- Top of page
- STOMACH CONTENTS
- SEAGRASS-HARVESTING EXPERIMENTS
- REVIEW OF DUGONG ANATOMY
- TUSK TIP GEOMETRY
- MICROWEAR ON TUSKS
- LITERATURE CITED
Most living and fossil sea cows of the subfamily Dugonginae (Dugongidae, Sirenia, Mammalia) are characterized by large upper incisor tusks, which are thought to play an important role (at least primitively) in feeding on seagrass rhizomes. Testing this hypothesis is difficult, because the only extant tusked sirenian (Dugong dugon) is morphologically and perhaps behaviorally aberrant. The tests attempted here involve examination of stomach contents of wild Recent dugongs, experiments using plastic replicas of diverse tusks to harvest seagrasses, gross anatomical observations on tusks and skulls, measurements of tusk tip geometry, and observations of microwear on tusks. We conclude that (a) male D. dugon (with erupted tusks) do not consume more rhizomes than females (without erupted tusks); (b) the tusks do not play a significant role in feeding in the modern dugong; (c) larger, more bladelike tusks are more effective at harvesting rhizomes, but the effect of shape was not experimentally separated from the effect of exposed tusk length; (d) some fossil dugongines show apparent cranial adaptations for downward and backward cutting motions of their large, bladelike tusks; (e) geometry of wear surfaces is consistent with use of at least the more bladelike tusks as cutting instruments; (f) preliminary observations of microwear in D. dugon do not indicate more than occasional use of the tusks in purposeful harvesting of rhizomes, and then only opportunistically by large adult males. The hypothesis of such tusk use by extinct dugongines (in contrast to the living species) is so far corroborated, but available data and tests do not suffice to establish this conclusively. Anat Rec, 290:523–538, 2007. © 2007 Wiley-Liss, Inc.
A quantitatively significant but poorly understood aspect of mammalian history is the long relationship between herbivorous marine mammals and the plants they have eaten. This history extends over the 50 million years of the fossil record of these mammals (mainly those in the Order Sirenia: dugongs and manatees), and chiefly involves the tropical-to-temperate, cosmopolitan marine angiosperms or seagrasses (Hydrocharitaceae and Potamogetonaceae), which today constitute one of the Earth's most productive ecosystems, as has presumably been true throughout the Cenozoic (Ivany et al., 1990). The greatly diminished diversity of modern sirenians, however, is a major obstacle to exploring how feeding adaptations, niche partitioning, and other aspects of the order's ecology evolved (Domning, 2001; see also review in Uhen, 2007, this issue).
The typical seagrass is a submerged marine plant that comprises parts both above ground (shoots and leaves) and below ground (roots and rhizomes). In most seagrasses, the rhizomes or underground stems compose at least 50% of the plant's biomass and are a rich source of carbohydrates in the form of sugars and starch, although the exact distributions of biomass and nutrients within the plant seem to vary seasonally (Lanyon et al., 1989). Therefore, they are a potentially significant resource for marine herbivores able to extract them. Several seagrass herbivores (dugongs, sea turtles, fish, etc.) often occur sympatrically and have to compete for plant resources in a community typically comprising fewer than a dozen angiosperm species. Therefore, a species' ability to extract seagrass rhizomes may be critical to its long-term survival in the system and to the overall pattern of niche partitioning among these competitors. Here, we examine this ability in the extant dugong (Dugong dugon) and its extinct relatives.
Although green turtles (Chelonia mydas) are major seagrass consumers, they do not disturb the rhizomes, and they also eat large amounts of algae, in contrast to manatees (Trichechus spp.) and dugongs (Lanyon et al., 1989; André et al., 2005; cf. simulation study by Aragones and Marsh, 2000); so it is doubtful whether they compete significantly with dugongs or manatees at the present time. With the possible exception of some members of the extinct mammalian Order Desmostylia, which were restricted to the North Pacific Ocean (Domning, 1978), no other marine animals are known to extract significant amounts of seagrass rhizomes (McRoy and Helfferich, 1980; Klumpp et al., 1989).
Sirenians, then, are the only known herbivores that have had the capacity to exploit rhizome resources in the tropical seagrass beds of most parts of the world at any time during the Cenozoic Era. Moreover, sirenians are almost exclusively consumers of angiosperms and eat algae in significant amounts only when angiosperms are scarce (e.g., after storms, Spain and Heinsohn, 1973; or in the range of the extinct Steller's sea cow [Hydrodamalis], Domning, 1978); so far as is known, this has always been true. Sirenians also eat animals on occasion (e.g., Powell, 1978; Preen, 1995), but never, apparently, as a major part of the diet. We, therefore, seem justified in considering tropical marine sirenians as obligate seagrass consumers for all practical purposes, and as the only potential consumers of seagrass rhizomes.
These conclusions apply in particular to the Dugongidae, which during the Holocene, and apparently throughout their history, have been exclusively marine and (except for hydrodamalines) tropical. Increasing evidence is emerging for the sympatric occurrence of three or more dugongid species at various times and places in the geological record (Domning, 1989a, 2001; Toledo and Domning, 1991; Aranda-Manteca et al., 1994). The presence of more than one sirenian species in a tropical seagrass community will likely prove to have been the rule and not the exception throughout the Tertiary history of seagrasses.
This finding becomes problematical when viewed in light of the low taxonomic diversity of present-day seagrasses (only 12 genera and 50 or so species worldwide; Phillips and Meñez, 1988). Moreover, the fossil record of seagrasses, scant though it is, gives no hint that this diversity was ever significantly greater: all known Tertiary seagrasses, even as far back as the Eocene, are referred to living genera, and many to living species (Larkum and den Hartog, 1989; Ivany et al., 1990). There is evidence (Lumbert et al., 1984; Ivany et al., 1990) that the Caribbean seagrass flora was more diverse in the Eocene than it is today, but not more diverse than the Indopacific seagrass flora of today.
Thus, we are faced with the general problem of explaining how it was possible for several sirenian species to coexist on such a narrow resource base. Several potential kinds of answers present themselves: (a) seagrass communities were more diverse in the past than their fossil record now reveals; (b) marine sirenians had more varied diets (including more algae, freshwater plants, and/or animals); or (c) it is in fact possible for several sirenian species to stably partition a seagrass assemblage of the level of diversity observed today.
The main methodological problem with any such venture into paleoecology is that of maintaining some link with the realm of testable hypotheses. The more factors allowed to vary from the present in a reconstruction of the past, the fewer and more tenuous such links become. It has, indeed, been suggested (Sickenberg, 1934) that the extinct sirenian Miosiren fed on molluscs, but this possible exception by itself does not threaten to change the overall picture outlined above. This study will, therefore, proceed on firmer ground by first exploring (and, if need be, eliminating) the alternative that postulates the least divergence from modern conditions. An initial working assumption is that tropical seagrass diversity (at least at the generic level) has not fluctuated dramatically during the Cenozoic and that all the tropical dugongids of the past were like the modern Dugong in their reliance on a seagrass diet.
Recent studies on the digestive system of the living D. dugon, together with much else that we know about their anatomy and physiology, have shown that modern Sirenia are extremely efficient in minimizing energy use (Aketa and Kawamura, 2001; Aketa et al., 2001, 2003). Despite what is known about their internal digestive efficiency, however, little is known about their means and efficiency of food acquisition.
Large tusks formed by the first upper incisor teeth are a prominent feature of D. dugon and many of its extinct relatives in the Family Dugongidae. These tusks vary considerably within and among taxa in size, shape, and degree of eruption and wear. In cases where several genera of dugongids occur sympatrically in the fossil record, differences in tusk morphology are among their most obvious points of contrast in presumably adaptive features and may offer some of the best clues to strategies of niche partitioning among these animals (Domning, 1989a, 2001). However, little direct evidence of the actual function of sirenian tusks has been reported. Display as a major function seems inconsistent with the fact that most of the tusk is always embedded in (and supported by) the premaxilla, with only a small portion exposed, and even that portion mostly concealed by the upper lip—a design better adapted for forceful use than for show. The tusks' past and/or present use in feeding, specifically for the extraction of seagrass rhizomes, has been conjectured (Domning, 1989a– c, 2001), but attempts to directly observe tusk use for feeding by wild dugongs (e.g., Vosseler, 1924–25) have not succeeded, and this conjecture is still in need of empirical support. This study seeks to provide this support by bringing a diversity of indirect techniques to bear on the question.
Only a single species of tusked sirenian (Dugong dugon) survives today to give us possible insight into this problem. Unfortunately, the modern dugong is atypical of its family in that its tusks are sexually dimorphic: although large in both sexes, they erupt and become worn only in adult males and in a few old, possibly postreproductive females (Marsh, 1980; Domning, 1995). This has led some writers (e.g., Anderson, 2002) to conclude that they serve only a social function. They are used by the males when attempting to mate, as weapons against rival males and possibly as instruments to roll females into position for mating; the pairs of parallel scars that are abundant on most dugongs are attributed to the tusks of aggressive males (Anderson and Birtles, 1978; Anderson, 1979; Marsh et al., 1984; Preen, 1989).
This, however, leaves two questions unanswered: do male dugongs also use their tusks in feeding, and did the tusks of their extinct, nondimorphic relatives function in feeding or only in social interactions? The following investigations were performed to answer these questions: (1) examination of dugong stomach contents to see whether adult males consume more or larger seagrass rhizomes than adult females; (2) experiments to determine the relative efficiency of different shapes and sizes of dugongid tusks as tools for rhizome extraction; (3) observations of the gross morphology of the tusks, rostral architecture, and other oral structures of Dugong and related fossil forms; (4) measures of tip geometry of tusks to determine their relative utility as tools; and (5) observations of microwear on Recent and fossil dugongid tusks. Tasks 1–3 were carried out by Domning, and tasks 4 and 5 by Beatty.
The Recent dugongs studied were from northeastern Australia and Papua New Guinea, where there exists a diverse flora of seagrasses with rhizomes of several different sizes. Dugongs in this region reportedly feed largely on species of Halophila and Halodule (Johnstone and Hudson, 1981; Marsh et al., 1982), whose rhizomes are <2 mm in diameter. Less frequent in the dugong diet are species of Cymodocea, Zostera, and Syringodium (rhizomes 1–3 mm); Thalassia hemprichii (2–5 mm); and Enhalus acoroides (10–15 mm; den Hartog, 1970; Meñez et al., 1983; Phillips and Meñez, 1988).
Dugongs use at least two different modes of feeding: cropping of seagrass leaves (e.g., when feeding on Amphibolis; Anderson, 1986), and rooting up the whole plant, during which their characteristic feeding trails are produced (e.g., Anderson and Birtles, 1978; De Iongh et al., 1995). These trails are typically approximately 10–25 cm wide (roughly the width of an adult dugong's facial disk) and several meters long; 1–3 trails are produced on a single dive (Heinsohn et al., 1977; Anderson and Birtles, 1978; De Iongh et al., 1995, 1997; Anderson, 1998). Such trails appear to be made most often by dugongs eating the smaller, more delicate seagrasses (Halophila, Halodule) growing on soft substrates, and less frequently on larger seagrasses (Zostera, Syringodium). Dugongs feeding in this manner typically stir up conspicuous clouds of silt (Anderson and Birtles, 1978) and are probably less vigilant for predators; they harvest rhizomes in this manner when predation risks from sharks are absent, and for short periods (∼11% of foraging effort) if risk of predation by sharks is minimal but present (Wirsing, 2005). It is thought that a protruding, soft-tissue knob on the upper jaw is used to plow through the upper 4–6 cm of sediment, turning up the rhizomes together with the shoots and leaves, which are then tucked into the mouth by the upper lip and its enlarged prehensile bristles (Gudernatsch, 1908; Marshall et al., 2003; H. Marsh and A. Preen, personal communication). This plowing through sediment can presumably cause incidental wear on the tusks, whether these are intentionally used for digging or not.
Arguably, a third mode of feeding occurs as a limit-case of trail-making. While foraging on leaves and rhizomes of small seagrasses like Halophila and Halodule, which offer little resistance to the animal's forward movement and require no tusk use for their excavation, dugongs are able to maintain headway, making feeding trails on the bottom. As the seagrass bed becomes denser, however, the feeding trails (each made on a single breath-hold dive) become shorter (Anderson and Birtles, 1978); and when dugongs feed on plants or invertebrates that are very resistant to excavation, they must remain in one spot during each dive and, hence, make a pit rather than a linear trail (Anderson, 1998; Domning, 2001).
As the rhizomes of their food plants vary toward the larger and more fibrous (as well as more deeply growing), dugongs apparently tend to feed more exclusively on the leaves. Harder substrates, and greater density of rhizome mats, would also discourage extraction of rhizomes. Dugongs extracted 75% of rhizome-root biomass from a Halodule-dominated meadow in one study (De Iongh et al., 1995), and are probably capable of extracting even more, whereas Florida manatees (Trichechus manatus latirostris) feeding on Syringodium beds can remove up to 96% of the total biomass despite their complete lack of tusks (Packard, 1984). Therefore, it seemed necessary, in examining the stomach contents (the first study reported here), to concentrate on dugongs eating still larger seagrasses (Thalassia) to determine the limits of Dugong's ability to excavate rhizomes.