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Ruminant Trace Minerals Deficiency and the Potential Link Between the Source and Rumen Interaction. A Review

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16 June 2023

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16 June 2023

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Abstract
Dietary inclusion of trace minerals (TM), such as copper (Cu), manganese (Mn) and zinc (Zn) is of importance to cover the ever-evolving requirements for growth, production, and reproduction in ruminants. Various sources of TM are commercially available, such as inorganic (ITM), organic (OTM) or hydroxy (HTM) forms, however their bioavailability and efficiency to improve ruminant zootechnical parameters may be highly influenced by ruminal solubility and effects on the rumen environment. The objective of this review was to compile the most up-to-date information on the ruminal solubility of ITM, OTM and HTM, and their effects on fermentation parameters and rumen microbiota, aiming to support specialists from the animal feed industry when choosing TM products for ruminant supplementation. Some commonly used ITM sources, like sulfates, have a high ruminal solubility, while oxides are less soluble. The ruminal solubility of OTM is mostly found to be high, however data on these TM forms are still lacking. Regarding HTM, ruminal solubility is reported to be low, nevertheless results are inconsistent. Considering rumen fermentation, ITM show a negative effect, OTM might improve, while HTM do not affect parameters like dry matter degradability, volatile fatty acid production, pH, or microbial protein synthesis. As to rumen microbiota, ITM do not affect microbial populations; OTM could decrease abundance of some specific bacteria, like fibrolytic microorganisms, while studies with HTM are missing or inconclusive. Further research is necessary to better understand the ruminal solubility kinetics of TM sources and the different interactions with fermentation parameters and rumen microbiota to successfully apply precision TM supplementation of ruminants, tackling deficiency occurrences.
Keywords: 
ruminant
;  
trace minerals
;  
solubility
;  
fermentation
Subject: 
Biology and Life Sciences  -   Animal Science, Veterinary Science and Zoology

1. Introduction

For most species the absorption site of trace minerals (TM) is located in the small intestine [1,2]. However, in ruminants and especially in the rumen, some interactions between microorganisms, minerals and other substances within the diet can occur resulting in reduced final mineral intestinal absorption [1]. These interactions could be influenced by factors such as solubility, hence the objective of this review was to compile an up-to-date reference on ruminal solubility of various TM sources currently used for supplementing ruminants and their effects on rumen fermentation parameters and microbial populations. The nutritional feeding systems for ruminants focus mainly on the global animal requirements [3,4], indicating dietary optimum levels of 10, 50 and 50 mg/kg DM, and regulatory maximum limits of 35, 150 and 120 mg/kg DM for Cu, Mn and Zn, respectively [5,6]. These TM are essential in animal feed, given their important physiological functions, such as participation in keratin, collagen and elastin synthesis; components or activators of enzymes; in addition to an important role for reproductive and immune systems [7,8,9]. In addition to the contribution to these metabolic functions, TM can also affect the ruminal environment and rumen function, given that rumen microorganisms require minerals for their growth (microbial protein synthesis) and fermentative activity [10,11,12]. Intestinal bioavailability of the dietary TM for ruminants is relatively quite low, reported levels are at 4-5%, 1-4% and 15-30% for Cu, Mn and Zn, respectively [3,13,14], while selecting the most optimal mineral source for supplementation is quite difficult. Furthermore, ruminal microbial uptake levels are not known. Insights on the ruminal solubility, microbial uptake, and effects on rumen environment of the various existing TM sources could support specialists from the animal feed industry when choosing TM products for dietary inclusion.

2. Trace mineral deficiency in ruminants

Trace mineral deficiency can often occur in ruminants in a marginal form (without any clinical signs)[15], especially in grazing and high producing animals [16]. One of the most widely spread TM deficiency is with Cu [17]. In a study assessing Cu deficiency in grazing sheep [18], it was found that serum and liver Cu content were not in the normal physiological range (7-24 µmol/L and 10-120 mg/kg fresh matter for serum and liver Cu concentration, respectively [19]), even though the Cu content of the grazed herbage (8.61 and 9.26 mg/kg DM for two analyzed pastures) was within the range to cover nutritional requirements for sheep (5-10 mg/kg DM) [5]. The low Cu absorption was mostly due to the high Mo content (>11 mg/kg DM) of the grass [15,18]. In a study assessing Cu deficiencies in grazing beef cattle herds [20], it was reported that approximately 39% (of a total of 2,007) of the reproduction cows and heifers, and 36% (of a total of 256) of the herds were marginally deficient. As for dairy cows, feeding a diet based on silage, pasture and hay (Cu content ranging from 6.5 to 9 mg/kg DM) without any Cu supplementation for a period of 161 days sharply decreased liver Cu from approximately 61 to 22 mg/kg DM [21].
The Mn content of ruminant diets is considered to supply sufficient quantities to cover the animals’ requirements, hence very little research has been carried out on this mineral with ruminants [2]. Considering that the most frequent TM deficiencies in ruminants occur related to Cu and Zn, research is rarely focused on Mn. However, Mn deficiencies can occur with diets containing high proportions of silages (red clover silage, grass silage) due to a lower bioavailability of Mn in silages compared to hay [22].
When it comes to Zn supplementation in ruminants, dietary inclusion levels need to be carefully evaluated given that the percentage of absorbed Zn decreases as dietary Zn increases [14,23]. Severe Zn deficiency in ruminants is rare under normal farming conditions, and it is easily diagnosed (serum Zn concentration < 0.5 mg/L) in comparison to marginal Zn deficiency, for which reliable indicators are lacking, apart from a positive response in production (growth, reproduction, or milk production) [15]. In a study with lactating Holstein dairy cows, a basal diet containing 31.2 mg/kg DM of Zn was supplemented with increasing levels (10, 20 or 30 mg/kg DM) of inorganic Zn (as coated ZnSO4). Results showed a linear increase of milk production, as well as total milk solids (fat and protein) in the Zn supplemented groups [24]. Supplementing Zn at levels of 40 or 80 mg/kg DM (as ZnSO4 or Zn hydroxychloride) in pre-ruminant crossbred calves (starting age 10 days) significantly improved growth performance (body weight, average daily gain and body length) when compared to non-supplemented animals after a 90 days period [25]. When considering Zn effect on reproduction, in a study with lactating dairy cows results showed that supplementing 80 or 120 mg/kg DM of Zn (as ZnSO4) for 90 days (45 days before and 45 days after calving) significantly improved reproductive efficiency (reduction in postpartum estrus interval, days to first insemination, service period, service per conception and increased conception rate) in both supplemented groups compared to no supplementation [26].
Trace mineral deficiencies affect the reproductive system and fertility in ruminants [27]. Blood concentrations of Cu and Zn were associated with luteal activity in Holstein dairy cows, showing improved reproduction parameters with higher blood TM concentrations [28]. In dairy goats, Cu deficiency mainly affected the reproductive system showing prolonged anestrus, embryonic resorption, high indices of retained placenta, small ovaries without viable follicles; while kids born from Cu-deficient goats were week, presenting neonatal and late ataxia [29].
The assessment of TM status of ruminants is often quite challenging, especially when clinical signs of deficiency are lacking [15]. Furthermore, the TM content of pasture herbage and forages are highly variable and influenced by factors such as region, season, harvest, or farming and feeding practices [30,31,32,33,34,35]; and have a strong effect on the TM status of ruminants [36,37,38,39]. The low level of TM in forages coupled with rumen antagonisms [17,40] can result in an epidemiology of TM deficiencies in ruminants [41]. Reducing TM deficiencies (especially marginal deficiencies) in ruminants can be limited trough TM supplementation of the cropping lands (ex. manure application) [42], or by dietary inclusion of TM in ruminant diets [41]. Given that the TM requirements in ruminants are not static [5,13], evolving with the selection for more feed-efficient and higher producing animals [16], TM physiological status could be affected by the ruminal solubility and bioavailability of different supplemental sources, like inorganic, organic or hydroxy TM. Considering this, choosing the optimal TM sources for ruminant supplementation can be quite challenging: a more rumen-soluble TM might have a higher bioavailability, however the occurrence of complexation with other minerals could also increase, making it less bioavailable. The optimal TM sources would be characterized by a high ruminal solubility coupled with a low reactivity with other elements in the rumen environment and the lack of negative effects on rumen fermentation parameters.

3. Available trace mineral forms for dietary inclusion

Trace mineral sources for supplementing ruminants are numerous and include inorganic (ITM), organic (OTM) or hydroxy (HTM) mineral forms [2,6,43,44]. The ITM salts such as carbonates, chlorides, oxides and sulfates are characterized as a specific metal (Cu, Mn, Zn) bound to a non-carbon-containing ligand [45,46,47,48,49], and are widely available at a low cost. These sources are traditionally used for livestock supplementation [50]. The OTM such as glycinates, amino acid-complexes, amino acid chelates or different proteinates are formed through specific processes, binding the metal component (Cu, Mn, Zn) to a carbon-containing ligand [51]. The HTM are defined as a specific metal (Cu, Mn, Zn) bound via a coordinated covalent bound with a hydroxyl ligand and are considered inorganic [14]. However, the covalent bound to an OH group instead of carbon containing ligands, make HTM seem like OTM [52]. In ruminant feed HTM (Cu, Mn and Zn) are provided in the form of copper hydroxy chloride (Cu-Hyd) [53], manganese hydroxy chloride (Mn-Hyd) [54] and zinc hydroxy chloride (Zn-Hyd) [55]. Other TM forms and sources are studied for ruminant supplementation, including nano minerals [56], or even different seaweeds [57,58], however little research is available on these last forms considering rumen solubility.

4. Trace mineral rumen solubility and effects on the ruminal environment

There are numerous studies addressing the overall effects of TM in ruminants, however still little is known about their ruminal solubility and effects on the rumen microbial populations. Ruminal solubility is to be considered when choosing a TM sources for dietary inclusion, given that it was identified as one of the factors closely related to TM relative bioavailability in ruminants [2,59]. Solubility of ITM in rumen fluid was found to be in close relation with their mineral presentation form: sulfates are considered highly soluble compared to oxides [60]. Even though it was demonstrated that OTM like glycinates, amino acid-complexes, amino acid chelates or different proteinates have a high stability in the 6.0 – 7.0 pH range (similar to the one found in the rumen environment [61]), showing minimum effect of enzymatic hydrolysis [51], solubility of OTM in rumen fluid, exposed to bacterial fermentative activity, could be significantly affected [60]. When considering ruminal solubility of HTM, they appear to be relatively insoluble, however results are not equivocal for the hydroxy form of Cu, Mn and Zn [62]. In the following, an overview of different solubility evaluation methods as well as the ruminal solubility of various sources (inorganic, organic and hydroxy) of Cu, Mn and Zn are presented while also considering effects on rumen fermentation parameters and microbial population changes.

4.1. Ruminal solubility evaluation methods

For an overview of TM solubility, the assessment can be performed through in vitro models with deionized water as a solvent [63]. However, even though TM solubilization in deionized water may be a good indicator of overall solubility of a specific TM, the ruminal solubility of TM may be affected by the rumen environment, and it was shown to be significantly lower when compared to solubility in deionized water [60]. Considering this, when assessing ruminal solubility of TM via in vitro studies, for a more factual representation of the various interactions in the ruminal environment, rumen fluid-based models are to be privileged. Key aspects, like donor animals, rumen fluid processing as inoculum, incubation substrate and buffer choice for in vitro fermentation techniques are well established for the assessment of rumen function (fermentation activity, gas production, nutrient degradation) [64], however for TM ruminal solubility, the techniques are not yet harmonized. One of the applied methods for the assessment of ruminal solubility of TM following in vitro fermentations (of 24, 48 hours or continuous fermentations) is the analysis of TM concentration in a centrifugation supernatant [65,66]. Based on this method, the final fermentation medium (mix of rumen fluid, buffer, substrate and various TM) is centrifuged (12,000 – 18,000 x g at 23oC for 15 minutes) to separate the particulate matter (feed particles, protozoa, bacteria and insolubilized TM) obtaining a supernatant (containing the solubilized minerals), which is analyzed for TM concentration. Next, the ruminal solubility of a specific TM may be expressed as an absolute value (based on the TM concentration of the supernatant) or a relative value (related to a sulfate TM, considered as 100 % rumen soluble). In recent studies [67,68], the ruminal solubility of various minerals was assessed based on a separation of the final fermentation medium (after 70 hours of fermentation) by multiple centrifugations: at 100 x g (5 minutes at 40C), to separate an insoluble fraction (containing feed particles, protozoa and insolubilized minerals); the obtained supernatant is then further centrifuged at 18,500 x g (20 minutes at 4oC) to separate a bacteria enriched fraction and a final supernatant, containing only solubilized minerals; the mineral concentration of each centrifugation fraction is then analyzed. Next, the ruminal solubility of TM can be expressed as a percentage of solubilized mineral in the final supernatant (based on the total mineral analyzed in the different centrifugation fractions.
The ruminal solubility of TM can also be determined using in vivo models. In a study by Arelovich et al. [69], the ruminal fluid (100 mL) sampled from rumen cannulated heifers (supplemented with different levels of TM), was first filtered with a cheesecloth, acidified (addition of 2 mL of 20% sulfuric acid solution) and centrifuged (16,000 x g) to obtain a supernatant (containing the solubilized minerals). Ruminal solubility of TM was expressed in absolute values based on the TM concentration of the supernatant. In other in vivo studies [62,70], the ruminal solubility of different TM sources was assessed following a supplementation with different levels of TM and analysis of the mineral concentration of the rumen content. Samples of rumen fluid were separated by ultracentrifugation (28,000 x g for 30 minutes at 4oC) in solids pellets (containing the insolubilized minerals) and a supernatant, considered to contain the rumen soluble minerals. The ruminal solubility of TM was expressed as an absolute value (based on the mineral concentration of the supernatant), or a relative value (as a percentage of whole ruminal mineral, calculated based on the total amount of rumen content samples and mineral concentration of the centrifugation fractions).

4.2. Copper ruminal solubility

One of the most commonly used inorganic Cu source for ruminant supplementation is CuSO4 [14], often used as a comparison basis for rumen solubility with other Cu sources. In a study by Deters et al. [63], the solubility of CuSO4 and glycinate bound Cu (Cu-Gly) in deionized water (at 5.2 pH) was 100% and 68.9%, respectively. In a similar study by Clarkson et al. [60], the solubility of a range of Cu sources ( CuSO4, CuCl2, CuO, CuCO3, Cu-Hyd, Cu EDTA, Cu proteinate and Cu acetate) was estimated in either deionized water or rumen fluid. The results showed that solubility across all Cu sources was lower in rumen fluid than in deionized water (mean relative solubility across all Cu sources was 33% and 64% in rumen fluid and deionized water, respectively). These findings suggest that the rumen environment has a significant effect on the solubility of different TM sources. Table 1 summarizes the available literature data on ruminal solubility of various Cu sources.
In an in vivo study [70], assessing the ruminal solubility of two sources of Cu (as CuSO4 and Cu-Hyd, respectively) it was found that the Cu concentration of the rumen fluid supernatant was higher with CuSO4 when compared to Cu-Hyd (approximately 0.65 and 0.20 mg/L for CuSO4 and Cu-Hyd, respectively), concluding that CuSO4 has a high, while Cu-Hyd has a low ruminal solubility. In a similar study by Genther and Hansen [62], at an inclusion level of 25 mg/kg DM of Cu, the ruminal solubility of CuSO4 was higher compared to Cu-Hyd (approximately 14 and 9 %, respectively). These results indicate well the rumen solubility of the two Cu sources, however the solid fraction, beside undegraded feed fractions and insoluble minerals, also contains rumen microorganisms (protozoa, bacteria), which could assimilate solubilized Cu. In an in vitro study, the solubility of CuSO4 in rumen fluid was found to be high, given that >50% of the total additional Cu was found in a final supernatant obtained after centrifugation of the final fermentation medium. Furthermore, approximately 18 to 27% of the supplemented Cu was analyzed in a bacteria enriched fraction, indicating that Cu might be assimilated by rumen bacteria [67].
Given the rumen antagonism of Cu with other minerals (mainly sulfur and molybdenum)[17,60], highly rumen soluble Cu sources (like CuSO4) often present a decreased bioavailability for ruminants, in relation with antagonist minerals present in the rumen content [43]. In order to limit the effect of the rumen environment on mineral additives, various methods, like lipid encapsulation or polymer coating were developed [71]. When comparing the rumen solubility of CuSO4 and an encapsulated mixture of different Cu sources (Enc. Cu; mix of tribasic copper chloride and CuSO4 with a polysaccharide polymer coating), Wilk et al. [66] found that Enc. Cu had a lower solubility when compared to CuSO4 (rumen fluid supernatant Cu concentration was 0.38 and 0.70 mg/kg for Enc. Cu and CuSO4, respectively).

4.3. Manganese ruminal solubility

Given that Mn is poorly absorbed by ruminants [72,73], and that it is considered that Mn content of the basal diet might cover the rumen microbial requirements [74], little research is focused on ruminal solubility of different Mn sources. In a study by Caldera et al. [70], the ruminal solubility of two Mn sources (MnSO4 and Mn-Hyd) was compared by administrating a pulse dose of 40 mg/kg DM of Mn to rumen canulated steers consuming a basal diet with a Mn content of 19.2 mg/kg DM. The ruminal solubility of the two Mn sources was assessed based on the Mn concentration of the rumen fluid supernatant (considered to contain the soluble Mn) and solid fraction (containing the insoluble Mn). After only 4 hours from the pulse dose administration, the mineral analysis of the two fractions showed a Mn content of approximately 0.7 mg/L and 9.0 mg/kg DM with the MnSO4; and 0.5 mg/L and 14.0 mg/kg DM with the Mn-Hyd in the supernatant and solid fraction, respectively. However, after 24 hours, the Mn content of the supernatant was approximately 0.3 and 0.5 mg/L, while of the solid fraction approximately 14.0 and 9.0 mg/kgDM with MnSO4 and Mn-Hyd, respectively. Furthermore, the reported relative solubility after 4 hours was about 20 and 10 %; and after 24 hours about 6 and 15 % for MnSO4 and Mn-Hyd, respectively. These findings indicate that both Mn sources (MnSO4 and Mn-Hyd) are quite soluble in the rumen. In a similar study, supplementing rumen cannulated steers with 60 mg/kg DM of Mn (as MnSO4 or Mn-Hyd), the ruminal solubility of MnSO4 showed no difference when compared to Mn-Hyd (relative solubility of approximately 65 and 66 % for MnSO4 and Mn-Hyd, respectively) [62]. In an in vitro study, the ruminal solubility of two inorganic Mn sources (MnSO4 and MnO) was assessed [67]. Results showed that MnSO4 and MnO are equally soluble in the rumen fluid after 70 hours of fermentation. However, when solubility was assessed at a shorter period (22 hours), MnSO4 showed a higher solubility when compared to MnO. The ruminal solubility of various Mn sources is summarized in Table 2.

4.4. Zinc ruminal solubility

In a recent in vitro study [67], the ruminal solubility of ZnSO4 was significantly higher when compared to ZnO (32 and 25 %; p < 0.05). Furthermore, of the total analyzed Zn (sum of total Zn in different fraction of the centrifuged rumen fluid), 27 to 38% and 19 to 24% for ZnSO4 and ZnO, respectively, was found in the bacteria enriched fraction, indicating not only that Zn might be assimilated by rumen bacteria, but also a higher ruminal bioavailability of ZnSO4 when compared to ZnO. In a similar study, Fellner et al. [65] analyzed the ruminal solubility of ZnO and HiZnox (a greater purity potentiated ZnO) using continuous in vitro fermentations. The results showed a lower solubility of ZnO when compared to HiZnox, based on the Zn concentration of the rumen fluid supernatant (0.4 and 0.5 mg/kg for ZnO and HiZnox, respectively).
The ruminal solubility of some Zn sources was also assessed using in vivo models. Following a supplementation with 60 mg/kg DM of Zn (as ZnSO4 or Zn-Hyd) to rumen canulated steers, the ruminal solubility after 24 hours was 15 and 10 % for ZnSO4 and Zn-Hyd, respectively [70]. In a similar study by Genther and Hansen [62], a lower ruminal solubility was reported for ZnSO4 when compared to Zn-Hyd (7 and 11 %, respectively) when animals were supplemented with 120 mg/kg DM of Zn. Another study on ruminal solubility of TM reported a high ruminal solubility when supplementing steers with 30, 250 and 470 mg/kg DM of Zn as ZnCl2 [69]. The solubility of Zn might also be affected by clay minerals ingested with different feeds, as shown in an in vitro study by Schlattl et al. [75]: the addition of a clay mixture (90% bentonite and 10% kaolinite) reduced Zn (as nitrous Zn) solubility by 42, 49 and 52% under ruminal (pH 7.02), abomasal (pH 2.00) and duodenal (pH 3.58) conditions. Table 3 summarizes the ruminal solubility of various Zn sources.

4.5. Trace mineral effects on rumen fermentation parameters

When considering rumen fermentation, Cu was identified as a TM with complex responses. In an in vivo study with rumen cannulated steers [70], supplementing Cu at levels of 10 mg/kg DM (as CuSO4 or Cu-Hyd) did not affect apparent dry matter (DM) digestibility, while apparent neutral detergent fiber (NDF) digestibility tended (p < 0.10) to be lower with CuSO4 when compared to Cu-Hyd (37.8 and 41.2 %, respectively). In a similar study [62], supplementing a high dosage of Cu (25 mg/kg DM) as CuSO4 decreased, while supplementing with Cu-Hyd did not affect rumen DM disappearance when compared with a control (CON, no Cu supplementation) diet (p < 0.03; 63.5, 64.4 and 65.6 % for CuSO4, Cu-Hyd and CON, respectively). In this study, the two Cu sources did not affect NDF degradation. In an in vitro study by Wilk et al. [66], it was found that Cu sources (Enc. Cu and CuSO4, respectively) did not affect DM degradability, while CuSO4 increased in vitro gas production, propionate concentration and decreased acetate to propionate ratio when compared to Enc. Cu. The two Cu sources did not affect in vitro methanogenesis. In a similar study [76], lipid encapsulated CuSO4 decreased acetate, increased butyrate molar proportion, and tended to decrease acetate to propionate proportion, but did not affect nutrient (DM, organic matter, crude protein and NDF) digestibility when compared to CuSO4. Table 4 presents a compilation of various Cu sources effects on rumen fermentation parameters.
When it comes to Mn effect on rumen fermentation, results of in vivo studies assessing the effects of supplementing different sources of Mn to rumen cannulated steers are various. A significant decrease of DM disappearance was shown with MnSO4, while Mn-Hyd did not affect DM disappearance (supplementation levels of 15 or 60 mg/kg DM of Mn); the two sources of Mn did not affect NDF degradability [62]. In another study on the effects of Mn supplementation (40 mg/kg DM as MnSO4 or Mn-Hyd), the DM digestibility was not affected by the treatments, while NDF digestibility tended to be lower with MnSO4 when compared to Mn-Hyd [70]. Varied results are equally reported when analyzing Mn effect on fermentation during in vitro studies with rumen fluid. In a study by Areolovich et al. [69], the addition of 100 mg/DM of Mn (as MnCl2) significantly increased DM degradation, without affecting volatile fatty acids (VFA) concentration. In a more recent study [67], an overall negative effect of Mn (600 mg/kg DM as MnO or MnSO4) was registered: decrease of total gas production, DM degradability and butyrate (% of total VFA) concentration. Table 5 presents the effects on rumen fermentation of some Mn sources.
Regarding Zn effect on rumen fermentation, results of early in vitro studies have shown that a high dosage of Zn (as ZnSO4) has a strong negative effect [79]. In more recent in vitro studies, the negative effects of Zn on rumen fermentation vary according to different sources of Zn. In a study by Fellner et al. [65], it was shown that an addition of 30 or 120 mg/kg DM of Zn as ZnO or HiZnox (a greater purity potentiated ZnO) affect differently the fermentation parameters: HiZnox reduced apparent DM disappearance, increased acetate to propionate ratio; ZnO reduced acetate, NH3-N and CH4 concentration, while both Zn sources increased culture pH. In another in vitro study [67], the total gas production and DM degradability was significantly reduced by ZnO, while ZnSO4 did not affect the fermentation parameters. Both inorganic Zn sources decreased the microbial protein synthesis. In a study assessing the effect of an organic source of Zn on rumen fermentation, it was found that the addition of 25 mg/kg DM of Zn as zinc proteinate (Zn-Prot) increased DM and organic matter digestibility, but did not affect acetate to propionate ration, nor CH4 concentration [80]. Table 6 compiles the effects on fermentation parameters of various inorganic and organic Zn sources.

4.6. Trace mineral effects on rumen microbiota

Studies addressing TM effects on rumen microbial community composition are still scarce, and the reported results do not always agree. Several studies with different Zn sources show that Zn can affect differently the rumen bacterial community. As shown by Ishaq et al. [82], Zn amino acid complex (Zn-AA) reduces rumen bacterial diversity, while ZnSO4 has no significant effect. Consistent with these results, total rumen bacterial populations decreased in lambs supplemented with 70 mg/kg DM of Zn (as Zn-AA) [81]. Furthermore, significant shifts in the relative abundance of fibrolytic bacteria populations, such as an increase of Ruminococcus albus and a decrease of Ruminococcus flavefaciens; or an increase of lactic acid producing bacteria (Streptococcus bovis) were noted; while the methanogenic Archaea abundance was not affected by Zn-AA supplementation [81]. In another study, supplementation of lactating Holstein dairy cows with increasing levels of Zn (10, 20 or 30 mg/kg DM as coated ZnSO4) significantly increased total bacteria and the main fibrolytic rumen microbial populations of Ruminococcus albus, Ruminococcus flavefaciens, Fibrobacter succinogenes and Butyrivibrio fibrisolvens [24].
Regarding Cu effect on rumen microbiota, supplementing a basal lactating dairy cows’ diet (Cu content of 8.51 mg/kg DM) with 7.5 mg/kg DM of inorganic Cu (as CuSO4 or coated CuSO4) significantly increased total bacteria populations and specific fibrolytic bacteria, such as Ruminococcus albus, Ruminococcus flavefaciens, Fibrobacter succinogenes and Butyrivibrio fibrisolvens, as well as some microbial enzyme activity (cellobiase, xylanase and pectinase), but decreased the populations of Prevotella ruminicola, Ruminobacter amylophilus and α-amylase activity [78].
The effects of inorganic and organic Mn on the rumen microbial ecosystem were observed in a study with ewe lambs [83]. The animals were fed a basal diet with a Mn level of 34.3 mg/kg DM and supplemented during 16 weeks with 182.7 and 184 mg/kg DM of Mn as inorganic (MnSO4) and organic (glycinate chelate) Mn, respectively. Inorganic Mn did not affect, while organic Mn decreased the variability (lower Shannon-Wiener diversity index) of eubacterial populations. Regarding enzymatic activity, α-amylase activity decreased with MnSO4, while carboxymethyl-cellulase activity increased with both Mn sources.
When comparing different levels of TM dietary inclusion, no noticeable alterations were observed in α and β-diversity of ruminal microbiota in beef heifers (virgin vs. pregnant) fed a control (no TM supplementation) diet (total intake of 13.7, 103.9 and 130.2 for Cu, Mn and Zn, respectively) or a high TM supplemented diet (total intake of 285.8, 953.4 and 1,051.8 mg/kg DM of Cu, Mn and Zn, respectively) [84,85]. Following a supplementation of lactating yaks with inorganic TM via slow release rumen boluses, some variations in the ruminal bacterial communities were observed, however the specific TM responsible for the changes was not clearly identified [86]. In a recent study with heat-stressed dairy steer [77], supplementing high levels of organic TM (28 and 350 mg/kg DM of Cu and Zn as Cu- and Zn-glycinate, respectively), no effects were registered on enteric CH4 production or rumen methanogenic microbial populations [77].

5. Conclusions

Results considering TM effects on rumen fermentation parameters, such as DM and NDF disappearance, VFA production, microbial synthesis are inconsistent, even when supplementation occurs with the same TM forms. These differences in effects on fermentation parameters might be influenced by the experimental design (in vitro or in vivo models), the supplemental TM dosages as well as the presence of other minerals (antagonists) in the ruminal environment. Furthermore, when selecting a TM source for ruminant supplementation, ruminal solubility should be taken into consideration, as the overall bioavailability of TM could be affected by higher rumen soluble minerals: a higher rumen solubility of a specific TM might improve its bioavailability, but at the same time a greater sensitivity to negative interactions (antagonism) with other minerals could be present, decreasing bioavailability. Based on this hypothesis, the observed TM deficiencies are not linked to dietary intakes, which may be sufficient, but to negative interactions with other minerals, a phenomenon dependent on the ruminal solubility of TM. Some ITM show a negative effect on ruminal fermentation parameters, but do not affect rumen microbiota. On the other hand, OTM might improve fermentative activity, while having negative effects on specific bacteria populations (ex. fibrolytic bacteria). However, there are a low number of studies with OTM and HTM, hence drawing any conclusions remains challenging. Further studies are necessary for the assessment of rumen solubility, bioavailability and effects on rumen fermentation and microbiota of different TM sources. A better understanding of the ITM, OTM and HTM solubility kinetics in the ruminal environment might help better understand and effectively address deficiencies by implementing precision feeding and TM supplementation of ruminant animals.

Author Contributions

Conceptualization, A.V. and C.G.; methodology, A.V and C.G..; software, A.V.; validation, A.C., N.C. and C.G.; formal analysis, A.V.; investigation, A.V. and C.G.; resources, A.V.; data curation, A.V.; writing—original draft preparation, A.V.; writing—review and editing, A.V., A.C., N.C and C.G; supervision, C.G.; project administration, A.V. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Conflicts of Interest

The authors declare no conflict of interest.

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Table 1. Ruminal solubility of different sources of copper
Table 1. Ruminal solubility of different sources of copper
Experimental model Cu dosage Cu source Solubilization time /supplementation period Ruminal solubility* Ref.
in vivo 5 and 25 mg/kg DM CuSO4 12 days ↑; ~ 17 and 14 % [62]
Cu-Hyd ↓; ~ 15 and 9 %
in vivo 20 mg/kg DM CuSO4 24 hours ↑; ~ 68, 30 and 12% after 4, 12 and 24 hours following ruminal administration [70]
Cu-Hyd ↓; ~ 15, 20 and 15% after 4, 12 and 24 hours following ruminal administration
in vitro 4, 12, 96 mg/kg DM (with 0.1% DM of S or 2% DM of urea) Cu-Lys 24 hours ↑ (with urea)↓ (with S) [59]
CuSO4 ↓ (with S)
in vitro 4 mM solution CuSO4 25 hours ↑; ~ 49% [60]
CuCl2 ↑; ~ 49%
CuO ↓; ~ 9%
CuCO3 ↓; ~ 19%
Cu-Hyd ↓; ~ 17%
Cu EDTA ↑; ~ 49%
Cu-Prot ↑; ~ 49%
Cu-Acet ↓; ~ 33%
in vitro 100 and 500 mg/kg DM CuSO4 22, 46 and 70 hours ↑; ~ 42, 37 and 57 % [67]
in vitro 12 mg/kg fresh matter CuSO4 24 hours ↑ [66]
Enc. Cu ↓
Cu: copper; GP: Gas production; VFA: Volatile fatty acids; A:P: Acetate to propionate ration; DMd: Dry matter degradability; MPS: Microbial protein synthesis; ↑: high; ↓: low; +: increase; -: decrease; =: no effect; ND: not determined; Cu-Lys: copper lysine; CuSO4: copper sulfate; CuCl2: copper chloride; CuO: copper oxide; CuCO3sulfate. carbonate; Cu-Hyd: copper hydroxychloride; Cu-EDTA: copper disodium edetate; Cu-Prot: copper proteinate; Cu-Acet: copper acetate; Cu-Gly: copper glycinate; Lip.Enc-CuSO4: lipid encapsulated copper sulfate; Enc. Cu: mix of tribasic copper chloride and copper sulfate within a polysaccharide polymer coating; *Ruminal solubility: where available, values of relative solubility were given.
Table 2. Ruminal solubility of different sources of manganese
Table 2. Ruminal solubility of different sources of manganese
Experimental model Mn dosage Mn source Solubilization time /supplementation period Ruminal solubility* Ref.
in vivo 40 mg/kg DM MnSO4 24 hours ↑; ~ 20, 12 and 6 % after 4, 12 and 24 hours following ruminal administration [70]
Mn-Hyd ↓; ~ 10, 7 and 15 % after 4, 12 and 24 hours following ruminal administration
in vivo 40 mg/kg DM MnCl2 16 days ↓ [69]
in vivo 15 and 60 mg/kg DM MnSO4 12 days ↑; ~ 62 and 65 % [62]
Mn-Hyd ↓; ~ 50 and 66 %
in vitro 600 mg/kg DM MnSO4 22, 46 and 70 hours ↑; ~ 94, 91 and 93 % [67]
MnO ↑; ~ 84, 88 and 93 %
Mn: Manganese; GP: Gas production; VFA: Volatile fatty acids; A:P: Acetate to propionate ration; DMd: Dry matter degradability; MPS: Microbial protein synthesis; ↑: high; ↓: low; +: increase; -: decrease; =: no effect; ND: not determined; MnSO4: manganese sulfate; Mn-Hyd: manganese hydroxychloride; MnCl2: manganese chloride; MnO: manganese oxide; *Ruminal solubility: where available, values of relative solubility were given.
Table 3. Ruminal solubility of different sources of zinc
Table 3. Ruminal solubility of different sources of zinc
Experimental model Zn dosage Zn source Solubilization time /supplementation period Ruminal solubility* Ref.
in vivo 60 mg/kg DM ZnSO4 24 hours ↑; ~ 39, 15 and 15 % after 4, 12 and 24 hours following ruminal administration [70]
Zn-Hyd ↓; ~ 10, 5 and 10 % after 4, 12 and 24 hours following ruminal administration
in vivo 30, 250 and 470 mg/kg DM ZnCl2 16 days ↑; linear increase of Zn concentration in the rumen fluid (2.26, 7.6 and 11.6 mg/L) [69]
in vivo 30 and 120 mg/kg DM ZnSO4 12 days ↓; ~ 12 and 7 % [62]
Zn-Hyd ↑; ~ 14 and 11 %
in vitro Nitrous-Zn ↓ (with clay) [75]
in vitro 500 mg/kg DM ZnSO4 22, 46 and 70 hours ↑; ~ 19, 17 and 32 % [67]
ZnO ↓; ~ 10, 9 and 25 %
in vitro 30 and 120 mg/kg DM ZnO ↓ [65]
HiZox 8 days continuous culture fermentation ↑
Zn: Zinc; GP: Gas production; VFA: Volatile fatty acids; A:P: Acetate to propionate ration; DMd: Dry matter degradability; MPS: Microbial protein synthesis; ↑: high; ↓: low; +: increase; -: decrease; =: no effect; ND: not determined; Zn-Gly: zinc glycinate; Zn-AA: zinc amino acid complex; ZnSO4: zinc sulfate; Zn-Hyd: zinc hydroxychloride; ZnCl2: zinc chloride; ZnO: zinc oxide; HiZox: high purity potentiated zinc oxide; Coat-ZnSO4: coated zinc sulfate; *Ruminal solubility: where available, values of relative solubility were given.
Table 4. Effects of different sources of Cu on rumen fermentation
Table 4. Effects of different sources of Cu on rumen fermentation
Cu source GP CH4 VFA A:P pH DMd NH3-N MPS Ref.
Cu-Lys ND ND ND ND ND - ND ND [59]
CuSO4 ND ND ND ND ND - ND ND
Cu-Gly ND = = = = ND + ND [77]
Lip.Enc. CuSO4 ND ND - + - = = = = [76]
CuSO4 ND ND ND ND = = ND ND [70]
Cu-Hyd ND ND ND ND = = ND ND
CuSO4 ND ND ND ND = - ND ND [62]
Cu-Hyd ND ND ND ND = = ND ND
CuSO4 = ND = = = = ND = [67]
CuSO4 + = = - = = ND ND [66]
Enc. Cu = = = = = = ND ND
CuSO4 ND ND + + - + - ND [78]
Coat. CuSO4 ND ND + + - + - ND
Cu: copper; GP: Gas production; VFA: Volatile fatty acids; A:P: Acetate to propionate ration; DMd: Dry matter degradability; MPS: Microbial protein synthesis; ↑: high; ↓: low; +: increase; -: decrease; =: no effect; ND: not determined; Cu-Lys: copper lysine; CuSO4: copper sulfate; CuCl2: copper chloride; CuO: copper oxide; CuCO3sulfate. carbonate; Cu-Hyd: copper hydroxychloride; Cu-EDTA: copper disodium edetate; Cu-Prot: copper proteinate; Cu-Acet: copper acetate; Cu-Gly: copper glycinate; Lip.Enc-CuSO4: lipid encapsulated copper sulfate; Enc. Cu: mix of tribasic copper chloride and copper sulfate within a polysaccharide polymer coating; Coat. CuSO4: coated (with hydrogenated fat) copper sulfate.
Table 5. Effects of different sources of Mn on rumen fermentation
Table 5. Effects of different sources of Mn on rumen fermentation
Mn source GP CH4 VFA A:P pH DMd NH3-N MPS Ref.
MnSO4 ND ND ND ND = = ND ND [70]
Mn-Hyd ND ND ND ND = = ND ND
MnCl2 ND ND = = = + = ND [69]
MnSO4 ND ND ND ND = - ND ND [62]
Mn-Hyd ND ND ND ND = = ND ND
MnSO4 - ND = = = - ND = [67]
MnO - ND = = = - ND =
Mn: manganese; GP: Gas production; VFA: Volatile fatty acids; A:P: Acetate to propionate ration; DMd: Dry matter degradability; MPS: Microbial protein synthesis; ↑: high; ↓: low; +: increase; -: decrease; =: no effect; ND: not determined; MnSO4: manganese sulfate; Mn-Hyd: manganese hydroxychloride; MnCl2: manganese chloride; MnO: manganese oxide.
Table 6. Effects of different sources of Zn on rumen fermentation
Table 6. Effects of different sources of Zn on rumen fermentation
Zn source GP CH4 VFA A:P pH DMd NH3-N MPS Ref.
Zn-Gly ND = = = = ND + ND [77]
ZnSO4 ND ND ND ND = = ND ND [70]
Zn-Hyd ND ND ND ND = = ND ND
ZnCl2 ND ND - - - + - - ND [69]
ZnSO4 ND ND ND ND = - ND ND [62]
Zn-Hyd ND ND ND ND = = ND ND
ZnSO4 - ND = = = = ND - [67]
ZnO - ND = = = - ND -
ZnO ND - = - + = - ND [65]
HiZox ND = = + + - = ND
Zn-Prot ND = = = ND + ND ND [80]
Zn-AA - - = ND = = = ND [81]
ZnSO4 ND ND + + = + - ND [24]
Coat. ZnSO4 ND ND + + = + - ND
Zn: zinc; GP: Gas production; VFA: Volatile fatty acids; A:P: Acetate to propionate ration; DMd: Dry matter degradability; MPS: Microbial protein synthesis; ↑: high; ↓: low; +: increase; -: decrease; =: no effect; ND: not determined; Zn-Gly: zinc glycinate; Zn-AA: zinc amino acid complex; ZnSO4: zinc sulfate; Zn-Hyd: zinc hydroxychloride; ZnCl2: zinc chloride; ZnO: zinc oxide; HiZox: high purity potentiated zinc oxide; Coat-ZnSO4: coated (with hydrogenated fat) zinc sulfate.
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