Mechanical disruption of seagrass in the digestive tract of the dugong

Mechanical disruption of seagrass by the dugong
J. M. Lanyon and G. D. Sanson
Further, Z. capricorni along with C. serrulata has fibre
bundles associated with the vascular bundles (Kuo, 1983).
According to Lees et al. (1982), a venation pattern with
numerous secondary veins such as is found in Z. capricorni
is likely to be more resistant to structural damage than other
arrangements because secondary veins add structural
strength. This type of venation may also be more effective
in restricting digestion by gut microorganisms, while plants
with a sparse network of secondary veins (Lees et al., 1982)
such as Halophila ovalis will be easier to fracture.
Factors other than leaf fibre may also affect breakability.
Halophila ovalis has higher water content as a percentage of
total weight than Z. capricorni (Lanyon, 1991), it lacks leaf
sheaths which represent a highly fibrous plant fraction, its
fibre is largely non-lignified (Lanyon, 1991), and its rhizomes
have cell walls that consist of non-cellulosic polysaccharides
(Baydoun & Brett, 1985). Halophila ovalis
appears to more readily break down under mechanical
pressure than Z. capricorni. We predict that the fibre of
Halophila ovalis may also be more digestible because reducing
particle size increases fibre digestibility (McLeod &
Minson, 1969). In dugong faecal samples, identifiable fragments
of Z. capricorni sometimes remain, while other
seagrass species are indistinguishable. In fact, most dugong
faeces are uniformly powder fine with only fibrous vascular
strands and no discernible tissue.
Mechanical processing of seagrass
Little is known of the mechanism of seagrass ingestion,
mainly through the difficulty of observing dugongs in the
wild. However, observations suggest that unlike most herbivorous
mammals, dugongs do not chew their food (Lanyon,
1991). When feeding on morphologically small seagrasses
such as their preferred genera Halophila and Halodule,
dugongs uproot the entire plant, creating feeding trails
through the substrate, with each feeding trail representing a
single feeding bout. Feeding trails range in length from 1 to
14 m (Heinsohn & Marsh, 1977; Anderson & Birtles, 1978)
and are generally between 10 and 20 cm wide (J. M. Lanyon,
pers. obs.). Dugongs remove an average of 63% of seagrass
from trails (Wake, 1975; Preen, 1993), the equivalent of
about 1 m 2 of seagrass from a conservatively sized trail,
within a feeding dive of c. 1 min (Anderson & Birtles, 1978;
Lanyon, 1991; Chivers et al., 2004). Thus, dugongs are
capable of uprooting vast quantities of seagrass in a short
period, and covering some distance at the same time. They
do not remain on the surface, chewing, between successive
feeding dives. In fact, the small gape and oral cavity of the
dugong and the lack of cheek pouches suggest that they do
not even have the capacity to retain food for chewing. Nor is
there evidence that they regurgitate their food to re-chew in
a manner similar to ruminants. Any mechanical processing
by the mouthparts occurs continuously as the food is
ingested.
The dugong is a combination of a bottom feeder, a
relatively poor diver and a herbivore feeding on low nutrient
food so that a large amount of food must be processed to
satisfy energetic requirements. It is quite likely that for the
dugong, feeding is a protracted activity as it is with other
grazing herbivores. On the basis of these considerations, we
suggest that the masticatory apparatus of the dugong has
developed to match a need for continuous cropping and
processing which mitigates against chewing, so that the
entire mouth cavity has been modified into a continuous
masticatory organ. The continual forward movement of the
dugong while feeding facilitates movement of seagrass into
the mouth. Initially, anterior and orthal movement of the
mandible (Lanyon & Sanson, 2006) secures seagrass between
the pads. The backwardly directed bristles on the
lower horny pad combined with mandibular retraction and
orthal movement would move seagrass backwards in the
mouth. The opposing pads are probably multifunctional so
that not only do they move food up from the ventral mouth
and back over the symphysial part of the mandible, but also
food is masticated on the way by the cornified papillae and
bristles on the pads and palate (Lanyon & Sanson, 2006),
rather like a conveyer belt.
However, this system can only work if the fracture
properties of the diet are such that hard enamelled organs
are not required. As described in this study, this is a peculiar
property of low fibre seagrasses. It is interesting that other
animals which utilize a seagrass food source can effectively
macerate the diet without teeth: for example waterfowl
(Thayer et al., 1984), which have a muscular gizzard; fish
(Pollard, 1984), which have gill rakers, and the green turtle
Chelonia mydas (Bjorndal, 1979, 1980). Each of these
animals has a ‘beak’ with which to ingest seagrass but no
tooth surfaces, and like other lower vertebrates lack a jaw
system capable of translational mastication. However, despite
the lack of teeth in the green turtle and the fact that it
does not masticate its food (Bjorndal, Bolten & Moore,
1990), the stomach contents are well macerated. Thus,
breakdown of the food must occur within the soft parts of
the digestive tract. In the green turtle, there are cornified
papillae in the oesophagus whose function remains largely
unknown, but it has been suggested that they may aid in
crushing the food (Skoczylas, 1978). In fish, seagrass is
macerated in the mouth, pharynx and stomach (Ogden,
1980). Similarly in the dugong, apart from the oral cavity,
breakdown could presumably occur in the muscular oesophagus
(Owen, 1838) and in the thick-walled (Osman Hill,
1945) and muscular small intestine (Owen, 1838) and stomach.
In fact, the process of detrition or wearing away of
the ingesta appears to account for a substantial proportion
of the physical particle reduction during the digestive
process of the dugong. Breakdown of seagrass during
passage through the mouthparts and digestive tract appears
to be facilitated by low fibre levels.
The dugong does not fit the generally accepted paradigm
of a mammalian hindgut fermenter in terms of development
of dentition. In fact, the dugong appears to have abandoned
a presumably ancestrally efficient dentition in favour of
development of soft mouthparts, which may be better
adapted for dealing with a seagrass diet that is low in fibre.
However, great development of the horny pads and the
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Journal of Zoology 270 (2006) 277–289 c 2006 The Authors. Journal compilation c 2006 The Zoological Society of London