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Review

A Review on Genus Halichondria (Demospongiae, Porifera)

by
Josephine Goldstein
1,2 and
Peter Funch
2,*
1
Marine Biological Research Centre, Department of Biology, University of Southern Denmark, 5230 Odense M, Denmark
2
Genetics, Ecology, and Evolution, Department of Biology, Aarhus University, 8000 Aarhus C, Denmark
*
Author to whom correspondence should be addressed.
J. Mar. Sci. Eng. 2022, 10(9), 1312; https://doi.org/10.3390/jmse10091312
Submission received: 14 August 2022 / Revised: 5 September 2022 / Accepted: 13 September 2022 / Published: 16 September 2022
(This article belongs to the Special Issue Filter-Feeding in Marine Invertebrates)
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Abstract

:
Demosponges of the genus Halichondria Fleming (1828) are common in coastal marine ecosystems worldwide and have been well-studied over the last decades. As ecologically important filter feeders, Halichondria species represent potentially suitable model organisms to link and fill in existing knowledge gaps in sponge biology, providing important novel insights into the physiology and evolution of the sponge holobiont. Here we review studies on the morphology, taxonomy, geographic distribution, associated fauna, life history, hydrodynamic characteristics, and coordinated behavior of Halichondria species.

1. Introduction

The genus Halichondria Fleming (1828) [1] (Demospongiae, Porifera; subgenera Halichondria and Eumastia) contains the most common marine sponge species of the North Atlantic [2], including the common “bread-crumb” sponge Halichondria (Halichondria) panicea Pallas (1766) [3] and Bowerbank’s horny sponge H. bowerbanki Burton (1930) [4]. The most studied species, H. panicea, occurs in habitats covering a broad range of salinities, temperatures, turbidities, and flow conditions [5,6] and has been recorded in marine intertidal and sublittoral zones down to depths of more than 500 m [2]. Halichondria panicea provides substrate for many other marine organisms, including a large and varied associated fauna [7,8,9], symbiotic algae [10,11], and numerous bacteria [12,13]. The life histories of Halichondria spp. are characterized by different modes of asexual and sexual reproduction [14], with the latter revealing strong species- and habitat-specific adaptations [15,16,17,18]. Halichondria sponges are filter feeders capable of processing large volumes of seawater (up to six times their own body volume per minute [19]) and efficiently retaining small food particles [20], thus playing a key role in nutrient recycling of coastal marine ecosystems [8]. Modular arrangement of their leuconoid aquiferous systems [21,22] has made it possible to study the hydrodynamic properties of the sponge filter-pump, which may help to shed light on the evolution of complex filter-feeding systems in sponges (cf. [23]). Despite their apparently simple bauplan without a nervous or muscular system, Halichondria spp. show coordinated responses to changing environmental conditions, including phototactic responses of larvae [24], sponge body shape changes [25], and contractile behavior [22,26,27,28]. The detailed mechanisms underlying coordinated behavior in sponges are still unclear [29], but existing data for Halichondria points out the importance of cellular communication based on a neuronal-like ‘toolkit’ and could serve as a milestone towards an improved understanding of tissue organization in the first animals.
The vast majority of studies on Halichondria (a total of 11,100 research articles according to Google scholar) are based on H. panicea (36.4% of total research articles) with a focus on the biological and ecological aspects, whereas much fewer studies within these research fields have addressed other species, such as H. bowerbanki (4.0%), H. melanadocia Laubenfels (1936) [30] (1.5%), H. moorei Bergquist (1961) [31] (1.0%), or H. semitubulosa Lamarck (1814) [32] (0.2%, Table 1).
Other studies have explored the metabolite chemistry of Halichondria, mainly for the species H. okadai Kadota (1922) [34] (26.8%, Table 1), for undefined species (Halichondria sp./spp., 12.5%), or on a genus-level (6.5%), reflecting partially unresolved and still ongoing taxonomic revisions of Halichondria species [35]. Molecular biology, including studies on the sponge microbiome, has mainly been investigated on H. okadai, H. japonica Kadota (1922) [34] (2.3%), H. cylindrata Tanita & Hoshino (1989) [36] (1.6%), and H. oshoro Tanita (1961) [37] (0.7%). Few morphological studies exist for H. melanadocia and H. glabrata Keller (1891) [38] (0.1%), while research on the hydrodynamics of sponges has remained restricted to H. panicea and H. coerulea Berquist (1967) [39] (0.1%). Despite the relevance of comparative studies on sponge cell biology, most Halichondria species have remained understudied (2.1%, Table 1). The aim here is to provide a compilation of studies concerning sponges in the genus Halichondria and point out existing knowledge gaps that may aid in future studies of these ecologically important demosponges.

2. Morphology, Taxonomy, and Distribution

The genus Halichondria is placed in the animal phylum Porifera, class Demospongiae, subclass Heteroscleromorpha, order Suberitida, and family Halichondriidae. Growth forms of Halichondria species include encrusting, massive, occasionally irregularly branching, or digitate sponges with smooth or papillate surfaces. An important morphological character to separate the two subgenera, Halichondria and Eumastia, is the absence or presence of short conical papillae on the sponge surface, respectively [2]. Members of the genus Halichondria typically form chimneys of variable size (up to 5 cm high) with conspicuous, relatively large oscula (2–4 mm in diameter). They are characterized by their firm but compressible texture and variable color, from olive-green (due to symbiotic algae) over orange-yellow to creamy-yellow [2] (cf. Appendix A, Figure A1). The siliceous spicule skeleton of Halichondria consists exclusively of oxeas or oxea derivates in a wide size range, which are arranged in an ectosomal crust (200–300 µm thick) and appear scattered or in tight bundles in the choanosome along with spongin fibers [2,40]. While the functional cell morphology and number of cell types in Halichondria has remained largely unknown, 18 distinct cell types which comprise four major cell families, including contractile, digestive, and amoeboid-neuroid cells, have recently been described in the freshwater demosponge Spongilla lacustris [41].
Species identification is traditionally based on morphological characteristics, such as the shape and structure of the skeleton and the size and form of spicules [42], but several of these characters show strong intra-specific variation and are, therefore, of rather poor quality to distinguish species. For instance, a variety of growth forms are represented by H. panicea, ranging from thin encrusting (Figure A1a) to erect ramose (Figure A1b), which seems to depend on the intensity of ambient water currents [43] (cf. [44]). Moreover, an extensive overlap of spicule sizes in different species has been documented [2]. Molecular data used in phylogenetic studies includes complete mitochondrial genomes of several Halichondria species [45,46,47] and mitochondrial and ribosomal markers [48,49]. The classification of genus Halichondria, as defined in [2], is still in need of a major revision at an ordinal level [35,50], as classification based on morphology disagrees with phylogenetic analyses using molecular data. Overall, morphological, biochemical, and molecular characters applied in recent phylogenetic analyses seem to point out that Halichondria is nonmonophyletic [51,52,53,54].
To date, about 100 Halichondria species are accepted [33,55,56]. They occur in different types of marine habitats around the world, being widespread in European [4,11,57,58], American [2], and Brazilian coastal waters of the Atlantic [59], but also in parts of the Baltic Sea [60], the White Sea [61], and the Mediterranean Sea [62]. Halichondria species also occur in the North Pacific, including Alaska [63,64], Japan [65], Korea [42,66], and the South China Sea [67]. The closely related species H. panicea, H. bowerbanki, and other species in this complex may serve as a suitable model to illuminate possible speciation events due to their overlapping distribution in the North Atlantic, where H. panicea is mainly found in shallow, protected coastal regions of the eastern parts, and shows adaptation to frequent air exposure, while H. bowerbanki is most common in exposed habitats of the western parts, where it tolerates high levels of siltation [11]. A molecular study based on a part of the mitochondrial marker COI suggests that North East Pacific H. cf. panicea is genetically distant from and forms a sister group to a species complex consisting of European H. panicea and H. bowerbanki [53]. Halichondria panicea has also been reported from the Tropical Southwestern Atlantic, along with other species such as H. magniconulosa Hechtel (1965) [68], H. cebimarensis, H. tenebrica, H. migottea, H. sulfurea Carvalho & Hajdu (2001) [59] and H. marianae Santos et al. (2018) [69]. Common species in the Pacific Ocean are H. japonica [65], H. okadai, H. oshoro [70], H. gageoenesis and H. muanensis Kang & Sim (2008) [42], while H. panicea and H. bowerbanki have been reported from Alaska [63,64] and Korea [66], respectively. Revisions of the classification system should include more molecular data and more species and be used to reevaluate the morphological characters used in the traditional classification [50] (cf. [53,54]).

3. The Holobiont Halichondria

Halichondria spp. occur on a variety of inorganic and organic hard substrates, including mussel banks, small stones and rocks, and macroalgae [8,9,43,71]. The sponges themselves provide habitat for a diverse associated fauna and various symbiotic microorganisms. The associated epi- and endofauna of H. panicea include various Arthropoda such as skeleton shrimps (Caprella spp.) and copepods, but also molluscs, e.g., the scallop Chlamys varia, annelids, platyhelminths, and demersal fish that prey almost exclusively upon sponge epifauna [7,8,9,10]. Symbiosis with the dinoflagellate Prorocentrum lima has been documented in H. okadai [72,73], and H. panicea seems to harbor (intracellular) green algae [10,11]. However, many Halichondria species have not been investigated, indicating numerous other yet undiscovered symbiotic interactions, e.g., with dinoflagellates, cryptophytes, microalgae, and diatoms [73]. While the growth of pathogenic bacteria on H. panicea can cause sponge mortality under stagnant flow conditions [74], sponges harbor diverse microbial assemblages that contribute positively to host metabolism and defense [12,75,76]. Halichondria spp. are characterized as low microbial abundance (LMA) sponges with high variability in their bacterial diversity across species and environments [12,13,76]. While only 7 operational taxonomic units (OTUs) of microorganisms have been identified in H. okadai from Korea [77], about 500 OTUs were detected in H. panicea and H. (Eumastia) sitiens Schmidt (1870) [78] from the White Sea [76], respectively, and 1779 OTUs seem to be unique to H. bowerbanki from the mid-Atlantic region of the eastern United States [13]. The microbiome of H. panicea is dominated by a core taxon of Alphaproteobacteria within the class Amylibacter which has recently been named ‘Candidatus Halichondribacter symbioticus’ [12,76,79,80,81,82]. Transmission of bacterial symbionts occurs in a mixed vertical (i.e., direct through reproduction) and horizontal mode (i.e., indirect through the environment) in H. bowerbanki; it is likely to vary across Halichondria species [13]. Metagenomics have revealed that distinct viromes with low similarity to known viral sequences are associated with H. panicea and H. sitiens, suggesting the existence of bacterial antiphage systems in sponges [76].
Halichondria sponges and their microbial symbionts produce a broad spectrum of mainly symbiont-derived bioactive metabolites [83] with cytotoxic or cell growth-inhibiting properties. Substances isolated from Halichondria sponges include halichondrin B and okadaic acid in H. okadai [72,84,85] or gymnostatins and dankastatins from an H. japonica-derived fungal strain [86] which may additionally serve Halichondria sponges as a defense mechanism against pathogens, predators, and biofouling [73,87]. Okadaic acid is a biotoxin known for its cyto-, neuro-, immune-, embryo-, and genotoxicity in marine animals [87,88,89] and has been suggested to protect the demosponge Suberites domuncula from bacterial and parasitic infections [87]. Epibiotic H. panicea can negatively affect the heart performance of blue mussels (Mytilus edulis), which may be due to the sponges’ release of excretory/secretory products. Such substances with cytotoxic properties and antimicrobial activity seem to benefit H. panicea in the competition for space and food across benthic fouling communities [90]. Neuroactive bacteria-derived compounds in H. panicea [73] suggest the relevance of symbiotic interactions for essential physiological processes such as coordinated behavior. The natural variability of sponge-microbe associations in Halichondria seems to provide a meaningful framework for modeling symbiotic interactions in metazoans (cf. [91]). In H. bowerbanki, for instance, changes in microbial communities after exposure to thermal stress have been documented [92], pointing out the relevance of future studies on sponges for assessing possible shifts in symbiont community composition and structure in response to global warming.

4. Life History

The life histories of Halichondria species typically include a reproductive period of 2–3 months in temperate regions [15,71,93]. Halichondria spp. are ovoviviparous and characterized by asynchronous gameto- and embryogenesis, while habitat-specific differences include successive hermaphroditism in White Sea populations of H. panicea and H. sitiens [18], simultaneous hermaphroditism in H. panicea and H. bowerbanki from the southwest coast of the Netherlands [16], incomplete gonochorism in Halichondria sp. from Mystic Estuary, US [15], or gonochorism in H. panicea from Kiel Bight, Germany [17]. In temperate regions, environmental parameters such as temperature and salinity drive the onset of sexual reproduction in H. panicea [17]. Differentiation of gametes from somatic cells has been observed in both H. panicea and H. semitubulosa, indicating the development of spermatocytes from choanocytes or archaeocytes, a process that may be species-dependent [62,94]. The larvae of Halichondria species are typically of parenchymella type and sometimes contain choanocyte chambers before settlement [24,95]. The release of Halichondria larvae seems to follow a light cue, being triggered by the onset of darkness in the temperate species H. panicea [96], while tropical H. melanadocia release larvae on exposure to light following a period of dark adaptation [24]. Phototactic responses of larvae range from positive to neutral to negative before settlement upon various hard substrates [24] (Figure A2a,b).
The growth of Halichondria sponges is dependent on temperature [70] and the concentration of available food, which mainly consists of bacteria and phytoplankton [97]. Pumping rates of H. panicea increase linearly with temperature and require relatively low energy demands for filtering large volumes of seawater [20,98], as expressed by F/R-ratios ≥15.6 L H2O (mL O2)−1, which are comparable to other filter-feeding marine invertebrates [19]. In contrast, the energetic cost of growth is high in sponges [20,99], with exponential growth at a maximum rate of 4% d−1 in H. panicea under natural conditions [100]. The weight-specific growth of H. panicea is constant over sponge size, which has been pointed out as a unique feature among most other filter-feeding invertebrates, reflecting the modular organization of sponges [100]. A study of H. panicea from the Western Baltic Sea suggested that stored glycogen reserves fueled sexual reproduction and that the sponges degenerated in the end of the following year after reproduction [71]. Tissue regression and high mortality during the colder months of the year have also been reported for temperate Halichondria sp. from the Mystic and Thames estuaries, US [57,101] and for Halichondria bowerbanki from New England, US [102], respectively, while the longevity of H. okadai in Japanese waters may exceed 3 years when considering asexual reproduction, i.e., fission and fusion of sponge fragments [14]. Halichondria panicea is capable of rapid regeneration of damaged parts, as expressed in ≥3-fold increased growth rates in response to predation [103] or during the reorganization of the aquiferous system in explant cuttings within approximately 6–10 days [22] (Figs. A2c-f), while other species, such as H. magniconulosa, seem to regenerate at slower rates [104]. Several Halichondria species, including H. lutea Alcolado (1984) [105], H. magniconulosa, and H. melanadocia have been recognized as important members of the Caribbean mangrove and coral reef communities, where they are preyed upon by fish [106,107]. H. panicea can also serve as a food source for hermit crabs, shrimp, large isopods (e.g., Idothea sp.), or the nudibranch Archidoris montereyensis, which may appear in such high density that it can eliminate large and long-lived sponge populations [63,64]. Halichondria sponges play an important role in nutrient recycling of coastal marine ecosystems due to their unique ability to retain small particles (≤0.1 µm) [20,108]. Regular tissue sloughing has been observed in H. panicea in response to sedimentation of organic material and settlement of small organisms on the sponge surface [109], along with seasonal remineralization of released H. panicea biomass following reproduction [8]. As the water pumping activity of H. panicea leads to an accumulation of pollutants, such as heavy metals, in direct proportion to ambient concentrations, their potential use as biomonitoring organisms has been proposed [40,110].

5. Hydrodynamics

As for other demosponges, the aquiferous system of Halichondria is leuconoid [21,40,111] and characterized by choanocytes organized in small spherical chambers which create a unidirectional flow of ambient water through a complex canal system [112,113]. The aquiferous elements of Halichondria act like a sieve for particles of variable size due to their aperture diameters (Figure A3a). As documented for H. panicea, they include numerous inhalant openings (ostia; 7–32 µm) through which seawater is drawn into incurrent canals (50–200 µm), finer incurrent canal branches (prosodi; 5 µm), and the prosopyles (1–4 µm) of choanocyte chambers (18–35 µm; Figure A3b) [113]. Here, choanocytes retain small food particles ≤0.1 µm [20] on their microvilli collars (Figure A4a). Each choanocyte chamber of H. panicea contains about 40–120 choanocytes at an estimated choanocyte chamber density of 18,000 mm−3 [113]. Water leaves choanocyte chambers through an apopyle (7–17 µm; Figure A4b) via excurrent canals (140–450 µm), which drain into an atrium (2.1 mm) from where the water exits the sponge in an excurrent jet through the osculum (1.2 mm) [113] (but see also [21]).
Each osculum represents a functional unit of aquiferous elements in a certain sponge volume (cf. Figure A2b–d), thus characterizing Halichondria sponges with multiple oscula as an array of several autonomous aquiferous modules [22,114,115]. The pumping rate of each aquiferous module is directly proportional to the density of choanocyte chambers in H. panicea [22], implying constant choanocyte densities for different Halichondria species. However, module size seems to determine the volume-specific pumping rates of H. panicea, which can reach a maximum of 15 mL min−1 (cm3 sponge)−1 in growing modules, as observed in single-osculum explants [26,27] (Figure A2c,d), while the modules in multi-oscula explants seem to pump at a lower maximum rate of 3 mL min−1 (cm3 sponge)−1 [22], probably due to a decrease in choanocyte chamber density with increasing module volume [116]. Based on the volume-specific pumping rate and choanocyte chamber density of H. panicea, the pumping rate per choanocyte chamber in a multi-oscula sponge can be estimated to (3/18,000)/60 = 2.78 × 10−6 mm3 s−1 = 2778 µm−3 s−1, and thus the pumping rate per choanocyte at an average of 80 choanocytes per chamber [113], to (2778/80 = 35 µm3 s−1). This value is in range with a previous estimate of (4.46 × 10−6 mm3 s−1/95 = 47 µm3 s−1) for the demosponge Haliclona permollis [113,117] (their Table 1, respectively). A recent hydrodynamic model on the pump characteristics of leuconoid sponges assumed the presence of flagellar vanes along with a glycocalyx mesh which distally connects the microvilli collars of choanocytes, as has been shown for the freshwater sponge Spongilla lacustris [118,119], in order to deliver observed pump pressures [23]. These ultra-structural features of choanocytes have so far not been documented in Halichondria (cf. Figure A4a), pointing out the need for further studies on ultrastructure and hydrodynamic properties, which may provide valuable insight into the evolution of demosponge filter-pump systems (cf. [120]).

6. Coordinated Behavior

At least three different basic cell types are found in Halichondria species, including choanocytes, pinacocytes, and amoeboid (mesohyl) cells [24,121]. The coordinated behavior of sponge cells mediates the hydrodynamic and physical properties of the aquiferous system required for efficient filter feeding under different environmental conditions. Communication between motile cells is the basic principle underlying continuous tissue reorganization, regeneration, and microscale movements in sponges [122,123,124,125]—a topic which has, unfortunately, so far only been addressed by a few studies on Halichondria spp. Continuous tissue remodeling in H. panicea, as expressed by fusion, shape changes, and movement of sponges, has been observed in aquaria and intertidal rocky pools [25]. Halichondria japonica explants have been shown to fuse with explants of the same sponge, while they reject cells from other H. japonica sponges or from H. okadai [126]. Several types of mesohyl cells seem to be involved in this process of “self and nonself” recognition in H. japonica, including amoeboid archaeocytes, motile (granule-rich) gray cells, and collencytes [126]. Recent work on H. panicea points out the importance of cellular transport for the removal of inedible particles from the aquiferous system [27]. At the same time, sponge sandwich cultures may provide a suitable method (Figure A2e,f) for studying the cell types and mechanisms mediating capture, transport, and digestion/removal of edible and inedible particles (Figure A5).
Coordinated behavior further includes contraction of various parts of the aquiferous system, including the osculum [26], in- and excurrent canals, ostia and apopylar openings of the choanocyte chambers, resulting in reduction and temporal shut down of the water flow through single-osculum explants of H. panicea [27,28]. Contractile behavior is common among sponges and seems to follow species-specific cycles of distinct frequency and intensity [127,128,129,130,131] which can be expressed in asynchronous patterns across conspecifics in H. panicea [28,132]. Contractions can occur spontaneously in H. panicea explants under undisturbed conditions in the laboratory and can be induced by chemical messengers (γ-aminobutyric acid and L-glutamate) or by mechanical stimulation with inedible particles [28]. Coordinated contractions of different aquiferous modules in H. panicea explants with multiple oscula have been observed in response to external stimuli [22]. Peristaltic-like waves of contraction travel through the sponge, resulting in osculum closure at speeds of up to 233 nm s−1 in H. panicea (15 °C) [28]. Comparatively, observed contraction speeds of up to 12 µm s−1 in the marine demosponge Tethya wilhema (26 °C) [129] and 122 µm s−1 in the freshwater demosponge Ephydatia muelleri (21 °C) [131] seem considerably higher, emphasizing the need for future studies on the contraction kinetics of Halichondria species. During contractions, H. panicea shows reduced pumping activity [19,26,27], an associated decrease in respiration rates [132], and local internal oxygen depletion [133]. These physiological changes have been suggested as adaptations to variable environmental conditions, including food limitation [134], resuspension of sediment during storm events [135] (cf. [136]), seasonal changes in water temperature, changes in illumination period, spawning events of other sponge species [128], and facilitation of suitable habitat for specific symbiotic microorganisms [132,133]. Contractions may serve Halichondria sponges as an important mechanism to protect the sponge filter-pump in distinct aquiferous modules from clogging and damage and seem to be mediated by exo- and endopinacocytes [22,27,28,134,137], while the underlying cellular pathways have remained unclear. Previous studies have described contractile epithelial cells in sponges that function based on a ‘toolkit’ of neuronal-like elements, including sensory cilia, conduction pathways, and signaling molecules [41,134,138,139,140]. The pinacocytes of other demosponges exhibit actomyosin-based contractility [41,130,137,139,141,142], and myosin type II has been isolated from cells of H. okadai [143].
It is likely that communication between sponge cells in Halichondria is based on the extracellular spreading of chemical messengers [41,123,144], neuronal-like receptors [145], and cell contacts via cellular processes/membrane junctions [146,147,148]. As the abovementioned examples emphasize, cellular communication pathways require further attention in future studies. More detailed information on the functional cell morphology of Halichondria, as can now be accessed using whole-body single-cell RNA sequencing (cf. [41]), is needed to shed light on the principles underlying coordinated behavior in sponges. We encourage future work on the LMA demosponge H. panicea as a model organism to revisit functional coordination pathways with an integral perspective on the underlying morphological structures combining molecular, cytological, and physiological techniques.

7. Conclusions

Halichondria sponges are well-studied and the literature represents a strong base for our present understanding of the ecology and physiology of demosponges. Previous work has mainly focused on H. panicea, paving the foundations for modeling sponge-microbe interactions, hydrodynamics of the sponge filter pump, and cell communication in demosponges. We encourage future research to fill in present knowledge gaps regarding the functional cell morphology and filter-pump characteristics of H. panicea, along with comparative studies including other Halichondria species, to improve and verify existing models based on this ubiquitous demosponge genus.

Author Contributions

Conceptualization, J.G. and P.F.; writing—original draft preparation, J.G.; writing—review & editing, P.F.; visualization, J.G.; project administration, P.F.; funding acquisition, P.F. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Independent Research Fund, grant number 8021-00392B.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We are grateful to three anonymous reviewers for providing valuable feedback on the manuscript. We further thank Héloïse Hamel and Janni Magelund Degn Larsen for supplementary photographs. Stereo-, light and scanning electron microscopy (SEM) images were acquired at the Marine Biological Research Centre, Kerteminde, University of Southern Denmark, and at the Interdisciplinary Nanoscience Center (iNANO), Aarhus University, Denmark.

Conflicts of Interest

The authors declare no conflict of interest.

Appendix A

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Figure A1. Growth forms of Halichondria panicea Pallas (1766) in the inlet to Kerteminde Fjord, Denmark (55°26′59″ N, 10°39′41″ E). (a) Growing on a piece of rope, collected in November 2020 and (b) with finger-shaped chimneys, found on wood in November 2020. Pictures: Héloïse Hamel.
Figure A1. Growth forms of Halichondria panicea Pallas (1766) in the inlet to Kerteminde Fjord, Denmark (55°26′59″ N, 10°39′41″ E). (a) Growing on a piece of rope, collected in November 2020 and (b) with finger-shaped chimneys, found on wood in November 2020. Pictures: Héloïse Hamel.
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Figure A2. Aquiferous module formation in Halichondria panicea. (a) Sponge cells after larval settlement, (b) development of choanocyte chambers (cc), excurrent canals (ex-c) and an osculum (osc) in a juvenile sponge, (c) single-osculum explant (side-view), (d) explant (top-view) with visible incurrent (in-c) and excurrent canals (ex-c), (e) sandwich culture with choanocyte chambers (cc), spicules (sp), and endopinacoderm (enp) lining aquiferous canals, (f) sandwich culture after addition of edible particles (tp) for tracing water flow in the incurrent canal (in-c) which is separated from the flow in the excurrent canal (ex-c) by endopinacocytes (enp) and mesohyl (m).
Figure A2. Aquiferous module formation in Halichondria panicea. (a) Sponge cells after larval settlement, (b) development of choanocyte chambers (cc), excurrent canals (ex-c) and an osculum (osc) in a juvenile sponge, (c) single-osculum explant (side-view), (d) explant (top-view) with visible incurrent (in-c) and excurrent canals (ex-c), (e) sandwich culture with choanocyte chambers (cc), spicules (sp), and endopinacoderm (enp) lining aquiferous canals, (f) sandwich culture after addition of edible particles (tp) for tracing water flow in the incurrent canal (in-c) which is separated from the flow in the excurrent canal (ex-c) by endopinacocytes (enp) and mesohyl (m).
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Figure A3. Schematic illustration of the aquiferous system in a functional module of Halichondria panicea. (a) Left: external surface with ostia (open circles), right: canal system with choanocyte chambers (black circles) and flow direction towards osculum indicated by arrows (b) water flow (arrows) through choanocyte chambers (cf. [111,117], their Figures 9d and 2b, respectively). Abbreviations: exp = exopinacoderm, os = ostium, in-c = incurrent canal, enp = endopinacoderm, pro = prosopyle, cc = choanocyte chamber, ap = apopyle, m = mesohyl, sp = spicule, ex-c = excurrent canal, at = atrium, osc = osculum.
Figure A3. Schematic illustration of the aquiferous system in a functional module of Halichondria panicea. (a) Left: external surface with ostia (open circles), right: canal system with choanocyte chambers (black circles) and flow direction towards osculum indicated by arrows (b) water flow (arrows) through choanocyte chambers (cf. [111,117], their Figures 9d and 2b, respectively). Abbreviations: exp = exopinacoderm, os = ostium, in-c = incurrent canal, enp = endopinacoderm, pro = prosopyle, cc = choanocyte chamber, ap = apopyle, m = mesohyl, sp = spicule, ex-c = excurrent canal, at = atrium, osc = osculum.
Jmse 10 01312 g0a3
Jmse 10 01312 g0a4 550
Figure A4. Halichondria panicea. SEM of cryo-fractured explants. (a) Choanocyte chamber with choanocytes (c) and their microvilli collars (mv) surrounding the flagellum (fl), (b) the fracture shows components of the aquiferous system with prosopyles (pro) and apopyles (ap) connected to incurrent (in-c) and excurrent canals (ex-c), respectively, embedded in mesohyl (m) with choanocyte chambers (cc) and spicules (sp).
Figure A4. Halichondria panicea. SEM of cryo-fractured explants. (a) Choanocyte chamber with choanocytes (c) and their microvilli collars (mv) surrounding the flagellum (fl), (b) the fracture shows components of the aquiferous system with prosopyles (pro) and apopyles (ap) connected to incurrent (in-c) and excurrent canals (ex-c), respectively, embedded in mesohyl (m) with choanocyte chambers (cc) and spicules (sp).
Jmse 10 01312 g0a4
Jmse 10 01312 g0a5 550
Figure A5. Exposure of Halichondria panicea to different particle types. Single-osculum explant (top-view) after (a) feeding on Rhodomonas salina (Cryptophyceae); note the red color originating from added algae, (b) exposure to inedible ink (Pelikan Scribtol, 2 × 104-fold diluted) for 1 h; note black color, and (c) recovery in particle-free seawater for 24 h. Pictures: Janni Magelund Degn Larsen.
Figure A5. Exposure of Halichondria panicea to different particle types. Single-osculum explant (top-view) after (a) feeding on Rhodomonas salina (Cryptophyceae); note the red color originating from added algae, (b) exposure to inedible ink (Pelikan Scribtol, 2 × 104-fold diluted) for 1 h; note black color, and (c) recovery in particle-free seawater for 24 h. Pictures: Janni Magelund Degn Larsen.
Jmse 10 01312 g0a5

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Table
Table 1. Number of research articles on Halichondria Fleming (1828) based on genus- and species-level (cf. [33]) according to Google Scholar (Web of Science) along with the main Web of Science research categories (accessed on 6 July 2022).
Table 1. Number of research articles on Halichondria Fleming (1828) based on genus- and species-level (cf. [33]) according to Google Scholar (Web of Science) along with the main Web of Science research categories (accessed on 6 July 2022).
SpeciesNo. Articles(%)Web of Science Categories (%)
Halichondria panicea4040 (229)36.4Marine Freshwater Biology (43.5), Ecology (19.2), Oceanography (16.2)
Halichondria okadai2980 (96)26.8Organic Chemistry (39.6), Pharmacology Pharmacy (16.7), Biochemistry Molecular Biology (14.5)
Halichondria sp./spp.1390 (73)12.5Organic Chemistry (34.3), Medicinal Chemistry (20.6), Pharmacology Pharmacy (20.6)
Genus Halichondria723 (14)6.5Organic Chemistry (21.4), Pharmacology Pharmacy (21.4), Biochemistry Molecular Biology (14.3)
Halichondria bowerbanki447 (10)4.0Ecology (50.0), Marine Freshwater Biology (40.0), Zoology (30.0)
Halichondria japonica260 (20)2.3Biochemistry Molecular Biology (30.0), Organic Chemistry (20.0), Fisheries (15.0)
Halichondria cylindrata173 (10)1.6Organic Chemistry (70.0), Medicinal Chemistry (30.0), Biochemistry Molecular Biology (10.0)
Halichondria melanadocia169 (17)1.5Marine Freshwater Biology (52.9), Ecology (29.4), Anatomy Morphology (50.0)
Halichondria moorei108 (2)1.0Marine and Freshwater Biology (50.0), Multidisciplinary Sciences (50.0)
Halichondria sitiens89 (5)0.8Biodiversity Conservation (20.0), Biology (20.0), Ecology (20.0)
Halichondria oshoro82 (2)0.7Microbiology (100.0)
Halichondria magniconulosa67 (2)0.6Applied Chemistry (50.0), Medicinal Chemistry (50.0), Ecology (50.0)
Halichondria semitubulosa25 (1)0.2Zoology (100.0)
Halichondria cartilaginea19 (0)0.2-
Halichondria genitrix19 (0)0.2-
Halichondria albescens18 (0)0.2-
Halichondria lutea18 (3)0.2Biochemistry Molecular Biology (66.7), Ecology (66.7), Evolutionary Biology (66.7)
Halichondria coerulea14 (1)0.1Ecology (100.0), Marine Freshwater Biology (100.0), Oceanography (100.0)
Halichondria glabrata14 (2)0.1Anatomy and Morphology (50.0), Biology (50.0), Food Science Technology (50.0)
Halichondria diazae13 (0)0.1-
Halichondria cebimarensis12 (1)0.1Ecology (100.0), Marine Freshwater Biology (100.0)
Halichondria phakellioides12 (1)0.1Fisheries (100.0), Limnology (100.0), Marine Freshwater Biology (100.0)
Halichondria attenuata11 (2)0.1Marine Freshwater Biology (50.0), Zoology (50.0)
Halichondria contorta10 (1)0.1Zoology (100.0)
Halichondria topsenti10 (0)0.1-
Halichondria oblonga9 (0)0.1-
Halichondria aspera8 (0)0.1-
Halichondria cristata7 (0)0.1-
Halichondria agglomerans5 (0)0.0-
Halichondria flava5 (0)0.0-
Halichondria kelleri5 (0)0.0-
Halichondria migottea5 (0)0.0-
Halichondria osculum5 (1)0.0Medicinal Chemistry (100.0), Pharmacology Pharmacy (100.0)
Halichondria colossea4 (0)0.0-
Halichondria marianae4 (2)0.0Marine Freshwater Biology (50.0), Zoology (50.0)
Halichondria prostrata4 (0)0.0-
Halichondria tenebrica4 (0)0.0-
Halichondria capensis3 (0)0.0-
Halichondria convolvens3 (0)0.0-
Halichondria elenae3 (1)0.0Ecology (100.0), Marine Freshwater Biology (100.0)
Other species316 (36)2.1Cell biology (100.0), Zoology (100.0)
Total11,100 (532)100.0Marine and Freshwater Biology (27.3), Organic Chemistry (17.5), Ecology (12.8)
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Goldstein, J.; Funch, P. A Review on Genus Halichondria (Demospongiae, Porifera). J. Mar. Sci. Eng. 2022, 10, 1312. https://doi.org/10.3390/jmse10091312

AMA Style

Goldstein J, Funch P. A Review on Genus Halichondria (Demospongiae, Porifera). Journal of Marine Science and Engineering. 2022; 10(9):1312. https://doi.org/10.3390/jmse10091312

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Goldstein, Josephine, and Peter Funch. 2022. "A Review on Genus Halichondria (Demospongiae, Porifera)" Journal of Marine Science and Engineering 10, no. 9: 1312. https://doi.org/10.3390/jmse10091312

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