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Hydroides dirampha (Mörch, 1863)
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Amelia Andree Desbiens 2018
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Summary | |
 Serpulidae, of phylum Annelida, are a major component of hard-bottomed benthic communities (Bastida-Zavala, 2008) and comprise some of the most renown biofouling organisms globally. Encrusting calcareous tubes demarcate the permanent habitat of these sessile marine polychaetes and can be found by the thousands across natural and artificial substrates (Bastida-Zavala, 2008) (Gollasch, 2002). Globalization of these biofoulers has been heavily enabled through accidental transportation of larvae in ballast waters and/or adult settlement on ship hulls (Allen, 1953; Sun et al, 2015). Several clades, including the Serpulae, Crucigera and Hydroides genera, within the Serpulid family demonstrate this biofouling potential with only a distinctive opercular structure to distinguish between species (Kupriyanova et al, 2008).
 Hydroides dirampha is one such species belonging to the Hydroides genus within the Serpulid family. First described by Mörch in 1863, this species is characterized by its anchor-shaped double-funnel operculum (Sun et al, 2015). Bar identification purposes, the operculum also serves to plug the tubule entrance (Bastida-Zavala & Ten Hove, 2002). The opercular structure is a modification of the branched tentacles (Schochet, 1973) used for suspended particle collection (Jeuniaux, 1969) and respiration (Bastida-Zavala & Ten Hove, 2002). Bristled epidermal projections called chaetae anchor the body into the tube to avoid displacement during this filter-feeding process (Kolbasova et al, 2014). Like many other Hydroides species, rapid development of planktotrophic larvae and sexual maturation post settlement enable successful H. dirampha colonization of many available submerged surfaces (Gibson et al, 2001).
H. dirampha has a globalized distribution across several (sub)tropical localities attributed to the combination of settlement success and artificial transportation discussed previously. Species are typically confined to subtidal shallow shelf depths (Bastida-Zavala & Ten Hove, 2002). Whilst perhaps not as successful as its infamous brother H. elegans (Haswell, 1883), this species is still a notable component of many problem biofouling communities internationally (AOLA, 2018). Specimens studied over the course of this semester were collected from Manly Harbor Queensland and can be found at several other locations across Australia (Sun et al, 2015). The unique ecology of biofouling marine worms makes H. dirampha an interesting species to investigate further.
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Physical Description |
General Morphology | |
Hydroides dirampha was first described by Mörch in 1963. Its physical form follows closely that of many related Hydroides and by extension Serpulid species with subtle distinction that make it morphologically unique (Bastida-Zavala & ten Hove, 2002). Its body is usually yellow to brown in color with pigmentation of the radioles amber to brown, as seen in Figure 2. Average body length is approximately 18mm with large individual variation (Bastida-Zavala & ten Hove, 2002; Sun et al, 2015).
Body
Figure 2: Ventral view of adult Hydroides dirampha with key morphological characters highlighted and labelled. Image Credit: Amelia Desbiens 2018.
As with all other polychaetes, the body of Hydroides dirampha is anterior-posteriorly elongated. A sizable abdomen ended with a posterior growth zone known as the pygidium is followed by a thoracic region covered in a membrane dubbed “the apron”. Both the thoracic and abdominal regions are banded with chaetigers comprised of unicini rows and protruding chaetae, as seen in Figure 3. A collared region of the thoracic membrane gives rise to a branchial crown made of approximately 20 ciliated tentacular radioles comprising approximately 1/3 of total body length. A differentiated radiole known as the operculum rises above the branchial crown (Bastida-Zavala & ten Hove, 2002; Sun et al, 2015).
Figure 3: Schematic drawing of Hydroides general morphology adapted from (Bastida-Zavala & ten Hove, 2002). Image Credit: Amelia Desbiens 2018.
Operculum
As seen in Figure 3, the operculum is comprised of a stalk peduncle that constricts before opening to a spined funnel. A secondary funnel comprised of verticil spines rises from within the first. A secondary pseudoperculum shorter in length is comprised of a bulbous projection atop a small peduncle (Bastida-Zavala & ten Hove, 2002). Growth of the secondary operculum is possible given the loss of the primary opercular structure (Okada, 1933; Schochet, 1973).
The opercular structure of Hydroides dirampha distinguishes it from all other Serpulid species. As seen in Figures 4 & 5, the verticil spines are characteristically inverted anchor-shaped. Approximately 14 verticil spines are present in each individual with approx. 30 radii of the primary funnel (Bastida-Zavala & ten Hove, 2002; Bastida-Zavala, 2008; Sun et al, 2015). Peduncle usually insert between first and second radioles on the left or right-hand sides (Sun et al, 2015). Total opercular length on average is 1.3 mm with an approximate width of 1mm (Bastida-Zavala & ten Hove, 2002; Sun et al, 2015).
 
Figures 4 & 5: SEM photo of Hydroides dirampha operculum. Specimen collected from Manly Harbor, Queensland. Image Credit: Amelia Desbiens 2018.
Chaetae and Uncini
Figure 6: Schematic drawings of Hydroidesdiramphachaetiger morphology as adapted from (Bastida-Zavala & ten Hove, 2002). (A) thoracic chaetae, (B) thoracic uncini, (C) abdominal trumpeted chaetae, (D) abdominal uncini, (E) collar bayonet chaetae. Image Credit: Amelia Desbiens 2018.
As mentioned previously, chaetae and uncini line the abdominal and thoracic segments of Hydroides dirampha’s body. These projections are used to anchor the body into the tube (Kolbasova et al, 2014). As seen in Figure 6, length, size and shape of these appendages differ depending on their locality. Thoracic chaetae attached to the apron are long (Figure 6A & 7) and accompanied by saw shaped uncini (Figure 6B). Six rows of chaetigers are standardized across most individuals of this species, as seen in Figure 7 & 9 (Bastida-Zavala & ten Hove 2002; Sun et al, 2015). One set of chaetae sit on the collar of the thoracic region and have an elongated bayonet shape with pointed teeth (Figure 6E). Abdominal chaetae are shortened and trumpeted shaped (Figure 6C) and paired with saw-shaped unicini (Figure 6D). Repetitions of abdominal chaetigers is highly variable between individuals depending of total body length (Sun et al, 2015).
 
Figures 7 & 8: Left image shows SEM photo of ventral view of thoracic chaetae. Right image shows SEM photo of abdominal uncini. Both photographs taken of Hydroides dirampha specimen collected from Manly Harbor, Queensland. Image Credit: Amelia Desbiens 2018.
Figure 9: Microscope photograph showing relative positioning of differentiated chaetal structure on Hydroides dirampha specimen from Manly Harbor, Queensland. Image Credit: Amelia Desbiens 2018.
Tube
The calcareous tube built by Hydroides dirampha is white in color with large variability in length depending on the individual. Tube orientation can be straight or spiraled, also depending on the individual (Bastida-Zavala & ten Hove, 2002). The exterior is lined with longitudinal ridges crossed with transverse ridges, as seen in Figure 10. The width tubes of each individual are also variable with average measurements of 1.4mm with an inner lumen width of approximately 0.9mm (Bastida-Zavala & ten Hove, 2002; Sun et al, 2015).
Figure 10: SEM photo of calcareous tube collected from Hydroides dirampha specimen found in Manly Harbor, Queensland. Image Credit: Amelia Desbiens 2018.
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A Comparative Analysis to H. elegans | |
As discussed above, Hydroides dirampha has distinctive morphological characteristics and measurements that distinguish it as its own species. Here we compare and discuss the difference in these anatomical characters of H. dirampha with that of world renown bio fouler Hydroides elegans.
Table 1: Shows morphological measurements for a range of anatomical characters of Hydroides dirampha and Hydroides elegans averaged from measurements of individuals by Bastida-Zavala & ten Hove (2002) & Sun et al (2015).
As can be seen from Table 1, H. elegans is in general a smaller organism than H. dirampha, with smaller measurements of tube width, opercular length & width, chaetae numbers and average body size. Differences in the shape of the verticil spines is also evident, as seen Figure 11, with each verticil spine possessing 2-4 lateral spinules (Sun et al, 2015).
Figure 11: SEM photo of Hydroides elegans opercular structure. Image Credit: Amelia Desbiens 2018.
Hydroides elegans, being one of the most successful biofouling polychaetes (Qiu & Qian, 1997), has a much larger distribution than that of Hydroides dirampha. It is hypothesized that this may be at least in part due to the size differences highlighted above. Smaller organisms mature faster and can settle more abundantly on surfaces (Thorson, 1949). Current scientific literature is generally lacking in its ability to address whether the physical differences described above have any proven ecological consequences. Much of life history, behavioral and physiological study has been conducted on H. elegans due to its global prosperity and extrapolated for use in other Hydroides species. The accuracy of continuing to use H. elegans as a model species is unknown given the differences highlighted above and requires further investigation.
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Ecology | |
Filter feeding
Figure 12: Typical feeding position of H. dirampha, showing extended branchial crown used in particle trapping and transport to the mouth. Image Credit: Amelia Desbiens 2018.
Serpulidae, and therefore by extension H. dirampha, use the feathery crown of radioles to collect particles (Jeuniaux, 1969). Water current across these tentacles are produced by cilia of the crown, whilst ciliary tracts lead particulates to the mouth. Detrital matter of 1-2 microns in size seem to be the food of choice, with other suspended particles like free-swimming algae too large to be filtered (Dales, 1957; Jeuniaux, 1969). Filtration rates for model Hydroides species have been determined (Dales, 1957; Jeuniaux, 1969), however these values have not been quantified for H. dirampha. Nevertheless, it can be agreed that smaller individuals have relatively higher filtration rates due to comparatively larger crowns across most Serpulid species (Dales, 1957).
Predation & Competition
Due to the protection offered by calcareous tubules, Hydroides dirampha does not have many natural predators. Biological limitations to distributions center more on competition for space (Ferguson et al, 2013). Associations with other species are likely when niche overlap is present. Several species with similar ecological requirements included but not limited to ectoprocts, barnacles and other fouling polychaetes are therefore known competitors to Hydroides species (Haines & Maurer, 1980).
Biofouling
 From colonization of ships, posts, nets, cages and ropes, biofoulers have the ability to cause severe economic damage (Fitridge, 2012). The wide variety of available surfaces spoil species for choice of place to settle and grow. The cost of damage caused by these organisms and subsequent removal effort is substantial in aquaculture and maritime industries (Gollasch, 2002; Fitridge, 2012). Current effort has focused on preventing initial settlement with anti-fouling coatings, however efforts in the engineering and chemical production of these products is still ongoing (Callow & Callow, 2011).
Figure 13: Shows biofouling potential of Hydroides on a range of maritime paraphernalia. Image Credit: (Dos Santos Schwan et al, 2015).
The anatomical and ecological characteristics of Hydroides dirampha lend itself well to biofouling. High temperatures and organic pollution concentration in many harbors and ports internationally make them hospitable places for these species (Allen, 1953). This location has enabled capture transportation of larvae in ballast water. Further, adult settlement on ship hulls and bottoms is also possible due to their proximity to marine vessels. Due to the adhesion strength of Hydroides tubules (Kavanagh et al, 2001), transportation at high speeds does not detach these organisms (Allen, 1953) allowing them to travel long distances with these watercraft whereafter colonization and settlement occur anew.
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Life History and Behaviour |
Reproductive Behaviour | |
Gonochoristic Hydroides adults undergo sexual reproduction (Gibson et al, 2001). Small eggs (approx. 50 microns in diameter) are fertilized by conical shaped sperm. Fertilization occurs externally in Hydroides dirampha, after mass spawning of both eggs and sperm into the water column. Large quantities of sperm are released, with a sizable amount presumably perishing, before successful encounter with an egg. Usually, sperm are released first, initializing the later release of eggs directly into suspended sperm aggregations that give the highest probability of fertilization occurring (Thorson, 1949; Gibson et al, 2001).
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Larval Development | |
Figure 14: Stages of larval development. (A) egg, (B) 2-cell stage, (C) 4-cell stage, (D) 8-cell stage, (E) early trocophore, apical view, (F) early trocophore, lateral view, (G) metatrocophore, lateral view, (H) 3-chaetiger larval stage, dorsal view, (I) early larval metamorphosis. Image Credit: (Gibson et al, 2001).
As seen in Figure 14, external fertilization of the egg initiates embryogenesis and blastulation (Gibson et al, 2001). The first cleavage occurs between 1-3h after fertilization (Figure 14B) proceeded by uniform cleavage through 4 and 8 cell stages (Figure 14C&D). The trocophore larvae that proceed this stage are characterized by a ciliated band circling the body used for feeding and swimming. Beating of the cilia in this planktotrophic larval stage facilitates movement and filtration of particles to the mouth (Strathmann, 1977). At this stage, a simple gut, starting with the mouth, is formed below the ciliated band with the anus exiting on the opposite side (Figure 14G) (Gibson et al, 2001). Progression past locophore morphology is initialized through the production of 3 body segments, synthesized by teloblasts in the posterior growth zone (Shimizu and Nakamoto, 2001). Each of these segments possesses distinctive chaetigers, as seen in Figure 14H&I.
The indirect development of Hydroides dirampha described above is ecologically advantageous in many ways. Larval stages of the life cycle enable dispersal across potentially large distances (Pechenik, 1999). The distinction of planktotrophy in H. dirampha further facilitates this dispersal ability due to elongation of the pelagic phase in comparison to lecithotrophic individuals. In addition, the requirement for only small eggs poor in yolk is energetically conservative and enables gamete production by relatively young mothers (Thorson, 1949; Pechenik, 1999; Gibson et al, 2001). These characteristics are typical of successful bioinvaders.
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Settlement | |
Metamorphosis and settlement follow the developmental stages outline above. Whilst solitary in nature, Hydroides species show clear gregarious settlement behaviour. Colonization of a new surface is often achieved through mass aggregation of large quantities of metamorphosing larvae (Scheltema et al, 1981). Settlement of biofouling species such as Hydroides elegans is often mediated by the biological composition of available space. Biofilms made of microorganisms and adsorbed organic matter are attractive places to settle given the right combination of bacterial components (Lau et al, 2002). Upon contact with prospective substrate, larvae actively explore the surface in order to assess its suitability (Lau et al, 2002). The accumulation of biofilms on many economically valuable maritime machinery and equipment has enabled the settlement and aggregation of biofouling species. The specific requirements for metamorphosis and attachment of Hydroides dirampha have not been quantified.
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Anatomy and Physiology | |
Circulatory and Digestive Systems
The circulatory system of Serpulid species is comprised of central and peripheral blood systems. Blood flows from the abdomen to the thorax through a sinus before running through dorsal, transverse and oesophageal vessels and eventually moving back down the ventral vessel to the tip of the abdomen. Vessels of the peripheral system extent into the branchial crown, collar and thoracic membranes (Hanson, 1950). The branchial crown is well supplied with blood due its function as respiratory “gill” projections as well as for locomotory agility for feeding (Bastida-Zavala and ten Hove, 2002). In most annelids it is accepted that digestion occurs extracellularly. The path of food intake is standardized with the digestive system starting at the mouth, entering the esophagus, then intestines before moving through the stomach and finally rectum (Jeuniaux, 1969). Species-specific traits of these systems are lacking for Hydroides dirampha.
Reproductive System
Adult Hydroides species are gonochoristic with notable absence of true gonads in either sex (Gibson et al, 2001). Instead germ cells are a product of blood vessel epithelium in the intersegmental septa. Broadcast spawning is common within Hydroides, where gametes are released through nephridiopores and expelled out of the tube with the help of ciliary beating of the faecal groove (Gibson et al, 2001). Serpulids, as iteroparous organisms, reproduce multiple times throughout their lives, however frequency of gamete release and fecundity of sexes within the Hydroides genus is extremely variable (Gibson et al, 2001) and has not been directly quantified for Hydroides dirampha.
Segmentation
As with all Annelids, Hydroides dirampha shows clear segmentation of the body (Shimizu & Nakamoto, 2001). The differentiation of body segments in Hydroides species occurs within a few days of fertilization, with the first three segments appearing simultaneously (Seaver et al, 2005) (see Figure 14). After transformation into juvenile form, further segments are added, usually originating from teloblasts in the posterior growth zone known as the pygidium (Shimizu & Nakamoto, 2001). There is, however, evidence in some Hydroides species of thoracic segment generation in the middle of the body rather than posteriorly (Seaver et al, 2005). Each segment derives its own set of chaetae and uncini (Shimizu & Nakamoto, 2001), with total number of body segments and corresponding chaetigers extremely variable across Hydroides dirampha individuals (Sun et al, 2015).
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Biogeographic Distribution | |
Figure 15 : International distribution of H. dirampha as collated by The Atlas of Living Australia (AOLA, 2018).
H. dirampha was originally documented in St Thomas (Mörch, 1863), but can now be found internationally as seen in Figure 15. Their distribution has been heavily enabled through transportation of planktonic larvae in ballast water and/or through settlement on ship hulls (Allen, 1953). This species can be found in tropical/subtropical localities including the Mediterranean, Indo-West Pacific, West and East Atlantic, South Africa, New Zealand as well as in coastal communities across several states of Australia (Sun et al, 2015). Presence in lagoons across the Caribbean appears “natural” (Sun et al, 2015), however distribution across temperatures of approx. 20-30 degrees Celsius and salinity ranges of 25-35% (Chan et al, 2013) seem to be adequate diagnostics for survival in any region.
The specimens examined over the course of this semester were collected from settlement plates in Manly Harbor, Queensland. Identification of H. dirampha at this location is previously undocumented. Finding this species in Manly Harbor waters supports suggestions of distribution mainly due to accidental ship transfer (Sun et al, 2015) and could further facilitate its distribution to many other localities with similar conditions in future years.
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Evolution and Systematics | |
Phylogeny of Serpulids
Serpulidae are currently categorized within the Sabellida order whose composition is currently debatable (Kupriyanova et al, 2006). The Serpulid family is divided into three sub-families, as seen in Figure 16, being Serpulinae, Spirorbinae and Filograninae. Most recent analysis of morphological characters by Kupriyanova (2003) show monophyletic Serpulinae and Spirorbinae as sister taxa with paraphyletic Filograninae less closely related (see Figure 16). However, in previous studies alternative tree compositions have been postulated (ten Hove, 1984; Fitzhugh, 1989). Morphological features have remained the primary classification mechanism, with genetic analyses only recently supplementing existing hypotheses (Kupriyanova et al, 2006).
Figure 16: Phylogeny of Serpulidae with emphasis on the branch composition of the Hydroides, Serpula and Crucigera clades within the Serpulinae sub-family. Tree composition hypothesis originally postulated by Kupriyanova (2003) congruent with data of 38 morphological characters, 28S and 18S genetic sequences. Adapted from (Kupriyanova et al, 2006).
Serpulae to Crucigera to Hydroides
Within the Serpulinae sub-family, Serpulae, Crucigera and Hydroides genera are the most speciose (Kupriyanova et al, 2008). This clade shows synapomorphies in morphological characters such as the collar bayonet-shaped chaetae, trumpeted abdominal chaetae, the presence of a pseudoperculum and a funnel-shaped operculum (Kupriyanova, 2003). Monophyly of this clade has been confirmed genetically and morphologically (Kupriyanova et al, 2008). Evolution of the opercular structure is most topical within these three groups with the most parsimonious hypothesis shown in Figure 17.
Figure 17: Hypothesis of opercular evolution between Serpulae, Crucigera and Hydroides genera. (A) shows funneled Serpula-type operculum, (B) Crucigera-type operculum with basal knobs originating from the bottom of opercular structure, (C) Hydroides-type operculum with defined verticils and basal knobs, (D) advanced Hydroides-type operculum with defined verticils and modified basal funnel originating from basal knobs. Adapted from (Kupriyanova et al, 2008).
Figure 17 shows the opercular structure’s evolution from a single funnel Serpula-like shape. Progression through time included the elongation of vertical spines and the development of basal knobs (Crucigera-like). Modification of the basal knobs into a secondary funnel shows the typical Hydroides form. Hydroides dirampha displays the most derived opercular condition with defined verticils and a secondary funnel as discussed previously.
Classification and Systematics
Synonyms of Hydroides dirampha (Mörch, 1863) as adapted from (Read & Fauchald, 2018).
Eucarphus serratus (Bush, 1910)
Eupomatus dirampha (Mörch, 1863)
Eupomatus lunulifer (Claparède, 1870)
Hydroides (Eucarphus) benzoni (Mörch, 1863)
Hydroides (Eucarphus) cumingii (Mörch, 1863)
Hydroides (Eucarphus) cumingii navalis (Mörch, 1863)
Hydroides (Eucarphus) dirampha (Mörch, 1863) [original]
Hydroides benzoni (Mörch, 1863)
Hydroides cumingii (Mörch, 1863)
Hydroides diramphus (Mörch, 1863)
Hydroides lunulifera (Claparède, 1870)
Hydroides malleophorus (Rioja, 1942)
Hydroides serratus (Bush, 1910)
Serpula (Hydroides) lunulifera (Claparède, 1870)
Vermilia benzonii (Mörch, 1863)
Vermilia cumingii (Mörch, 1863)
Vermilia dirampha (Mörch, 1863)
Classification (Read & Fauchald, 2018):
Kingdom – Animalia
Phylum – Annelida
Class – Polychaeta
Order – Sabellida
Family – Serpulidae
Genus – Hydroides
Species – H. dirampha
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Conservation and Threats | |
As discussed previously, H. dirampha is distributed internationally and able to survive in a wide range of temperatures and salinity concentrations. Nevertheless, changes in salinity, temperature, CO2 concentration and pH as a result of climate change may affect this organisms’ ability to continue thriving. These climatic factors are influential in the determination of settlement success and larval development. In a laboratory setting, temperature changes had no effect on survivorship of Hydroides (Qiu & Qian, 1997), however the elongation of trocophore development duration may increase the likelihood of predation in a natural setting (Pechenik, 1999). Further, decreasing salinity impedes settlement ability (Qiu & Qian, 1997).
Biomineralising organisms like H. dirampha are also subject to the effects of changing abiotic factors on their ability to synthesize calcareous tubes and shell and thereby protect themselves (Pörtner, 2008). Decreases in water pH and increases CO2 concentration impede tube-dwelling organisms’ capacity to secrete CaCO3 (Chan et al, 2013). Decreasing salinity also negatively impacts the mechanical strength and integrity of tubes (Chan et al, 2013) due to changes in the composition ratio of calcium (Klein et al, 1996). Rising temperature seem to prevent or at least lessen the severity of these mineralization changes in Hydroides species (Chan et al, 2013), in congruence with lack of temperature effects on other developmental procedures (Qiu & Qian, 1997). Due to the likely occurrence of combinations of these climatic factors in future years, there is potential for H. dirampha persistence due to the remedial effects of temperature rise.
The potentially negative influence of changing climate factors on other species may clear space and reduce competition (Peck et al, 2015). The indirect consequences of such biodiversity loss could positively impact the distribution of H. dirampha due to declines in competition for settlement space and increases in total available space due to death or migration of affected species. Whether persistence of this species is desirable in any capacity is another question entirely.
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References | |
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