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DIGESTIVE ENZYMES IN AFRICAN GIANT LAND ( MARGINATA) DURING

ENZIMAS DIGESTIVOS DEL CARACOL GIGANTE AFRICANO (ARCHACHATINA MARGINATA), DURANTE LA ESTIVACIÓN

Ademolu, K.O.1*; Fakeye, O.D.1; Dedeke, G.A.1; Ajayi, O.A.1 and Idowu, A.B.1

1Biological Sciences Department. University of Agriculture. Abeokuta. Nigeria. *[email protected]

ADDITIONAL KEYWORDS PALABRAS CLAVE ADICIONALES Gut regions. Tracto digestivo.

SUMMARY The activities of digestive enzymes in the gut of protein. In many developing regions of African giant , Archachatina countries meat production from domestic marginata were investigated during aestivation livestock is not sufficient to meet the high induced in the laboratory by the withdrawal of demands for animal protein (Adedire et water and food for three weeks. All studied α al.,1999). Revitalization of some wild animal enzymes, amylase, -glucosidase, cellulase, lipase, like snail could assist in combating and protease, were detected on the gut regions (oesophagus, , stomach and intestine). this challenge (Ajayi and Tewe, 1985). Aestivated had significantly lower enzyme However, raising of snails in captivity is activities in all the gut regions than the active faced with problem of feeding and nutrition. snails. Furthermore the stomach recorded the Ademosun and Imevbore (1988) opined that highest enzyme activities of all the gut regions. commercial snail farming should use food stuffs which are not competed for by other RESUMEN livestock. Ademolu et al. (2007) similarly observed that snails consumed poultry Se investigaron las actividades de las enzimas dropping based diet and recorded a better del tracto digestivo del caracol gigante africano Archachatina marginata durante la estivación, growth performance than snails fed with inducida en laboratorio mediante retirada del agua conventional feeds. Furthermore, snails y alimento durante tres semanas. Todas las enzimas have been reported to consume household estudiadas, amilasa, α-glucosidasa, celulasa, wastes which were converted and utilized lipasa y proteasa fueron encontradas en las for their growth and egg production regiones del tracto digestivo (estómago, intestino, (Amusan and Omidiji, 1999; Ademolu et al., esofago y bulbo oral). Los caracoles en estivación 2011). tienen, en todas las regiones del tracto digestivo, In Nigeria, snails aestivate during the actividades enzimáticas significativamente meno- dry season months of November-March. res que los caracoles activos. En el estómago, se During this period, the mouth is registró la mayor tasa de actividad enzimática de todo el tracto digestivo. temporarily closed by a whitish calcium material called (Odaibo, 2003). INTRODUCTION This process is adaptive in nature as it assists the snails to survive the adverse The African giant land snails are atmospheric condition when water and food regarded as delicacies and important source are partially not available. Ademolu et al.

Recibido: 16-2-11. Aceptado: 12-9-12. Arch. Zootec. 62 (237): 73-77. 2013. ADEMOLU, FAKEYE, DEDEKE, AJAYI AND IDOWU

(2009) recently reported that the activities mined following the methods described by of glycosidases in the foot muscles Archa- Adedire et al. (1999) and Ademolu et al. chatina marginata reduced significantly (2009). All the enzyme assays were done in during aestivation. triplicates. The digestive tracts of giant land snails The data from the experiment were are endowed with multiples of enzymes like subjected to analysis of variance (ANOVA), cellulase, trypsin, lipase, α-glucosidase and separation of significant means was done protease (Adedire et al., 1999). However, so by Student-Newman Kuel (SNK). far in literature, no attention has been paid to the digestive enzymes of snails during RESULTS aestivation like had been done for snails during active periods. This study therefore The result of amylase assay in the gut examines the digestive enzymes activities region shows that active snails recorded in the gut of A. marginata during aestivation. significantly higher activities (p<0.05) in all This will help to understand their digestion the gut regions than aestivated snails (table biology and utilization of nutrients during I). Stomach has the highest amylase activity this period. followed by the crop. The α-glucosidase activities in the gut table II MATERIALS AND METHODS regions of the snails are shown in . Active snails recorded a significantly higher Forty individuals of A. marginata (130 ± α-glucosidase activity in all the gut regions 0.02 g; obtained from the Department of except the oesophagus. The stomach Forestry and Wildlife Management, Univer- followed by the crop recorded highest α- sity of Agriculture, Abeokuta, Nigeria), were glucosidase activity. randomly divided into two groups of twenty The cellulase activity is found to be individues: active snails and aestivated statistically higher in active snails than the snails. Each group was further divided into aestivated ones. The stomach similarly 4 baskets (45 x 20 x 21 cm) containing 5 snails recorded the highest activity while the in- each to avoid over crowding. testinal recorded the least (table III). Active snails were fed with pawpaw Table IV shows the result of protease leaves ad libitum and drinking water was activity in the gut regions of both active and also provided daily. Aestivated snails were aestivated snails. Gut regions of active snails denied water and food and thus formed epiphragm in the mouth aperture after three Table I. Activity of amylase (Abs/min) in the weeks. The two groups were observed for gut regions of Archachatina marginata snails. three months. (Actividad de la amilasa (Abs/min) en las regiones The snails were dissected using the del tracto digestivo de caracoles Archachatina methods of Segun (1975). The various marginata). regions of alimentary canal (oesophagus, crop, stomach and intestine) were carefully Gut regions Active snails Aestivated snails dissected out and each region homogenized separately in 20 mL of phosphate buffer (PH Intestine 7.0±0.1a 5.0±0.02b 7.0). The homogenate was centrifuged at Oesophagus 5.0±0.2a 3.0±0.1b a b 4000 r.p.m. for 30 min. The sediment was Stomach 11.0±0.11 9.0±0.2 Crop 9.0±0.01a 7.0±0.15b discarded while the supernatant was used as enzyme extract. ab α Mean values in the same row with different Cellulase, -glucosidase, amylase, superscript are significantly different (p<0.05). protease and lipase activities were deter-

Archivos de zootecnia vol. 62, núm. 237, p. 74. DIGESTIVE ENZYMES IN AFRICAN GIANT LAND SNAIL DURING AESTIVATION

Table II. Activity of α-glucosidase (Abs/min) Table IV. Activity of protease (Abs/min) in in the gut regions of Archachatina marginata the gut regions of the experimental snails. snails. (Actividad de la α-glucosidase (Abs/min) (Actividad de la proteasa (Abs/min) en las regio- en las regiones del tracto digestivo de caracoles nes del tracto digestivo de caracoles Archachatina Archachatina marginata). marginata).

Gut regions Active snails Aestivated snails Gut regions Active snails Aestivated snails

Intestine 21.0±0.1a 18.0±0.13b Intestine 44.0±0.41a 32.0±0.14b Oesophagus 18.0±0.16a 24.0±0.04a Oesophagus 29.0±0.21a 15.0±0.22b Stomach 41.0±0.23a 27.0±0.32b Stomach 59.0±0.15a 26.0±0.11b Crop 32.0±0.15a 22.0±0.22b Crop 38.0±0.10a 29.0±0.30b abMean values in the same row with different abMean values in the same row with different superscript are significantly different (p<0.05). superscript are significantly different (p<0.05). had a higher protease activity than the present in all the gut regions of the alimentary aestivated snails. However, intestine recor- canal of A. marginata during periods of ded highest activity out of all the regions. activity and aestivation. The various Aestivated snails had a significantly carbohydrases detected in the gut of the (p<0.05) lower lipase activity in their gut experimental snails are highly needed for regions than active snails (table V). Intestine digestion and utilization of various carbohy- recorded the least activity while stomach drates consumed by snails. Amylase has the highest activity. presence in the gut was not surprising as it is needed to hydrolyze starch which is the DISCUSSION main component of pawpaw leaves consu- med by the snails. The high activity of α- African giant land snail is well equipped glucosidase was not unexpected as it is with various enzymes to cater for its responsible for the breakdown of cellobiose, multivarious feeding habit (Yoloye, 1994). the product of cellulose hydrolysis which is This study confirms this as protease, lipase, the common part of plant cell ( Pigman and α-glucosidase, amylase and cellulase were Horton, 1970). Higher α-glucosidase activity

Table III. Activity of cellulase (Abs/min) in Table V. Activity of lipase (Abs/min) in the gut regions of the experimental snails. (Acti- gut regions of the experimental snails. (Acti- vidad de la celulasa (Abs/min) en las regiones del vidad de la lipasa (Abs/min) en las regiones del tracto digestivo de caracoles Archachatina tracto digestivo de caracoles Archachatina marginata). marginata).

Gut regions Active snails Aestivated snails Gut regions Active snails Aestivated snails

Intestine 15.0±0.04a 11.0±0.08b Intestine 8.0±0.17a 5.0±0.1b Oesophagus 18.0±0.02a 15.0±0.18b Oesophagus 14.0±0.80a 9.0±0.20b Stomach 36.0±0.3a 32.0±0.02b Stomach 19.0±0.12a 15.0±0.1b Crop 24.0±0.19a 21.0±0.1b Crop 12.0±0.01a 8.0±0.01b abMean values in the same row with different abMean values in the same row with different superscript are significantly different (p<0.05). superscript are significantly different (p<0.05).

Archivos de zootecnia vol. 62, núm. 237, p. 75. ADEMOLU, FAKEYE, DEDEKE, AJAYI AND IDOWU was observed in the gut regions of both in the foot muscle of A. marginata during active and aestivated snails. This parallels aestivation. the report of Umezurike (1976) where a high Stomach region recorded the highest α-glucosidase activity was found in the gut activity for all the enzymes assayed. Stomach of land snail . This reveals of snails is the central region of alimentary that the major diet of the experimental snails canal that receives most food substances is plants based and thus are more herbi- for digestion (Segun, 1975). In a related vorous. The presence of cellulase in the gut experiment, Adedire et al. (1999) reported of the experimental snails is noteworthy. that hepatopancrease recorded the highest This is not synthesized by and its enzymatic activities in the gut of A. margi- presence in these snails suggests a symbiotic nata. These higher enzymatic activities relationship between microorganisms and recorded for the stomach in this study might the snails. Microbes help in digestion of not be unconnected to the closeness of the snails by either secreting enzymes or supply two organs (stomach and ) of vitamins (Akinnusi, 2002; Idowu et al., and hence possible backward ciliary and 2008). muscular movement of enzymes into the The presence of protease and lipase in stomach (Segun, 1975; South, 1992). the gut regions suggests that the experi- mental snails consumed fatty and proteic CONCLUSION food substance along with their normal carbohydrate diets. Amusan and Omidiji Aestivation significantly reduces the (1999) had earlier observed that earthworms, activities of digestive enzymes of the snails, ants and mush room formed parts of snails thereby lowering their nutrient uptake from feed while in captivity and the wild. the diet consumed. Snails cannot afford Enzymatic activities in the gut regions of reduction in these enzymes as they are active snails were significantly higher than responsible for utilization of nutrients in those of a aestivated snails. During their diets. Basically, reduced activities of aestivation the mouth aperture of the snails amylase and cellulase mean low energy is closed and feeding is thus impossible derivation from the diets which in turns unlike active snails that were and leads to poor productivity. drinking continuously. Secretion of enzy- Therefore, for maximum/optimum snail mes is in direct response to the presence of production in captivity, aestivation should nutrients (Terra et al., 1996) and when there be avoided in the dry season by continually was no substrate to act upon, it resulted to moistening the habitat of the snails. Also, low enzymes activities as observed in this good management practices should be put study. Ademolu et al. (2009) similarly in place like: regular cleaning, pest control observed reduced activities of glycosidases and good stocking density.

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