Rumen Solubility of Copper, Manganese and Zinc: Comparison
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The dietary inclusion of trace minerals (TMs), 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 TMs 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.

  • ruminant
  • trace minerals
  • solubility
  • fermentation

1. Introduction

For most species, the absorption site of trace minerals (TMs) is located in the small intestine [1,2][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]. The nutritional feeding systems for ruminants focus mainly on the global animal requirements [3,4][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][5][6]. These TMs 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 playing an important role for reproductive and immune systems [7,8,9][7][8][9]. In addition to the contribution to these metabolic functions, TMs 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][10][11][12]. Intestinal bioavailability of the dietary TMs for ruminants is relatively low, as reported levels are at 4–5%, 1–4% and 15–30% for Cu, Mn and Zn, respectively [3,13[3][13][14],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. 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 [2,6,16,17][2][6][15][16]. The ITM salts such as carbonates, chlorides, oxides and sulfates are characterized as a specific metal (Cu, Mn or Zn) bound to a non-carbon-containing ligand [18,19[17][18][19][20][21],20,21,22], and they are widely available at a low cost. These sources are traditionally used for livestock supplementation [23][22]. The OTMs such as glycinates, amino acid complexes, amino acid chelates or different proteinates are formed through specific processes, binding the metal component (Cu, Mn or Zn) to a carbon-containing ligand [24][23]. The HTMs are defined as a specific metal (Cu, Mn or Zn) bound via a coordinated covalent bond with a hydroxyl ligand and are considered inorganic [14]. However, the covalent bond to an OH group instead of carbon-containing ligands makes HTMs seem like OTMs [25][24]. In ruminant feed, HTMs (Cu, Mn and Zn) are provided in the form of copper hydroxy chloride (Cu-Hyd) [26][25], manganese hydroxy chloride (Mn-Hyd) [27][26] and zinc hydroxy chloride (Zn-Hyd) [28][27]. Other TM forms and sources are studied for ruminant supplementation, including nano-minerals [29][28] or even different seaweeds [30,31][29][30]; however, little research is available on these last forms considering rumen solubility.

3. Trace Mineral Rumen Solubility and Effects on the Ruminal Environment

There are numerous studies addressing the overall effects of TMs 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 source for dietary inclusion, given that it was identified as one of the factors closely related to TM relative bioavailability in ruminants [2,32][2][31]. The solubility of ITMs in rumen fluid was found to be in close relation to their mineral chemical form: sulfates are considered highly soluble compared to oxides [33][32]. OTMs like glycinates, amino acid complexes or different proteinates have a high stability in the 6.0–7.0 pH range (similar to the one found in the rumen environment [34][33]), showing a minimum effect of enzymatic hydrolysis [24][23]. However, their solubility in rumen fluid, exposed to bacterial fermentative activity, could be significantly affected [33][32]. When considering the ruminal solubility of HTMs, they appear to be relatively insoluble; however, results are not equivocal for the hydroxy forms of Cu, Mn and Zn [35][34]. In the following, after an overview of different solubility evaluation methods, 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.

3.1. Ruminal Solubility Evaluation Methods

For an overview of TM solubility, the assessment can be performed through in vitro models with deionized water or a 0.1 N HCl solution as a solvent [36,37][35][36]. However, even though TM solubilization in deionized water or a HCl solution may be a good indicator of the overall solubility of a specific TM, the ruminal solubility of TMs may be affected by the rumen environment, and it was shown to be significantly lower when compared to solubility in deionized water [33][32]. Considering this, when assessing ruminal solubility of TMs 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 and nutrient degradation) [38][37]; however, for TM ruminal solubility evaluation, the techniques are not yet harmonized. One of the applied methods for the assessment of ruminal solubility of TMs following in vitro fermentations (of 24, 48 h or continuous fermentations) is the analysis of TM concentration in a centrifugation supernatant [39,40][38][39]. Based on this method, the final fermentation medium (mix of rumen fluid, buffer, substrate and various TMs) is centrifuged (12,000–18,000× g at 23 °C for 15 min) 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 whole TM quantity recovered in the supernatant) or a relative value (related to a sulfate TM, considered as 100% rumen-soluble). In recent studies [41[40][41],42], the ruminal solubility of various minerals was assessed based on a separation of the final fermentation medium (after 70 h of fermentation) by multiple centrifugations: at 100× g (5 min at 4 °C), to separate an insoluble fraction (containing feed particles, protozoa and insolubilized minerals); the obtained supernatant is then further centrifuged at 18,500× g (20 min at 4 °C) to separate a bacteria-enriched fraction and a final supernatant, containing only solubilized minerals; and the mineral concentration of each centrifugation fraction is then analyzed. Next, the ruminal solubility of TMs can be expressed as a percentage of the solubilized mineral in the final supernatant (based on the total mineral analyzed in the different centrifugation fractions). The ruminal solubility of TMs can also be determined using in vivo models, supplementing rumen-cannulated animals (direct supplementation in the diet or a pulse dose via the cannula) [43][42]. In a study by Arelovich et al. [44][43], the ruminal fluid (100 mL) sampled from rumen-cannulated heifers (supplemented with different levels of TMs), was first filtered with a cheesecloth, acidified (addition of 2 mL of 20% sulfuric acid solution) and centrifuged (16,000× g) to obtain a supernatant (containing the solubilized minerals). The ruminal solubility of TMs was expressed in absolute values based on the TM concentration of the supernatant. In other in vivo studies [35[34][44],45], the ruminal solubility of different TM sources was assessed following a supplementation with different levels of TMs and the analysis of the mineral concentration of the rumen content. Samples of rumen fluid were separated by ultracentrifugation (28,000× g for 30 min at 4 °C) in solid pellets (containing the insolubilized minerals) and a supernatant, considered to contain the rumen-soluble minerals. The ruminal solubility of TMs 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). Other in vivo TM solubility evaluation methods include the in sacco method [46][45], evaluating the rumen disappearance rate of a mineral substrate from rumen-incubated nylon bags (50 µm pore size). However, the method does not allow for the assessment of truly solubilized minerals, only the disappearance from the nylon bags, hence it is not best suited for the evaluation of TM rumen solubility, especially for fine TMs.

3.2. Copper Ruminal Solubility

One of the most commonly used inorganic Cu sources for ruminant supplementation is CuSO4 [14], often used as a comparison basis for rumen solubility with other Cu sources. Table 1 summarizes the available literature data on the ruminal solubility of various Cu sources. In a study by Deters et al. [36][35], the solubility of CuSO4 and glycinate bound Cu (Cu-Gly) in deionized water (at 5.2 pH) was 100% and 68.9%, respectively.
Table 1. Ruminal solubility of different sources of copper (Cu), based on all studies on Cu content analysis of a supernatant obtained after centrifugation of sampled rumen fluid (in vivo studies) or fermentation medium (in vitro studies).
Animals Experimental Model Supplementation Type Cu Dosage Cu Source Solubilization Time/

Supplementation Period		 Centrifugation Ruminal Solubility * Ref.
35][34], 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 the ruminal solubility of TMs reported a high ruminal solubility when supplementing steers with 30, 250 and 470 mg/kg DM of Zn as ZnCl2 [44][43]. 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. [53][52]: 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.

3.5. Trace Mineral Effects on Rumen Fermentation Parameters

When considering rumen fermentation, Cu was identified as a TM with complex responses. Table 4 presents a compilation of various Cu sources’ effects on rumen fermentation parameters.
Table 4.
Effects of different sources of copper on rumen fermentation.
Cu Source pH DMd GP CH4 VFA A:P NH3-N MPS Ref.
Rumen-cannulated steers in vivo Feed inclusion 5 and 25 mg/kg DM CuSO4 12 days 28,000× g ↑; ~17 and 14% [35][34]
Cu-Hyd ↓; ~15 and 9%
Rumen-cannulated steers in vivo
Cu-Met + + + = = + + + [54][53]
Pulse dose via rumen cannula 20 mg/kg DM CuSO4 4, 12 and 24 h 28,000× g ↑; ~68, 30 and 12% after 4, 12 and 24 h following ruminal administration [45][44]
Cu-Hyd ↓; ~15, 20 and 15% after 4, 12 and 24 h following ruminal administration
Rumen-cannulated steers in vitro Fermentation medium 4, 12, 96 mg/kg DM

(with 0.1% DM of S or 2% DM of urea)		 Cu-Lys 24 h 1200× g ↑ (with urea)

↓ (with S)		 [32][31]
CuSO4 ↓ (with S)
Rumen-cannulated dairy cows in vitro Fermentation medium 4 mM solution CuSO4 25 h 2000× g ↑; ~49% [33][32]
CuCl2 + = =
 
Cu: copper; GP: gas production; VFA: volatile fatty acids; A:P: acetate-to-propionate ratio; DMd: dry matter degradability; MPS: microbial protein synthesis; +: increase; -: decrease; =: no effect; Cu-Met: copper methionine; CuCl2: copper chloride; TBCC: tribasic copper chloride; Cu-Lys: copper lysine; CuSO4: copper sulfate; RP-CuSO4: rumen-protected copper sulfate; Cu-Hyd: copper hydroxychloride; 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.
In an in vivo study with rumen-cannulated steers [45][44], 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 [35][34], supplementing a high dosage of Cu (25 mg/kg DM) as CuSO4 decreased, 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. [40][39], it was found that Cu sources (Enc. Cu and CuSO4) did not affect DM degradability, while CuSO4 increased in vitro gas production, propionate concentration and decreased the acetate-to-propionate ratio when compared to Enc. Cu. The two Cu sources did not affect in vitro methanogenesis. In a similar study [59][58], lipid-encapsulated CuSO4 decreased acetate, increased butyrate molar proportion and tended to decrease the acetate-to-propionate proportion, but it did not affect nutrient (DM, organic matter, crude protein and NDF) digestibility when compared to CuSO4. When it comes to Mn’s 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 in 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 [35][34]. 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 [45][44]. Varied results are equally reported when analyzing Mn’s effect on fermentation during in vitro studies with rumen fluid. In a study by Areolovich et al. [44][43], the addition of 100 mg/DM of Mn (as MnCl2) significantly increased DM degradation, without affecting volatile fatty acids’ (VFAs) concentration. In a more recent study [41][40], an overall negative effect of Mn (600 mg/kg DM as MnO or MnSO4) was registered: a decrease in total gas production, DM degradability and butyrate (% of total VFA) concentration. Table 5 presents the effects on rumen fermentation of some Mn sources.
Table 5.
Effects of different sources of manganese on rumen fermentation.
Mn Source pH DMd GP VFA A:P GP CH4NH3-N MPS Ref.
VFA A:P NH3-N MPS Ref.
MnSO4 = =   =
Zn-Gly      [43][42]
=     = = = +   [58][57] = = = + +
Mn-Hyd = =   +      
ZnSO4 = =     =       [43][42] TBCC = = + = = + MnSO4 = ==        =
 
Zn-Hyd[45 =] =     +  [44] CuSO
    4 Mn-Hyd- +   = =  +      + -   [  55][  
ZnSO454]
= =             [45][44] RP-CuSO4 - +     + + -  
MnCl2 = +   = = =   [44][43]
Zn-Hyd = =             Cu-Lys   -       MnSO  4 = -          
ZnSO4[ =35 -][  34]
  -    [32][31] for big particles’ separation; 18,500× g for bacteria and supernatant separation ↑; ~19, 17 and 32% at 22, 46 and 70 h
CuSO4[41]  [40]
-             Mn-Hyd = CuCl2 ↑; ~49%
ZnO ↓; ~10, 9 and 25% at 22, 46 and 70 h CuO ↓; ~9%
CuCO3 ↓; ~19%
Cu-Hyd ↓; ~17%
Cu-EDTA ↑; ~49%
Cu-Prot ↑; ~49%
Cu-Acet ↓; ~33%
Rumen-cannulated dry dairy cows in vitro Fermentation medium 100 and 500 mg/kg DM CuSO4 22, 46 and 70 h 100× g for big particles’ separation; 18,500× g for bacteria and supernatant separation ↑; ~42, 37 and 57% after 22, 46 and 70 h following administration [41][40]
Close-up dairy cows in vitro Fermentation medium 12 mg/kg fresh matter CuSO4 24 h 13,000× g ↑ [40][39]
Enc. Cu ↓
Cu: copper; ↑: high; ↓: low; Cu-Lys: copper lysine; CuSO4: copper sulfate; CuCl2: copper chloride; CuO: copper oxide; CuCO3: copper carbonate; Cu-Hyd: copper hydroxychloride; Cu-EDTA: copper disodium edetate; Cu-Prot: copper proteinate; Cu-Acet: copper acetate; 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.
In a similar study by Clarkson et al. [33][32], 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. In an in vivo study [45][44] 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 ruminal solubility, while Cu-Hyd has a low ruminal solubility. In a similar study by Genther and Hansen [35][34], 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 the rumen solubility of the two Cu sources well; however, the solid fraction, beside undegraded feed fractions and insoluble minerals, also contains rumen microorganisms (protozoa and bacteria), which could have assimilated Cu during the fermentation process. 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 [41][40]. Given the rumen antagonism of Cu with other minerals (mainly sulfur and molybdenum) [33[32][46],47], highly rumen-soluble Cu sources (like CuSO4) often present a decreased bioavailability for ruminants, in relation to antagonist minerals present in the rumen content [16][15]. In order to limit the effect of the rumen environment on mineral additives, various methods, like lipid encapsulation or polymer coating, were developed [48][47]. 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. [40][39] 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).

3.3. Manganese Ruminal Solubility

Given that Mn is poorly absorbed by ruminants [49,50][48][49] and that it is considered that Mn content of the basal diet might cover the rumen microbial requirements [51][50], little research is focused on the ruminal solubility of different Mn sources. In a study by Caldera et al. [45][44], 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 h 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 h, the Mn content of the supernatant was approximately 0.3 and 0.5 mg/L, while that of the solid fraction was approximately 14.0 and 9.0 mg/kgDM with MnSO4 and Mn-Hyd, respectively. Furthermore, the reported relative solubility after 4 h was about 20% and 10%, and after 24 h, it was about 6 and 15% for MnSO4 and Mn-Hyd, respectively. These findings indicate that both Mn sources (MnSO4 and Mn-Hyd) are not highly 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) [35][34]. In an in vitro study, the ruminal solubility of two inorganic Mn sources (MnSO4 and MnO) was assessed [41][40]. Results showed that MnSO4 and MnO are equally soluble in the rumen fluid after 70 h of fermentation. However, when solubility was assessed at a shorter period (22 h), MnSO4 showed a higher solubility when compared to MnO. The ruminal solubility of various Mn sources is summarized in Table 2.
Table 2. Ruminal solubility of different sources of manganese (Mn), based on all studies on Mn content analysis of a supernatant obtained after centrifugation of sampled rumen fluid (in vivo studies) or fermentation medium (in vitro studies).
Animals Experimental Model Supplementation Type Mn Dosage Mn Source Solubilization Time/

Supplementation Period		 Centrifugation Ruminal Solubility * Ref.
Zn Dosage Zn Source Solubilization Time/

Supplementation Period Centrifugation Ruminal Solubility * Ref.
Rumen-cannulated steers in vivo Pulse dose via rumen cannula 40 mg/kg DM MnSO4 4, 12 and 24 h 28,000× g ↑; ~20, 12 and 6% after 4, 12 and 24 h following ruminal administration [45
Rumen-cannulated steers in vivo] Pulse dose via rumen cannula 60 mg/kg DM ZnSO4 4, 12 and 24 h 28,000× g[44]
↑; ~39, 15 and 15% after 4, 12 and 24 h following ruminal administration [45][44] Mn-Hyd ↓; ~10, 7 and 15% after 4, 12 and 24 h following ruminal administration
Zn-Hyd ↓; ~10, 5 and 10% after 4, 12 and 24 h following ruminal administration Rumen-cannulated heifers in vivo Feed inclusion 40 mg/kg DM MnCl2 16 days 16,000× g ↓ [
Rumen-cannulated heifers in vivo44 Feed inclusion 30, 250 and 470 mg/kg DM ZnCl2 16 days 16,000× g][ ↑; linear increase in Zn concentration in the rumen fluid (2.26, 7.6 and 11.6 mg/L)43]
[44][43] Rumen-cannulated steers in vivo Pulse dose via rumen cannula 400 mg/kg DM MnSO4 24 h 28,000× g ↓ at 10 h following ruminal administration [52↓ at 10 h; ↑ at 14 h following ruminal administration
Rumen-cannulated steers in vivo Feed inclusion] 30 and 120 mg/kg DM[51 ZnSO4]
12 days 28,000× g ↓; ~12 and 7% [35][34] Mn-Hyd ↑ at 10 h following ruminal administration
Zn-Hyd ↑; ~14 and 11% Mn-Met
Rumen-cannulated dairy cows in vitro Fermentation

medium		 240 mg/kg DM ZnO 24 h 10,000× g; supernatant filtered (Grade 389 ashless filters) ↑; 65.3% (without clay);

↓; 16.5% (with clay)		 [53][52]   [ Rumen-cannulated heifers
52][51] Rumen-cannulated dry dairy cowsin vivo Pulse dose via rumen cannula in vitro Fermentation

medium40 mg/kg DM		 MnSO
Zn-Hyd4 24 h 28,000× g ↑ at 4 and 6 h; ↓ at 18 h following ruminal administration =[43] 500 mg/kg DM ZnSO +4  [42]
22, 46 and 70 h   =100× g     Mn-Hyd ↓ at 4 and 6 h; ↑ at 18 h following ruminal administration
    + + = +
Zn-Met = =  [56][55]   =       Rumen-cannulated steers in vivo Feed inclusion 15 and 60 mg/kg DM MnSO4 Rumen-cannulated dry dairy cows12 days in vitro28,000× g Fermentation

medium
Coat. CuSO↑; ~62 and 65% at 15 and 60 mg/kg DM [35][34]
30 and 120 mg/kg DM 4ZnO Mn-Hyd ↓; ~50 and 66%at 15 and 60 mg/kg DM
Rumen-cannulated dry dairy cows in vitro Fermentation medium 600 mg/kg DM MnSO4 22, 46 and 70 h 100× g for big particles’ separation; 18,500× g for bacteria and supernatant separation ↑; ~94, 91 and 93% at 22, 46 and 70 h [41][40]
MnO ↑; ~84, 88 and 93% at 22, 46 and 70 h
Mn: Manganese; ↑: high; ↓: low; MnSO4: manganese sulfate; Mn-Hyd: manganese hydroxychloride; MnCl2: manganese chloride; Mn-Met: manganese methionine; MnO: manganese oxide; * Ruminal solubility: where available, values of relative solubility were given.

3.4. Zinc Ruminal Solubility

In a recent in vitro study [41][40], 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% of ZnSO4 and ZnO, respectively, were 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. [39][38] 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). Table 3 summarizes the ruminal solubility of various Zn sources.
Table 3. Ruminal solubility of different sources of zinc (Zn), based on all studies on Zn content analysis of a supernatant obtained after centrifugation of sampled rumen fluid (in vivo studies) or fermentation medium (in vitro studies).
Animals Experimental Model Supplementation Type
8 days continuous culture fermentation
=
12,000×
g
+     +↓ [39][38]
+     [57] HiZox ↑
Zn: Zinc; ↑: high; ↓: low; ZnSO4: zinc sulfate; Zn-Hyd: zinc hydroxychloride; ZnCl2: zinc chloride; ZnO: zinc oxide; HiZox: high-purity potentiated zinc oxide; * Ruminal solubility: where available, values of relative solubility were given.
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 h was 15 and 10% for ZnSO4 and Zn-Hyd, respectively [45][44]. In a similar study by Genther and Hansen [
=
 
 
     
    CuSO4 = + MnSO4 = -  - = =   = [
[56]
41][
ZnCl2 = -     - - -   [44][43] Cu-Gly =     = = = +   [
ZnSO4 = -        58][57]
40]     [35][34] Lip.Enc. CuSO4 = =     - - = = [59][58]
CuSO4 = =             [45][44]
Cu-Hyd = =            
MnO = - - = =   =
MnSO4 = -   -       [52][51]
Mn-Hyd = +   +      
Zn-Hyd = =             Mn-Met = =   +    
ZnSO4  = = -   = =   - [41][40]
ZnO = - -   = =   - CuSO4 = -            
ZnO +[35][34]
=   - = - -   [39][38] Cu-Hyd = =  
HiZox + -        = = +   
=   CuSO4 = = =   = =   =
Zn-Prot  [41][40]
+   = = =     [62][61] CuSO4 = = + = = -     [40][39]
Zn-AA = = - - =   =   [63][62 Enc. Cu = = = = = =    
CuSO4 - +     + + -   [60][59]
Coat. CuSO4 - +     + + -
Mn: manganese; GP: gas production; VFA: volatile fatty acids; A:P: acetate-to-propionate ratio; DMd: dry matter degradability; MPS: microbial protein synthesis; +: increase; -: decrease; =: no effect; MnSO4: manganese sulfate; Mn-Hyd: manganese hydroxychloride; MnCl2: manganese chloride; MnO: manganese oxide; Mn-Met: manganese methionine.
Regarding Zn’s 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 [61][60]. 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. [39][38], it was shown that an addition of 30 or 120 mg/kg DM of Zn as ZnO or HiZnox (a greater purity potentiated ZnO) affects the fermentation parameters differently: HiZnox reduced the apparent DM disappearance and increased the acetate-to-propionate ratio; and ZnO reduced the acetate, NH3-N and CH4 concentration, while both Zn sources increased culture pH. In another in vitro study [41][40], the total gas production and DM degradability were 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 the acetate-to-propionate ratio nor CH4 concentration [62][61]. Table 6 compiles the effects on fermentation parameters of various inorganic and organic Zn sources.
Table 6.
Effects of different sources of zinc on rumen fermentation.
Zn Source pH DMd
]
ZnSO
4
=
+
 
 
+
+
-   [64][63]
Coat. ZnSO4 = +     + + -  
Zn: zinc; GP: gas production; VFA: volatile fatty acids; A:P: acetate-to-propionate ratio; DMd: dry matter degradability; MPS: microbial protein synthesis; +: increase; -: decrease; =: no effect; Zn-Gly: zinc glycinate; ZnSO4: zinc sulfate; Zn-Hyd: zinc hydroxychloride; Zn-Met: zinc methionine; ZnCl2: zinc chloride; ZnO: zinc oxide; HiZox: high-purity potentiated zinc oxide; Zn-Prot: zinc proteinate; Zn-AA: zinc amino acid complex; Coat. ZnSO4: coated (with hydrogenated fat) zinc sulfate.

3.6. Trace Mineral Effects on Rumen Microbiota

Studies addressing TMs’ 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 the rumen bacterial community differently. As shown by Ishaq et al. [65][64], the 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) [63][62]. Furthermore, significant shifts in the relative abundance of fibrolytic bacteria populations, such as an increase in Ruminococcus albus and a decrease in Ruminococcus flavefaciens or an increase in lactic acid-producing bacteria (Streptococcus bovis), were noted, while the methanogenic Archaea abundance was not affected by Zn-AA supplementation [63][62]. 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 [64][63]. Regarding Cu’s 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 it decreased the populations of Prevotella ruminicola, Ruminobacter amylophilus and α-amylase activity [60][59]. The effects of inorganic and organic Mn on the rumen microbial ecosystem were observed in a study with ewe lambs [66][65]. 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 show effects, 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 the 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 1051.8 mg/kg DM of Cu, Mn and Zn, respectively) [67,68][66][67]. Following the supplementation of lactating yaks with inorganic TMs 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 [69][68]. In a recent study with heat-stressed dairy steers [58][57], supplementing high levels of organic TMs (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 [58][57].

 

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