The biology and functional morphology of Humphreyiastrangei (Bivalvia: Anomalodesmata: Clavagellidae): anAustralian cemented `watering pot' shell

Brian Morton

The Swire Institute of Marine Science and Department of Ecology and Biodiversity, The University of Hong Kong, Hong Kong, China

(Accepted 17 September 2001)

Abstract

Amongst the watering pot shells of the Clavagellidae (Anomalodesmata), the least well known is

Humphreyia, with a single species H. strangei. Unlike representatives of the other extant clavagellid genera,

i.e. Clavagella and Brechites, however, where juveniles are unknown, there is a single juvenile (plus adult

specimens) of H. strangei available for study. The Clavagellidae contains the weirdest of all bivalves,

encased in a huge (in proportion to the tiny juvenile shell) adventitious tube with an anterior `watering

pot'. The juvenile H. strangei is dimyarian with a large foot and byssal groove, and a large pedal gape; the

entire body is enclosed within a bag-like periostracum-covered mantle cavity. Upon permanent residence,

however, the anterior watering pot component of the adventitious tube is cemented to the chosen

substratum, the adductor muscles are lost and the foot and pedal gape greatly reduced; the fourth pallial

aperture closes and the pedal gape and the tubules of the watering pot are similarly occluded. Once

cementation is achieved, further growth anteriorly is impossible and the adventitious tube is secreted

posteriorly, to house the long siphons, and subsequently can be added to as growth increments.

Anatomically, H. strangei has a typical anomalodesmatan arrangement of mantle cavity and digestive

organs so that it is, probably, a suspension feeder. Inside the pericardium, however, is a pair of unique

proprioreceptors which probably serve to monitor rectal tonus and thus control defecation, co-ordinated

with siphonal retraction and extension. They probably also prevent over-®lling of the capacious rectum. It

is believed that cementation and adventitious tube formation occur at the time of sexual maturity and this

change in lifestyle between juvenile and adult represents a form of metamorphosis ± quite distinct from

that which occurs in all bivalves between the pediveliger and juvenile stages ± and seems to be unique to

Humphreyia and probably Brechites. This family of anomalodesmatan bivalves is thus actually stranger

than the already aberrant watering pot would suggest.

Key words: watering pot shells, Humphreyia strangei, cementation, adventitious tube formation, juvenile

anatomy, adult anatomy, pericardial proprioreceptors, life-history changes

INTRODUCTION

In concert with its evocative speci®c name, Humphreyiastrangei is enigmatic because, as will be shown, despite anumber of papers on it, the only extant species of thisclavagellid genus is, really, unstudied. First the name.Humphreyia was erected by Gray (1858a: 316±317)`after Mr George Humphrey, the conchologist and shelldealer [who] though comparatively an uneducatedperson, he was far in advance of the state of naturalhistory in his time'! The speci®c name was in honour ofMr Strange who delivered two specimens to Englandfrom `shoal' water in Sydney `Bay', Australia (Adams

1854: 91, pl. 15, ®g. 5). Adams (1854) placed it in thegenus Aspergillum. Subsequently, the species was drawnto the attention of J. E. Gray who published two paperson it (Gray, 1858a,b) describing the structure of theadventitious tube and erecting for it the family Hum-phreyiadae, now abandoned.

There are few illustrations of H. strangei: Gray(1858a,b) illustrated both specimens (®gs 1 & 2 of bothpapers) in the shell collection of Mr H. Cuming. Adams(1854: 91), whose illustrations of H. strangei were alsoof the specimens in the H. Cuming collection, describedthem as `one attached to a stone (paralectotype, NHMLondon Reg. No. 1969 261), and the other to the valveof a Mytilus (actually a species of Brachidontes) (lecto-type, NHM London Reg. No. 1968 667). Subsequently,Gray's ®g. 1 was reproduced by L. A. Smith (1962a,

*All correspondence to: Brian Morton.E-mail: bmorton@hkucc.hku.hk

J. Zool., Lond. (2002) 258, 11±25 # 2002 The Zoological Society of London Printed in the United Kingdom DOI:10.1017/S0952836902001164

®g. 5) and by Keen & Smith (1969: 1858, ®g. 32[7]). Anew illustration of H. strangei was published by B. J.Smith (1998: 413, ®g. 9.11C) and photographs of thelectotype (see above) from Sydney Harbour (and otherspecimens) were provided by B. J. Smith (1971) andB. J. Smith (1976), respectively, and by Lamprell &Healy (1998: 223, 654).

E. A. Smith (1909, ®g. 1) illustrated the shell andexternal appearance of a juvenile specimen ofH. strangei obtained from Western Port Bay, Victoria,Australia. Morton (1984a) reproduced E. A. Smith's®gure of H. strangei, illustrated its shell, internally andexternally, and further illustrated the gross internalanatomy of the specimen (BM(NH) 1910, 12. 31.1). Inthe absence of an authenticated adult shell and tube toexamine, Morton (1984a) could not be sure thatE. A. Smith's specimen was a juvenile of H. strangei (aswill be seen, however, it is) and so the anatomicalfeatures described could, similarly, not be comparedwith those of an adult, only B. J. Smith (1971: text ®gsE & F) providing two very general illustrations of theanatomy of this life-history stage.

In the collections of the Western Australian Museum,Perth, are three specimens ascribed to H. strangei,i.e. two dried tubes and a (poorly) preserved, but other-wise intact adult individual. These three specimens formthe basis of this study of the biology and anatomy ofone of the `strangest' of all bivalves. I have alsoattempted to reconstruct a life history for this speciesbased on the Western Australian Museum adults andthe single extant juvenile specimen of H. strangei (E. A.Smith, 1909), the only known clavagellid juvenile.

MATERIALS AND METHODS

The lectotype, paralectotype and juvenile specimen ofH. strangei in the collections of the Natural HistoryMuseum, London (see earlier), have been examined.Not wishing to damage the type material of this rarespecies, however, permission was given for me toexamine in greater detail the three adult adventitioustubes of H. strangei in the mollusc collection of theWestern Australian Museum, Perth, as follows:

1. Port Jackson, New South Wales (WAM S12727). Atube removed from its substratum.

2. Kerslake Collection No. 1076 (WAM S12726),Blyth, Tasmania. A tube attached to a calcareoussubstratum.

3. From the sandy bottom of Goss Passage, 31±34 mdepth, off the eastern shore of Long Island, WallabiGroup, Houtman-Abrolhos Islands, Western Australia(WAM S12725). A tube removed from its substratum.

Specimen 3 above also contained the animal. Thiswas in a poor state of preservation, but it was examinedexternally and the organs of the mantle cavity alsostudied from the left side following an incision along thelength of the mantle to the pedal disc. Subsequently, thespecimen was sectioned transversely at 6 mm along itsentire length and every tenth section kept and alternate

slides stained in either Ehrlich's haematoxylin and eosinor Masson's trichrome.

DISTRIBUTION

Humphreyia strangei was thought to be restricted to thetemperate waters of southern and south-eastern SouthAustralia (Smith, 1976: 197, map 2) although specimensin the palaeontological collection of the Western Aus-tralian Museum (see below) are from Western Australia,and the third specimen reported upon here was collectedfrom the Houtman-Abrolhos Islands, Western Aus-tralia, at 1148E and 28±298S, greatly therefore extendingthe range of the species into the sub-tropics. Cotton(1961) also records it from south-west Western Aus-tralia. B. J. Smith (1971) provides a catalogue ofspecimens of H. strangei and their localities in themuseums of Australia and elsewhere. The species occurssub-tidally, E. A. Smith (1909) recording that the juve-nile specimen was obtained from c. 8 m on a stonybottom. B. J. Smith (1971) records one adult specimenfrom 200 m depth. Lamprell & Healy (1998) record thespecies from depths of between 7 and 200 m.

RECORDS OF FOSSIL HUMPHREYIA

L. A. Smith (1962a,b) regarded Humphreyia as the mostrecent species in the clavagellid line of evolution toappear in the fossil record. Supposedly restricted tosouthern Australia in Recent times (but see the abovereference to a living individual from the Houtman-Abrolhos Islands), H. strangei has been recorded as afossil from Abattoirs Bore, Dry Creek Sands, SouthAustralia (Ludbrook, 1955). In the Western AustralianMuseum, however, there are broken adventitious tubes(regrettably only siphonal components and not thecemented anterior ends) from the carbonate sands ofRoe Plains, Madura District, southern Western Aus-tralia (WAM 79.2190, ®ve specimens, 1976; WAM79.2193, eight specimens, 1978). The fossils which makeup the Roe Calcarenite are of late Pliocene age,i.e. ~ > 2 million years ago, and were laid down at a timewhen the Roe Sea was warmer than at any subsequenttime in southern Australia (Kendrick, Wyrwoll &Szabo, 1991).

TAXONOMY

There is a discrete literature on the Anomalodesmata(Dall, 1889), both fossil and Recent, which has beenreviewed by Morton (1981, 1985a). In the Palaeozoic,the sub-class, represented notably by members of thePholadomyidae (Morton, 1980) and a number of nowextinct other families (Runnegar, 1972, 1974), wasdominant in many marine habitats. During this time,the number of anomalodesmatan families increased, butthen levelled out in the Mesozic (Skelton et al., 1990)

Brian Morton12

and declined in the Cenozoic, possibly because of afailure to compete with more generalist heterodonts andpterioids (Morton, 1995). Today, the sub-class com-prises 14 extant families and constitutes c. one-sixth ofbivalve familial diversity. Most families, however, arerepresented by a few (often only one) genera and manyof these are also monospeci®c (Morton, 1985a). Themost recent phylogenetic analysis of the sub-class wascreated by cladistic means based on all known anato-mical characters of the constituent families (Harper,Hide & Morton, 2000). Although the Anomalodesmatacontains some of the most exotic bivalves, e.g. fourfamilies of deep-sea predators feeding on the abysso-benthic plankton, the watering pot shells of theClavagellidae d'Orbigny, 1844 are particularly anoma-lous. The Cretaceous clavagellid Ascaulocardiumarmatum possessed such bizarre morphological speciali-zations that Pojeta & Sohl (1987: 1) referred to it as `theultimate variation on the bivalve paradigm'. Morton(1985a) believes that modern anomalodesmatans havebeen driven into highly specialized niches through com-petition with the more recent Pterioida andHeterodonta in, generally, hard and soft intertidal andshallow-water habitats, respectively, so that nearly allspecies are considered `rare'. All clavagellids, forexample, have rarely been seen, or at least reportedupon, alive.

Specimens of Clavagella have been described byOwen (1835), Soliman (1971) and Morton (1984b). Theanatomies of species of Brechites have been described byLacaze-Duthiers (1883), Purchon (1956, 1960) andMorton (1984a, 2002). Morton (2002) provides a morecomprehensive list of minor papers on this genus.Purchon (1956, 1960) and Morton (2002) are the onlypeople to have described a living clavagellid (Brechites).Savazzi (1982, 1999, 2000) describes the patterns ofclavagellid adaptation to tube-dwelling and cementedmodes of life.

Australia has a number of species of Clavagellidaeand the alpha taxonomy of the family based mostly onspecimens from this country has been described byB. J. Smith (1971, 1976, 1998) updating the moregeneral classi®cation of L. A. Smith (1962a,b).B. J. Smith (1976) recognized three genera, i.e. Clava-gella Lamarck, 1818; Brechites Guettard, 1770 andHumphreyia Gray, 1858 with, respectively, four (Clava-gella, Bryopa, Dacosta and Stirpulina), three (Brechites,Penicillus and Foegia) and two (Humphreyia andNipponoclava) sub-genera collectively encompassing17 species and sub-species. Savazzi (2000), however,considers Bryopa to represent a third morphological(boring) entity (actually a fourth, Humphreyia havingbeen previously ignored) to the facultative semi-endolithic Clavagella and the infaunal Brechites andtheir respective allies. Morton (2002), however, notesthat B. vaginiferus, one of the most widely-distributedspecies, does cement its adventitious tube to rocks butonly in some habitats.

The Japanese sub-genus Nipponoclava (Smith, 1976)once associated with Humphreyia, is clearly not ce-

mented (as is Humphreyia) and is now placed withinfaunal Brechites-like taxa (Habe, 1977). Humphreyiastrangei is, thus, the only species of the genus and theonly representative of a morphological type, i.e. epi-faunally cemented as opposed to infaunally so, likeBrechites vaginiferus (Morton, 2002). This study is,therefore, of a bivalve which has never been seen alive,of which there are few preserved adult specimens (whichhave not been even adequately examined), and which isa Recent example of the adoption of the cementedlifestyle. There is, however, a single juvenile specimen inexistence (see earlier; there being no other known juve-nile clavagellid). This paper thus reports upon one ofthe rarest and `strangest' representatives of one of themost anomalous families of the Anomalodesmata andBivalvia. It investigates speci®cally the hitherto sus-pected anatomical changes that occur in not only this,but also other representatives of the family, e.g.Brechites, to achieve the very peculiar adult `watering-pot', but in this case cemented, lifestyle.

ANATOMY

The shell and adventitious tube

The juvenile

The juvenile of H. strangei has been described byMorton (1984a), but it was uncertain then whether thisonly existing specimen was H. strangei. Now, by com-paring it with an adult H. strangei, it can be concludedthat it is a juvenile of this species. It is here brie¯ydescribed again, to facilitate comparison with the adultand to allow an interpretation of the pattern of growthexhibited by this species and the associated life-historychanges. The juvenile is illustrated in Fig. 1 (afterE. A. Smith, 1909), seen from the left lateral and ventralaspects. The shell is juvenile, the entire body is encasedin a brown periostracum to which sand grains adhereposteriorly and there is a, proportionally, very largepedal gape. (See Appendix for all abbreviations used in®gures.)

The juvenile shell (after Morton, 1984a) is small(Figs 1 & 2a), subquadrangular and about 3 mm longand 2 mm tall. It is equivalve and posteriorly elongate,giving it a slightly heteromyarian form. The shell valvescomprise a prismatic outer layer and a sheet nacre innerlayer (Taylor, Kennedy & Hall, 1973). The externalsurface of each valve appears to be ®nely and radiallypustulate. Internally (Fig. 2b), the juvenile shell is unitedby a tiny, opisthodetic, external primary ligament, theinternal surface of which is calci®ed to form a litho-desma. There are no hinge teeth, but along the shell'sdorsal margin the periostracum is thickened and whatYonge (1978) termed `fused', but this is not so ± itsimply covers the surface as a somewhat thickened pad.

Around the true shell is secreted the `saddle' which isbest seen in the uncemented juvenile (Fig. 2a). This isclearly produced from the mantle margin as the animal

13The biology and function morphology of Humphreyia strangei

grows in the usual bivalve way so that as seen internally(Fig. 2a), located on it are the approximately equal scarsof the anterior and posterior adductor muscles and thepallial line. There is no pallial sinus. The `saddle'comprises ®ne concentric growth lines and during this,early, process of growth, the shell becomes squarer,i.e. the ventral edge of the juvenile shell is added tomore, thereby creating a more quadrate shape. At thispoint, true shell growth ceases and the adventitious tubeis formed.

The adult

An adult adventitious tube of H. strangei is illustratedin Fig. 3 (WAM S12727). Dorsally (Fig. 3a), the juvenileshell and `saddle' are hidden by calcareous concretionsthat have poured over them possibly from the siphons.The animal occupies the enlarged base of the tube whichis ventrally (Fig. 3b, c) cemented to the substratum. Inthis old individual, the original adventitious tube has®ve additional growth increments which are thought tobe secreted, as has been described for Brechites vagini-ferus by Morton (1984a), from the apices of the siphonsas a liquid and which then pours down the previousincrement, internally, to achieve progressive elongationin length with age. Note, however, that the anterior

Brian Morton14

SAG

P

SV

PED

SV

SAG

Fig. 1. A juvenile Humphreyia strangei specimen as seen from

the left and ventral aspects. For abbreviations see Appendix.

(After E. A. Smith, 1909.)

“SA” SV

(a)

(b)

PA

FP LI PRL

AA

PL

2 mm

Fig. 2. Humphreyia strangei: (a) an external view of the right;

(b) an internal view of the juvenile left shell valves. For

abbreviations see Appendix. (After Morton, 1984a.)

AT

DR

(c)

VR

AS

10 mm

(b)

LR

(a)

Fig. 3. Views of a Humphreyia strangei cemented tube which

has been separated from the substratum (WAM S12727):

(a) dorsal; (b) anterior; (c) ventral. For abbreviations see

Appendix.

base, once cemented, cannot grow further. The attach-ment surface thus mirrors the surface texture of thechosen substratum, i.e. it is xenomorphic. The tube inFig. 3 is curved and there are dorsal, ventral and lateralridges, so that it is square in transverse section.

A second, younger tube is illustrated in Figs 4 & 5(WAM S12726). Seen from the dorsal aspect (Fig. 4),the juvenile shell and saddle are obvious. The base ofthe tube is, in this specimen, still attached to its sub-stratum, an old bivalve shell of another species. Aroundthe `saddle', however, has been secreted a ®rst, or

primary watering pot, presumably when the animal wasstill unattached, and then a second larger one which iscemented to the substratum. Posteriorly, the animalthen produced its adventitious tube. This specimen isillustrated from the right side in Fig. 5. The juvenileshell and saddle are obvious but, in this specimen, thelatter was produced in two stages and then the primarywatering pot was secreted. A few small tubules areevident at its edge. The secondary watering pot wasproduced next and this has numerous, occluded tubulesat its edge and which are formed where the specimencemented itself to the old shell substratum. Posteriorly,the cemented watering pot was ®rst produced into ashort extension and on which the tube ridges ®rstappear. The adventitious tube was then secreted withwell-developed ridges, e.g. laterally, but at the end of theprimary adventitious tube, subsequent tube growth hasextended it.

It should be noted that neither of the above driedtubes of H. strangei had sand grains or other detritusattached to them. These had probably been cleaned offduring curation and with handling and age. A thirdadult specimen (WAM S12725) had been collected aliveand is illustrated in Figs 6 & 7. Dorsally (Fig. 6), thespecimen is as earlier described except that the primaryadventitious tube has sand grains attached, whereas thesecondary growth has fewer and is clean apically. More-over, this specimen has what seems to be a sheet ofperiostracum covering the tube. It is probably notperiostracum, however, but an otherwise organic ®lmsimilar to that thought to be secreted by radial areno-philic glands in the apices of the siphons of Brechitesvaginiferus (Morton, 1984a). The tube of the WAMS12725 specimen of H. strangei has been further

15The biology and function morphology of Humphreyia strangei

AT

SU

SWP10 mm

PWP

‘SA’

SV

Fig. 4. An adult Humphreyia strangei tube as seen from the

dorsal view and still attached to an old bivalve shell sub-

stratum (WAM S12726). For abbreviations see Appendix.

EAT

LR

STG

ESWP

5 mm

TU

SWP

PWP

‘SA’

SV

AT

Fig. 5. An adult Humphreyia strangei tube, as seen from the right side showing the true shell, saddle and adventitious

components (WAM S12726). For abbreviations see Appendix.

illustrated from the anterior and posterior aspects. Seenfrom the antero-ventral view (Fig. 7a), inside the tube,the approximate position of the external saddle andbeyond its margins laterally, is white. This is calciumcarbonate cement that is produced by the mantle dor-sally and which fuses, internally, the saddle and anteriorwatering pot and posterior adventitious tube into asingle, solid structure. How this is done has beendescribed for B. vaginiferus in detail (Morton, 2002). Onthis internal white area are what seem to be old, butnow non-functional, muscle scars. Similarly, wateringpot tubules are occluded. Internally, too, arising fromaround the edge of the internal saddle area is perios-

tracum. Seen posteriorly (Fig. 7b), the square shape ofthe H. strangei tube is clearly evident.

The postulated process of tube formation will bedescribed and discussed later.

The body

Juvenile. The juvenile of H. strangei was described byMorton (1984a). The siphons (Fig. 8) are long andenclosed within a tube of periostracum. There is a largepedal gape (also see Fig. 1) and a fourth pallial aperture.The ctenidia are paired and comprise the inner demi-branch and the ascending lamella only of the outerdemibranch. The inner and outer labial palps are small.Very importantly, there are anterior and posterior ad-ductor muscles but no, detectable, pedal retractors.There is a visceral mass with a well-developed foot whichhas a byssal groove. It is suspected that, as in mostbivalves (Yonge, 1962), the juvenile of H. strangei had asmall byssus. Postero-dorsally is a heart, penetrated by arectum and which, posteriorly, hangs freely in the supra-branchial chamber and ends in an anus. This and thepresence of obvious digestive diverticula suggest that thejuvenile H. strangei had the usual bivalve gut andprocessed food particles collected by the ctenidia andlabial palps, again in the usual bivalve manner.

Adult. The adult specimen of H. strangei, removedfrom its tube (WAM S12725), is illustrated in Fig. 9.Seen from the dorsal view (Fig. 9a), the pedal disc isheart-shaped and beneath the mantle can be seen thedark digestive diverticula, the heart and rectum and theposterior kidneys. The siphons extend posteriorly. Inventral view (Fig. 9b), the periostracum-covered pedaldisc has a tiny pedal gape. In left lateral view (Fig. 9c),the same structures are seen, but the periostracum-covered siphons are covered apically in sand grains andother particles of detritus.

The adult specimen of H. strangei has been dissectedfrom the left side and illustrated as though it were aliving animal, not a shrivelled cadaver (Fig. 10).

The musculature

As described earlier, the juvenile of H. strangei possessesboth anterior and posterior adductor muscles. The adultof H. strangei loses the adductor muscles, so that it isessentially amyarian as in Brechites which does,however, possess anterior (but not posterior) pedalretractor muscles (Morton, 2002). The pallial musclesare, however, well-developed and these can be divided,functionally if not morphologically, into pedal disc,ventral and siphonal retractors (Fig. 10).

The mantle

The juvenile of H. strangei does not possess a pedal disc,but anteriorly there is a large pedal gape. There is also a

Brian Morton16

Fig. 6. An adult Humphreyia strangei tube, as seen from the

dorsal view, and separated from its substratum and alive at the

time of collection (WAM S12725). For abbreviations see

Appendix.

Fig. 7. An internal view of an adult Humphreyia strangei tube

as seen from: (a) anterior end; (b) posterior end (WAM

S12725). For abbreviations see Appendix.

small fourth pallial aperture. In the adult, the pedalgape (Figs 9b & 10) is reduced to a tiny aperture and thefourth pallial aperture does not exist. In the adult, thepedal disc is heart-shaped when seen from the antero-ventral perspective (Fig. 9b). It is also covered byperiostracum and orientated such that it will lie ¯atagainst the substratum (Fig. 9c).

The siphons are long and make up most of the

posterior region of the body (Figs 9c & 10). Becausemantle fusion is of type C, i.e. involving the inner,middle and the inner surfaces (only) of the outer mantlefolds (Yonge, 1982), the periostracal grooves are unitedeverywhere, except at the pedal gape and the siphonalapertures (and the fourth pallial aperture in the juve-nile), so that the body and most notably the siphons arecovered by periostracum.

17The biology and function morphology of Humphreyia strangei

OD A R PA H

DD

OLP

AA

ILP

F

PED

BG

IDP

1 mm

FPA

ES

IS

Fig. 8. The organs of the juvenile Humphreyia strangei mantle cavity and body as seen from the right side. For abbreviations see

Appendix. (After Morton, 1984a.)

(a) (b)

(c)

K H

R H DD

5 mm

PDPED

SAG

ES

IS

P

PED

Fig. 9. A preserved Humphreyia strangei specimen removed from its tube (WAM S12725) and as seen from: (a) dorsal aspect;

(b) ventral aspect; (c) lateral aspect. For abbreviations see Appendix.

The folds are separate, anteriorly to create the siphonalapertures. Seen from the posterior (Fig. 11), the siphonscomprise a simple unfringed exhalant aperture and alarger slightly-fringed inhalant. Around the siphons, onthe middle mantle fold, are about 18 papillae which aresensory and seen in both Brechites and Clavagella, forwhich they are further described (Morton, 1984a,b). Thesiphons are also covered posteriorly by particles of sand,shell fragments and sediment (SAG). The glue whichholds the fragments in place is secreted by arenophilicradial mantle glands located in the middle mantle fold ofthe siphonal apices. These have also been described byMorton (1984a,b) for Brechites and Clavagella and arenot illustrated again here.

The structure of the siphonal wall is illustrated inFig. 12. Externally, the periostracum is two-layered andcomprises an inner layer which stains blue in Masson'strichrome and is c. 50 mm thick, and an outer layerwhich is thin (< 10 mm) and stains red in the same stain.Its outer surface is thrown into long ®brous strands.

Beneath the thin outer epithelium is a region of largevacuolated areas, which probably represent a haemo-coel. Internal to this is a zone of longitudinal muscleblocks followed by a layer of circular muscles. Beneaththis is a layer of loose, again haemocoelomic connectivetissue, followed by a second zone of longitudinal muscleblocks that are also interspersed by strands of obliquemuscles. Beneath the tall inner epithelium and betweenthe inner layer of longitudinal muscles are numerousgland cells which probably, as in Brechites vaginiferus(Morton, 1984a, 2002), produce the calcium carbonatematerial which forms the adventitious tube. There arealso 18 pallial nerves matching the number of sensorypapillae at the siphonal apices (Fig. 11).

Brian Morton18

ES

IS

P

5 mm

IBCSRMO

VRM‘SA’HG

PDRM

PD

MG

PED

T

CSS/MG

ILP

OLPDD ST ID

HK R

OD SBC

Fig. 10. A reconstruction of an adult Humphreyia strangei as seen from the left side and showing the organs of the mantle cavity

and visceral mass. For abbreviations see Appendix.

ES

SP SAG

IS

5 mm

Fig. 11. A reconstruction of Humphreyia strangei siphons as

seen from the anterior aspect. For abbreviations see Ap-

pendix.

OP

VC

CM

OM

IE PNSG

LM

100 µm

LM

OE

IP

Fig. 12. A transverse section through a part of the Hum-

phreyia strangei siphons to show the various layers. For

abbreviations see Appendix.

Organs of the mantle cavity

The ctenidia of the H. strangei juvenile are relativelylarge and comprise inner demibranchs and theascending lamellae only of the outer demibranchs. Thectenidial ciliation was adjudged by Morton (1984a) tobe of type E (Atkins, 1936). The same situation occursin the adult (Fig. 10) and the ctenidia extend right upinto the greatly elongated siphons. Also in the juvenile,the labial palps are proportionally large (Morton,1984a) and have a connection with the ctenidia whichcan be classi®ed as Category 3 (Stasek, 1963). The sameis true of the adult, and the labial palps (Fig. 10) occupythe same position and have the same relationship withthe ctenidia as in the juvenile.

The visceral mass

The immature juvenile of H. strangei has a visceral masswith, posteriorly, a proportionately large foot and abyssal groove (Morton, 1984a). In the adult, however,the visceral mass has a relatively reduced foot and thereis no byssal groove (Fig. 10). The swollen visceral mass,however, contains the digestive system (see later) butalso contains mature paired testes antero-ventrally andovaries postero-dorsally.

At the base of the visceral mass above the foot lie thelarge pedal ganglia (Fig. 13). Separate from and inequi-lateral to these are the paired statocysts (STAT). Theseare some 40 mm in diameter and each comprises acapsule lined by ciliated cells (CI). Inside each capsule isone large (10 mm) statolith (STA) and many smallerstatoconia (STC). These are all crystalline, and thestatocysts are thus of Type B3 (Morton, 1985b) as alsoseen in Brechites and Clavagella (Morton, 1984a,b).

The digestive system

The course of the intestine in the visceral mass is illu-strated in Fig. 10. The conjoined style-sac and midgutpasses down into the visceral mass from the stomach.The position of the stomach is indicated by the sur-rounding dark digestive diverticula. In the visceral mass,the midgut, following separation from the crystallinestyle-sac, makes one or two slight turns ventrally and

soon becomes the wider hindgut. This passes upwardsinto the visceral mass until dorsally it widens yet furtherand turns posteriorly as the rectum. This penetrates theventricle of the heart and the paired kidneys dorsally andthen extends beyond the visceral mass to project into thesupra-branchial chamber of the mantle cavity.

It has not been possible to reconstruct the structure ofthe stomach from the tissue sections. Notwithstanding,the oesophagus is a ¯attened tube some 700 mm in width(Fig. 14a) and surrounded by a muscular coat. Its wallsare folded into eight pleats so that the cells range inheight from 12 to 25 mm and have cilia 10 mm long. Aswith the stomach, it has not been able to determine thestructure of the conjoined style sac and midgut, butwhen the latter (Fig. 14b) separates from the former it isa narrow tube, only c. 250 mm in diameter. Its cells arec. 12 mm tall. The hindgut (Fig. 14c), however, possessesa typhlosole, the cells of which are 25 mm tall and thecilia c. 25 mm long. Finally, the hindgut, close to theheart, loses its typhlosole and becomes an enormouslydistended rectum (Fig. 14d), which is a tube c. 800 mm indiameter. Its cells, however, are only c. 6mm tall and arefringed by cilia c. 10 mm long. The rectum is, like theoesophagus, surrounded by a thick muscular coat and,beneath it, towards the posterior end of the distal limbsof the kidneys and thus close to the supra-branchialchamber, are the visceral ganglia.

The pericardium

The heart (Fig. 10) is located within a pericardium,between the digestive diverticula and paired kidneys. Itcomprises a ventricle, penetrated by the rectum andlateral auricles. The posterior pericardium is shown intransverse section in Fig. 15. It is separated from theposterior end of the visceral mass by transverse muscle®bres. In it can be seen the rectum surrounded by thedistal limbs of the kidneys and within which are theproximal ones. The cells of the distal limb tubulescontain kidney concretions (Fig. 16) c. 5 mm in diameter.The pericardium is surrounded by the supra- and infra-branchial chambers, the former lined by tall (180 mm)supra-branchial gland cells also seen in Clavagellaaustralis (Morton, 1984b) that may represent ahypobranchial gland (Morton, 1977). The ctenidial axisis separate from the epithelium of the ctenidium itself,as in many anomalodesmatans (Morton, 1985a).

Within the distal limbs of the kidneys, however, issomething of especial interest (Figs 15 & 16). Appearinglike tiny pedal retractor muscles, two thin (40 mm)paired blocks of muscles arise from the dorsal mantleand are thus attached to the adventitious tube (orinternal saddle) and extend downwards and attach tothe ventral surface of the pericardium. Ventrally, eachmuscle block is in intimate contact with a large (100 mm)ganglion which, because of its position, is not one of thefused and distinctive visceral ganglia (Fig. 14d), but aspecialized structure with nervous connections, albeitvia the cerebro-pleural-visceral connective, posteriorly,

19The biology and function morphology of Humphreyia strangei

CI

STC

PEG 50µm

STA

STAT

Fig. 13. A transverse section through the Humphreyia strangei

pedal ganglia showing the statocysts. For abbreviations see

Appendix.

to these and, anteriorly, the cerebral ganglia. Lateral toeach ganglion is what is believed to be a sensorystructure which comprises hollow sacs c. 100 mm inhorizontal diameter with thickened (8 mm) internalepithelial linings. These structures are considered to be apair of specialized proprioreceptors. Each one resemblesa disc to which dorsal and ventral proprioreceptormuscles attach, so that as they either contract or relax,the hollow sensory sacs (PSS) adjacent to each proprio-receptor ganglion will either compress or expand,respectively, and so stimulate it and thence, the cerebro-pleural and visceral ganglia.

DISCUSSION

Humphreyia strangei, the only species of the genus, isknown since at least the late Pliocene (L. A. Smith,1962b) and is restricted to southern Australia. Hitherto,it was considered to be con®ned to south-eastern Aus-tralia, but material in the Western Australian Museumshows that it is also found in Western Australia, both asa fossil and, more importantly, as a living individualfrom the sub-tropical Houtman-Abrolhos Islands onthe west coast. L. A. Smith (1962b) believed that Hum-phreyia had evolved from a Brechites-like, i.e. an

infaunal, ancestor and not a boring Clavagella.Although L. A. Smith (1962b) gave no evidence insupport of this suggestion, this study does so. Represen-tatives of Clavagella always attach by the left valve tothe wall of their crypt and the right valve is free inside it.Such clavagellids also have both anterior and posterioradductor and pedal retractor muscles, the latter albeitbeing much reduced (Morton, 1984b). Conversely, thejuvenile shell valves and saddle of Brechites and its alliesare marginally united with an adventitious tube and arefused together internally. There is also a perforated`watering pot' anteriorly and, internal to this, themantle is formed into a pedal disc (Morton, 1984a,2002). Clavagella australis does not have a pedal disc(Morton, 1984b). The situation in H. strangei is thesame as in B. vaginiferus where both juvenile shell valvesare marginally united with and incorporated into theadventitious tube, and a few tubules are manufacturedas the anterior watering pot is produced. Because,H. strangei is epifaunal, i.e. cemented to its substratum,however, the watering pot, which is most well-developedin species of Brechites and allied genera, is producedonly to a limited extent and any tubules that are formed,and the pedal gape, are occluded so that the adultH. strangei has little or no contact with the environmentanteriorly unlike the situation in B. vaginiferus which is

Brian Morton20

(a)

(b)

(C)

TY DK

200 µm

(d)

MC

VG

MC

Fig. 14. Transverse sections of a Humphreyia strangei through: (a) oesophagus; (b) midgut; (c) hindgut; (d) rectum. For

abbreviations see Appendix.

intimately connected with interstitial water (Morton,2002). Anterior adventitious tube growth in H. strangeiis therefore restricted and serves only to cement theanimal to its substratum. Further growth is, thus, onlypossible posteriorly to accommodate the enlargingsiphons. The juvenile with a relatively large foot, and abyssal groove suggesting an early ability to produce abyssus, however, can probably project both structuresthrough the relatively large pedal gape, possibly toeffect locomotion and to help it ®nd a suitable sub-stratum before byssal attachment and, eventually,cementation. Probably as postulated for B. vaginiferus,therefore, H. strangei undergoes a number of stages inits life history which are illustrated in Fig. 17.

First, there is probably an undescribed planktoniclarva, followed by a settling pediveliger stage. Thissettles to produce, second, an active juvenile (Fig. 17a)which has been described by Morton (1984a) andherein. Importantly, this possesses a normal pair ofadductor muscles which means that the animal func-

tions like a typical bivalve and must be able to, at leastpartially, close its shell valves. Once a habitat is chosenby the juvenile for permanent occupation (Fig. 17b),further growth occurs, the shell saddle is produced, andthe mantle cavity is greatly expanded beyond themargins of the true valves so that they become orientedhorizontally to each other. The adductor muscles pre-sumably degenerate at this stage The animal thusoccupies a bag-like mantle covered mostly by perios-tracum. The third, cemented, adult stage (Fig. 17c) isformed when the anterior watering pot is produced,possibly in two stages, the ®rst uncemented, the secondso attached. The fourth, fully adult stage develops anadventitious tube posteriorly to house the now greatlyenlarged siphons (Fig. 17d) and this, only, can beelongated as further growth occurs in this direction but,again, not anteriorly. Humphreyia strangei is, thus, ®rst,a free-living mobile juvenile, then an epifaunal, initiallybyssally-attached bivalve which subsequently cementsto a substratum, and ®nally becomes a matureBrechites-like watering pot shell, albeit with occludedpedal gape and tubules.

Most aspects of the anatomy of H. strangei arereminiscent of Brechites and to, a much lesser extent,Clavagella. Clavagella australis, for example, is di-myarian throughout its life and, moreover has aninternal amphidetic ligament located between chondro-phores, whereas those of Humphreyia and Brechites areopisthodetic, the former at least with a lithodesma.There is no suggestion either that Clavagella nor itsallies has a juvenile life-history stage that is any differentfrom the adult, unlike Humphreyia and Brechites and itsallies. Because of its adult lifestyle, however, the juvenilefoot and pedal gape of H. strangei are greatly reduced inthe adult and the fourth pallial aperture and watering-pot tubules close. The adult also loses its adductor andpedal musculature, the latter also possibly not beingpresent in the juvenile. The organs of food collection

21The biology and function morphology of Humphreyia strangei

R

M

PM

SBC

CA

PCPG

IBCDK

TTF

VM

PGPK

PG

CA

PM

HG

500 µm

Fig. 15. A transverse section of a Humphreyia strangei body through the pericardium. For abbreviations see Appendix.

PM

50 µm

KC

PCPG PM DK PSS

Fig. 16. Humphreyia strangei. A, A detail of one pericardial

proprioreceptor. For abbreviations see Appendix.

and processing in the mantle cavity and intestine, re-spectively, however, are retained and in proportion tothose of the juvenile. Of interest is that the siphonsbecome greatly enlarged, so that growth subsequent toattachment is only possible posteriorly. Also of interestis that in H. strangei this, as in Brechites vaginiferus,necessitates the great elongation of the rectum to expelfaeces ef®ciently from the now remote exhalant aper-ture. In this context too, the rectum is, also as in B.vaginiferus (Morton, 2002), greatly enlarged in diameterand externally muscularized. In a typical bivalve, therectum would be narrow, like the hindgut, but in thisanimal, contractions of its muscular sheath have to beused to push the faeces through the rectum to theexhalant siphon. Cilia alone could not do this task.

Extending from the dorsal saddle to the ventralpericardium are tiny muscles, each crossing a specializedganglion and associated, vacuolated, sensory chambers(Fig. 18). Clavagella australis possesses a pair of tinyposterior pedal retractor muscles that are attached to

the true shell and extend into the posterior region of thevisceral mass, via the kidneys, and close to the cerebro-pleural-visceral connective which, however, they do nottouch. The two muscles described for H. strangei couldthus be remnant posterior pedal retractor muscles. If so,however, they have been relocated from the true shellonto the adventitious tube and attached internally tothe pericardium, and not ending within the posteriorvisceral mass as in Clavagella and most other bivalves.They could, therefore, be new structures. What,however, is their function? As the proprioreceptormuscles (Fig. 18) contract and relax, they would com-press and enlarge the vacuolated sensory chambers(PSS) of the nerve disc respectively, and thereby stimu-late the associated proprioreceptor ganglia (PG) (whichmust also be new structures) that, in turn, innervate thecerebro-pleural ganglia anteriorly and/or the visceralganglia posteriorly via the cerebro-pleural-visceral con-nective. Probably this proprioreceptor prevents therectum becoming too engorged with faeces. If it did itwould put pressure on the kidney haemocoel around theproprioreceptors causing the tonus of the muscles tochange and thereby stimulate the nerves to, eventually,expedite defecation. Such a receptor may also functionin relation to the contraction and relaxation of thesiphons (within the exhalant of which is the extendablerectum) and which, as in B. vaginiferus (Morton, 2002),must have powerful effects upon the tonus of the bodyorgans.

For example, the siphons of H. strangei can beretracted deeply into the tube as in Brechites vaginiferus(Morton, 2002), so that their extension must be byhydraulic means as neither genera has adductor musclesto achieve this. A proprioreceptor which functions toachieve the same state of tonus, among the Bivalvia, isseen in some representatives of the Tellinoidea, i.e. theventral pallial cruciform muscles and organ of Erviliacastanea (Morton, 1990).

Brian Morton22

(a) (b) (c) (d)

Fig. 17. Postulated stages in Humphreyia strangei growth from a juvenile to an adult. For a description see text.

AT M

PM

PSS

100 µm

PMPC

C-P-V-CONN

PG

To cerebro-pleuralganglia

To visceralganglia

Fig. 18. One Humphreyia strangei pericardial proprioreceptor.

For abbreviations see Appendix.

Humphreyia stangei thus represents amongst extantclavagellids, an hitherto largely unappreciated fourthmode of life, i.e. cementation, that has evolved veryrecently, probably from a Brechites-like ancester, pos-sibly Nipponoclava (B. J. Smith, 1976). Morton (2002),for example, has shown that in some habitats, Brechitesvaginiferus does cement itself to stones and rocks.Harper & Morton (2002) and Morton & Harper (2001)have shown that cementation in the Anomalodesmatahas evolved in two additional phylogenies, i.e. theMyochamidae and Cleidothaeriidae, and again in both,quite recently. Thus, although the Anomalodesmata hasa long history stemming from the Palaeozoic to theRecent, especially the Pholadomyidae (Morton, 1980),cementation in the sub-class is a modern phenomenonand has, thus, evolved quite independently in the abovethree families. Cementation in the Myochamidae andCleidothaeriidae has been described by Harper &Morton (2000) and Morton & Harper (2001), respec-tively. In H. strangei, cementation is probably bysecretions produced from the siphons and which mayalso create both the cemented watering pot and theadventitious tube in a manner similar to that describedfor B. vaginiferus by Morton (1984a, 2002).

The ®nal point about H. strangei is that, as this studyshows, there is a form of ontogenetic metamorphosiswhich occurs at the end of the juvenile phase, essentiallyaf®liated with a loss of mobility and adoption of thecemented mode of life. As far as is known, such achange, unlike cementation in other bivalves, includingMyochama and Cleidothaerus (but juveniles of these arealso unknown) where the setting pediveliger transformsinto the cemented juvenile which then grows into theadult, seems to be unique to Brechites and, now Hum-phreyia, among the Clavagellidae.

Acknowledgements

This research was undertaken in July and August 2000during the tenure of a Research Associateship at theWestern Australian Museum, Perth. I am grateful to theExecutive Director of the Museum for the provision ofbasic facilities, to S. Slack-Smith for permission toaccess the molluscan collection, to G. W. Kendrick forallowing me to examine fossil specimens in the palaeon-tological collection, and to both persons and D. S. Jonesfor much kind hospitality and the bene®t of stimulatingdiscussions.

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Brian Morton24

APPENDIX

Abbreviations used in the ®gures

A AnusAA Anterior adductor muscle (or scar)AS Attachment surfaceAT Adventitious tubeBG Byssal grooveCA Ctenidial axisCI CiliaCM Circular musclesC-P-V-CONN Cerebro-pleural-visceral connectiveCSS/MG Conjoined style sac and midgutDD Digestive diverticulaDK Distal limb of kidneyDR Dorsal ridgeEAT End of primary adventitious tubeES Exhalant siphonESWP Posterior extension of secondary watering potF FootFP Fused periostracumFPA Fourth pallial apertureH HeartHG Hind±gutHYG Hypobranchial glandIBC Infra±branchial chamberID Inner demibranchIE Inner epitheliumILP Inner labial palpIP Inner layer of periostracumIS Inhalant siphonI'SA' Internal saddle areaK KidneyKC Kidney concretionLI LithodesmaLM Longitudinal musclesLR Lateral ridgeM MantleMC Muscular coatMG Mid±gutO OvaryOD Outer demibranchOE Outer epithelium

OLP Outer labial palpOM Oblique muscle ®bresOP Outer layer of periostracumOTU Occluded tubuleP PeriostracumPA Posterior adductor muscle (or scar)PC PericardiumPD Pedal discPDRM Pedal disc retractor musclesPED Pedal gapePEG Pedal gangliaPG Proprioreceptor ganglionPK Proximal limb of kidneyPL Pallial linePLS? Pallial line scar?PM Proprioreceptor musclePN Pallial nervePRL Primary ligamentPSS Proprioreceptor sensory sacPWP Primary watering potR Rectum`SA' `Saddle' area of shell valve (plus internally)SAG Sand grainsSBC Supra-branchial chamberSG Siphon glandSP Sensory papillaSRM Siphonal retractor musclesST StomachSTA StatolithSTAT StatocystSTC StatoconiaSTG Subsequent tube growthSU SubstratumSV Shell valveSWP Secondary watering potT TestisTF Transverse muscle ®bresTU Watering pot tubulesTY TyphlosoleVC Vacuolated cellsVG Visceral gangliaVM Visceral massVR Ventral ridgeVRM Ventral retractor muscles

25The biology and function morphology of Humphreyia strangei