Polydora colonia Moore, 1907

David, Andrew A. & Williams, Jason D., 2012, Morphology and natural history of the cryptogenic sponge associate Polydora colonia Moore, 1907 (Polychaeta: Spionidae), Journal of Natural History 46 (23 - 24), pp. 1509-1528 : 1512-1520

Polydora colonia Moore, 1907

( Figures 1–6 )

Polydora colonia Moore 1907: 199–201 , fig. 18–23; Hartman 1945: 32–33; Blake 1971: 15–17, fig. 10a–10l; Dauer 1974: 193, 193 (Table), 194, 195; Read 1975: 404; Blake 1983; 254–255; Aguirre et al. 1986: 375–377, fig. 1A–1G; Radashevsky 1993: 21, 23; Blake 1996: 180; Martin 1996: 170 (Table); Radashevsky 1996: 691; Martin and Britayev 1998: 244 (Table); Tena et al. 2000: 65 (Table); Ruellet 2004: 356; Neves et al. 2007: 323 (Table); Neves and Rocha 2008: 625 (Table), 626, 627 (Table); Orensky and Williams 2009: 234; Occhipinti-Ambrogi et al. 2010: 218, 221 (Table); Cangussu et al. 2010: 227 (Table); Zenetos et al. 2010: 395 (Table); Simon 2011: 39; David and Williams 2011: 1–10, figs. 1–4, Table 1.

Polydora hoplura inhaca Day, 1957: 468 , fig. 18.2N.

Polydora ancistra Jones, 1962: 185–187 , fig. 55–65.

Materials examined

USA, New York, Point Lookout, Town of Hempstead East Marina (40 ◦ 35’37.71" N, 73 ◦ 35’07.09" W) from the red beard sponge M. prolifera attached to floating docks, September and October 2007, September , October , November and December 2008, January and March 2009, coll. J. Williams ; July , September , October , November 2010, coll. J. Williams and A. David ( USNM 1156935 and USNM 1156936 ), 780 specimens examined from M. prolifera ; from crumb of bread sponge Halichondria bowerbankii from same location on November 2010, coll. J. Williams and A. David ( USNM 1196937 ), 60 specimens examined in total from H. bowerbanki . USA, Massachusetts, Woods Hole, Hadley Harbor from pilings, coll. J. Blake 1967 ( USNM 301179 ), 22 whole specimens, three regenerating specimens examined. Argentina, South Atlantic Ocean from sediment, coll. Oliver and Salanoure ( USNM 345346 ), 12 specimens examined. Spain, Malaga, Mediterranean Coast , coll. G. San Martin 14 June 1983 ( Museo Nacional de Ciencias Naturales , MNCN 16.01/10720), one specimen regenerating posterior end; Mediterranean Coast coll. G. San Martin 29 April 1983 ( MNCN 16.01/10706), two posterior ends and two middle pieces.

Adult morphology

Largest specimen 8 mm in length and 51 chaetigers. In life, body light yellow with pigmentation absent in mature worms; preserved specimens white in colour. Eyes absent in adults except for one 24-chaetiger worm with two pairs of eyes. Prostomium rounded anteriorly to slightly bifid extending posteriorly as a short caruncle to the middle of chaetiger two, nuchal organ as ciliary band on either side of caruncle ( Figure 1A,B ). Palps long, extending posteriorly for approximately 13 chaetigers on adult specimens ( Figures 1A , 2A ), palps with frontal cilia lining food groove and nonmotile cirri on papillae along lateral edges of food groove and scattered on abfrontal surface; presence of laterofrontal cirri not confirmed ( Figure 2B ).

Chaetiger 1 with neurochaetae; without notochaetae. Capillary notochaetae of chaetigers 2, 4, 6 and subsequent chaetigers in three successive rows, two vertical and one row positioned dorsally, posterior seven chaetigers with stout boat hooks except for specimens regenerating posterior ends ( Figures 1C,G , 2E,F ); generally two boat hooks per chaetiger and typically accompanied by two capillary chaetae, hooks variable in curvature from slightly curved tip to highly curved ( Figure 2E ). Capillary neurochaetae of chaetigers 2–4, 6 and subsequent chaetigers in two vertical rows. Hooded hooks begin on chaetiger 7 and extend to posterior chaetigers with three to five hooks per chaetiger, hooded hooks bidentate with large distal fang and smaller secondary tooth; shaft with manubrium and tapering to the base ( Figure 1F ). Glandular pouches in chaetigers 7–10, with largest glands from chaetiger 9–10; glands opening to exterior through small papillae ventral to rows of neurochaetae.

Chaetiger 5 modified; approximately twice the size of chaetigers 4 and 6, with three or four major modified spines decreasing in size posteriorly, each with a small and large apical tooth distal to a subterminal collar ( Figures 1D , 2C,D ), major spines alternating with pennoned companion setae; with dorsal fascicle of three capillary notochaetae ( Figures 1E , 2C,D ) and ventral fascicle of two capillary neurochaetae.

Branchiae from chaetiger 7 or 8, reaching maximum size on chaetiger 14, decreasing in size posteriorly ( Figures 1A , 2A ). Pygdium cup shaped with dorsal gap ( Figures 1B , 2E,F ). Table 1 summarizes major taxonomic features in P. colonia from geographical regions where it has been described and the distribution of the species is shown in Figure 3 .

Ecology and feeding biology

On Long Island, New York, P. colonia was found on the red beard sponge, M. prolifera and the crumb of bread sponge, H. bowerbanki . Polydora colonia and its sponge host, M. prolifera appear in the shallow subtidal area on pilings and floating docks approximately in late June. The worms reach densities as high as 7.9 ± 1.4 worms/mm 3 (n = 16) by mid-July to early August. Sponge colonies increase during September and October but are almost non-existent during the winter months (late December to February) when the host sponge ( Figure 4A,B ) can only be collected in the lower subtidal areas. Worms produce tubes on the surface of the sponge by cementing detritus material together with mucus; the worms can also extend their burrows into the tissue of the host sponge. The tubes can be intertwined to form compact masses; average length of a single tube was 0.97 ± 0.21 cm (n = 20). Heavily colonized sponges ( Figure 4B ) can have more than 200 individual tubes on the surface of a 100-cm 2 sponge branch. In this study, M. prolifera also harboured gammarids ( Corophium sp. ), sabellid worms ( Sabella sp. ), nereid worms ( Nereis sp. ) and scaleworms ( Lepidonotus sp. ). Polydora colonia was the dominant polychaete worm inhabiting M. prolifera ; the only other spionid associated with the host sponge was Dipolydora socialis (Schmarda 1861) .

Gut contents of P. colonia were typically yellow to orange in appearance ( Figure 4C ). Materials from the gut included sand grains and partially digested sponge and spicules ( Figure 4D ). Around half (53 of 100) of the worms examined contained sponge, as evidenced by spicules and/or sponge material, in their gut and half of them (50 of 100) had sand grains in the gut. No sponge material was found in individuals associated with H. bowerbanki .

Reproduction

Mean number of chaetigers in complete (non-regenerating) adult worms was 30 ± 6 (n = 552). Ovigerous chaetigers begin as early as chaetiger 12 (14 ± 1.2; n = 30) and end as early as chaetiger 20 (25 ± 3.2; n = 30) with eggs crowding the coelomic spaces. Egg capsules and larvae of P. colonia were found in all months sampled. Egg capsules are arranged in a string attached to the inside of the mucous tubes by double filaments. Extracted egg strings had a mean number of egg capsules per string of 7 ± 2.9 (n = 30); however, complete strings were difficult to extract and these probably represent incomplete strings. Mean number of eggs per capsule was 15 ± 3 (n = 30). Based on the average number of ovigerous chaetigers and eggs per capsule, the total fecundity of P. colonia is estimated to be 165 eggs per brood. Mean egg diameter was 121.0 ± 16.0 µm (n = 100).

Of the 30 egg strings examined, 10% showed evidence of adelphophagia. Adelphophagic larvae were observed at the six- and seven-chaetiger stage. In one egg string about 25 nurse eggs were consumed by a single larva. Eggs were consumed whole by the larva and were broken down in the gut approximately 2–3 minutes after ingestion.

The earliest free-swimming larval stage found was a seven-chaetiger larva, 0.5 mm in length containing a large amount of yolk, presumably from ingestion of eggs ( Figure 5A ). Head of larva rounded with two pairs of eyes, with lateral eyes approximately twice the size of medial eyes. Prototroch divided and well developed. Melanophores present on chaetigers 4, 5 and 6 and pygidium. Chaetae as long bristles, longest in chaetiger one and decreasing in length posteriorly.

The 13-chaetiger larva (1 mm in length) was already settled on the surface of the sponge ( Figure 5B ). Prostomium rounded with two pairs of eyes; lateral eyes larger than medial. Palps long and flexible; caruncle absent. Pigmentation in irregular patches on most chaetigers. Nototrochs present on segments 2 and 3, lacking on segment 5. Chaetiger 5 well differentiated but major spines not visible externally. Lipid reserves restricted to the posterior region, from chaetigers 9 to 13. Pygidium rounded.

Asexual reproduction via architomy (fragmentation of the worm into an anterior and posterior end and subsequent regeneration to form two individuals) was commonly observed in the field based on specimens from New York ( Figure 5C ). This is the first record of architomy in the genus Polydora . In addition, architomy was observed in 12% (three of 25) of the specimens from Massachusetts and in the specimens from Spain. Morphogenesis during architomy and impacts of temperature on regeneration in specimens of P. colonia are reported separately ( David and Williams 2011).

Symbionts

A species of ciliate of the genus Urceolaria (diameter 46 µm) was found attached to specimens of P. colonia . Ciliate prevalence was 25% (25 of 100) on the adult worms examined. The disc-shaped ciliate was found attached to the palps, anterior and posterior chaetigers and pygidium ( Figure 6A ). The basal disc of the ciliates had a band of radiating ribs ( Figure 6B ) and three or four concentric rings around the middle portion of the main body of the ciliate ( Figure 6C ). Specimens that harboured Urceolaria did not appear to be affected negatively compared with uninfected worms (e.g. females with eggs harboured the ciliates).

One endoparasitic copepod larva of the genus Cymbasoma , 1-mm in length ( Figure 6D ), was found inside the coelom of an incomplete worm at about chaetiger 14. Prevalence of Cymbasoma was 1% (1 of 100) in the worms examined. The larva of Cymbasoma possessed two pairs of antennae; one central pair of fused antennae and one non-fused pair ( Figure 6D,E ). The abdominal region is tubular and segmented, characterized by a protective sheath (0.5 mm in length), which encloses the thoracic appendages ( Figure 6F ). The protective sheath terminates in a cone with multiple vertical rows of short, blunt extensions.

Figures

Figure 1. Polydora colonia, adult morphology based on light microscopy (USNM1156935, 1156936, 1156937). (A) Anterior end, dorsal view showing ciliates (arrow) attached to chaetigers 5, 6 and 7. (B) Anterior end, lateral view. (C) Posterior chaetigers and pygidium, dorsal view showing curved boat hooks. (D) Notochaetae from chaetiger 5. (E) Three modified fifth chaetiger spines with companion chaetae. (F) Bidentate hooded hooks from chaetiger 10. (G) Two boat hooks from the posterior end. Scale: 250 µm (A); 100 µm (B, C); 25 µm (D–G).

Figure 2. Polydora colonia, adult morphology based on scanning electron microscopy. (A) Overview of P. colonia. (B) Ventral view of palps showing the food groove lined by frontal cilia (fc) and papillae (pa). (C) Fifth chaetiger showing modified spines (arrow). (D) Single fifth chaetiger spine and dorsal fascicle of notochaetae. (E) Posterior end of worm showing cupshaped pygidium along with boat hooks of varying curvature. (F) Posterior end and pygidium showing boat hooks on posterior chaetigers. Scale: 500 µm (A); 50 µm (B); 100 µm (C); 25 µm (D); 200 µm (E, F).

Figure 3. Map showing worldwide distribution of Polydora colonia. References for records: 1, Moore 1907, Blake 1971; 2, present study; 3, Hartman 1945; 4, Dauer 1974; 5, Jones 1962; 6, Radashevsky unpublished; 7, Neves and Rocha 2008, Cangussu et al. 2010; 8, Blake 1983; 9, Day 1957; 10, Aguirre et al. 1986, Tena et al. 2000, Zenetos et al. 2010, Occhipinti-Ambrogi et al. 2010.

Figure 4. Polydora colonia and its sponge host Microciona prolifera. (A) Uncolonized branch of Microciona prolifera. (B) Colonized branch of M. prolifera showing the network of worm tubes on surface of the sponge. (C) Regenerating adult worm with gut containing sponge material. (D) Gut contents showing orange sponge material and two sponge spicules (arrows). Scale: 10 mm (A, B); 200 µm (C); 50 µm (D).

Figure 5. Polydora colonia, larvae and individual regenerating after architomic division. (A) Seven-chaetiger larva, dorsal view. (B) 13-chaetiger larva that settled on the sponge, dorsal view. (C) Individual with four original segments regenerating anterior and posterior ends. Scale: 100 µm (A); 250 µm (B, C).

Figure 6. Symbionts of Polydora colonia, scanning electron micrographs. (A) The ciliate Urceolaria sp. attached to the posterior end of a regenerating worm. (B) Oblique lateral view of oral surface of Urceolaria sp. showing main ring. (C) Lateral view of Urceolaria sp. showing the oral (or) and aboral (ab) region. (D) Overview of the parasitic copepod Cymbasoma sp. with one pair of non-fused antennae (arrowhead showing intact non-fused antenna and arrow showing point of attachment of the second non-fused antenna) and one pair of fused antennae (fu). (E) Abdominal region showing protective sheath that houses the thoracic appendages, arrow pointing to posterior end of the sheath. (F) Lateral view of non-fused antenna. Scale: 100 µm (A); 40 µm (B, C); 500 µm (D); 200 µm (E, F).