Effects of dietary fermented mealworm larvae and stocking density on performance, blood stress indicator and intestine parameters of broilers
Abstract
The present study was conducted to evaluate the effects of the supplementation of defatted mealworm larvae meal fermented with probiotics as a new antibacterial feed additive to the diet of broilers reared under normal- (NSD) and high- (HSD) stocking density on growth performance, blood and slaughtering parameters, microorganism content and morphology of ileum and short-chain fatty acids content of ceca. A total of four hundred and fifty one-d-old Ross 308 male broiler chicks were randomly distributed into six groups of similar mean weight, each containing five replicates. Experimental treatments consisted of a 2 x 3 factorial arrangement with two levels of stocking density (12 birds/m2 as NSD and 18 birds/m2 as HSD) and three different mash diets: CONT- a corn-soybean meal-based diet containing no fermented defatted mealworm larvae meal (FDM) (0%); FDMLP- the diet obtained by supplementing DM fermented with Lactobacillus plantarum to the CONT diet (0.4%); FDMLB- the diet obtained by supplementing DM fermented with Lactobacillus brevis to the CONT diet (0.4%). HSD significantly decreased the growth performance except feed conversion ratio (FCR), carcass yields (CYs), Lactobacillus spp. content and villus height (VH) and villus surface area (VSA) of ileum and short-chain fatty acids (SCFAs) concentrations of ceca, but, increased the blood heterophil/lymphocyte (H/L) ratio and Escherichia coli content and crypt depth (CD) of ileum of broilers compared to NSD. The FDMLP and FDMLB diets significantly improved the FCR and increased final body weight (BW), BW gain, Lactobacillus spp. content and VH and VSA of ileum and SCFAs concentrations of ceca, however, reduced the blood H/L ratio and Escherichia coli content and CD of ileum of broilers when compared to the CONT diet. In conclusion, FDMLP and FDMLB can be utilized as new antibacterial feed additives in broiler diets regardless of stocking density.
Article Details
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Sarica, Ş, Yavuz, M., Sanli, E., Kati, A., Altuntas, S., Alatas, M., Ekici, M., Yazarel, S., & Keskintas, A. (2024). Effects of dietary fermented mealworm larvae and stocking density on performance, blood stress indicator and intestine parameters of broilers. Journal of the Hellenic Veterinary Medical Society, 75(3), 7887–7902. https://doi.org/10.12681/jhvms.35709
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- V. 75 N. 3 (2024)
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Riferimenti bibliografici
Alqaseem ZM Abo, Ahmed SA, Ahmed EA, Iraqi KG El (2018) Effect of
different stocking densities as an environmental stressing factor on
broiler behaviour and performance. Benha Vet Med J 34(2):51-65.
Altaf MT, Mahmud A, Mehmood S, Saime S (2019) Effects of supple
mented growth promoters on performance and intestinal morphology
in broilers reared under different stocking densities. Brazil J Poult
Sci 21(4):1-6.
Anonymous (1992) A possible way to count coliform bacteria groups and
E. coli numbers in feedstuffs and diets: A possible number (EMS).
Turkish Official Newspaper, an 21, No.21118.
AOAC 2007. Association of Official Analytical Chemists. 18 th. Edition,
W.D.C. USA.
Aslam B, Khurshid M, Arshad MI, Muzammil S, Rasool M, Yasmeen
N, Shah T, Chaudhry TH, Rasool MH, Shahid A, Xueshan X, Baloch
Z (2021) Antibiotic resistance: One health one world outlook. Fron
tiers in Cell Infect. Microbiol 11:1-20.
Benzertiha A, Kierończyk B, Kolodziejski P, Pruszyńska-Oszmalek E,
Rawski M, Józefiak A (2020) Tenebrio molitor and Zophobas mo
rio full-fat meals as functional feed additives affect broiler chickens’
growth performance and immune system traits. Poult Sci 99 (1):196
Borrelli L, Coretti L, Dipineto L, Bovera F, Menna F, Chiariottti L, Nizza
A, Lembo F, Fioretti A (2017) Insect-based diet, a promising nutri
tional source, modulates gut microbiota composition and SCFAs pro
duction in laying hens. Sci Reports/7:16269/1-12.
Boroojerdi NN, Rajabzadeh M (2021) The effect of replacing dried meal
worm with soybean meal on growth performance and carcass charac
teristics of broiler chickens. Res Square 1-16.
Calik A, Ergün A (2015) Effect of lactulose supplementation on growth
performance, intestinal histomorphology, cecal microbial population
and short-chain fatty acid composition of broiler chickens. Poult Sci
(9):2173-2182.
Calik A, Ceylan A, Ekim B, Adabi SG, Dilber F, Bayraktaroglu AG,
Turgay T, Ozen D, Sacakli P (2017) The effect of intra-amniotic and
posthatch dietary synbiotic administration on the performance, intes
tinal histomorphology, cecal microbial population, and short-chain
fatty acid composition of broiler chickens. Poult Sci 96(1):169-183.
Cengiz O, Koksal BH, Tatli O, Sevim O, Ahsan U (2015) Effect of di
etary probiotic and high stocking density on the performance, car
cass yield, gut microflora and stress indicators of broilers. Poult Sci
(10):2395-2403.
Chen H, Yu J, Ran X, Wu J, Chen Y, Tan B, Lin S (2023) Effects of yel
low mealworm (Tenebrio molitor) on growth performance, hepatic
health and digestibility in juvenile largemouth bass (Micropterus sal
moides). Anim 13 (1389):1-13.
Duncan DB (1955) Multiple Range Test and Multiple F Tests. Biometrics 11:1-42.
Elahi U, Xu CC, Wang J, Lin J, Wu SG, Zhang HJ, Qi GH (2022) Insect
meal as a feed ingredient for poultry. Anim Biosci 35(2):332-346.
Finke M (2007) An estimate of chitin in raw whole insects. Zoo Biol
(2):105-115.
Gasco L, Finke M, van Huis A (2018) Can diets containing insects pro
mote animal health? J. Insects as Food and Feed 4(1):1-4.
Gomes AVS, Quinteiro-Filho WM, Ribeiro A, Ferraz-de-Paula V, Pin
heiro ML, Baskeville E, Akamine AT, Astolfi-Ferreira CS, Ferreira
AJP, Palermo-Neto J (2014) Overcrowding stress decreases macro
phage activity and increases Salmonella Enteritidis invasion in broil
er chickens. Avian Pathol 43(1):82-90.
Goo D, Kim JH, Choi HS, Park GH, Han GP, Kil DY (2019) Effect of
stocking density and sex on growth performance, meat quality and
intestinal barrier function in broiler chickens. Poult Sci 98(3):1153
Gross WB, Siegel HS (1983) Evaluation of the heterophil/lymphocyte
ratio as a measure of stress in chickens. Avian Dis 27(4):972-979.
Hadj Saadoun J, Luparelli AV, Caligiani A, Macavel LI, Maistrello L, Ne
viani E, Galaverna G, Sforza S, Lazzi C (2020) Antimicrobial bio
masses from lactic acid fermentation of black soldier fly prepupae
and related by-products. Microorg 8(11):1-16.
Hajati H, Negarandeh R (2021) Does mealworm (Tenebrio molitor) can
be considered as a functional additive in Japanese quail’s diets?. Iran
J Appl Anim Sci 11(4):835-843.
Hong J, Han T, Kim YY (2020) Mealworm (Tenebrio molitor larvae) as an
alternative protein source for monogastric animal: A Review. Anim
(2068):1-20.
Hooge DM, Sims MD, Sefton AE, Spring P, Connolly A (2003) Effect of
dietary mannan oligosaccharide with or without bacitracin or virgin
iamycin, on live performance of broiler chickens at relatively high
stocking density on new litter. J Appl Poult Res 12(4):461-467.
Houshmand M, Azhar K, Zulkifli I, Bejo MH, Kamyab A (2012) Effects of
prebiotic, protein level, and stocking density on performance, immu
nity, and stress indicators of broilers. Poult Sci 91(2):393-401.
Islam Md M, Jang CJ (2017) Efficacy of mealworm and super mealworm
larvae probiotics as an alternative to antibiotics challenged orally
with Salmonella and E. coli infection in broiler chicks. Poult Sci
(1):27-34.
Józefiak A, Engberg RM (2017) Insect proteins as a potential source of an
timicrobial peptides in livestock production. A Review. J Anim Feed
Sci 26(2):87-99.
Józefiak A, Kierończyk B, Rawski M, Mazurkiewicz J, Benzertiha A,
Gobbi P, Nogales-Mérida S, Swiatkiewicz S, Józefiak D (2018) Full
fat insect meals as feed additive-the effect on broiler chicken growth
performance and gastrointestinal tract microbiota. J Anim Feed Sci
(2):131-139.
Khalil F, Ibrahim RR, Emeash HH, Hassan AHA (2021) Probiotic supple
mentation alleviated stress and improved performance, meat quality
sensory acceptability and microbiological status of broilers. J Adv Vet
Res 11(2):93-101.
Kridtayopas C, Rakangtong C, Bunchasak C, Loongyai W (2019) Effect
of prebiotic and synbiotic supplementation in diet on growth perfor
mance, small intestinal morphology, stress, and bacterial population
under high stocking density condition of broiler chickens. Poult Sci
(10):4595-4605.
Kwon GT, Yuk HG, Lee SJ, Chung YH, Jang HS, Yoo JS, Cho KH, Kong
H, Shin D (2020) Mealworm larvae (Tenebrio molitor L.) exuviae as
a novel prebiotic material for BALB/c mouse gut microbiota. Food
Sci Biotechnol 29(4):531-537.
Lee JH, Kim TK, Cha Ji Y, Yang HW, Yong HI, Choi YS (2022) How to
develop strategies to use insects as animal feed: digestibility, func
tionality, safety and regulation. J Anim Sci Technol 64(3):409-431.
Li J, Miao Z, Tian W, Yang Y, Wang J, Yang Y (2017) Effects of different
rearing systems on growth, small intestinal morphology and seleceted
indices of fermentation status in broilers. Anim Sci J 88(6):900-908.
Li XM, Zhang MH, Liu SM, Feng JH, Ma DD, Liu QX, Zhou Y, Wang XJ,
Xing S (2019) Effects of stocking density on growth performance,
growth regulatory factors and endocrine hormones in broilers under
appropriate environments. Poult Sci 98(12):6611-6617.
Li Y, Xing S, Wang X, Li X, Zhang M, Feng J (2022) Effects of increasing
stocking density on the performance and ileal microbiota of broilers.
J Poult Sci 59(3):261-296.
Luparelli AV, Hadj Saadoun J, Lolli V, Lazzi C, Sforza S, Caligiani A
(2022) Dynamic changes in molecular composition of black soldier
f
ly prepupae and derived biomasses with microbial fermentation.
Food Chem X14. 1-9.
Meena NN, Waiz HA, Chavhan DM, Tosawada K (2022) Impact of stock
ing density on broiler chicken performance, blood biochemistry, and
carcass attributes in an intensive rearing system. Iran J Appl Anim
Sci 12(4):803-812.
Menezes AGT, Ramos CL, Dias DR (2018) Combination of probiotic
yeast and lactic acid bacteria as starter culture to produce maize
based beverages. Food Res Int 111:187-197.
Mulyono M, Yunianto VD, Suthama N, Sunarti D (2019) The effect of
fermentation time and Trichoderma levels on digestibility and chemi
cal components of Black Soldier fly (Hermetia illucens) larvae. Live
stock Res. Rural Develop 31(10):1-4.
Nooreh Z, Taherpour K, Gharaei MA, Shirzadi H, Ghasemi HA (2021) Ef
fects of a dietary direct-fed microbial and Ferulago angulate extract
on growth performance, intestinal microflora, and immune function
of broiler chickens infected with Campylobacter jejuni. Poult Sci
(3):1-10.
Oddon SB, Biasato I, Imarisio A, Pipan M, Dekleva D, Colombino E,
Capucchio MT, Meneguz M, Bergagna S, Barbero R, Gariglio M,
Dabbou S, Fiorilla E, Gasco L, Schiavone A (2021) Black soldier fly
and yellow mealworm live larvae for broiler chickens: Effects on bird
performance and health status. J Anim Physiol Anim Nutr 105(Suppl
:10-18.
Peng W, Talpur MZ, Zeng Y, Xie P, Li J, Wang S, Wang L, Zhu X, Gao P,
Jiang Q, Shu G, Zhang H (2022) Influence of fermented feed additive
on gut morphology, immune status and microbiota in broilers. BMC
Vet Res 18(218):1-16.
Rafiq K, Hossain MT, Ahmed R, Hasan Md M, Islam R, Hossen Md I,
Shaha SN, Islam MR (2022) Role of different growth enhancers as al
ternative to in-feed antibiotics in poultry industry. Fron Vet Sci 8:1-9.
Rashidi N, Ghorbani MR, Tatar A, Salari S (2019) Response of broiler
chickens reared at high density to dietary supplementation with lico
rice extract and probiotic. J Anim Physiol Anim Nutr 103(1):100-107.
Ross 308 Broiler: Nutrition Specification. (2007) http:/www.natchix.co.
za/pdf/nutrition_specifications.pdf.
Sakamoto K, Hirose H, Onizuka A, Hayashi M, Futamura N, Kawamura
Y, Ezaki T (2000) Quantitative study of changes in intestinal mor
phology and mucus gel on total parenteral nutrition in rats. J Surgical
Res 94(2):99-106.
Sanchéz-Muros MJ, Barrosa FG, Manzano-Agugliaro F (2014) Insect
meal as renewable source of food for animal feeding: A review. J
Cleaner Prod 65:16-27.
Sedgh-Gooya S, Torki M, Darbernamieh M, Khamisabadi H, Abdolmoha
madi A (2022) Growth performance and intestinal morphometric fea
tures of broiler chickens fed on dietary inclusion of yellow mealworm
(Tenebrio molitor) larvae powder. Vet Med Sci 8(5):2050-2058.
Senol M, Nadaroglu H, Dikbas N, Kotan R (2014) Purification of chiti
nase enzymes from Bacillus subtilis bacteria TV-125, investigation
of kinetic properties and antifungal activity against Fusarium culmo
rum. Annals Clin Microbiol Antimic 13(35):1-7.
Shakeri M, Zulkufli I, Soleimani AF, O’Reilly EL, Eckersall PD, Anna
AA, Kumari S, Abdullah FFJ (2014) Response to dietary supple
mentation of L-glutamine and L-glutamate in broiler chickens reared
at different stocking densities under hot, humid tropical conditions.
Poult Sci 93(11):2700-2708.
Shazali N, Foo HL, Loh TC, Choe DW, Rahim RA (2014) Prevalence of
antibiotic resistance in lactic acid bacteria isolated from the faeces of
broiler chicken in Malaysia. Gut Pat 6(1):1-7.
Shi H, Zhang M, Wang W, Devahastin S (2020) Solid-state fermentation
with probiotics and mixed yeast on properties of okara. Food Biosci
:1-8.
Son YJ, Hwang IK, Nho CW, Kim SM, Kim SH (2021) Determination
of carbohydrate composition in mealworm (Tenebrio molitor L.)
larvae and characterization of mealworm chitin and chitosan. Foods
(640):1-15.
Song J, Xiao K, Ke YL, Jiao LI, Hu CH, Diao QY, Shi B, Zou XT (2014)
Effect of a probiotic mixture on intestinal microflora morphology
and barrier integrity of broilers subjected to heat stress. Poult Sci
(3):581-588.
Sugiharto S (2022) Dietary strategies to alleviate high-stocking-densi
ty-induced stress in broiler chickens-a comprehensive review. Arch
Anim Breeding 65(1):21-36.
SPSSWIN (2007) SPSS for Windows 6.1.4. SPSSWIN. Istanbul, Turkey.
Xue G, Cheng S, Yin J, Zhang R, Su Y, Li X, Li J, Bao J (2021) Influence
of pre-slaughter fasting time on weight loss, meat quality and carcass
contamination in broilers. Anim Biosci 34 (6):1070-1077.
Zhang HY, Piao XS, Zhang Q, Li P, Yi JQ, Liu D, Li Y, Wang Q (2013)
The effects of Forsythia suspense extract and berberine on growth
performance, immunity, antioxidant activities and intestinal micro
biota in broilers under high stocking density. Poult Sci 92(8):1981
