Bathybdella sawyeri

source: researchgate

The deep-sea fish leech Bathybdella sawyeri Burreson has recently been collected from two sites on

the South East Pacific Rise at approximately14° and 17°S, 2623–2586 m depth. Leeches were

obtained from washings of vent mussels Bathymodiolus thermophilus (Mytilidae) and clams

Calyptogena magnifica (Vesicomyidae) collected with a grab by a submersible, or were found attached

to the cheliped of the crab Cyanagraea praedator (Bythograeidae) collected in baited traps at 14°S.

Most individual leeches had morphology typical of B. sawyeri as originally described, with suckers of

approximately equal size, but all specimens collected from the crab C. praedator had unusually large

oral suckers that were distinctly larger than the caudal sucker. However, internal morphology of the

specimens from C. praedator was identical to B. sawyeri on the basis of serial sections; thus all

specimens were identified as B. sawyeri. The only previous report of B. sawyeri is from the Galápagos

Rift, so these collections extend the range to the South East Pacific Rise.

Introduction

Bathybdella sawyeri Burreson was described from material collected on the first Galápagos Rift

Biology Expedition in the eastern Pacific Ocean in 1979 (Burreson 1981). Most specimens collected

have been found free in washings from clumps of mussels Bathymodiolus thermophilus Kenk & Wilson

(Mytiloida: Mytilidae), the clam Calyptogena magnifica Boss & Terner (Veneroida: Vesicomyidae), or

the vestimentiferan tube worm Riftia pachyptila Jones (Sabellida: Siboglinidae). Bathybdella sawyeri is

unusual in a number of respects including depth of capture, high abundance, and reproductive system

anatomy. Like all members of the family Piscicolidae, the leech feeds on fish blood as evidenced by

nucleated red blood cells in the gut, although no specimen has ever been collected from a fish host.

Because of its common association with invertebrates, it seems likely that B. sawyeri leaves the fish

host after each blood meal and attaches to the hard surface of various invertebrates or other hard

substrate until ready to feed again.

Recent collections at two sites along the South East Pacific Rise have extended the range of B.

sawyeri and also provided specimens from the crab Cyanagraea praedator de Saint Laurent

(Decapoda; Bythograeidae) that differ from B. sawyeri in size of the oral sucker. In this paper we

describe the morphological variability and discuss some aspects of the biology of the leech.

Material and Methods

The specimens were collected during the French diving cruise BIOSPEEDO, using R/V L’Atalante and

D/S Nautile, from 31 March to 13 May 2004, Chief scientist D. Jollivet (CNRS, Roscoff), and carried

out along the South East Pacific Rise between 7°24'S and 21°33'S (Jollivet et al. 2004) (Fig. 1). The

majority of the leech specimens were found free from washings of the bivalves C. magnifica and B.

thermophilus or the crabs Bythograea thermydron Williams (Decapoda: Bythograeidae) and C.

praedator and of what is likely a new genus and species of fish (Ophidiiformes: Bythitidae) collected

using the grab of the submarine or with baited traps. Eleven specimens were attached to the cheliped

of the crab C. praedator collected in baited traps, and two were on the external part of the hinge of a

clam C. magnifica. Seven specimens came from four dives on the Oasis site (17°25.38'S,

113°12.29'W, 2586 m) and eleven specimens from the Pagoda site (13°59.06'S, 112°28.94'W, 2623

m), nearly 6 km N of Oasis. Onboard, the leeches were fixed either in formalin or in 95% ethanol for

DNA analysis.

Material examined

Oasis site, 17°25.38’S, 113°12.29’W, 2586 m.

PL 1582, 22.04.2004, baited trap C2: 1 specimen in formalin, found with 3 crabs B. thermydron and 2

bythitid fish gen. et sp. nov. Muséum National d'Histoire Naturelle (MNHN), Paris, France AH1-12VV.

PL 1583, 24.04.2004, basket 1: 1 sp. in formalin, with clams C. magnifica, MNHN AH1-13VV.

PL 1586, 27.04.2004, basket 1: 2 sps. in formalin, with mytilid B. thermophilus, MNHN AH1-14VV.

PL 1589, 30.04.2004, baited trap B3: 3 sps. in formalin, with 5 crabs B. thermydron, MNHN AH1-

15VV.

Pagoda site (marker BS 17), 13°59.06'S, 112°28.94'W, 2623 m.

PL 1592, 04.05.2004, baited trap F2: 6 sps. (2 in formalin, 4 in ethanol), on crab C. praedator, MNHN

AH1-16VV. Baited trap F2: 1 sp. in formalin, serial transverse sections, on crab C. praedator. Basket

1: 4 sps. in formalin, on crab C. praedator, MNHN AH1-17VV.

In addition to the newly collected specimens, the holotype (USNM 65773) and paratypes (USNM

65774, 65775) of B. sawyeri housed in the U. S. National Museum were re-examined, as well as 109

individuals collected on Woods Hole Oceanographic Institution Alvin Dive 884. That dive occurred on

January 25, 1979 on the Galápagos Rift (00°47.69'N, 86°07.7'W). Leeches were from washings of

tubeworms R. pachyptila and bivalves B. thermophilus. These leeches are housed at the U. S.

National Museum, but are uncatalogued.

Habitat of the hosts

Oasis vent site

The Oasis site is characterized by a milky fluid diffusing from crevices, where the temperature

varies between 2 and 7°C, surrounded by a very abundant vent community composed of mussels, B.

thermophilus, clams, C. magnifica, a stalked barnacle, Neolepas n. sp., sea anemone Chondrophellia

cf. coronata (Verrill) (Actinostolidae), the crabs B. thermydron and Munidopsis subsquamosa

Henderson (Galatheidae), and a recently described shrimp, Nematocarcinus burukovskyi Komai &

Segonzac (Nematocarcinidae) (Komai & Segonzac 2005). Numerous fish occur in this environment

such as Ilyophis saldanhai Karmovskaya & Parin (Synaphobranchidae), Thermychthys hollisi (Cohen,

Rosenblatt & Moser) (Bythitidae) (Nielsen & Cohen in press), a very abundant Ophidiidae species, and

one hagfish species.

Pagoda vent site (BS 17)

This site is composed of two black smokers covered by an apparently declining tubeworm

polychaete colony (Alvinellidae); temperature varied from 2°C in the vicinity of the black smokers to

10°C near the tubeworm colony. A surprising abundance of the crab C. praedator (12 specimens were

collected in a baited trap) was observed among the alvinellid colony. A small number of fish

(Ophidiidae) was present within 3 m of the trap.

Results

All leeches from the Oasis site were typical B. sawyeri with maximum length of 11 mm and

suckers of equal size (maximum 1.0 mm in diameter). Photographs taken in life showed them to be

colorless except for the red blood in the gut that was visible through the transparent body wall. Most

leeches from Oasis were engorged with blood (Fig. 2).

All leeches from Pagoda site were attached to the crab C. praedator. They were unusual in that

the overall length of the leeches was larger (13 mm) than typical B. sawyeri and the oral sucker was

distinctly larger than the caudal sucker (Fig. 3). There was little variation in the leeches from Pagoda;

they were all 13 mm in length and all had an oral sucker with a diameter of 1.3 mm and a caudal

sucker with a diameter of 1.0 mm. A single leech from Pagoda that was serial sectioned transversely

for its entire length revealed an internal anatomy identical with B. sawyeri in all respects.

All 109 leeches examined from Alvin dive 884 were typical B. sawyeri in terms of sucker size, with

one possible exception. A single leech, 9 mm in length, had an oral sucker that was larger than the

caudal sucker, 0.8 mm vs 0.6 mm. The other leeches were remarkably consistent with the holotype

and paratypes of B. sawyeri and had suckers that were approximately equal in size.

Discussion

The collections reported here extend the range of B. sawyeri from the Galápagos Rift to the South

East Pacific Rise, and suggest that the leech is widely distributed at vent sites in the Pacific Ocean.

None of the leeches from the Oasis site was sectioned, but externally they are identical to B. sawyeri.

The leeches from the Pagoda site were not originally identified as B. sawyeri because of the large oral

sucker. However, the serial sections revealed that the internal anatomy of these leeches is identical to

B. sawyeri, including 6 pairs of testisacs, and the very unusual reproductive system that has a large

bilobed sprematheca connected via conducting tissue to paired, deep lateral invaginations of the

epidermis (Burreson 1981). These leeches clearly belong in the genus Bathybdella based on internal

anatomy, but the oral sucker is unusually large for B. sawyeri. It is possible that the leeches from the

Pagoda site are a separate species of Bathybdella; however, we have chosen to identify the leeches

with the large oral sucker as B. sawyeri because the internal anatomy is identical with that species.

DNA sequence data will likely be necessary to confirm the identification or provide evidence that it is a

separate species.

It is also interesting that all the leeches from Pagoda were collected from the crab C. praedator,

and none of the leeches from Oasis were collected on this crab. The association with C. praedator is

likely not specific, however. Many marine leeches are known to associate with decapod crustaceans,

mainly for hard surface attachment sites after they leave the fish host, and often for sites of cocoon

deposition (Meyer & Barden 1955; Daniels & Sawyer 1975; Sloan et al. 1984; Khan and Paul 1995).

Leeches in the collections reported here were also recovered from clams, supporting the notion that

they are attaching to any hard substrate available after leaving the fish host.

Specimens of B. sawyeri never have been recovered from a fish host, but few fish have actually

been collected from vent sites. Thus, it is tempting to speculate that the leech feeds on the

hemolymph of the clam C. magnifica or the tube worm R. pachyptila. Both these species have

hemoglobin free in the hemolymph giving it a red color resembling the red color of the leech gut

contents. However, histological sections of the leech gut reveal the abundance of nucleated red blood

cells typical in size and morphology to fish red blood cells. Their presence is evidence that B. sawyeri,

like all other leeches in the family Piscicolidae, feeds on fish blood. Although they were not directly

observed on the two Bythitidae fish collected in the baited trap C2 from the Oasis site, these leeches

are most probably parasitic of this fish. They may, however, be parasitic also on other fish species

present at the sites visited during the BIOSPEEDO cruise between 7°24'S and 21°33'S (Jollivet et al.

2004) including a species of the family Ophidiidae, visible in large numbers on the video documents

taken at the same sites, but not captured. Marine leeches vary considerably in their host specificity.

Many species occur only on a single species of fish (Burreson 1977), while other species feed on a

wide variety of fish hosts (Burreson & Zwerner 1982); the host specificity of B. sawyeri is unknown.

The unusually high abundance of B. sawyeri at vent sites, noted previously by Burreson (1981), is

supported by the collection of over 100 specimens from a single Alvin dive at the Galápagos Rift in

1979. The high abundance of leeches observed on or among invertebrates suggests that B. sawyeri

leaves the fish host after each blood meal and attaches to any hard substrate available. When ready

to feed again individuals must reattach to a fish, but finding a fish host (by random contact) is likely not

difficult considering the high abundance of demersal fishes in the vent areas. When ready to

reproduce, marine leeches mate and deposit cocoons (egg cases), containing usually a single egg, on

any hard substrate available, including the carapaces of decapod crustaceans. A search for clusters

of leech cocoons on the hard surface of the various invertebrates or other hard substrate at thermal

vent sites should be productive. Almost nothing is known of the biology of B. sawyeri at vent sites, but

the high abundance of the leech suggests that the life cycle of B. sawyeri is completed in the vicinity of

the vents, with fish hosts for feeding, and hard substrate for cocoon deposition, in abundance.