Evidence for the presence of nasal salt glands in the Hadrosauridae (Ornithischia)

Journal of Arid Environments (1981) 4, 43-57

Evidence for the presence of nasal salt glands in the Hadrosauridae (Ornithischia)

Peter

J.

Whybrow*

Accepted 11 February 1980 The subcutaneous nasal glands of some Recent reptiles and birds, mainly secreting salts of sodium and potassium, are sometimes contained within depressions in the skull; they lie above or in front of the orbit. Similar preorbital or circumnarial depressions in the skull of certain ornithischian dinosaurs (Hadrosaurinae) and lateral chambers within the hollow crests of others (Lambeosaurinae) may therefore have contained similar glands; 'troughs' in the premaxillae below the external nares would have prevented hypertonic solutions from entering the mouth. In the genus Parasaurolophus the nasal bones appear to have migrated into the distal part of the crest. The nature of the sediments and of the flora of the Late Cretaceous of north-western North America suggests that salt glands would have been essential to hadrosaurs, which fed on harsh terrestrial vegetation growing in a salt-rich environment.

Introduction The bizarre supracranial development in the Lambeosaurinae (Fig. 1) has been a source for speculation since Lambe (1920) showed the crests to be hollow and comprised of a series of convoluted passages formed by paired premaxillary and nasal bones. Numerous theories describing crest function in these ornithopod ornithischian dinosaurs can be dismissed as highly improbable. For example, Nopcsa (1929) believed that males had crests but females did not. This simple idea was easily shown to be false by Sternberg's stratigraphical evidence that Nopcsa's 'males' became extinct earlier than his 'females'. Improbable also are the suggestions that the crest was used as a defensive weapon (Abel, 1924) or as an attachment area for a proboscis (Wilfarth, 1938). Because of the probable semiaquatic habits of these animals, Colbert (1945, 1955) and Romer (1945) imagined them submerged for long periods using air stored in the crest. Considerations of hydrostatic pressure and volume invalidate this theory and likewise Sternberg's contention (1935, 1939, 1942, 1953) that the crest cavity prevented water from entering the lungs during underwater feeding. Wiman's belief (1931) that hadrosaur's 'bellowing' capacity might have been increased if the crest cavity acted as a resonating chamber has been resuscitated by Heaton (1971). Earlier workers tended to overlook two factors in forming their theories. First, the internal volume of the crest cavity in the fossil cannot be the same as that in the living animal. Epithelial tissue, cartilage, glandular masses and nasal mucosa would have reduced the internal air capacity. Second, any interpretation of crest function in lambeosaurines must also explain why the contemporary subfamily Hadrosaurinae, lacking crests, did not develop similar structures; this is important as the postcranial anatomy is, excepting minor differ• Department of Palaeontology, British Museum (Natural History), Cromwell Road, London

SW7 SBD, U.K.

0140-1963/81/010043+17 S02.00/0

© 1981 Academic Press Inc. (London) Limited

44

P. ]. WHYBROW

Ca)

Cb)

CC)

Cd)

(8)

en

Figure 1. Variation in crest shape and size in lambeosaurines. AIl skuIl silhouettes show the crest is formed by the dorsal growth of the nasal and premaxillae bones (black). (a) Corythosaurus

intermedius; (b) Lambeosaurus magnacristatus; (c) Corythosaurus frontalis; (d) Corythosaurus casuarius; (e) Corythosaurus brevicristatus; (f) Lambeosaurus lambei. All skulls are drawn to a

common scale and are after Dodson (1975).

ences, essentially the same and conservative in both subfamilies (Ostrom, 1961). Further, except for the nasal and premaxillary bones, the hadrosaurine skull maintains a conservative form; this emphasises Romer's point (1945) that the principal diagnostic feature of the various hadrosaurid genera is the degree of expansion of the bones surrounding the external nares. The large number of hadrosaur skulls found and their superb state of preservation (Plate 1) has facilitated recent detailed studies such as those by Ostrom (1961, 1963), Heaton (1972), Hopson (1975), Dodson (1975) and Weishampel and Jensen (1979). Ostrom (1961) reasonably suggests that the expansion of the narial tract is to improve the olfactory capability of larnbeosaurines in seeking food and evading predators. However, Ostrom himself notes that the hadrosaurines, lacking crests, failed to adopt a similar olfactory improvement. Dodson's allometric study on 36 lambeosaurine skulls provides a more reasoned base for any interpretation of crest function by showing the genus Procheneosaurus to be a juvenile of Corythosaurus. He also suggests that Cheneosaurus may be a juvenile of Hypacrosaurus. Further he shows that the valid lambeosaurine species from the Oldman Formation (Middle Campanian) are Corythosaurus casuarius Brown and Lambeosaurus lambei Parks, both with male and female forms osteologically distinguishable; L. magnacristatus Sternberg, with male and female forms possibly distinct; and the enigmatic Parasaurolophus walkeri Parks.

EVIDENCE FOR SALT GLANDS IN ORNITHISCHIA

45

Cb)

ee)

Cd)

Figure 2. Skulls of four hadrosaurines (flat-headed) to show the pre-orbital depression containing the salt gland (stippled). (a) Edmontosaurus; (b) Prosaurolophus; (c) Saurolophus; (d) Lophorthon. After Hopson (1975).

Lambe (1920) proposed a third subfamily, the Saurolophinae, to include those hadrosaurs having solid, incipient crests (Fig. 2(c)). The present paper follows Sternberg's classification (1953, 1954) in which only two subfamilies of the Hadrosauridae are recognised, the Hadrosaurinae and the Lambeosaurinae and notes. the irreconcilable problem (Ostrom, 1961) that the type-genus of the family, Hadrosaurus foulki Leidy, cannot be placed in either subfamily because the skull is unknown. Although I have only one hadrosaur skull available for examination, the published evidence suggests to me that recent work on nasal salt glands in Recent reptiles and birds might apply to hadrosaurian dinosaurs. The physiological importance of a nasal salt gland to hadrosaurs wiIl be discussed. The suggestion by several workers, Broom (1913), Ewer (1965), Halstead (1975) and Charig (1979), that a salt gland was located in the antorbital fossa of some thecodonts and some dinosaurs is discussed and can be dismissed. During the final preparation of this paper, Osmolska (1979) published a paper entitled 'Nasal salt gland in dinosaurs'. Her contribution will be discussed. Salt glands in Recent reptiles and birds

The term salt gland denotes any gland in the head of reptiles and birds which, irrespective of anatomical origin, has an osmo-regulatory function and secretes hypertonic solutions of sodium and/or potassium. By definition this term therefore includes the lachrimal, posterior orbital and nasal gland of marine and terrestrial reptiles and the nasal gland of marine and terrestrial birds. Nasal glands in reptiles and birds have been known for some time but their function was not proved until 1957 when Schmidt-Nielsen et al. showed that in oceanic birds the gland secreted a hypertonic solution of sodium chloride. Since 1957 the importance of a salt secretory gland to extinct reptiles and birds has been ignored by most palaeontologists even though evidence exists for their presence especially in marine animals. Marsh (1880) described supra-orbital depressions in Hesperornis and Ichthyornis which have recently

46

P.

r. WHYBROW

(Whybrow, ms.) been suggested to contain salt glands. Similarly, depressions can be seen in the posterior nasal region of the ichthyosaur Ophthalmosaurus (Why brow, personal observation). Historically, the glands probably first appeared in the Amphibia, serving to clean and moisten the nasal passages. Bolt (1974) believed such a gland to be present in a trematopsid amphibian. When the vertebrates became truly terrestrial they lost two avenues for osmotic and ionic exchange, the gills and the skin; consequently it would be necessary for water and salt regulation to be partly taken over by the salt glands as both the reptilian and the avian kidneys are known to be less efficient in concentrating salts than is the mammalian kidney. Further, any animal able to excrete salt quickly through the gland would be able to minimise water loss and take advantage of a salt rich diet. For example, the herbivorous marine iguana (Amb£vrhynchus cristatus) is uniquely adapted to the rocky shores of the Galapagos archipelago. When on land it is continually bathed in salt spray and has no access to freshwater. It is an excellent swimmer and feeds from underwater beds of algae (Viva) which are in osmotic equilibrium with sea water and high in potassium salts. Appropriately, the marine iguana has a large nasal salt gland, constituting 0·06 per cent of its body weight and extending over the orbits (Fig. 3). Schmidt-Nielsen & Fange (1958) examined this animal and found a short duct empties the secretions into the nasal cavity which acted as a reservoir for the secreted fluids; the posterior part of the narial tract is here partly occluded by an S-shaped ridge which prevents the fluids from flowing back into the oesophagus; this is important for comparison with fossils. The fluid is expirated as a shower of fine drops (Darwin, 1889). The marine iguana has one of the highest rates of sodium salt secretion and the highest known rate of potassium salt secretion of any reptile, the latter obviously reflecting its specialised diet. Similarly, the Galapagos land iguana feeds mainly on cactus and, again in an area lacking freshwater, secretes as much as 50 times more potassium salts than sodium. The iguanas and those xerophilic lizards having salt glands can vary the ratio of sodium and potassium salts according to their diet or environment. One reason for this is that the duct system, as far as but not including the keratinised external nares, contains a layer of columnar epithelial cells similar in structure to the main secretory cells of the salt gland. The ducts could therefore act to modify the primary secretion from the gland by reabsorbing or secreting chlorides and bicarbonates of sodium or potassium (peaker & Linzell, 1975).

Figure 3. The Marine Iguana, Amblyrhynchus cristatus, with the supra-orbital and nasal area dissected to show the large nasal salt gland (black). Redrawn from Peaker and LinzeII (1975).

EVIDENCE FOR SALT GLANDS IN ORNITHISCHIA

n

47

ant

Figure 4. Dissection of the nasal region of an Ostrich, Struthio camelus, to show the position of the nasal salt gland (black) lying in the anterior part of the frontal. The duct from the gland passes through the antorbital fossae to the nostrils. The frontal (fro) and the lachrimal (lac) are indicated, also the position of the external nares (n) and the antorbital fossa (ant). Adapted from Technau (1936). Technau (1936) found the ostrich to have large nasal glands with ducts to the external nares. Schmidt-Nielsen (1963) showed that exposing an ostrich to high ambient temperatures and depriving it of freshwater prompted salt secretion. The fluid collected show high and variable concentrations of potassium and sodium salts; the potassium concentration was 5 to 10 times higher than that of sodium, an obvious advantage to the ostrich as it is known to drink from soda and salt lakes (Schmidt-Nielsen, 1964). Important from the palaeontological viewpoint, the ostrich skull is modified to accommodate the salt glands (Fig. 4), with troughs some 4 mm deep in the anterior edge of the frontals. Similarly, the Emperor Penguin which eats marine fishes and lives in a habitat without freshwater, has extensive troughs over the orbits to accommodate large salt glands, (Plate 2). The above examples show the importance to an animal of a salt-secreting mechanism which enable it to survive in a hostile environment. Especially interesting is that the presence of salt glands can be deduced from troughs and depressions, in the frontal and supraorbital regions.

Innervation and blood supply to the salt glands There is little information concerning these matters in Recent reptiles, but information published on Recent birds (Hanwell et al., 1971a, b) is relevant. Blood is supplied to the gland at all times and especially so during secretion. The artery to the gland, the internal ophthalmic, arises from the internal carotid and, after following the orbital wall divides into anterior and posterior branches, to the anterior and posterior areas of the gland respectively. The anterior branch continues to the beak. During secretion, usually when the bird is at rest, cardiac output increases dramatically so that there is an increase in blood flow through all organs but most of all through the salt glands. In geese, for example, kidney blood flow is about 8 ml g-I min -I, cardiac muscle flow 2·2 ml g-I min -1 while salt gland blood flow may be as much as 26·9 ml g-I min-I. Ducts from the glands pass anteriorly to the external nares and secretions are either shaken out by the bird or flow along premaxillary grooves to drip off the tip of the beak. Both methods help prevent secretions from entering the mouth. Innervation appears to be from a ganglion (not the Gasserian) closely applied to the Vth cranial nerve (peaker & Linzell, 1975) where it passes through the orbit (Fig. 5). Dissection of the nerves is difficult as they pass through dense bone, but staining techniques show that fibres from the vnu and IXth cranial nerves enter this ethmoidal or 'secretory nerve' ganglion. Given this information for Recent animals, can the location of salt glands be shown in hadrosaurian dinosaurs?

48

P. J. WHYBROW

Figure 5. Innervation of the salt gland by the secretory nerve ganglion (sec) which is closely applied to the Vth cranial nerve (Vth). Preganglionic fibres (pre) and postganglionic fibres (pos) are indicated, and the salt gland has been partly sectioned. After Peaker and Linzell (1975).

Hadrosaur salt glands Hopson (1975) suggested that the cranial crests of hadrosaurs were used for display. He believes that the strongly depressed areas surrounding the external nares in flat-headed and solid-crested hadrosaurs housed an inflatable diverticulum that served as a visual display organ. He thought that the preorbital nasal humps in Kritosaurus, Lophorhothon, Prosaurolophus indicated stages in the evolution of the hump (Fig. 6) as a principal combat weapon. In the hollow-crested lambeosaurines, Hopson inferred that the diverticula were present between the dorsal margin of the lower lobe of the premaxilla and the nasal, two elements which fail to meet in all lambeosaurines and between which there is a gap leading into the crest cavities. Further (p. 41), 'In lambeosaurines, the nasal bones and premaxillae have grown around the diverticula so that they are incorporated into the bony skull.' He then suggests that the 'nasal specialisations of lambeosaurines are best interpreted as modifications serving to enhance vocalisation function', also, 'The elevation of the nasal capsule and diverticula to the dorsal surface of the skull would have formed a conspicuous swollen dome on the head.' I agree with Hopson that Hadrosauridae may have had inflatable diverticula, but I believe he has over-emphasised their importance and influence on the facial area of the skull. Ostrom (1961) emphasised that the hadrosaurian hollow crest is definitely related to the nasal apparatus, to which the circumnarial depressions in flat-headed forms are likewise related. Versluys (1936) believed that the narial depressions accommodated cartilaginous nasal capsules and gland masses while Heaton (1972), referring to Corythosaurus excavatus, believed Jacobson's organ to have been present and 'confined to the region of premaxillonasal contact where the passages united'. Thus, using Recent animals as analogues the circumnarial depressions in hadrosaurines may have contained salt glands. The convolutions within the crests of lambeosaurines may be due to the presence of salt glands or their duct system. The crests themselves may also have served two other functions, recognition within species or thermoregulation. The size of these herbivorous dinosaurs (?2-3 tons) shows they must have eaten large amounts of plant material; the nasal salt glands were presumably correspondingly large in order to remove the excessive amounts of salts absorbed. The secretions from the glands must therefore have been copious and there is evidence of this. In all hadrosaurs the area

Plate 1. Skull of Corythosaurus casuartus (AMNH 5338). The salt gland is believed to have lain

over most or part of the upper premaxillary lobe (pm'). The lower premaxillary lobe (pm) and the nasal are indicated. Photograph courtesy of the American Museum of Natural History.

[ facin.~

/Jag, 4HI

Plate 2. The deep 'troughs'

III

the skull of the Emperor Penguin, Aptenodytes forsteri, are indicated by arrows.

EVIDENCE FOR SALT GLANDS IN ORNITHISCHIA

A

49

(f)

~

(Cl/2~;~ ,'''

se-.

( e)

f·~~~:;',.r.: .: ~-c

'---" (b)

/

Figure 6. Hopson's morphological stages in the 'evolution' of the lateral diverticula (stippled) and cranial crests from a kritosaur ancestor (a). (b) Lophorhothon; (c) Prosaurolophus; (d) Saurolophus ; (e) Edmontosaurus ; (f) Corythosaurus. Redrawn from Hopson (1975). of the beak below the external nares has a strongly concave upper surface (Ostrom, 1961) that may have been covered by keratinised tissue in life. This 'trough' seated in the flared premaxillae would have prevented any secretions from entering the mouth. An analogous device is present in ducks and geese where ridges along the margin of the bill stop the secretions, emerging from the external nares, from flowing into the mouth. As mentioned above, innervation of the salt gland is from a ganglion closely applied to the Vth cranial nerve. Ostrom (1961, fig. 64) shows the deep groove of the ramus opthalmicus, the sensory branch to the snout, branching off anterior to the trigeminal foramen in Corythosaurus and Lambeosaurus and suggests a similar condition in Anatosaurus. Blood supply to the gland via the internal ophthalmic should be shown by the presence of foramina and this is seen in Kritosaurus incuroimanus Parks (R.O.M.P. 4514) (Parks 1920) where foramina pass through the nasal below the preorbital 'hump'. This suggests that the subcutaneous salt glands lay in the preorbital depressions, with ducts passing to the external nares. The salt glands can be reconstructed in lambeosaurines by using Ostrom's detailed description of the cavities in 'Corythosaurus excavatus', which is actually a female of C. casuarius (Dodson, 1975). Briefly described here, the narial passages ascend posteriorly and convolute to form two S-shaped passages separated by median lamellae of the dorsal processes of the premaxilla. The passages then expand into inferior lateral chambers which join into a common median dorsal chamber. A common canal then descends into the internal nares (Heaton, 1971). It is interesting that the S-shaped passages resemble those of the marine iguana. The ventral part of this passage could then have acted as a trap for fluids secreted from the glands housed in the inferior lateral chambers. Perhaps the suggested subcutaneous position of the gland in the flat-headed hadrosaurs is the same in the crested forms, as I agree with Hopson that the premaxillae and nasal bones 5

P.

50

r. WHYBROW

have grown around all the organs of the circumnarial depressions. However, it is puzzling why the dorsal part of the premaxillary lobe and nasal fail to meet in lambeosaurines (except Parasaurolophus, but see below). Perhaps the glands lay near the gap between these bones, their ducts leading either into the crest cavities or subcutaneously down the strong groove formed by the premaxillary lobes and then via the nasal cavity to the external nares. Ostrom (1962) suggested that the function of the crest passages was to increase the area for olfaction. It has recently been shown (Dodson, 1975), that the genus 'Procheneosaurus' is actually a juvenile of Corythosaurus; the dorsal growth of the premaxillae and nasal bones, which leaves no sign of the internasal vacuity seen in flat-headed forms, becomes apparent only when body weight reaches about one-third of the estimated adult value. If Ostrom's suggestion is correct, then juvenile corythosaurs would seem to have had poorer olfaction than their parents. On the other hand, Dodson (1975) suggested this growth of the crest indicated the onset of puberty; although expansion of the crest at puberty might playa role in sexual display, it could just as well indicate an increase in salt gland function with increase in body size. The enigmatic genus Parasaurolophus is known only from four specimens no two of which are contemporaneous and there is only one complete skull, P. walkeri. The crest in this genus is apparently entirely formed by the premaxillae and details of the internal structure are known only from P. cyrtocristatus (Ostrom, 1963) and an indeterminate Parasaurolophus species (Weishampel & Jensen, 1979). It is therefore difficult to do more than suggest where the salt glands were in this genus. As previously mentioned, in the Lambeosaurinae the premaxillae and the nasals grew around all organs within the nasal cavity and moved them upwards and backwards to the top of the skull. In P. walkeri the greater part of the tubelike crest is formed by the premaxillae and still shows the deep external groove which, in Corythosaurus casuarius, separates the two lobes of that bone. Parks (1922) noted in his description of the crest in P. walkeri (Fig. 7(b)) that this groove terminates distally in or near two deep pits. He states that the inferior pit 'is so deep that it cannot be separated from its fellow of the opposite side by more than 25 mm. The superior pit is smaller and seems to pass through the terminal expansion as a sort of slit like opening'. Slightly below the dorsal curve of the upper lobe of the premaxilla, 170 mm from the end of the crest, another deep pit is described continuing distally as a groove. Above and behind the first pit is a rugose area 55 mm in length.

/,,).'::'~:~'

"';".

~~ (a)

Figure 7. Parasaurolophus walkeri showing (a) the detail at the distal part of the crest that suggests the remains of the nasals, and (b) the only complete known skull of Parasaurolophus, (a) redrawn from Parks (1922) and a cast of P. walkeri; (b) from Ostrom (1963).

EVIDENCE FOR SALT GLANDS IN ORNITHISCHIA

51

I suggest this area may be homologous with the upper and lower premaxillary lobe area in C. casuarius and therefore represents the remains of the nasals (Fig. 7(a)). Thus the element at the base of the crest which Russell (1946) described as the nasal would actually seem to be the prefrontal. Weishampel & Jensen (1979, fig. 2) also conclude this bone to be the prefrontal though their interpretation of the, position of the nasal bone differs from that described above. My examination of a cast of P. walkeri leads me to believe that the pits noted by Parks do exist and that salt glands may have been situated within the distal parts of the crest passages. However, I cannot suggest the route by which secretions reached the exterior other than by the external nares. Perhaps, as suggested for C. casuarius, the glands were subcutaneous; if so secretions could have flowed through ducts situated in the grooves between the upper and lower lobes of the premaxilla.

Salt glands situated in the antorbital fossae In some archosaurs one or more antorbital fossae are present. Broom (1913) in his description of the Triassic pseudosuchian Euparkeria suggested that this opening may have housed a gland. Ewer (1965) thought the fossae in this animal contained salt glands, a suggestion also published by Halstead (1975) and Charig (1979). This idea can be dismissed for two reasons. (1) In Recent birds salt glands are never located in antorbital fossae. The fossae are covered by skin that slightly expands and contracts as the bird breathes. The fossae therefore function as part of the respiratory system. (2) In Recent birds and reptiles that have a nasal salt gland, the gland is always positioned in a bony trough or depression and never in a hole in the skull. The Hadrosaur environment Having shown that hadrosaurs probably possessed salt glands, the published evidence of their environment must be examined for clues as to why this function would have been beneficial. The sediments help to understand the environment utilised by hadrosaurs. From the Upper Aptian Cloverly sequence to the extinction of the hadrosaur fauna in the Late Maestrichtian, the sediments of western North America are typified by cycles of freshwater fluviatile deposits that inter-finger or merge with brackish or marine sediments. This depositional sequence was influenced by the Laramide orogeny and the Cretaceous epicontinental sea. The orogeny to the west of the shallow basin gave rise to periods of volcanicity which frequently deposited ash over large areas of terrestrial and shallow marine sedimentation. Bentonites occur throughout the Cloverly (Ostrom 1970), Fox Hill (Waage, 1968), Edmonton (Russel & Chamney, 1967) and western Oldman (Lerbekmo, 1963) Formations. The lateral impersistence of some rock types is striking in the terrestrial deposits compared with the lateral continuity of coal or lignite beds as found in the Edmonton (Allan, 1922) and Hell Creek (Waage, 1968) Formations. Sandstones, siltstones and claystones form diachronous local units (Dodson, 1971). In the sandstone, where almost all hadrosaur fossils are found, clay pebbles are common and indicate reworking of the underlying clays by increased stream flow. In the Edmonton, a brackish water fauna has infiltrated freshwater strata to form the Drumheller tongue (Tozer, 1956), a 50 ft series of sandy limestones containing oyster shells some 600 ft above the marine Bearpaw Formation. Sandy coquinoid limestones from the Red Deer River (Ower, 1960; Tozer, 1956) and foraminifera from two Oldman samples (Dodson, 1971) show terrestrial sedimentation to have been interrupted by brackish conditions. Conversely, the marine deposits show signs of terrestrial influence. The Fox Hills Formation which underlies the hadrosaur bearing Hell Creek beds has been considered by Waage (1968) to be equivalent to a considerable part of the Lance series. Within the Fox Hills Iron Lightning member, Waage found hadrosaur teeth, dinosaur limb

52

P. J. WHYBROW

bones and vertebrae, theropod claws and bird bone fragments. In addition, the earliest known hadrosaur, Claosaurus, was found in the shallow marine Niobrara Chalk. Dodson (1971) suggests a braided stream environment for the Oldman Formation. I suggest that such an environment was present from the deposition of the Cloverly Formation up to the time of hadrosaur extinction at the end of the Cretaceous. To summarise the North American depositional events, I quote from Allen (1975) whose description of Lower Cretaceous events in the Wealden Formation of England is comparable. He states, 'Such rapid and repetitive transformations of a fresh-to-brackish mudswamp into an extensive sandplain, with little increase in average water level, require tectonic or climatic explanations. The new facies model supposes the periodic uplift of the horsts increased the river gradients and frequencies of storm and flood, leading to the development of braided streams; and then, possibly, of confluent alluvial fans. Subsequent downfaulting or geomorphic decay of the blocks reduced streamflow and bedload, exposing nearby sands and gravels to denudation. Finally, as in the deltaic model, the eroded sandplains sank beneath the abundant suspension load and the transgressive mudswamp regime reasserted itself, once more with tenuous marine connections and/or sensitivity to evaporation.' The major difference between this model and the North American strata is that the 'tenuous marine connections' were more dominant and transgressive.

The food of hadrosaurs Having described the sedimentological environment that hadrosaurs had to contend with, the flora growing on these sediments must be examined. The plants are very poorly known, probably because of their removal by the fluctuating levels of the braided stream systems. Ostrom (1964) describing hadrosaur dentition concluded that 'the teeth indicate a diet consisting of resistant, perhaps even woody terrestrial plants and are quite inconsistent with a diet of softer plant types of aquatic origin'. Also, 'comparable dentitions amongst modern herbivores are almost without exception used to grind siliceous, fibrous or woody tissues'. In correlating the meagre published flora of hadrosaur-bearing strata, suggestive of hadrosaur diet, Ostrom showed an average of 85 per cent terrestrial and 15 per cent aquatic flora to be present. Coprolites from the Oldman Formation show pollen of hemlock, various dicotyledons and monocotyledons (Lilliaceae, Typhaceae), (Waldman & Hopkins, 1970) and conifer pollen is absent. Obviously conifers do not shed pollen the year round. Sternberg (1926) despite "having spent many years collecting hadrosaurs, only records six autochthonous tree stumps, apparently conifers, from the Edmonton series; fossil logs range through but are uncommon in the Oldman. From this evidence it is likely that large coniferous forests did not exist, yet the fossilised needles of the conifer Cunninghamites elegans found in the stomach of a mummified flat-headed hadrosaur, Anatosaurus annectens, (Krausel, 1922), are frequently quoted as food for all hadrosaurs. Equally, this hadrosaur could have been poisoned by the conifer or the other fruits and seeds it had eaten. As hadrosaurs are eminently adapted as terrestrial bipeds, Ostrom argued strongly for their terrestrial diet and habitat despite previous suggestions that they were aquatic. I agree with Ostrom and suggest that a braided stream environment would create contiguous terrestrial and aquatic floral habitats for hadrosaurs to take advantage of. Except in times of flood, the terrain would have few areas of deep water for hadrosaurs to contend with; they were still terrestrial even if they waded thigh-deep through ponds or sluggish channels. One constituent of the Late Cretaceous flora that is definitely autochthonous is the scouring rush Equisetum (Dodson, 1975). Lull & Wright (1942) believed that it may have formed an important part of hadrosaur diet and I am sure they were correct. Equisetum has been found in hadrosaur-bearing strata of the Oldman, Edmonton and Lance Formations (Dodson, 1975; Russell & Chamney, 1967; Dorf, 1942; Berry, 1924). Patches of this plant, growing now, may be up to half a kilometre across and cover tens of square metres. The underground rhizomes survive washing out, fire, burial and drought (Hauke, 1963). Important as an all-year food supply to animals, the plant is normally evergreen and the aerial stems contain

EVIDENCE FOR SALT GLANDS IN ORNITHISCHIA

53

abundant starch. Equisetum can grow in poorly drained soil or in water 1 m in depth. Silica is formed in the aerial stems and, because of the deep root system of the rhizomes, high concentrations of mineral salts are found in the entire plant. Extensive beds of fossil Equisetum are found in the Lower Cretaceous Wealden deposits of England (Allen, 1941, 1947, 1959). If the occurrence of this plant in the Wealden and in the American Upper Cretaceous is comparable, then any dinosaur, such as the Wealden Iguanodon or an American hadrosaur, wishing to graze from the equivalent of a grassy field might feed mainly from Equisetum. Ostrom (1961) shows an antero-posterior movement of the lower against the upper teeth and notes occlusal striations parallel to the tooth row in Anatasaurus annectens. No doubt hadrosaurs varied their foraging much like any modern herbivore, but the siliceous stems of Equisetum would surely cause more tooth striae than any other terrestrial or aquatic fodder. The environment and hadrosaur salt glands An animal requires a salt gland if its food is rich in salt and its kidney cannot quickly excrete the excess ingested. The predominance of the clay minerals, montmorillonite, illite and bentonite, in the terrestrial sediments, indicates that the soils, and therefore the plants would be rich in sodium and potassium salts. Falls of volcanic ash would further add to the mineral complex of the soils. Differences of opinion exist regarding the Late Cretaceous climate. Subtropical, tropical and warm temperate conditions have been inferred. Dodson (1971) found 'rootlets' formed as tubes of oxidised iron in Oldman sediments, also calcareous concretions, ironstones and desiccation cracks. Sternberg (1926) noted sections of fossil trees encrusted with chalcedony and the medullary cavities of dinosaur bones filled with quartz. This example is important as it has been noted that in alkaline soils, particularly where the exchange complex is saturated with sodium, silica is especially mobile (Cooke & Warren, 1973). These features indicate that whatever the general Late Cretaceous climate there were dry periods enabling minerals to concentrate in the soils. Obviously plants living on these mineral-enriched soils would take up sodium and potassium salts as well as silica. Although Equisetum may have been the Late Cretaceous 'grass', its mineral salt content and that of, sedges, saxifrages, vines and viburnums (Ostrom, 1964) would have been so high that the presence of a salt-secretory gland in hadrosaurs would have been most advantageous. Discussion Recent birds inhabiting salt marsh areas have smaller salt glands (Fig. 8) than related forms feeding from estuarine or marine environments. Russell (1967, in Russell & Chamney, 1967) emphasised that the main factor controlling hadrosaur distribution is environment, not time. He suggests that on the basis of contemporaneous faunal correlations flat-headed hadrosaurines preferred environments associated with brackish water swamps while hollow-crested lambeosaurines preferred marginal lowlands of a more continental habitat. Certainly the circumnarial (preorbital) area available for salt glands is much greater in hadrosaurines than in an equivalent size lambeosaur. Enlargement of the gland prompted by a salty diet could occur more easily under the skin than when surrounded by bone. The size of the salt gland in hadrosaurines and lambeosaurines does seem to agree with the environmental distribution as suggested by Russell. However, increase in salt gland size in lambeosaurs could be accomplished by an increase in crest size. The disadvantage of enclosing the gland in bone might be offset by increasing the length of the duct system. I noted above the columnar cells similar to the salt gland cells are present in the reptilian duct system. Therefore, small gland size within the crest may he complemented by a long duct system as seen the duct (crest) length in Parasaurolophus. Further, increase in gland size might be seen as an increase in the size of the crest. Dodson

P. ]. WHYBROW

54

Ca)

Figure 8. Supraorbital size of the nasal salt gland in four species of wading bird that inhabit salt-marsh and estuarine environments. Note that the size of the salt gland increases owing to the time spent in feeding from a more marine environment. All species shown feed from invertebrates. Size of the gland increases towards the marine species (d). (a) Wood Sandpiper; (b) Common Sandpiper; (c) Knot; (d) Little Auk. From Peaker and Linzell (1975). Stippling shows the salt glands. (1975) shows Lambeosaurus magnacristatus to have the biggest lambeosaur crest and is a valid species, ecologically separate from other lambeosaurs, being found from an area more subject to marine influence. Against the suggestion made above, and previously, that the gland in lambeosaurs was contained within the crest, is that it maintained its subcutaneous position as suggested in flat-headed hadrosaurs. The glands' position would then be over most of the premaxillary lobe in front of the orbit. This would be the most simple suggestion for salt gland location in lambeosaurs, although I do feel that the duct system from the gland may have entered the crest passages. Finally, no hollow-crested hadrosaurs have yet been found in north western American deposits younger than those above the major marine transgression of the Bearpaw and Pierre sea. Yet flat-headed hadrosaurs together with the ubiquitous Triceratops (with salt glands?) still existed after this marine transgression. Perhaps a restricted habitat and climatic change at this time prompted an ecological 'barrier' to the survival of hollow-crested hadrosaurs but favoured their lowland swamp dwelling relatives.

Discussion on Osmolska (1979), 'Nasal salt gland in dinosaurs' This paper was received while the above was being finally prepared. It is pleasing to note that similar speculations on dinosaur physiology can be arrived at independently. However, there are significant differences between my speculations and those of Osmolska. First, she suggests that all large herbivorous dinosaurs possessed nasal salt glands. Second, as the external nares, in the fossil, are large with a distinct depression around them, she suggests that in this area salt glands were located. Intuitively, I cannot agree with Osmolska on the first point and, on the second, I am certain that the supra or preorbital position of the nasal gland in Recent birds and reptiles shows that innervation of it, and arterial blood supply to it, requires that the gland cannot be located within the external nares in dinosaurs. The term nasal salt gland means that the secretions exit via the external nares not that the glands were located within them. Also in Recent birds and reptiles, the ducts from the gland are long and can contain cells to modify the primary secretions. Despite the large nostril size in herbivorous dinosaurs, I do not believe there is space for the duct system, the gland and respiratory function. I agree with her conclusion that the antorbital fossae do not house salt glands. Also, I agree more with her 'less plausible alternative' which is that the development of a large salt gland 'may have been independent of the climatic conditions and drinking water supply'. Her alternative to this suggestion was that the salt gland developed in dinosaurs as a water saving mechanism during seasonal droughts. Although there were dry periods during the

EVIDENCE FOR SALT GLANDS IN ORNITHISCHIA

55

Late Cretaceous of North America, examination of the rocks does not indicate long periods of aridity that would prompt salt gland development by dinosaurs as a response to desert conditions. Conclusions Despite the hazards of speculating on certain physiological functions in extinct animals, there is evidence that hadrosaur dinosaurs possessed a nasal salt secretion gland. Preorbital circumnarial depressions housed the gland in flat-headed hadrosaurs. In crested hadrosaurs supracranial growth of the premaxillae and nasal bones either included the salt glands within part of the crest cavity or positioned the glands subcutaneously above the orbits. The duct system from the glands in lambeosaurs is thought to have passed through the crest cavities to the external nares. Examination of the sediments making the terrain of the hadrosaur habitat show potassium and sodium to have been present. The soils formed from these sediments would enable plants to further concentrate those minerals so that hadrosaur food would be high in potassium or sodium salts. Extra-renal excretion of these salts is required at the reptilian kidney cannot discharge large amounts of potassium, sodium and chloride salts. Expanded or flared premaxillary 'troughs' ventral to the external nares helped prevent salt solutions secreted via the salt gland duct system, which opens into the external nares, . from entering the mouth. Not all herbivorous dinosaur skulls have preorbital or supraorbital depressions that may have housed salt glands, so it is impossible to suggest that all herbivorous dinosaurs had salt glands. I sincerely thank John Attridge and Dr Alan Charig for their advice when considering my speculations on salt glands in hadrosaurs. I also thank Dr Dick Jefferies for his advice. References Abel, O. (1924). Die neuen Dinosaurierfunde in der Oberkreide Canadas. Naturtoissenschaften, 12: 709-716. Allan, J. A. (1922). Geology of the Drumheller coal field, Alberta. Research Council of Alberta, Report 4: 1-78. Allen, P. (1941). A Wealden soil-bed with Equisetites lyelli (Mantell). Proceedings of the Geologists' Association, 52: 362-374. Allen, P. (1947). Notes on Wealden fossil soil-beds. Proceedings of the Geologists' Association, 57: 303-314. Allen, P. (1959). The Wealden environment: Anglo-Paris basin. Philosophical Transactions of the Royal Society of London, B, 242: 283-346. Allen, P. (1975). Wealden of the weald: a new model. Proceedings of the Geologists' Association, 86: 389-437. Berry, E. W. (1924). The food value of an equisetum from the Lance formation of Saskatchewan. Canadian Field Naturalist, 38: 131-132. Bolt, J. R. (1974). Osteology, function and evolution of the trematopsid (Amphibia: Labyrinthodontia) nasal region. Fieldiana: Geology, 33: 11-30. Broom, R. (1913). On the South African pseudosuchian Euparkeria and allied genera. Proceedings of the Zoological Society of London, (1913): 619-633. Charig, A. J. (1979). A New Look at the Dinosaurs. London: Heinemann. 160 pp. Colbert, E. H. (1945). The Dinosaur Book. American Museum of Natural History Man and Nature Publication, 14: 156 pp. Colbert, E. H. (1955). Evolution of the Vertebrates. New York: John Wiley. 479 pp. Cooke, R. U. & Warren, A. (1973). Geomorphology in Deserts. London: Batsford. 374 pp. Darwin, C. (1889). Journal of Researches into the Natural History and Geology of the Countries Visited during the Voyage of H.M,S. Beagle Round the World. London: Nelson. 615 pp.

56

P. J. WHYBROW

Dodson, P. (1971). Sedimentology and taphonomy of the Oldman Formation (Campanian), Dinosaur Provincial Park, Alberta (Canada). Palaeogeography, Palaeoclimatology, Palaeoecology, 10: 21-74. Dodson, P. (1975). Taxonomic implications of relative growth in Lambeosaurine hadrosaurs. Systematic Zoology, 24: 37-54. Dorf, E. (1942). Upper Cretaceous flora of the Rocky Mountain region. Publications. Carnegie Institution of Washington, 508: 79-159. Ewer, R. F. (1965). The anatomy of the thecodont reptile Euparkeria capensis Broom. Philosophical Transactions of the Royal Society of London, B, 248: 379-435. Halstead, L. B. (1975). The Evolution and Ecology of Dinosaurs. London: Peter Lowe. 112 pp. Hanwell, A., Linzell, J. L. & Peaker, M. (1971a). Salt-gland secretion and blood flow in the goose. Journal of Physiology, 213: 373-387. Hanwell, A., Linzell, J. L. & Peaker, M. (1971b). Cardiovascular responses to salt-loading in conscious domestic geese. Journal of Physiology, 213: 389-398. Hauke, R. (1963). A taxonomic monograph of the genus Equisetum subgenus Hippochaete. Beihefte zur Nova Hedwigia, 8: 1-123. Heaton, M. J. (1972). The palatal structure of some Canadian Hadrosauridae (Reptilia: Ornithischia). Canadian Journal of Earth Sciences, 9: 185-205. Hopson, J. A. (1975). The evolution of cranial display structures in hadrosaurian dinosaurs. Paleobiology, 1: 21-43. Krausel, R. (1922). Die Nahrung von Trachodon. Palaeontologische Zeitschrift, 4: p. 80. Lambe, L. M. (1920). The hadrosaur Edmontosaurus from the upper Cretaceous of Alberta. Memoirs. Geological Survey Branch, Department of Mines, (and Technical Surveys) Canada. 102: 1-79. Lerbekmo, J. F. (1963). Petrology of the Belly River Formation. Sedimentology, 2: 54-86. Lull, R. S. & Wright, N. E. 1942. Hadrosaurian dinosaurs of North America. Special Papers. Geological Society of America. 40: 1-242. Marsh, O. C. (1880). Odontornithes: a Monograph on the Extinct Toothed Birds of North America. Washington: Government Printing Office. 201 pp. Nopcsa, F. (1929). Sexual differences in ornithopodous dinosaurs. Palaeobiologica. 2: 187-201. Ostrom, J. H. (1961). Cranial morphology of the hadrosaurian dinosaurs of North America. Bulletin of the American Museum of Natural History, 122: 33-186. Ostrom, J. H. (1962). The cranial crests of hadrosaurs. Postilla, 62: 1-29. Ostrom, J. H. (1963). Parasaurolophus cyrtocristatus, a new crested Hadrosaurian Dinosaur from New Mexico. Fieldiana, 14: 143-168. Ostrom, J. H. (1964). A reconsideration of the paleoecology of hadrosaurian dinosaurs. American Journal of Science, 262: 975-997. Ostrom, J. H. (1970). Stratigraphy and paleontology of the Cloverly Formation (Lower Cretaceous) of the Bighorn Basin area, Wyoming and Montana. Bulletin of the Peabody Museum History, 35: 1-234. Osmolska, H. (1979). Nasal salt gland in dinosaurs. Acta Palaeontologica Polonica, 24: 205-215. Ower, J. R. (1960). The Edmonton Formation. Journal of the Alberta Society of Petroleum Geologists. 8: 309-323. Parks, W. A. (1920). The osteology of the trachodont dinosaur Kritosaurus incurvimanus. University of Toronto Studies. Geological Series, 11: 1-74. Parks, W. A. (1922). Parasaurolophus walkeri, a new genus and species of crested trachodont dinosaur. University of Toronto Studies. Geological Series, 13: 1-32. Parks, W. A. (1923). Corythosaurus intermedius, a new species of trachodont dinosaur. University of Toronto Studies. Geological Series, 15: 1-57. Peaker, M. & Linzell, J. L. (1975). Salt Glands in Birds and Reptiles. Monographs of the Physiological Society. No. 32. Cambridge: Cambridge University Press. 307 pp. Romer, A. S. (1945). Vertebrate Paleontology (2nd ed.), Chicago. University of Chicago Press. 491 pp. Russell, D. A. (1967). A census of dinosaur specimens collected in western Canada. Natural History Papers. National Museums of Canada, 36: 1-13. Russell, D. A. & Chamney, T. P. (1967). Notes on the biostratigraphy of dinosaur and microfossil faunas in the Edmonton Formation (Cretaceous), Alberta. Natural History Papers. National Museums of Canada, 35: 1-22.

EVIDENCE FOR SALT GLANDS IN ORNITHISCHIA

57

Russell, L. A. (1946). The crest of the dinosaur Parasaurolophus. Contributions of the Royal Ontario Museum of Zoology and Palaeontology, 11: 1-5. Schmidt-Nielsen, K, Jorgensen, C. B. & Osaki, H. (1957). Secretion of hypertonic solutions in marine birds. Federation Proceedings, 16: 113-114. Schmidt-Nielsen, K & Fange, R. (1958). Salt glands in marine reptiles. Nature, 182: 783-785. Schmidt-Nielsen, K. (1963). Osmotic regulation in higher vertebrates. Harvey Lectures, 58:

55-93.

Schmidt-Nielsen, K (1964). Desert animals: Physiological problems of Heal and Water. Oxford. Clarendon Press. 277 pp. Sternberg, C. M. (1926). Notes on the Edmonton Formation of Alberta. Canadian Field Naturalist, 40: 102-104. Sternberg, C. M. (1935). Hooded hadrosaurs of the Belly River series of the upper Cretaceous: a comparison, with description of a new species. Bulletin. National Museums of Canada. Department of Mines, 52: 1-37. Sternberg, C. M. (1939). Were there proboscis-bearing dinosaurs? Discussion of cranial protuberances in the Hadrosauridae. Annals and Magazine of Natural History, 3: 556-560. Sternberg, C. M, (1942). New restoration of a hooded duck-billed dinosaur. Journal of Paleontology, 16: 133-134. Sternberg, C. M. (1953). A new hadrosaur from the Oldman Formation of Alberta: discussion of nomenclature. Bulletin. National Museums of Canada, 128: 275-286. Sternberg, C. M. (1954). Classification of American duck-billed dinosaurs. Journal of Paleontology, 28: 382-383. . Sternberg, C. M. (1964). Function of the elongated nasal tube in the hooded hadrosaurs. Journal of Paleontology, 38: 1003-1004. Technau, G. (1936). Die Nasendruse der Vogel. Journalfur Ornithologie, 84: 511-617. Tozer, E. T. (1956). Uppermost Cretaceous and Paleocene non-marine molluscan faunas of western Alberta. Memoirs. Geological Survey Branch, Department of Mines (and Technical Surveys) Canada, 280: 1-125. Waage, K M. (1968). The type Fox Hills Formation, Cretaceous (Maestrichtian), South Dakota. Part 1. Stratigraphy and palaeoenvironments. Bulletin of the Peabody Museum of Natural History, 27: 1-175. Waldman, D. & Hopkins, W. S., Jr. (1970). Coprolites from the Upper Cretaceous of Alberta, Canada, with a description of their microflora. Canadian Journal of Earth Sciences, 7:

1295-1303.

Weishampel, D. B. & Jensen, J. A. (1979). Parasaurolophus (Reptilia: Hadrosauridae) from Utah. Journal of Paleontology, 53: 1422-1427. Wilfarth, M. (1938). Gab es russeltragende Dinosaurier? Zeitschrift der Deutschen Geologischen Gesellschaft, 90: 87-100. Wiman, C. (1931). Parasaurolophus tubicen, n. sp. aus der Kreide in New Mexico. Nova Acta Regiae Societatis Scientiarum Upsaliensis, 7: 1-11. Versluys, J. (1936). Kranium und Visceralskelett der Sauropsiden. Reptilien, 4: 699-808. In Bolk, L., Goppert, E., Kallius, E. & Lubosch W. (Eds), Handbuch der Vergleichenden Anatomie der Wirbeltiere. Berlin und Wien: Urban and Schwarzenberg. 1016 pp.