Mechanical disruption of seagrass in the digestive tract of the dugong

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Mechanical disruption of seagrass by the dugong J. M. Lanyon and G. D. Sanson Table 4 Effect of grinding on particle size distributions expressed as median (M) particle size (mm) of the leaf fraction of five dried seagrasses and three terrestrial grasses Median (M) particle size (mm) Breakability NDF (% dm) 0 grinds 100 grinds 500 grinds Index Rank Mean SE Seagrass Halophila ovalis 287.6 164.7 55.9 231.1 1 42.6 0.9 (n=5) Halodule uninervis (n) 220.6 185.9 69.2 151.4 2 50.8 0.7 (n=5) Halodule uninervis (b) 230.1 190.1 104.4 125.7 3 54.2 1.1 (n=5) Cymodocea serrulata 161.5 114.4 70.9 90.6 5 52.5 0.9 (n=5) Zostera capricorni 155.5 131.6 73.9 81.6 6 62.6 1.7 (n=5) Terrestrial grass Triticum aestivum 214.5 166.2 93.8 120.7 4 42.0 (n=1) Koeleria setacea 193.7 148.4 146.1 47.6 8 57.0 (n=1) Erharta erecta 176.0 124.8 106.3 69.7 7 62.8 (n=1) Number of grinds refers to the number of grinds after milling. Grasses are assigned a breakability rank according to their breakability index, from most breakable (rank 1) through to least breakable (rank 8). NDF, neutral detergent fibre level expressed as a percentage of dry matter. Breakability index 250 200 150 100 50 0 30 35 40 45 50 55 60 65 Percentage NDF components. The nature of these leached materials was not investigated here. Fibre analysis There was a significant difference in fibre levels between seagrass species (F=1226.76; d.f.=1, 49; Po0.001). The NDF content of seagrass leaves ranged between 42.64 0.9% dry matter in Halophila ovalis to 62.6 1.7% in Z. capricorni (Table 4). The NDF content of Halophila ovalis was comparable to that of young wheat T. aestivum. Zostera capricorni had NDF levels that were comparable to the two mature terrestrial grasses. Discussion Particle size reduction Masticatory efficiency H. ovalis C. serrulata H. uninervis (n) H. uninervis (b) Z. capricorni Figure 8 Relationship between breakability index and mean neutral detergent fibre (NDF) level (% dry matter; n=5) of the leaf fraction of each of five seagrass species. Seagrasses in the stomach of the dugong were well macerated, presumably by the mouthparts. The mean particle sizes of the stomach contents of dugongs in this study were comparable to those of dugongs from elsewhere (Marsh et al., 1999). Masticatory or occlusal efficiency (characterized by production of a greater number of small particles) does not appear to alter in a manner that is consistent with age nor with the occlusal surface area of the mouthparts of the dugong. Dugongs with greater occlusal surfaces did not have greater occlusal efficiency. Further, particle size distribution of the stomach contents did not appear to correlate with the composition of the diet in terms of seagrass species. However, determining the dietary composition for dugongs based on stomach contents was problematic because most of the ingesta were too finely ground to be identifiable. In contrast, variation in faecal particle size distributions could be attributed to species composition of the diet. The only seagrass species that could be consistently identified in the faeces was Z. capricorni. Preen (1993) also found identifiable Z. capricorni in the faeces but could not distinguish other species. Rather than indicate that Z. capricorni was more prevalent in the dugong’s diet, this result could equally indicate that Z. capricorni was less digestible. Zostera capricorni was present as larger particles so that the resultant particle distribution tended to have a greater median particle size than those faecal samples in which Z. capricorni was absent. Zostera capricorni is one of the seagrasses least preferred by dugongs (Preen, 1993). In other faecal samples, the largest particle size class (i.e. 41.6 mm) comprised vascular bundles only. These were also found in dugong faeces examined by Anderson & Birtles (1978). Otherwise, dugong faeces were uniformly very fine, which was unusual compared with the faeces of other herbivores that generally have a higher proportion of larger particulate matter. Bertram & Bertram (1968, p. 389) also remarked on the ‘smooth, greenish clay-like faeces’ of the dugong. The uniformity of the faeces may be accounted for by considerable postoral particle size reduction of seagrass ingesta. Interestingly, Bjorndal (1979) has remarked on the well-digested appearance of faeces of green turtles feeding on seagrasses. 284 Journal of Zoology 270 (2006) 277–289 c 2006 The Authors. Journal compilation c 2006 The Zoological Society of London
J. M. Lanyon and G. D. Sanson Mechanical disruption of seagrass by the dugong Post-oral reduction The proportion of particle breakdown that is directly attributable to the mouthparts was not determined in the dugong. By the time seagrass reached the stomach, it was well macerated so that only between 18 and 30% of the dry matter of the digesta was particulate matter greater than 1.6 mm long, and up to 10% of the digesta was small enough to pass through the 500 mm sieve. However, considerable particle size reduction occurred along the length of the digestive system, that is post-orally. Particle size was reduced post-orally, that is by about 50% between the oesophagus and the pyloric region of the stomach of the dugong. Post-oral processing presumably includes detrition through friction of ingesta passage and/or by muscular action in the stomach. The well-packed nature of the stomach contents combined with strong muscular contractions may facilitate particle breakdown. Further, treatment with low pH, as occurs in the stomach, is known to soften plant tissue so that it is more amenable to physical (Wilson, McLeod & Minson, 1989) and fermentative breakdown (Parra, 1978). However, seagrasses do not appear to be susceptible to direct tissue lysis by low pH as would be found in the stomach. Further, particle reduction because of fermentation was probably negligible in the stomach, based on negligible volatile fatty acids (VFA) production in this organ (Murray et al., 1977). Considerable particle reduction also occurred in the small intestine. It is probable that this reduction occurred mainly through the processes of mechanical detrition and, perhaps, enzymatic digestion. The low fibre content and breakability of seagrasses probably account for a large part of the particle size reduction during passage through the digestive tract. Further particle reduction because of fermentation and detrition occurred in the hindgut region. Interestingly, particle reduction in the caecum was generally low, that is in two of the three dugongs examined, it contributed less than 1% of the post-gastric breakdown. Presumably, this could be due to the extremely small size of the caecum, that is 15 cm long in a hindgut of up to 30 m in length, suggesting that this organ may be functionally vestigial. Therefore, in the dugong, processes other than dental may contribute substantially to particle breakdown. Detrition may be a significant component, with fermentation more important further down the gut (Nocek & Kohn, 1988). The effectiveness of these processes may depend on the passage rate of particles through the digestive tract of the dugong. Digesta passage rates are slow, with mouth to anus retention times of 146–166 h (6–7 days) for particulate matter (Lanyon & Marsh, 1995). When feeding on a low fibre diet such as Halop. ovalis, apparent digestibility during this slow passage is high (Murray et al., 1977). Seagrass breakdown When subjected to mechanical pressures, seagrasses appear to rupture more readily than terrestrial grasses. One major difference between these two plant groups is the amount and distribution of the structural components of plant tissue, that is fibre. Fibre confers mechanical strength on plants and is a major obstacle to physical breakdown (Lees et al., 1981; Lees, Howarth & Goplen, 1982). The degree of particle size breakdown in herbivores has been directly linked to fibre levels (e.g. Parra, 1978; Lees et al., 1981, 1982; Spalinger et al., 1986). Although terrestrial grasses have supportive tissues throughout the plant body to resist gravity (Raven, Evert & Curti, 1976), seagrasses have conspicuously reduced supportive and protective tissues (Dawes & Lawrence, 1983; Lanyon et al., 1989). Leaf blades are thin and flattened (Phillips & Meñez, 1988), cell walls are thin, cuticle is reduced (Kuo, 1983) and there is a marked decrease in vascular tissue (Fahn, 1974). Seagrasses are supported by the water column and must be sufficiently flexible to accommodate the energy of water currents. Further, seagrasses are fully hydrated with water contents of 90–95% compared with 75–80% for terrestrial grasses (Best, 1981). These characteristics are among the most influential in providing mechanical support to the leaf blade (Tomlinson, 1980). Large intercellular spaces or gas lacunae are also common in seagrasses (Tomlinson, 1980; Phillips & Menez, ˜ 1988), resulting in low tissue mass compared with terrestrial grasses. These features are reflected in the low NDF levels of seagrasses compared with terrestrial grasses and may account for the increased susceptibility of seagrass to physical rupture. In vitro comparisons indicated differences in breakability of seagrass species. This is not surprising given the taxonomic variation in morphology and anatomy within the seagrasses (Lanyon, 1986; Kuo & McComb, 1989). Both fresh and dried Z. capricorni leaf did not break as readily as the other seagrass species, having a lower breakability index that fell within the range of terrestrial grasses. The order of breakability of seagrasses based on this index roughly corresponded to their fibre levels and to the order of diet preference of the seagrasses by the dugong (Lanyon, 1991; Preen, 1993). Cymodocea serrulata was less breakable than its fibre level would suggest, indicating that not only fibre level but also the composition and distribution of fibre may affect breakability. Interestingly, C. serrulata is ranked as a less preferred species throughout most of the dugong’s range (Preen, 1993). We suggest that NDF levels may be reflected in the amount of vascular tissue and associated fibre bundles in each seagrass species, and that the distribution of these fibres may be reflected in breakability. Vascular bundles are highly visible in the leaf fraction of seagrasses and in some cases are used as taxonomic tools (Lanyon, 1986). Halophila ovalis has one prominent longitudinal vein with less prominent marginal vascular bundles running around the perimeter of the lamina and few well-spaced secondary veins (Lanyon, 1986). The number of longitudinal veins in other species ranges from three in Halodule spp. to 13–17 in C. serrulata: these species have no prominent cross-veins. In contrast, Z. capricorni has a significantly greater density of vascular fibres with numerous prominent and close crossveins running at right angles to five longitudinal veins. Journal of Zoology 270 (2006) 277–289 c 2006 The Authors. Journal compilation c 2006 The Zoological Society of London 285
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Mechanical disruption of seagrass in the digestive tract of the dugong

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