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The biology and life cycle of the Rhizocephala (Cirripedia)
Abstract
This review describes aspects of the life cycle and ecology of the Rhizocephala emphasizing (i) comparison with more conventional Cirripedia, and (ii) evolutionary and phylogenetic perspectives. Despite numerous extreme specializations to living as parasites in other Crustacea, most features of the rhizocephalan life cycle resemble those seen in other Cirripedia, and only the process of host invasion and the ensuing redifferentiation of the adult parasite represent truly unique features. Larval biology of the Rhizocephala has developed under selection pressures induced by the difficulty of locating the substratum for settlement, host defences against parasite invasion, and the special demands imposed on the sexual system of a parasite. Thus rhizocephalans have (i) lecithotrophy coupled with very small-sized larvae, (ii) special sensory organs in the cyprid, (iii) a very rapid host invasion accomplished by minute, female stages, and (iv) dwarf males nourished by the adult female parasite, such that it emulates a true hermaphrodite. This review also surveys the nature and underlying causes of the numerous effects that rhizocephalan parasites can induce on their hosts in terms of morphology, physiology, and behaviour. The ‘host control’ induced by rhizocephalans ensures that both male and female hosts accept the parasite as their own brood and care for it accordingly. This, and other details of host-parasite co-evolutions are discussed. © 1995, Marine Biological Association of the United Kingdom. All rights reserved.
... Thus, the adult rhizocephalan female body is formed de novo from this instar and does not inherit any organs from the larva (Høeg and Lützen 1995;Glenner 2001). The body of an adult female consists of two parts: an interna, a system of ramifying rootlets located in the host hemocoel, and an externa, a sac-like structure located outside the host (Høeg 1995;Noever et al. 2016). Interna and externa are connected via the stalk, piercing the host's cuticle (Høeg 1995;Noever et al. 2016). ...
... The body of an adult female consists of two parts: an interna, a system of ramifying rootlets located in the host hemocoel, and an externa, a sac-like structure located outside the host (Høeg 1995;Noever et al. 2016). Interna and externa are connected via the stalk, piercing the host's cuticle (Høeg 1995;Noever et al. 2016). ...
... So far, this is the only described case of age-related differentiation of musculature in Rhizocephala. Perhaps, the presence of circular musculature in the externa is necessary mainly for ventilation of the mantle cavity and pushing the larvae to the mantle opening and taking them out of the externa (Høeg 1995). At the same time, it appears to be less important for those externae that either have not started reproduction or have come to the end of their life cycle. ...
Circulatory systems are characteristic of most multicellular animals. In parasitic organisms, which may differ strikingly from their free-living relatives, such systems remain the least studied. Rhizocephala (Pancrustacea: Cirripedia) are among the morphologically most derived parasitic crustaceans. In the adult rhizocephalan female, transport presumably takes place along the lacunar system inside the interna rootlets and the externa. The aim of our study was to visualize and describe the lacunar and muscular systems in the externa of Polyascus polygeneus and Parasacculina pilosella (fam. Polyascidae) using micro-computed tomography and confocal microscopy. The lacunar system in the externae of both species consists of the stalk lumen, mesentery lacuna accompanying the visceral mass and mantle lacunae. These elements of the lacunar system are similar to those previously described in Peltogasterella gracilis (fam. Peltogasterellidae). However, the interposition of these elements differs. The organization of the muscular system mostly corresponds to previous descriptions in other rhizocephalan species, however some unexpected results were obtained. For example, P. polygeneus has an age-related differentiation of mantle musculature, which was not described before for any rhizocephalan species. Obtained data on lacunar and muscular systems organization allow us to assume the change in the externa body axes in the family Polyascidae.
... Adults of the rhizocephalans are dramatically transformed due to their endoparasitic lifestyle and do not resemble their free-living relatives [1]. The body of a reproducing female consists of two functional parts: an interna, a system of trophic rootlets infiltrating the host's body, and an externa, a temporary reproductive organ [2,3]. Males are extremely reduced and incorporated into the externa [2,3]. ...
... The body of a reproducing female consists of two functional parts: an interna, a system of trophic rootlets infiltrating the host's body, and an externa, a temporary reproductive organ [2,3]. Males are extremely reduced and incorporated into the externa [2,3]. ...
... The phylogenetic position of the family Mycetomorphidae is still uncertain. Previously, rhizocephalans were split into two suborders, Kentrogonida and Akentrogonida, based on the life cycle and morphological features [2,20,21]. Mycetomorphidae was placed among other akentrogonids in the first phylogenetic analysis conducted on cumulative characteristics such as morphology of externa and cyprid larvae and presence/absence of male cyprid instar [22]. However, the mycetomorphid cyprid larvae are similar to the kentrogonids [18]. ...
Mycetomorpha vancouverensis is an enigmatic parasitic barnacle from the family Mycetomorphidae, known for its unclear phylogenetic position within Rhizocephala. Specimens of M. vancouverensis were collected from infected Neocrangon communis shrimps near the South Kuril Islands. Detailed morphological studies were conducted using histological techniques and scanning electron microscopy, and 18S rDNA sequences were used to resolve the phylogenetic position of M. vancouverensis within Rhizocephala. Morphological analysis revealed a complex externa structure with spermatogenic bodies and the presence of a main trunk in the interna. Some of the side branches of the interna invade the host’s nerve tissue and are modified into specialized goblet-shaped organs. These invasive rootlets are morphologically similar to the goblet-shaped organs in the family Peltogastridae. Molecular analysis confirmed that the Mycetomorphidae is a sister group to the Peltogastridae. At the same time, peltogastrids were recovered as polyphyletic. Our findings contribute to the understanding of the evolution of parasitic barnacles and highlight the unique adaptations of Mycetomorphidae within the broader context of Rhizocephala.
... The wide abdomen of a host fe male crab provides better protection to parasitic ex ternae as compared to the narrow abdomen of males (Høeg 1995) and, therefore, many rhizocephalans prefer female hosts (Yamaguchi et al. 1999, Alvarez et al. 2001, Mouritsen et al. 2018, Yang et al. 2018, Al-Wazzan et al. 2021). However, some rhizocephalans parasitize males more frequently than females (Galil & Lützen 1995, Alvarez et al. 1999, Barón et al. 2021). ...
... It is believed that crabs parasitized by sacculinid rhizocephalans do not molt after externa emergence and their growth decreases. At the same time, parasitization by nonsacculinid rhizocephalans does not affect the molt of the hosts (Høeg 1995). We observed such a molt of externa-bearing H. dentata individuals in the laboratory. ...
... Externa-bearing H. den tata also appeared to continue growing and, there fore, the sizes of non-parasitized and parasitized crabs did not significantly differ. Rhizocephalan parasitism causes modifications of the secondary sex characteristics in the host (Høeg 1995). Male hosts parasitized by rhizocephalans become morphologically and behaviorally feminized. ...
We studied the population and reproductive characteristics of the stone crab Hapalogaster dentata (De Haan, 1849) (Anomura: Lithodidae) parasitized by Briarosaccus hoegi (Rhizocephala: Peltogastridae) from Peter the Great Bay (northwestern Sea of Japan) in 2023. The sex structure of the H. dentata population was female-biased and represented by 39.1% males and 60.9% females. The size-frequency distribution differed between males and females. The prevalence of parasitization of H. dentata by B. hoegi reached 6.7%. No relationship between crab sex and parasitization prevalence was found. Most of the parasitized specimens (94.8%) had only a single parasitic externa. The non-parasitized and parasitized crabs did not differ in main carapace length. The pleopods in most of the externa-bearing females were shortened or completely atrophied. H. dentata produced 1 clutch per year with ovigerous females occurring from October to May. An obvious delay in embryonic development was observed in winter. None of the parasitized H. dentata females were ovigerous. Externae with embryos of B. hoegi were found from May to July.
... It is known that decapods infected by rhizocephalan crustaceans undergo parasitic castration and do not participate in reproduction [2,20]. In Peter the Great Bay, the prevalence of infection in P. middendorffii was estimated at 4.62% in the 1990s [1] and 20.83% in 2014-2015 [7]. ...
Some aspects of the reproductive biology of the widespread boreal hermit crab Pagurus middendorffii Brandt, 1851 were studied. Samples were collected monthly from November 2022 to November 2023 at a depth of 1–3 m in Zhitkov Bay (Russky Island, Peter the Great Bay, Sea of Japan). About 38% of the specimens were infected with parasitic crustaceans. Among healthy hermit crabs, the size of the calcified part of the carapace (SL) ranged from 1.9 to 6.6 mm (average 4.53±0.95) for males, from 1.9 to 5.5 mm (average 3.67±0.68) for females, and from 1.9 to 5.3 mm (average 3.56±0.62 mm) for ovigerous females. The male to female ratio during the study period varied from 0.6 to 4.0 with an average of 2.2. Spawning commenced in late October and ceased in late November, the incubation period lasted 6.5 months, and the embryonic diapause was absent. Repeated spawning was not observed. A comparative analysis of the reproductive characteristics of hermit crabs from different areas showed that changes in the temperature regime influence the timing of spawning and the duration of the incubation period, which significantly increases due to the slow embryo development at low temperatures in some species and due to the embryonic diapause in others.
Background
The endoparasitic rhizocephalan Parasacculina sinensis has a radically simplified morphology and primarily infests decapods crustaceans. Rhizocephalan barnacles usually absorb nutrients from the host through a complex rootlet system (the interna), and also change the morphology, physiology and behavior of their hosts. However, little is known about the transcriptomic landscape, ultrastructural details and gene expression of the interna rootlets in the group. In this study, we investigated the structural and molecular signatures of the interna of P. sinensis by using detailed histological staining and transcriptomic analyses.
Results
The interconnected F-actin nodal network, lipid droplets, and nucleus of interna rootlets were visualized using fluorescence straining. We successfully obtained a clean transcriptome of P. sinensis and conducted functional analyses of interna embedded within host hepatopancreas, claw muscle, and eyestalk. The gene ontology (GO) terms related to translation, metabolic process, biosynthetic process, cellular process were highly expressed in the top 10% transcripts from the interna. The GO category of shared differential expression of genes (DEGs) among internae was related to embryonic development. The Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway neuroactive ligand-receptor interaction and the GO term neurotransmitter transporter activity were identified in the shared DEGs among internae. The interna entangled within host hepatopancreas, eyestalk and claw muscle fibers had similarities and differences in the functional biology. Additionally, the interna specific candidate genes probably involved in host immune, lipid metabolism, molting and growth were identified.
Conclusions
Our study demonstrates an in-depth function of interna rootlets of P. sinensis and reveals potential mechanisms of parasite host control. This study provides novel information to further investigate the evolutionary drivers of parasitism in barnacles.
Sex allocation theory predicts the adaptive allocation of resources to male versus female reproduction in simultaneous hermaphrodites in response to individual characteristics or environmental factors. Because parasites uptake resources from their hosts, their presence could affect the sex allocation of the hosts. We investigated the effects of infestation status and infestation intensity by the rhizocephalan barnacle Boschmaella japonica on reproduction, including sex allocation, of the host intertidal barnacle Chthamalus challengeri. Feeding activity was also examined as a factor related to resource intake. Both male and female reproductive investment decreased with increasing parasite infestation, and the sex allocation of large infested hosts was more male-biased than that of large uninfested hosts. Moreover, in contrast to the model prediction that male investment does not change under resource limitation, male investment decreased in infested hosts whose resources were taken by parasites. This reduction in male investment could be explained by changes in mating group size, since infested hosts have shorter penises and consequently are able to access fewer mating partners.
Carcinus aestuarii is representative of lagoons and is currently defined as a cosmopolitan species across different geographical regions. The objective of this study was to ascertain the species composition, prevalence, density, sex, and seasonal distribution of epibionts hosted by C. aestuarii in the Çanakkale Strait. Samples of C. aestuarii were collected seasonally in Çardak Lagoon (Çanakkale Strait) summer, autumn, winter, and spring using a static traditional eel trap. It was observed that the crabs were extensively colonized with bivalves, barnacles, polychaetes, and amphipods, and carried epibionts in the carapace and abdominal region. Additionally, it was observed that males exhibited a greater prevalence of epibionts than females, and that the epibiont load on the crab increased during the winter season. This study reports the first recorded instance of Anomia sp. and Sacculina carcini on C. aestuarii. The study on the invasion of the green crab is of significant importance to gain insight into the behavior, dispersal patterns, and impacts of the species. The knowledge presented here may then be utilized in the development of strategies for the management and control of invasive species, thereby contributing to the conservation of ecosystems and the maintenance of biodiversity.
More than 130 specimens representing various growth stages of Rehbachiella kinnekullensis Müller, 1983, have permitted a detailed description of its ontogeny. It begins with a nauplius already able to swim and feed actively. The 30th stage is about 1.7 mm long, but still immature. Because the type specimens belong to earlier instars, the original diagnosis of Muller (1983) is emended. Details of the limb apparatus of late instars suggest that the animals were able to filter-feed by this stage, possibly while swimming close to the bottom. Two larval series are distinguished by size and morphology in their early stages, but their structural differences become almost balanced subsequently. This is interpreted as intraspecific differentiation rather than as existence of two species. The entire postnaupliar feeding apparatus of Branchiopoda, which is basically adapted to filtration, is recongnized here as an apomorphic character of this group. Branchiopoda comprise the two monophyletic units Anostraca and Phyllopoda (Calmanostraca, with Notostraca and Kazacharthra, and Onychura). Rehbachiella shares all major aspects of the branchiopod apparatus, which led to identify it as an ancestral marine branchiopod. Moreover, there are indications that Rehbachiella is a representative of the anostracan lineage, i.e. a representative of the stem-group of Sarsostraca, which include the Devonian Lipostraca and the extant Euanostraca. The long larval sequence of Rehbachiella and selective external features, including the locomotory and feediang apparatus, are evaluated for their bearing upon the phylogeny of Branchiopoda and Curstacea in general. This study on Rehbachiella supports the monophyly of the crown-group Crustacea (sensu Walossek & Muller 1990). It also has revealed that only the first maxilla was morphologically and functionally included into the crustacean head, while subsequent limbs were addted to the head in a stepwise manner and became modified separately within the different crustacean lineages, which is of great relevance when evaluating the relationships between these.
Peltogaster curvatus is reported from Norwegian waters for the first time. The percentage of infection was 5.5 on Pagurus cuanensis and 0.9 on Pagurus prideauxi. A brief account is given of the size of the parasites and the hosts, and of the distribution of P. cu.rva.tus. A new synonym of Pagurus prideauxi is noted: Cancer bemhardus Strom 1788 (non Cancer bemhardus L.).