Growth performance, immune status and intestinal fermentative processes of young turkeys fed diet with additive of full fat meals from Tenebrio molitor and Hermetia illucens

https://doi.org/10.1016/j.anifeedsci.2021.114994Get rights and content

Highlights

  • Monensin improved performance of turkeys, while the insect meals had no such effect

  • Meals from Hermetia illucens exerted stronger immune and antioxidant effect than monensin

  • Insect meals limited the bacterial enzymatic activity as same as monensin

Abstract

Full-fat insect meals were used in young turkeys feeding as feed additives to exert beneficial changes in the intestinal bacterial ecosystem functioning as well as in the immune and antioxidant systems. Two full-fat insect flours obtained from Tenebrio molitor (TM) and Hermetia illucens (HI) insects were added to the base diet (C) in the amount of 3 g/kg and compared to the control and to the effects following common monensin (MON) addition (dietary treatments: C, MON, TM, and HI). Although, the addition of full-fat insect meals to the diet didn't improve performance results such as monensin, it does exerted anti-inflammatory, immunostimulatory and antioxidant changes in turkeys’ blood. The HI and TM dietary treatments caused beneficial reduction in the blood total cholesterol content as well as increase in phosphorus which was not noted in MON treatment. The results indicated that in comparison to the control diet without any additives, the MON, TM and HI additives showed non-selective bacteriostatic properties, without adverse intensification of protein fermentation and pH digesta rise in the caeca of young turkeys. The addition of TM and HI similar as MON reduced the enzymatic activity of caecal microbiota, and decreased caecal concentration of all short-chain fatty acids, except butyric one. The caecal ammonia and dry matter concentration, and pH value of digesta were not affected by dietary treatments.

Introduction

Insects can be used as an alternative source of protein and fat in poultry feed (Marono et al., 2017; Józefiak and Engberg, 2017). Insect full–fat meals obtained from black soldier fly larvae, housefly maggots and pupae, mealworms, silkworm pupae, locusts, grasshoppers and crickets have been used as a replacement for soybeans or as a feed additive in the diet of various livestock animals (Sanchez-Muros et al., 2014; Bovera et al., 2015, 2016; Józefiak et al., 2016, 2018; Biasato et al., 2017; Kierończyk et al., 2018b). In Europe, the use of insect meal in the production of poultry meat is not yet authorized, and it may be possible that the current legal restrictions will be revised (EFSA, 2016).

According to Veldkamp et al. (2012), full fat insect meals contain a high amount of crude protein (350–600 g/kg of dry matter (DM)) with comparable amino acids composition to that of soybean. Particularly, in the case of lysine content, which ranges from 60 to 80 g/kg of crude protein (Makkar et al., 2014). Full–fat insect meals also contain large amounts of fat, (310–550 g/kg) (Ramos-Elorduy et al., 2002; Józefiak et al., 2016; Benzertiha et al., 2019; Kierończyk et al., 2018a). Furthermore, full-fat insect meals are a rich source of calcium (50–80 g/kg DM) and phosphorous (6–15 g/kg DM) (Arango Gutierrez et al., 2004; St-Hilaire et al., 2007; Yu et al., 2009). Insect larvae also contain chitin which is a main part of their exoskeleton. Finke (2007) indicated that the estimated chitin content of insect species ranged from 2.7 to 49.8 mg/kg and 11.6–137.2 mg/kg (dry matter basis).

Although, chitin may negatively affect protein digestibility (Longvah et al., 2011), many researchers have shown that it has a positive effect on immune and antioxidant functions in poultry (Sanchez-Muros et al., 2014; Bovera et al., 2016; Lee et al., 2008). In addition to chitin, antimicrobial peptides (AMPs) also have a stimulating effect on the immune system (Dutta and Das, 2016; Józefiak and Engberg, 2017). Literature data show that AMP are peptides with a wide range of activity against bacteria, fungi and viruses (Thacker, 2013; Józefiak and Engberg, 2017; Wu et al., 2018). Inclusion of small amounts of full-fat insect meals (0.5–2 g/kg) in the diet of broiler chickens can modulate the composition of the gut microbiota (Józefiak et al., 2018). Research by Ramos-Elorduy et al. (2002) has shown that due to the high content of crude protein and fat in insect larvae, their use in broiler diets should be limited to 100 g/kg of the total dry matter of the diet. However, according to Józefiak and Engberg (2017), in chicken diets based on soybean meal they can be used with no adverse effect on feed consumption, body weight gain (BWG) or feed conversion ratio (FCR).

Administration of coccidiostats among others monensin with feed is an effective method of preventing coccidiosis in poultry. Treatment with monensin acted to affect a number of bacterial genera within the chicken cecum and act to reduce lactobacilli populations in the ileum and caecum (Danzeisen et al., 2011). Studies carried out so far in turkey chicks have shown the effect of monensin on the acquisition of immunity against coccidiosis (Arczewska-Włosek and Świątkiewicz, 2015; Chapman, 2008; Mathis, 1993). Although there are reports of the possibility of stimulating the immune system, monensin may also accumulate in tissues and be toxic from errors in the calculation and formulation of medicated feed, inadequate mixing, and exposure of nonintended species to medicated rations (Chapman, 2008). In this context, the idea of using alternative nutrition methods as a factor supporting immunoprophylaxis in stimulating immunity while maintaining high performance, is highly justified. In the future, they may find use in the prevention of coccidiosis in poultry. Therefore, it has been hypothesized that the small dietary addition of 3 g/kg full-fat insect meal, can be functional feed additives that improve the metabolism and growth performance of turkeys and also stimulate their immune and antioxidant system and limiting bacterial activity in different gastrointestinal segments in a similar or more effective way than monensin. This study was conducted to determine whether the addition of full-fat insect meals from Tenebrio molitor and Hermetia illucens in the amount of 3 g/kg to the basal diet has a more beneficial effect than monensin on the metabolism, immune, antioxidant status, bacterial activity in different gastrointestinal segments and growth performance of turkeys.

Section snippets

Animals and diets

The experiment was carried out in a poultry house at the experimental facilities of the Department of Poultry Science, University of Warmia and Mazury in Olsztyn, Poland. A total of 224 one-day-old male Hybrid Converter turkeys were obtained from a local commercial hatchery, Grelavi in Kętrzyn (Poland). Birds were randomly divided into four treatment groups, with eight replicates of seven birds each. The duration of the experiment was 28 days. The birds were kept in cages (0.5 × 1 m), and all

Results

Compared to turkeys from group C, TM, and HI, the birds from MON group excelled them with respect to higher BW and DBWG (both, P < 0.05) and better FCR (P < 0.05) (Table 4).

In comparison to group C, lower plasma content of TC (P < 0.05) and higher content of P (P < 0.001) were noted in the turkeys from groups TM and HI. In the turkeys from group TM, plasma AST activity (P < 0.05) was lower than in the turkeys from group C. The plasma Cu content in the turkeys from group HI was found to be lower

Discussion

According to the available literature, insects are a rich source of antimicrobial peptides (AMPs), which can be used as an alternative to antibiotics in livestock production to improve animals’ growth and health or to treat infections (Józefiak and Engberg, 2017; Pretorius, 2011). In the present study, the addition of ionophore coccidiostatic monensin to the feed improved the growth performance of turkeys, while no such effect was observed when Tenebrio molitor or Hermetia illucens meal was

Conclusions

The addition of monensin to the growing turkey diet improved their growth performance, while the addition of full-fat Tenebrio molitor or Hermetia illucens meal had no such effect. The results obtained in the present study indicated that the relative small dietary addition of 3 g/kg full-fat insect meal, both from Tenebrio molitor or Hermetia illucens, exerted similar intestinal effects to those resulted from the addition of antibiotic monensin to a feed, and it limited the bacterial enzymatic

Author statement

Conceptualization – Jan Jankowski, Krzysztof Kozłowski, Katarzyna Ognik; Data curation – Krzysztof Kozłowski, Katarzyna Ognik, Jerzy Juśkiewicz; Formal analysis - Anna Stępniowska, Jerzy Juśkiewicz, Katarzyna Ognik; Funding acquisition - Jan Jankowski, Damian Józefiak, Katarzyna Ognik, Anna Stępniowska, Zenon Zduńczyk; Investigation - Katarzyna Ognik, Zenon Zduńczyk; Methodology - Krzysztof Kozłowski, Damian Józefiak, Jan Jankowski; Resources - Jan Jankowski, Katarzyna Ognik; Supervision - Jan

Declaration of Competing Interest

We declare that all listed authors meet and agree on the following criteria:

This study is original and has not been published elsewhere.

All data presented in the manuscript have been checked and are reliable.

All authors have read and accepted the manuscript as it is submitted for publication.

All authors have approved the final version of the manuscript for publication.

Acknowledgements

This work was partially supported by project TEAM TECH no. POIR.04.04.00-00-204E/16-00, entitled: Insects as novel protein sources for fish and poultry" and partially by project of Ministry of Science and Higher Education (Warsaw, Poland) in frame of the program entitled "Regional Initiative of Excellence" for the years 2019-2022, no. 010/RID/2018/19.

References (69)

  • G.F. Mathis

    Toxicity and acquisition of immunity to coccidia in turkeys medicated with anticoccidials

    J. Appl. Poult. Res.

    (1993)
  • M.J. Sanchez-Muros et al.

    Insect meal as renewable source of food for animal feeding: a review

    J. Clean. Prod.

    (2014)
  • G. Secci et al.

    Mechanical separation process for the value enhancement of Atlantic horse mackerel (Trachurus trachurus), a discard fish

    Innov. Food Sci. Emerg. Technol.

    (2017)
  • D.P. Smith et al.

    Prevalence and numbers of bacteria in broiler crop and gizzard contents

    Poult. Sci.

    (2006)
  • D. Zhang et al.

    Functional analyses of the digestive b-glucosidase of formosan subterranean termites (Coptotermes formosanus)

    J. Insect Physiol.

    (2012)
  • AOAC

    Official Methods of Analysis of the Association of the Official Analytical Chemists

    (2005)
  • G.P. Arango Gutierrez et al.

    Compositional, microbiological and protein digestibility analysis of larval meal of Hermetia illucens (Diptera: stratiomyidae) at Angelopolis-Antioquia

    Colombia. Rev. Fac. Nac. Agron. Medellin.

    (2004)
  • A. Arczewska-Włosek et al.

    The efficacy of selected feed additives in the prevention of broiler chicken coccidiosis under natural exposure to Eimeria spp

    Ann. Anim. Sci.

    (2015)
  • A. Benzertiha et al.

    Insect oil as an alternative to palm oil and poultry fat in broiler chicken nutrition

    Animals

    (2019)
  • I. Biasato et al.

    Effects of dietary Tenebrio molitor meal inclusion in free‐range chickens

    J. Anim. Physiol. Nutr.

    (2016)
  • L. Borrelli et al.

    Insect-based diet, a promising nutritional source, modulates gut microbiota composition and SCFAs production in laying hens

    Sci. Rep.

    (2017)
  • F. Bovera et al.

    Yellow mealworm larvae (Tenebrio molitor, L.) as a possible alternative to soybean meal in broiler diets

    Br. Poult. Sci.

    (2015)
  • F. Bovera et al.

    Use of Tenebrio molitor larvae meal as protein source in broiler diet: Effect on growth performance, nutrient digestibility, and carcass and meat traits

    J. Anim. Sci.

    (2016)
  • D.M.E. Bowdish et al.

    Immunomodulatory properties of defensins and cathelicidins

    Curr. Top. Microbiol. Immunol.

    (2006)
  • H.D. Chapman

    Coccidiosis in the turkey

    Avian Pathol.

    (2008)
  • S. Chu et al.

    Extracellular pH regulation in microdomains of colonic crypts: effects of short-chain fatty acids

    Proc. Natl. Acad. Sci.

    (1995)
  • A. Cieślak et al.

    A note on comparison of two extraction methods used to quantify C18 fatty acids in feed and digesta of ruminants

    J. Anim. Feed Sci.

    (2009)
  • S. Dabbou et al.

    Black soldier fly defatted meal as a dietary protein source for broiler chickens: effects on growth performance, blood traits, gut morphology and histological features

    J. Anim. Sci. Biotechol.

    (2018)
  • M. Dabek et al.

    Distribution of β-glucosidase and β-glucuronidase activity and of β-glucuronidase gene gus in human colonic bacteria

    FEMS Microbiol. Ecol.

    (2008)
  • J.L. Danzeisen et al.

    Modulations of the chicken cecal microbiome and metagenome in response to anticoccidial and growth promoter treatment

    PLoS One

    (2011)
  • P. Dutta et al.

    Mammalian antimicrobial peptides: promising therapeutic targets against infection and chronic inflammation

    Curr. Top. Med. Chem.

    (2016)
  • U. Dz

    266, Polish Act of Law of 15 January 2015 on the Protection of Animals Used for Scientific or Educational Purposes

    (2015)
  • EFSA et al.

    Revision of the currently authorised maximum copper content in complete feed

    EFSA J.

    (2016)
  • EU Commission Implementing Regulation No 495/2011 of 20 May

    Amending Regulation (EC) No 109/2007 As Regards the Composition of the Feed Additive Monensin Sodium

    (2011)
  • Cited by (0)

    View full text