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Protodrilidae (Annelida: Polychaeta) from the Hawaiian Islandsand Comparison with Specimens from French Polynesia1

Julie H. Bailey-Brock,2,5 Claude Jouin-Toulmond,3 and Richard E. Brock4

Abstract: Three species of Protodrilidae were collected from the islands ofO‘ahu and Ni‘ihau in the Hawaiian chain, including specimens closely resem-bling Parenterodrilus taenioides ( Jouin, 1979), described from Mo‘orea (FrenchPolynesia). Others are probably an undescribed species of Parenterodrilus thatwas found in fine sand substrate collected off Wai‘anae, O‘ahu. A third species,Protodrilus albicans Jouin, 1970, described from Banyuls-sur-Mer (MediterraneanSea) and recorded from Mo‘orea and Tahiti as well, was also collected fromO‘ahu. Depths and habitat characteristics are given for these new records tothe Hawaiian fauna. It is suggested that the wide geographical distribution ofthe different ‘‘cosmopolitan species’’ of Protodrilidae is related both to the dis-persal by free-swimming larvae and to the ancient origin of this interstitialfauna.

Protodrilidae have long been considereda family of ‘‘Archiannelida’’ due to their smallsize, ventral ciliary gliding, ventral pharyngealorgan, and lack of conspicuous external seg-mental structures. Interstitial polychaetespreviously called ‘‘archiannelids’’ are now re-garded as specialized as opposed to primitivefrom an evolutionary perspective for Pro-todrilidae, Protodriloididae, Saccocirridae,Polygordiidae, Nerillidae, Dinophilidae, andDiurodrilidae (Westheide 1985, Purschkeand Jouin-Toulmond 1988, Bailey-Brock1999, Bailey-Brock et al. 2003).

Protodrilidae have well-developed sensory

structures (Purschke 1990a,b,c, 1993), epider-mal glands, epidermal ciliation, and a me-dioventral ciliary field. In Protodrilidae,Parenterodrilus Jouin, 1992 (Astomus is a syn-onym), living in coral sands, is unique in hav-ing a vestigial nonfunctioning gut, no mouth,no symbiotic bacteria, and a peculiar bodyshape ( Jouin 1979). The ultrastructure of thecephalic sense organs and central nervoussystem demonstrates the sister-group rela-tionship to Protodrilus and the derived posi-tion of Parenterodrilus (Purschke and Jouin-Toulmond 1993, 1994).

The ultrastructure of the ciliated epider-mis suggests transepidermal absorption ofnutrients ( Jouin 1992). Experiments madeon living animals, with ferritin added to theseawater in contact with the animals, demon-strated that after 30 min the epidermis hasfew subcuticular coated vesicles containingferritin, this substance being already concen-trated in endosomes in the apical part of epi-dermal cells and in secondary lysosomes morebasally ( Jouin-Toulmond 1994).

The males of Parenterodrilus taenioides( Jouin 1979), like Protodrilus species, havelateral organs and sperm ducts, and the ultra-structure of the spermatozoa is basically thesame in the two genera ( Jouin-Toulmondand Purschke 2004). Adaptations that facili-tate reproduction in Protodrilus include trans-fer of sperm by spermatophores deposited in

Pacific Science (2010), vol. 64, no. 3:463–472doi: 10.2984/64.3.463: 2010 by University of Hawai‘i PressAll rights reserved

1 Funding for J.H.B.-B. and R.E.B. provided in partby the U.S. Environmental Protection Agency, Environ-mental Monitoring and Assessment Program for theHawaiian Islands, 2002–2004. Manuscript accepted 21August 2009.

2 Zoology Department, University of Hawai‘i atManoa, 2538 McCarthy Mall, Honolulu, Hawai‘i 96822.

3 Universite Pierre et Marie Curie-Paris 6, CNRS-UMR 7144 AD2M Station Biologique, BP 74 29682Roscoff Cedex, France.

4 Water Resources Research Center, University ofHawai‘i at Manoa, Honolulu, Hawai‘i 96822.

5 Corresponding author.

the external milieu and then collected by thefemale epidermis and internal fertilization( Jagersten 1952, Jouin 1970, von Nordheim1989, 1991a,b, Purschke 2006). The eggs arespawned and attached on sand grains; the lar-vae have a pelagic life, and metamorphosisdepends on the availability of suitable habitatsubstratum ( Jagersten 1952).

Previous records from the Hawaiian Is-lands include Protodrilus sp. (Bailey-Brock1987) from the southeast shore of O‘ahu. Inthis paper, we discuss Protodrilus spp. thatwere collected on O‘ahu from sewage outfallsites and live specimens from Kawainui BeachPark that were examined briefly in the labora-tory but did not survive in aerated shallowcontainers of sand. Collections of coral sandsand reef rubble were made during an exten-sive coastal Estuarine Monitoring Program(EMAP) initiated by the U.S. EnvironmentalProtection Agency. For comparison, previ-ously unpublished data on specimens col-lected in French Polynesia ( by C.J.-T.) arepresented.

materials and methods

Sand cores (11 cm diameter, 5 cm deep) werecollected by divers, fixed in 10% formalin for24 hr or longer and elutriated over 0.5 mmand 0.25 mm sieves to extract the infauna.Protodrilids and other polychaetes were re-tained on the sieves and transferred to etha-nol for storage. Parenterodrilus specimenswere placed on slides with two drops of glyc-erol and examined microscopically. Protodrilusspecimens were stained with Carmalum andmounted in gelatin-glycerol or in Canadabalsam after dehydration. Illustrations weremade with the aid of a compound microscopeand drawing tube. Only fixed, unrelaxedspecimens of Hawaiian material were exam-ined.

Hawaiian localities where sand cores con-taining protodrilids were collected by diversare as follows: Ni‘ihau: Station 1, 21� 57.913 0

N, 160� 7.428 0 W, located in Keawanui Bayjust seaward of a sand beach on the north-western section of the coast of Ni‘ihau (sedi-ment comprised 50%–60% carbonate sandsof medium grain size), collected by EMAP

divers on 18 June 2002, at 4.85 m depth.O‘ahu: Two sites were investigated: (1) sew-age outfall monitoring stations at Wai‘anae,off the west coast of O‘ahu (sedimentscomprised medium- to fine-grain carbonatesands), sampled 7–9 June 2004 at depths of27–33.5 m; (2) Kuhio Beach, part of an ex-tensive sand beach at Waikıkı on the southcoast of O‘ahu (clean medium- to fine-grainsands), collected 12 October 2006 and Febru-ary 2007 at 5 m depth.

In French Polynesia, live mature speci-mens of Protodrilus albicans were collected incoarse sand near the water’s edge of beachesin Mo‘orea (Irioa) and Tahiti (Vairao). Theywere examined for reproduction: spermato-phores, sperm transfer, spawning, and younglarvae were observed microscopically inMo‘orea in July 1981.

Specimens studied have been deposited inthe Museum National d’Histoire Naturelle(mnhn) and in J.B.-B.’s personal collection atthe University of Hawai‘i.

results

Parenterodrilus taenioides ( Jouin, 1979)Figure 1

Astomus taenioides Jouin, 1979:2448.Parenterodrilus taenioides.—Jouin, 1992:1833.

material examined. Hawai‘i, Ni‘ihau:Four specimens collected from Keawanui Bay,4.85 m depth, June 2002, sediment comprised50%–60% medium-grain carbonate sands;O‘ahu: two specimens collected at Waikıkı,Kuhio Beach, clean medium- to fine-grainsands, 5 m depth, collected in October 2006.Prepared slides of specimens in J.B.-B.’s per-sonal collection at the University of Hawai‘i.

morphology. The fixed and unrelaxedHawaiian specimens measure about 6.5 mmlong and 0.15 mm wide and are dorsoven-trally flattened and distinctly annulated atthe segment borders (Figure 1A,D,E). Theanterior region has a pair of palps that areterminal in position, possess canals, and arecovered with cilia (Figure 1B,C ). The brainappears as an internal dense area just behind

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Figure 1. Parenterodrilus taenioides, specimen from Ni‘ihau (Hawai‘i). A, Entire specimen; B, anterior region; C, part ofa palp showing cilia; D, segments from midbody region; E, posterior end with pygidium. Note lobes with ducts ofadhesive gland cells. Scale bars: A, 100 mm; B, D, E, 50 mm; C, 10 mm.

the base of the palps. Longitudinal musclesare more evident in the posterior region,which has two flaring pygidial lobes with ad-hesive glands (Figure 1E). The salivary glandscould not be detected on fixed specimens. Inthe Polynesian specimens they were foundonly on ultrastructural sections ( Jouin 1992).

The specimens were immature when col-lected in June. Comparison of the character-istics of the Hawaiian male specimens withthose of specimens from Mo‘orea would beuseful. Females are unknown.

remarks. Parenterodrilus taenioides wasdescribed from specimens collected in coralsands (about 1.5 m deep) at Mo‘orea, FrenchPolynesia. This is the first record of the spe-cies at another locality. It is a Pacific species,probably restricted to sublittoral coral sandsnear coral colonies, where the species canthrive due to the presence of abundant dis-solved and particulate organic matter in thoseareas. The new collection sites off Ni‘ihau(4.85 m depth) and Kuhio Beach on O‘ahu(5 m depth) are adjacent to extensive shallowcoral reefs and are deeper than the type local-ity.

Nutrition in P. taenioides is not fully under-stood. Jouin (1992) established that the vesti-gial gut contained intracellular unidentifiedcrystals and suggested a bioaccumulation rolefor this residual organ. Symbiotic bacteriawere not detected in the cuticle, epidermis,or vestigial gut, and transport of particulateor dissolved organic matter through the epi-dermal cells (transepidermal ¼ parenteral ab-sorption) is most likely the means of organicuptake ( Jouin 1992, Jouin-Toulmond 1994).This is unusual for a free-living adult annelidand unique to this genus, which is otherwisesimilar in morphological features to otherprotodrilids. The residual gut is reduced to athin canal with a very narrow ciliated lumen.The salivary glands (detected with electronmicroscopy) are present in some anteriorbody segments, as in Protodrilus species, butin P. taenioides the secretion is released at theepidermal ventral surface of the prostomium( Jouin 1992).

A few sexually mature male specimenswere examined in February 1991 in Mo‘orea.The males of P. taenioides, like those of Proto-

drilus species, have lateral organs and spermducts, and the ultrastructure of the spermato-zoa is essentially the same in the two genera( Jouin-Toulmond and Purschke 2004). Fe-males are still unknown, but it is likely thatthe species has a planktonic larva like Proto-drilus species. This could explain the cur-rent geographical extension of the speciesthrough the Pacific Ocean (Mo‘orea inFrench Polynesia and the Hawaiian Islands).

Parenterodrilus sp.Figure 2

material examined. Hawai‘i, O‘ahu:West coast: One immature specimen col-lected from sand substrate off Wai‘anae,June 2004, at depths of 27–33.5 m, sedimentscomprised medium- to fine-grain carbonatesands. Specimen in J.B.-B.’s personal collec-tion at the University of Hawai‘i.

morphology. Only one immature speci-men was collected. Key feature is the dor-soventrally flattened body, wider than P.taenioides (about 3 mm long and 0.26 mmwide in this fixed unrelaxed specimen). Theother characters (segmentation, ciliated ce-phalic palps [Figure 2A,B,C,D], two-lobedpygidium [Figure 2E], and absence of amouth and functional gut) are similar to thoseof the type species, P. taenioides. Comparisonof the characteristics of Hawaiian specimens,especially the male specimens, with those ofspecimens from Mo‘orea would be useful.

Protodrilus albicans Jouin, 1970Figures 3, 4

material examined. Hawai‘i, O‘ahu:Kuhio Beach, Waikıkı, nine specimens, col-lected 12 October 2006. Clean medium- tofine-grain sands were collected as part of abeach nourishment study. Specimens depos-ited in mnhn (reference collection numberPNT 11, one male and one female); maturespecimens also in J.B.-B.’s personal collec-tion.

France: Mediterranean, Banyuls-sur-mer(type locality), coarse sand near the water’sedge of Le Troc beach.

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French Polynesia: island of Mo‘orea,coarse sand near the water’s edge of beaches,east part of Irioa; island of Tahiti at Vairao.Specimens deposited in mnhn (reference col-lection number PNT 12, two males and onefemale). Specimens on slides prepared byC.J.-T. also in J.B.-B.’s personal collection.

morphology. The morphology andwhite color of the preserved Hawaiian speci-mens are similar to those of the Mediterra-nean specimens, but the Hawaiian specimens

are smaller: up to 50 segments in the longestspecimens, 9 mm long and 0.22 mm wide.The shape and position of the three pairs ofprostomial sensory organs are the same as inthe Mediterranean specimens: in the most an-terior part of prostomium, two unpigmentedocelli that were previously called ‘‘statocysts’’(see Purschke 1990c) located near each other;two long (800 mm) ciliated palps reaching,when oriented posteriorly, the level of seg-ment four; and more posteriorly on the pro-

Figure 2. Parenterodrilus sp., specimen from west coast of O‘ahu (Hawai‘i). A, Entire specimen; B, anterior region; C,part of a palp showing cilia; D, segments of midbody region; E, posterior end with pygidial lobes turned down ven-trally. Scale bars: A, 100 mm; B, D, E, 50 mm; C, 10 mm.

Protodrilid Polychaetes from Hawai‘i and French Polynesia . Bailey-Brock et al. 467

stomium two well-developed dorsal ciliatednuchal organs not easily observed on thesefixed specimens. Epidermal glands are abun-dant all along the body, but the ‘‘bacillaryglands’’ as well as the general body ciliation,both easily seen in living animals, are moredifficult to identify on fixed specimens. Pygi-dium with two well-developed adhesive lobes

(Figure 3B). Along the esophagus, salivaryglands are present in the first nine to 10body segments (Figure 3A,C ).

Sexually mature specimens: All specimenscollected in October 2006 were sexually ma-ture. As in other species of Protodrilus, the go-nads are present in segments following theanterior ones that contain the salivary glands.

Figure 3. Protodrilus albicans. A–C: Specimen from Kuhio Beach (Hawai‘i). A, Anterior part of a fixed male, profileview (ciliation not represented); B, posterior part of body with pygidial lobes and ducts of adhesive gland cells; C, di-agram of a male showing localization of salivary glands up to segment 10, of gonads from segment 12, and of lateralorgans in segments 7 to 16. D: Specimen from Mo‘orea, lateral view of a trochophore larva. b, brain; m, mouth; mid,midgut; o, ocellus; p, palp; sg, salivary glands; ‘‘st,’’ unpigmented ocellus (so-called ‘‘statocyst’’); sto, stomodeum; v,valvula. Scale bars: A, 100 mm; B, 50 mm; D, 10 mm.

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In the females the gonads extend, on bothsides of the digestive tract, all along the bodyfrom segments 11 or 12 posteriorly, except inthe three to five prepygidial segments. Ineach mature segment there is a large number(40–60) of small mature oocytes (about 35mm in diameter).

In the males the gonads extend as in thefemales from segment 11 or 12 posteriorly;paired lateral organs are present in segmentseven (as a pair of small, round glandulardimples), and from segment eight to 16 aspaired continuous ciliated lateral grooves(Figure 3C ); the sperm ducts could not beobserved on these fixed specimens. The gen-eral morphology and the reproductive char-acters of the sexually mature specimens,

which are good specific characters in the ge-nus Protodrilus, are similar in the Hawaiianand Mediterranean specimens.

comparisons. The specimens collectedfrom the islands of Mo‘orea and Tahiti,French Polynesia, were sexually mature inJuly 1981. These specimens (Figure 4) aresmaller than the Mediterranean ones: thetotal number of segments ranges from 33to 43, and they are 6–7 mm in length and0.16 mm wide. In the anterior part of theprostomium, the Polynesian specimens havetwo pigmented ocelli on the external borderof each ‘‘statocyst.’’ Such pigmented ocelliare absent in both the Mediterranean andHawaiian specimens. The other features, es-pecially those of the mature specimens (fertile

Figure 4. Protodrilus albicans, photomicrographs of a live mature female specimen from Vairao (Tahiti). A, Dorsalview of head (one palp missing), peristomium with muscular pharyngeal organ, and first two body segments; B, lateralview of a fertile segment, showing the right coelomic cavity, limited by 2 septa (s), containing numerous small matureoocytes. Scale bars: A, 100 mm; B, 50 mm.

Protodrilid Polychaetes from Hawai‘i and French Polynesia . Bailey-Brock et al. 469

region extending from segment 11 to seg-ment 30 or 40, presence of numerous smalloocytes in females [Figure 4B], and extent oflateral organs [segments seven to 16] andpresence of four pairs of sperm ducts inmales), are in accordance with the descrip-tion of the Mediterranean specimens of P.albicans.

reproduction and larvae. Male andfemale specimens from Banyuls-sur-mer andfrom Mo‘orea kept isolated in laboratory con-ditions reproduced easily: several spermato-phores deposited by the males on sand grainsor on the substratum were taken up by the fe-male epidermis. As in other Protodrilus species( Jagersten 1952), spermatozoa from sperma-tophores crossed the epidermis and body wallof the females, reaching the coelomic cavities.Then fertilized mature females spawned clus-ters of eggs that became attached to the sub-stratum. Young swimming larvae appearedabout 10 hr later.

The hatching larvae, about 40 mm long,had the same morphology in both the Ban-yuls and Mo‘orea specimens. At this stage(Figure 3D), only one lateral pigmented ocel-lus and one ring of cilia forming the proto-troch are present in the young larva; 1 to 2days later, a second lateral ocellus and threeother rings of cilia at the prototroch areformed. The foregut (stomodeum) is orientedposteriorly. A remarkable element of thislarva is the ‘‘ameboid’’ valvula located in theforegut, at the connection with the midgut.A similar valvula was described for the firsttime in the larva of Protodrilus adhaerens(‘‘ameboid protuberance’’) by Jagersten(1952). In several other Protodrilus speciesthis valvula is composed of only a simple tuftof cilia. In P. albicans and P. adhaerens, ciliaare also present, embedded in the mobile pro-tuberance that allows swallowing of smallfood particles from the stomodeum into themidgut.

The similar size and number of coelomicmature oocytes in the Mediterranean, Poly-nesian, and Hawaiian specimens suggest asimilar larval development for the Hawaiianspecimens.

remarks. Protodrilus albicans was de-scribed from the Mediterranean. Populations

of morphologically very similar specimensare present in the Hawaiian Islands (O‘ahu,Kuhio Beach) and have also been collectedin Mo‘orea ( by C.J.-T.) in the same biotopeas in Banyuls-sur-Mer (i.e., in coarse sand ofbeaches near the water’s edge).

Most specific characters (general size andbody shape, extent of salivary glands, extentof gonads and lateral organs in males, num-ber and size of mature oocytes in each fertilesegment of females) are similar in the Medi-terranean, Polynesian, and Hawaiian speci-mens. Thus, for the time being, we considerthe Mediterranean and Pacific populations ofP. albicans as belonging to the same species.More detailed studies on live material, and ul-trastructural and molecular studies on thesedifferent geographical populations will benecessary to detect possible differences atsubspecies or species level.

discussion

Five Protodrilus species were collected in coralsands from Mo‘orea and Tahiti by C.J.-T.Two are undescribed species, and three arevery similar to European species: P. adhaerensJagersten, 1952; P. hypoleucus Armenante,1903; and P. albicans. These appear to be‘‘cosmopolitan species’’ previously knownfrom the Mediterranean (Naples, Banyuls-sur-mer) and the Northeast Atlantic (GullmarFjord, Channel, Roscoff ) (Westheide 1990).

Colonization of new sites along shorelinescould be accomplished by Protodrilus albicanswith a peculiar behavior of the species ( Jouin1970): live specimens from Banyuls-sur-Merwere observed emerging from the sedimentand swimming in the water above the sedi-ment, an uncommon behavior in protodrilids,which generally stick on sand particles whendisturbed. In addition, dispersal of the speciescan also occur by planktonic larval dispersion,a biological character common to all Protodri-lus species ( Jagersten 1952). In contrast, twospecies of the genus Protodriloides Jouin,1966, have a direct benthic development: thelarge yolky eggs develop into juveniles in acocoon attached to sand grains (Swedmark1954, Jouin 1962). Colonization of new sitesis then accomplished by dispersal of eggs in

470 PACIFIC SCIENCE . July 2010

cocoons, or adults, attached to grains of sedi-ment, as reported in the cosmopolitan speciesProtodriloides chaetifer (wrongly cited as Proto-drilus chaetifer in Sterrer [1973]).

The current wide geographical distribu-tion of the different ‘‘cosmopolitan species’’of Protodrilus can be linked both to the dis-persal by free-swimming larvae and to the an-cient age of this interstitial fauna. Severalauthors (Sterrer 1973, Westheide 1977) havesuggested that the interstitial fauna is veryold, and, as such, Protodrilus albicans and otherspecies of the genus found on coasts of theNortheast Atlantic, the North Sea, the Medi-terranean Sea, and in Pacific island groupscould be relict species of the Tethys Sea,which extended from the Caribbean to Indo-nesia via the Mediterranean during the Ceno-zoic, 65 million yr ago.

acknowledgments

We are most grateful to Andre Toulmond,Station Biologique Roscoff; Sue Monden,Zoology Department, University of Hawai‘i,for the illustrations in Figures 1 and 2; andalso to Xiufu Shuai, Water Resources Re-search Center, University of Hawai‘i, for pre-paring the final illustrations in electronicformat. We thank Alan Kam and the staff ofthe Wormlab, University of Hawai‘i, for col-lecting, sorting, and preserving the speci-mens. Thanks also to B. Salvat and the staffof the Antenne MNHN and EPHE (Ecolepractique des Hautes Etudes) for facilitiesand in the collection of material for labora-tory studies in Mo‘orea ( July 1973, July1981, February 1991).

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