Bijdragen lot de Dierkunde, 60 (3/4) 215-224 (1990)
SPB Academie Publishing bv, The Hague
Host utilization during ontogeny by two pycnogonid species
(Tanystylum duospinum and Ammothea hilgendorfi) parasitic on the
hydroid Eucopella everta (Coelenterata: Campanulariidae)
David J. Russel postscript: Joel W. Hedgpeth
1 2 1629 Notre Dame Drive, Mountain View, CA 94040, USA; 5660 Montecito Ave., Santa Rosa, CA
95404, USA
Keywords: Pycnogonids, host, hydroids, ontogeny, Monterey Bay
Abstract along the rocky California coast. Of such hydroids
the Ostrich plume hydroid Aglaophenia struthio-
The calyptoblast hydroids Aglaopheniastruthionides (Murray, nides(Murray, 1860) attracts several species includ-
1860), Eucopella (= Campanularia) everta (Clark, 1896), and ing Pycnogonum stearnsi Ives, 1892, Tanystylum
Abietinaria spp. in the low intertidal zone at Mussel Point, Pa- spp., Achelia spp., Nymphopsis spinosissima cific often bear the adult Grove, Monterey Bay, California, pyc- (Hall, 1912), and Ammothea hilgendorfi (Böhm, nogonids Tanystylum duospinum Hilton, 1939 and Ammothea 1879). At Mussel Point, Pacific Grove, adults of hilgendorfi (Böhm, 1879). Larval stages of these pycnogonids
were found living and feeding on Eucopella everta. The larvae the sea spider Tanystylum duospinum Hilton, 1939
of Tanystylum duospinum are ectoparasitic. Those of Am- found are frequently on the hydroid Aglaophenia
mothea hilgendorfiare endoparasitic in the gastrovascular cavi- struthionides, and less often on other hydroids,
ties of hydranths. Larvae of both species feed on the gut con- bryozoans, and tunicates. Adults of the pyc- tents of Eucopella everta, often on the same hydroid colony. nogonid Ammothea hilgendorfi, less abundant at
Mussel Point during this study, were found on the
Résumé hydroids Eucopella everta (Clark, 1896), Aglao-
and Abietinaria Larval phenia struthionides, spp.. Les Hydroïdes calyptoblastes Aglaophenia struthionides (Mur- stages of both pycnogonid species were found only ray, 1860), Eucopella(= Campanularia)everta (Clark, 1896) et often the colonies. on Eucopella everta, on same Abiet inaria spp., sont souvent parasités par les Pycnogonides The occurrence of two similar forms undergoing adultes Tanystytum duospinum (Hilton, 1939) et Ammothea hil-
larval on the same substrate gendorfi(Böhm , 1879) dans la zoneintertidale inférieure à Mus- development provided
Les sel Point, Pacific Grove, Monterey Bay, Californie. stades an opportunity to make comparisons of the mode larvaires de ces Pycnogonides ont été trouvés vivant et se nour- of parasitism and to examine the possibilities of rissant sur Eucopella everta. Les larves de Tanystytum duospi- resource partitioning. num sont ectoparasites. Les larves d’Ammothea hilgendorfi sont endoparasites dans les cavités gastrovasculaires des
Les hydrants. larves des deux espèces se nourissent du contenu
d’ digestif Eucopella everta, souvent sur la même colonie Materials and methods d’Hydroïdes.
All material was collected from low intertidal areas
at Mussel Point, Pacific Grove, Monterey Bay,
Introduction California, between 18 April and 30 May, 1980.
Hydroid colonies were generally collected from red
Several of species pycnogonids are found associat- algae (Prionitis, Gastroclonium, and Gigartina ed with colonies in the low intertidal from hydroid zone spp.), but occasionally rocks. Both homo- 216 D.J. Russel - Host utilization during ontogeny by two pycnogonid species
of geneous hydroid clusters (colonies consisting a regained the substrate. A larva dislodged in a cur-
clusters in and single species) and heterogeneous (consist- rent was swung an arc, rapidly regained a
the substrate. ing of two or more species growing closely together) foothold on
both and later Undisturbed larvae found were kept separate during collecting protonymphon at-
back the in the laboratory. Samples brought to tached to Eu. everta as notedabove, were often ob-
observed while Some colo- inserted the laboratory were fresh. served to have the proboscis through
for week without and wall into the coelen- nies were kept up to one feeding, perisarc body hydroid in aquaria and finger bowls with constantly running teron. In one such individual, observed over a ten
time seawater at approximately 14°C, during which minute period, feeding was seen to be suctorial. Ex-
observations made. additional were pansion of the pycnogonid's gut from anterior to
Identification of larval Tanystylum duospinum posterior caused fluid to be drawn from the hy-
made the found into into was by arranging stages a con- droid's coelenteron the pycnogonid. After a tinuous developmental series, and then working variable length of time a contraction of the pyc- backwards from the adult. The earliest larval form nogonid gut, starting at the posterior and moving observed possessed threepairs of larval appendages anteriorly, forced much of the ingested material and lacked any adult walking legs. back into the hydroid coelenteron.The process was
repeated at irregular intervals. More advanced lar-
vae (stages V and VI of Dogiel, 1913) possessing
Results their first and second pairs of walking appendages
and an unpigmented exoskeleton (Figs. 1 & 2) were
in Tanystylum duospinum Hilton, 1939 foundattached to the host hydroid the same sorts
is feed in Tanystylum duospinum a small, inadequately of places and appeared to the same manner. known species found mostly on hydroids. It is simi- T. duospinum with three and four pairs of walking lar in habit to T. californicum Hilton, 1939, a more legs and a clear exoskeleton was not observed feed- conspicuous species because of its heavier pigmen- ing, nor was an attachment thread seen in these tation. is central Califor- It so far known from the stages.
Adult The of T. found nia coast. Tanystylum duospinum were most advanced stage duospinum found most abundantly on fronds of Aglaophenia on Eu. everta had a maximum leg span of only 4 struthionides, but were collected from a variety of mm, still possessed functional cheliforesand a clear substrates including the hydroids Abietinaria and exoskeleton, and had an incompletely developed
Sertularella, a tunicate Archidistoma sp., and an fourth pair of walking legs. This corresponds close- arborescent bryozoan. Females with developed ly with the earliest stage of T. duospinum foundon
in their struthionides. eggs legs and males carrying egg masses Aglaophenia Larger T. duospinum
males with four of and were occasionally found. No carrying pro- fully developed pairs walking legs tonymphon larvae were seen. a leg span of up to 10 mm were found on A.
Protonymphon larvae with clear exoskeletons struthionides, Abietinaria, and Sertularella but were found, firmly attached by the grip of the two were not found on Eu. everta. The small eight-
while chelifores, on the stolons, stalks, and hydrothecae legged individuals were light straw in color, of When darker Eucopella everta. larvae were gently the larger specimens were a golden brown
from the the of the fouled pulled substrate, breaking grip and were occasionally by epiphytes. chelifores, they retained a connection with the hydroid via a thread formed by secretion of the ce- Ammothea hilgendorfi (Böhm, 1879) ment gland. The thread,which may be at least twice This species, formerly known along the California the length of the larva, acts as a safety line, prevent- coast as Lecythorhynchus marginatus Cole, 1904
the animal from from the substrate north Pacific ing being swept (or hilgendorfi) occurs along the if the chelifores lose their grip. In still water a larva shores from China and Japan, southern Alaska and was observed to slowly ascend the line, until it Washington, and along the California coast as far - 217 Bijdragen tot de Dierkunde, 60 (3/4) 1990
Fig. 1. Tanystylum duospinum, larva (stage V, Dogiel 1913), ventral view.
Fig. 2. Tanystylum duospinum larva (stage VI, Dogiel 1913), dorsal view. ,
Fig. 3. Ammothea hilgendorfi, larva (stage IV, Dogiel 1913) encysted in hydranth of Eucopella everta.
Fig. 4. Ammothea hilgendorfi, larva (stage V, Dogiel 1913), encysted in Eucopella everta.
south as Baja California, but not in the Gulf of species of the California intertidal zone as well as
California (Child, 1979). It is the largest intertidal Japanese shores". It is most oftenfound associated species on the California coast and is considered by with various hydroids, but also occurs in crevices,
Hedgpeth (1975) to be "one of the characteristic under stones, and in algal holdfasts. In Japan A. 218 D.J. Russel - Host utilization during ontogeny by two pycnogonid species
Fig. 5. A. hilgendorfi,larva (stage uncertain) attached to deteri- Fig. 6. A. hilgendorfi, larvae (sameas Fig. 9), double infestation
orating hydranth of Eucopella everta. Legs consisting of three of a single Eucopella everta hydranth.
pairs of stubs without extensions of the gut.
hilgendorfi has also been implicated as a possible the chelifores, directed forward, held the pyc-
of holothurian with ectoparasite a (Ohshima, 1927).* nogonid in place. Slightly larger pycnogonids
The earliest developmental stage ofA. hilgendor- longer legs (stage V of Dogiel, 1913) were also fi was observed in large galls derived from hy- found in an identical orientation (Figs. 4, 5).
dranths of Eucopella everta. Both hydranth and At the next observed stage the capsule, and often
parasite were encased in a capsule attached within most or all of the hydrotheca and hydranth of the
the but outward The three original hydrotheca, extending infected hydroid were absent (Fig. 9).
considerably beyond the hydrothecal margin (Fig. pairs of walking legs of the now exposed pycno-
Each contained small which 3). hydranth a pycnogonid gonid were present as stubs no longer con-
with tained the branches of the in the (stage IV, Dogiel, 1913) a proboscis, cheli- gut seen two
cerae, a small pair of appendages, and three pairs preceding stages. Occasionally two pycnogonids at
of short walking legs. The gut was clearly branched. this stage were found at theend of a single hydroid
Within the hydranth the pycnogonid proboscis was stalk (Fig. 6).
of inserted into the coelenteron the hydroid stalk, In the next developmental stage the pycnogonid's
These walking legs were well developed (Fig. 7).
legs still lacked extensions of the they waved * gut; A few years ago Stock (1979) described a species of slowly in walking motions similarto thoseof a nor- Anoplodactylus from an ophiuroid from Aldabra collected by
Sloan mal adult this (1979), and a few years later he described a species of Pyc- pycnogonid. Pycnogonids at stage
nosomia the from an asteroid in Philippines (Stock, 1981).Thus were also found in double infections, occasionally
Jan Stock has contributed to our knowledge of pycnogonid in- sharing a stalk with a pycnogonid at the previously
festation in two of the five major classes ofechinoderms; the re- described stage. cently discovered deep sea class Concentricycloidea seem unlike- The last pre-adult stage seen was found detached ly sustenance for pycnogonids, but they will probably show up
on crinoids. [J.W.H.] from the stalk, and walking slowly over the stolons, Bijdragen tot de Dierkunde, 60 (3/4) - 1990 219
Discussion
It has long been known that pycnogonids prey upon
hydroids, and that some species invade hydranths
and their as larvae encyst during early developmen-
tal stages, forming a sac or gall in the process.
Often several species of pycnogonids have been
recorded from the same species of hydroid (not
necessarily at the same time), and some pyc-
nogonids are associated with several species of
hydroids (see tabular summary of Heifer &
Schlottke, 1935: 198-199). Dogiel (1913: 617, 685)
thought he observed two species of pycnogonids
the forming similar galls on same hydroid colony at
this doubted Lebour the same time, but was by
(1916). Most of the observations of hydroid galls
and other varieties of pycnogonid infestation of
coelenterates have been incidental to studies of pyc-
nogonid development, with little attention paid to
the hydroids, other than as fortuitous culture media
for embryological studies.
Despite the early observations of the phenome-
Beneden Allman non by Van (1844), (1859), Hodge
(1862), Semper (1874), Dohrn (1869), and the more
detailedobservations of Hallez (1905) and Dogiel
(1913), there is very little informationabout the ex- Fig. 7. A. hilgendorfi larva VII, Dogiel 1913), attached , (stage act nature of the modifications of the hydranths to remnant of Eucopella everta hydranth by chelifores; distend-
caused by infestation ("parasitism") of larval pyc- ed gut extending into the chelifores but not into the three pairs
of walking legs. nogonids (although Hallez suggested that the
process is analogous to gall formation in plants),
and no considerationhas been given to the different
impact of potentially competing species on the
same species of hydroids. Unpublished notes and stalks, and hydrothecae of the Eu. everta colony. drawings by Martin D. Burkenroad (communicated
The three pairs of walking legs still lacked exten- by J.W. Hedgpeth) made in Bermuda in 1942 of sions of the and the chelifores formation gut, were now gall by Anoplodactylus petiolatus achelate. (Kroyer, 1845) in Clytia sp. indicate that the gall
Active feeding of the encysted pycnogonid on the tends to resemble a gonangium.
observed. direct The infestation of coelenterates larval hydroid was not However, a con- by pyc- nection between the pycnogonid and hydroid gut nogonids has not been observed, or at least noticed, was demonstrated in live whole-mount prepara- very frequently in North Pacific waters. Hilton tions. Pressure on the pycnogonid forced a flow of (1916) observed the infestation of early stages of fluid from the into the coelenteron of 1904 in Tubularia gut directly Anoplodactylus erectus Cole, the hydroid stalk. Pressure on the stalk caused fluid crocea (L. Agassiz, 1862) and remarks that the lar- to flow back into the pycnogonid gut. In neither vae "were very abundant in the digestive cavities of
there of fluid four case was any leakage at the junction nearly every polyp. In some cases three or of host and parasite. might be found in one place." The manner of in- 220 D.J. Russel - Host utilization during ontogeny by two pycnogonid species
Fig. 8. Colony of Eucopella. Drawing by G.H. Hilgard, from Abbott (1987).
festation was not observed in adequate detail. In a son (1986) have indeed surmised that infestation later paper Hilton (1934) remarks casually that may occur when medusae are resting or spawning
"Specimens of the hydroid Syncoryne from on the bottom, and that benthic pycnogonids may
Washington near Friday Harbor show immature then be able to attach to jellyfish. This suggestion
of specimens some species within the coelenteric was made to account for infestationof bathypelag-
These observations do ic for cavity." not appear to have scyphozoans, but seems even more plausible been repeated. The most remarkable infestation is such neritic forms as Polyorchis. that of the anthomedusan of of Polyorchis penicillatus Only 13 the approximately 700 species pyc-
(Eschscholtz, 1829) by larvae of Acheliaalaskensis nogonids have previously been observed feeding
(Cole, 1904) in Japan (Okuda, 1940). In this case while on a host organism (King, 1973). The host it- the pycnogonids are apparently ectoparasitic as lar- self may be the food source, being parasitized vae, adhering to the outer surface of the manu- (Allman, 1862; Dogiel, 1913; King, 1973) or preyed brium. This association is remarkablebe- especially on (King, 1973), or the host may simply provide a cause the polyp stage of Polyorchis is as yet surface from which food such as small attached unknown, and the manner in which a benthic or- plants, animals, microorganisms, or detritus is ob- ganism like a pycnogonid can infest a free swim- tained.
surmised. is ming medusa can only be Polyorchis The present study shows that the early develop-
Child Harbi- mental and common in the Monterey Bay area. & stages of Tanystylum duospinum Bijdragen tot deDierkunde, 60 (3/4) - 1990 221
9. of Fig. Study notes protonymphonstage of Tanyslylum duospinum by Donald P. Abbott, from Abbott (1987: 365, 367, rearranged). 222 D.J. Russel - Host utilization during ontogeny by two pycnogonid species
Acknowledgements
I am indebted to Stanford University for making such a course
as Biology 176H possible, and to my fellow students in the
course who contributed much to making it a pleasant and
memorable learning experience. I wish to thank Dr. Joel W.
Hedgpeth for advice and help in preparing this paper and with
the literature. My greatest debt is to the late Professor Donald
P. Abbott, who followed this study with energy and interest and
recommended publication, and I dedicate this paper to his
memory. David J. Russel
I thank Galen Howard Hilgard for permission to use her
drawing of the Eucopella colony, and to the Stanford University
Press for permission to use this and other material from Don
Abbott's "Observing marine invertebrates." I also thank Dr.
H. I Edmund Smith for assistance with photography. am
pleased that it has been possible to include this evidence of the
interaction between student and professor to honor Jan Stock,
who in a distant land has also labored valiantly in the cause of
classical zoology. Joel W. Hedgpeth
Postscript
This paper by David Russel was developed from his project
during the Spring Quarter of 1980 when he was enrolled in
Donald P. Abbott's (1920-1986) famous course in invertebrate
zoology that emphasized the functional morphology of the
animals living in the Monterey (California) tidal zone. Classes
lasted all day, often starting with anearly morning low tide trip,
and the rest of the time in the laboratoryobserving the animals,
of of Ser- Fig. 10. Infestation of Anoplodactylus sp. a species alive if possible. Don stayed with his students, often in the back
tularia, Bermuda, 1936. After a drawing by Martin D. Bur- of the room, working with the same animals brought in by the kenroad. students, and lecturing as the occasion demanded. It was inver-
tebrate zoology as seldom taught these days, and it cannever be
done just that way again, with its emphasis on "asking the Ammothea feed from the hilgendorfi directly gut animals", and his warning to "cultivate a suspicious attitude contents of the hydroid Eucopella everta. Both spe- toward people who do phylogeny." cies of pycnogonid often occur on the same hydroid A selection ofDon's informal,annotated drawings made dur-
The ing the class sessions, together with a few by his students were colony. early developmental stages of T. gathered together during his last days and published in com- duospinum are ectoparasitic, while those of A. hil- memoration of his course and his way of teaching (Abbott, gendorfi are endoparasitic. While adults of neither 1987). The sketch of Eucopella, illustrating the nature of this species were seen to feed, adults of T. duospinum small, dainty hydroid (Fig. 8) is by his student, later his assis-
were found in abundance Galen Howard is odd that these minute on only one substrate, tant, Hilgard. It dainty,
colonies, located on such ephemeral substrates the thalli of Aglaophenia struthionides, a hydroid whose color as
seaweeds should be hosts to two different pycnogonids, one in- is matched by the color of the adult pycnogonid. festing the hydranths to form galls, the other attacking from the By adopting different strategies (ecto-, and en- outside, but both living as adults in very different situations in doparasitism) while employing basically similar the tidal zone.
suctorial methods T. and A. feeding duospinum Abbott's drawings of the protonymphon larva of the ecto-
parasitic Tanystylum a structure not observed hilgendorfi effectively divide a given hydroid col- duospinumreveal
before in this larval stage of other species: the flat, paddle-like ony into two non-overlapping resources for food
surfaces on the ventral distal part of the legs (see Fig. 9). It has and space, and thus avoid competition. long been known that the protonymphon varies in different spe-
cies; some have long thread-like whips at the ends of the two - 223 Bijdragen tot de Dierkunde, 60 (3/4) 1990
In: pairs of larval legs and in others the filament extends from the Burkenroad, M.D., 1939. Hydroids on pelagic Sargassum.
no struc- Quantitative observations on the pelagic Sargassum vegeta- large spine at the base of the chelifores, or there is such
fig. 20). It has been tion of the western North Atlantic. Bull. Bingham ture at all (see Arnaud & Bamber, 1987: 41, oceanogr.
6: 23-25. considered that the protonymphon larva is not very motile, but Coll.,
its host, and Child, C.A., 1979. Shallow-water Pycnogonida of the Isthmus clings tothe egg mass at birth and somehow gets to
coasts Smithson. 1 have been guilty of conveying this idea as fact in Hedgpeth& of Panama and the of Middle America.
1-86. more Zool., 293: i-v, Haderlie (1980). This has been picked up and made even Contr.
association be- dogmatic by Salazar-Vallego & Stock (1987). Abbott did not Child, C.A. & G.R. Harbison, 1986. A parasitic
to label structures when tween pycnogonid and a scyphomedusa in midwater. J. label this structure; it was not his habit a
biol. Ass. 66: 113-117. he did know what they were rather than provoke misunderstand- mar. U.K.,
coast of North ing. He also did not label the unique gland peculiar to the pro- Cole, L.J., 1904. Pycnogonida of the West
Harriman Alaska 10: tonymphonthat supplies the duct in the spine at the base ofthe America. Exped., 249-330, pis.
he is XI-XXVI. chelifore; if there was a duct did not see it, but it possible
surface which V.A., 1913. Studien an Pantopoden. Z. it may have been replaced by a porous ventral Dogiel, Embryologische
107 XVII-XXII. would have made the paddle-like structures possible. In any wiss. Zool., (4): 575-741, pis.
1869. Ueber und Bau der event he did comment on the active movement of the larval ap- Dohrn, A., Entwicklung Pycnogo-
V-VI. pendages both forward and backwards, in "broad sweeping niden. Jena. Z. Med. Naturwiss., 5: 138-157, pis.
threads Observations le des larves de movements" that suggest swimmingability. Attachment Hallez, P., 1905. sur parasitisme
Phoxichilidium chez Archs. Zool. exp. gén., may be developed after the larva finds its host [for an obituary Bougainvillea.
3: pl. VI. of Donald P. Abbott, see Newberry & Hadfield, 1987]. (4) 133-144,
1975. In: S.F. Another promising location for studies may be Bermuda. In Hedgpeth, J.W., Pycnogonida. Light (ed.) (re-
Intertidal invertebrates May of 1936 Martin D. Burkenroad made some preliminary vised by R.I. Smith & J.T. Carlton),
California 201-210 of studies of pycnogonid infestation of hydroids (mostly on float- of the central coast: (University
drafted ing Sargassum). He made many drawings and some text, California Press, Berkeley).
J.W. Haderlie, 1980. Pycnogonida: the sea mostly speculation on the nature of the parasitism involved. Un- Hedgpeth, & E.C.
his had time and In: R.H. Morris, D.P. Abbott & E.C. Haderlie fortunately papers at some got very damp, spiders.
had rusted and stained the and the (eds.), Intertidal invertebrates of California: 636-640 (Stan- paper clips pages drawings
were damaged. His observations had stimulated him to some ford University Press, Stanford). preliminaryspeculations that parasitism by pycnogonidscaused Helfer, H. & E. Schlottke, 1935. Pantopoda. Bronn's Kl. Ordn.
resemble the of 5 1-314. galls in calyptoblast hosts to gonangium gym- Tierreichs, (4) (2):
noblast hydroids, and that the formation of such galls required Hilton, W.A., 1916. The life history of Anoplodactylus erectus
Pomona 8 25-34. deep invasion to regions of active growthby the pycnogonid lar- Cole. J. Ent. Zool. Coll., (1):
Russel has stated 1934. Notes on parasitic [sic] from vae. Unfortunately little more than what can Hilton, W.A., pycnognids
of California. J. Ent. Zool. Pomona 26 be made of this material. There is, however, a retrievable draw- the shores Coll., (4):
of infestation in a of Sertularia which is not one 57. ing an species ,
of the hosts usually encountered in these studies (Fig. 10). Mor- Hodge, G., 1862. Observations on a species of pycnogon (Phox-
an explain order ris & Mogelberg (1973) list ten species of Sertularia associated ichilidium coccineum). With attempt to the
9: 33-43. with Sargassum in Bermuda, but Burkenroad (1939) mentioned of its development. Ann. Mag. nat. Hist., (3)
King, P.E., 1973. Pycnogonids: 1-144 (Hutchinson, London & only two. The species illustrated here from his drawing seems to
be Sertularia inflata (Versluys, 1899) [for anobituary of Burken- St. Martin's Press, New York).
on life history of Anaphia road, see Schram, 1986]. Lebour, M.V., 1916. Notes the
Ass. petiolata (Kröyer). J. mar. biol. U.K., 11 (1): 51-56.
Morris, B. & D. Mogelberg, 1973. Pycnogonida. In: Identifica-
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