Download Rapid digestion of fish prey by the highly invasive `detritivore

Journal of Fish Biology (2010) 76, 1019–1024
doi:10.1111/j.1095-8649.2009.02531.x, available online at www.interscience.wiley.com
Rapid digestion of fish prey by the highly invasive
‘detritivore’ Oreochromis mossambicus
R. G. Doupé* and M. J. Knott
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 fish 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 fish; gut residence time; Mozambique tilapia.
Tilapias (Pisces: Cichlidae) are among the most widely distributed exotic fishes 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 fishes
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 (Garcı́a-Berthou,
2007), and the ability to flexibly exploit food resources through dietary shifts would
be of clear benefit 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; Whitfield & Blaber, 1978; De Silva et al., 1984),
apart from some seemingly coincidental consumption of aquatic invertebrates and
zooplankton, and larval fishes and eggs (Fagade, 1971; Bowen & Allanson, 1982;
Maitipe & De Silva, 1985; de Moor et al., 1986; Arthington & Blüdhorn, 1994; Fuselier, 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: [email protected]
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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 (Doupé & Burrows, 2008).
Doupé et al. (2009a) recently showed that under experimental tank conditions,
O. mossambicus would readily consume common Australian macrophytes with or
without a periphyton (i.e. detritus) coating; however, the test fish 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 fish flake.
These observations raised two questions; the first was whether the tested plants
provided sufficient protein for fish body maintenance, and the second followed 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, Doupé et al. (2009b) described for the
first time significant predatory effects by different sizes of O. mossambicus against
10 juvenile Australian freshwater fish species under experimental tank conditions,
and also found prey fish remains in 16% of 176 wild-caught O. mossambicus.
Of the few groups of fishes 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 efficient 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 fish
flesh. Doupé et al. (2009b) demonstrated that 1) fish prey are readily consumed by
O. mossambicus 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. mossambicus within hours
of capture. The hypothesis of this paper is that fish-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 fish, and the results are
discussed in a context of the trophic status of O. mossambicus and the threat this
species poses to native fishes.
Approximately 100 adult O. mossambicus representing small (mean ± s.e. LT ,
total length, 83·55 ± 3·07 mm), medium (125·44 ± 1·84 mm) and large (222·66 ±
3·38 mm) size classes of mixed sex [similar to the sizes used by Doupé et al. (2009b)]
were captured from local wild populations near Townsville, Queensland (19◦ 15 S;
128◦ 50 E). Doupé et al. (2009b) found that 97–100% 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 findings, c. 100 juvenile L. calcarifer in the 10 mm size class (mean ± s.e.
LT = 10·01 ± 0·17 mm) were obtained from the Marine and Aquaculture Research
Facilities Unit at James Cook University. All O. mossambicus were held in captivity
© 2010 The Authors
Journal compilation © 2010 The Fisheries Society of the British Isles, Journal of Fish Biology 2010, 76, 1019–1024
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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 fixed 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 fish 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 l−1 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 fish 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
fish (n = 54) when examined at either 2, 4, 6, 8, 12 or 24 h following consumption.
It seems highly likely that all prey fish were digested within 1 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 fragment in one medium-sized
fish and occasional scales in only a few other individuals of all size classes. Apart
from these remaining hard parts, there were no other readily identifiable prey fish
remains in the guts.
Fishes that consume more plant material often show comparatively significant
increases in their gut length (Kramer & Bryant, 1995). The gut lengths of O. mossambicus used in this study were 4·2–6·3 times longer than the fish themselves, and
there was a highly significant correlation between LT and total gut length (rs =
0·96, P = 0·001); a similar relationship is found in O. niloticus (Peterson et al.,
2006). The long narrow tilapia gut is characteristic of both herbivore and detritivore fishes (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 reflect an adaptation to consuming sediments
and their contents (Peterson 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. mossambicus, indicating an adaptation to consuming plant cellulose. These morphological and physiological observations seem to
uphold the popular trophic classification 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 fish 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 fish prey in this study reiterates the observations by Doupé et al. (2009b)
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of ready predatory effects by O. mossambicus on juvenile fishes. 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 fish prey in the current study suggests both food types are taken up similarly rapidly. Following capture of wild adult
O. mossambicus, Doupé et al. (2009b) immediately euthanized and placed deceased
fish in ice slurry before the removal and examination of the fresh gut contents within
a few hours of death. Of the 29 fish containing any prey fish remains, it was only
body hard parts (i.e. scales and bones) that were found in all guts, with the skin and
flesh of unidentifiable fish species being found in five individuals. Given the pace of
digestion in the data presented here, Doupé et al. (2009b) may have been fortunate
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 fish 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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Journal compilation © 2010 The Fisheries Society of the British Isles, Journal of Fish Biology 2010, 76, 1019–1024