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Review

Utilization of the Viscum Species for Diet and Medicinal Purposes in Ruminants: A Review

by
Onke Hawu
1,2,*,
Khuliso Emmanuel Ravhuhali
1,2,
Mutshidzi Given Musekwa
1,2,
Nkosomzi Sipango
1,2,
Humbelani Silas Mudau
1,2,
Kwena Hilda Mokoboki
1,2 and
Bethwell Moyo
3
1
Department of Animal Science, School of Agricultural Sciences, Faculty of Natural and Agricultural Sciences, North-West University, Mmabatho 2735, South Africa
2
Food Security and Safety Niche Area, Faculty of Natural and Agricultural Sciences, North-West University, Mmabatho 2735, South Africa
3
Department of Animal Production, Fort Cox Agriculture and Forestry Training Institute, Middledrift 5685, South Africa
*
Author to whom correspondence should be addressed.
Animals 2022, 12(19), 2569; https://doi.org/10.3390/ani12192569
Submission received: 24 August 2022 / Revised: 21 September 2022 / Accepted: 23 September 2022 / Published: 26 September 2022
(This article belongs to the Section Animal Nutrition)

Abstract

:

Simple Summary

True mistletoe (of the Viscum species) is a semi-parasitic, perennial browse species that is found attached to its host—a shrub or a tree. It has important pharmaceutical and chemical properties that allow it to be used for a variety of purposes, including livestock production. Mistletoes are cheap and are a readily available source of minerals and protein for livestock, especially during the dry season. They grow primarily on the outer branches of the tree crown; however, they also frequently grow directly on the tree trunk in order to consume its nutrients and water, thereby affecting their host’s quality and development. Many countries are expected to discover and explore the potential of Viscum spp. and their management tools, which we investigate through this review.

Abstract

A cost-effective, alternative protein and mineral source such as the Viscum species can be key to livestock production. Viscum spp. are used as feed in many semi-arid and arid regions globally, particularly during feed shortages. The species’ feeding value, and their pharmaceutical attributes, have been recognized worldwide, albeit with variation in nutritive value from one host to another. The antinutritional factors found in Viscum spp. may benefit livestock when consumed in moderation due to their immunomodulatory, proapoptotic, and antimicrobial properties. The Vachellia species are known to be the common hosts for Viscum spp. Further, even though Viscum spp. inhibit host tree development by reducing carbon absorption and the host tree’s carbohydrates, the efforts to regulate their infestation should not result in the plant’s total eradication due to the benefits to livestock (as well as in fodder and medicine). This review will help to improve understanding of Viscum species control measures, while also increasing the productivity of ruminants.

1. Introduction

Finding inexpensive alternative protein sources such as the Viscum species is necessary since livestock productivity has continued to be severely constrained by the cost of livestock feed. True mistletoe (of the genus Viscum) is a semi-parasitic, perennial browse species that attaches to its host, shrubs or various tree species [1,2]. It is mainly dispersed by frugivorous birds from one host to another [1]. It has fodder value, as well as anthelmintic and therapeutic properties with evergreen leaves [2,3]. The genus Viscum contains many species that are primarily found in America, Africa, Asia, and Europe [4]. The Viscum spp. found in southern Africa include V. verrucosum, V. rotundifolium, V. anceps, V. songimveloensis, and V. combreticola [5,6,7]. They are fodder resources for ruminants, especially during dry periods when good quality forage is scarce [8]. Öztürk et al. [3] highlighted that the Viscum species extract nutrients and water from their host; hence, they are a rich fodder resource for ruminants.
True mistletoes are ingested and preferred by livestock without any reported digestive orders [9]. Even though their ecological importance for birds, medicinal properties, and fodder value for livestock are known, they are still regularly removed from orchards and rangelands/forests due to their detrimental effect on the host plant [10]. This research aims to help improve understanding of Viscum species control measures, while also increasing the productivity of ruminants. This means that developing mitigation strategies to minimize its spread should take into account a more balanced understanding that incorporates knowledge of its nutritive value as a source of protein, as well as its negative impact on rangelands. In this paper, we reviewed the primary uses of Viscum spp. in the livestock industry as well as in other human endeavors.

2. Description of the Viscum Species

True mistletoe (Viscum spp.) is an evergreen hemiparasitic plant that inhabits trees. Yellowish flowers, small yellowish green leaves, and waxy, white berries characterize this parasitic plant (Figure 1). Some of the species have leaves while some do not have leaves (Table 1). For example, V. album, when on the branch of a host tree, will grow as much as 60–90 cm long with a drooping yellowish evergreen shrub. It has densely packed forking branches that are 5 cm long, leathery, oval- to lance-shaped leaves that are placed in pairs on branches. The bisexual, or unisexual, blooms are arranged in tight spikes and have consistent symmetry [11]. However, some Viscum spp. have smooth, round, green stems that are covered in sessile, yellowish blooms in tiny clusters (Figure 2). The flowers of the Viscaceae family are narrow, tubular, dioecious, with (or without) a corolla, and thus pollinated by insects and the wind [12].

3. Adaptation of the Species

Viscum spp. grow on the branches of various tree species. They extract nutrients and water from the host plant for their survival [22]. Although their leaves may photosynthesize, they do so at a slower rate than their hosts [23]. Ahmad et al. [24] highlighted that they contain a functionally low amount of chlorophyll, and their low capability for photosynthesis explains their capability to adapt to dry conditions. They can survive in semi-arid regions, deserts, temperate woodlands, and semi-tropic wetlands [25]. It has been suggested that true mistletoes selectively parasitize host species that are high in nitrogen since nitrogen is frequently a limiting resource for plants [26]. Moreover, in South Africa, the genus Vachellia are the most important hosts of Viscum spp. Clark et al. [27] highlighted that there are just four Viscum species in South Africa that are unique or specific to a single host, which is a relatively low number.

4. Negative Impact and Control of the Viscum Species

It has been extensively researched for years how common Viscum spp. affect woody species, particularly in rangelands and in plantations. Mistletoe inhibits host tree development by reducing carbon absorption and host tree carbohydrates, all of which have an impact on the quality and quantity of woody species produced and the soil’s nutrient cycle [28]. Within its current range, mistletoe abundance has been growing, and the intensification of climatic stress in the form of protracted droughts has increased the rate of tree mortality in mistletoe-infected woody species, thus altering the dynamics of the community [29]. Moreover, true mistletoe spp. induce nutrient and water stress, which, in turn, changes the phyto-hormone profile, as well the defense mechanism of the host plant and causes affected trees to be more susceptible to insect attacks [30]. To overcome such problems, mistletoe spp. infestations should be controlled or managed in the rangelands.
Viscum spp. can be controlled using mechanical, chemical, or biological means. The single most successful approach to eradicate mistletoe in rangelands or forests is mechanical removal of mistletoe by clipping infected branches; however, this requires a large amount of labor and finances [28]. The use of chemicals as a control measure has been documented. Further, injecting a chemical into the trunk of a plant with mistletoe has been proposed [31]. However, this method does not address the root of the infestation and entails the possibility that the dosage will either fail to eradicate the mistletoe or harm the host plant. Livestock browse preferably on mistletoes when available; this, therefore, suggests that livestock can be used as biological agents to control the spread of mistletoe spp. However, it is unknown whether livestock have a comparable preference for mistletoes on plant hosts.

5. Crude Protein and Fiber Fraction of Viscum Species

The high prices of livestock’s more conventional feeds make Viscum spp. a nutritionally suitable feed for ruminants during particularly dry periods. Grasses during this period normally deteriorate and lose their nutritive value. The nutritive value of Viscum spp. usually varies from one host to another due to link-specific nutrient transfer characteristics [32]. Previous studies have reported that Viscum spp. have a crude protein (CP) content of more than 80 g/kg DM, which is considered to be enough for rumen microbes in growing ruminants (cattle, sheep, and goats) [2,33]. This further highlights the importance of Viscum spp. during the dry season, as they address protein deficiencies when the CP content of grasses is between 20 and 60 g/kg DM. Hawu et al. [34] highlighted that low CP content usually decreases feed intake, and adversely affects ruminant growth and productivity.
The fiber content of forage is one of the most vital parameters to consider as this will affect both feed intake and digestibility for ruminants. Viscum spp. contain relatively low fiber concentrations, as shown in Table 2; this is due to their low photosynthesis capacity. Viscum spp. may not produce some more complex carbon materials such as fiber, which are, however, produced by other woody browse species [35]. Consequently, Viscum spp. do not have high acid detergent fiber, neutral detergent fiber, or acid detergent lignin content, thus making them highly digestible. Therefore, the low fiber content in Viscum spp. does not constrain the use of Viscum spp. as a fodder for ruminants that are adept at utilizing forages that are high in fiber.

6. Potential of Viscum Species as a Source of Minerals for Ruminants

Minerals play an important role in the metabolic functions of livestock. These functions assist with supporting growth, development, immune function, and the reproductive performance of livestock [39,40]. Viscum spp. are known as a source of minerals such as phosphorous (P), iron (Fe), calcium (Ca), magnesium (Mg), zinc (Zn), copper (Cu), and other minerals that are required for ruminants’ wellbeing (Table 3). Umucalılar et al. [41] reported average Ca (13 g/kg), P (3 g/kg DM), Fe (110 g/kg DM), Cu (10 g/kg DM), and Zn (41 g/kg DM) in V. album from different plant hosts.
Numerous physiological processes depend on calcium. Calcium (Ca) plays an important role in blood clotting, membrane permeability, nerve conduction, muscle contraction, enzyme activity, and hormone secretion [42,43]. The concentration level of Ca in Viscum spp. is higher than the 5.8 g/kg required by growing calves [44]. However, there may be a need to reduce the Ca concentration level in ruminant diets that contain Viscum spp. in order to avoid toxicity. Phosphorus is an essential component of adenosine triphosphate (ATP) and nucleic acid, it is also important for the formation of teeth and bones [45]. The concentration level of P in Viscum spp. is equivalent to the 2 g/kg that is required by lactating cows [44]. Iron is required for the synthesis of hemoglobin and myoglobin, as well as several other enzymes that aid in the formation of ATP via the electron transport chain [46]. Hill and Shannon [47] highlighted that Zn plays a variety of roles in immunity and disease resistance. Moreover, Zn is essential for growth and cell division, where it is required for protein and DNA synthesis, insulin activity, ovary and testis metabolism, and liver function [48,49,50]. Copper performs a physiological role in cellular respiration, bone development, heart health (functions), the formation of connective tissue, the myelination of the spinal cord, and in keratinization and pigmentation processes [51,52]. The concentration level of Cu in V. verrucosum is equivalent to the 0.01–0.02 g/kg required by growing lambs [53]. These mineral values, as mentioned above, suggest that Viscum spp. can be fed to ruminants without mineral supplementation since these values are higher than the minimum mineral requirement [54,55].
Table 3. Mineral content (g/kg DM) of Viscum ssp.
Table 3. Mineral content (g/kg DM) of Viscum ssp.
SpeciesCaKPMgNaZnCuSFeMnReferences
V. album1325332.57 21.114.429.299[41,56,57]
V. verrucosum7697271.20.020.03 0.440.05[2]

7. Antinutritional Factors Associated with Viscum ssp.

Plants use phytochemicals as a defense mechanism against diseases and other external threats [58]. There is increasing interest in studying the bioactivity and the antinutritional factors (ANFs) (phytochemicals) of Viscum spp. To clarify, antinutritional factors are plant components that have the potential to negatively impact livestock productivity. Several authors have reported the presence of ANFs in Viscum spp., as shown in Table 4. García-García et al. [57] reported that Viscum spp. contain ANFs such as tannins, saponins, alkaloids, and flavonoids; further, Viscum spp. depend on the host they grow on. In contrast, it has been discovered that some ANFs might benefit livestock when consumed in moderation. Wang et al. [59] stressed that flavonoids have various bioactive effects, such as cardio protective, anti-inflammatory, and antiviral. Saponin has a number of biological effects on livestock, such as hemolysis of erythrocytes, a decrease in blot (in ruminants), a reduction in the activity of smooth muscles, an inhibition of enzymes, a reduction in nutrient absorption, and an alteration in cell wall permeability, and thus produces some poisonous effects when ingested [60,61]. High tannin concentrations in ruminants are known to reduce palatability, feed intake, and degradability [34], while low tannin concentrations are known to have health benefits such as antiviral and antibacterial effects [62]. In relation to greenhouse gases, tannins are regarded as an important alternative in mitigating carbon dioxide (CO2), as well as methane (CH4) [63]. The same authors found that the addition of tannins into Nellore bulls’ urine had an effect on the reduction in CH4. OS van Cleef et al. [64] also concluded that the inclusion of highly taniniferous plants effectively mitigated the emission of CH4 in beef steers’ excreta.

8. Health Benefits of Viscum Species in Livestock

In many parts of the world, Viscum spp. have been consumed for a long period of time as an herbal tea and as a supplement to health care [8]. Furthermore, Viscum spp. have been used to improve livestock health, or simply as forage, when feedstuffs are limited due to drought [10,67]. Previous studies have highlighted that Viscum spp. have immunomodulatory, proapoptotic, and antimicrobial properties [8,68]. According to Ishiwu et al. [67], in Nigeria, rural farmers give the leaves of Viscum spp. to goats that have newly given birth, even though they do not, in reality, know of their health benefits. Moreover, Ohikhena et al. [61] highlighted that Viscum spp. are used to treat vision weakness and for promoting muscular relaxation prior to delivery. Drury [69] also highlighted the use of decoctions from Viscum spp. berries in cows to promote the expulsion of the afterbirth and to stop bleeding. In Nigeria, Viscum spp. are used to treat bacterial infections, skin conditions, diarrhea, diabetes, and prostate cancer in livestock [70]. It was reported that salmonellae in sheep rumen fluid were inhibited by diets containing V. verrucosum [71]. Further, Madibela and Jansen [72] highlighted that tanniferous species such as Viscum spp. can reduce the fecal egg count in ruminants. Apart from ruminants, Korean mistletoe enhanced lymphocytes and reduced Salmonella spp. of ceca in broiler hens [73]. Furthermore, Viscum spp. are used to treat infertility, epilepsy, rheumatism, and menopausal syndrome in humans [74].

9. The Use of Viscum Species in Ruminant Diets

The Viscum species are used as feed in many semi-arid and arid regions around the world, particularly during the dry season. Viscum spp. are rich sources of proteins and minerals, even though they contain antinutritional factors. Several studies have found that true mistletoes, when combined with other feed sources, can help reduce ruminant forage crop requirements in dryland areas. According to Jibril et al. [33], V. album can substitute sorghum stover by up to 50% in rams’ diets, without negatively affecting the growth performance. Similarly, Abubakar et al. [9] came to the conclusion that Red Sokoto Bucks can consume mistletoe leaf meal for up to 22.5% of their diet without any negative effects on the animals’ ability to produce. In an in vitro study, Ndagurwa and Dube [32] found that V. verrucosum had higher in vitro dry matter degradability, in vitro gas production, and in vitro metabolizable energy than Acacia karroo, thus making Viscum spp. a potential alternative browse for goats in semi-arid regions. Ramatsi et al. [2] also found that the in vitro dry matter degradability of V. verrucosum ranged from 510–517 g/kg at 72 h.
Apart from livestock ruminants, studies also show the positive effects of Viscum spp. in nonruminant livestock. It was reported that V. album improved the growth, meat, and carcasses of rabbits (Oryctolagus cuniculus), and can be added into rabbits’ diet at amounts of up to 15% [70]. Further, Ologhobo et al. [75] concluded that V. album had no effect on the growth performance, biochemical profile, and carcass characteristics of broilers.

10. Conclusions

Viscum spp. have the potential to serve as a substitute source of feed for ruminant animals due to their nutritional makeup, medicinal properties, and livestock acceptance. The utilization strategy will be of paramount importance and will be determined through establishing the correct mistletoe inclusion level in relation to low quality roughages. Even though the species does have detrimental impacts, it is advised that mistletoe control management in rangelands be conducted with caution. Moreover, the efforts taken to regulate it should not result in the plant’s total eradication due to the benefits it provides in terms of fodder, medicine, and in other areas. Future research may be required to assess the livestock preference of each species when present in different hosts. Again, there is a need to assess the palatability index of different Viscum species.

Author Contributions

Authors O.H., K.E.R., M.G.M., N.S., H.S.M., K.H.M. and B.M. All participated equally to the review article draft. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Teodoro, G.S.; van den Berg, E.; Arruda, R. Metapopulation dynamics of the mistletoe and its host in savanna areas with different fire occurrence. PLoS ONE 2013, 8, 65836. [Google Scholar] [CrossRef]
  2. Ramantsi, R.; Mnisi, C.M.; Ravhuhali, K.E. Chemical composition and in vitro dry matter degradability of mistletoe (Viscum verrucosum (Harv.)) on Vachellia nilotica (L.) in North West Province of South Africa. Trop. Agric. 2019, 96, 53–60. [Google Scholar]
  3. Öztürk, Y.E.; Gülümser, E.; MUT, H.; Başaran, U.; Doğrusöz, M.Ç. A preliminary study on change of mistletoe (Viscum albüm L.) silage quality according to collection time and host tree species. Turk. J. Agric. Forest. 2022, 46, 104–112. [Google Scholar] [CrossRef]
  4. Kleszken, E.; Timar, A.V.; Memete, A.R.; Miere, F.; Vicas, S.I. On Overview of Bioactive Compounds, Biological And Pharmacological Effects Of Mistletoe (Viscum Album L.). Pharmacophore 2022, 13, 10–26. [Google Scholar] [CrossRef]
  5. Okubamichael, D.Y.; Griffiths, M.E.; Ward, D. Host specificity, nutrient and water dynamics of the mistletoe Viscum rotundifolium and its potential host species in the Kalahari of South Africa. J. Arid Environ. 2011, 75, 898–902. [Google Scholar] [CrossRef]
  6. Ndagurwa, H.G.T.; Dube, J.S. Evaluation of potential and effective rumen digestion of mistletoe species and woody species browsed by goats in a semi-arid savanna, southwest Zimbabwe. Anim. Feed Sci. Technol. 2013, 186, 106–111. [Google Scholar] [CrossRef]
  7. Oosthuizen, D.; Balkwill, K. Viscum songimveloensis, a new species of mistletoe from South Africa. S. Afr. J. Bot. 2018, 115, 194–198. [Google Scholar] [CrossRef]
  8. Majeed, M.; Rehman, R.U. Phytochemistry, Pharmacology, and Toxicity of an Epiphytic Medicinal Shrub Viscum album L. (White Berry Mistletoe). In Medicinal and Aromatic Plants; Aftab, T., Hakeem, K.R., Eds.; Springer Nature: Cham, Switzerland, 2021; pp. 287–301. [Google Scholar] [CrossRef]
  9. Abubakar, A.D.; Abubakar, M.; Yerima, J. Response of Red Sokoto Bucks Fed Graded Levels of Mistletoe Leaf Meal. Niger. J. Anim. Sci. Technol. 2021, 4, 74–80. [Google Scholar]
  10. Kim, C.W.; An, C.H.; Lee, H.S.; Yi, J.S.; Cheong, E.J.; Lim, S.H.; Kim, H.Y. Proximate and mineral components of Viscum album var. coloratum grown on eight different host tree species. J. Forest. Res. 2019, 30, 1245–1253. [Google Scholar] [CrossRef]
  11. Maul, K.; Krug, M.; Nickrent, D.L.; Müller, K.F.; Quandt, D.; Wicke, S. Morphology, geographic distribution, and host preferences are poor predictors of phylogenetic relatedness in the mistletoe genus Viscum L. Mol. Phylogenet. Evol. 2019, 131, 106–115. [Google Scholar] [CrossRef]
  12. Muche, M.; Muasya, A.M.; Tsegay, B.A. Biology and resource acquisition of mistletoes, and the defense responses of host plants. Ecol. Process 2022, 11, 24. [Google Scholar] [CrossRef]
  13. Patel, B.P.; Singh, P.K. Viscum articulatum Burm. f.: A review on its phytochemistry, pharmacology and traditional uses. J. Pharm. Pharmacol. 2018, 70, 159–177. [Google Scholar] [CrossRef]
  14. Adeneye, A.A. Subchronic and chronic toxicities of African medicinal plants. In Toxicological Survey of African Medicinal Plants; Kuete, V., Ed.; Elsevier: Amsterdam, The Netherlands, 2014; pp. 99–133. [Google Scholar] [CrossRef]
  15. Aparicio Martínez, A.; Gallego Cidoncha, M.J.; Vázquez, C. Reproductive biology of Viscum cruciatum (viscaceae) in southern Spain. Int. J. Plant Sci. 1995, 156, 42–49. [Google Scholar] [CrossRef]
  16. Smith, D.; Barkman, T.J.; de Pamphilis, C.W. Hemiparasitism. In Encyclopedia of Biodiversity, 2nd ed.; Scheiner, M.S., Ed.; Elsevier Inc.: Amsterdam, The Netherlands, 2001; pp. 70–78. [Google Scholar] [CrossRef]
  17. Besri, M. Viscum cruciatum: A threat to the olive production in the Moroccan Rif Mountains. IOBC WPRS Bull. 2005, 28, 169. [Google Scholar]
  18. Sunil Kumar, K.N.; Puneeth, V.S.; Tamizh, M.M.; Rubeena, M. Monograph on quality standards of Viscum angulatum B. Heyne ex DC. Indian J. Nat. Prod. Resour. 2021, 11, 320–332. [Google Scholar] [CrossRef]
  19. Wiens, D.; Tölken, H.R. Viscaceae. In Flora of Southern Africa; Leistner, O.A., Ed.; Botanical Research Institute: Pretoria, South Africa, 1979; Volume 10, pp. 43–56. [Google Scholar]
  20. Sosnovsky, Y.; Krasylenko, Y.; Nachychko, V. Viscum meyeri (Viscaceae)—A new name for Viscum anceps, an old-established mistletoe species endemic to southern Africa. Phytotaxa 2021, 523, 284–290. [Google Scholar] [CrossRef]
  21. Wiens, D.; Barlow, B.A. Translocation heterozygosity in southern African species of Viscum. Bothalia 1980, 13, 161–169. [Google Scholar] [CrossRef]
  22. Anselmo-Moreira, F.; Teixeira-Costa, L.; Ceccantini, G.; Furlan, C.M. Mistletoe effects on the host tree Tapirira guianensis: Insights from primary and secondary metabolites. Chemoecology 2019, 29, 11–24. [Google Scholar] [CrossRef]
  23. Al-Rowaily, S.L.; Al-Nomari, G.S.; Assaeed, A.M.; Facelli, J.M.; Dar, B.M.; El-Bana, M.I.; Abd-ElGawad, A.M. Infection by Plicosepalus curviflorus mistletoe affects the nutritional elements of Acacia species and soil nutrient recycling in an arid rangeland. Plant Ecol. 2020, 221, 1017–1028. [Google Scholar] [CrossRef]
  24. Ahmad, S.; Mir, N.; Sultan, S. White-berry mistletoe (Viscum album L.): A hemiparasitic plant: Occurrence and ethnobotanical use in Kashmir. J. Pharmacog. Phytochem. 2018, 7, 1831–1833. [Google Scholar]
  25. Türe, C.; Böcük, H.; Aşan, Z. Nutritional relationships between hemi-parasitic mistletoe and some of its deciduous hosts in different habitats. Biologia 2010, 65, 859–867. [Google Scholar] [CrossRef] [Green Version]
  26. Okubamichael, D.Y.; Griffiths, M.E.; Ward, D. Host specificity in parasitic plants—Perspectives from mistletoes. AoB Plants 2016, 8, plw069. [Google Scholar] [CrossRef] [PubMed]
  27. Clark, N.F.; McComb, J.A.; Taylor-Robinson, A.W. Host species of mistletoes (Loranthaceae and Viscaceae) in Australia. Aust. J. Bot. 2020, 68, 1–13. [Google Scholar] [CrossRef]
  28. Szmidla, H.; Tkaczyk, M.; Plewa, R.; Tarwacki, G.; Sierota, Z. Impact of common mistletoe (Viscum album L.) on Scots pine forests—A call for action. Forests 2019, 10, 847. [Google Scholar] [CrossRef]
  29. Griebel, A.; Watson, D.; Pendall, E. Mistletoe, friend and foe: Synthesizing ecosystem implications of mistletoe infection. Environ. Res. Letters 2017, 12, 115012. [Google Scholar] [CrossRef]
  30. Griebel, A.; Metzen, D.; Pendall, E.; Nolan, R.H.; Clarke, H.; Renchon, A.A.; Boer, M.M. Recovery from Severe Mistletoe Infection After Heat- and Drought-Induced Mistletoe Death. Ecosystems 2022, 25, 1–16. [Google Scholar] [CrossRef]
  31. Bhat, K.A.; Akhtar, S.; Dar, N.A.; Bhat, M.I.; Bhat, F.A.; Rizwan, R.; Horielov, O.; Krasylenko, Y. Mistletoe Eradicator-A Novel Tool for Simultaneous Mechanical and Chemical Control of Mistletoe. J. Vis. Exp. 2022, 181, e63455. [Google Scholar] [CrossRef]
  32. Ndagurwa, H.G.T.; Dube, J.S. Nutritive value and digestibility of mistletoes and woody species browsed by goats in a semi-arid savanna, southwest Zimbabwe. Livest. Sci. 2013, 151, 163–170. [Google Scholar] [CrossRef]
  33. Jibril, J.A.; Gazali, Y.M.; Dantani, M.; Alamin, H.; Zannah, B.B. Performance of Balami Rams Fed Graded Levels of Mistletoe Leaves (Viscum album) and Sorghum Stover in Semi-Arid Zone of Borno State, Nigeria. Niger. J. Anim. Sci. Technol. 2020, 3, 25–31. [Google Scholar]
  34. Hawu, O.; Ravhuhali, K.E.; Mokoboki, H.K.; Lebopa, C.K.; Sipango, N. Proximate analysis, in vitro dry matter degradability and palatability index of legume residues and maize straws for ruminants. Legume Res. 2022, 45, 601–607. [Google Scholar] [CrossRef]
  35. Watson, L.H.; Owen-Smith, N. Phenological influences on the utilization of woody plants by eland in semi-arid shrubland. Afr. J. Ecol. 2002, 40, 65–75. [Google Scholar] [CrossRef]
  36. Atalay, A.İ. Determination of nutritive value and anti-methanogenic potential of mistletoe leaves (Viscum album) grown on different host. Int. J. Agric. Forest. Life Sci. 2020, 4, 120–123. [Google Scholar]
  37. Madibela, O.R.; Boitumelo, W.S.; Letso, M. Chemical composition and in vitro dry matter digestibility of four parasitic plants (Tapinanthus lugardii, Erianthenum ngamicum, Viscum rotundifolium and Viscum verrucosum) in Botswana. Anim Feed Sci Technol. 2000, 84, 97–106. [Google Scholar] [CrossRef]
  38. Madibela, O.R.; Mabutho, S.; Sebolai, B. Dry matter and crude protein degradability of four parasitic plants (Mistletoes) associated with browse trees in Botswana. Trop. Anim. Health Prod. 2003, 35, 365–372. [Google Scholar] [CrossRef] [PubMed]
  39. Tripathi, D.; Mani, V.; Pal, R.P. Vanadium in biosphere and its role in biological processes. Biol.l Trace Elem. Res. 2018, 186, 52–67. [Google Scholar] [CrossRef]
  40. Diniz, W.J.; Reynolds, L.P.; Borowicz, P.P.; Ward, A.K.; Sedivec, K.K.; McCarthy, K.L.; Kassetas, C.J.; Baumgaertner, F.; Kirsch, J.D.; Dorsam, S.T.; et al. Maternal vitamin and mineral supplementation and rate of maternal weight gain affects placental expression of energy metabolism and transport-related genes. Genes 2021, 12, 385. [Google Scholar] [CrossRef] [PubMed]
  41. Umucalılar, H.D.; Gülşen, N.; Coşkun, B.E.H.İ.Ç.; Hayirli, A.; Dural, H.Ü.S.E.Y.İ.N. Nutrient composition of mistletoe (Viscum album) and its nutritive value for ruminant animals. Agroforest. Syst. 2007, 71, 77–87. [Google Scholar] [CrossRef]
  42. Hernández-Castellano, L.E.; Hernandez, L.L.; Bruckmaier, R.M. Endocrine pathways to regulate calcium homeostasis around parturition and the prevention of hypocalcemia in periparturient dairy cows. Animal 2020, 14, 330–338. [Google Scholar] [CrossRef]
  43. Gałęska, E.; Wrzecińska, M.; Kowalczyk, A.; Araujo, J.P. Reproductive Consequences of Electrolyte Disturbances in Domestic Animals. Biology 2022, 11, 1006. [Google Scholar] [CrossRef]
  44. National Research Council. Nutrient Requirements of Beef Cattle; National Academy Press: Washington, DC, USA, 1996.
  45. Ikusika, O.O.; Mpendulo, C.T.; Zindove, T.J.; Okoh, A.I. Fossil shell flour in livestock production: A Review. Animals 2019, 9, 70. [Google Scholar] [CrossRef]
  46. Bhalakiya, N.; Haque, N.; Patel, P.; Joshi, P. Role of trace minerals in animal production and reproduction. IntJ. Livest. Res. 2019, 9, 1–12. [Google Scholar] [CrossRef]
  47. Hill, G.M.; Shannon, M.C. Copper and zinc nutritional issues for agricultural animal production. Biol. Trace Elem. Res. 2019, 188, 148–159. [Google Scholar] [CrossRef]
  48. Bakhshizadeh, S.; Aghjehgheshlagh, F.M.; Taghizadeh, A.; Seifdavati, J.; Navidshad, B. Effect of zinc sources on milk yield, milk composition and plasma concentration of metabolites in dairy cows. S. Afr. J. Anim. Sci. 2019, 49, 884–891. [Google Scholar] [CrossRef] [Green Version]
  49. Angeles-Hernandez, J.C.; Miranda, M.; Muñoz-Benitez, A.L.; Vieyra-Alberto, R.; Morales-Aguilar, N.; Paz, E.A.; Gonzalez-Ronquillo, M. Zinc supplementation improves growth performance in small ruminants: A systematic review and meta-regression analysis. Anim. Prod. Sci. 2021, 61, 621–629. [Google Scholar] [CrossRef]
  50. Fadl, A.M.; Abdelnaby, E.A.; El-Sherbiny, H.R. Supplemental dietary zinc sulphate and folic acid combination improves testicular volume and haemodynamics, testosterone levels and semen quality in rams under heat stress conditions. Reprod. Domest. Anim. 2022, 57, 567–576. [Google Scholar] [CrossRef] [PubMed]
  51. Cortinhas, C.S.; Freitas Júnior, J.E.D.; Naves, J.D.R.; Porcionato, M.A.D.F.; Silva, L.F.P.; Rennó, F.P.; Santos, M.V.D. Organic and inorganic sources of zinc, copper and selenium in diets for dairy cows: Intake, blood metabolic profile, milk yield and composition. Rev. Bras. de Zootec. 2012, 41, 1477–1483. [Google Scholar] [CrossRef]
  52. Wysocka, D.; Snarska, A.; Sobiech, P. Copper-an essential micronutrient for calves and adult cattle. J. Elementol. 2019, 24, 101–110. [Google Scholar] [CrossRef]
  53. Pugh, D.G. Feeding Practices in Sheep. In MSD and the MSD Veterinary Manual; Merck & Co., Inc.: Rahway, NJ, USA, 2020. [Google Scholar]
  54. MacPherson, A. Trace-mineral status of forages. In Forage Evaluation in Ruminant Nutrition; Givens, D.I., Owen, E., Axford, R.F.E., Amed, H.M., Eds.; CAB International: Wallingford, UK, 2000; pp. 345–370. [Google Scholar]
  55. National Research Council. Nutrient Requirements of Dairy Cattle, 7th ed.; National Academy Press: Washington, DC, USA, 2001.
  56. Mutlu, S.; Osma, E.; Ilhan, V.; Turkoglu, H.I.; Atici, O. Mistletoe (Viscum album) reduces the growth of the Scots pine by accumulating essential nutrient elements in its structure as a trap. Trees 2016, 30, 815–824. [Google Scholar] [CrossRef]
  57. García-García, J.D.; Anguiano-Cabello, J.C.; Arredondo-Valdés, R.; Candido del Toro, C.A.; Martínez-Hernández, J.L.; Segura-Ceniceros, E.P.; Govea-Salas, M.; González-Chávez, M.L.; Ramos-González, R.; Esparza-González, S.C.; et al. Phytochemical characterization of Phoradendron bollanum and Viscum album subs. austriacum as Mexican mistletoe plants with antimicrobial activity. Plants 2021, 10, 1299. [Google Scholar] [CrossRef]
  58. Djmouai, D.; Saidi, M.; Rahmani, Z.; Djmouai, A. Qualitative phytochemical analysis and estimation of antioxidant activities, phenolics, flavonoids and tannins. J. Fundam. Appl. Sci. 2016, 8, 1–4. [Google Scholar]
  59. Wang, T.Y.; Li, Q.; Bi, K.S. Bioactive flavonoids in medicinal plants: Structure, activity and biological fate. Asian J. Pharm.l Sci. 2018, 13, 12–23. [Google Scholar] [CrossRef]
  60. Egbuna, C.; Ifemeje, J.C. Biological functions and anti-nutritional effects of phytochemicals in living system. IOSR J. Pharm. Biol. Sci. 2015, 10, 10–19. [Google Scholar]
  61. Ohikhena, F.U.; Wintola, O.A.; Afolayan, A.J. Proximate composition and mineral analysis of Phragmanthera capitata (Sprengel) Balle, a mistletoe growing on rubber tree. Res. J. Bot. 2017, 12, 23–31. [Google Scholar] [CrossRef]
  62. Huang, Q.; Liu, X.; Zhao, G.; Hu, T.; Wang, Y. Potential and challenges of tannins as an alternative to in-feed antibiotics for farm animal production. Anim. Nutr. 2018, 4, 137–150. [Google Scholar] [CrossRef] [PubMed]
  63. Siniscalchi, D.; Cardoso, A.D.S.; Corrêa, D.C.D.C.; Ferreira, M.R.; Andrade, M.E.B.; da Cruz, L.H.G.; Ruggieri, A.C.; Reis, R.A. Effects of condensed tannins on greenhouse gas emissions and nitrogen dynamics from urine-treated grassland soil. Environ. Sci. Pollut. Res. 2022, 1–10. [Google Scholar] [CrossRef] [PubMed]
  64. van Cleef, F.O.S.; Dubeux, J.C.B.; Ciriaco, F.M.; Henry, D.D.; Ruiz-Moreno, M.; Jaramillo, D.M.; Garcia, L.; Santos, E.R.S.; DiLorenzo, N.; Vendramini, J.M.B.; et al. Inclusion of a tannin-rich legume in the diet of beef steers reduces greenhouse gas emissions from their excreta. Sci. Rep. 2022, 12, 1–11. [Google Scholar]
  65. Ologhobo, A.D.; Akangbe, E.; Adejumo, I.O.; Ere, R.; Agboola, B. Haematological and histological evaluation of African mistletoe (Viscum albium) leaf meal as feed additive for broilers. Annu. Res. Rev. Biol. 2017, 15, 1–7. [Google Scholar] [CrossRef]
  66. Malada, P.M.; Mogashoa, M.M.; Masoko, P. The evaluation of cytotoxic effects, antimicrobial activity, antioxidant activity and combination effect of Viscum rotundifolium and Mystroxylon aethiopicum. S. Afr. J. Bot. 2022, 147, 790–798. [Google Scholar] [CrossRef]
  67. Ishiwu, C.N.; Obiegbuna, J.E.; Aniagolu, N.M. Evaluation of chemical properties of mistletoe leaves from three trees (avocado, African oil bean and kola). Niger. Food J. 2013, 31, 1–7. [Google Scholar] [CrossRef]
  68. Szurpnicka, A.; Kowalczuk, A.; Szterk, A. Biological activity of mistletoe: In vitro and in vivo studies and mechanisms of action. Arch. Pharmacal. Res. 2020, 43, 593–629. [Google Scholar] [CrossRef] [PubMed]
  69. Drury, S. Herbal remedies for livestock in seventeenth and eighteenth century England: Some examples. Folklore 1985, 96, 243–247. [Google Scholar] [CrossRef]
  70. Iso, I.E.; Kennedy, O.O.O. Growth performance, carcass and meat quality of rabbits fed mistletoe leaf meal diet. J. Livest. Sci. 2021, 12, 220–228. [Google Scholar] [CrossRef]
  71. Letso, M.; Thela, N. The substitution of a parasitic plant (Viscum verrucosum) for lucerne hay in sheep diets. Int. J. Livest. Res. 2013, 3, 33–41. [Google Scholar]
  72. Madibela, O.R.; Jansen, K. The use of indigenous parasitic plant (Viscum verrocosum) in reducing faecal egg counts in female Tswana goats. Livest. Res. Rural Dev. 2003, 15, 9. [Google Scholar]
  73. Kim, J.H.; Kim, D.W.; Kang, K.H.; Jang, B.G.; Yu, D.J.; Na, J.C.; Kim, S.H.; Lee, D.S.; Suh, O.S.; Choi, K.D.; et al. Effects on dietary Korean mistletoe on performance and blood characteristics in broilers. Korean J. Poult. Sci. 2007, 34, 129–136. [Google Scholar] [CrossRef]
  74. Saleh, I.; Maigandi, S.A.; Hudu, M.I.; Abubakar, M.I.; Shehu, A.U. Uses and chemical composition of Misletoe (Viscum album) obtained from different species. Dutse J. Agric. Food Sec. 2015, 2, 8–12. [Google Scholar]
  75. Ologhobo, A.D.; Oluseun, A.I.; Owoeye, T.; Esther, A. Influence of mistletoe (Viscum album) leaf meal on growth performance, carcass characteristics and biochemical profile of broiler chickens. Food Feed Res. 2017, 44, 163–171. [Google Scholar] [CrossRef]
Figure 1. Viscum rotundifolium in Limpopo Province, photo taken by KE Ravhuhali.
Figure 1. Viscum rotundifolium in Limpopo Province, photo taken by KE Ravhuhali.
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Figure 2. Viscum verrucosum Harv. in North West Province, photos taken by O Hawu.
Figure 2. Viscum verrucosum Harv. in North West Province, photos taken by O Hawu.
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Table 1. Viscum species and their distribution.
Table 1. Viscum species and their distribution.
DistributionReferences
Viscum spp. with leaves
V. articulatumAsia, Australia[13]
V. albumAsia, Europe and Nepal[14]
V. cruciatumAsia, Africa and Europe[15,16,17]
V. rotundifoliumAfrica[5]
Viscum spp. without leaves
V. angulatumAsia[18]
V. combreticolaAfrica[19]
V. ancepsAfrica[20]
V. songimveloensisAfrica[7]
V. verrucosum Harv.Africa[21]
Table 2. Chemical composition (g/kg DM) of Viscum species.
Table 2. Chemical composition (g/kg DM) of Viscum species.
SpeciesDM (g/kg)CPEENDFADFADLReferences
V. album96015080339202 [33,36]
V. verrucosum912121 27624475[2,32]
V. rontudifolium 163 241121[37,38]
DM: dry matter, CP: crude protein, EE: ether extract, NDF: neutral detergent fiber, ADF: acid detergent fiber, and ADL: acid detergent lignin.
Table 4. Antinutritional factors content (g/kg DM) in Viscum species.
Table 4. Antinutritional factors content (g/kg DM) in Viscum species.
SpeciesTanninsSaponinsPhenolicOxalatePhytatesFlavonoidsReferences
V. album9933 158227 [65]
V. rontudifolium7.3 28.3 2.4[66]
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Hawu, O.; Ravhuhali, K.E.; Musekwa, M.G.; Sipango, N.; Mudau, H.S.; Mokoboki, K.H.; Moyo, B. Utilization of the Viscum Species for Diet and Medicinal Purposes in Ruminants: A Review. Animals 2022, 12, 2569. https://doi.org/10.3390/ani12192569

AMA Style

Hawu O, Ravhuhali KE, Musekwa MG, Sipango N, Mudau HS, Mokoboki KH, Moyo B. Utilization of the Viscum Species for Diet and Medicinal Purposes in Ruminants: A Review. Animals. 2022; 12(19):2569. https://doi.org/10.3390/ani12192569

Chicago/Turabian Style

Hawu, Onke, Khuliso Emmanuel Ravhuhali, Mutshidzi Given Musekwa, Nkosomzi Sipango, Humbelani Silas Mudau, Kwena Hilda Mokoboki, and Bethwell Moyo. 2022. "Utilization of the Viscum Species for Diet and Medicinal Purposes in Ruminants: A Review" Animals 12, no. 19: 2569. https://doi.org/10.3390/ani12192569

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