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Carcass and meat quality of rabbits fed Tithonia tubaeformis weed

ABSTRACT

The objective of this study was to use different parts of the Tithonia tubaeformis plant in feed for fattening rabbits and then observe the effects on carcass and meat quality. Forty-eight weaned rabbits (35 days of age) were randomly assigned to four groups (n = 12 by treatment). Animals were fed ad libitum a control diet as well as three experimental diets, with addition of Tithonia tubaeformis leaves, whole plant, and stems. Rabbits were slaughtered after 63 days of age without fasting. Results indicate that live weight (0.917), skin (0.79), feet (6.679), and lumbar circumference of the carcass (0.707) have higher positive correlations with hot carcass. There were no significant differences between treatments for all variables measured, except for kidneys and kidney fat. pH and color values were different among treatments. The results indicate that Tithonia tubaeformis leaves or the whole plant could be added to feed for growing rabbits.

Keywords:
color; invasive plant; meat; texture

Introduction

Rabbit meat has several advantages over other meats due to its fatty acids profile, high protein content, several vitamins and minerals, and low cholesterol and sodium contents (Para et al., 2015Para, P. A.; Ganguly, S.; Wakchaure, R.; Sharma, R.; Mahajan, T. and Praveen, P. K. 2015. Rabbit has the potential of being a possible alternative to other meats as a protein source: A brief review. International Journal of Pharmacy and Biomedical Research 2:17-19.). However, rabbit meat has low consumption per capita and, consequently, production is low. There are some problems associated with rabbit production, including the cost of feed, as well as digestive complications, especially with fattening rabbits, which affect productive parameters, e.g., daily gain, feed intake, among other factors. The use of plants in feed is an area that has been gaining interest over the past few years with regard to rabbit production research, as plants contain bioactive compounds that can improve carcass and meat quality (Cardinali et al., 2015Cardinali, R.; Cullere, M.; Dal Bosco, A.; Mugnai, C.; Ruggeri, S.; Mattioli, S.; Castellini, C.; Trabalza Marinucci, M. and Dalle Zotte, A. 2015. Oregano, rosemary and vitamin E dietary supplementation in growing rabbits: Effect on growth performance, carcass traits, bone development and meat chemical composition. Livestock Science 175:83-89. https://doi.org/10.1016/j.livsci.2015.02.010
https://doi.org/10.1016/j.livsci.2015.02...
; Kone et al., 2016Kone, A. P.; Cinq-Mars, D.; Desjardins, Y.; Guay, F.; Gosselin, A. and Saucier, L. 2016. Effects of plant extracts and essential oils as feed supplements on quality and microbial traits of rabbit meat. World Rabbit Science 24:107-119. https://doi.org/10.4995/wrs.2016.3665
https://doi.org/10.4995/wrs.2016.3665...
). The use of nutritional antioxidants in livestock systems is considered the key to improve rabbit production (Elwan et al., 2019Elwan, H. A. M.; Elnesr, S. S.; Mohany, M. and Al-Rejaie, S. S. 2019. The effects of dietary tomato powder (Solanum lycopersicum L.) supplementation on the haematological, immunological, serum biochemical and antioxidant parameters of growing rabbits. Journal of Animal Physiology and Animal Nutrition 103:534-546. https://doi.org/10.1111/jpn.13054
https://doi.org/10.1111/jpn.13054...
). Several healthy plants have been used for feeding fattening rabbits, as they are a source of phytochemicals used as antioxidants or antimicrobials (Zeng et al., 2015Zeng, Z.; Zhang, S.; Wang, H. and Piao, X. 2015. Essential oil and aromatic plants as feed additives in non-ruminant nutrition: a review. Journal of Animal Science and Biotechnology 6:7. https://doi.org/10.1186/s40104-015-0004-5
https://doi.org/10.1186/s40104-015-0004-...
; Dalle Zotte et al., 2016Dalle Zotte, A.; Celia, C. and Szendro, Zs. 2016. Herbs and spices inclusion as feedstuff or additive in growing rabbit diets and as additive in rabbit meat: a review. Livestock Science 189:82-90. https://doi.org/10.1016/j.livsci.2016.04.024
https://doi.org/10.1016/j.livsci.2016.04...
). Bilberry pomace was used as a feeding strategy to improve fatty acid content in rabbit meat (Dabbou et al., 2017Dabbou, S.; Renna, M.; Lussiana, C.; Gai, F.; Rotolo, L.; Kovitvadhi, A.; Brugiapaglia, A.; Helal, A. N.; Schiavone, A.; Zoccarato, I. and Gasco, L. 2017. Bilberry pomace in growing rabbit diets: effects on quality traits of hind leg meat. Italian Journal of Animal Science 16:371-379. https://doi.org/10.1080/1828051X.2017.1292413
https://doi.org/10.1080/1828051X.2017.12...
). Cardinali et al. (2015)Cardinali, R.; Cullere, M.; Dal Bosco, A.; Mugnai, C.; Ruggeri, S.; Mattioli, S.; Castellini, C.; Trabalza Marinucci, M. and Dalle Zotte, A. 2015. Oregano, rosemary and vitamin E dietary supplementation in growing rabbits: Effect on growth performance, carcass traits, bone development and meat chemical composition. Livestock Science 175:83-89. https://doi.org/10.1016/j.livsci.2015.02.010
https://doi.org/10.1016/j.livsci.2015.02...
used oregano, rosemary, and vitamin E as feed supplements for enhancing growth performance and carcass traits in fattening rabbits. Kone et al. (2016)Kone, A. P.; Cinq-Mars, D.; Desjardins, Y.; Guay, F.; Gosselin, A. and Saucier, L. 2016. Effects of plant extracts and essential oils as feed supplements on quality and microbial traits of rabbit meat. World Rabbit Science 24:107-119. https://doi.org/10.4995/wrs.2016.3665
https://doi.org/10.4995/wrs.2016.3665...
used onion, cranberry, strawberry, and their extracts as feed supplements to increase productive performance and meat quality.

An invasive plant is considered as an exotic species in an ecosystem (Richardson and Pysek, 2006Richardson, D. M. and Pysek, P. 2006. Plant invasions: merging the concepts of species invasiveness and community invasibility. Progress in Physical Geography: Earth and Environment 30:409-431. https://doi.org/10.1191/0309133306pp490pr
https://doi.org/10.1191/0309133306pp490p...
). However, when a native species changes environment and is permitted to colonize new areas and become dominant, it can be considered as an invasive species (Valéry et al., 2008Valéry, L.; Fritz, H.; Lefeuvre, J. C. and Simberloff, D. 2008. In search of a real definition of the biological invasion phenomenon itself. Biological Invasions 10:1345-1351. https://doi.org/10.1007/s10530-007-9209-7
https://doi.org/10.1007/s10530-007-9209-...
). The genus Tithonia is widely distributed in Mexico and Central America and has eleven recognized species divided in two groups: annual and perennial plants. Tithonia tubaeformis is an annual herbaceous plant with stems from 1 to 3 m, round, with colors ranging from yellow to brown, alternate leaves ranging in size from 2 to 11 cm, and stalks from 10 to 45 cm. The flowering season is from August to November (Duke, 1982Duke, J. C. 1982. Revision of Tithonia. Rhodora 84:453-522.). This plant is an annual weed, which grow mainly in maize cultures, and is considered problematic as it grows after rainy seasons (Ochoa Martinez et al., 1999Ochoa Martinez, D. L.; Zavaleta-Mejía, E.; Mora-Aguilera, G. and Johansen, R. M. 1999. Implications of weed composition and thrips species for the epidemiology of tomato spotted wilt in chrysanthemum (Dendranthema grandiflora). Plant Pathology 48:707-717. https://doi.org/10.1046/j.1365-3059.1999.00397.x
https://doi.org/10.1046/j.1365-3059.1999...
), providing competition for soil nutrients (Sánchez-Blanco and Guevara-Féfer, 2013Sánchez-Blanco, J. and Guevara-Féfer, F. 2013. Plantas arvenses asociadas a cultivos de maíz de temporal en suelos salinos de la ribera del lago de Cuitzeo, Michoacán, México. Acta Botánica Mexicana 105:107-129.).

There is no evidence that Tithonia tubaeformis has been used for feeding rabbits, but García et al. (2016)García, S.; Santos, R. E.; Posadas, C.; Morón, F. J. and Rosales, C. A. 2016. Composición de la dieta de cabras en pastoreo en un matorral xerófilo. In: Perspectivas y avances de la producción animal en México. Lee Rangel, H. A.; Ramírez Tobías, H. M.; Roque Jimenez, J. A., eds. Universitaria Potosina, SLP, México. found this plant in the diet composition of grazing goats in a xerophilous scrub. The leaves of Tithonia tubaeformis are used in traditional medicine to alleviate skin problems (Gheno-Heredia et al., 2011Gheno-Heredia, Y. A.; Nava-Bernal, G.; Martínez-Campos, A. R. and Sánchez-Vera, E. 2011. Las plantas medicinales de la organización de parteras y médicos indígenas tradicionales de Ixhuatlancillo, Veracruz, México y su significancia cultural. Polibotánica 31:199-251.), while Bello-Gonzalez et al. (2015)Bello-González, M. A.; Hernández-Muñoz, S.; Lara-Chávez, M. B. N. and Salgado-Garciglia, R. 2015. Plantas útiles de la comunidad indígena nuevo San Juan Parangaricutiro, Michoacán, México. Polibotánica 39:175-215. found that the cooked flowers of this plant can be used to improve digestive problems in humans. Molina-Mendoza et al. (2012)Molina-Mendoza, J. L.; Galván-Villanueva, R.; Patiño-Siciliano, A. and Fernández-Nava, R. 2012. Plantas medicinales y listado florístico preliminar del Municipio de Huasca de Ocampo, Hidalgo, México. Polibotánica 34:259-291. identified Tithonia tubaeformis as a medicinal plant and part of floristic composition in Huasca, Hidalgo, Mexico. Nevertheless, Hinojosa Dávalos et al. (2013)Hinojosa Dávalos, J.; Gutiérrez Lomelí, M.; Siller López, F.; Rodríguez Sahagún, A.; Morales Del Río, J. A.; Guerrero Medina, P. J. and Del Toro Sánchez, C. L. 2013. Screening fitoquímico y capacidad antiinflamatoria de hojas de Tithonia tubaeformis. Biotecnia 15:53-60. studied properties of this plant using methanol:water extracts and found mainly pirogalic and cathecol as phytochemical compounds and an anti-inflammatory response. The use of this plant in feed for fattening rabbits leads to an increase in productive performance, carcass traits, and meat quality and is influenced by the secondary metabolites that are stored in different concentrations in the plant.

The objective of this study was to use different parts of the Tithonia tubaeformis plant for feeding fattening rabbits to observe effects on carcass and meat quality.

Material and Methods

Animals used in this trial were housed in an experimental rabbit station in Tulancingo, Hidalgo, Mexico (Latitude 20°06′ and Longitude 98°38′). The institutional committee on animal use (case no. 002/18) approved the care and management of rabbits.

Forty-eight weaned rabbits (35 d) were randomly assigned to four treatments (two replicates of six animals each). Rabbits (n = 6 per cage) were housed in cages (90×60 cm) adapted with manual feeders and automatic drinkers. The average temperature inside the house was 20 °C. The breeds used were crosses of New Zealand, California, and English Pot (NZ×C×EP) with an average weight of 1165.52±124.06 g. Feed was pelletized using a pellet machine model SKJ120 (Shandong, China). Isoproteic (16% of crude protein) and isoenergetic (2.3 Mcal.kg−1 of digestible energy) experimental diets were formulated according to the methods used by De Blas and Mateos (2010)De Blas, C. and Mateos, G. G. 2010. Feed formulation. p.222-232. In: Nutrition of the rabbit. 2nd ed. de Blas, C. and Wiseman, J., eds. Cab International, Wallingford, UK. and were offered to the animals. Nutrient requirements were obtained from NRC (1977)NRC - National Research Council. 1977. Nutrient requirements of rabbits. 2nd rev. ed. National Academic Press, Washington, DC, USA. tables. This study was performed with four treatments: control and Tithonia tubaeformis leaves, stems, and whole plant (Table 1).

Table 1
Ingredient composition of the experimental diets

The weed was obtained in the Mezquital Valley in Hidalgo State in the center of Mexico, from a maize cultivation field. After transportation to the lab, the plant was separated into leaves, stems, and whole plant and dried at room temperature for five days in the shadow. All parts were ground using a miller (Mexicana de Suministros Agropecuarios SA de CV, Tulancingo, Hidalgo, México) and a 5-mm diameter sieve. Once ground, the weed was stored in a dark plastic container until use, and a proximal analysis was determined (crude protein – 8.3, 19.6, 4.3; ash – 5.93, 14.17, 4.05; ether extract – 8.3, 19.6, 4.3; crude fiber – 33.1, 8.1, 46.7; neutral detergent fiber – 60.43, 20.5, 61.52; and acid detergent fiber – 24.84, 8.82, 42.94) for whole Tithonia tubaeformis plant, leaves, and stems, respectively).

Rabbits were slaughtered at 63 d of age in the facilities of the meat laboratory in Tulancingo, Hidalgo, Mexico, without being previously subjected to fasting. The animals were stunned and processed according to national legislation (NOM-033-SAG/ZOO-2014). Once rabbits were slaughtered, they were dissected to obtain hot carcasses, liver, kidney, digestive system, bladder, and skin. The empty body weight was calculated minus the gastrointestinal and bladder content to determine the live weight of rabbits. Carcasses were then stored in refrigeration at 4 °C for 24 h. The dorsal and carcass length of the animals were determined by measuring from the atlas to the last ischia vertebra. The pelvis and lumbar circumference of the animal and carcass were measured using a measuring tape.

The carcasses were sectioned after 24 h of refrigerated storage as indicated by Blasco et al. (1993)Blasco, A.; Ouhayoun, J. and Masoero, G. 1993. Harmonization of criteria and terminology in rabbit meat research. World Rabbit Science 1:3-10. https://doi.org/10.4995/wrs.1993.189
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. The head was cut at the atlas level, the forequarter was obtained by cutting between sixth and seventh ribs, the thoracic cage was determined by cutting the last rib, and the loin was attained in sixth and seventh lumbar vertebrae by cutting the abdominal wall transversally to the vertebral column to eventually obtain the foreleg. All these parts were weighed separately.

Meat color was measured on the loin surface at room temperature (22 °C) using a portable colorimeter i-Lab S560 (Microptix, Wilton, Maine, USA). The values were recorded in terms of CIELab color space using an Illuminant D65 2° standard observer as indicated in American Meat Science Association meat color measurement guidelines (AMSA, 2012AMSA - American Meat Science Association. 2012. Meat color measurement guidelines. Champaign, IL, USA.) using lightness (L*), redness (a*), and yellowness (b*) values. pH was determined using a pH meter for meat Hanna model HI99163 (Hanna instruments, Cluj-Napoca, Romania). Water holding capacity was measured according to the method described by Honikel (1987)Honikel, K. O. 1987. How to measure the water-holding capacity of meat? Recommendation of standardized methods. In: Evaluation and control of meat quality in pigs. Current Topics in Veterinary Medicine and Animal Science, vol. 38. Tarrant P. V.; Eikelenboom, G. and Monin, G., eds. Springer, Dordrecht, Germany.. Cooking losses were measured in loins, and samples were put into a plastic bag and cooked at 80 °C until reaching an internal temperature of 68 °C. Cooked samples were cooled at room temperature and then weighed, while cooking loss values were calculated by differences in weight before and after cooking and expressed as a percentage. Once samples were cooled, a texture profile analysis was carried out following the method described by Bourne (1978)Bourne, M. C. 1978. Texture profile analysis. Food Technology 35:62-66.. Six cubes (1 cm each side) for each loin were used, and samples were cut parallel to muscle fibers. The texture analyzer Brookfield model CT3 (Brookfield, Middleboro, MA, USA) was set to compression at 50% of the sample and perpendicular to the muscle fiber direction using 1 mm.s−1 of crosshead speed. A TA3/1000 probe and a TA-BT-KIT base were used. The samples were compressed twice, and force-time curves of deformation were obtained through Texture Pro CT software, which produced hardness, resilience, cohesiveness, and springiness values.

Pearson's correlation coefficients were calculated using the PROC CORR procedure from the SAS software (Statistical Analysis System, version 9.0) to determine the relationship between morphometric measurements and carcass quality. Carcass traits and meat quality variables were analyzed by least squares following the General Lineal Model procedure using SAS software. The statistical model used was:

y ij = μ + β i + ε ij ,

in which Yij = dependent variable, μ = mean of the variable, βi = fixed effect of i-th rabbit of the group, and εij = experimental error associated with the observation Yij. When statistical differences were found (P<0.05) a Tukey comparison test was used.

Results

Animal morphometric measures are correlated to carcass characteristics (Table 2), and all variables were significant, except hip circumference of the carcass (HCC). Live weight (0.917), skin (0.79), foot (0.58), and lumbar circumference of the carcass (0.707) had higher positive correlations with hot carcass. These results suggest that these indicators were the best predictors of hot carcass weight. It is possible that live weight associated with lumbar circumference carcass should be used to obtain carcass weight. It could, therefore, be used to classify rabbit carcass into several classes according to meat quality.

Table 2
Correlation coefficients between live animal and carcass morphometric measurements in fattening rabbits fed Tithonia tubaeformis

The carcass quality of fattening rabbits fed Tithonia tubaeformis (Table 3) had no significant differences (P>0.05) among treatments, except for kidneys and kidney fat. Rabbits fed the whole plant showed an increase in kidney weight, but lower levels of fat. These effects were significant, since using leaves or the stem of this plant should result in a leaner carcass.

Table 3
Carcass quality of rabbits fed different parts of Tithonia tubaeformis plant

Meat quality parameters detected in rabbits fed Tithonia tubaeformis (Table 4), in particular pH and color values, were different (P<0.05) among treatments, while the pH value was lower in the stem treatment.

Table 4
Meat quality of fattening rabbits fed different parts of Tithonia tubaeformis plant

Hardness was lower in meat of rabbits fed the whole Tithonia tubaeformis plant. Resilience was higher (P<0.01) in samples of cooked meat from rabbits fed leaves and whole plant. Moreover, cohesiveness and springiness were higher (P<0.01) in meat from animals fed Tithonia tubaeformis leaves. These results are important as the whole plant produces a tender meat and is more resilient than other treatments. It is possible that Tithonia tubaeformis has molecules that soften rabbit meat, although other studies would be necessary to determine this. The hardness value indicates that the meat of animals fed the whole Tithonia tubaeformis plant or leaves showed less resistance to cutting than other treatments, including the control group.

Discussion

A correlation coefficient should be used to deduce carcass quality, mainly live weight, skin, foot, and lumbar circumference. These measurements produced higher positive correlation coefficients in this study. It is possible to use the variables live weight (0.91), skin (0.79), and foot (0.68) to predict hot carcass weight because they have the highest correlation coefficients, although it would be important to perform another statistical analysis to confirm this assumption. However, Yalçin et al. (2006)Yalçin, S.; Onbajilar, E. E. and Onbaşilar, İ. 2006. Effect of sex on carcass and meat characteristics of New Zealand White rabbits aged 11 weeks. Asian-Australasian Journal of Animal Science 19:1212-1216. https://doi.org/10.5713/ajas.2006.1212
https://doi.org/10.5713/ajas.2006.1212...
reported a negative correlation between lumbar circumference and carcass length. Nevertheless, Mousa-Balabel et al. (2017)Mousa-Balabel, T. M.; El-Sheikh, R. A. and El-Nenny, N. S. 2017. Prediction of Californian rabbits body weight from their body characteristics in Egypt. Life Science Journal 14:52-56. found moderate positive correlations between body weight and tail length, head length and tail length, and chest girth and ear length in New Zealand rabbits. Moreover, Akinsola et al. (2014)Akinsola, O. M.; Nwagu, B. I.; Orunmuyi, M.; Iyeghe-Erakpotobor, G. T; Eze E. D.; Abanikannda, O. T. F.; Onaadepo, O. E. U.; Okud, E. U. and Louis, U. 2014. Prediction of bodyweight from body measurements in rabbits using principal component analysis. Annals of Biological Sciences 2:1-6. described a high positive correlation between body weight and linear body measurements, particularly body weight and chest girth (0.939). Rabbit linear measurement should be used for predicting carcass quality and for choosing animals for meat production in selected markets. Singh et al. (2015)Singh, N.; Gulati, H. K.; Sihag, S.; Dalal, D. S.; Kapoor, P. K. and Malik, A. K. 2015. Effect of spirulina (Arthrospira platensis) and thyme (Thymus vulgaris) supplementation on growth performance of rabbits. Haryana Veterinarian 54:117-120. used spirulina (5%) and thyme (3%) as feed supplements for fattening rabbits, but they did not improve body measurements, except for abdominal girth gain during a period of eight weeks. Anhita et al. (2016aAnhita, K. C.; Rajeshwari, Y. B.; Prabhu, T. M.; Vivek Patil, M.; Shilpa Shree, J. and Anupkumar, P. K. 2016a. Effect of supplementary feeding of azolla on growth performance of broiler rabbits. ARPN Journal of Agricultural and Biological Science 11:30-36.) concluded that using azolla as feed supplement at 1.5 and 3% in diets did not affect growth performance in broiler rabbits after feeding for 12 weeks.

Supplementation of diets with natural additives from the plants containing bioactive molecules have shown promising results in improving carcass traits and meat quality (Alagawany et al., 2019Alagawany, M.; Elnesr, S. S. and Farag, M. R. 2019. Use of liquorice (Glycyrrhiza glabra) in poultry nutrition: Global impacts on performance, carcass and meat quality. World's Poultry Science Journal 75:293-304. https://doi.org/10.1017/S0043933919000059
https://doi.org/10.1017/S004393391900005...
). Carcass characteristics are used to determine carcass yield. As previously mentioned, the results indicate that there were no differences among treatments in carcass quality. Dressing percentage was approximately 60% in all treatments. Kidney weight was higher in the group consuming whole plants, but the other groups were similar to the control treatment, which may be due to a part of the plant having a chemical compound that affects this organ. Adebayo et al. (2009)Adebayo, J. O.; Balogun, E. A. and Oyeleke, S. A. 2009. Toxicity study of the aqueous extract of Tithonia diversifolia leaves using selected biochemical parameters in rats. Pharmacognosy Research 1:143-147. reported a high tolerance to Thitonia diversifolia aqueous extract for seven days in rats; however, Fakunle and Abatan (2007)Fakunle, J. O. and Abatan, M. O. 2007. The toxicological effects of aqueous leaf extract of Tithonia diversifolia gray in rats. Journal of Animal and Veterinary Advances 6:1223-1226. found significant changes in hematological, biochemical, and histopathological parameters in rats after 14 d of experiment. It is likely that adverse changes in organs depend on time of feeding with this plant, but some histological studies should be conducted to verify these findings. Nonetheless, Tithonia tubaeformis leaves or stems could be used in rabbit feeding. Meanwhile, Anhita et al. (2016bAnhita, K. C.; Rajeshwari, Y. B.; Prabhu, T. M.; Devarnvadagi, A. S.; Rohith, K. J. and Shilpa Shree, J. 2016b. Carcass and meat quality traits of broiler rabbits when supplement with azolla. Journal of Experimental Zoology 19:417-420.) reported that the inclusion of fresh azolla in broiler rabbit feed for 12 weeks did not affect carcass traits, organs, or chemical composition of meat. Some studies have demonstrated that the use of Silybum marianum (Cullere et al., 2016Cullere, M.; Dalle Zotte, A.; Celia, C.; Renteria-Monterrubio, A. L.; Gerencsér, Zs.; Szendro, Zs.; Kovács, M.; Kachlek, M. L. and Matics, Zs. 2016. Effect of Silybum marianum herb on the productive performance, carcass traits and meat quality of growing rabbits. Livestock Science 194:31-36. https://doi.org/10.1016/j.livsci.2016.10.012
https://doi.org/10.1016/j.livsci.2016.10...
), Amaranthus dubius (Molina et al., 2018Molina, E.; González-Redondo, P.; Moreno-Rojas, R.; Montero-Quintero, K. and Sánchez-Urdaneta, A. 2018. Effect of the inclusion of Amaranthus dubius in diets on carcass characteristics and meat quality of fattening rabbits. Journal of Applied Animal Research 46:218-223. https://doi.org/10.1080/09712119.2017.1287078
https://doi.org/10.1080/09712119.2017.12...
), and Lythrum salicaria (Kovitvadhi et al., 2016Kovitvadhi, A.; Gasco, L.; Ferrocino, I.; Rotolo, L.; Dabbou, S.; Malfatto, V.; Gai, F.; Peiretti, P. G.; Falzone, M.; Vignolini, C.; Cocolin, L. and Zoccarato, I. 2016. Effect of purple loosestrife (Lythrum salicaria) diet supplementation in rabbit nutrition on performance, digestibility, health and meat quality. Animal 10:10-18. https://doi.org/10.1017/S1751731115001822
https://doi.org/10.1017/S175173111500182...
) in feed does not affect rabbit carcass quality. The use of all these plants had no recorded negative impact on carcass quality, but in all cases, the authors suggested using them as dietary supplements for growing rabbits. It is possible that these suggestions were influenced by cost, as they help to produce a low-cost rabbit feed.

The intake of Tithonia tubaeformis suggests an increase in kidney fat weight in the group consuming leaves, but a decrease in the group fed the whole plants as feed. The leaves of this plant could be utilized for feeding rabbits because all carcass characteristics are similar to the control group, and some of them are slightly higher, e.g., dressing percentage, chilled carcass, and weights of fore and intermediate parts of the carcass. These findings are similar to those reported by Fathi et al. (2019)Fathi, M.; Abdelsalam, M.; Al-Homidan, I.; Ebeid, T.; Shehab-El-Deen, M.; Abd El-Razik, M.; Abou-Emera, O. and Mostafa M. 2019. Supplemental effects of eucalyptus (Eucalyptus camaldulensis) leaves on growth performance, carcass characteristics, blood biochemistry and immune response of growing rabbits. Annals of Animal Science 19:779-791. https://doi.org/10.2478/aoas-2019-0023
https://doi.org/10.2478/aoas-2019-0023...
, who found that eucalyptus leaves did not affect dressing and fore or hind parts of the rabbit carcass. Similar results were found in slaughter traits of rabbits fed diet supplemented with ginger powder (Mancini et al., 2018Mancini, S.; Secci, G.; Preziuso, G.; Parisi, G. and Paci, G. 2018. Ginger (Zingiber officinale Roscoe) powder as dietary supplementation in rabbit: life performances, carcass characteristics and meat quality. Italian Journal of Animal Science 17:867-872. https://doi.org/10.1080/1828051X.2018.1427007
https://doi.org/10.1080/1828051X.2018.14...
), quebracho and chestnut (Mancini et al., 2019Mancini, S.; Moruzzo, R.; Minieri, S.; Turchi, B.; Cerri, D.; Gatta, D.; Sagona, S.; Felicioli, A. and Paci, G. 2019. Dietary supplementation of quebracho and chestnut tannins mix in rabbit: effects on live performances, digestibility, carcass traits, antioxidant status, faecal microbial load and economic value. Italian Journal of Animal Science 18:621-629. https://doi.org/10.1080/1828051X.2018.1549514
https://doi.org/10.1080/1828051X.2018.15...
), or garlic and turmeric powder (Alagawany et al., 2016Alagawany, M.; Ashour, E. A. and Reda, F. M. 2016. Effect of dietary supplementation of garlic (Allium sativum) and turmeric (Curcuma longa) on growth performance, carcass traits, blood profile and oxidative status in growing rabbits. Annals of Animal Science 16:489-505.) as growth promoters.

Some weeds can be used to feed animals, and Tithonia tubaerformis could be one of them. This weed is usually a competition for cultivated plants such as maize and should be used for rabbit feeding, but its influence on meat quality is limited because almost all traits were similar. Meat weight was slightly higher in the group fed Tithonia tubaeformis leaves (765 g.kg−1 of leg), and dissectible fat was lower in this group (6.43 g.kg−1 of leg) compared with the control. Larzul and Gondret (2005)Larzul, C. and Gondret, F. 2005. Aspects génétiques de la croissance et de la qualité de la viande chez le lapin. INRA Productions Animales 18:119-129. stated that meat:bone ratio is a good predictor of meat content in carcass, while Molina et al. (2018)Molina, E.; González-Redondo, P.; Moreno-Rojas, R.; Montero-Quintero, K. and Sánchez-Urdaneta, A. 2018. Effect of the inclusion of Amaranthus dubius in diets on carcass characteristics and meat quality of fattening rabbits. Journal of Applied Animal Research 46:218-223. https://doi.org/10.1080/09712119.2017.1287078
https://doi.org/10.1080/09712119.2017.12...
reported a good meat yield independently of amaranth inclusion levels in the diet. However, North et al. (2018)North, M. K.; Dalle Zotte, A. and Hoffman, L. C. 2018. The effects of quercetin supplementation on New Zealand white grower rabbit carcass and meat quality - A short communication. Meat Science 145:363-366. https://doi.org/10.1016/j.meatsci.2018.07.014
https://doi.org/10.1016/j.meatsci.2018.0...
demonstrated that quercetin inclusion increases meat:bone ratio, maybe because quercetin decreases bone weight by altering bone structure.

There are many factors that modify the pH of rabbit meat, such as breed, carcass cooling rate, preslaughter handling, feeding conditions, and muscle localization (Hulot and Ouhayoun, 1999Hulot, F. and Ouhayoun, J. 1999. Muscular pH and related traits in rabbits: a review. World Rabbit Science 7:15-36. https://doi.org/10.4995/wrs.1999.378
https://doi.org/10.4995/wrs.1999.378...
). In this study, as previously indicated, groups fed diets supplemented with Tithonia tubaeformis leaves and stems have higher pH values than the control or whole-plant group. These results may be influenced by antioxidant compounds found in the different parts of the plant. Hinojosa Dávalos et al. (2013)Hinojosa Dávalos, J.; Gutiérrez Lomelí, M.; Siller López, F.; Rodríguez Sahagún, A.; Morales Del Río, J. A.; Guerrero Medina, P. J. and Del Toro Sánchez, C. L. 2013. Screening fitoquímico y capacidad antiinflamatoria de hojas de Tithonia tubaeformis. Biotecnia 15:53-60. reported that Tithonia tubaeformis contains antioxidant compounds such as phenols and flavonoids. Some studies reported that pH was not affected by diets supplemented with ginger powder (Mancini et al., 2018Mancini, S.; Secci, G.; Preziuso, G.; Parisi, G. and Paci, G. 2018. Ginger (Zingiber officinale Roscoe) powder as dietary supplementation in rabbit: life performances, carcass characteristics and meat quality. Italian Journal of Animal Science 17:867-872. https://doi.org/10.1080/1828051X.2018.1427007
https://doi.org/10.1080/1828051X.2018.14...
), quercetin (North et al., 2018North, M. K.; Dalle Zotte, A. and Hoffman, L. C. 2018. The effects of quercetin supplementation on New Zealand white grower rabbit carcass and meat quality - A short communication. Meat Science 145:363-366. https://doi.org/10.1016/j.meatsci.2018.07.014
https://doi.org/10.1016/j.meatsci.2018.0...
), Amarantus dubius (Molina et al., 2018Molina, E.; González-Redondo, P.; Moreno-Rojas, R.; Montero-Quintero, K. and Sánchez-Urdaneta, A. 2018. Effect of the inclusion of Amaranthus dubius in diets on carcass characteristics and meat quality of fattening rabbits. Journal of Applied Animal Research 46:218-223. https://doi.org/10.1080/09712119.2017.1287078
https://doi.org/10.1080/09712119.2017.12...
), and quebracho and chestnut tannin mix (Mancini et al., 2019Mancini, S.; Moruzzo, R.; Minieri, S.; Turchi, B.; Cerri, D.; Gatta, D.; Sagona, S.; Felicioli, A. and Paci, G. 2019. Dietary supplementation of quebracho and chestnut tannins mix in rabbit: effects on live performances, digestibility, carcass traits, antioxidant status, faecal microbial load and economic value. Italian Journal of Animal Science 18:621-629. https://doi.org/10.1080/1828051X.2018.1549514
https://doi.org/10.1080/1828051X.2018.15...
). However, Cullere et al. (2016)Cullere, M.; Dalle Zotte, A.; Celia, C.; Renteria-Monterrubio, A. L.; Gerencsér, Zs.; Szendro, Zs.; Kovács, M.; Kachlek, M. L. and Matics, Zs. 2016. Effect of Silybum marianum herb on the productive performance, carcass traits and meat quality of growing rabbits. Livestock Science 194:31-36. https://doi.org/10.1016/j.livsci.2016.10.012
https://doi.org/10.1016/j.livsci.2016.10...
added Silybum marianum to rabbit feed and found an increase in pH values, which is supposedly linked to glycolytic metabolism in the muscle intermediated by silibinin presence in Silybum marianum.

Meat color is affected by animal diet, which in turn modifies the metabolism, glycogen storage, pH, and antioxidant accumulation (Mancini, 2013Mancini, R. 2013. Meat color. p.177-198. In: The science of meat quality. Kerth, C. R., ed. Wiley-Blackwell, Ames, IO, USA. https://doi.org/10.1002/9781118530726.ch9
https://doi.org/10.1002/9781118530726.ch...
). As previously mentioned, pH was influenced by Tithonia tubaeformis. Lightness (L*), redness (a*), and yellowness (b*) values were modified when this plant was supplemented to rabbits. The presence of antioxidant compounds such as phenols and flavonoids in this plant could be responsible for differences in color in this study. Papuc et al. (2017)Papuc, C.; Goran, G. V.; Predescu, C. N.; Nicorescu, V. and Stefan, G. 2017. Plant polyphenols as antioxidant and antibacterial agents for shelf-life extension of meat and meat products: Classification, structures, sources, and action mechanisms. Comprehensive Reviews in Food Science and Food Safety 16:1243-1268. https://doi.org/10.1111/1541-4337.12298
https://doi.org/10.1111/1541-4337.12298...
mentioned that polyphenols present in plant extracts or byproducts preserve meat color better than synthetic antioxidants used in meat and meat products. Simonová et al. (2010)Simonová, M. P.; Chrastinová, L.; Mojto, J.; Lauková, A.; Szabóová, R. and Rafay, J. 2010. Quality of rabbit meat and phytoadditives. Czech Journal of Food Sciences 28:161-167. found no significant differences in color parameters (L* and b*). Volek et al. (2018)Volek, Z.; Bureš, D. and Uhlířová, L. 2018. Effect of dietary dehulled white lupine seed supplementation on the growth, carcass traits and chemical, physical and sensory meat quality parameters of growing-fattening rabbits. Meat Science 141:50-56. https://doi.org/10.1016/j.meatsci.2018.03.013
https://doi.org/10.1016/j.meatsci.2018.0...
reported non-significant differences in pH and meat color of rabbits fed white lupin seed. Mancini et al. (2018)Mancini, S.; Secci, G.; Preziuso, G.; Parisi, G. and Paci, G. 2018. Ginger (Zingiber officinale Roscoe) powder as dietary supplementation in rabbit: life performances, carcass characteristics and meat quality. Italian Journal of Animal Science 17:867-872. https://doi.org/10.1080/1828051X.2018.1427007
https://doi.org/10.1080/1828051X.2018.14...
observed an increase in L* and b* when ginger powder was supplemented to rabbits. However, North et al. (2018)North, M. K.; Dalle Zotte, A. and Hoffman, L. C. 2018. The effects of quercetin supplementation on New Zealand white grower rabbit carcass and meat quality - A short communication. Meat Science 145:363-366. https://doi.org/10.1016/j.meatsci.2018.07.014
https://doi.org/10.1016/j.meatsci.2018.0...
fed rabbits quercetin and did not find any differences among the groups regarding color parameters. Similar results were found by Koné et al. (2019)Koné, A. P.; Desjardins, Y.; Gosselin, A.; Cinq-Mars, D.; Guay, F. and Saucier, L. 2019. Plant extracts sand essential oil product as feed additives to control rabbit meat microbial quality. Meat Science 150:111-121. https://doi.org/10.1016/j.meatsci.2018.12.013
https://doi.org/10.1016/j.meatsci.2018.1...
, using an oil extract from a mix of different plants. Other studies did not find differences in color when feeding diets containing barley, wheat, or corn dried distillers grains (Alagón et al., 2015Alagón, G.; Arce, O.; Serrano, P.; Rodenas, L.; Martínez-Paredes, E.; Cervera, C.; Pascual, J. J. and Pascual, M. 2015. Effect of feeding diets containing barley, wheat and corn distillers dried grains with solubles on carcass traits and meat quality in growing rabbits. Meat Science 101:56-62. https://doi.org/10.1016/j.meatsci.2014.10.029
https://doi.org/10.1016/j.meatsci.2014.1...
) or billberry pomace (Dabbou et al., 2017Dabbou, S.; Renna, M.; Lussiana, C.; Gai, F.; Rotolo, L.; Kovitvadhi, A.; Brugiapaglia, A.; Helal, A. N.; Schiavone, A.; Zoccarato, I. and Gasco, L. 2017. Bilberry pomace in growing rabbit diets: effects on quality traits of hind leg meat. Italian Journal of Animal Science 16:371-379. https://doi.org/10.1080/1828051X.2017.1292413
https://doi.org/10.1080/1828051X.2017.12...
).

The meat texture profile analysis demonstrated that supplementation with Tithonia tubaeformis has a significant effect compared with control diet. The treatment of whole plants produced a softer rabbit meat compared with the other groups. These results suggest that this plant contains a compound that affects meat hardness. Hernández-Martínez et al. (2018)Hernández-Martínez, C. A.; Treviño-Cabrera, G. F.; Hernández-Luna, C. E.; Silva-Vázquez R.; Hume, M. E.; Gutiérrez-Soto, G. and Méndez-Zamora, G. 2018. The effects of hydrolysed sorghum on growth performance and meat quality of rabbits. World Rabbit Science 26:155-163. https://doi.org/10.4995/wrs.2018.7822
https://doi.org/10.4995/wrs.2018.7822...
found that hardness and gumminess of rabbit meat decrease when sorghum is replaced by hydrolyzed sorghum, suggesting that it is due to an increase in nutrient synthesis and assimilation.

Hernández-Martínez et al. (2018)Hernández-Martínez, C. A.; Treviño-Cabrera, G. F.; Hernández-Luna, C. E.; Silva-Vázquez R.; Hume, M. E.; Gutiérrez-Soto, G. and Méndez-Zamora, G. 2018. The effects of hydrolysed sorghum on growth performance and meat quality of rabbits. World Rabbit Science 26:155-163. https://doi.org/10.4995/wrs.2018.7822
https://doi.org/10.4995/wrs.2018.7822...
found that hardness and gumminess of rabbit meat decrease when sorghum is replaced by hydrolyzed sorghum, suggesting it is due to an increase in the nutrient synthesis and assimilation. However, Alagón et al. (2015)Alagón, G.; Arce, O.; Serrano, P.; Rodenas, L.; Martínez-Paredes, E.; Cervera, C.; Pascual, J. J. and Pascual, M. 2015. Effect of feeding diets containing barley, wheat and corn distillers dried grains with solubles on carcass traits and meat quality in growing rabbits. Meat Science 101:56-62. https://doi.org/10.1016/j.meatsci.2014.10.029
https://doi.org/10.1016/j.meatsci.2014.1...
used diets containing barley, wheat, or corn dried distillers grains for growing rabbits, and no differences among treatments were found for meat texture analyzed with Warner-Bratzler blade.

Conclusions

Tithonia tubaeformis is a weed plant that is scarcely used for feeding animals, and could be used for fattening rabbits since carcass and meat quality parameters were similar among control and treatments. The use of whole plant or leaves produces tender meat than the control diet. All of these values indicate that Tithonia tubaeformis leaves or whole plant could be added to growing rabbit feed. Feed costs could be reduced, since it is a commonly found weed.

Acknowledgments

The authors would like to thank the PRODEP program for providing financial support to this work. Project number DSA/103.5/16/10281. SEP-PFCE 2018.

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    » https://doi.org/10.1186/s40104-015-0004-5

Publication Dates

  • Publication in this collection
    28 Nov 2019
  • Date of issue
    2019

History

  • Received
    27 May 2019
  • Accepted
    06 Oct 2019
Sociedade Brasileira de Zootecnia Universidade Federal de Viçosa / Departamento de Zootecnia, 36570-900 Viçosa MG Brazil, Tel.: +55 31 3612-4602, +55 31 3612-4612 - Viçosa - MG - Brazil
E-mail: rbz@sbz.org.br