What did plesiosaurs eat and how do we know?
Types of evidence for diet
Pollard (1990) classified 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 stronger than others! Martill et al. (1994) identify eight categories to assess the strength of evidence for trophic links in the Middle Jurassic Oxford Clay (see Table 1).
|1. Incontrovertible evidence. Stomach|
contents, distinctive bite marks.
2. Close association of fossil finds. Pliosaur teeth near
3. Functional morphological analysis. Dental morphology, size,
4. Proxy evidence as in 1 above from other deposits. Stomach contents in related taxa.
5. Comparison with extant homologues or analogues. Killer
whale, great white shark, gavial, dolphin, sperm whale.
6. Geochemical data
7. Sedimentological/biostratinomic data
8. Supposed relationships
et al. 1994), with possible examples for plesiosaurs where available.
The following evidence provides information on diet in plesiosaurs. The superscript number refer to the types of evidence in table 1.
Precoprolites, coprolites and bite marks (1, 2)
‘Precoprolites’ are gut contents, regurgitates and intestinal residues (Pollard, 1990). Exceptional conditions are needed for soft stomach contents to be preserved. Stomach contents are direct evidence for diet, especially if undigested (Pollard, 1990), but they are rare in plesiosaurs (Sato and Tanabe, 1998). Teuthid cephalopod hooklets are present in one pliosaur from the Lower Oxford Clay of Peterborough, alongside sparse fish teeth and an indeterminate reptile tooth (Martill et al. 1991). The hooklets closely resemble those of the contemporaneous belemnite, Belemnoteuthis antiquus. It is possible that these have a secondary origin, i.e. 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 only evidence that ammonoid cephalopods were consumed by plesiosaurs. Local and seasonal variation in the availability of prey is a factor that can influence diet (Massare, 1987; Martill et al. 1994), so stomach contents in a few specimens may not be fully representative of that species’ diet.
Coprolites are direct evidence for diet, but for which species? Coprolites are relatively common in Mesozoic marine strata and while they are probably from large marine reptiles, it isn’t possible to positively identify any as plesiosaurian in origin. Coprolites must be used in association with criteria 2, 3 and 5 (table 1) to determine ‘who did it?’.
Pliosaur bite marks are present on many bones, including a small isolated Kimmeridge Clay plesiosauroid propodial (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 acquiring food so functional analysis of the jaws and dentition (teeth) is useful for determining diet (Pollard, 1990). Evidence for twist-feeding in some pliosaurs comes from their strong triangular shaped skulls, deeply rooted large teeth, and expanded mandibular symphysis (Martill et al. 1994). These characteristics would resist torsional forces when rolling in the water. A detailed analysis of the functional morphology of the skull has been performed for 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. 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).
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 from carcasses because their skulls were lightly built (Brown and Cruickshank, 1994) with compressed mandibular rami and weak mandibular symphysis, so they were unable to resist torsion (Cruickshank, 1994)/ Plesiosaur teeth were not used for chewing so the size of prey in these forms was directly limited by the size of their gullet (Massare, 1988). The shape of the sclerotic ring suggests the eyes were flattened to assist with underwater vision (Lambert et al. 2001), and they were oriented upwards in many plesiosaurs. This suggests that they ambushed prey from below rather than from above. This contradicts a traditional interpretation for elasmosaurids using their necks to dart down at fish from above water (‘hunting platforms’) (Storrs, 1993; Everhart, 2002). Some pliosauroid eyes are positioned laterally (Massare, 1988) (see Storrs and Taylor, 1996), which suggests that they attacked prey on the same level in the water column. It is important to note that the function of the (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).
Hearing and smell
Stapes (ear bones) 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 that may have helped channel water into them, with flow maintained by hydrodynamic pressure over the posteriorly placed external nares, caused by movement of the animal through the water. In this hypothesis, the water may have been ‘tasted’ during its passage through the nasal ducts by olfactory epithelia. However, a study by Buchy et al. (2006) questions the position of the internal nares, and proposes 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 probably ‘sprinted’ in short bursts possibly using large flippers to take very fast moving prey “by stealth rather than pursuit” (Martill, 1992). The plesiosauroids were more likely 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 gastroliths and gizzards are common in herbivorous birds, but 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). The difference may be genuine and could represent different functional regimes between pliosaurs and plesiosaurs (Storrs, 1993).
What was the function of gastroliths in plesiosaurs? They may have has a role in buoyancy control (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 or even multi-purpose (Storrs, 1993).
Analogy (5, 8)
Plesiosaurs were air-breathing reptiles and must have surfaced frequently. They could have dived for food for limited periods of time, but such behaviour is difficult to determine for an extinct animal with no modern descendants or close relatives (homalogues). Analogy can be used to infer diet in marine reptiles. Martill et al. (1994) regarded several extant marine organisms including cetaceans, penguins and pinnipeds as analogous to plesiosaurs in many aspects. Massare (1987) presented 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), while the teeth of killer whales (Orcinus orcus) share many similarities with pliosauromorphs (fig 10. B and D) (Massare, 1987). Killer whales eat large vertebrates, so pliosaurs probably did, too. Plesiosauroid 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 (Carcharodon) (Martill and Naish, 2000). If plesiosaurs were ectotherms (e.g. Chatterjee and Small, 1989) then they would presumably be able to go for considerable periods of time without food.
Incomplete carcasses (2, 5)
Isolated bones and partial articulated skeletons are found in many Mesozoic deposits and may be indicative of twist-feeding and shake-feeding (Martill et al. 1994). The bones may have been dropped by large pliosaurs in the water column, although it is also possible they dropped from floating carcasses.
Predator or scavenger?
Evidence for scavenging of floating corpses comes from dinosaurs in stomach contents (Taylor et al. 1993) and pterosaurs (Massare, 1987). Predation consists of several phases: (1) search, (2) capture, (3) penetration, (4) ingestion (= subjugation), (5) digestion, and (6) defecation (Brett, 1990). Phases 1 to 3, in particular, will have repercussions on the biology of the predatory organism (table 3).
|Predation phase evidence in Plesiosauria#000000; font-family: Arial, Helvetica, sans-serif; font-size: small;">|
1. Search: Large eyes, olfactory 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-ingestion breakage may provide direct ichnological (trace fossil) evidence for predatory behaviour, but diagnostic bite marks can represent both predation and scavenging. Predation can only be inferred if subsequent regrowth of the damaged prey (bone/shell) is present, as this would provide evidence for an unsuccessful attack. A pliosaur tooth embedded in the femur of a Metriorhynchus crocodylomorph from the Oxford Clay is on display in the Thinktank Brimingham Science Museum. The bone has regrown around the tooth, providing direct evidence of predatory behaviour in pliosaurs – the Metriorhynchus got away.
Since plesiosaurs are so diverse it is sensible to split the group into ecological guilds independent of their taxonomy. Massare (1987) divided large aquatic reptiles into groups based on their tooth form and placed the groups into triangular morphospace. (fig 11). Of seven marine reptile ecological guilds, the Plesiosauria occupy three: ‘pierce’, ‘cut’, and ‘general’. Subsequently, a new guild has since been proposed.
The pliosaur Pachycostasaurus (fig 13) from the Oxford Clay or 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 unusual case is Aristonectes, which has hundreds of tiny delicate teeth (fig 14). An additional guild has been proposed to accommodate such oddities: a ‘trap guild’ (Chatterjee and Small, 1989). This may be analogous to the extant crab eater 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. It is unlikely than any plesiosaurs were strict suspension feeders in the sense of modern baleen whales (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). Many pliosaurs were pursuit predators of various sized prey, and opportunistic feeders in the ‘general’ and ‘cut’ guilds of Massare (1987). Twist feeding in large pliosaurs was likely (Taylor, 1992).
The plesiosauroids such as Plesiosaurus were more specialised feeders (Maisch and Rucklin, 2000) belonging to two guilds, the ‘pierce 1’ and ‘general’ guilds. Their teeth were used to pierce small soft-bodied prey such as fish and cephalopods (Massare, 1987). Some taxa diversified from these feeding groups and were perhaps filter feeders (trap guild). Hard and soft-bodied cephalopods also formed part of the diet of all plesiosaurs. Plesiosaurs hunted visually and possibly had a directional sense of olfaction.