Salt tolerance

Salt is one of the main abiotic stresses affecting crop yields around the world (Zörb et al., Reference Zörb, Geilfus and Dietz2019). Seed germination is one of the most sensitive physiological phenomena to stress in the lifecycle of plants (Al-Turki et al., Reference Al-Turki, Davy, Al-Ammari and Basahi2022), and seeds of O. viciifolia withstand moderate saline environments (up to 400 mM). In this sense, seeds of O. viciifolia retain germinability under high salinity, displaying tolerance mechanisms such as physiological dormancy till the occurrence of favourable conditions (Li et al., Reference Li, Wu and Sexton2021a, Reference Li, Zhu, White, Wei and Wu2021b). Karamian and Ataei-Barazande (Reference Karamian and Ataei-Barazande2013) reported decreasing germination rates in O. viciifolia with increasing salinity levels over 200 mM NaCl and indicated that germination was totally inhibited at 400 mM NaCl which is higher than for Trifolium repens L. (up to 180 mM) (Chu et al., Reference Chu, Gao, Chen, McCullough, Jespersen, Sapkota, Bagavathiannan and Yu2022), Trifolium pratense L. (up to 240 mM) (Asci, Reference Asci2011) and M. sativa (up to 257 mM) (Kadri et al., Reference Kadri, Chaabena, Abdelguerfi and Laouar2021). The germination of O. viciifolia is considered more tolerant to salinities c. 170 mM NaCl than other Onobrychis species (Uzun et al., Reference Uzun, Avci, Ozcan and Sancak2017).

Saline-alkaline conditions resulted in oxidative stress and the accumulation of proline in seedlings of O. viciifolia (Wu et al., Reference Wu, Li, Zhu and Li2021). Along with organic osmolytes, O. viciifolia under salinity also increased the production of reactive oxygen species (ROS) scavengers such as catalase, superoxide dismutase, glutathione reductase and ascorbate peroxidase (Beyaz, Reference Beyaz2019). In fact, O. viciifolia can grow without much yield and quality loss in salt-affected areas (c. 109 mM NaCl), where it can provide enough high-quality forage production for livestock without altering its macro-mineral content (Temel et al., Reference Temel, Keskin, Şimşek and Yilmaza2016a, Reference Temel, Keskin, Şimşek and Yilmaza2016b) (Fig. 3a). Nonetheless, Wu et al. (Reference Wu, Feng, Li and Du2017a, Reference Wu, Feng, Wang and Du2017b) reported reduced growth and chlorophyll and water contents, diminished root potassium concentration, and increased malondialdehyde (MDA) concentration and relative membrane permeability in O. viciifolia shoots under salinity (100 mM NaCl). This study also reported that, when supplied exogenously, proline and silicon improved salt stress tolerance in O. viciifolia by mitigating sodium toxicity (Fig. 3a). Under salinity, O. viciifolia maintain better cellular function and overall physiological homoeostasis evidenced by less drastic imbalance in intracellular Na⁺/K⁺ ratio than M. sativa (Li et al., Reference Li, Fukuda and Yang2010; Beyaz Reference Beyaz2019) which is one of the key determinants of plant salt tolerance under climate change (El Sabagh et al., Reference El Sabagh, Islam, Skalicky, Ali Raza, Singh and Anwar Hossain2021).

Drought tolerance

Drought is the largest contributor to world-wide crop losses (Lesk et al., Reference Lesk, Rowhani and Ramankutty2016; Santos-Medellín et al., Reference Santos-Medellín, Liechty, Edwards, Nguyen, Huang, Weimer and Sundaresan2021). In this general context that is exacerbated by climate change (Cook et al., Reference Cook, Mankin and Anchukaitis2018), O. viciifolia produces indehiscent fruits (pods) that break down slowly, promoting seed survivorship during drought periods (Majidi and Barati, Reference Majidi and Barati2011; Avci and Kaya, Reference Avci and Kaya2013). In this sense, organic, hydrogel and mineral seed coating improved germination speed of O. viciifolia with and without drought (Mehrabi and Chaichi, Reference Mehrabi and Chaichi2012). Contradictorily, Kintl et al. (Reference Kintl, Huňady, Vymyslický, Ondrisková, Hammerschmiedt, Brtnický and Elbl2021) showed that O. viciifolia did not respond positively to the seed coating under drought. Uncoated seeds exhibited a greater drought resistance than the coated seeds which showed a sharp, significant decline of germination capacity and a great increase in the dead seed percentage due to the death of a fraction from the hard seeds.

Nasirzadeh et al. (Reference Nasirzadeh, Khorram and Heydari2005) reported that O. viciifolia can be considered as a semi-resistant species to drought. Adult plants of O. viciifolia tolerate exposure to the combined effects of drought and ozone (Bungener et al., Reference Bungener, Balls, Nussbaum, Geissmann, Grub and Fuhrer1999). The response mechanisms of O. viciifolia to drought include osmotic adjustment (Dehabadi, Reference Dehabadi1997; Irani et al., Reference Irani, Majidi, Mirlohi, Zargar and Karami2015a, Reference Irani, Majidi, Mirlohi, Karami and Zargar2015b; Beyaz, Reference Beyaz2019; Beyaz and Yildiz, Reference Beyaz and Yildiz2021), ROS scavenging, reduced transpiration (Roy et al., Reference Roy, Núñez-Delgado, Wang, Kader, Sarker, Hasan and Dindaroglu2021), increasing stomatal resistance and water use efficiency (Dehabadi et al., Reference Dehabadi, Kemp, Barker and Hodgson1993a, Reference Dehabadi, Kemp, Barker and Hodgson1993b; Dehabadi, Reference Dehabadi1997; Huang et al., Reference Huang, Liu, Tian and Wu2020), and increasing carotenoid contents with decreasing chlorophyll contents (Irani et al., Reference Irani, Majidi, Mirlohi, Zargar and Karami2015a, Reference Irani, Majidi, Mirlohi, Karami and Zargar2015b). In addition, O. viciifolia tolerance to drought involves also morphological adaptations such as a deep root system (Koch et al., Reference Koch, Dotzenko and Hinze1972; Dehabadi, Reference Dehabadi1997; March-Salas et al., Reference March-Salas, van Kleunen and Fitze2021) and reduced leaf area (Dehabadi et al., Reference Dehabadi, Kemp, Barker and Hodgson1993b). Besides all its responses to drought, O. viciifolia shows reduced plant heights which resulted in significant yield losses when exposed to severe drought (Irani et al., Reference Irani, Majidi, Mirlohi, Zargar and Karami2015a, Reference Irani, Majidi, Mirlohi, Karami and Zargar2015b). In this sense, Bolger and Matches (Reference Bolger and Matches1990) found a higher yield potential for O. viciifolia in spring than in summer, possibly indicating higher water use efficiency. To tide over periodic drought stress, Malisch et al. (Reference Malisch, Salminen, Kölliker, Engström, Suter, Studer and Lüscher2016) highlighted the importance of harvesting at optimal stages to have good forage performance for O. viciifolia.

Onobrychis viciifolia have greater ability to resist drought and adapt to dry habitats compared to several forage species. Considering the field capacity as the upper limit of soil water availability, O. viciifolia had the widest range of adaptability to soil water compared to other crop species such as Astragalus adsurgens, Elymus nutans and Lolium multiflorum (Huang et al., Reference Huang, Liu, Tian and Wu2020). Moreover, O. viciifolia exhibited a lower average lower limit of relative soil water content compared to A. adsurgens, E. nutans, and L. multiflorum. In addition, O. viciifolia closed stomata more rapidly with the decrease of relative soil water content, suggesting that the species had better drought resistance and allowed plants to keep water in plant tissues (Huang et al., Reference Huang, Liu, Tian and Wu2020). The intrinsic water use efficiency (WUE_i) represents an important indicator of the adaptability for higher plants to climate change (Weiwei et al., Reference Weiwei, Xinxiao, Guodong, LI and LIU2018). WUEi increased more rapidly in O. viciifolia than the other three forage under moderate water deficit (Huang et al., Reference Huang, Liu, Tian and Wu2020).

High temperatures tolerance

Onobrychis viciifolia is an alternative forage for semi-arid regions, where M. sativa and Trifolium sp. cannot be sown. Although there is little published data, there is considerable observational evidence that O. viciifolia is tolerant to relatively high temperatures. Maximum air temperatures of above 32°C did not affect O. viciifolia in small plots in northern Greece and southern Spain (Carbonero et al., Reference Carbonero, Mueller-Harvey, Brown and Smith2011). However, O. viciifolia exhibits poor growth following periods of high ambient temperatures and few plants survived at 35°C due to severe leaf loss causing plant death because high metabolic rates cannot be supported by existing leaf area or taproot carbohydrates even under well-watered conditions (Kallenbach et al., Reference Kallenbach, Matches and Mahan1996). High temperatures at the beginning of summer interrupt regrowth under traditional and intensive cutting regimes in southern Italy (De Falco et al., Reference De Falco, Landi and Basso2000a, Reference De Falco, Landi, Basso and Sulas2000b). Onobrychis viciifolia had a higher rate of biomass accumulation compared to M. sativa. However, M. sativa tended to grow faster during the warmer months (July–September) in Texas (USA).

Agronomic advantages

Global climate change is predicted to impact on soil fertility through the physical, chemical, and biological properties of soil due to rise in temperature, alternation in precipitation patterns, increase in greenhouse gases concentration in the atmosphere, etc. (Mondal, Reference Mondal, Choudhary, Mishra and Varma2021; Bibi and Rahman, Reference Bibi and Rahman2023). In addition, climate change could lead to the loss of soil function for fertility maintenance and greater dependence on mineral fertilizers (Pareek, Reference Pareek2017). For centuries, O. viciifolia was widely grown across Europe before commercial fertilizers were used. The species does not need fertile soil to thrive if its requirements for lime and humidity are satisfied. Onobrychis viciifolia can thrive in less fertile soils than M. sativa and T. repens and can also grow well in more fertile soils. Medicago sativa and T. repens will, however, produce better yields in fertile and irrigated lands, but O. viciifolia provides better outcomes growing in low fertility soils compared with M. sativa (Benaiges, Reference Benaiges1971; Demdoum, Reference Demdoum2012).

Mature plants of O. viciifolia have over 2-m-long taproots, partly responsible for its drought tolerance. The root is quite branched, especially at the bottom and multiples thin lateral roots constitute the bulk of the root system (Carbonero et al., Reference Carbonero, Mueller-Harvey, Brown and Smith2011; Mora-Ortiz and Smith, Reference Mora-Ortiz and Smith2018). The O. viciifolia root systems rivals M. sativa for its ability to access deep subterranean waters (Mora-Ortiz and Smith, Reference Mora-Ortiz and Smith2018). In the Mediterranean Basin, O. viciifolia prefers altitudes above 600 m, but it performs well when cultivated in a range between 100 and 2500 m (García Salmerón et al., Reference García Salmerón, Montserrat, Buendía, Ruiz-del-Castillo and Allue1966; Demdoum, Reference Demdoum2012).

Agronomic disadvantages

Onobrychis viciifolia is a forage legume of renewed interest worldwide, with equally weighted advantages and disadvantages that prevent many farmers from considering this crop a viable alternative to other forage legumes. In this sense, a wide distribution of O. viciifolia in productive grassland systems is hampered by the limited availability of high-performing cultivars adapted to different environmental conditions (Subedi, Reference Subedi2018; Sheppard et al., Reference Sheppard, Cattani, Ominski, Biligetu, Bittman and McGeough2019). In fact, O. viciifolia weaknesses are related to its lower yield when compared to other forage legumes, its poor competitive ability against weeds especially during the establishment year, a limited persistence, susceptibility to waterlogging and frost (Sheehy and Popple, Reference Sheehy and Popple1981; Liu et al., Reference Liu, Baines, Lane and Davies2010), low tolerance to frequent cutting (Malisch et al., Reference Malisch, Suter, Studer and Lüscher2017), and susceptibility to diseases such as powdery mildew or Phytophthora root rot (Sears et al., Reference Sears, Ditterline and Mathre1975; Carbonero et al., Reference Carbonero, Mueller-Harvey, Brown and Smith2011). Onobrychis viciifolia prefers well-drained soils and does not grow well in heavy soils or under flood irrigation (García Salmerón et al., Reference García Salmerón, Montserrat, Buendía, Ruiz-del-Castillo and Allue1966; Demdoum, Reference Demdoum2012; Anderson, Reference Anderson2016). Onobrychis viciifolia does not perform properly in acidic soils. Poor O. viciifolia establishment was obtained on soils at pH lower than 6 (Bland, Reference Bland1971; Carbonero et al., Reference Carbonero, Mueller-Harvey, Brown and Smith2011). In Spain, O. viciifolia is traditionally cultivated on neutral or slightly alkaline brown-earth soils.

Onobrychis viciifolia died out primarily during winter due to aerial interspecific competition, resulting in reduced root reserves (Liu et al., Reference Liu, Baines, Lane and Davies2010). Persistence of O. viciifolia appears to be dependent on minimal pressure from competing plants, harvest or grazing, and good growth conditions from midsummer into fall, allowing for adequate root reserves for survival. It is possible that judicious use of glyphosate in late season might lessen competition in that critical period as O. viciifolia is more glyphosate-tolerant than M. sativa (Peel et al., Reference Peel, Ransom and Mott2013).

Crop residue

Due to its deep, extensive and nodulated roots system, O. viciifolia uses water reserves in deep soil layers, increases carbon sequestration, reduces moisture and nutrient loss through leaching and runoff, prevents soil erosion, and improves the physicochemical and microbiological properties of the soil, including reductions on nitrification rates (Sergeeva, Reference Sergeeva1955; Komainda et al., Reference Komainda, Küchenmeister, Küchenmeister, Breitsameter, Wrage-Mönnig, Kayser and Isselstein2019; Clemensen et al., Reference Clemensen, Villalba, Lee, Provenza, Duke and Reeve2022). The irrigated cultivation of O. viciifolia accumulate in the soil up to 16.2 t/ha/year of residues, which represents approximately four times the quantity left by M. sativa (4.2 t/ha/year) (Sergeeva, Reference Sergeeva1955). This could be explained by its high root biomass compared to other cultivated legumes (Bolat, Reference Bolat2019; Rossi et al., Reference Rossi, Mao, Merino-Martín, Roumet, Fort, Taugourdeau, Boukcim, Fourtier, Del Rey-Granado, Chevallier, Cardinael, Fromin and Stokes2020). In fact, O. viciifolia can be used for soil organic matter improvement (Porqueddu et al., Reference Porqueddu, Ledda and Roggero2000; Wu et al., Reference Wu, Zhao, Liu, Wang, Qiu, Alexandrov and Jothiprakash2018). In view of these studies, cultivating O. viciifolia would help increasing the role of agricultural soils as carbon sinks to mitigate climate change.

In addition to supplies biologically fixed N₂, O. viciifolia displays a range of adaptations for the acquisition and retention of other important resources. O. viciifolia has excellent resource use efficiency in low input environments (Carbonero et al., Reference Carbonero, Mueller-Harvey, Brown and Smith2011). By virtue of their large active root systems and mycorrhization, O. viciifolia can efficiently accelerate the absorption of water and nutrients (Kong et al., Reference Kong, Pei, Du, Sun and Zhang2014). Onobrychis viciifolia has the ability to acquire phosphorous via specialized root structures, through arbuscular mycorrhizal associations under controlled environment (Kong et al., Reference Kong, Pei, Du, Sun and Zhang2014). The large rooting systems of O. viciifolia function to increase soil organic C by reducing erosion, reducing microbial respiration (via lack of tillage). As a result, nutrients are retained in the cropping system for use by subsequent crops (Carbonero et al., Reference Carbonero, Mueller-Harvey, Brown and Smith2011).

Fossil fuel burning in the energy sector is a major contributor to greenhouse gas emissions. Biofuels, considered as a substitute for fossil fuels, have become top priority due to its eco-friendly nature (Prasad et al., Reference Prasad, Kumar, Sheetal and Venkatramanan2020). In addition to the biodiesel production from the legume (Ndukwu and Onyeoziri, Reference Ndukwu and Onyeoziri2022), all the biomass of O. viciifolia can serve to produce second-generation biofuel due to its high N content (Slepetys et al., Reference Slepetys, Kadziuliene, Sarunaite, Tilvikiene and Kryzeviciene2012). Moreover, the use of O. viciifolia showed potential for methane production in biogas plants (Hunady et al., Reference Hunady, Ondriskova, Hutyrova, Kubikova, Hammerschmiedt and Mezera2021).

Onobrychis viciifolia contains phenolic compounds (tannins) that can influence soil nutrient dynamics by inhibiting microbial activity, which could slow N mineralization rates and minimize N losses in field (Clemensen et al., Reference Clemensen, Villalba, Rottinghaus, Lee, Provenza and Reeve2020, Reference Clemensen, Villalba, Lee, Provenza, Duke and Reeve2022; Slebodnik et al., Reference Slebodnik, Reeve, Norton, MacAdam and Lee2019). Tannins, at low concentrations in the soil, may increase some enzyme activity (Adamczyk et al., Reference Adamczyk, Karonen, Adamczyk, Engström, Laakso, Saranpää, Kitunen, Smolander and Simon2017), inactivate other soil enzymes, in part due to their antibiotic properties (Benoit and Starkey, Reference Benoit and Starkey1968; Field and Lettinga, Reference Field, Lettinga, Hemingway and Laks1992; Joanisse et al., Reference Joanisse, Bradley, Preston and Munson and2007; Triebwasser et al., Reference Triebwasser, Tharayil, Preston and Gerard2012), and to the formation of tannin–protein complexes (Adamczyk et al., Reference Adamczyk, Sietiö, Biasi and Heinonsalo2019). Dehydrogenase enzymatic activity was reported to be higher in O. viciifolia than M. sativa sown plots (Clemensen et al., Reference Clemensen, Villalba, Rottinghaus, Lee, Provenza and Reeve2020, Reference Clemensen, Villalba, Lee, Provenza, Duke and Reeve2022).

Atmospheric di-nitrogen fixation

Crop production is dependent on inorganic N and other fertilizers inputs to resupply nutrients lost as harvested grain and forage, via soil erosion/runoff, and by other natural or anthropogenic causes (Schlautman et al., Reference Schlautman, Barriball, Ciotir, Herron and Miller2018; Bibi and Rahman, Reference Bibi and Rahman2023). Nitrogen-fertilizers are one of the most monetary and environmentally expensive inputs in agricultural settings, which are currently more expensive than ever before (Herrera et al., Reference Herrera, Rubio, Häner, Delgado, Lucho-Constantino, Islas-Valdez and Pellet2016; Adjesiwor and Islam, Reference Adjesiwor and Islam2016). The mobility of applied inorganic N fertilizers results in less than 50% fertilizer N-recovery efficiency by the first crop with substantial amounts of the remaining N leaving the cropping system as N₂O and NO₃ (Crews and Peoples, Reference Crews and Peoples2004; Ladha et al., Reference Ladha, Pathak, Krupnik, Six and van Kessel2005). Onobrychis species are soil enriching via the fixation of atmospheric N. The symbiosis between legumes and root-nodule bacteria supplies biologically fixed N to natural and agroecosystems around the globe (Crews, Reference Crews1993). This form of N is directly incorporated into the growing plant, overcoming problems of low fertilizer N-recovery efficiency. Onobrychis viciifolia is able to provide relief from reliance on synthetic N while supplying high forage quality in low-input agricultural ecosystems (Carbonero et al., Reference Carbonero, Mueller-Harvey, Brown and Smith2011). While N₂ fixation in legumes is considered to have higher energy and carbon requirements than N assimilation by plants using reduction of NO₃ for growth, the energy is supplied via solar radiation rather than through fossil fuels; thus, the resulting CO₂ respired by the nodules originates though photosynthesis and is not a net contributor to atmospheric CO₂ concentrations (Crews and Peoples, Reference Crews and Peoples2004; Jensen et al., Reference Jensen, Peoples, Boddey, Gresshoff, Henrik, Alves and Morrison2012).

Onobrychis species form symbioses with bacteria belonging to the genera Mesorhizobium, Rhizobium and Bradyrhizobium (Baimiev et al., Reference Baimiev, Baimiev, Gubaidullin, Kulikova and Chemeris2007). In field conditions, Nitrogen deficiency symptoms were reported in O. viciifolia despite plants being abundantly nodulated, which indicates that the strain of N-fixing bacteria present was inefficient or short lived (Burton and Curley, Reference Burton and Curley1968; Schneiter et al., Reference Schneiter, Whitman and Larson1969), but these symptoms disappeared with time in plants nodulated by effective strains (Prévost et al., Reference Prévost, Bordeleau and Antoun1987a). Small young nodules are generally the most effective in O. viciifolia and are scarce in early stages of growth in the field (Burton and Curley, Reference Burton and Curley1968). In this sense, it seems likely that O. viciifolia is dependent on some mineral N at early growth stages and later growth stages benefit significantly from an effective symbiosis (Carbonero et al., Reference Carbonero, Mueller-Harvey, Brown and Smith2011). However, the N-fixing system of O. viciifolia is very sensitive to low levels of nitrate under glasshouse conditions (Hume and Withers, Reference Hume and Withers1985). Onobrychis viciifolia can be cross inoculated by Rhizobium species isolated from different leguminous species (Burton and Curley, Reference Burton and Curley1968; Prévost et al., Reference Prévost, Bordeleau and Antoun1987a). Furthermore, inoculating O. viciifolia with rhizobia isolated from three arctic legume species improved biological nitrogen fixation during cold phases of the growing season (Prévost et al., Reference Prévost, Bordeleau and Antoun1987a, Reference Prévost, Bordeleau, Caudry-Reznick, Schulman and Antoun1987b). Based on acetylene reduction rates, the general effect of adding strains of Rhizobium to other strains of Rhizobium in symbiosis with O. viciifolia was additive (Hill, Reference Hill1980). Kong et al. (Reference Kong, Pei, Du, Sun and Zhang2014) demonstrated that the inoculation of arbuscular mycorrhizal fungi can improve mycorrhizal infection rate and plant growth, accelerating the absorption of water and nutrients by the roots compared with uninoculated plants. Kon (Reference Kon1980) established that O. viciifolia, when infected with the appropriate Rhizobium spp. and arbuscular fungi, produced more and larger nodules and, consequently, a greater nodule dry weight and exhibited greater N₂ fixation than plants infected with only the rhizobia in a glasshouse conditions. Over two-year experiments, O. viciifolia fixed 106 kg N ha/year in rain-fed Mediterranean conditions, which was below the usual range of 130–160 kg N ha/year and quite far from the potential value of 270 kg N ha/year from non-Mediterranean areas (Provorov and Tikhonovich, Reference Provorov and Tikhonovich2003; Re et al., Reference Re, Piluzza, Sulas, Franca, Porqueddu, Sanna and Bullitta2014) (Table 1). Issah et al. (Reference Issah, Schoenau, Lardner and Knight2020) quantified biological N₂ fixation using ¹⁵N isotope dilution and estimated resource partitioning in O. viciifolia under controlled conditions. The percentage of N derived from atmosphere was 81% corresponding to estimated N contributions of 65 kg N ha/year. In view of previous works, cultivating O. viciifolia would help mitigating climate change through the reduction of N fertilizers and related greenhouse gasses emissions. As well, the cultivation of O. viciifolia would support farmers on their efforts to cope with climate change and to face increasing costs of N fertilizers.

Table 1.

Effective bacterial and mycorrhiza strains for Onobrychis viciifolia inoculation

Weed and pest control

Climate change is opening new geographic windows for disease outbreaks, insect herbivory and weed infestations in crops worldwide (Bajwa et al., Reference Bajwa, Farooq, Al-Sadi, Nawaz, Jabran and Siddique2020; Gullino et al., Reference Gullino, Albajes, Al-Jboory, Angelotti, Chakraborty, Garrett, Hurley, Juroszek, Lopian, Makkouk, Pan, Pugliese and Stephenson2022). The inclusion of O. viciifolia can reduce number and cover of weeds in cereal fields (Cirujeda et al., Reference Cirujeda, Marí, Murillo, Aibar, Pardo and Solé-Senan2019). Mummey and Ramsey (Reference Mummey and Ramsey2017) concluded that O. viciifolia may be a useful bridge species for improving soil conditions while allowing for weed control during restoration of invasive crested wheatgrass (Agropyron cristatum (L.) Gaertmn.) stands, improving conditions for native species establishment in dry rangeland in North America. In addition, O. viciifolia can offer a multitude of ecosystem services by supporting biodiversity and hosting important enemies of crop pests in agricultural landscapes. For example, González et al. (Reference González, ŠtroblŠtrobl, Janšta, Hovorka, Kadlec and Knapp2022) found almost 147 morphospecies of hymenopteran parasitoids in O. viciifolia patches providing a low-cost strategy for biological pest control in Brassica napus L. fields. According to these studies, cultivating O. viciifolia would improve biological control of pests just when their impacts are growing due to climate change.

Honey production

The change in climatic conditions is bound to have an impact on the physiology, distribution and survival of bees (Le Conte and Navajas, Reference Le Conte and Navajas2008; Smoliński et al., Reference Smoliński, Langowska and Glazaczow2021). Under this scenario, conservation of honeybees remains a challenging task (Wood et al., Reference Wood, Michez, Paxton, Drossart, Neumann, Gérard, Vanderplanck, Barraud, Martinet, Leclercq and NJ2020). As O. viciifolia is self-sterile, it relies on flower visitors for cross-pollination and requires multiple visits to maximize pollination (Bogoyavlenskii, Reference Bogoyavlenskii1955, Reference Bogoyavlenskii1974; Kropacova and Haslbachova, Reference Kropacova and Haslbachova1969). Bee pollination of O. viciifolia gave an increase of seed productivity by more than 30% (Pankov, Reference Pankov2013). Consequently, its flowers are a rich source of pollen and nectar, attracting ten times more bees than Trifolium repens L. and M. sativa (Rosov, Reference Rosov1952; McGregor, Reference McGregor1976; Kells, Reference Kells2001; Deveci and Kuvanci, Reference Deveci and Kuvanci2012). Onobrychis viciifolia is visited by managed and indigenous pollinator insect species, including Apis, Bombus and Osmia in southern Alberta (Canada), Eastern Washington (USA), the British Isles (UK), Europe and Japan (Richards and Edwards, Reference Richards and Edwards1988; Horne, Reference Horne1995; Clement et al., Reference Clement, Griswold, Rus, Hellier and Stout2006; Howes, Reference Howes2007; USDA SARE, 2007; Westphal et al., Reference Westphal, Bommarco, Lamborn, Petanidou, Potts, Roberts, Szentgyörgyi, Vaissière, Woyciechowski and Steffan-Dewenter2008; Taki et al., Reference Taki, Okabe, Makino, Yamaura and Sueyoshi2009). Rozen et al. (Reference Rozen, Ozebek, Ascher, Sedivy, Praz, Monfared and Mueller2010) noted that O. viciifolia is the only pollen source for Osmia avosetta Warncke bees in Turkey. In addition, different studies have described a very diverse pollinator community, dominated by Bombus and different bee species, foraging on O. viciifolia in Italy, Canada, USA, Europe and Turkey (Ricciardelli d'Albore and Roscioni, Reference Ricciardelli D'Albore and Roscionii1990; Kells, Reference Kells2001; Clement et al., Reference Clement, Griswold, Rus, Hellier and Stout2006; Decourtye et al., Reference Decourtye, Mader and Desneux2010; Manino et al., Reference Manino, Patetta, Boglietti and Porporato2010; Özbek, Reference Özbek2011; Pearce et al., Reference Pearce, O'Neill, Miller and Blodgett2012; Richards, Reference Richards2019). Richards and Edwards (Reference Richards and Edwards1988) found that bumblebees visited O. viciifolia flowers at a much greater rate than western honeybees in Canada. As previously stated, O. viciifolia is a good nectar and pollen source for many pollinator species and, additionally, it shows a long-lasting flowering period to offer bee pasture for western honeybees (Apies mellifera L.). and wild bees (Szalai, Reference Szalai2001). In addition, weeds in O. viciifolia crops are mainly represented by melliferous species in Russia (Pankov, Reference Pankov2014). When grown as a forage crop, O. viciifolia is mown late so flowering has normally finished, maximizing its value as a bee forage crop (Ayers, Reference Ayers1993). With a reduced number of flowers per plant under drought, O. viciifolia maintained similar per-flower nectar production (Phillips et al., Reference Phillips, Shaw, Holland, EL, RD, JM and JL2018). Onobrychis viciifolia can yield up to 400 kg/ha of honey (Howes, Reference Howes2007) with a distinctive taste, smell, texture and colour (Vereshchagin et al., Reference Vereshchagin, Nickolay and Alexandra2015), which constitute an additional revenue (Pankov, Reference Pankov2012). Recently, it has been demonstrated that the caffeine present in the nectar of O. viciifolia reduces the infection of bumblebees (Bombus terrestris) by the microsporidian parasite Nosema bombi Fantham and Porter (Folly et al., Reference Folly, Koch, Farrell, Stevenson and Brown2021). Growing O. viciifolia may promote a diversification of agronomic production with honeybee related products, which is key to stand the impacts of climate change (Zhang et al., Reference Zhang, Clair, Dolezal, Toth and O'Neal2022).

Reducing greenhouse gas emissions from livestock

The livestock sector plays an important role in climate change as it accounts for 15% of human-induced greenhouse gases emissions (Hur et al., Reference Hur, Kim, Yim, Yoon, Lee and Jo2024). Methane represents the second largest anthropogenic greenhouse-effect gas after carbon dioxide (CO₂) (IPCC, Reference Masson-Delmotte, Zhai, Pirani, Connors, Péan, Berger, Caud, Chen, Goldfarb, Gomis, Huang, Leitzell, Lonnoy, Matthews, Maycock, Waterfield, Yelekçi, Yu and Zhou2021). Livestock, enteric fermentations or effluents, contributes about 1/3 of the global methane emissions (Saunois et al., Reference Saunois, Stavert, Poulter, Bousquet, Canadell, Jackson, Raymond, Dlugokencky, Houweling, Patra, PK, Arora, VK, Bergamaschi, Blake, DR, Bruhwiler, Carlson, KM, Castaldi, Chandra, Cevoisier, Crill, PM, Curry, CL, Frankenberg, Gedney, Hegglin, MI, Hugelius, Ishizawa, Ito, Janssens-Maenhout, Jensen, KM, Kleinen, Krummel, PB, RL, GG, Maksyutov, McDonald, KC, Miller, PA, JR, Müller, Murguia-Flores, Naik, Niwa, Noce, O'Doherty, Parker, RJ, Peng, Peters, GP, Prinn, Ramonet, Regnier, Riley, JW, JA, Simpson, IJ, Smith, SJ, LP, BF, Tohjima, Tubiello, FN, Viovy, Voulgarakis, Weber, TS, van der Werf, GR, RF, Wunch, Yin, Yoshida, Zhang, Zhang, Zhao, Zheng, Zhu, Zhu and Zhuang2020). From an environmental point of view, feeding ruminants with forage containing condensed tannins may offer potential benefits. Nitrogen balance studies performed on sheep fed with conserved O. viciifolia have shown a reduction in excretion of urinary N, whereas the opposite pattern was observed with M. sativa (Aufrere et al., Reference Aufrere, Dudilieu and Poncet2008; Theodoridou et al., Reference Theodoridou, Aufrere, Andueza, Pourrat, Le Morvan, Stringano, Mueller-Harvey and Baumont2010). Urinary N can pollute water resources through excessive nitrate levels (Hoste and Niderkorn, Reference Hoste and Niderkorn2019) and is quickly converted to nitrogen oxide, a greenhouse gas 298 times more potent than carbon dioxide (Vallero, Reference Vallero2019). Moreover, sheep fed O. viciifolia increased faecal N excretion, which contributes to organic matter accumulation more than urinary N (Aufrere et al., Reference Aufrere, Dudilieu and Poncet2008; Theodoridou et al., Reference Theodoridou, Aufrere, Andueza, Pourrat, Le Morvan, Stringano, Mueller-Harvey and Baumont2010), reducing N loses to the atmosphere. Condensed tannins contribute to shift the proportion of excreted N from urine to faeces (Stewart et al., Reference Stewart, Beauchemin, Dai, MacAdam, Christensen and Villalba2019; Lagrange et al., Reference Lagrange, Beauchemin, MacAdam and Villalba2020), given the capacity of tannins to bind proteins in the acidic rumen environment and release proteins at greater pH in the intestines for digestion and absorption (Mueller-Harvey et al., Reference Mueller-Harvey, Bee, Dohme-Meier, Hoste, Karonen, Kölliker, Lüscher, Niderkorn, Pellikaan, Salminen and Skøt2019). Enteric methane emissions, another greenhouse gas, were reduced in ruminants consuming O. viciifolia (Hatew et al., Reference Hatew, Hayot Carbonero, Stringano, Sales, Smith, Mueller-Harvey, Hendriks and Pellikaan2015, Reference Hatew, Stringano, Mueller-Harvey, Hendriks, Hayot-Carbonero, Smith and Pellikaan2016; Petrič et al., Reference Petrič, Komáromyová, Batťányi, Kozłowska, Filipiak, Łukomska, Ślusarczyk, Szumacher-Strabel, Cieślak, Várady, Kišidayová and Váradyová2022). This reduction depends on the phenological stage and the chemical composition of the biomass. In vitro, methane production in O. viciifolia hays showed a tendency to increase with the advancement of phenological stage. The best period to cut O. viciifolia for hay making was between early and late flowering, when the forage offers high organic matter digestibility, low methane production and more efficient microbial fermentation (Guglielmelli et al., Reference Guglielmelli, Calabro, Primi, Carone, Cutrignelli, Tudisco, Piccolo, Ronchi and Danieli2011). At flowering stage, in vitro gas and methane productions were cultivar dependant (Kaplan, Reference Kaplan2011; Ülger and Kaplan, Reference Ülger and Kaplan2016). Hatew et al. (Reference Hatew, Hayot Carbonero, Stringano, Sales, Smith, Mueller-Harvey, Hendriks and Pellikaan2015) suggested that conserved O. viciifolia accessions collected worldwide exhibited substantial variation in terms of their effects on rumen in vitro methane production, revealing some promising accessions for future investigations. Additionally, the methane yield depended on the chemical composition of the biomass (Amaleviciute-Volunge et al., Reference Amaleviciute-Volunge, Slepetiene and Butkute2020). The results obtained in metabolic cages indicated that the inclusion of O. viciifolia in silage reduces the digestibility of organic matter in vivo on castrated male sheep compared to pure timothy (Phleum pratense L.), and methane emissions were proportionately lower (Niderkorn et al., Reference Niderkorn, Copani and Ginane2016). A trial on dairy cows, including 50% O. viciifolia silage in a ration of grass silage, resulted in a reduction of 6.0% methane emissions per kg of dry matter ingested. Silage of O. viciifolia allowed improved milk in quantity and quality (Huyen et al., Reference Huyen, Fryganas, Uittenbogaard, Mueller-Harvey, Verstegen, Hendriks and Pellikaan2016a, Reference Huyen, Desrues, Alferink, Zandstra, Verstegen, Hendriks and Pellikaan2016b). The consumption of O. viciifolia pellets by gastrointestinal nematode-infected lambs decreased methane emission by affecting ruminal methanogens without undesirable changes in the ruminal microbiome or animals' health (Petrič et al., Reference Petrič, Komáromyová, Batťányi, Kozłowska, Filipiak, Łukomska, Ślusarczyk, Szumacher-Strabel, Cieślak, Várady, Kišidayová and Váradyová2022). Adding O. viciifolia into M. sativa prior to ensiling suppressed silage proteolysis and mitigated rumen CH₄ in a proportion-dependent manner, with a minor negative effect on dry matter digestibility (Rufino-Moya et al., Reference Rufino-Moya, Blanco, Bertolín and Joy2019). Therefore, co-ensiling of M. sativa with O. viciifolia could be used as a promising strategy not only to produce high-quality legume silage but also to reduce N excretion and mitigate rumen CH₄ (Wang et al., Reference Wang, Chen, Bai, Zhang, Su, Franco, Ding, Zhang, Zhang and Guo2022). Lower values of CH₄ per kg intake were recorded with O. viciifolia silage compared to pure Phleum pratense L. silage (Niderkorn et al., Reference Niderkorn, Copani, Martin, Maxin, Torrent, Rochette and Ginane2019). Similar effects were observed in vitro when O. viciifolia was mixed with Lolium perenne L. or Dactylis glomerata L. (Niderkorn et al., Reference Niderkorn, Baumont, Le Morvan and Macheboeuf2011, Reference Niderkorn, Mueller-Harvey, Le Morvan and Aufrère2012) and in vivo when O. viciifolia was included in diets of dairy cows (Huyen et al., Reference Huyen, Fryganas, Uittenbogaard, Mueller-Harvey, Verstegen, Hendriks and Pellikaan2016a). The significant reduction of total digestive tract neutral detergent fibre digestibility in the presence of O. viciifolia compared to pure P. pratense was likely the main driver for the reduction of CH₄ emissions. In addition, the acetate:propionate ratio in the rumen, which is strongly related to the availability of hydrogen as a substrate for methanogenic archaea to form CH₄, was lower for P. pratense-O. viciifolia and Trifolium pratense-O. viciifolia than for pure P. pratense, highlighting the potential of O. viciifolia silage to decrease CH₄ emissions via a modification of the fermentative microbial ecosystem in the rumen (Warner et al., Reference Warner, Bannink, Hatew, Van Laar and Dijkstra2017). In addition, the reduction of NH₃ emissions and urea in milk were more pronounced than the reduction in methane emissions (McMahon et al., Reference McMahon, Majak, Mcallister, Hall, Jones, Popp and Cheng1999; Guglielmelli et al., Reference Guglielmelli, Calabro, Primi, Carone, Cutrignelli, Tudisco, Piccolo, Ronchi and Danieli2011; Niderkorn et al., Reference Niderkorn, Baumont, Le Morvan and Macheboeuf2011; Williams et al., Reference Williams, Moatea, Hannaha, Ribauxa, Wales and Eckard2011; Theodoridou et al., Reference Theodoridou, Aufrère, Niderkorn, Andueza, Le Morvan, Picard and Baumont2011; Chung et al., Reference Chung, Mc Geough, Acharya, McAllister, McGinn, Harstad and Beauchemin2013; Copani et al., Reference Copani, Ginane, Quereuil, Anglard and Niderkorn2015).

Nutritive value of sainfoin

The nutritional value of O. viciifolia is determined by variety, growth stage and growing environment. Several studies have quantified the nutritional values, mainly the concentrations of crude protein, neutral detergent fibre and acidic detergent fibre, of O. viciifolia at different stages of growth. After 42 days of regrowth, the nutritive value of O. viciifolia was comparable to the first growth vegetative stage, with crude protein ranging between 148–186 g/kg, and neutral detergent fibre and acid detergent fibre concentration ranging 365–454 g/kg and 337–397 g/kg, respectively (Table 2).

Table 2.

Nutritional value of Onobrychis viciifolia at different stages of growth

Freshly harvested forage, silage and hay of O. viciifolia have similar quality and nutritive value (Table 3). The tannins in O. viciifolia silage can reduce the proteolysis that takes place in the silo (Wilkins and Jones, Reference Wilkins and Jones2000). Incorporation of O. viciifolia into M. sativa forage improves fermentation in laboratory silos. Optimal ruminal fermentation with silage was obtained with a proportion of 60/40 for M. sativa and O. viciifolia, respectively (Wang et al., Reference Wang, Barbieri, Berg and McAllister2007). The inclusion of O. viciifolia in grass silage has been shown to improve forage quality, fermentation as well as protein protection against microbial and enzymatic degradation (Lee et al., Reference Lee, Scott, Tweed, Minchin and Davies2008; Lorenz et al., Reference Lorenz, Eriksson and Udén2010; Copani et al., Reference Copani, Le Morvan and Niderkorn2014). Onobrychis viciifolia can be offered as dehydrated granules (Gaudin, Reference Gaudin2017), but the necessary technological treatments, high temperature and high pressure, can cause a possible destruction of the tannins and a conversion of the tannins from the free majority form to the bound form attached to proteins (Terrill et al., Reference Terrill, Rowan, Douglas and Barry1992, Reference Terrill, Mosjidis, Moore, Shaik, Miller, Burke, Muir and Wolfe2007; Minnee et al., Reference Minnee, Woodward, Waghorn and Laboyrie2002; Lorenz, Reference Lorenz2011).

Table 3.

Characteristics and nutritive value of Onobrychis viciifolia feeding forms

Onobrychis viciifolia was found to increase by 17% the proportion of omega-3 polyunsaturated fatty acid and unsaturated fatty acids in milk and cheese fat from lactating cattle (Girard et al., Reference Girard, Dohme-Meier, Wechsler, Kreuzer and Bee2015, Reference Girard, Dohme-Meier, Wechsler, Goy, Kreuzer and Bee2016), due to condensed tannins modulating the activity of bacteria involved in the processes of biohydrogenation (Vasta et al., Reference Vasta, Yáñez-Ruiz, Mele, Serra, Luciano, Lanza, Biondi and Priolo2010; Buccioni et al., Reference Buccioni, Pauselli, Viti, Minieri, Pallara, Roscini, Rapaccini, Marinucci, Lupi, Conte and Mele2015). In addition, it has been reported that condensed tannins of O. viciifolia reduced protein degradation in the rumen leading to reductions in rumen ammonia concentrations and N losses in urine (Scharenberg et al., Reference Scharenberg, Arrigo, Gutzwiller, Wyss, Hess, Kreuzer and Dohme2007b). Condensed tannins also increased the plasma concentration of essential amino acids, indicating that the protein escaped from the rumen is digested in the intestine leading to faster animal growth rates and increased milk production (Waghorn et al., Reference Waghorn, Jones, Shelton and McNabb1990; Waghorn, Reference Waghorn2008; Girard et al., Reference Girard, Dohme-Meier, Wechsler, Goy, Kreuzer and Bee2016).

Nutritional benefits

Onobrychis viciifolia is particularly valued for its content of condensed tannins, which have been shown to improve animal health by reducing bloat (McMahon et al., Reference McMahon, Majak, Mcallister, Hall, Jones, Popp and Cheng1999; Sottie, Reference Sottie2014; Wang et al., Reference Wang, Mcallister and Acharya2015), and by diminishing gastro-intestinal parasites (Hoste et al., Reference Hoste, Torres-Acosta, Sandoval-Castro, Mueller-Harvey, Sotiraki, Louvandini, Thamsborg and Terrill2015; Desrues et al., Reference Desrues, Mueller-Harvey, Pellikaan, Enemark and Thamsborg2017). In fact, the intake of O. viciifolia fresh leaves (10–20% of the dry matter of M. sativa) reduces bloat in cattle by 27% (McMahon et al., Reference McMahon, Majak, Mcallister, Hall, Jones, Popp and Cheng1999) compared to those consuming 100% M. sativa. Consequently, O. viciifolia could be grazed, offered in as hay or silage ad libitum. When O. viciifolia is grown in a mixture with M. sativa, it has been shown to reduce bloat incidence in beef cattle relative to the grazing of pure M. sativa (Sottie, Reference Sottie2014; Malisch et al., Reference Malisch, Lüscher, Baert, Engström, Studer, Fryganas, Suter, Mueller-Harvey and JP2015). Condensed tannins of O. viciifolia hay has shown reduced egg per gram of faeces, and female fertility of parasitic nematodes when fed to livestock (Azuhnwi et al., Reference Azuhnwi, Hertzberg, Arrigo, Gutzwiller, Hess, Mueller-Harvey, Torgerson, Kreuzer and Dohme-Meier2013; Arroyo-Lopez et al., Reference Arroyo-Lopez, Manolaraki, Saratsis, Saratsi, Stefanakis, Skampardonis, Voutzourakis, Hoste and Sotiraki2014). Anti-parasitic properties of O. viciifolia tannins have been demonstrated by both in vitro (Barrau et al., Reference Barrau, Fabre, Fouraste and Hoste2005) and in vivo studies (Molan et al., Reference Molan, Hoskin, Barry and McNabb2000a, Reference Molan, Waghorn, Min and McNabb2000b, Reference Molan, Waghorn and McNabb2002; Hoste et al., Reference Hoste, Torres-Acosta, Sandoval-Castro, Mueller-Harvey, Sotiraki, Louvandini, Thamsborg and Terrill2015). Moreover, sheep increase their intake of O. viciifolia through time when parasitized (Gaudin et al., Reference Gaudin, Costes-Thiré, Villalba, Hoste, Gerfault and Ginane2019) and show high preferences for the legume despite the high availability of alternative legumes without tannins like cicer milkvetch (Villalba et al., Reference Villalba, Miller, Hall, Clemensen, Stott, Snyder and Provenza2013).

Onobrychis viciifolia has an antiparasitic effect on the most important sheep nematodes (Ríos-De Álvarez et al., Reference Ríos-De Álvarez, Greer, Jackson, Athanasiadou, Kyriazakis and Huntley2008; Komáromyová et al., Reference Komáromyová, Mravčáková, Petrič, Kucková, Babják, Urda Dolinská, Königová, Maďarová, Pruszyńska-Oszmałek, Cieslak, Čobanová, Váradyová and Várady2021; Petrič et al., Reference Petrič, Komáromyová, Batťányi, Kozłowska, Filipiak, Łukomska, Ślusarczyk, Szumacher-Strabel, Cieślak, Várady, Kišidayová and Váradyová2022). Similar results were obtained with goats (Paolini et al., Reference Paolini, Prevot, Dorchies and Hoste2005). While goats are more willing than sheep to consume tanniferous feeds, the potential for self-medication has been demonstrated in both species concerning H. contortus (Gaudin et al., Reference Gaudin, Costes-Thiré, Villalba, Hoste, Gerfault and Ginane2019). Regular feeding on O. viciifolia pastures by small ruminants could therefore be used to improve host resilience and thus reduce pasture contamination. The anthelmintic bioactivity of O. viciifolia is maintained in hay or silage (Ojeda-Robertos et al., Reference Ojeda-Robertos, Manolaraki, Theodoridou, Aufrere, Halbwirth, Stich, Regos, Treutter, Mueller-Harvey and Hoste2010). Berard et al. (Reference Berard, Holley, McAllister, Ominski, Wittenberg, Bouchard, Bouchard and Krause2009) proved that O. viciifolia silage and hay reduced the excretion of Escherichia coli by cattle. The consumption of O. viciifolia by small ruminants has also been associated with effects on coccidia (Saratsis et al., Reference Saratsis, Regos, Tzanidakis, Voutzourakis, Stefanakis, Treuter, Joachim and Sotiraki2012) and on infestations by gastrointestinal nematodes (Hoste et al., Reference Hoste, Torres-Acosta, Sandoval-Castro, Mueller-Harvey, Sotiraki, Louvandini, Thamsborg and Terrill2015). These findings contribute to the further development of sustainable grass–legume systems, as evidence for the successful cultivation of O. viciifolia as an alternative legume species (Malisch et al., Reference Malisch, Suter, Studer and Lüscher2017).