Journal of Fish Biology (2010) 76, 10191024 doi:10.1111/j.1095-8649.2009.02531.x, available online at www.interscience.wiley.

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Rapid digestion of sh prey by the highly invasive detritivore Oreochromis mossambicus

R. G. Doup * and M. J. Knott e
Australian Centre for Tropical Freshwater Research, James Cook University, Queensland 4811, Australia (Received 17 March 2009, Accepted 9 November 2009)
Stomach residence time was tested over 24 h in three size classes of Oreochromis mossambicus using juvenile Lates calcarifer. In all 63 observations, the sh prey was digested within 24 h of consumption and most probably within 1 h, suggesting a need to re-evaluate the trophic status and 2010 The Authors potential effects of this highly invasive species.
Journal compilation 2010 The Fisheries Society of the British Isles

Key words: exotic sh; gut residence time; Mozambique tilapia.

Tilapias (Pisces: Cichlidae) are among the most widely distributed exotic shes in the world (Canonico et al., 2005). The Mozambique tilapia Oreochromis mossambicus (Peters), for example, has established feral populations in every nation in which they have been introduced (i.e. >90; De Silva et al., 2004). This includes Australia, where it has continued to invade the eastern and western coastlines for c. 30 years. Oreochromis mossambicus is also listed by the IUCN among those invasive shes believed to create the most adverse ecological effects (Lowe et al., 2000). Tilapias have been shown to respond to changes in their environment through facultative feeding, and examples of trophic plasticity have raised speculation that at least some tilapia populations may have evolved to utilize a wider range of food resources (Bowen & Allanson, 1982; McKaye & Marsh, 1983; McKaye et al., 1995). This is particularly important because successful invaders often display phenotypic plasticity for many traits that may assist dispersal and persistence (Garca-Berthou, 2007), and the ability to exibly exploit food resources through dietary shifts would be of clear benet in novel environments (Holway & Suarez, 1999). Like most tilapias, O. mossambicus is thought to be primarily herbivorous or a herbivore and detritivore (Bruton & Boltt, 1975; Whiteld & Blaber, 1978; De Silva et al., 1984), apart from some seemingly coincidental consumption of aquatic invertebrates and zooplankton, and larval shes and eggs (Fagade, 1971; Bowen & Allanson, 1982; Maitipe & De Silva, 1985; de Moor et al., 1986; Arthington & Bl dhorn, 1994; Fuseu lier, 2001; Maddern et al., 2007). Until recently, there has been no direct proof for
*Author to whom correspondence should be addressed. Tel.: +61 7 4781 5201; fax: +61 7 4781 5589; email: Rob.Doupe@jcu.edu.au

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active predation by O. mossambicus on non-plant food resources or for their broader ecological effects, despite the magnitude of this invasion (Doup & Burrows, 2008). e Doup et al. (2009a) recently showed that under experimental tank conditions, e O. mossambicus would readily consume common Australian macrophytes with or without a periphyton (i.e. detritus) coating; however, the test sh continued to lose body mass regardless of their sustained consumption and body mass could only be maintained by the supplementary feeding of a high protein commercial sh ake. These observations raised two questions; the rst was whether the tested plants provided sufcient protein for sh body maintenance, and the second followed that if protein deciency was responsible for the loss of body condition, then would an alternative form of protein be required (Bowen, 1979), thus triggering trophic plasticity in this species. In a subsequent study, Doup et al. (2009b) described for the e rst time signicant predatory effects by different sizes of O. mossambicus against 10 juvenile Australian freshwater sh species under experimental tank conditions, and also found prey sh remains in 16% of 176 wild-caught O. mossambicus. Of the few groups of shes known to derive their nutrition from the benthos (i.e. ilyophagy, see Allen, 1936), it is only the tilapias that have true stomachs and a gut structure and function that are remarkably similar to mammals, so that digestion and absorption generally correlates with diet (Caceci et al., 1997; Sklan et al., 2004). Moreover, the middle region of the tilapia stomach contains acid-producing gastric glands (Caceci et al., 1997), where pH values are <2 (Moriarty, 1973; Bowen, 1976). These highly acidic conditions cause cell lyses by rupturing the walls and membranes of consumed foods, thereby exposing the cell contents to digestive enzymes of the gut for rapid processing (Payne, 1978). Moriarty (1973) reported that for Oreochromis niloticus (L.), secretion of acidic juice occurred in response to feeding and caused a highly efcient assimilation of blue-green algae (Payne, 1978). Bowen (1976) showed the rapid digestion of benthic detritus by O. mossambicus but not of a high protein food resource such as sh esh. Doup et al. (2009b) demonstrated that 1) sh prey are readily consumed by e O. mossambicus in aquaria and 2) little more than sh prey body hard parts such as scales and bones remained in the guts of wild-caught O. mossambicus within hours of capture. The hypothesis of this paper is that sh-prey is so rapidly digested in the stomach of O. mossambicus that little or no evidence of piscivory remains soon after ingestion. This is tested by measuring post-consumption digestion rate in three size classes of O. mossambicus using a representative prey sh, and the results are discussed in a context of the trophic status of O. mossambicus and the threat this species poses to native shes. Approximately 100 adult O. mossambicus representing small (mean s.e. LT , total length, 8355 307 mm), medium (12544 184 mm) and large (22266 338 mm) size classes of mixed sex [similar to the sizes used by Doup et al. (2009b)] e were captured from local wild populations near Townsville, Queensland (19 15 S; e 128 50 E). Doup et al. (2009b) found that 97100% of all offered (n = 20) 10 mm LT Lates calcarifer (Bloch) were consumed by all sizes of O. mossambicus and that gape limitations became apparent at prey sizes of 20 mm LT . Based on these ndings, c. 100 juvenile L. calcarifer in the 10 mm size class (mean s.e. LT = 1001 017 mm) were obtained from the Marine and Aquaculture Research Facilities Unit at James Cook University. All O. mossambicus were held in captivity
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for 2 weeks before testing and were allowed to graze freely on periphyton, detritus and macrophytes in their holding tanks. Predation tests took place in 21, 30 l aquaria that were blacked-out on all sides and covered with clear plexiglass. The tanks contained aerated fresh water that was maintained at 26 C and subjected to a 12L:12D photoperiod. There was no structure in the tanks apart from an air stone xed to the centre of the tank lid. For every size class, a single O. mossambicus was placed in each tank for a 24 h acclimation period, during which the sh were not fed. Subsequently, a single L. calcarifer was released into the tank. The time of prey consumption was noted, and triplicate groups of O. mossambicus were systematically removed at 1, 2, 4, 6, 8, 12 and 24 h postconsumption for a total of seven replicate groups of O. mossambicus per size class (i.e. n = 21) and 63 individual tests in total. The O. mossambicus removed were immediately anaesthetized using 80 mg l1 of AQUI-S (http://www.aqui-s.com) in the presence of pure oxygen and then euthanized by overdose (Anon., 2006). Following death, the fresh guts were immediately removed and the stomach microscopically examined (i.e. <3 min post mortem) for the presence of L. calcarifer. No prey sh were found in the stomachs of any size classes (n = 9) of O. mossambicus at 1 h post-consumption, and none were detected in the stomachs of any other sh (n = 54) when examined at either 2, 4, 6, 8, 12 or 24 h following consumption. It seems highly likely that all prey sh were digested within 1 h of ingestion by O. mossambicus. A subsequent examination of the entire intestinal tract in all 63 sh revealed a single piece of unidentiable bone fragment in one medium-sized sh and occasional scales in only a few other individuals of all size classes. Apart from these remaining hard parts, there were no other readily identiable prey sh remains in the guts. Fishes that consume more plant material often show comparatively signicant increases in their gut length (Kramer & Bryant, 1995). The gut lengths of O. mossambicus used in this study were 4263 times longer than the sh themselves, and there was a highly signicant correlation between LT and total gut length (rs = 096, P = 0001); a similar relationship is found in O. niloticus (Peterson et al., 2006). The long narrow tilapia gut is characteristic of both herbivore and detritivore shes (Horn, 1989; Stevens & Hume, 1995) and is thought to increase the retention times and exposure to digestive processes of refractory compounds (German & Horn, 2006). This may also reect an adaptation to consuming sediments and their contents (Peterson et al., 2006). The presence of cellulases in sh guts is also thought to characterize the diets of primary herbivores and detritivores (Prejs & Blaszczyk, 1977), and Saha et al. (2006) described cellulase-producing bacterial ora in the intestinal tract of O. mossambicus, indicating an adaptation to consuming plant cellulose. These morphological and physiological observations seem to uphold the popular trophic classication of O. mossambicus as being a herbivore and detritivore. Moreover, Moriarty (1973) and Caceci et al. (1997) speculated that the strongly acidic environment of the tilapia gut may be related to an evolutionary transition from omnivore to herbivore. The data presented here, however, clearly indicate rapid digestion of sh prey in the stomach and strongly implicate a major role for stomach acids in the digestive process in O. mossambicus (Payne, 1978; Bowen et al., 2006). This also suggests that O. mossambicus is more likely a functional omnivore and supports the notion of it being a facultative piscivore. Indeed, the offering of sh prey in this study reiterates the observations by Doup et al. (2009b) e
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of ready predatory effects by O. mossambicus on juvenile shes. Both pieces of evidence indicate that it is an invasive species of consequence, and its continued and unchecked spread throughout the world should be treated with concern. Bowen (1976) showed that in fast-growing juvenile O. mossambicus, the gut residence time for benthic detritus comprising diatoms, bacteria and organic matter was about one hour. The similar residence time for sh prey in the current study suggests both food types are taken up similarly rapidly. Following capture of wild adult O. mossambicus, Doup et al. (2009b) immediately euthanized and placed deceased e sh in ice slurry before the removal and examination of the fresh gut contents within a few hours of death. Of the 29 sh containing any prey sh remains, it was only body hard parts (i.e. scales and bones) that were found in all guts, with the skin and esh of unidentiable sh species being found in ve individuals. Given the pace of digestion in the data presented here, Doup et al. (2009b) may have been fortunate e to have found even that amount of evidence for predatory effects. It further suggests that the characteristic detritus of examined O. mossambicus guts are largely indigestible remnants of unknown foods, and that the failure of some previous studies to identify sh prey may be a sampling artefact.
The use of sentient animal subjects in this study was approved by the James Cook University Animal Experimentation Ethics Review Committee (Permit No. A1245). We thank A. Lymbery and S. Bowen for kindly commenting on the draft manuscript.

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2010 The Authors Journal compilation 2010 The Fisheries Society of the British Isles, Journal of Fish Biology 2010, 76, 10191024