Seasonal Biochemical Variations in Mediterranean Halophytes and Salt-Tolerant Plants: Targeting Sustainable Innovations in Ruminant Health
Abstract
1. Introduction
2. Materials and Methods
2.1. Plant Collection and Processing
2.2. Nutritional Assessments
2.3. Preparation of the Extracts
2.4. Total Phenolic (TPC), Flavonoid (TFC), and Condensed Tannin Contents (CTCs) of the Extracts
2.5. Phenolics Profiling by High-Performance Liquid Chromatography–Diode Array (HPLC-DAD)
2.6. In Vitro Antioxidant Properties
2.7. Statistical Analysis
3. Results
3.1. Nutritional Assessments
3.2. Phenolic Profiling and Antioxidant Properties
3.3. Principal Component Analysis (PCA) and Relative Antioxidant Capacity Index (RACI)
3.4. Individual Phenolic Composition
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
Sp | Spring; |
Su | Summer; |
Au | Autumn; |
Wi | Winter; |
CCMAR | Centre of Marine Sciences; |
UAlg | University of Algarve; |
ICNF | Instituto da Conservação da Natureza e das Florestas; |
DM | Dry matter; |
N | Total nitrogen; |
CP | Crude protein; |
TL | Total lipid; |
Ca | Calcium; |
K | Potassium; |
Na | Sodium; |
Mg | Magnesium; |
Cu | Copper; |
Zn | Zinc; |
Mn | Manganese; |
Fe | Iron; |
Se | Selenium; |
MP-AES | Microwave plasma atomic emission spectrometer; |
CHO | Total carbohydrate; |
GE | Gross energy; |
DMSO | Dimethyl sulfoxide; |
TPC | Total phenolic content; |
TFC | Total flavonoid content; |
CTC | Condensed tannin content; |
DMACA-HCl | 4-Dimethylaminocinnamaldehyde-hydrochloric acid; |
GAE | Gallic acid equivalent; |
QE | Quercetin equivalent; |
CE | Catechin equivalent; |
DW | Dry weight; |
RSA | Radical scavenging activity; |
CCA | Copper chelation assay; |
ICA | Iron chelation assay; |
BHT | Butylated hydroxytoluene; |
EDTA | Ethylenediamine tetraacetic acid; |
FRAP | Ferric reducing antioxidant power; |
SEM | Standard error of the mean; |
IC50 | Half inhibitory concentration; |
RACI | Relative antioxidant capacity index; |
PCA | Principal component analysis; |
HI | Helichrysum italicum picardii; |
PL | Pistacia lentiscus; |
LM | Limoniastrum monopetalum; |
CM | Cladium mariscus; |
CS | Calystegia soldanella; |
PC | Plantago coronopus; |
CC | Crucianella maritima; |
MM | Medicago marina; |
IC | Inula crithmoides. |
Appendix A
Species (Family) (Voucher No.) | Location | Season | Date | Organs |
Min. Temp. (ºC) |
Max. Temp. (ºC) |
Total Rainfall (mm) |
---|---|---|---|---|---|---|---|
Helichrysum italicum subsp. picardii (Asteraceae) (XBH32) | Tavira 37°07′51.8″ N, 7°36′37.6″ W | Sp | Apr/2017 | L/S | 14 | 24 | 25 |
Su | Jul/2017 | L/S/FL | 18 | 30 | 1 | ||
Au | Oct/2017 | L/S/FL | 14 | 26 | 25 | ||
Wi | Jan/2018 | L/S | 6 | 16 | 50 | ||
Inula crithmoides (Asteraceae) (XBH04) | Olhão 37°01′11.7″ N, 7°53′04.8″ W | Sp | Apr/2017 | L/S | 14 | 24 | 25 |
Su | Jul/2017 | L/S | 18 | 30 | 1 | ||
Au | Oct/2017 | L/S/FL | 16 | 26 | 25 | ||
Wi | Jan/2018 | L/S | 6 | 16 | 50 | ||
Pistacia lentiscus (Anacardiaceae) (XBH06) | Portimão 37°07′34.7″ N, 8°36′02.3″ W | Sp | Apr/2017 | L/S | 10 | 24 | 10 |
Su | Jul/2017 | L/S | 14 | 30 | 1 | ||
Au | Oct/2017 | L/S/FR | 12 | 26 | 10 | ||
Wi | Jan/2018 | L/S/FR | 2 | 16 | 100 | ||
Cladium mariscus (Cyperaceae) (XBH03) | Faro 37°01′03.3″ N, 7°59′18.1″ W | Sp | Apr/2017 | L | 14 | 22 | 25 |
Su | Jul/2017 | L/I | 18 | 30 | 1 | ||
Au | Oct/2017 | L/I | 16 | 26 | 25 | ||
Wi | Jan/2018 | L | 6 | 16 | 50 | ||
Calystegia soldanella (Convolvulaceae) (XBH07) | Portimão 37°07′23.1″ N, 8°36′10.7″ W | Sp | Apr/2018 | L/S/FL | 10 | 20 | 10 |
Su | Jul/2018 | L/S | 12 | 26 | 1 | ||
Au | Oct/2017 | L/S | 12 | 26 | 10 | ||
Wi | Jan/2018 | L/S/FL | 2 | 16 | 100 | ||
Medicago marina (Fabaceae) (XBH41) | Portimão 37°07′23.1″ N, 8°36′10.7″ W | Sp | Apr/2018 | L/S/FL | 10 | 20 | 10 |
Su | Jul/2018 | L/S/FR | 12 | 26 | 1 | ||
Au | Oct/2017 | L/S | 12 | 26 | 10 | ||
Wi | Jan/2018 | L/S | 2 | 16 | 100 | ||
Plantago coronopus (Plantaginaceae) (XBH02) | Olhão 37°01′32.8″ N, 7°53′04.4″ W | Sp | Apr/2018 | L/S/FL | 12 | 20 | 100 |
Su | Jul/2018 | L/S/FL | 16 | 26 | 1 | ||
Au | Oct/2017 | L/S/FL | 16 | 26 | 25 | ||
Wi | Jan/2018 | L | 6 | 16 | 50 | ||
Limoniastrum monopetalum (Plumbaginaceae) (XBH05) | Portimão 37°07′34.7″ N, 8°36′02.3″ W | Sp | Apr/2017 | L/S | 10 | 24 | 10 |
Su | Jul/2017 | L/S/FL | 14 | 30 | 1 | ||
Au | Oct/2017 | L/S | 12 | 26 | 10 | ||
Wi | Jan/2018 | L/S | 2 | 16 | 100 | ||
Crucianella maritima (Rubiaceae) (XBH40) | Portimão 37°07′23.2″ N, 8°36′12.3″ W | Sp | Apr/2017 | L/S | 10 | 24 | 10 |
Su | Jul/2017 | L/S/FL | 14 | 30 | 1 | ||
Au | Oct/2017 | L/S | 12 | 26 | 10 | ||
Wi | Jan/2018 | L/S | 2 | 16 | 100 |
Species | Season | Nutritional Parameters | Energy | Mineral Content | |||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
DM | CP | A | TL | CHO | GE | Ca | K | Mg | Na | Cu | Fe | Mn | Zn | ||
Helichrysum italicum subsp. picardi (Asteraceae) | Sp | 314.6 | 87.6 | 58.1 | 99.6 | 754.6 | 4.6 | 11.7 | 12.7 | 1.5 | 3.2 | 17.1 | 330.2 | 64.0 | 58.0 |
Su | 458.6 | 42.5 | 55.1 | 90.9 | 811.5 | 4.5 | 10.8 | 15.0 | 1.6 | 2.7 | 13.7 | 138.8 | 52.7 | 42.2 | |
Au | 549.4 | 39.4 | 61.2 | 142.7 | 756.7 | 4.7 | 13.4 | 9.7 | 1.4 | 2.4 | 15.6 | 325.9 | 67.4 | 53.5 | |
Wi | 496.3 | 60.0 | 67.6 | 137.8 | 734.7 | 4.7 | 14.7 | 7.0 | 1.4 | 3.0 | 19.6 | 405.2 | 71.0 | 60.9 | |
Inula crithmoides (Asteraceae) | Sp | 97 | 95.7 | 269.0 | 61.1 | 574.2 | 3.5 | 11.8 | 12.0 | 10.6 | 79.4 | 5.8 | 207.3 | 14.8 | 14.3 |
Su | 161.8 | 90.5 | 326.6 | 74.2 | 508.7 | 3.3 | 10.8 | 9.5 | 10.0 | 91.5 | 5.5 | 235.5 | 13.0 | 13.8 | |
Au | 124.6 | 65.6 | 240.6 | 87.7 | 606.0 | 3.7 | 12.9 | 12.1 | 7.6 | 67.2 | 7.7 | 452.9 | 14.4 | 20.3 | |
Wi | 104.3 | 91.4 | 324.9 | 79.0 | 504.7 | 3.4 | 11.0 | 10.8 | 6.6 | 97.7 | 4.0 | 227.8 | 12.6 | 20.5 | |
Pistacia lentiscus (Anacardiaceae) | Sp | 484.5 | 60.1 | 63.0 | 67.5 | 809.4 | 4.4 | 24.2 | 9.2 | 1.9 | 1.2 | 2.3 | 43.0 | 9.9 | 16.7 |
Su | 494.6 | 74.5 | 50.2 | 77.3 | 798.1 | 4.5 | 13.2 | 13.5 | 1.4 | 1.5 | 2.8 | 48.0 | 8.9 | 9.3 | |
Au | 479.9 | 52.5 | 55.1 | 106.7 | 785.7 | 4.6 | 18.5 | 11.8 | 1.9 | 1.5 | 1.8 | 61.0 | 8.2 | 8.0 | |
Wi | 504.3 | 66.4 | 50.8 | 94.9 | 787.9 | 4.6 | 21.6 | 8.5 | 1.8 | 1.6 | 1.9 | 62.9 | 9.4 | 9.1 | |
Calystegia soldanela (Convolvulaceae) | Sp | 121.4 | 97.3 | 110.2 | 250.1 | 542.5 | 5.2 | 17.5 | 21.5 | 2.2 | 7.1 | 2.3 | 239.8 | 12.4 | 28.3 |
Su | 84.3 | 67.2 | 128.4 | 166.0 | 638.4 | 4.6 | 33.6 | 5.0 | 6.1 | 19.0 | 1.2 | 75.1 | 28.6 | 45.8 | |
Au | 163.3 | 102.5 | 178.9 | 141.9 | 576.7 | 4.3 | 31.3 | 7.4 | 6.2 | 30.9 | 5.4 | 57.0 | 33.1 | 45.5 | |
Wi | 224.6 | 189.4 | 161.9 | 148.8 | 499.8 | 4.6 | 17.6 | 28.7 | 3.1 | 23.5 | 12.8 | 74.8 | 15.3 | 48.5 | |
Cladium mariscus (Cyperaceae) † | Sp | 449.1 | 87.3 | 71.7 | 53.3 | 787.8 | 4.3 | 6.9 | 4.4 | 0.8 | 8.1 | 3.9 | 186.0 | 40.7 | 15.2 |
Su | 585.5 | 51.8 | 49.4 | 48.9 | 850.0 | 4.3 | 1.6 | 3.9 | 0.7 | 1.4 | 7.7 | 214.0 | 20.0 | 21.1 | |
Au | 559.1 | 54.5 | 82.9 | 52.9 | 809.8 | 4.2 | 3.8 | 2.3 | 0.7 | 5.7 | 5.9 | 42.8 | 29.1 | 20.4 | |
Wi | 469.4 | 57.8 | 75.1 | 51.1 | 816.0 | 4.2 | 3.8 | 2.4 | 0.7 | 4.9 | 9.6 | 32.3 | 49.0 | 24.7 | |
Medicago marina (Fabaceae) | Sp | 376.6 | 132.7 | 68.5 | 53.8 | 745.1 | 4.4 | 22.3 | 8.0 | 1.6 | 5.3 | 1.6 | 162.7 | 10.2 | 22.0 |
Su | 307 | 79.4 | 71.6 | 55.1 | 793.9 | 4.3 | 28.2 | 4.7 | 2.9 | 8.5 | 2.9 | 94.3 | 11.1 | 34.5 | |
Au | 271.8 | 66.9 | 85.7 | 53.0 | 794.5 | 4.2 | 28.8 | 2.1 | 1.9 | 11.7 | 3.8 | 380.6 | 12.8 | 45.3 | |
Wi | 400.2 | 139.4 | 67.1 | 45.9 | 747.7 | 4.4 | 21.9 | 7.7 | 2.0 | 6.7 | 2.9 | 140.3 | 14.0 | 41.7 | |
Plantago coronopus (Plantaginaceae) | Sp | 251.6 | 87.6 | 129.1 | 74.6 | 708.7 | 4.2 | 19.7 | 9.8 | 2.5 | 17.6 | 4.6 | 430.8 | 31.3 | 34.1 |
Su | 127.6 | 71.5 | 154.7 | 81.0 | 692.8 | 4.1 | 23.9 | 8.1 | 3.3 | 22.8 | 7.5 | 328.2 | 17.1 | 66.7 | |
Au | 152.5 | 63.9 | 149.1 | 71.5 | 715.5 | 4.0 | 20.2 | 5.3 | 3.1 | 19.9 | 10.5 | 499.9 | 17.3 | 38.9 | |
Wi | 280.9 | 116.1 | 151.3 | 76.9 | 655.6 | 4.1 | 32.5 | 7.4 | 2.4 | 23.0 | 4.9 | 116.3 | 12.6 | 25.8 | |
Limoniastrum monopetalum (Plumbaginaceae) | Sp | 291.3 | 108.7 | 180.5 | 44.1 | 666.7 | 3.8 | 41.0 | 7.2 | 9.8 | 31.0 | 0.8 | 68.2 | 10.5 | 26.7 |
Su | 374.2 | 60.6 | 148.3 | 35.7 | 755.4 | 3.8 | 36.8 | 5.9 | 6.9 | 27.0 | 1.1 | 57.6 | 9.9 | 10.2 | |
Au | 495.5 | 62.8 | 187.1 | 34.4 | 715.8 | 3.7 | 58.2 | 7.9 | 12.9 | 13.3 | 1.8 | 92.9 | 15.6 | 9.1 | |
Wi | 322.8 | 108.3 | 204.8 | 43.7 | 643.2 | 3.7 | 60.4 | 7.4 | 15.3 | 17.0 | 2.6 | 64.7 | 16.4 | 20.3 | |
Crucianella maritima (Rubiaceae) | Sp | 174.8 | 65.6 | 125.3 | 54.7 | 754.4 | 4.1 | 9.2 | 11.7 | 3.4 | 11.8 | 4.5 | 346.9 | 27.2 | 36.9 |
Su | 473.3 | 47.0 | 130.0 | 75.9 | 747.0 | 4.1 | 3.4 | 8.9 | 5.0 | 8.8 | 4.7 | 284.4 | 34.5 | 32.3 | |
Au | 573.9 | 47.2 | 130.0 | 66.6 | 756.2 | 4.1 | 3.4 | 4.8 | 5.3 | 5.9 | 6.4 | 388.7 | 45.4 | 29.5 | |
Wi | 359.9 | 59.2 | 127.1 | 74.0 | 739.7 | 4.1 | 2.4 | 10.1 | 2.5 | 4.8 | 6.1 | 451.5 | 58.0 | 54.0 |
Species | Season | CCA | DPPH | FRAP | ABTS | ||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Helichrysum italicum subsp. picardi (Asteraceae) | Sp | >1 | 0.43 | ± | 0.01 c | 0.74 | ± | 0.11 b | 0.63 | ± | 0.13 a,b | ||
Su | >1 | 0.29 | ± | 0.01 a,b | 0.32 | ± | 0.02 a | 0.30 | ± | 0.02 a | |||
Au | >1 | 0.27 | ± | 0.00 a | 0.45 | ± | 0.04 a | 0.30 | ± | 0.06 a | |||
Wi | >1 | 0.33 | ± | 0.01 b | 0.40 | ± | 0.03 a | 0.86 | ± | 0.14 b | |||
Pistacia lentiscus (Anacardiaceae) | Sp | 0.18 | ± | 0.02 a | 0.03 | ± | 0.01 a | 0.07 | ± | 0.00 a,b | 0.03 | ± | 0.00 a |
Su | 0.13 | ± | 0.02 a | 0.04 | ± | 0.01 a | 0.07 | ± | 0.00 a,b | 0.04 | ± | 0.00 a,b | |
Au | 0.18 | ± | 0.02 a | 0.04 | ± | 0.00 a | 0.09 | ± | 0.01 b | 0.04 | ± | 0.01 b | |
Wi | 0.17 | ± | 0.01 a | 0.03 | ± | 0.00 a | 0.05 | ± | 0.00 a | 0.03 | ± | 0.00 a | |
Cladium mariscus † (Cyperaceae) | Sp | >1 | 0.30 | ± | 0.00 a | 0.25 | ± | 0.02 a | 0.29 | ± | 0.03 b | ||
Su | >1 | 0.24 | ± | 0.02 a | 0.21 | ± | 0.03 a | 0.12 | ± | 0.01 a | |||
Au | >1 | 0.25 | ± | 0.01a | 0.18 | ± | 0.05 a | 0.20 | ± | 0.02 a,b | |||
Wi | >1 | 0.26 | ± | 0.03 a | 0.27 | ± | 0.01 a | 0.23 | ± | 0.03 b | |||
Plantago coronopus (Plantaginaceae) | Sp | >1 | 0.25 | ± | 0.02 a,b | 0.23 | ± | 0.01 a | 0.47 | ± | 0.06 a | ||
Su | >1 | 0.30 | ± | 0.03 b | 0.29 | ± | 0.01 a | 0.55 | ± | 0.13 a | |||
Au | >1 | 0.20 | ± | 0.03 a | 0.32 | ± | 0.05 a | 0.40 | ± | 0.10 a | |||
Wi | >1 | 0.17 | ± | 0.02 a | 0.20 | ± | 0.01 a | 0.33 | ± | 0.04 a | |||
Limoniastrum monopetalum (Plumbaginaceae) | Sp | 0.65 | ± | 0.03 a | 0.12 | ± | 0.01 a | 0.09 | ± | 0.01 a | 0.11 | ± | 0.02 a,b |
Su | 0.58 | ± | 0.03 a | 0.12 | ± | 0.01 a | 0.13 | ± | 0.01 a,b | 0.06 | ± | 0.01 a | |
Au | 0.92 | ± | 0.11 b | 0.18 | ± | 0.00 b | 0.18 | ± | 0.03 b | 0.15 | ± | 0.02 a,b | |
Wi | 0.66 | ± | 0.04 a,b | 0.14 | ± | 0.01 a | 0.11 | ± | 0.01 a,b | 0.16 | ± | 0.03 b |
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Rt (min) | No. | Compound | P. lentiscus Wi | H. italicum Su | C. mariscus Su † | P. coronopus Wi | L. monopetalum Su |
---|---|---|---|---|---|---|---|
2.6 | 1 | Gallic acid | 13.81 | <0.01 | 0.01 | <0.01 | 3.79 |
4.6 | 2 | 3.4-Dihydroxybenzoic acid | 0.22 | 0.36 | n.d. | 0.33 | 0.27 |
5.4 | 3 | Neochlorogenic acid | 0.39 | 2.52 | n.d. | 0.07 | 0.52 |
8.1 | 4 | Gentisic acid | 33.80 | 5.53 | 3.79 | ||
8.4 | 5 | p-Hidroxybenzoic acid | 0.17 | <0.01 | |||
9.9 | 6 | Catechin hydrate | 2.43 | 1.92 | 0.77 | 0.12 | |
10.0 | 7 | 4-Hydroxybenzaldehyde | <0.01 | ||||
10.7 | 8 | 3-Hydroxybenzoic acid | 0.84 | 0.19 | n.d. | 0.14 | 1.24 |
11.6 | 9 | Vanillic acid | 12.62 | 0.14 | 0.05 | 0.41 | |
12.2 | 10 | Chlorogenic acid | 1.29 | 9.12 | 2.96 | 2.12 | |
12.3 | 11 | 4-O-Caffeoylquinic acid | n.d. | 1.76 | |||
12.6 | 12 | Caffeic acid | 0.74 | 0.89 | 0.73 | 0.76 | 6.79 |
13.5 | 13 | Syringic acid | 2.62 | 0.35 | |||
13.6 | 14 | Epigallocatechin gallate | 0.05 | <0.01 | 0.72 | ||
13.9 | 15 | Epicatechin | 25.59 | 2.38 | 0.88 | 0.51 | 0.57 |
14.9 | 16 | Ourateacatechin | 34.72 | 1.76 | n.d. | 0.41 | 0.95 |
15.2 | 17 | Umbelliferone | 0.15 | n.d. | 0.41 | 0.05 | |
15.9 | 18 | Coumaric acid | <0.01 | 0.16 | <0.01 | 1.19 | 0.40 |
16.8 | 19 | Taxifolin | n.d. | 0.36 | |||
16.9 | 20 | Coumarin | 0.01 | n.d. | |||
17.0 | 21 | Ferulic acid | 0.51 | 1.38 | 0.81 | 0.06 | |
17.6 | 22 | Salicylic acid | 2.59 | 1.64 | 5.36 | 0.48 | |
19.1 | 23 | Naringenin-7-glucoside | 2.78 | 0.82 | 0.01 | 1.18 | |
20.3 | 24 | Luteolin-7-O-glucoside | 5.47 | 3.58 | 0.46 | 5.36 | 0.23 |
21.3 | 25 | Rosmarinic acid | 0.60 | 0.12 | 0.58 | ||
21.4 | 26 | Rutin | 0.54 | 0.09 | |||
22.2 | 27 | Ellagic acid | 0.24 | 0.26 | <0.01 | ||
22.6 | 28 | Cinnamic acid | 0.21 | 0.38 | n.d. | 0.26 | 0.34 |
25.9 | 29 | Quercetin | 0.06 | 0.03 | 0.07 | ||
28.8 | 30 | Morin | 0.03 | n.d. | |||
31.7 | 31 | Flavone | |||||
32.6 | 32 | Chrysin | 0.12 | n.d. | |||
∑Phenolics | 138.91 | 27.91 | 9.22 | 23.03 | 25.43 |
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Oliveira, M.; Pereira, C.G.; Castañeda-Loaiza, V.; Rodrigues, M.J.; Neng, N.R.; Hoste, H.; Ben Hamed, K.; Custódio, L. Seasonal Biochemical Variations in Mediterranean Halophytes and Salt-Tolerant Plants: Targeting Sustainable Innovations in Ruminant Health. Appl. Sci. 2025, 15, 7625. https://doi.org/10.3390/app15147625
Oliveira M, Pereira CG, Castañeda-Loaiza V, Rodrigues MJ, Neng NR, Hoste H, Ben Hamed K, Custódio L. Seasonal Biochemical Variations in Mediterranean Halophytes and Salt-Tolerant Plants: Targeting Sustainable Innovations in Ruminant Health. Applied Sciences. 2025; 15(14):7625. https://doi.org/10.3390/app15147625
Chicago/Turabian StyleOliveira, Marta, Catarina Guerreiro Pereira, Viana Castañeda-Loaiza, Maria João Rodrigues, Nuno R. Neng, Hervé Hoste, Karim Ben Hamed, and Luísa Custódio. 2025. "Seasonal Biochemical Variations in Mediterranean Halophytes and Salt-Tolerant Plants: Targeting Sustainable Innovations in Ruminant Health" Applied Sciences 15, no. 14: 7625. https://doi.org/10.3390/app15147625
APA StyleOliveira, M., Pereira, C. G., Castañeda-Loaiza, V., Rodrigues, M. J., Neng, N. R., Hoste, H., Ben Hamed, K., & Custódio, L. (2025). Seasonal Biochemical Variations in Mediterranean Halophytes and Salt-Tolerant Plants: Targeting Sustainable Innovations in Ruminant Health. Applied Sciences, 15(14), 7625. https://doi.org/10.3390/app15147625