Physics and Chemistry of the Earth 66 (2013) 33–37

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Physics and Chemistry of the Earth

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The aquaculture potential of Tilapia rendalli in relation to its feedinghabits and digestive capabilities

1474-7065/$ - see front matter � 2013 Elsevier Ltd. All rights reserved.http://dx.doi.org/10.1016/j.pce.2013.09.006

⇑ Corresponding author. Tel.: +27 7 1481 9981.E-mail address: hlophesam@gmail.com (S.N. Hlophe).

S.N. Hlophe ⇑, N.A.G. MoyoAquaculture Research Unit, School of Agricultural and Environmental Sciences, Faculty of Science and Agriculture University of Limpopo, Private Bag X1106, Sovenga 0727,South Africa

a r t i c l e i n f o

Article history:Available online 16 September 2013

Keywords:Growth performanceDigestive enzymesOreochromis mossambicusFlag Boshielo Dam

a b s t r a c t

Tilapia rendalli is a predominately macrophagous fish. However, it was able to colonise an oligotrophicdam (Flag Boshielo) with limited macrophytes. Therefore, the diet of T. rendalli in this dam was investi-gated; its stomach contents were examined over 12 months. A size related dietary shift was evident.Juveniles fed mainly on zooplankton while sub-adult and adult fish grazed on both macrophytes andmarginal vegetation. T. rendalli’s ability to strive in an environment with limited food resources led toa subsequent study to determine its aquaculture potential. Its growth performance was compared to thatof the commonly cultured Oreochromis mossambicus. Juveniles of both species were fed a commercial tila-pia diet for 60 days. Specific growth rate and protein efficiency ratio was comparable to that of O. mos-sambicus (P > 0.05, ANOVA). Feed conversion ratio was significantly higher (P < 0.05) in T. rendalli(1.43) than in O. mossambicus (1.25) indicating a better efficiency in feed utilisation by O. mossambicus.At a physiological level, protease, lipase and cellulase activities did not differ significantly between thetwo fish species (P > 0.05). Amylase activities were significantly higher (P < 0.05) in T. rendalli than inO. mossambicus. The highest amylase activities were recorded in the proximal intestines as 26.34 and22.00 lmol/min/mg protein in T. rendalli and O. mossambicus respectively. This may be an indicator thatT. rendalli is better equipped to digest plant diets. T. rendalli may be the aquaculture species of choice foremerging fish farmers who cannot afford the highly priced fishmeal as a protein source in fish diets.

� 2013 Elsevier Ltd. All rights reserved.

1. Introduction

Aquaculture is currently the fastest growing food producingsector with an average rate of 8–10% per year (Tacon et al.,2011). However, the contribution of Sub-Saharan Africa to thisgrowth remains insignificant (FAO, 2011). Tilapias are the thirdmostly cultured fish species after carps and salmonids (El-Sayed,2006). In South Africa, Oreochromis mossambicus is the most widelycultured tilapia species and the culture of Tilapia rendalli is minus-cule. Much effort has been put by both government and non-gov-ernmental organisations to expand production in warm wateraquaculture with limited success. South Africa is a water scarcecountry and aquaculture will inevitably optimise utilisation of thisscarce resource.

T. rendalli (red-breasted tilapia) can potentially play an impor-tant role in South African aquaculture. T. rendalli like all tilapiasis well equipped to utilise plant diets with teeth in its pharyngealbone to truncate plant cell walls and expose their contents to thedigestive juices (Skelton, 2001). T. rendalli has several attributesthat make it a good candidate for aquaculture (El-Sayed, 2006);

feeding at low trophic level – macrophytes (Weliange et al.,2006), resistance to handling stress and disease, relatively fastgrowth, ability to reproduce readily in captivity and tolerance toa wide range of environmental conditions (temperature, low dis-solved oxygen levels, high ammonia levels). In spite of these qual-ities, the culture of T. rendalli in South Africa is still not fullyexploited.

For a fish species to be a good aquaculture candidate, it musthave fast growth rates. This growth performance is dependent onthe fish’s ability to break down and utilise the nutrients in its diet.Digestive enzymes are a good indicator of digestive capabilities infish; their activities control the effective breakdown and utilisationof nutrients in a diet, optimising growth and productivity (Chanet al., 2004; Debnath et al., 2007; Mohanta et al., 2008). Character-isation of digestive enzymes provides important information con-cerning the digestive capability of fish to hydrolyse protein,carbohydrate and lipid of feed ingredients (Essa et al., 2010; Santoset al., 2013).

The ability of a fish species to opportunistically feed on a varietyof food resources makes it a preferred species for aquaculture(El-Sayed, 2006). Therefore, the objectives of the current studywere to investigate the feeding habits of T. rendalli in a dam thathas very limited macrophytes (Flag Boshielo Dam). Furthermore,

34 S.N. Hlophe, N.A.G. Moyo / Physics and Chemistry of the Earth 66 (2013) 33–37

its growth performance and digestive capabilities (activity ofdigestive enzymes) under intensive culture were compared to thatof the widely cultured O. mossambicus.

2. Materials and methods

2.1. The diet of T. rendalli at Flag Boshielo Dam

Fish sampling was done at Flag Boshielo Dam (South Africa)monthly between February, 2010 and February, 2011 using sienenets and rod and line. T. rendalli were killed by placing on ice;stomach from each fish was removed fixed in 10% formalin. Inthe laboratory, each stomach was opened and food items identifiedunder a microscope (50�). The contribution of the food items byfrequency of occurrence was determined (Hyslop, 1980). Diversityof food items among size groups was established using Shannondiversity indices (Shannon and Weaver, 1949).

T. rendalli showed opportunistic feeding habit tendencies in FlagBoshielo Dam since its preferred macrophyte diet was limited. Itthen became prudent to investigate the aquaculture potential ofT. rendalli under an intensive culture regime. Firstly, its growth per-formance under intensive culture (fed a commercial tilapia diet)was compared to that of the widely cultured O. mossambicus. Sec-ondly, their digestive capabilities at a physiological level werecompared by measuring the activities of digestive enzymes (prote-ase, amylase, lipase and cellulase).

2.2. Growth performance of T. rendalli and O. mossambicus

In a completely randomised design experiment, a total oftwelve 1 m3 fibre glass tanks connected to a recirculating systemwere used. Twenty juvenile T. rendalli (11.5 ± 1.5 g) and twentyO. mossambicus (13.01 ± 1 g) were stocked in each tank. All fishwere hand-fed commercial tilapia pellets (crude protein 34%, en-ergy, 17 MJ/kg, fat 2.97% and fibre 2.3%) at 4% of their body weightper day. Feed was offered three times daily at 0900, 1300 and1700 h for 60 days. At the end of the feeding experiment, all fishwere weighed individually.

Growth performance was measured using the following in-dexes: Specific growth rate (SGR) was determined according toWinberg (1956): SGR = [(In Wt � In W0)/t] � 100; where: Wt = finalbody weight (g), W0 = initial body weight (g), t = time feeding per-iod (days), In = natural Logarithm (log)�10. Feed utilisation wasmeasured using feed conversion ratio (FCR) = food consumed (g)/mass gained (g) and protein efficiency ratio (PER) = total gain (g)/protein intake (g).

2.3. Digestive enzyme activities

For the determination of digestive enzyme activities in thedigestive tract of T. rendalli and O. mossambicus, 10 fish from eachtank were used. These fish were sacrificed 12 h after the last feed-ing. The fish were killed with a blow on the head and dissected onice. pH was measured in the stomach, proximal and distal intes-tines using a Crison Basic 02 pH meter form Lasec-SA. The tip ofthe microelectrode (diameter 4 mm) was inserted in small slitsmade in the stomach, proximal major coil and distal major coilintestines (Smith et al., 2000). The pH recorded in the different or-gans at collection was used to determine the pH of the buffer atwhich enzyme activity was measured. Enzyme activity in thestomach was determined in a glycine buffer (pH 2). In the proximaland distal intestines, the pH was 7; therefore enzyme activity wasmeasured in a phosphate buffer (pH 7). The stomach, proximal anddistal intestines from each treatment were separately homoge-nised (1:2 w/v) with 50 mM Tris–HCl buffer (pH 7.5) in an ice

water bath and centrifuged at 4 200�g for 60 min at 4 �C. The float-ing lipid fraction was discarded and the supernatant was stored at�20 �C until used.

Enzyme measurements were done in triplicate. Protease activ-ity was determined using the method of Bezerra et al. (2005). Amy-lase activity was determined by the 3,5-dinitrosalicylic acidmethod (Bernfeld, 1951). Cellulase activity was determined usingthe same procedure used for amylase activity, substituting thestarch substrate with carboxyl-methyl-cellulose (1% w/v). Lipaseactivity was determined using the method of Markweg et al.(1995). The protein concentration was computed using Lowryet al. (1951)’s method that uses bovine serum albumin as astandard.

2.4. Statistical analysis

One way analysis of variance (ANOVA) was used to determinesignificant differences on the growth performance parameters(SGR, PER and FCR) between T. rendalli and O. mossambicus. Oneway ANOVA was also used to identify any significant differencesin the activities of the digestive enzymes in the different parts ofthe digestive tract of T. rendalli and O. mossambicus. Significant dif-ferences were separated by Tukey’s test.

3. Results

3.1. The diet of T. rendalli at Flag Boshielo Dam

Cyperus sexangulasris and Panicum schinzi were the main fooditems found in the stomach regardless of fish size (Table 1). Thefrequency of occurrence of these plant diets (macrophytes) in-creased with increasing fish size. Zooplankton was the most impor-tant food item for T. rendalli fry (<2 cm). The importance ofzooplankton decreased as the fish size increased. Fish <2 cm stan-dard length (SL) generally did not feed on macrophytes as it wasfound only in 6% of the stomachs in this group. T. rendalli startedfeeding on macrophytes at 5 cm (SL; 9–10 g). Macrophytes werefound in 100% the stomachs of fish >15 cm. The diversity (Shan-non–Weiner (H1) of food items was lower (0.18) in the diet of fry(<2 cm) and highest (0.99) for the 15–19.9 cm size group (Table 1).

3.2. Growth performance of T. rendalli and O. mossambicus

T. rendalli recorded slightly lower SGR and PER than O. mossam-bicus, these differences however, were not significantly different(p > 0.05, ANOVA). The FCR on the other hand was significantlylower (p < 0.05) in T. rendalli than in O. mossambicus (Table 2).

3.3. Enzyme activities in the digestive tract of T. rendalli

Protease activity was higher in the distal intestine, followed bythe proximal intestine and the stomach had lowest activity forboth fish species (Fig. 1). There were no significant differences(P > 0.05) in protease activities for both species in the stomach,proximal or distal intestines.

Amylase activities were significantly higher in the proximalintestine than in the distal intestines or the stomach for both fishspecies. T. rendalli had significantly higher (p < 0.05) amylase activ-ity than O. mossambicus in the proximal and distal intestines(Fig. 2).

On the contrary, lipase activities were significantly higher in thestomach of O. mossambicus (4.54 lmol/min/mg protein) than inthat of T. rendalli (2.13 lmol/min/mg protein). Lipase activity inthe intestines however, was not significantly different betweenthe two fish species (Fig. 3).

Table 1Frequency of occurrence (%) of the main feed items in different length groups of Tilapia rendalli at Flag Boshielo Dam.

Length groups (SL-cm) <2 2–5 5–9.9 10–14.9 15–19.9 20–30

N 55.00 40.00 83.00 58.00 82.00 16.00Macrophytes 6.00 60.00 95.20 97.40 100.00 100.00Algae 35.00 42.00 49.40 57.90 50.00 11.10Zooplankton 100.00 75.00 67.50 57.90 50.00 11.10Chironomids 30.00 50.00 54.20 52.60 75.00 50.20Teleosts 0.00 0.00 29.40 32.60 34.50 35.00Detritus 25.00 80.00 90.40 100.00 87.50 88.90Insects 0.00 58.00 63.90 65.80 62.50 65.00H1 0.18 0.76 0.82 0.83 0.99 0.75

Table 2Specific growth rate (SGR), feed conversion ratio (FCR), protein efficiency ratio (PER)of T. rendalli and O. mossambicus fed commercial tilapia pellets.

Variable T. rendalli O. mossambicus

IBW (g) 11.50 ± 0.50 13.01 ± 1.00FBW (g) 49.12 ± 1.91 49.50 ± 0.08SGR (%/day) 2.23 ± 0.98a 2.42 ± 1.02a

FCR 1.43 ± 0.57a 1.25 ± 0.06b

PER 2.57 ± 0.94a 2.43 ± 0.03a

IBW –initial body weight, FBW – final body weight. Values are mean of four rep-licates ± standard deviations.Values in the same row with the similar superscripts are not significantly different(P > 0.05).

Stomach Proximal intestine Distal intestine

Prot

ease

act

ivity

(µm

ol/m

in/m

g pr

otei

n)

Organ

T. rendalli

O. mossambicus

Fig. 1. Protease activity in the stomach, proximal and distal intestines of Tilapiarendalli and Oreochromis mossambicus.

Stomach Proximal intestine Distal intestine

Am

ylas

e ac

tivity

(µm

ol/m

in/m

g pr

otei

n)

Organ

T. rendalli

O. mossambicus

Fig. 2. Amylase activity in the stomach, proximal and distal intestines of Tilapiarendalli and Oreochromis mossambicus.

0

5

10

15

20

25

30

Stomach Proximal intestine Distal intestine

Lip

ase

activ

ity (

µmol

/min

/mg

prot

ein)

Organ

T. rendalli

O. mossambicus

Fig. 3. Lipase activity in the stomach, proximal and distal intestines of Tilapiarendalli and Oreochromis mossambicus.

Table 3Cellulase enzyme activity (lmol/min/mg protein) in the stomach, proximal and distalintestines of Tilapia rendalli and Oreochromis mossambicus.

Stomach Proximal intestine Distal intestine

Cellulase activityT. rendalli 0.43 ± 0.00a 0.00 ± 0.00b 0.72 ± 0.01c

O. mossambicus 0.70 ± 0.43a 0.00 ± 0.00b 0.61 ± 0.00c

NB: values in the same block (enzyme – organ) with different superscripts aresignificantly different (P < 0.05).

S.N. Hlophe, N.A.G. Moyo / Physics and Chemistry of the Earth 66 (2013) 33–37 35

Marginal activities of cellulase were recorded in the stomachand distal intestine of both fish. No cellulase activity was recordedin the proximal intestine (Table 3). Cellulase activity was not sig-nificantly different between the fish species.

4. Discussion

In its natural environment (Flag Boshielo Dam), adult T. rendallifeed predominately on plant diets. Fry <2 cm (SL) fed mostly onzooplankton as the stomach at this size was not fully developed.This is evidenced by the lower diversity of feed items recordedfor this size group. Like most fish, T. rendalli experiences a size re-lated dietary shift as it starts feeding on zooplankton and beforebecoming specialised (Adeyemi et al., 2009; Elnady et al., 2010).

36 S.N. Hlophe, N.A.G. Moyo / Physics and Chemistry of the Earth 66 (2013) 33–37

Whitfield (1983) states that zooplankton is the major nutritionalsource of larval fish in most aquatic environments because of itshigher energy content relative to other organisms of equivalentsize. T. rendalli at Flag Boshielo Dam started feeding on marginalvegetation between 3 and 5 cm and the importance of the marginalvegetation increased with fish size. Similarly, the Shannon andWeaver diversity index shows that the diversity of food itemsfound in the stomach of T. rendalli increased with increasing fishsize, with older fish feeding on a variety of feed items than juve-niles. Flag Boshielo Dam is oligotrophic and has very limited mac-rophytes, adult T. rendalli were opportunistically feeding on otherplants particularly marginal vegetation. Detritus was also animportant food item for T. rendalli, the micro-organisms in it mayhave provided a protein source. This implies that T. rendalli areopportunistic feeders during periods when resources are scarceand may switch to a more specialised diet when resources areplenty. T. rendalli has the ability to utilise higher plants becauseit possesses bi-cuspid teeth and pharyngeal teeth which enable itto truncate and break down plant material. It is also able to secretehydrochloric acid in the stomach which help to further break downthe cell walls and expose its contents to digestive juices.

O. mossambicus is reported to have better growth performancethan T. rendalli (El-Sayed, 2006; Pauly et al., 1988). This however,is based on different studies conducted under different productionsystems. In order to account for any differences caused by the pro-duction system, in the present study the growth performance ofthe two fish species was compared under the same culture system.Although O. mossambicus has higher SGR and PER, these resultswere comparable as they were no significant differences. The sig-nificantly lower FCR recorded in O. mossambicus on the other hand,shows that O. mossambicus was able to utilise its diet moreeffectively.

Low pH (pH 2) was recorded in the stomach of both fish and thisshows that they secrete hydrochloric acid (HCl). Low stomach pHhas been reported in other tilapias (Getachew, 1989). The hydro-chloric acid secreted in the stomach helps to convert the inactivezymogen pepsinogen into the active protease enzyme pepsin,and also softens and initiate the breakdown of food (Perschbacheret al., 2010; Yúfera et al., 2012). In tilapias it is also significant inthe rupturing of cell walls of macrophytes and the thick walledgelatinous coated blue-green algae.

Protease activity was not significantly different between thetwo fish species. This supports the PER results observed whenthe two species were compared. Therefore, T. rendalli even thoughnot widely cultured as O. mossambicus, has a potential to produceenough protease enzymes to effectively utilise proteins in its diet.High proteolytic activities in herbivorous fish has also been re-ported by Chaudhuri et al. (2012) who found high protease activi-ties in Terapon jarbua and the protease activity did not differ fromthat of fish which fed primarily on animal diets. The high proteaseactivity recorded in these fish may be critical in efficiently utilisingthe low protein content in their natural plant diet. Hofer (1982)pointed out that in order to make up for the lower protein in theirdiets, herbivorous fish increased the amount of feed consumed andenzyme secreted. The activity of proteolytic enzymes is crucial inan aquaculture species since these enzymes are critical in the util-isation of protein (the most expensive nutrient) in formulated diets(Lundstedt et al., 2004; Montoya et al., 2010). Protein utilisationconsequently affects growth performance, production andprofitability.

The higher amylase activities recorded in the proximal intes-tines of T. rendalli suggest that this fish has a high capacity for car-bohydrate digestion than O. mossambicus and can be fed on highcarbohydrate based diets. Fish species that are able to effectivelyutilise carbohydrates are preferred in aquaculture because carbo-hydrates are inexpensive and readily available (Papoutsoglou and

Lyndon, 2003). Since fish feed to satisfy their energy requirements(De Silva and Anderson, 1995), when the energy in the diet is noteffectively utilised, protein may be used to meet the energy de-mand. Lipase activity was similar in both fish species. The proximalintestine is an ideal site for amylase and lipid digestion, because ofthe alkaline environment (Halver and Hardy, 2002; Klahan et al.,2009).

Tilapias normally do not produce cellulase in the gastrointesti-nal tract (El-Sayed, 2006). In this, study very low cellulase activitywas detected. This shows that both fish species have the capacityto break down cellulose albeit at low levels. These results confirmearlier studies that T. rendalli has a limited ability to digestcellulose in their natural plant diets (Hlophe and Moyo, 2011).Low cellulase activities have been reported for O. mossambicus(Saha et al., 2006).

5. Conclusion

This study shows that at the physiological level, T. rendalli hashigher amylase activities than O. mossambicus, it is inferred herethat T. rendalli is better equipped to utilise plant based diets. Cellu-lase activity was low in both species; therefore, the utilisation ofhigh cellulose diets may be enhanced by adding exogenous cellu-lase enzyme. It is thus recommended that further studies be under-taken to determine the growth performance of these fish when fedplant based proteins. T. rendalli may be a better species to be raisedon plant based diets especially in developing countries like SouthAfrica where rural farmers may not afford expensive fishmealbased diets.

Acknowledgements

The authors acknowledge the National Research Foundation forfunding this study. Our utmost appreciation is also extended to Mr.G. Geldenhuys for technical support.

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