Diet and senses in plesiosaurs
Types of evidence for diet
What did plesiosaurs eat and how do we know? Pollard (1990) classified the different types of evidence for diet in prehistoric organisms into three broad categories: 'direct', 'indirect' and 'general'. Direct evidence consists of various grades of stomach contents, indirect evidence includes bite marks, and general evidence consists of functional analyses. Some evidence is stonger and Martill et al. (1994) identify 8 categories to assess the strength of evidence for trophic links (see Table 1).
Criteria and example for plesiosaurs where necessary.
1. Incontrovertible evidence. Stomach
contents, distinctive bite marks.
Table 1. Criteria for determining trophic links (modified from Martill et al. 1994)
The following evidence provides information on diet in plesiosaurs
Precoprolites, coprolites and bite marks (1, 2)
'Precoprolites'is a term used to include gut contents, regurgitates and intestinal residues (Pollard, 1990). Exceptional conditions are needed for the preservation of soft stomach contents. Stomach contents are direct evidence for diet, especially if undigested (Pollard, 1990), but they are rare in plesiosaurs (Sato and Tanabe, 1998). In one pliosaur, teuthid cephalopod hooklets are present anlongside rarer fish teeth and an indeterminate reptile tooth (Martill et al. 1991). The cephalopod hooklets in a pliosaur from the Lower Oxford Clay of Peterborough closely resemble those of the contemporaneous Belemnoteuthis antiquus. It is possible that these have a secondary origin, that is, from the stomachs of prey ingested by the pliosaur, but this is unlikely. A plesiosaur specimen from Northern Japan preserves ammonoid jaw apparatus (possibly two taxa) concentrated in abundance in the stomach region (Sato and Tanabe, 1998), this is the first and only evidence that ammonoid cephalopods were consumed by plesiosaurs. Local and seasonal variation in the availability of prey is a factor that can influece diet (Massare, 1987; Martill et al. 1994). Accordingly, stomach contents in a few specimens may not be fully representative.
Coprolites are direct evidence for diet - but the diet of what? Coprolites are relatively common in Mesozoic marine strata and while they are probably from large marine reptiles, it isn't possible to positively identify them as plesiosaurian in origin. Coprolites must be used in association with criteria 2, 3 and 5 (table 1) to determine 'who did it'.
Possible pliosaur bite marks are present on small isolated Kimmeridge Clay marine reptile bones including small plesiosauroid limbs (fig 4) (Martill, 1994) and ichthyosaur vertebrae (Martill, 1992). One specimen of Pliosaurus brachyspondylus contains the remains of a thyreophorean dinosaur (Taylor et al. 1993).
Functional morphology of the skull (3)The jaws are the primary structure for aquiring food o functional analysis of the jaws and dentition is typically useful for detemining diet (Pollard, 1990). Evidence for twist-feeding in some pliosaurs comes from their strong triangular shaped skulls, very deeply rooted large teeth, and expanded mandibular symphysis (Martill et al. 1994). A detailed analysis of the functional morphology of the skull in two well-known pliosaurs, Rhomaleosaurus zetlandicus from the Lower Jurassic (Taylor, 1992) and Pliosaurus brachyspondylus from the Upper Jurassic (Taylor and Cruickshank, 1993). Rhomaleosaurus is interpreted as feeding on a wide range of prey and forcibly dismembering large prey based on assesment of its osteology and musculature. In P. brachyspondylus, the cranium is robust and the posterior teeth are unusually recurved (fig 5) to act as a ratchet to pull struggling prey into the mouth (Taylor and Cruickshank, 1993). Large postorbital openings in all plesiosaurs contained well-developed M. adductor mandibulae muscles to ensured a powerful bite (Massare, 1988, Cruickshank and Fordice
Plesiosaurs occur in a wide range of forms able to deal with prey of all sizes (Martill et al. 1994). The small-headed 'plesiosauromorphs' were unable to rip chunks off carcasses because their skulls were lightly built (Brown and Cruickshank, 1994) and unable to resist torsion (Cruickshank, 1994) (e.g. compressed mandibular rami and weak symphysis). Plesiosaur teeth were not used for chewing so the size of prey in these forrms was directly limited by the size of their gullet (Massare, 1988). The eyes were flattened (as evidenced by the sclerotic ring) to assist with underwater vision (Lambert et al. 2001) and were oriented upwards in many plesiosaurs. This suggests that they ambushed prey from below rather than from above, or as traditionally depicted, with implausible swan-necks darting down at fish from above the air-water interface ('hunting platforms') (Storrs, 1993; Everhart, 2002). Some pliosauroid eyes are positioned laterally (Massare, 1988) (see Storrs and Taylor, 1996). This indicates that they attacked prey on the same level in the water column. It is important to note that the function of the inflexible (Storrs, 1993) long neck is still unresolved (Martill et al. 1994), although it likely served as a mechanism for approaching prey without being detected (Massare, 1988). It did not have the flexibility to strike prey as do some snakes and pleurodiran turtles (Pough et al. 1996).
hearing and smell
Stapes are rarely preserved in plesiosaurs but where known, it is evident they were of no use in hearing (Storrs and Taylor, 1996), in air at least (Lambert et al. 2001). An olfactory system (Cruickshank et al. 1991) (fig 8) has been suggested as a common adaptation in the Plesiosauria (Brown and Cruickshank, 1994). The anteriorly placed internal nostrils have palatal grooves to channel water into them, the flow of which would be maintained by hydrodynamic pressure over the posteriorly placed external nares during locomotion. During its passage through the nasal ducts, the water would have been 'tasted' by olfactory epithelia. However, a recent study by Buchy et al. 2006 questions the position of the internal nares, proposing that they are actually located at the rear of the palate (the posterior interpterygoid vacuities).
Post-cranial Functional Morphology.
Swimming capabilities have implication for diet (Robinson, 1975; Massare, 1988). Plesiosauroids and pliosauroids had different locomotoay repertoires. The latter 'sprinted' in short bursts possibly using large flippers to take very fast moving prey "by stealth rather than pursuit" (Martill, 1992). The plesiosauroids were typically endurance swimmers with lower flipper aspect ratios and drag-inducing long necks (Robinson, 1975). Massare (1988) comes to similar concusions based on the hydrodynamic properties of Mesozioc reptiles and calculated speeds of 2.3 m/sec (= slow ambush predator) for plesiosauroids and slightly faster (= pursuit predator) speeds for pliosauroids (For more information on locomotion in plesiosaurs, visit the locomotion page)
Gastroliths (3, 5)
The intentional swallowing of stones has been known in plesiosaurs and living and extinct crocodiles for a long time (see Williston, 1893, 1894, 1904). The significance of gastroliths in prehistoric reptiles has been investigated by Kobayashi et al. (1999) who observed that in herbivorous birds, gastroliths and gizzards are common, but they are absent in carnivorous birds. The presence of gastroliths is common in plesiosaurs. Pollard (1990) notes that plesiosauroid stomach contents "usually contain gastroliths", (fig 9) and this is especially the case in elasmosaurids (see Everhart, 2000, and Cicimurri and Everhart, 2001). Gastroliths are rarer in pliosaurs (Storrs, 1993; Sato and Tanabe, 1998) but gastroliths are reported in one specimen cf. Liopleurodon sp. Martill, (1992), along with a fraction of sand), and isolated gastroiths are reported in Rhomaleosaurus (Smith, 2007). Recent discoveries of large pliosaurs in Arizona also preserve gastroliths (Schmeisser, pers. comm), so it is possible that the difference is the result of bias: pliosauroids tend to be large and difficult to work on (Forrest, pers. comm. 2002). Alternatively, the differecne may be genuine and could represent different functional regimes between pliosaurs and plesiosaurs (Storrs, 1993).So what was the function of gastrliths in plesiosaurs? A role in buoyancy control may be possible (Chatterjee and Small, 1989), this would be a less physiologically expensive way of attaining negative buoyancy than pachyostosis (Martill and Naish, 2000). Recent work by Don Henderson (2006) suggests that gatroliths have a role in stability within the water cloumn, rather than buoyancy control. Where present, gastroliths are usually found in small concentrations, although 100 are known for some elasmosaur specimens (Everhart, 2002). The relative weight could be insignificant in large animals (Ciccimurri and Everhart 2001, Everhart, 2002), although it only takes a few grams to tip a balance. Gastroliths may alternatively have been used for grinding food in the gut. Gastroliths may have had a dual purpose or even multi-purpose (Storrs, 1993).
Analogy (5, 8)
Plesiosaurs were air-breathing reptiles and must have surfaced frequently. They could not have dived for food for prolonged periods of time. However determining the details of such behaviour is problematic. Analogy can be used to infer diet in marine reptiles. Martill et al. (1994) assumed a number of extant marine organisms including cetaceans, penguins and pinnipeds to be analogous to plesiosaurs in many aspects, and Massare (1987) presents a number of similarities between the teeth of marine reptiles and modern large marine carnivores (fig 10). The teeth of the piscivorous gavial (Gavialis gangeticus) show similarities with plesiosauromorphs (fig 10. A and C) and the teeth of killer whales (Orcinus orcus), which can eat large mammals, show many similarities with pliosauromorphs (fig 10. B and D) (Massare, 1987). Plesiosaurid teeth also interlock, another adaptation of piscivores (Benton, 1990). A 'rushing upwards' style of attack is inferred for large pliosauromorphs, an analogy drawn from the modern great white shark (Charcharodon) (Martill and Naish, 2000). As preumed ectotherms (Chatterjee and Small, 1989), plesiosaurs could presumably go for considerable periods of time without food.
Incomplete carcasses (2, 5)
Isolated bones and partial articulated skeletons are found in many deposits and may be indicative of twist feeding and shake feeding (Martill et al. 1994). The bones were probably dropped by large pliosaurs in the water column, although is is also possible that they dropped from floating carcasses.
Because plesiosaurs are so diverse it is sensible to split the group into ecological guilds, independent of taxonomy. Massare (1987) performed a division for all of the large aquatic reptilian groups based on tooth form and presented the results in a triangular diagram (fig 11). Of seven guilds, the Plesiosauria is present in three: 'pierce', 'cut' and 'general', although subsequent guilds have since been proposed.
Predator or scavenger?
Evidence for scavenging of floating corpses comes from stomach contents including dinosaurs (Taylor et al. 1993) (see above) and pterosaurs (Massare, 1987). Predation consists of phases: (1) search, (2) capture, (3) penetration and (4) ingestion (= subjugation), (5) digestion and (6) defecation (Brett, 1990). Phases 1 to 3 will especially invoke repercussions on the biology of the predatory organism (table 3).
|Predation phase evidence in Plesiosauria|
1. Search Large eyes, olfaction system, locomotor adaptation.
2. Capture Tooth and functional morphology, Isolated bones and articulated but incomplete skeletons of possible prey.
3. Penetration Tooth and functional morphology: i.e. fast snapping muscular jaws and supporting pterygoid flanges.
Pre-ingestive breakage' can be direct ichnological evidence but diagnostic bite marks can represent both predation and scavenging. Predation can only be inferred if subsequent regrowth of the damaged prey (bone/shell) can be observed. This would be evidence of an unsuccessful attack. A Metriorhynchus skeleton on display in the Thinktank Birmingham Science Museum has a pliosaur tooth embedded in its femur. Fossils of carnivores preserved in the act of predation are rare, and none are known for the Plesiosauria.
The heavily set pliosaur Pachycostasaurus (fig 13) from Peterborough, UK (Dawn, 1997) does not fit neatly into any of the categories proposed by Massare (1987). It is regarded as a generalsistic feeder. Its pachyostotic ribs allowed it to traverse the seafloor, perhaps searching for benthic prey. Another ususual case arises for Aristonectes, which has hundreds of tiny delicate teeth (fig 4). An additional guild has been proposed to accommodate such oddities: a 'trap guild' (Chatterjee and Small, 1989). This may be analogous with the extant crabeater seal, which has sieve-like teeth for capturing krill (Martill et al. 1994). Cryptoclidus also has similar teeth and shares its environment with the very common decapod crustacean (Mecochirus). This relationship fulfills criteria 2 of table 1. However, it is unlikely than any plesiosaurs were strict suspension feeders in the way baleen whales feed today (Colin and Janis, 1997).
All plesiosaurs were predatory carnivores belonging to one or more of four ecological feeding guilds. Pliosaurs were top carnivores in their respective foodwebs (Martill, 1992, Martill et al, 1994; Sato and Tanabe, 1998), perhaps only exceeded in ferociousness by large mosasaurs in Cretaceous ecosystems. Plesiosaurs were pursuit predators of various sized prey and opportunistic feeders that can be classified in the general and cut guilds of Massare (1987). Twist feeding in large pliosaurs was likely (Taylor, 1992). The plesiosauroids such as Plesiosaurus were less generalised feeders (Maisch and Rucklin, 2000) but still belonged to two guilds, the pierce 1 and general guilds. Their teeth were used to pierce small soft-bodied prey, especially fish (Massare, 1987). Some taxa have diversified from these feeding groups and perhaps used filter feeding (trap guild). Hard and soft-bodied cephalopods also formed part of the diet of all plesiosaurs. Plesiosaurs hunted visually and perhaps employed a directional sense of olfaction.