and sessile epifauna whereas at higher latitudes algae can successfully compensate grazer-induced tissue loss by continuous growth at the prevailing low water temperatures. Accordingly, floating seaweeds can bridge large oceanic distances especially at high latitudes allowing for connectivity among distant benthic populations of algae and associated rafters.

Mating behavior of nemerteans: present knowledge and future directions

In most nemertean species, members of the two sexes aggregate before fertilization takes place. Few specific studies on the mating behaviour of nemerteans have been conducted but several observational reports indicate that important processes known from other organisms, such as sexual selection and sperm competition, may also be at work in nemerteans. Herein, we review some of these observations and discuss their possible implications. We produce a summary table and reproduce some important observations, placing them in an evolutionary context. Four types of gamete‐transfer mechanisms are distinguished: (1) free‐spawning, where members of both sexes release gametes freely into the water column; (2) mucus‐spawning, where gametes are released within a mucus matrix; (3) internal fertilization, where spermatozoans are transferred to the immediate vicinity of oviducts, which they penetrate; and (4) gamete transfer aided by specific structures. While little is known about the last transfer mechanism, anecdotal observations are mainly available for the first three mechanisms. Mating interactions frequently involve more than two individuals. In several species, individuals only invest part of their gametes in a single mating interaction, apparently saving additional gametes for potential future mating events. These observations suggest that males of some species are exposed to mating competition. Males might counteract sperm competition by producing large numbers of sperm, as suggested by their high fertilization potential. Previous authors inferred that sperm morphology may be an adaptation to spawning behavior and possibly also to the risk of sperm competition. Based on the results of our analysis and the above observations, we suggest that sexual selection and sperm competition are not uncommon in nemerteans.

Microplastic: What Are the Solutions?

The plastic that pollutes our waterways and the ocean gyres is a symptom of upstream material mismanagement, resulting in its ubiquity throughout the biosphere in both aquatic and terrestrial environments. While environmental contamination is widespread, there are several reasonable intervention points present as the material flows through society and the environment, from initial production to deep-sea microplastic sedimentation. Plastic passes through the hands of many stakeholders, with responsibility for environmental contamination owned, shared, or rejected by plastic producers, product/packaging manufacturers, government, consumers, and waste handlers.

The future of nemertean taxonomy (phylum Nemertea) — a proposal

Submitted: 15 January 2016 Accepted: 6 March 2016 doi:10.1111/zsc.12182 Sundberg, P., Andrade, S.C.S., Bartolomaeus, T., Beckers, P., von D€ ohren, J., Kr€amer, D., Gibson, R., Giribet, G., Herrera-Bachiller, A., Juan, J., Kajihara, H., Kvist, S., K anneby, T., Sun S.-C., Thiel, M., Turbeville, J.M. , Strand, M. (2016). The future of nemertean taxonomy (phylum Nemertea) — a proposal. —Zoologica Scripta, 45: 579–582. Corresponding author: Per Sundberg, University of Gothenburg, Department of Marine Sciences, Gothenburg, Sweden. E-mail: per.sundberg@gu.se Per Sundberg, University of Gothenburg, Department of Marine Sciences, Gothenburg, Sweden.. E-mail: per.sundberg@gu.se S onia C. S. Andrade, Departamento de Gen etica e Biologia Evolutiva, IB-Universidade de, S~ao Paulo, Brazil, S~ao Paulo, Brazil. E-mail: soniacsandrade@gmail.com Thomas Bartolomaeus, Patrick Beckers, J€orn von D€ohren, and Daria Kr€amer, University of Bonn, Institute of Evolutionary Biology and Animal Ecology, Bonn, Germany. E-mails: tbartolomaeus@evolution.uni-bonn.de, pbeckers@evolution.uni-bonn.de, jdoehren@evolution.uni-bonn.de, dkraemer@evolution.uni-bonn.de Ray Gibson, 94 Queens Avenue, Meols, Wirral, CH47 0NA, U.K. E-mail: bfginc@hotmail.co.uk Gonzalo Giribet, Museum of Comparative Zoology, Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA. E-mail: ggiribet@g.harvard.edu Alfonso Herrera-Bachiller, and Juan Junoy, Departamento de Ciencias de la Vida, Universidad de Alcal a, Madrid, Spain. E-mails: alfonso@herrerabachiller.com, juan.junoy@uah.es Hiroshi Kajihara, Faculty of Science, Hokkaido University, Sapporo, Japan. E-mail: kazi@mail.sci.hokudai.ac.jp Sebastian Kvist, Department of Natural History, Royal Ontario Museum, Toronto, Canada and Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Canada. E-mail: sebastian.kvist@utoronto.ca Tobias K anneby, Swedish Museum of Natural History, Department of Zoology, Stockholm, Sweden. E-mail: Tobias.Kanneby@nrm.se, tobiaskanneby@gmail.com Shi-Chun Sun, Institute of Evolution & Marine Biodiversity, Ocean University of China, Qingdao, China. E-mail: sunsc@ouc.edu.cn Martin Thiel, Facultad Ciencias del Mar, Centro de Estudios Avanzados en Zonas Áridas (CEAZA), Millennium Nucleus Ecology and Sustainable Management of Oceanic Island (ESMOI), Universidad Cat olica del Norte, Coquimbo, Chile. E-mail: thiel@ucn.cl James M. Turbeville, Department of Biology, Virginia Commonwealth University, Richmond, VA, USA. E-mail: jmturbeville@vcu.edu Malin Strand, Swedish Species Information Centre, The Sven Lov en Centre for Marine Sciences, Str€omstad, Sweden. E-mail: malin.strand@slu.se

Float and Raft: Role of Buoyant Seaweeds in the Phylogeography and Genetic Structure of Non-buoyant Associated Flora

Many seaweed species (primary rafters) float at the sea surface and travel with marine currents after detachment from benthic habitats. Various studies have confirmed that dispersal via floating sporophytes and/or gametophytes influences the phylogeography and genetic population structure of these buoyant seaweeds. In addition, non-buoyant seaweeds (secondary rafters) that grow attached to or intermingled with these primary floaters may also become dispersed by rafting on their floating hosts. Here, we examine reports of non-buoyant seaweed species associated with buoyant seaweeds and discuss potential consequences for their phylogeography and/or genetic population structure. We found that mostly red and brown algae have been reported with floating seaweed rafts, most of them growing as epiphytes and some as obligate parasites (e.g. endophytes) that travel with their hosts. Molecular evidence suggests dispersal associated with primary floaters in 16 non-buoyant seaweeds, although colonization of distant sites could also have occurred via other floating substrata such as wood, buoys, and other man-made materials. Transoceanic dispersal has been inferred for non-buoyant seaweeds (for example, Gracilaria chilensis and Capreolia implexa) based on low levels of genetic structure and shared haplotypes among populations separated over vast distances of open ocean (e.g. New Zealand–Chile). Some non-buoyant species suspected or shown to be dispersed by rafting are from intertidal habitats, and these algae can resist physiologically stressful conditions during long trips at the sea surface. However, subtidal and low intertidal non-buoyant species have higher potential to be transported because they cohabit with common raft-forming kelps, often growing on them as epiphytes. We conclude that buoyant seaweeds play an important role in driving the phylogeography, evolution, connectivity and distribution of non-buoyant associated seaweeds. Dispersal of non-buoyant seaweeds via these floating seaweeds may have been underestimated in the past.

Juvenile Sphaeroma quadridentatum invading female-offspring groups of Sphaeroma terebrans

Female isopods Sphaeroma terebrans Bate 1866 are known to host their offspring in family burrows in aerial roots of the red mangrove Rhizophora mangle. During a study on the reproductive biology of S. terebrans in the Indian River Lagoon, Florida, USA, juvenile S. quadridentatum were found in family burrows of S. terebrans. Between September 1997 and August 1998, each month at least one female S. terebrans was found with juvenile S. quadridentatum in its burrow. The percentage of S. terebrans family burrows that contained juvenile S. quadridentatum was high during fall 1997, decreased during the winter, and reached high values again in late spring/early summer 1998, corresponding with the percentage of parental female S. terebrans (i.e. hosting their own juveniles). Most juvenile S. quadridentatum were found with parental female S. terebrans, but a few were also found with reproductive females that were not hosting their own offspring. Non-reproductive S. terebrans (single males, subadults, non-reproductive females) were never found with S. quadridentatum in their burrows. The numbers of S. quadridentatum found in burrows of S. terebrans ranged between one and eight individuals per burrow. No significant correlation between the number of juvenile S. quadridentatum and the numbers of juvenile S. terebrans in a family burrow existed. However, burrows with high numbers of juvenile S. quadridentatum often contained relatively few juvenile S. terebrans. The majority of juvenile S. quadridentatum found in family burrows of S. terebrans were smaller than the juvenile S. terebrans that were cared for by their mothers. The results indicate that the presence of S. quadridentatum in S. terebrans family burrows may negatively affect the duration of extended parental care in S. terebrans. It is not known why parental female S. terebrans are not able to discriminate against juvenile S. quadridentatum. Possibly, the fact that the two species are closely related facilitates S. quadridentatum sneaking into S. terebrans family burrows.

The smile of Amphiporus nelsoni Sanchez, 1973 (Nemertea: Hoplonemertea: Monostilifera: Amphiporidae) leads to a redescription and a change in family

ABSTRACT A common intertidal hoplonemertean species, Amphiporus nelsoni Sanchez, 1973, from Chile is re-described based on the investigation of material from the type locality and one other locality in Chile. The species is transferred to the genus Prosorhochmus Keferstein, 1862 (Prosorhochmidae) based on the presence of a dorsal epidermal fold, i.e., “prosorhochmid smile” on the bilobed head, truncated stylet basis, well-developed frontal organ with characteristic epithelial specialization, structure of the nephridial system and other characters of internal anatomy. Placement of this species into Prosorhochmus expands the geographical distribution of the genus, previously known only from the North Atlantic and Mediterranean, to the South Pacific. Interestingly, Prosorhochmus nelsoni (Sanchez, 1973) is characterized by separate sexes and oviparity, unlike all the other members of the genus, which combine hermaphroditism with ovoviviparity. We compare P. nelsoni to the other species of Prosorhochmus and reassess some of the morphological characters used in the systematics of the genus.