Mollusca, Polyplacophora, Leptochitonidae - University College Dublin

Marine Biology Research, 2009; 5: 193199

ORIGINAL ARTICLE

Parasitic foraminifers on a deep-sea chiton (Mollusca, Polyplacophora, Leptochitonidae) from Iceland

JULIA D. SIGWART*

Downloaded By: [Sigwart, Julia D.][University College Dublin] At: 15:55 11 March 2009

National Museum of Ireland, Natural History Division, Dublin, Ireland, and Queen’s University Belfast, School of Biological Sciences, Belfast, UK

Abstract Epibiotic foraminifers selectively settle on the most food-rich area of the host substrate, even when the species acts as a facultative ectoparasite in later life stages. In 398 specimens examined of the deep-sea chiton Leptochiton arcticus from Iceland, 46% show evidence of infestation by foraminifers, with many showing extensive shell damage from present and past bioeroding epibionts. Disturbances to the inner layer of the host shell are indicative of parasitism, as evidenced both by wound healing calcification and protrusions of the foraminiferan tubules. The epibionts employ different feeding strategies at different stages of their life cycle, taking advantage of nutrient availability from the posterior respiration currents and excrement of the chitons as juveniles, and feeding parasitically as adults. Epibiont persistence on individual hosts through successive generations, or long-term continuous bioerosion by epibionts allow larger adult parasitic foraminifers of Hyrrokkin sarcophaga to penetrate the thick tail valve of a chiton and feed parasitically on the host tissue. The proportion of chitons infested increases with host size, indicating that epibionts are accumulated through a chiton’s life, seemingly without major detriment to host survivorship.

Key words: Arctic, benthic ecology, epibiota, facultative parasitism, Foraminifera

Introduction Parasites of deep-sea organisms are poorly understood, particularly those of benthic macroinvertebrates (Bray 2005). However, much can be inferred about the nature of relationships between hosts and epibionts from morphology, and especially from ontogenetic series that are available from systematic large-scale survey collections. Relatively few parasites have been recognised or reported for polyplacophoran molluscs (chitons), and all are endoparasitic (e.g. Ball & Neville 1979; Avdeev & Sirenko 2005; Schwabe et al. 2006). This study reports the first shell-borne ectoparasite known from a chiton, on the deep-sea species Leptochiton arcticus (Sars, 1878). Chitons are distinctive benthic marine invertebrates with eight interlocking dorsal shell valves, which generally feed as grazers on algae or bacterial mats. The predominantly deep-sea family Leptochitonidae is considered ‘primitive’ within polyplacophorans.

Epibiotic foraminifers on deep-sea chitons are frequently observed (e.g. Kaas & Van Belle 1985, figure 91), but have never been addressed in a context of chiton biology. Many aspects of deep-sea chiton biology are very poorly understood and are generally inferred only from the larger, intertidal species. Evidence of parasitism by a foraminifer on a deep-sea mollusc was first suggested by Todd (1965). Active foraminiferan parasitism was confirmed by Alexander & DeLaca (1987) on scallops from Antarctica. Another parasitic deep-sea foraminiferan species in the North Atlantic is also known to feed on other bivalves as well as on sponges and coral hosts (Cedhagen 1994). Epibiotic foraminifers are known from all seas and have an extensive fossil record (Neumann & Wisshak 2006). Species in many families of these complex protists are capable of forms of bioerosion (also referred to as drilling or boring), although the mechanisms remain unclear (Veńec-Peyre´ 1996; Wisshak & Ru¨ggeberg 2006; Beuck et al. 2008).

*Correspondence: Julia D. Sigwart, National Museum of Ireland, Natural History Division, Merrion Street, Dublin 2, Ireland. E-mail: [email protected] Published in collaboration with the University of Bergen and the Institute of Marine Research, Norway, and the Marine Biological Laboratory, University of Copenhagen, Denmark (Accepted 24 April 2008; Published online 13 February 2009; Printed 20 March 2009) ISSN 1745-1000 print/ISSN 1745-1019 online # 2009 Taylor & Francis DOI: 10.1080/17451000802266641

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Some forms are even capable of active parasitism. Parasitic foraminifers on molluscs are epibiotic on the outer surface of the shell, but etch vertical channels through the host shell and feed on the host tissue within (Alexander & DeLaca 1987; Cedhagen 1994). A large dataset based on a comprehensive survey of the Icelandic benthos from the BIOICE survey provides insights into the distribution of hosts and parasites. This study examined the ontogeny of the interaction through all growth stages of the host chitons, adding to the knowledge both of foraminiferan microhabitats and the epibiota of polyplacophoran molluscs.


Materials and methods All specimens were collected by the BIOICE (Benthic Invertebrates of Icelandic Waters) project. The material was collected from a total of 48 survey stations in Icelandic waters between July 1992 and September 2001 (Figure 1). All samples were initially fixed in 10% formalin and later transferred to 70% ethanol. Polyplacophorans were sorted out in the Sandgerdi Marine Centre. All material is held in the collections of the Icelandic Museum of Natural History, Reykjavik (IMNH). Identification of all polyplacophorans specimens was confirmed by the author. All specimens of Leptochiton arcticus were individually examined and measured. As many specimens are longitudinally curled in death, width at the body midpoint is taken

as a proxy for overall size. All measurements reported were taken from an average of three successive calliper measures (0.01 mm). The morphology of foraminifers on the dorsal surface of the shell and the epibionts’ penetration to the ventral surface of the shell were examined by dissection of a subsample of six host specimens. The presence and number of epibiotic foraminifers was recorded for individual specimens taking note of placement on specific valves or the girdle surface. Additionally, evidence of pitting and scarring on valve margins was also recorded as evidence of epibionts (Figure 2). The total foraminifer population observed represents several species, not all of which are parasitic (see Results section). For purposes of statistical analysis, individual chitons were scored for presence or absence of epibiotic foraminifers, where presence was considered to be indicated by either present epibiotic foraminifers on the shells or past infestation demonstrated by scarring. Specific counts of scars and attachment points of individual foraminifera were recorded for a subset of 80 infested specimens. For statistical analysis, all chitons were divided into four size classes each of one standard deviation in range (1.7 mm; see Table I). The largest individuals span slightly more than one standard deviation, so all chitons larger than 5.1 mm wide grouped into a single size class. Because only presence/absence data are available for the epibionts for all specimens, the presence of epibiotic foraminifers and the size of

Figure 1. Map of Iceland showing distribution of chitons collected by the BIOICE programme. Outline dots indicate stations where chitons were collected but no specimens of Leptochiton arcticus; grey solid dots indicate stations where L. arcticus specimens were collected but no epibiotic foraminifers were present; black solid dots indicate stations where L. arcticus specimens were collected with epibiotic foraminifers.


Foraminiferan epibionts on a deep-sea chiton

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Figure 2. Photograph and line drawing of Leptochiton arcticus specimen heavily infested with epibiotic foraminifers, with anterior at top. White spots on line drawing indicate foraminifers or bioeroded scars caused by foraminifers; light grey areas indicate posterior margins of intermediate valves that have been completely broken away by the bioerosion of epibionts. Scale bar10 mm.

individuals on which they occurred was compared using a chi-square. Other physical factors, such as depth, salinity, bottom temperature, were compared to host size and visually assessed for potential correlative patterns. Results In total, 398 individual specimens of Leptochiton arcticus were recorded ranging from 0.45 to 7.70 mm in width. Of those, 46% (n 183) showed evidence of epibiotic foraminifers as present epibionts or scars from past epibiont attachments. The largest number of individual foraminifers (of all species) recorded was 41 foraminifers on a single chiton (width 5.60 mm). Epibiotic foraminifers were present on chitons at all stages of growth collected. Many of the juvenile specimens identified were not infested; the smallest individual with epibiotic foraminifers was

0.60 mm wide. The oldest (largest) individuals were heavily infested; the widest specimen with no evidence of epibionts was 7.15 mm wide. The prevalence of epibiotic foraminifers increased significantly with host size ( x2 103; df 3; p B0.001). More than 80% of the largest chitons showed evidence of infestation, although foraminifers were observed on juvenile specimens and on chitons in all stages of growth (Figure 3; Table I). Water temperature, salinity, and depth were not significantly related to presence or size of chitons or the presence of epibiotic foraminifers. However, chitons from the deepest sample stations tended not to host epibionts, except for on the largest chitons in those samples (Figure 3). The distribution of foraminifers on the chitons was significantly influenced by the specific shell valve within individual hosts in all size classes ( x2 34.5; df 21; p B0.032). The majority of epibiotic

Table I. Number of Leptochiton arcticus specimens in five size classes, and number with epibiotic foraminifers present (including presence of bioeroded scars from past infestation). Size range (mm width)

0.601.69

1.703.39

3.405.09

5.106.79

6.807.70

Total recorded

Number with epibionts Number not infested Number of specimens % infested

7 82 89 8

28 58 86 33

93 47 140 66

47 15 62 76

6 1 7 86

183 215 398 46

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J. D. Sigwart C. lobatulus, and C. wuellerstorfi in decreasing order of abundance (G. Gudmundsson, personal communication). Cibicides refulgens may also act as a facultative parasite (Alexander & DeLaca 1987). The presence of the parasitic foraminifers is visible on the ventral (internal) surface of chiton shells in two ways. Black, star-like protrusions surrounding the channel bored by the foraminifers, are visible through the transparent inner layer of the chiton shell (Figure 5). Also, opaque white spots and ‘clouds’ of dense calcium deposits show evidence of defensive localized calcification to heal the channels bored by parasites.


Figure 3. Scatter plot indicating depth distribution of Icelandic Leptochiton arcticus specimens of varying sizes, with (black dots) and without (white dots) infesting epibiotic foraminifers.

foraminifers are settled on the posterior part of the chitons, especially on the tail valve, with also a slightly elevated density on the head valve (Figure 4). More than 70% of the individual foraminifers observed were present on the posterior three valves of the host chitons, with 43% on the tail valve alone. In addition to foraminifers observed in situ on the host chiton, effects of previous infestations can be observed by the damage to the posterior margin of intermediate plates, which have been bioeroded in series of round scars (Figure 2). The parasitic foraminifer Hyrrokkin sarcophaga Cedhagen, 1994, was observed on many specimens of Leptochiton arcticus; the foraminifer was identified based on the umbilical morphology and the distinctive brown film around the perimeter of larger specimens. Three other species in the genus Cibicides were also observed as epibionts on L. arcticus: C. refulgens,

Figure 4. Bar chart indicating distribution of individual epibiotic foraminifers recorded on specific valves of the chiton host (I, head valve; VIII, tail valve). A subset of 80 infested chiton specimens were examined for number and position of epibionts (n 286).

Discussion This study provides the first record of shell-borne parasitism in a polyplacophoran mollusc. Individual specimens of Leptochiton arcticus show substantial infestation by parasitic foraminiferans, in the form of scars and pits caused by foraminiferan bioerosion as well as attached epibionts. Bioerosion is caused by Hyrrokkin sarcophaga, and potentially by Cibicides spp., on the chitons. The potential presence of Cibicies refulgens as a minority epibiont cannot be excluded, and this species is also known to act as an eroding epibiont (Alexander & De Laca 1987; Beuck et al. 2008). Parasitism by H. sarcophaga is evident from invasive channels to the ventral shell surface associated with the dorsal epibionts. Bivalves infested with H. sarcophaga have been repeatedly observed to defend themselves by increased localized calcification to seal the channels bored by the parasitic foraminifers (Freiwald & Scho¨nfeld 1996; Lo´pez Correa et al. 2005, Figure 1; Beuck et al. 2008). This is in contrast to infested corals, which do not appear to heal wounds by local concentrated calcification (Freiwald & Scho¨nfeld 1996; Beuck et al. 2007). Chitons exhibit a similar response to their fellow molluscs, although it is far less dramatic than the response described in bivalves. Veńec-Peyre´ (1996) observed that bioeroding foraminifers may be highly selective in their settlement; however, previous studies on bivalve epibionts and parasites have shown a random patter of settlement over the upper valve (Mullineaux & DeLaca 1984; Alexander & DeLaca 1987; Cedhagen 1994). Foraminifers epibiotic on chitons show a pronounced settlement pattern with a preference for terminal, and especially the posterior, region of the host (Figure 4). Interestingly, the tail valve of a chiton is thicker than all other individual valves, especially around the pronounced posterior mucro (indicated with a chevron on Figure 2). As this is the most difficult area on a chiton to penetrate, because of the shell thickness, preferential settlement must be stimulated by factors other than parasitism.



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Figure 5. Line drawing and photograph of ventral right side of tail valve from specimen of Leptochiton arcticus showing black star-shape marks associated with parasitic Hyrrokkin sarcophaga attached on the dorsal (outer) shell surface. Opaque white calluses are visible within the shell matrix, above the transparent ventral inner hypostracum. Scale bar 5 mm.

Bioerosion on the chitons’ intermediate valves is frequently so intense that epibiotic foraminifers apparently eroded away their own substrate, leaving round scars on the valve margins (Figure 2). It is impossible to determine whether these fallen foraminifers were feeding parasitically when they were attached. These shell margins may afford the best access to the mantle flesh of the host, and severely bioeroded areas in some specimens leave muscle tissue exposed between valves when the chiton is curled. On the other hand, the evidence that the shell substrate at these margins is prone to breakage or collapse indicates it may be a less advantageous region for settlement. Alexander & DeLaca (1987) observed that in the epibiotic foraminifer Cibicides refulgens, adult specimens fed parasitically on the host through channels etched in the host shell, while juveniles fed by suspension feeding. Infested specimens of L. arcticus clearly accumulate epibionts throughout their life, since a greater proportion of larger animals are infested. The foraminifers and scars on the shell surface show wide ontogenetic variation, which also indicates that new epibionts continue to settle throughout the life of the chiton. The same pattern has been reported in infested bivalves (Freiwald & Scho¨nfeld 1996). Hyrrokkin sarcophaga is known primarily from the northeastern Atlantic but has not previously been reported from Iceland. The majority of records show a distribution from 200 to 500 m depth (Freiwald &

Scho¨nfeld 1996). This study agrees with this general range although shallower and deeper records are included (Figure 3). The range of the host species, L. arcticus, is known from as shallow as 10 m (Kaas & Van Belle 1985) and extends into deeper waters: a sample from the BIOICE survey was found at 2270 m, but as the chitons were preserved only as dry specimens they were not included in this assessment. Epibiotic lifestyles may be linked to poor environmental nutrient availability (Austin & Evans 2000). Association with a biotic substrate may improve the local availability of food resources. Although the presence of epibiotic foraminifers are not significantly correlated with any abiotic factors recorded for the BIOICE survey stations, they are positively correlated with overall depth. Similarly, the epibiotic bryozoans are not correlated to explicit abiotic factors, but are clearly clustered in localized regions. Interestingly, Austin & Evans (2000) studied populations of benthic foraminifers on a transect of the southwestern coast of Iceland, and noted that populations increased with greater nutrient availability in deeper water. (The area of their survey is in an area with populations of L. arcticus but no recorded epibiotic foraminifers.) Epibiotic foraminifers are noted to settle primarily on filter-feeding hosts (Alexander & DeLaca 1987). Barnacles are also known to selectively settle on filterfeeding hosts in preference to non-living substrates (Buschbaum 2001; Venerus et al. 2005). Potentially these epibionts benefit from proximity to the inhalant


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and exhalent currents generated by feeding bivalves and corals and suspended particulate nutrients. Although chitons feed by grazing, they do generate inhalant and exhalent respiratory currents. Exhalent respiration is directed posteriorly under the muscular girdle (Kaas & Van Belle 1985). Chitons also excrete nitrogenous waste through a nephridiopore within the gill row, and produce faecal pellets through a central posterior anus. Inhalant respiratory currents or chiton waste may provide a small but concentrated nutrient stream within the pallial cavity and at the posterior end of the animal. Foraminifers settling on the posterior part of a chiton may have access to a rich food source for juveniles, while subsequent generations of epibionts or gradual increasing bioerosion of the shell substrate eventually permit parasitic drilling by adults. The relatively high incidence of settlement on the head valve (Figure 4) could also result from active selection by larval foraminifers. Settlement on the anterior end may benefit from the inhalant respiratory current generated by the chiton, drawing in water to the ventral gills, or it could indicate selection by the foraminifers without the sophistication to distinguish the posterior or anterior end accurately. Foraminifers demonstrate selectivity in their settlement, but the parasitism of H. sarcophaga is not limited to one host species (Cedhagen 1994). Leptochiton arcticus adds another taxonomic class of molluscan hosts to previous records for parasitic Foraminifera. Hyrrokkin sarcophaga is also not limited to a single host species of chiton; however, they infest L. arcticus more frequently and in dramatically higher density than any other host chiton observed so far. Shell morphology and ontogenetic series provide a proxy for understanding the biology of hostparasite relationships. Based on the known biology of shallower species, it is possible to infer that H. sarcophaga uses a combination of feeding strategies suspension feeding and parasitism at different life stages. Although bioerosion by the epibiotic foraminifers have a visible destructive impact on the shell valves of chitons, their presence does not seem to negatively affect survivorship, as animals persist to large adult size despite infestation. Acknowledgements This work was supported by an award from the BIOICE programme to pay for a study visit to the SMC. The author thanks G. Gudmundsson (IMNH) and G. Helgason (SMC) for support in Iceland, and G. Dyke for helpful comments on this

manuscript. Max Wisshak and an anonymous referee provided constructive and improving reviews.

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