JOURNAL OF MORPHOLOGY 189:l-16 (1986)

The Morphology of ldiocranium russeli (Amphibia: ), With Comments on Miniaturization Through Heterochrony

MARVALEE H. WAKE Department of Zoology and Museum of Vertebrate Zoology, University of California, Berkeley CA

ABSTRACT Idiocranium russeli is among the smallest species of caecili- ans. The morphology of the skull (e.g., small, widely spaced dermal elements, retention of cartilaginous remnants) and of the posterior vertebrae (incomplete development, retention of a postvertebral notochord) indicate that hetero- chrony, or change in timing of development, has resulted in the miniaturiza- tion of the species. The pattern is apparently a progenetic one, characterized by early offset of development (see Alberch et al., '79). Other unique features of osteology (e.g., extensive sphenethmoid development) correlate with the burrowing habit of the species and may have arisen to compensate for proge- netic effects. Several features of the myology, neurology, and visceral morphol- ogy are correlated with miniaturization as well. Reproductive maturity occurs at approximately 75 mm total length; gonads are proportionately small, but other aspects of reproductive morphology are typical of direct-developing .

Zdiocranium russeli is one of the smallest berch et al., '79). Analysis of heterochrony in species. Collected only once near a lineage presumably already constrained the Cameroon-Nigerian border in 1934-1935 developmentally and phylogenetically by by the British Museum (Natural History) ex- body elongation and limb loss may yield in- pedition led by Ivan T. Sanderson, the species sight into pattern of evolution. This study is characterized by a number of unique char- analyzes characters of Idiocranium common acters. Several (reviewed below) were listed to the gymnophione lineage, and the nature by Parker ('36) in the type description. As- of variation of these characters in a minia- pects of the ecology and behavior were re- turized taxon. It considers how small size counted by Sanderson ('37). Forty-eight may be achieved, and how the morphological paratypes were reported by Parker ('36)to be characteristics of the taxon are correlated in the British Museum (Natural History) and with its biology, especially its fossorial habits the Museum of Zoology, Cambridge Univer- and its direct-development mode of reproduc- sity, U.K. Available for study were the holo- tion. A comparison with other West African type (BMNH 1936.3.4.29) and 16 paratypes caeciliids also may be instructive in the ab- from the BMNH, 28 specimens from Cam- sence of opportunities to recollect the species, bridge, and three specimens from the Mu- if it still exists. seum of Comparative Zoology, Harvard University. Investigation of Idiocranium pro- MATERIALS AND METHODS vides information relevant to several prob- Forty-eight specimens (27 females, 13 lems in evolutionary morphology. Little was males, and eight juveniles) of Idiocranium known of its morphology; thus its relation- russeli were examined, ranging from 50 mm ships to other gymnophione taxa are not well total length (TL) immatures to among the assessed. Miniaturization as a develop- largest known adults (114 mm TL). Fifteen mental and evolutionary phenomenon is re- specimens were X-rayed, one cleared and ceiving renewed attention (Hanken, '84); heterochrony, or alteration of developmental "program," has been proposed as a mecha- Address reprint requests to M.H. Wake, Department of Zool- nism for such phenomena (Gould, '77; Al- ogy, University of California, Berkeley, CA 94720.

0 1986 ALAN R. LISS, INC. 2 M.H. WAKE stained with alizarin, one cleared and stained mosal, and the large nasofrontal fontanelle with alizarin and sudan black, two cleared that exposes much of the dorsal surface of and stained with alizarin and Alcian blue, the sphenethmoid. The absence of pre- and and two prepared as serial frontal sections postfrontals and ectopterygoids was also (head and tail) stained with hematoxylin- noted. Taylor (‘69) reiterated these charac- eosin, picro-ponceau, or Mallory’s trichrome. ters. They are indicated in Figure 1A-C, and In addition, gonads, kidney, urogenital ducts, compared to those of a more ‘typical’ skull lung, and skin were prepared for histological (Afiocaecilia taitana; Fig. 1D-F). examination, and scales were stained and These and other osteological features can mounted. The head and body wall muscula- be evaluated in more detail based on cleared ture were dissected before clearing and stain- and stained (Fig. 1) and sectioned material. ing. Other West African taxa (Geotrypetes In the skull of a specimen 113 mm in total seraphin6 G. grandisonae, Herpele squalos- length (MCZ 21811; skull 5.2 mm long), the toma, Schistometopum thomense, and Scole nasopremaxillary bones are separated medi- comorphus kirkii) were variously X-rayed, ally, approaching contact only for the second cleared and stained, dissected, and sectioned 10% of their lengths. Anteromedially they for comparison of morphological characters. diverge to expose the mesethmoid process, Table 1 presents counts and measurements which is more fully ossified than in most of various characters. The morphology and other species (Fig. 2) (see Wake and Hanken, some features of the natural history of the ’82). The connecting bar of the nasal compo- species are reported here, for the paratype nent to the premaxillary is very thin; the series constitutes the entire sample of this nasal process widens only in the middle of its unique genus and species. length. The cartilaginous nasal cupulae are unusually large, and project bilaterally so as RESULTS to square the outline of the snout. The pos- External morphology teromedial divergence of the nasopremaxil- The type description (Parker, ’36) summa- laries exposes much of an exceptionally well- rizes many of the salient features of external ossified sphenethmoid complex. Dorsally the morphology. The eye is visible as a small, sphenethmoid is domed and smooth, and its dark dot beneath the skin of the head; the medial suture is complete. There are no su- snout is long and pointed, the mandible un- tures between any of the dermal elements, derslung. The tentacle is globular, nearer the and they are usually separated by gaps of nostril than the eye. Parker reported 83-90 0.25-0.5 mm. The small frontals lie adjacent (mode 86) primary annuli and 21-29 (mode to the nasopremaxillary posterior projec- 24) secondary annuli, presumably for the full tions, the squamosals, and the front ends of sample of 49 specimens. For my sample of 47, the parietals. The maxillaries are excluded I find 81-88; (% = 84.0) primary annuli and from contact with the frontals by the long 20-31 (?T = 26.0) secondary annuli (Table 1). nasopremaxillae, a condition unique among Variation in primary counts is probably due caecilians. The eye socket is formed of the to Parker’s inclusion of the two collar folds posterior margin of the maxillary and the in his counts; variation in secondaries is anterior margin of the squamosal, but socket probably due to my inclusion of the short size and eye position may vary. In one cleared postvent annuli. The vent has 6-8 lobes and and stained specimen, the left socket is poorly is subterminal. formed, nearly occluded by the squamosal. In Parker reported that the specimens were that specimen and one other, one eye lies “blue-grey above, lighter beneath.” They have faded in preservative to greyish-brown to yellow-brown dorsally, and cream-colored Fig. 1. Skulls of Idiocranium russeli (A-C) and Afm ventrally. The skin of the lower jaw margin caecilia taituna (D-F). Note reduction of dermal ele- and of that around the eye, tentacle, and ments of I. russeli. A. taituna is a small but not miniaturized species. A. Dorsal views. B,E. Ventral nostril is also cream-colored. views. C,F. Hyoid apparatus. Camera lucida drawings of skulls to same scale. Cartilage is heavily stippled. Ab- Osteology breviations: bo, basioccipital; cb, ceratobranchial; ch, The skull has several unique features ceratohyal; f, frontal; lc, laryngeal cartilages; m, max- which were mentioned by Parker (’36): the illa; mp, maxilla palatine; nc, nasal cupula; npm, naso- premaxillary; 0,orbit; p, parietal; pa, pseudangular; pq, great reduction of the frontals, the concomi- pterygoquadrate; sq, squamosal; sph, sphenethmoid st, tant nasopremaxillary contact with the squa- stapes; tc, tracheal cartilage; v, vomer. Bar = 0.1 mm. n

A TABLE 1. Measurements(mm) and counts forIdiocranium russeli Head width Specimen Total Primary Secondary Head Head width at jaw Eye to Eye to Tentacle Body Sex No. length annuli annuli length at nostrils articulation tentacle nostril to nostril width Vertebrae

Q MCZ 21811 113 83 26 5.3 1.4 3.4 1.4 2.1 0.7 3.5 91 BMNH 26 5.2 1.2 3.2 1.4 1.9 0.7 Q 1946.9.5.77 82 3.3 90 111 30 5.3 1.4 3.3 1.4 2.0 Q 1946.9.5.84 105 87 4.2 93 29 5.2 1.6 3.1 1.3 1.7 0.5 Q 1946.9.5.73 104 84 94 1.9 0.6 5.0 1946.9.5.76 104 85 22 5.2 1.3 3.2 1.4 91 0 2.2 0.6 4.3 0 1946.9.5.83 104 83 25 5.2 1.2 3.5 1.7 0.6 4.2 91 83 27 5.2 1.8 3.2 1.4 Q 1946.9.5.72 103 1.8 0.5 3.5 90 82 28 Q 1946.9.5.78 102 5.0 1.0 3.0 1.1 1.5 0.4 3.4 90 87 92 Q 1946.9.5.71 102 27 5.3 1.1 3.5 1.4 1.8 0.6 4.1 82 89 Q MCZ 20946 99 25 4.9 0.9 3.0 1.4 1.9 0.6 4.0 85 90 Q MCZ 21812 96 29 4.5 1.0 2.9 1.1 1.6 0.5 3.4 BMNH 0 1946.9.5.74 96 84 26 ------90 Q 1946.9.5.80 95 86 27 5.0 1.0 2.9 1.3 1.9 0.5 3.8 92 Q 1946.9.5.79 95 85 24 5.1 1.2 3.0 1.3 1.7 0.5 3.7 90 Q 1946.9.5.75 94 82 24 5.1 1.4 3.4 1.4 1.7 0.5 4.0 91 Q 1946.9.5.86 85 85 31 4.9 1.1 3.0 1.3 1.7 0.5 3.9 88 0 1946.9.5.81 77 83 26 4.6 1.0 2.5 1.3 1.5 0.4 2.5 91 Imm 1946.9.5.85 67 85 29 3.8 0.9 2.6 1.0 1.5 0.4 2.9 90 Imm 1946.9.5.82 50 86 24 3.9 0.45 1.9 0.8 1.2 0.3 1.7 86 CAMBRIDGE* 24 4.8 1.0 3.0 1.4 Q 104 83 1.7 0.5 4.4 1 28 5.4 0 2 105 81 1.1 2.3 1.3 1.3 0.5 4.0 Imm 3 61 81 26 3.3 0.8 2.1 0.8 1.2 0.3 2.2 Imm 4 73 86 25 3.3 0.8 2.4 0.9 1.4 0.4 2.6 Q 5 88 84 29 4.3 0.9 2.2 1.0 1.5 0.4 3.6 Imm 6 65 86 29 3.5 0.6 2.0 0.5 1.2 0.3 2.2 Q 7 95 82 25 4.7 1.1 2.9 1.6 1.6 0.4 3.5 Q 8 110 84 23 6.6 1.4 2.4 1.5 1.5 0.5 3.5 0 9 104 83 30 5.0 1.2 3.3 2.2 1.8 0.6 3.9 10 107 84 27 4.5 1.1 2.8 1.3 1.8 0.5 3.5 0 81 P 11 110 29 4.2 0.9 2.7 1.2 1.6 0.4 4.0 12 103 82 25 4.3 1.0 3.4 1.2 1.6 0.5 3.7 0 82 Q 13 96 27 3.8 2.9 3.4 85 1.0 1.1 1.5 0.4 3.2 0 14 98 85 24 4.5 1.0 3.0 1.2 1.5 0.5 0 15 113 31 4.9 1.0 3.3 1.4 1.8 0.5 4.1 Q 16 109 85 24 4.0 1.0 3.1 1.2 1.6 0.5 4.3 Q 17 98 83 32 4.7 0.9 2.9 1.3 1.7 0.5 4.0 0 18 86 29 72 3.1 0.8 2.2 0.9 1.3 0.4 3.0 (continued) HETEROCHRONY AND MINIATURIZATION IN CAECILIANS 5

under the squamosal, the other in the socket. The squamosal overlaps the quadrate poste- riorly and the dentigerous part of the maxil- lary anteriorly. The posterolateral margin of I I I I I I I I I I; the parietal overlaps the otic capsule. The left and right otic elements are separated dorsomedially. Ventrally, the fused maxillopalatine bears two rows of teeth, the nasopremaxillary a single row (the medial continuation of the labial tooth row) and the vomer a single row *em*ee*mIow (the continuation of the lingual tooth row). 0000000000 The palatine forms the lateral and posterior margins of the choanae. The vomers are small and form the medial borders of the choanae. They are widely separated medially and expose the length of the sphenethmoid. The 0s basale, into which otic capsules and occipital elements are incorporated, has lat- eral flanges anterior to the otic capsules which bear cartilaginous surfaces that artic- ulate with the quadrate. Anterolaterally, there are dorsal (orbital cartilage remnant) and ventral (trabecular remnant) bars of car- tilage between the 0s basale and the sphen- ethmoid. The pterygoquadrate is very large and bears the angled articulation surface for the lower jaw. The stapes is large and block- like. The columellar component is short and has a cartilage-capped articular surface that abuts the quadrate. The stapedial foot plate is very large, filling a concomitantly large oval window. The stapes is not perforated by the stapedial artery. The lower jaw consists of two elements: the dentigerous pseudodentary and the pseudar- ticular. The latter bears a long retroarticular process which is 1.0 mm of the 3.8 mm length of the jaw. A small (0.15 mm) remnant of Meckel's cartilage lies between the juncture of the two elements of the jaw, even in large adults. Teeth The teeth of I. russeli are bicuspid and re- curved (Fig. 3), similar to those of other Afri- can caeciliids (Wake and Wurst, '79). The teeth located medially on the rami of the dentaries are considerably larger than those more posteriorly. Tooth replacement patterns were analyzed for the three cleared and stained specimens. A virtually full comple- ment of stage F teeth (mature, ankylosed, functional; see Wake, '76, '80b) is maintained in each tooth row (see Table 2). Replacement crowns in stages a-d (rarely e) were present for most loci. The sample is too small for 6 M.H. WAKE

Fig. 2. Photomicrogrpah of frontal section through top of skull of I. russeli. Note gap between nasopremaxillae, exposed extent of mesethmoid-sphenethmoid complex, and scant cartilage at anterior end of mesethmoid. Abbreviations: me, mesethmoid; n, nasal; os, olfactory sac; sg, skin glands. Bar = 0.1 mm.

TABLE 2. Tooth data for Idiocranium russeli* Tooth counts? Premaxillary- Specimen Dentary Splenial maxillary Vomeropalatine Stage$ (%) No. teeth teeth teeth teeth abcdefg BMNH 1946.9.5.72 24 1 30 21 5.4 6.9 13.1 5.4 5.4 58.5 5.4 1946.9.5.74 17 4 28 23 1.6 10.2 9.4 7.9 4.7 56.7 9.4 MCZ 21811 20 4 26 23 1.0 3.8 5.7 6.7 0 69.5 14.3 *Data are taken from cleared and stained specimens. +Toothcounts are of stage f teeth. *Stages a-e are developing tooth crowns; stage f is that of ankylosed, functional crowns; stage g is the unoccupied space of a shed tooth. (See Wake, '76, and text for discussion.) statistical analysis, but it suggests that vari- for other caecilians. The vertebrae are block- ation in tooth number in adults is not highly like, rather than elongate. All vertebrae but correlated with size (or probably age). the atlas have posteriorly directed dia- and parapophyses for articulation with the bicip- Vertebrae and ribs ital ribs. The second through eighth or ninth There are slightly fewer vertebrae in the vertebrae have a slight keel on the neural column than in other caecilians, except for arch where dorsal head muscles insert. All of members of the genus Grandisonia which the vertebrae have the pronounced ventral also has some diminutive species. Individu- keel characteristic of caecilians and many als in a sample of 19 I. russeli have 86-94 other fossorial forms. A small block of noto- (% = 90.5) vertebrae. The atlas has a small chord remains in the center of the centrum centrum and has the large atlantal cotyles of each vertebra, as noted by Lawson ('66) mentioned by Wake ('70) for caecilians. The and Wake ('70). articular facets have a deep cartilaginous The most noteworthy aspect of the verte- pad. The structure of the remaining verte- bral column is the reduced development of brae resembles that reported by Wake ('80c) the posterior components. Even in the larg- HETEROCHRONY AND MINIATURIZATION IN CAECILIANS 7 duction, as suggested by Nussbaum (‘77, ’83) and demonstrated by Bemis et al. (’83) in Dermophis mexicanus. The muscle is shorter than in many species (Wake, personal obser- vation), originating over the first four body segments. The intermandibularis is dis- tinctly segmental (Fig. 5B). Four extrinsic eye muscles are present, one of only 2-3 fi- bers. Because of their positions, I infer that - these are rectus superior, r. inferior, and ob- Fig. 3. Camera lucida drawing of lingual view of teeth liquus inferior; the attenuate muscle is prob- of I. russeli Tooth crowns are bicuspid, the labial cusp ably the r. externus. small. Abbreviations: jr, jaw ramus; pd, pedicel; tc, tooth The trunk musculature is relatively invar- crown. Bar = 0.5 mm. iant in caecilians (Naylor and Nussbaum, ’80, Nussbaum and Naylor ’82).The musculature est (113 mm TL) specimen cleared and of Idwcranium is much like that of Geotry stained, the notochord is retained through- petes seraphini as summarized by Nussbaum out life. It extends as a rod posterior to the and Naylor (’821, though I am not convinced terminal vertebra (Fig. 4A-B). It is con- of the extent of myosepta in the obliquus nected to the unmineralized notochordal externus superficialis muscle. component of the centrum of the penultimate and last vertebrae. Paired small lateral Brain and spinal cord blocks of cartilage lie beside the posterior The topology of the brain is that of most notochord, and intervertebral joints may caecilians, with large olfactory bulbs, dorsal have been forming before and after these and ventral olfactory tracts, enlarged cere- blocks, for the notochordal cartilage is less bral hemispheres that expose a median pi- dense and resembles ontogenetic segmenta- neal-thalamic complex, small medullary tion formation. A block of notochordal carti- lobes, and a recurved diencephalon. Some lage, reduced in size in each vertebra comparisons of Idiocranium with data on anteriorly in the sequence, occurs indepen- other species from the literature, especially dently in the third and fourth posteriormost Kuhlenbeck (‘22), are warranted. Concomi- vertebrae. This component is not embryonic tant with the elongation of the anterior end cartilage (Alciati blue positive) in the more of the skull, the olfactory lobes are relatively anterior vertebrae. The dia- and parapo- larger and somewhat more tapered ante- physes are also cartilaginous on the terminal riorly. The Jacobson’s organ is small and vertebrae. Ribs are partially mineralized on embedded in the Harderian gland. The cra- the second and third posteriormost verte- nial nerve complement is typical of caecili- brae, and entirely cartilaginous on the last ans. Large dorsal and ventral olfactory vertebra. Further, the neural arch of the last nerves are present; the trigeminal and facial vertebra is incomplete dorsally. are also large, as are their ganglia. The optic nerves are very small, and the trochlear nerve is absent. The abducens innervates the The general pattern of head and body mus- retractor tentaculi muscle. The tongue is in- culature is that of non-rhinatrematid caecili- nervated by the glossopharyngeal and hy- ans. The head musculature is characterized poglossal nerves. The vagus nerve originates by a large, fan-shaped depressor mandibulae from some six roots. that appears to have anterior and dorsal The hindbrain tapers into the spinal cord. components (Fig. 5A). These originate from A complex “spinal accessory” nerve includes the parietals and squamosals, and insert an- components of spinal nerves 1and 2. Paired terodorsally on the retroarticular process of spinal nerves serve each body segment. An- the lower jaw. The three adductor muscles teriorly, they exit through foramina in the are small, and the interhyoideus posterior vertebrae, but after the first six, exit inter- muscle is large and fan-shaped, originating vertebrally. on fascia overlying body wall musculature and inserting posteroventrally on the re- The tentacle troarticular process (Fig. 5A). The interhyoi- The paired tentacles are chemosensory deus posterior major has dorsal and ventral structures whose lumina open to the Jacob- components. It is likely involved in jaw ad- son’s organ, then to the epithelium of the 8 M.H. WAKE

A - B Fig. 4. Camera lucid drawings of posteriormost ver- vertebra is represented only by cartilaginous flanges, tebrae of a specimen of I. rwseli 113 mm in total length. and the terminal cartilaginous notochord is retained Note increased retention of cartilage (heavily stippled) throughout life. A. Dorsal view. B. Ventral view. Abbre- in centrum, articulations with ribs, and rib ends in pro- viations: ce, centrum; na, neural arch; no, notochord ri, gressively more posterior vertebrae, so that the terminal rib. Bar = 1.0 mm.

olfactory bulb. The tentacles are extrusible talline, adherent to the cornea and retina, structures, protacted and retracted by extrin- and the cornea is attached to the overlying sic muscles which are homologous to the re- dermis (Fig. 8). The retina has the eight- tractor and levator bulbi of other . layered structure typical of nearly all verte- They are derived from the rectus externus brates. An attenuate optic nerve is present, and levator mandibulae, respectively (see as are four tiny extrinsic muscles. The large Wake, ’85 for review). Harderian gland fills the back part of the The tentacle of Idiocranium lies in a chan- socket. nel in the maxilla, emerging just behind and below the nostril. The tentacle is “globular” The ear (Parker, ’36; Taylor, ’68) as opposed to elon- The optic capsule is proportionately large gate. The channel epithelium of the tentacle and dilated in Idiocranium, and the large is continuous with the epidermis, and the stapes is free in the oval window. The inner epithelium of the outer wall of the tentacle ear is similar to that reported by Wever (“75) is also epidermal (Fig. 6). A connective tissue and Wever and Gans (‘76), and White and cover is perforated by the lumen, which is Baird (‘82) for nonichthyophiid caecilians. lined by a scant columnar epithelium. The ldiocraniurn has a small papilla neglecta and retractor tentaculi muscle is very long, prob- a large (auditory) papilla. The ably concomitant to the extreme anterior amphibian papilla lies in a recess, and is emergence of the tentacle. The tentacular partially covered by an arm of limbic tissue, channel is lubricated by secretions of the so that the aperture is reduced pig. 7B). The Harderian gland. saccular macula is elongate, as are the sac- culus itself and the perilymphatic cistern. Eye The latter structures are separated by a well- The structure of the eye is discussed in defined Reissner’s membrane (Fig. 7A,B). detail in Wake ’85 and compared with other species. It is summarized here. The socket is Lung formed of the maxillary-squamosal margins. Only the right lung is well developed, the The orbit lies under a thick layer of glandu- left represented by a very small outpocket- lar skin. The lens is well developed and crys- ing. In a 104-mm-TLspecimen the lung is 13 HETEROCHRONY AND MINIATURIZATION IN CAECILIANS 9

A

B Fig. 5. Camera lucida drawings of head musculature lines, and associated musculature by heavy lines. Abbre- of 1. russeli. Depressor mandibulae is in two bundles; viations: dm, depressor mandibulae; ds, dorsal spinal intermandibularis is of numerous bundles; interhyoi- musculature; gh, geniohyoid ih, interhyoideus; ihp, in- deus posterior, an adductor of the jaw, has dorsal and terhyoideus posterior; im, intermandibularis; pdn, pseu- ventral components. A. Right lateral view. B. Ventral dodentary; r, rectus cervicis; rf, reflected flap; sar, view. Hyobranchial apparatus is indicated by dotted subarcualis rectus. Bar = 1.0 mm. mm long, or 12.5% total length - proportion- The lung is supported along most of its length ally shorter than in other taxa of caecilians by independent, branched, semicircles of car- (Wake, personal observation). However, the tilage (Fig. 9) as in several other species lung has the complex organization typical of (Marcus, '23; Wake, '74; Pattle et al., '77). caecilians. The lung is compartmented and Furthermore, Marcus and Wake both noted highly vascularized, with a large, elongate that smooth muscle connected the free ends pulmonary artery and pulmonary vein, and of the cartilages. Marcus tentatively indi- many capillaries underlie the epithelium. cated and Wake elaborated upon a passive 10 M.H. WAKE

Fig. 6. Frontal section through right tentacle of I. m, muscle; pc, perilymphatic cistern; R, Reissner’s mem- russeli, illustrating lumen and retractor musculature. brane; sc, saccular cavity. Bars = 0.1 mm. Abbreviations: b, bone; ep, epidermis; mrt, musculus retractor tentaculae: sg, skin gland; ta, tentacle aper- Fig. 8. Frontal section through left eye of I. russeli. ture; te, tentacular epithelium. Bar = 0.1 mm. The eye is very small and heavily covered by skin, but has a well developed lens and retina. The eye lies in the Harderian gland, and atop the tentacular retractor mus- Fig. 7. Sections (7A, 7B) of inner ear of I. russeli. A. cle. Abbreviations: b, bone; br, brain; d, dermis; ep, epi- Dorsal anterior component. B. Medial posterior compo- dermis; hg, Harderian gland; 1, lens; m, muscle; mrt, nent including amphibian papilla. Abbreviations: ap, musculus retractor cloacae; re, retina; sg, skin gland. amphibian papilla; b, bone; br, brain; It, limbic tissue; Bar = 0.1 mm. recoil mechanism of inspiration, as carti- atria and a muscular elongate tapering ven- lages rebound following smooth muscle con- tricle. The interior of the ventricle is thrown traction during expiration, which is also into many potential channels by the elongate facilitated by body wall contraction. muscular cords. The vessels entering and leaving the heart are much more elongate The heart and the general circulation than the general diagrams in Lawson (‘70) The heart begins at 26.4% TL in the body. indicate. The common carotids are paired at In the 104-mm:TL specimen, it is 6.25 mm the level of their emergence from the heart long, elongate, and has thin-walled paired and branch only as they enter the head. A HETEROCHRONY AND MINIATURIZATION IN CAECILIANS 11 single right systemic arch is present, whence issues the dorsal aorta. The pulmonary trunk contributes the right pulmonary artery, and a single large pulmonary vein enters the atrium from the lung. The general pattern of vascularization is as Lawson (’70) described for Hypogeophis. Other visceral organs The liver in the specimens dissected is *20 mm long, or 20% of the total length. It has 20-28 fan-like lobes, and its surface has a scattering of melanophores. A small, saccu- lar gall bladder is attached to the penulti- mate lobes. The spleen is small (4 mm long), reddish, and spindle-shaped, attached to the body wall and the stomach by the mesogaster and the gastrosplenic ligament. The pan- creas is large, pale, and diffusely massed on the mesentery of the intestine. The stomach is recognizable as an elongate, highly mus- cular region of the gut tube; the intestine is somewhat coiled, an unusual state for caeci- lians. The “rectum,” immediately preceding the cloaca, is a dilated rather thin-walled region of the intestine. The cloaca receives the intestine and the urogenital ducts ofboth sexes (see below). Integument The skin is composed of a thin, slightly keratinized epidermis and a thick dermis that contains mucous and “poison” glands, melanophores, capillaries, and dermal scales (Fig. 10). Numerous capillaries lie just under the epidermal basement membrane. The der- mis contains thick layers of fibrous and some elastic connective tissue. The melanophores lie just under the epidermis, and over the scale pockets, and beside the poison and mu- cous glands. The skin glands are a monolayer in the dermis, and are of two major types (Fig. 10). Mucous glands are small (0.5-0.8 mm diam- eter) and lie just under the epidermis. There are several per body segment, with ducts to the surface of the epidermis. They are typi- cally vacuolated and have basal nuclei around their periphery. The “poison” glands are much larger, typically 0.13 mm in diam- Fig. 9. Frontal section through mid-lung of I. russeli. eter. There are usually 2-3 per body segment Note the ends of the cartilaginous semicircular support structures, the associated smooth muscle fibers, and the in a sagittal section; hence they are numer- complexly elaborated respiratory epithelial surface. Ab- ous around the body. The glands are filled breviations: al, alveolus; c, cartilage; ca, capillary, e, with a granular acidophilic secretory prod- epithelium; sm, smooth muscle. Bar = 0.1 mm. uct. The glands have large ducts to the skin Fig. 10. Frontal section through posterior body wall surface. of I. russeli. Note skin glands, scale structure (mineral- The scales occur in the posterior body seg- ized denticles atop connective tissue base plate), and ments, as described for the species by Taylor association of scale pocket and annulus with segmental muscle septum. Abbreviations: a, annulus; d, dermis; ep, epidermis; m, muscle; mg, mucous gland my, myotomal septum; pg, poison gland; s, scale; sp, scale pocket. Bar = 0.1 mm. 12 M.H. WAKE

(‘72). The scales lie in pockets bounded by of growth in the species, nor even size at connective tissue in the dermis. Typically hatching; thus inferences about age at first there are two pockets per segment in a sag- reproduction cannot be made. The sample ittal section of dorsal skin. Each pocket con- includes 26 females, 13 males, and eight tains three scales per section. Each scale is immatures. composed of an unmineralized base plate that The testes of 1. russeli are reduced, 1-5 appears to be a bilayer of connective tissue, lobes on each side (one specimen has a large and a series of dorsal mineralized denticles lobe only on the right side). Lobes reduce of diverse shapes (Fig. 10). Each scale has a slightly in length posteriorly. The length of thin cellular (generative?) layer on its ven- the testis is 5-10 mm, or 5-10% of the total tral side. The scales are small relative to length of the , in contrast to the 10- those of other species; a sample of 15 from 20% typical of adult males of most species. several annuli averages 0.8 x 0.45 mm in The testes show active spermatogenesis, with diameter. Taylor (’72) reported that the larg- many loculi in different stages of develop- est scale from one specimen that he observed ment in each lobe (see Fig. 34, Wake, ’68). A was 1.4 x 1.6 mm, with several approxi- large proportion of locules contain maturing mately 1.0 x 1.5 mm. Scales are dorsoven- spermatids, and several have evacuating trally flattened and ovoid in shape (Fig. 10). ducts that enter the longitudinal duct in the The denticles are flatter and further apart center of the testis. Three to six transverse than in most species (Wake, personal obser- ducts extend to the anterior part of the kid- vation), and arranged in typical concentric ney, and sperm are eventually transported circles. I do not observe the “fore to aft” by the archinephric ducts (see below). Well- increase in size reported by Taylor; scales developed interstitial tissue is present, and show much variation in size within pockets the spermatogenic cycle is in’a late stage 4 and among annuli. (Wake, ’68). The paired Mullerian glands (derived from Urogenital morphology and reproductive the Mullerian ducts; see Wake, ’70a, ’80c) are biology some 8 mm long and adjoin the cloaca. They The reproductive biology of the species is are composed of series of simple tubular known only from the report of Sanderson glands whose lumina are continuous with (‘37). The taxon is one of several direct devel- the central lumen of the duct. The columnar opers (eggs laid on land, development secretory cells have large, granular basal nu- through metamorphosis before hatching, clei. The cells are densely packed so that thus circumventing a free-living larval stage; nuclei appear to be in 2-3 layers. The lumen Wake, ’77b, ’82). Sanderson reported that of the duct is lined with ciliated epithelial many females were found coiled around cells. Secretory activity is correlated with ac- clutches of eggs with embryos in diverse tive spermatogenesis and perhaps sperm stages of development. These specimens are transport among terrestrial (see dis- not deposited in any museum, according to cussion in Wake, ’80c). my multiple inquiries. The females and The cloaca is described by Wake (‘72) and clutches were found as the mat of swamp compared to that of other species. That of grasses was rolled back, revealing the fe- Zdiocranium has the typical sites of entrance males with their young atop pedicels of earth, of archinephric ducts, Mullerian glands and surrounded by “moats” of water. Sanderson oviducts, with no partitioning relative to the reported that the females spat at him as they intestinal aperture. Cloacae are simple; both were uncovered - a functional near-impossi- sexes have a dimorphic but apparently spe- bility, to my notion. cies-specific organization of dorsal, ventral, Sexual maturity, as indicated by gonad and transverse muscles and connective tis- maturation, occurs at > 70 mm total length. sue structure. The vent is transverse, with The gonads of a 67-mm specimen are undif- 10-12 lobes. As in all other species of caecili- ferentiated; a 77-mm male has paired testes, ans, the terminal part of the cloaca is eversi- each of a single lobe. Females 85 mm and ble, constituting an intromittent organ for longer have mature ovaries containing ova sperm transport and internal fertilization of several size classes, and Parker (’36) re- when inserted into the vent of the female. A ported a 90-mm female with a laid clutch of stout retractor muscle extends from the ven- eggs. These sizes at maturity are smaller tral body wall to the phallodeum. Zdiocran- than suggested by Parker. Nothing is known ium lacks blind sacs, a feature of cloaca1 HETEROCHRONY AND MINIATURIZATION IN CAECILIANS 13 specimen is composed of deep columnar cells, and is hypertrophied and somewhat convo- luted. The cells appear swollen, probably due to fluid accumulation. Numerous capillaries lie in the thin fibromuscular layer bounding the epithelium, suggesting hypervasculari- zation. This condition, coupled with the pres- ence of a single lysed ovum in the anterior region of the duct, suggests that 1)ovulation has just begun, or 2) laying of the clutch has just occurred. The morphology of the paired, elongate kidneys is generally typical of that of all terrestrial species (Wake, '68). Glomeruli usually occur in pairs-a condition not often observed in other species, and perhaps a ves- tige of their segmental origin in this dimin- utive species. The archinephric or Wolffian duct is the sole unit of urine transport in both sexes (Wake, '70a). No accessory urinary ducts are Fig. 11. Camera lucida drawing of uneverted cloaca1 present. In females, the ducts transport urine male intromittent organ. The phallodeum is the poste- only. Collecting ducts from multiple neph- rior part of the cloaca which is extruded through the rons join the archinephric duct. In males, the vent and inserted into the vent of the female to effect ducts also transport sperm. The sperm exit sperm transport. The pattern of lobes and ridges is spe- cies-specific. Cloaca is opened ventrally and pinned open, the transverse ducts into unmodified neph- exposing entire surface. Abbreviations: a, annulus; lo, rons, whose collecting ducts bear the sperm lobes; mrp, retractor muscle of the phalloderm; tv, trans- to the archinephric ducts. verse connective tissue ridges; ve, vent. Bar = 1.0 mm. The fat bodies are well developed, 4-10 lobes on each side, held by the mesentery of the gonad. The length of the fat body unit is morphology presumed primitive (see Wake, 15-30 mm, correlated with body size. There '72) and has sets of muscles that form pro- are no observable differences between the nounced ridges and terminate in the phallo- sexes. deum (Fig. 11). Males have the urinary bladder attached The ovaries are paired, elongate (8-17 mm), by mesentery to the m. retractor cloacae. In hollow sacs containing ova in three stages of Idiocranium the anterior lobe is four times development. A class of 4-10 large (1.0-1.4 as long as the posterior and extends fully mm x 0.6-0.9 mm) yolky ova is present in beyond the mesentery. In females the blad- each ovary, each ovum surrounded by a flat- der lobes are nearly equal, the anterior only tened, follicular monolayer. The largest class slightly longer than the posterior. See Wake of ova may be at maximum size, for the state ('70b) for comparative data. of the oviduct (see below) and the presence of a cytolyzed ovum in it suggest that ovulation DISCUSSION has just begun (see Wake, '68, for compara- Miniaturization and functional morphology tive data on ovarian structure). A class of in Idiocranium greater numbers (6-15) of vitellogenic ova The proportions of a number of organs and (0.5-0.7 mm diameter) and clusters of 15-25 some of the unique aspects of their structure previtellogenic oocytes (0.2-0.3 mm diame- in Idiocranium are associated with the un- ter) are interspersed among the well-yolked usually small size of the species. Lungs, liver, ova. Corpora lutea were observed in the one and gonads are relatively smaller than in ovary sectioned. other caecilians. The number of testis lobes The oviducts are elongate (40-50 mm), is more highly variable than observed in reaching from the end of the liver to their other taxa. entrance into the cloaca. Development of the Several features of the skull are associated oviducts is discussed by Wake ('70a). The lu- with miniaturization and its mode of acqui- minal epithelium of ducts of the sectioned sition (see below). Truncation of development 14 M.H. WAKE is suggested by the reduction of the frontals, the reduction of the dermal elements. The the large dorsal fontanelle, the large cartila- particular shape of the nasal cupulae may ginous nasal cupulae, the small vomers, and also facilitate burrowing. the absence of sutures or overlap among Yet other features may be correlated with many dermal elements. The dorsal and ven- the demands of feeding mechanics. Morphol- tral fontanelles are particularly construed as ogy and osteology suggest a typical “strong evidence for truncation; for comparison with bite’’ mechanism (see Bemis et al., ’83). The an ontogenetic series of Dermophis mexi- long retroarticular process and the large canus, a Central American caeciliid, indi- number of teeth in this small taxon may cates that the stage of development of the facilitate such a mode of feeding. Nothing is elements forming the fontanelles in Zdiocran- known of prey preferences in Zdiocranium; I ium is that of a midterm fetus of Dermophis, have not been able to identify prey from 50- were dermal bone development to cease in year-old gut contents. Skulls of Zdocranium Dermophis at that stage. have large articulation facets of the lateral A number of components of the skull re- flanges of the 0s basale and the quadrate. main cartilaginous throughout life in Zdi- These are present in the skulls of other small ocranium. Several of these are typical of all species, such as Afiocaecilia taitana. How- caecilians: the hyoid apparatus is rarely min- ever, they are present in larvae and juveniles eralized (Wake, personal observation). The of Geotrypetes grandisonae and juveniles of rims of the nasal capsules and the anterior G. seraphini and D. mexicanus, but not in component of the mesethmoid process re- large adults of these taxa. The juncture of main cartilaginous in virtually all taxa of these elements is firmly bound by fibrous caecilians, even in large, old specimens. Yet connective tissue in large adults. It is tempt- throughout life, Zdiocranium retains small ing to suggest increased skull kinesis in blocks of orbital and trabecular cartilage at small species to allow strong bites on large the juncture of the sphenethmoid complex prey, especially given the loose quadrate and and the 0s basale and a small block of Meck- squamosal associations, which occurs as a el’s cartilage at the pseudodentary-pseudar- developmental phase in other taxa (see Wake ticular junction. This is a characteristic of a and Hanken, ’82). This awaits corroboration. number of small species (Grandisonia alter- The morphology of special sensory units is nuns and G. breuis, J. Straub, personal com- apparently correlated with miniaturization. munication; Afiocaecilia taitana, Wake, per- The eyes are reduced, correlated with fosso- sonal observation) but is an ontogenetic fea- riality, not miniaturization. However, both ture of Dermophis mexicanus. Diverse the olfactory and the otic components are functions (viz., kinesis, shock absorption dur- disproportionately large in Zdiocranium. The ing burrowing) have been suggested (Straub, olfactory lobes of the brain are elongate; the personal communication), but never tested. otic capsules are inflated, the inner ear well In Dermophis, the cartilages are completely developed, and the oval window and foot- replaced by bone in older adults, the Meck- plate of the stapes proportionally large for el’s cartilage first, the trabecular second, and caecilians. Hanken (‘84) has suggested that the orbital last. Furthermore, in Zdiocranium in urodeles the sensory capsules have a min- the nasal cupulae are larger and of a more imum functional size, which, if met, dictates defined shape throughout life than in other skull conformation in miniature forms. In species. Yet, the mesethmoid process is less other words, other elements of the skull may cartilaginous, and more ossified in older be reduced further than those of the sensory specimens than in other caecilians. units, which get no smaller than their func- Some features of the skull of Zdiocranium tional minimum. These units therefore “dic- probably are consequences of miniaturiza- tate” skull proportions as a consequence of tion correlated with demands of function and relative growth. This principle may apply in habitat, rather than simple consequences of Zdiocranium to olfactory and otic components. cessation of development. I suggest that the Vertebral development also suggests trun- extensive mineralization of the spheneth- cation of development. Retention of a post- moid complex, including its domed shape and tail notochord and. lack of ossification of ter- rounded completeness dorsally and ven- minal vertebrae and ribs suggest that devel- trally, and the extensive ossification of the opment stopped before these elements were mesethmoid are correlated with the burrow- completed. Development in caecilians is ing mode of the species and compensate for highly cephalized, the last body segments HETEROCHRONY AND MINIATURIZATION IN CAECILIANS 15 forming well after gastrulation is complete Alberch, Museum of Comparative Zoology, (Wake, unpublished observation).An individ- Harvard University, and Kenneth A. Joysey, ual embryo, fetus, or juvenile is in effect an Museum of Zoology, Cambridge University, ontogenetic series as a consequence of this also graciously loaned specimens. Kath anteroposterior sequence of development. Thomas, Cindy Hillery, and Addye Brown Yet, only Idiocranium retains the notochord prepared the sectioned material. This work and terminal chondrification in adulthood. A was supported by the National Science diversity of developmental variations of ter- Foundation. minal ends of tails obtains, including the postnotochordal tail of lungfish and salaman- LITERATURE CITED ders (Percy, ’62), and of some teleosts (Meu- Alberch, P., S.J. Gould, G.F. Oster, and D.B. Wake (1979) nier and Kirschbaum, ’78, ’791, but these are Size and shape in ontogeny and phylogeny. Paleobiol- unlike the skeletal variance in Idiocranium. ogy 5~296-317. I do not see that any functional advantage Bemis, W.E., K. Schwenk, and M.H. Wake (1983) Mor- phology and function of the feeding apparatus in Der- can be attributed to such vertebrae and sug- mophis mexicanus (Amphibia: Gymnophiona). Zool. J. gest that their lack of development is corre- Linn. SOC.77~75-96. lated with a genetic or epigenetic truncation Gould, S.J. 11977) Ontogeny and Phylogeny. Cambridge, of development. Mass: Harvard University Press. Hanken, J. (1984) Miniaturization and its effects on cra- The evolutionary mechanism through nial morphology in plethodontid salamanders, genus which miniaturization in this taxon is Thorius (Amphibia: Plethodontidae): I. Osteological achieved appears to be the heterochronic variation. Biol. J. Linn. Sac. 23~55-75. phenomenon of progenesis (Gould, ’77; Al- Kuhlenbeck, H.(1922) Zur Morphologie des Gymnophi- onengehirns. Jen. Zeit. Med. Nat. 58~453484. berch et al., ’79) which typically results in Lawson, R. (1966) The development of the centrum of paedomorphosis and size decrease. The epi- Hypogeophis rostratus (Amphibia, Apoda) with special genetic alteration of the developmental pro- reference to the notochordal (intervertebral) cartilage. gram relative to other species of caecilians J. Morphol. 118~137-148. Lawson, R. (1970) The caecilian cardio-vascular system that produces the osteological, myological, and intra-amphibian relationships. J. Zool. Lond. and other features of small size in Idiocrun- 160~199-299. ium may be a consequence of early initiation Marcus, H. (1923) Beitrag zur Kenntnis der Gymnophi- of 0, the offset of development signal. This onen VI. Uber den Ubergang von der Wasser - zur Luftatmung mit besonderer Beriicksichtigung des hypothesis is corroborated by the presence of Atemmechanismus von Hypogeophis. Zeitschr. Anat. a number of features of structure in large Entw. 69:328-343. Idiocranium as noted above that are features Meunier, F.J., and F. Kirschbaum (1978) Etude anato- of fetal, larval, or juvenile stages of other, miaue et histoloeiaue du sauelette axial de Eipenman- niLuirescens (Rgahphichtiyidae, Gymnotoidii). Acta related, species. Another heterochronic mode, Zool. (Stockh.) 59:215-228. neoteny, with prolonged growth, character- Meunier, F.J., and F. Kirschbaum (1979) Etude anato- istically produces paedomorphosis not neces- mique et histologique du squelette axial de la region sarily associated with size change. When size caudale de Gymnarchus niloticus. Arch Zool. Exp. Gen. 120:415-430. is affected through neoteny, however, it is in Naylor, B.G., and R.A. Nussbaum (1980) The trunk mus- the direction of gigantism, not miniaturiza- culature of caecilians (Amphibia: Gymnophiona). J. tion, and hypertrophy of elements, not Morphol. 166~259-273. reduction. Nussbaum, R.A. (1977) Rhinatrematidae: a new family of caecilians (Amphibia: Gymnophiona). Occ. Pap. Mus. All of the evidence points to progenesis as Zool. Univ. Mich. 682:l-30. the phenomenon responsible for much of the Nussbaum, R.A. (1983) The evolution of a unique dual structure, and possibly much of the biology, iaw-closingY mechanism in caecilians (Amohibia: Gvm- of Idiocranium. Corroboration awaits anal- nophiona) and its bearing on caecilian ancestry. J. Zool. Lond. 199:545-554. yses and comparison of the “ontogenetic tra- Nussbaum, R.A., and B.G. Naylor (1982) Variation in jectory” of the species, and recollection in the trunk musculature of caecilians (Amphibia: Gym- order to contribute crucial data on popula- nophiona). J. Zool. Lond 198~383-398. tion biology, ecology, and behavior. Parker. H.W. (1936) The amohibians of the Mamfe Divi- son, Cameroons. (1) Zoogeography and systematics. ACKNOWLEDGMENTS Proc. Zool. Sac. Lond. 1936~135-163. Pattle, R.E., C. Schock, J.M. Creasey, and G.M. Hughes I am particularly grateful to A.G.C. Gran- (1977) Surpellic films, lung surfactant, and their cellu- dison of the British Museum, Natural His- lar origin in newt, caecilian, and frog. J. Zool. Lond. 182~125-136. tory, for loan of the paratype series and for Percy, R. (1962) The post-notochordal tail in Dipnoi and permission to prepare some specimens for os- Urodela. Trans. Zool. Soc. Lond. 29~357-391. teological and histological examination. Pere Sanderson, I.T. (1937) Animal Treasure. New York Vi- 16 M.H. WAKE

king Press. Wake, M.H. (1980a) Morphometrics of the skeleton of Taylor, E.H. (1968) The Caecilians of the World A Taxo- Dermophis mexicanus (Amphihia: Gymnophiona). Part nomic Review. Lawrence, Kans.: University of Kansas I. The vertebrae, with comparisons to other species. J. Press. Morphol. 165t117-130. Taylor, E.H. (1969) Skulls of Gymnophiona and their Wake, M.H. (1980b) Fetal tooth development and adult significance in the of the group. Univ. Kan- replacement in Dermophis mexicanus (Amphibia: sas Sci. Bull. 48585-687. Gymnophiona): fields versus clones. J. Morphol. Taylor, E.H. (1972) Comparative anatomy of caecilian 1661203-216. anterior vertebrae. Univ. Kansas Sci. Bull. 51:219- Wake, M.H. (1980~)Structure and function of the male 231. Mullerian gland in caecilians, with comments on its Wake, D.B. (1970) Aspects of vertebral evolution in the evolutionary significance. J. Herpetol. 15t17-22. modern Amphibia. Forma et Functio 3:33-60. Wake, M.H. (1982) Diversity within a framework ofcon- Wake, M.H. (1968) Evolutionary morphology of the cae- straints: amphibian reproductive modes. In D. Mossa- cilian urogenital system. Part I. The gonad and fat kowsky and G. Roth (eds.): Environmental Adaptation bodies. J. Morphol. 126:291-332. and Evolution. Stuttgart Gustav Fischer, pp. 87-106. Wake, M.H. (1970a) Evolutionary morphology of the cae- Wake, M.P.H. (1985) The comparative morphology and cilian urogenital system. Part 11. The kidneys and the evolution of the eyes of caecilians (Amphibia: Gymno- urogenital ducts. Acta Anat. 75321-358. phiona). Zoo. Morph. 105:277-295. Wake, M.H. (1970b) Evolutionary morphology of the cae- Wake, M.H., and G.Z. Wurst (1979) Tooth crown mor- cilian urogenital system. Part 111. The bladder. Herpe- phology in caecilians (Amphibia: Gymnophiona). J. tologica 26:120-128. Morphol. 1591331-342. Wake, M.H. (1972) Evolutionary morphology of the cae- Wake, M.H., and J. Hanken (1982) The development of cilian urogenital system. Part N.The cloaca. J. Mor- the skull of Dermophis mexicanus (Amphibia: Gymno- phol. 136:353-366. phiona), with comments on skull kinesis and amphib- Wake, M.H. (1974) The comparative morphology of the ian relationships. J. Morphol. 173t203-223. caecilian lung. Anat. Rec. 178:483. Wever, E.G. (1975) The caecilian ear. J. Exp. Zool. 191353- Wake, M.H. (1976) The development and replacement of 72. teeth in vivparous caecilians. J. Morphol. 148:33-64. Wever, E.G., and C. Gans (1976) The caecilian ear: fur- Wake, M.H. (1977a) Fetal maintenance and its evolu- ther observations. Proc. Natl. Acad. Scie. 73:3744- tionary signfkance in the Amphibia: Gymnophiona. J. 3746. Herpetol. 11t379-386. White, J.S., and I.L. Baird (1982) Comparative morpho- Wake, M.H. (197713) The reproductive biology of caecili- logical feat,ures nf t,hs caecilian inner ear with com- ans: an evolutionary perspective. In S. Guttman and ments on the evolution of amphibian auditory D. Taylor (eds.): The Reproductive Biology of the Am- structures. Scan. Elect. Micr. 1982t1301-1312. phibia. New York: Plenum Press, pp. 73-102.