Microsporidia-nematode associations in methane seeps reveal basal fungal parasitism in the deep sea

The deep sea is Earth’s largest habitat but little is known about the nature of deep-sea parasitism. In contrast to a few characterized cases of bacterial and protistan parasites, the existence and biological significance of deep-sea parasitic fungi is yet to be understood. Here we report the discovery of a fungus-related parasitic microsporidium, Nematocenator marisprofundi n. gen. n. sp. that infects benthic nematodes at Pacific Ocean methane seeps on the Pacific Ocean floor. This infection is species-specific and has been temporally and spatially stable over two years of sampling, indicating an ecologically consistent host-parasite interaction. A high distribution of spores in the reproductive tracts of infected males and females and their absence from host nematodes’ intestines suggests a sexual transmission strategy in contrast to the fecal-oral transmission of most microsporidia. N. marisprofundi targets the host’s body wall muscles causing cell lysis, and in severe infection even muscle filament degradation. Phylogenetic analyses placed N. marisprofundi in a novel and basal clade not closely related to any described microsporidia clade, suggesting either that microsporidia-nematode parasitism occurred early in microsporidia evolution or that host specialization occurred late in an ancient deep-sea microsporidian lineage. Our findings reveal that methane seeps support complex ecosystems involving interkingdom interactions between bacteria, nematodes, and parasitic fungi and that microsporidia parasitism exists also in the deep sea biosphere.

Range extension and reproduction of the barnacle Balanus perforatus in the eastern English Channel

The distribution of the warm-water barnacle, Balanus perforatus, was surveyed along the south coast of England and the north-east coast of France between 1993 and 2001, repeating work carried out between the 1940s and 1960s. The species has recovered from catastrophic mortality during the severe winter of 1962–1963 and was found over 120 km (UK) and 190 km (France) east of previous records on both sides of the Channel. The presence of the species in the eastern Channel refutes suggestions in the 1950s that larvae, and hence adults, would not be found east of the Isle of Wight because of reproductive sterility close to the limits of distribution. Brooding of specimens translocated to Bembridge, Isle of Wight, commenced in May, earlier than previously observed in British waters, and continued until September. The stage of embryo development at Bembridge in mid-August was comparable to that of the large population at Lyme Regis, Dorset 100 km further west. However the size of brood per standard body weight was greater at Lyme Regis. Factors influencing the rate of colonization and further geographic range extension of the species as a possible result of climate change, are discussed.

Growth and breeding of a primitive stalked barnacle Leucolepas longa (Cirripedia: Scalpellomorpha: Eolepadidae: Neolepadinae) inhabiting a volcanic seamount off Papua New Guinea

A pedunculate barnacle, Leucolepas longa, occurs in densities over 1000 individuals m[minus sign]2 on the summit of a small seamount near New Ireland, Papua New Guinea. Most of the population grows on vesicomyid clams projecting from sulphide-rich sediments, or on their dead shells, but the barnacle also settles on rock and on tubes of a vestimentiferan. Collections of several hundred barnacles allowed comparison of population and reproductive characteristics. The barnacle is a suspension feeder with a lightly-armoured stalk that can grow to 40 cm above the bottom. Growth appears to be rapid and both reproduction and recruitment are continuous. The barnacles brood egg masses within the capitular chamber and 46% of one sample was brooding. Lecithotrophic nauplii released upon retrieval to the surface were cultivated for 45 days. Metamorphosis to Stage IV yielded an actively swimming larva about 1 mm long overall, which still contained lipid reserves, indicating capacity for wide dispersal

Population-Dynamics Of Mytilicola-Intestinalis In Mytilus-Edulis In South West England

The population dynamics of Mytilicola intestinalis Steuer in mussels (Mytilus edulis L.) from the River Lynher, Cornwall, England, have been studied over 3 years. By transplanting uninfested mussels from the River Erme, South Devon, into the Lynher mussel bed, the study was extended to the growth and development of new infestations under natural conditions. Female Mytilicola intestinalis are shown to breed twice, and two generations of parasites coexist for most of the year, with recruitment taking place in summer and autumn. One generation contributes its first brood to the autumn recruits before overwintering and contributing its second brood to the following summer's recruits. The other generation overwinters as juvenile and immature stages to contribute its two broods successively to the summer and autumn recruits. Environmental temperatures are believed to control the rates of development at all stages rather than acting as triggers in the onset or cessation of breeding at specific times. There is no evidence to support the contention that heavily infested mussels are killed, and parasite mortality is shown to be density-independent.

Relationship Between Infestation By Mytilicola-Intestinalis Steuer (Copepoda Cyclopoidea) And Condition Index Of Mytilus-Edulis In Southwest England

Seasonal cycles in the condition index of Mytilus edulis from three sites in southwest England are described. These are analysed in relation to host length, stage of gonad development and parasite burden by linear regression analysis. An effect on the condition index due to the presence of Mytilicola intestinalis can be detected only in the sublittoral mussels in those few winter months when the mean intensity of infestation is over about 25 parasites per host. In all cases studied, the magnitude of the effect due to variation in host length, stage of gonad development, seasonal cycles and environmental factors is greater than that due to parasitism.

Heterospecific mating and species recognition in the planktonic marine copepods Temora stylifera and T. longicornis

Many planktonic copepods use diffusible pheromone or hydromechanical signals to remotely detect the presence of potential mates. To determine whether these mating signals also play a role in species recognition and mate choice, we observed and video recorded (3D) mate-finding and pursuit behaviors in heterospecific and conspecific mating crosses in a pair of congeneric, partially sympatric species (Temora stylifera and T. longicornis) in the laboratory. The species appear to have asymmetrical pre-mating isolation, with T. longicornis males readily pursuing T. stylifera females to mate contact and capture, but with little mate-finding activity observed in the reverse cross. Males of T. longicornis pursuing heterospecific females executed a number of behaviors known to facilitate successful pheromone trail following and mate capture in conspecific mating, including accelerated swimming in a ‘signal-scanning’ mode to recover a lost pheromone trail, reversal of the tracking direction in cases when the male initiated tracking in the incorrect direction, and accelerated swimming speeds when in the presence of a pheromone signal but prior to locating the trail. Detailed analyses of mate-tracking behavior in T. longicornis male × T. stylifera female crosses gave no indication that males were aware they were pursuing heterospecific females prior to mate contact, indicating that diffusible pheromone and hydromechanical signals are not used, either singly or in combination, for species recognition in this mating pair. Heterospecific mating attempts among sympatric, congeneric copepods may commonly proceed to mate capture, and incur fitness costs to either or both mating partners.

Intersex in the clam Scrobicularia plana (Da Costa): Widespread occurrence in English Channel estuaries and surrounding areas

Estuarine clams Scrobicularia plana were sampled from 108 intertidal locations around the English Channel and adjacent areas. Although S. plana is believed to be a strict gonochorist, 58% of the populations sampled included intersexed individuals (described as male clams exhibiting ovotestis). Over the entire region, on average, 8.6% of male clams exhibited intersex, although proportions of affected males ranged from 0% to 53% depending on location. The severity of intersex was assessed using a simple classification scale, with the majority of individuals showing low levels of impact. Sex ratios were significantly skewed at some sites. There were no significant relationships between the incidence and severity of intersex; or of associations with size or parasitism of individual clams. Intersex in S. plana is a useful tool to assess endocrine disruptive effects in estuaries, although mechanisms of impact and causative agents remain uncertain.

Are Prorocentrum hoffmannianum and Prorocentrum belizeanum (Dinophyceae, Prorocentrales), the same species? An integration of morphological and molecular data.

The taxonomic assignment of Prorocentrum species is based on morphological characteristics; however, morphological variability has been found for several taxa isolated from different geographical regions. In this study, we evaluated species boundaries of Prorocentrum hoffmannianum and Prorocentrum belizeanum based on morphological and molecular data. A detailed morphological analysis was done, concentrating on the periflagellar architecture. Molecular analyses were performed on partial Small Sub-Unit (SSU) rDNA, partial Large Sub-Unit (LSU) rDNA, complete Internal Transcribed Spacer Regions (ITS1-5.8S-ITS2), and partial cytochrome b (cob) sequences. We concatenated the SSU-ITS-LSU fragments and constructed a phylogenetic tree using Bayesian Inference (BI) and maximum likelihood (ML) methods. Morphological analyses indicated that the main characters, such as cell size and number of depressions per valve, normally used to distinguish P. hoffmannianum from P. belizeanum, overlapped. No clear differences were found in the periflagellar area architecture. Prorocentrum hoffmannianum and P. belizeanum were a highly supported monophyletic clade separated into three subclades, which broadly corresponded to the sample collection regions. Subtle morphological overlaps found in cell shape, size, and ornamentation lead us to conclude that P. hoffmanianum and P. belizeanum might be considered conspecific. The molecular data analyses did not separate P. hoffmannianum and P. belizeanum into two morphospecies, and thus, we considered them to be the P. hoffmannianum species complex because their clades are separated by their geographic origin. These geographic and genetically distinct clades could be referred to as ribotypes: (A) Belize, (B) Florida-Cuba, (C1) India, and (C2) Australia.

Identifying predictable foraging habitats for a wide-ranging marine predator using ensemble ecological niche models

Aim: Ecological niche modelling can provide valuable insight into species' environmental preferences and aid the identification of key habitats for populations of conservation concern. Here, we integrate biologging, satellite remote-sensing and ensemble ecological niche models (EENMs) to identify predictable foraging habitats for a globally important population of the grey-headed albatross (GHA) Thalassarche chrysostoma. Location: Bird Island, South Georgia; Southern Atlantic Ocean. Methods: GPS and geolocation-immersion loggers were used to track at-sea movements and activity patterns of GHA over two breeding seasons (n = 55; brood-guard). Immersion frequency (landings per 10-min interval) was used to define foraging events. EENM combining Generalized Additive Models (GAM), MaxEnt, Random Forest (RF) and Boosted Regression Trees (BRT) identified the biophysical conditions characterizing the locations of foraging events, using time-matched oceanographic predictors (Sea Surface Temperature, SST; chlorophyll a, chl-a; thermal front frequency, TFreq; depth). Model performance was assessed through iterative cross-validation and extrapolative performance through cross-validation among years. Results: Predictable foraging habitats identified by EENM spanned neritic (<500 m), shelf break and oceanic waters, coinciding with a set of persistent biophysical conditions characterized by particular thermal ranges (3–8 °C, 12–13 °C), elevated primary productivity (chl-a > 0.5 mg m−3) and frequent manifestation of mesoscale thermal fronts. Our results confirm previous indications that GHA exploit enhanced foraging opportunities associated with frontal systems and objectively identify the APFZ as a region of high foraging habitat suitability. Moreover, at the spatial and temporal scales investigated here, the performance of multi-model ensembles was superior to that of single-algorithm models, and cross-validation among years indicated reasonable extrapolative performance. Main conclusions: EENM techniques are useful for integrating the predictions of several single-algorithm models, reducing potential bias and increasing confidence in predictions. Our analysis highlights the value of EENM for use with movement data in identifying at-sea habitats of wide-ranging marine predators, with clear implications for conservation and management.

Identifying predictable foraging habitats for a wide-ranging marine predator using ensemble ecological niche models

Aim: Ecological niche modelling can provide valuable insight into species' environmental preferences and aid the identification of key habitats for populations of conservation concern. Here, we integrate biologging, satellite remote-sensing and ensemble ecological niche models (EENMs) to identify predictable foraging habitats for a globally important population of the grey-headed albatross (GHA) Thalassarche chrysostoma. Location: Bird Island, South Georgia; Southern Atlantic Ocean. Methods: GPS and geolocation-immersion loggers were used to track at-sea movements and activity patterns of GHA over two breeding seasons (n = 55; brood-guard). Immersion frequency (landings per 10-min interval) was used to define foraging events. EENM combining Generalized Additive Models (GAM), MaxEnt, Random Forest (RF) and Boosted Regression Trees (BRT) identified the biophysical conditions characterizing the locations of foraging events, using time-matched oceanographic predictors (Sea Surface Temperature, SST; chlorophyll a, chl-a; thermal front frequency, TFreq; depth). Model performance was assessed through iterative cross-validation and extrapolative performance through cross-validation among years. Results: Predictable foraging habitats identified by EENM spanned neritic (<500 m), shelf break and oceanic waters, coinciding with a set of persistent biophysical conditions characterized by particular thermal ranges (3–8 °C, 12–13 °C), elevated primary productivity (chl-a > 0.5 mg m−3) and frequent manifestation of mesoscale thermal fronts. Our results confirm previous indications that GHA exploit enhanced foraging opportunities associated with frontal systems and objectively identify the APFZ as a region of high foraging habitat suitability. Moreover, at the spatial and temporal scales investigated here, the performance of multi-model ensembles was superior to that of single-algorithm models, and cross-validation among years indicated reasonable extrapolative performance. Main conclusions: EENM techniques are useful for integrating the predictions of several single-algorithm models, reducing potential bias and increasing confidence in predictions. Our analysis highlights the value of EENM for use with movement data in identifying at-sea habitats of wide-ranging marine predators, with clear implications for conservation and management.