Journal of Fish Biologl: Q}lO) 76, nl9-rcz4

doi:10.1 1 I 1/i.1095-8649.2009.02531.x, available online at www.interscience.wiley.com

Rapid digestion of fish prey by the highly invasive 'detritivore' mossambicus

R. G. DouP6* aNo M. J. Kno'rr'

Australian Centre for Tropical Freshwater Research, Jantes Cook Universiti, QueensLand 481 l, Australia

(Received I7 Msrch 2009, Accepted 9 November 2009)

Stornach residencc lime was tesfed over 24 h in three size classes of Ore

Tilapias (Pisces: Cichlidae) are among the most widely distributed exotic lishes in the world (Canonico et al., 20Ail. The tilapia Oreoclrromis mossQrnbicus $ (Peters), for example, has established feral populations in every nation in which they have been introduced (f.e. >90; De Silva er a1.,2004). This includes Australia, where it has continued to invade the eastern and western coastlines for c. 30 years. a Oreochromis mossambicus is also listed by the IUCN atnong those invasive lishes believecl to create the most adverse ecological effects (Lowe et a1.,2000). ,T 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 resclurces (Bowen & Allanson, 1982; McKaye & Marsh, 1983; McKaye et a1..1995). This is particularly important because successful invaders often display phenotypic plasticity for many traits that may assist dispersal and persistence (Garcfit-Berthou, 2007). and the ability to flexibly exploit lbod resources through dietary shifts would be ol' clear benelit in novel environmenls (Holway & Suarez. 1999). Like most tilapias, O. mossembicus is thought to be primarily herbivorous or a herbivore and derririvore (Bruton & Boltt, 1975; Whitlield & Blaber. 19'18 De Silva et a|.,1984), apart from some seemingly coincidental consurnption of aquatic invertebrates and zu:plankton, and larval lishes and eggs (Fagade,l97l; Bowen & Ailanson, 1982; Maitipe & De Silva, 1985; de Moor et a1.,1986', Arthington & Bliidhom, 1994; Fuse- lier, 2001; Maddern et at., 2A07). Until recently, there has been no direct proof for

'&Author to u,h<.rm correspondence shoultl be addressed. Tel.: +61 7 4'181 5201'. fax: +61 7 4781 55891 email: Rob.Doupe @jcu.edu.au r019 o 2010 The Authors Jounral compilation ..j 2010'I'he Fisheries Society of the Ilritish lsles 1020 R. G. DOUPE AND M, J. KNOTT active predation by O. mossambic'us on non-plant food resources or for tleir broacler ecological effects, despite the magnitude of this invasion (Doup6 & Burrows, 2008). Doup6 et al. (2009a) recently showed that under experimental tank conditions, O. mossamhicas would readily consume common Australian macrophytes with or without a periphyton (i.e. ) coating; however, the test ljsh 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 lish flake. These observations raised two questions: the first was whether the tested plants provided sufficient protein for lish body maintenance, and the second fbllowed that if- protein deficiency 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, Doup6 et al. (2009h) described fbr the first time significant predatory effects by ditferent sizes of O. tnossanthica^r against l0 juvenile Australian freshwater fish species under expedmental tank conditions, and also found prey fish remains in 16% o{ 176 wild-caught O. mossambicus. Of the f-ew groups of lishes known to derive their nutrition liom 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 er 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 exposirrg the cell contents to digestive enzymes of the gut for rapid processing (Payne, 1978). Moriarty (1973) reported that for Oreochrornis niloticus (L.), secretion of acidic juice occurred in response to leeding and caused a highly efficient assimilation of blue-green (Payne,1978). Bowen (1976) showed rhe rapid digestion of benthic detritus by O. mossambicus but not of a high protein food resource such as fish flesh. Doup6 et al. (2009b) demonsrrated that l) fish prey are readily consumed by o. ntossambicus in aquaria and 2) little more than fish prey body hard parts such as scales and bones remained in the guts of wild-caught O. mossambicas within hours of capture. The hypothesis of this paper is that fish-prey is so rapidly digestcd in the stomach of O. mossambicus that linle or no evidence of piscivory remains soon after ingestion. This is tested by measuring post-consumption digestion rate in three size classes of o. mos,sctmbicus using a representative prey fish, and the results arc discussed in a context of the trophic status af O. mossambicus and the threat this specics poses t0 nativc lishes. Approximalely 100 adult O. mossambicus representing small (mean * s.n. 11, total length, 83.55 * 3.07 mm), medium (125.44 * 1.84 mm) and large (222.66 * 3.38 mm) size classes of rnixed sex [similar ro the sizes used by Doup6 et at. (2009b)] were captured fiom local wild populations near Townsville, Queensland (19" l5' s; t28'' 50' E). Doup6 et al. (2009b) found that 97-100o/a of a)l offered (n : 20) l0 mm L7 Lotes calcariJbr (Bloch) were consumed by all sizes of o. mossambicus and that gape limitations became apparent at prey sizes of >20 mm 11. Based on these findings, c. 100 juvenile L. calcarifer in the l0 mm size class (mean * s.e. Lr : 10'01 + 0'17 mm) were obtained from the Marine and Research Facilities Unit at James Cook University. All O. mossambicus were held in captivity

Jounraf conrpilation o 2010 The Fisheries Society ol'rbe Ilritish Istes,ktunut of l'i,r!t Bioktsy;t1:i?,ttT,i:iitlT PREY GUT RESIDENCE TIME IN OREOC'HROMIS MOSSAMBICUS 1021

fbr 2 weeks before testing and were allowed to graze freely on periphyton, detritus and macrophytes in their holding ranks. Predation tests took place in 2I,30l aquaria that were blacked-out on all sides and covered with clear plexiglass. The tanks contained aerated fresh water that was maintained c and subjectedto a l2Ll2D photoperiod. There was no structure ^t26" in the tanks apart from an air stone fixed to tho centre ol'tl,e tank lid. For every size class, a single o. mossambicss was placed in each tank for a 24 h acclimation period, during which the fish were not f-ed. subsequently, a single L. calc'arifer was released into the tank. The time of prey consumption was noted, and triplicate groups of O. mossamhicus were sysrematically removed at 1, 2,4, 6. 8, I2 and 24 h post- consumption 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.mosssmbiors removed were immediately anaesthetized using 80 mg l-r of AQUI-S (http://www.aqui-s.com) in the presence of pure oxygen and then euthanized by overdose (Anon., 2006). Follow- ing death, the fresh guts were irnmediately removed and the stomach rnicroscopically examined (i.e. <3 min post martem) for the presence af L. calcarifer. No prey fish were lbund in the stclrnachs of any size classes (n : 9) of O. mossam- bicus at t h post-consumption, and none were detected in the stomachs of any other fish (n : 54) when examined at either 2, 4,6,8, 12 or 24 h following consumption. It seems highly likely that all prey tish were digested within I h of ingestion by O. mossambicus. A subsequent examination of the entire intestinal tract in all 63 fish revealed a single piece of unidentifiable bone tiagrnent in one meriium-sizecl fish and occasional scales in only a f-ew other individuals of all size classes. Apart from these retnaining hard parts, there were no other readily identifiable prey tish remains in the guts. Fishes that consume tnore plant rnaterial often show cornparatively signilicant increases in their gut length (Kramer & Bryant, 1995). The gut lengths of o. mossam- bica.r used in this study were 4.2-6.3 dmes longer than the Iish thernselves, and there was a highly signilicant corelation between 11 and total gut length (r, - 0'96, P: 0'001); a similar relationship is found in O. nitoticus (Peterson et al., 2006). The long narrow tilapia gut is characteristic of both herbivore ancl detriti- vore fishes (Horn, 1989; stevens & Hume, 1995) and is thought to increase the retention times and exposure to digestive processes of refractory compounds (Ger- rlan & Horn, 2006). This may also reflect an adaptation to consulning sedirnents and their contents (petersr.rn et al., 2006). The presence of cellulases in fish 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 flora in the intestinal tract of O. mossambicas, indicating an adaptation to consum- ing plant cellulose. These morphological and physiological observations seem to uphold the popular trophic classification <>f O. mossambicus as being a herbivore and detritivore. Moreover, Moriarly Q973) and caceci et al. (1997) speculated that the strongly acidic environment of the tilapia gut may be related to an evolutionary transition fiom to herbivore. The data presented here, however, clearly indicate rapid digestion of lish 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-,2a06). This also suggests that o. mossambicus is more likely a func- tional omnivore and supports the notion of it being a facuhative piscivore. Indeed. the offering of fish prey in this study reiterates tire observations by Doup6 et al. (2009b)

rO 2010 The Authors 'I'he Journal compilalion C 2010 Fisheries Society oi the British Isles, Joumal of Fish Birtlogy 201(1.76, l}lg-1021 lo22 R. G, DOUPE AND M. J, KNOTT

of ready predatory effects by O. mossumbicus on juvenile lishes. Both pieces o1' evidence indicate that it is an 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 resi- dence time for benthic detritus comprising , bacteria and organic matter was 'about one hour'. The similar residence tirne fbr lish prey in the cunent study sug- gests both food types are taken up similarly rapidly. Following capture of wild adult O. mossambicus,Doupd et al. (2009b) immediately euthanized and placed deceased fish in ice slurry before the removal and examination of" the tiesh gut contents within a few hours of death. of the 29 lish containing any prey Iish remains, it was only body hard parts (i.e. scales and bones) that were fbund in all guts, with the skin and llesh of unidentiliable fish species being found in five individuals. Given the pace of digestion in the data presented here, Doup6 et al. (2009b) may have been fbrtunate to have found even that amount of evidence for predatory effects. It further suggests that the characteristic detritus of examined O. moss(tmbicas guts are largely indi- gestible remnants of unknown foods, and that the failure of some previons studies to identify fish prey may be a sampling arrefacr.

The use of sentient subjects in this study was approved by the James Cook Uni- versity Animal Experimentation Ethics Review Committee (Permit No. A1245), We thank A. Lymbery and S. Bowen fbr kindly commenting on the draft manuscript.

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Electronic Reference

Lowe, S., Browne, M., Boudelas, S. & De Poorter, M. (2000). 100 of the World's Worst Invasive Alien Specie,s * A Se.lectionfrotn the Global In,-a,sive Species Database. Gland: Invasive Species Specialist Group (ISSG), World Consenration Union (IUCN). Avail- able at http://www.issg.org/database/species/reference-filesi l00English.pdf

G; 2010 The Authors Joumal conrpilation (O 2010 'I'he Fisheries Society of rhe British lsles, Joumal of Fish Bktktgy 2O1Q,76, 1019-1024