ARTIGO

An overview of Vicia faba role in ecosystems sustainability and perspectives for its improvement

Vicia faba na sustentabilidade dos ecossistemas e perspetivas para o seu melhoramento

Maria Manuela Veloso^1,3,*, Célia Mateus^2,3 and Maria José Suso⁴

 

¹Unidade de Investigação de Biotecnologia e Recursos Genéticos, INIAV, Quinta do Marquês, 2784-505 Oeiras, Portugal. * Email: mveloso.inrb@gmail.com

²Unidade de Investigação de Sistemas Agrários e Sanidade Vegetal, INIAV, Quinta do Marquês, 2784-505 Oeiras, Portugal

³ LEAF, Linking Landscape, Environment, Agriculture and Food, Instituto Superior de Agronomia, /Universidade de Lisboa, Tapada da Ajuda 1349- 017 Lisboa, Portugal

⁴ Plant Breeding Department, Institute for Sustainable Agriculture (IAS), Spanish National Research Council (CSIC), Córdoba, Spain

 

ABSTRACT

Faba bean (Vicia faba L.) that is grown world-wide as a protein source for food and feed also offers ecosystem services such as N₂ fixation and enhancement of wild fauna diversity such as bee-pollinators and other beneficial organisms. Thus, it helps to mitigate the pollinator decline and it is recognized that also contributes to pest control not only in the crop itself but also in the neighbouring/associated crops by attracting predators and parasitoids. Despite this importance, the global faba bean cultivation area has declined due to its low yield performance and susceptibility to biotic and abiotic factors. To face these constraints, it is relevant to implement adequate breeding programs using the available germplasm and always taking in consideration the pollination and mating system of faba bean. The aim of this paper is 1) to review the role of faba bean in cropping systems; 2) to assess the applicability of different molecular markers to understand the genetic diversity of faba bean germplasm; 3) to analyse the role of pollination and the mixed-mating system underpinning breeding strategies; 4) to assess the natural enemies affecting faba bean and to analyse the genetic sources of resistance to them.

Key words: genetic resources, biological nitrogen fixation, mating system and breeding, pollinator, pest control

 

RESUMO

A faveira (Vicia faba L.), cultivada mundialmente, é uma importante fonte de proteína na alimentação humana e animal. Tem também um papel relevante em serviços do ecossistema, como na fixação do N₂ e no aumento da diversidade dos polinizadores e outros auxiliares. Contribui, deste modo, para impedir o declínio dos polinizadores e, ao atrair predadores e parasitoides, contribui para o controlo de pragas nesta cultura e nas culturas vizinhas. Apesar de ser reconhecida a sua importância nos sistemas agrários, a área cultivada tem diminuído, a nível mundial, como consequência da sua baixa produtividade e suscetibilidade a fatores bióticos e abióticos. Para ultrapassar estes constrangimentos é fundamental implementar programas de melhoramento adequados, utilizando o germoplasma existente e atendendo sempre ao facto da faveira ser parcialmente alogâmica. Este trabalho tem como objetivos: 1) rever o papel desempenhado pela faveira nos sistemas culturais; 2) avaliar a aplicabilidade de diferentes marcadores moleculares no estudo e compreensão da sua diversidade genética; 3) analisar o papel dos polinizadores nas estratégias de melhoramento; 4) avaliar os inimigos naturais que afetam a faveira e analisar as fontes de resistência existentes.

Palavras-chave: recursos genéticos, fixação biológica do azoto, melhoramento, polinizadores, controlo de inimigos naturais.

 

Introduction

Faba bean (Vicia faba L.) is an important grain legume, as a protein source for human and animal consumption. In addition, faba bean has also a valuable agronomic function considering its high capacity of N₂ fixation and its ability to facilitate diversification of the agro-ecosystems by indirectly enhancing associated diversity of wild fauna (Köpke and Nemecek, 2010). A key environmental service of the faba bean crop is providing a feeding source of nectar and pollen to pollinators and beneficial insects. Recently, the interest in this crop has been renewed (Duc et al., 2014), because of the pollinators’ decline world-wide. It is cultivated across various climate environments and, as a result of human selection, it is a versatile crop also used as forage, vegetable and as green manure. The long period of cultivation under different selective pressures, both stabilizing selection on the one side and directional and disruptive selection on the other side (Suso and Cubero, 1986) and across such diverse environments has resulted in the differentiation of distinct germplasm groups based on seed size (paucijuga, minor, equina and major) and region of adaptation (Mediterranean, winter and spring types) (Muratova, 1931; Cubero, 1973,1974; Link et al., 1996; Flores et al., 2013).

It is the seventh most produced grain legume worldwide (FAOSTAT, 2013) and, in Europe, the production is equivalent to 1,168,000 ton, being the UK the leader producer, followed by France, Italy, Spain and Germany (Eurostat, 2014). In Portugal, its area of cultivation is presently restricted to 675 ha, with a production of 5,973 ton in 2012 (GPPAA, 2005; INE, 2013).

Although global faba bean acreage and production has experienced a steady reduction over the past decades, demand for faba bean in the world market lead to its increased production in Australia and France, in recent years (Brown, 2009).

Nowadays, the limiting natural resources of land and water, in addition to climate change, have put a high pressure on ongoing breeding programs (Pandey et al., 2016). The major objectives of faba bean breeding are similar to those of other grain legumes and include yield and resistance/tolerance to biotic/abiotic stresses. However, considering the partial allogamy of faba bean, it is important to identify the adequate breeding approach and type of cultivar for each particular environment (Suso et al., 2001). It is a crop that has no wild relatives and so, only cultivated forms are available for breeding (Duc et al., 2010; Gnanasambandam et al., 2012).

In this review, we briefly assess the role of faba bean for a sustainable agriculture. Then, we analyse the genetic diversity and the relationships among faba bean germplasm from diverse geographic locations, using different molecular markers. We also examine the potential role of pollination and mating system diversity in V. faba breeding strategies. Finally, we analyze the diversity of natural enemies (i.e diseases, parasites and arthropods) affecting this crop and the sources of resistance already identified in faba bean.

Agronomic potential of Vicia faba

Role for ecosystem sustainability

The increasing use of fertilizers has affected the nitrogen (N) cycle, resulting in a high concentration of reactive nitrogen in the biosphere, with negative consequences on the climate, ecosystems and health (Galloway et al., 2003).

Cropping systems with legumes reduce nitrous oxide emissions and have positive phytosanitary effects, with higher environmental benefits, than cropping systems without legumes (Reckling et al., 2016).

In Europe, grain legumes fix about 13 times more N per hectare than temporary pastures and about 20 times more than permanent pastures, thus reducing the need to introduce N in intensive field crops. Faba bean is one of the crops with the highest N₂ fixation rate among cool season grain legumes (Hauggaard-Nielsen et al., 2011), being responsible for 86.9 Gg of total N fixed in the EU 27 countries, in 2009 (Baddeley et al., 2013).

Systems involving faba bean as, for example, crop rotation or intercropping, which have the capacity to capture atmospheric N₂ are cheaper and a more sustainable alternative than conventional agriculture (Köpke and Nemecek, 2010; Carranca, 2013). Consequently, the N benefit from faba bean to subsequent crops is often high.

Crop rotation

Crop rotation is a planned succession of crops of different genus or species. The rotation may vary from two or three years, aiming to balance nutrient demands, soil structure improvement and reduction of pest populations, diseases and weeds (Carranca, 2013). In rotation, faba bean can be used in between the seasons of cereal (winter wheat, winter barley and silage maize) or other cash crops (Carranca et al., 1999; Amanuel et al., 2000; Köpke and Nemecek, 2010; Paull et al., 2011; Carranca, 2013).

Faba bean should not be used in successive years in order to avoid yield losses mainly due to fungal infections. The minimum number of break years required to reduce the risk of fungal infections is considered to be 4 years (Stoddart et al., 2010). Faba bean acts as a break crop in intensive cereal-dominated crop rotations and so, is a key species for enhancing the sustainability of the agroecosystems (Jensen et al., 2010; Köpke and Nemecek, 2010).

Intercropping

Intercropping is the practice of growing simultaneously two or more compatible crops in close proximity to promote interaction between them and increase the productivity per unit of land (Carranca, 2013). It is a widely distributed practice due to its high and more stable productivity in a wide range of crop combinations (Pelzer et al., 2012; Carranca, 2013). Intercropping may minimize crop failure due to adverse effects of biotic and abiotic factors (Jensen et al., 2010; Fernández-Aparicio et al., 2011), protect soil against erosion, provide a good weed control (Wolfe et al., 2013), improve the use of limited resources, increase stability of yield and provide higher returns (Tilman et al., 2006; Agegnehu et al., 2008).

Intercropping is common in the tropics (Agegnehu et al., 2008; Lithourgidis et al., 2011) and China (Fan et al., 2006), but is less common in temperate climates, because high input monocropping with precise applications of fertilizers and pesticides has higher revenues (Köpke and Nemecek, 2010; Schröder and Köpke, 2012). However, intercropping is becoming more used for low input and organic agriculture systems (Köpke and Nemecek, 2010). The most significant advantage of grain legumes in intercropping is that nitrogen fixed by the legume may be transferred to a non-legume intercropping partner (Jamont et al., 2013). Faba bean has also been intercropped with oil crops, as for example oil-seed rape (Jamont et al., 2013). Intercropping faba bean with rapeseed resulted in complementary use of N resources and the complementary root architecture between the two crops reduces plant competition for the N-soil at the beginning of their development (Jamont et al., 2013).

On the other hand it was found that maize promotes N₂ fixation in intercropping system with faba bean and recently, Li et al. (2016) explained the reason for that. It was demonstrated the facilitative root-root interactions that constitute a mechanism for a positive relationship between productivity and plant diversity in ecosystems.

Generally, the design of intercropping systems with grain legumes is currently a case-by-case work. Although many general principles have been established, transferability of experience from one system to the other is still limited.

Diversity in Vicia faba

Origin and distribution

The Vicia genus belongs to the Fabaceae family together with Lathyrus, Lens, Pisum and Vavilovia (Smýkal et al., 2015). The best known species of the genus are V. faba (faba bean) and V. sativa. Faba bean is an ancient crop and numerous studies have been performed on its origin and domestication. Cubero (1973, 1974) suggested a Near Eastern center of origin with four different radiations: to Europe; along the North African coast to Spain; along the Nile to Ethiopia; from Mesopotamia to India. Secondary centers of diversity are postulated to have occurred in Afghanistan and Ethiopia (Harlan, 1969). The migration of faba bean to South America, probably during the fifteenth century, occurred with the Spanish and Portuguese sailors (Duc et al., 2015). The time of introduction of faba bean in China is uncertain (Wang et al., 2012). According to Zong et al. (2009) winter faba bean from China “appears to be in a different gene pool from the rest of the world” reproductively isolated from the European, African and Asian gene pools. A relatively recent development of winter faba beans occurred in Europe, in the nineteenth century, as an hybridization result of Russian and French small seeded populations (Duc et al., 2015).

Based on differences in seed weight, shape, size and leaflet density, four botanical varieties have been recognised: V. faba paucijuga (very small seed size and fewer than four leaflets per leaf), V. faba minor (small seed), V. faba equina (intermediate seed size) and V. faba major (with flattened and large seed) (Muratova, 1931; Cubero, 1973, 1974). Equina and major botanical groups constitute the richest groups in genetic variability (Cubero, 1974).

According to Terzopoulos and Bebeli (2008), in Europe, there are the Central and the Northwest European gene pools. The Mediterranean gene pool is a mixture of V. faba major, minor and equina (Link et al., 1996).

The remains of faba bean in archaeological excavations in the Mediterranean and Central Europe are dated between the third and second millenia BC. This grain legume was cultivated in the Iberian Peninsula before 4000 BC (Zapata et al., 2004) and carbonized seeds of the minor botanical type from the Early Bronze Age were found in Portugal (Zohary et al., 2012).

Diversity analysis through molecular markers

The wild ancestor of faba bean remains unknown. All botanically faba bean relatives are diploid species with 14 chromosomes, while faba bean is a diploid with 12 chromosomes and a very large genome (13,000 Mbp; Johnston et al., 1999) due to a high number of retrotransposons copies (Pearce et al., 1996; Hill et al., 2005; Tomás et al., 2016). Despite the large genome, different molecular markers were successfully used to assess the genetic diversity and the relationships existing between faba bean accessions, namely, Random Amplified Polymorphic DNA (RAPD) (Link et al., 1995), Amplified Fragment Length Polymorphism (AFLP) (Zeid et al., 2003; Zong et al., 2009; Gresta et al., 2010), Inter Simple Sequence Repeats (ISSR) (Terzopoulos and Bebeli 2008; Wang et al., 2012), Simple Sequence Repeats (SSR) (Akash et al., 2012; Yang et al., 2012; Oliveira et al., 2016). Long terminal repeat (LTR) retrotransposons markers such as, Sequence Specific Amplified Polymorphism (SSAP) (Sanz et al., 2007; Ouji et al., 2012), Target Region Amplification Polymorphism (TRAP) (Kwon et al., 2010), and Inter-Retrotransposon Amplification Polymorphism (IRAP) (Tomás et al., 2016) are also useful for the analysis of genetic diversity. Recently, Kaur et al. (2014) used Single Nucleotide Polymorphism (SNP) markers to assess the diversity of faba bean from different geographical locations.

The studies using these markers indicate a large amount of variation within each faba bean accession. Link et al. (1995) using RAPDs, identified three major clusters within the 28 inbred lines from Europe and Mediterranean: European large-seeded, European small seeded and Mediterranean germplasm. Wang et al. (2012) using ISSRs concluded that accessions from North China had the highest genetic diversity, while accessions from Europe were genetically closer to those from Africa. Yang et al. (2012) using SSRs obtained four distinct clusters based on the geographic origin: China, other Asian countries and Algeria; Europe, Syria, India and Sudan; Egypt and Ethiopia; Tunisia, South America and North America. Kaur et al. (2014) using SNPs also observed a clear differentiation between faba bean genotypes that were clustered into two main groups: I) South America and Australia; II) China, Europe, North Africa and Australia.

Recently, Oliveira et al. (2016) when screening fifty three faba bean landraces from Continental Portugal and Spain, the Macarronesian Islands of Azores, Madeira and Tenerife and from Morocco, Egypt and Ethiopia, with 26 SSRs, concluded that, based on geography, no population structure could be detected. As Kaur et al. (2014) suggested, these observations may be a consequence of the high level of heterozygosity of faba bean, presumably due to the partially allogamous nature of the species.

Pollination in Vicia faba breeding strategies

The pollination phenomenon and the management and protection of wild pollinators are issues of paramount importance to our food supply system. It is considered important for the production of local crops in order to promote sustainable development (Díaz et al., 2015). Growing faba bean enhances the diversity of flowering resources and may help to maintain wild bee pollinators’ abundance and diversity. Faba bean is likely to play a role in the necessary pattern of seasonal flowering phenology and longevity needed to support a greater range of pollinators (Köpke and Nemecek, 2010).

Variability in Vicia faba mating system and diversity of pollinators

Faba bean is an entomogamous partially allogamous crop with a mixed mating system. The level of allogamy can be variable, ranging from 4 to 84% with a mean around 30 to 60% (Bond and Pope, 1974; Link, 1990; Link et al., 1994a; Suso and Moreno, 1999; Suso et al., 2001; Gasim et al., 2004). These large differences in outcrossing rate apparently depend on genetic and environmental factors as well as on the different methods and markers used in their estimation (Suso et al., 2001). Suso and Moreno (1999) and Suso et al. (2008), when studying the effect of environmental factors on faba bean cultivars outcrossing rate, observed a substantial variation associated with geographical location and found that annual variation at each location was far less important.

A reasonable description of the faba bean mating system could be as follows: there is a mixed mating system with a location dependent outcrossing rate that retains a fairly constant proportion of self and cross-pollinated individuals. Intermediate levels of selfing could be evolutionarily stable for wide ranges of environmental conditions (reviewed in Goodwillie et al., 2005). Suso and Maalouf (2010) showed that faba bean intermediate levels of outcrossing could be maintained because upwards selection for allogamy results in populations with increased selfing. However, selection for autogamy increases the level of outcrossing. Besides, self-pollination occurred in two different ways: geitonogamy or autogamy. The amount of outcrossing, geitonogamy and autogamy is influenced by the flower discovery, attraction and reward traits. V. faba plants exhibit spectacular variation in flower phenology, design and display, and much of the functional basis of this diversity is associated with the levels of outcrossing. All these factors are described by Suso et al. (2005) and Suso and Maalouf (2010). Floral traits increasing the level of outcrossing include enhanced inflorescence production during the beginning of flowering, but with few flowers open simultaneously per inflorescence. However, variation among plants in reward traits and in shape had limited influence. Although, low nectar reward and short floral tubes should be taken into account in order to increase outcrossing rates. Patterns of floral variation suggested that the mating system was rather firmly controlled by floral pollinator related traits. Breeders should be aware of the need to take into account the biology/structure/function of the flowers and the needs of the pollinators, that is, the inter-phase of plant-and-pollinator.

Considering that outcrossing varies geographically, the most suitable floral traits influencing outcrossing depend on local environmental conditions, particularly the composition of the pollinator fauna (Vogler et al., 1999). Faba bean is visited by a great number of solitary and social bees (Bond and Kirby, 1999, 2001; Pierre et al., 1996, 1999) but the pollinator species can vary from location to location. For instance, Pierre et al.(1999) found that, in Rennes (France), pollinator fauna is composed by Bombus terrestris L. (or B. lucorum L.) and honeybees (Apis mellifera L.), which are not very numerous. However, in Córdoba (Spain), it is mainly composed by one species of Eucera (Eucera numida Lep.), which is present at high density. Benachour et al. (2007) and Aouar-Sadli et al. (2008) studied the pollinating insects of V.faba in different regions of Algeria and concluded that: species of the Eucera genus, E. numida Lep. and E. pulveracea Dours., were the most effective pollinators.

Cunningham and Le Feuvre (2013) showed that provision of honeybee hives to V. faba fields consistently leads to higher and less variable yield. Nayak et al. (2015) found that the benefits of insect pollination to the production of winter field bean variety “Clipper” were as much as 185% compared to autonomous self-pollination. Bartomeus et al. (2014) observed that at landscape level, there is clear benefit delivered by pollinators on yield. However, the dependence on pollinators varies between cultivars (Suso and Río, 2014; 2015). According to Andersson et al. (2014), the number of developed pods is higher on organic farms compared to conventional ones. Garibaldi et al. (2014) suggested that new practices for integrated management of both honey bees and diverse wild insect assemblages will enhance global crop yields.

Pollination management for breeding strategies

Two basic philosophies have been held by faba bean breeders to deal with the partial allogamy of V. faba: (a) synthetic varieties and (b) pure line cultivars.

Synthetic varieties, produced by inter-crossing a number of parental lines on the basis of their general combining ability, make use of yield, yield stability and resistance to biotic and abiotic stresses mediated by heterosis in faba bean (Link et al., 1994b, 1996; Abdelmula et al., 1999; Arbaoui and Link, 2008; Gasim and Link, 2007; Terzopoulos et al., 2008; Maalouf et al., 2008). It is necessary to point out that F1-hybrid cultivars are not yet bred due to instability of male-sterile systems and because seed production is prohibitively expensive (Gnanasambandam et al., 2012; Zeid et al., 2004).

Based on the faba bean mixed mating system, synthetic varieties could be an objective in order to improve the sustainability of the crop by means of genetically heterogeneous cultivars and to integrate insect pollinators. Considering that the magnitude of heterosis expressed in cultivars depends on its average heterozygosity, and therefore on the rate of outcrossing, geographic variation in outcrossing rate must be taken into account in breeding strategies. To develop synthetics varieties, breeders have to choose a method to suit the level of natural crossing in the area where they have to work. According to Suso et al. (2001), in a situation of predominant sel?ng, parents with a high level of per se performance and a small inbreeding depression are preferable; however, on the other hand, in a location with high level of outcrossing, reliable selection of the parents with high General Combining Ability (GCA), based on poly-cross and top-cross tests, would be the approach. Alternatively, a strategy to increase the level of outcrossing is the managing of pollinator behaviour through selection for appropriate floral traits, as has been proposed in the Crops Design System (CDS) approach. This knowledge-based approach was first proposed by Suso et al. (2005) and Suso and Río (2015) specifically for faba bean, and it has been advocated by other researchers (Bailes et al., 2015).

Several authors have suggested transforming the mating system of faba beans towards autogamy (Kambal, 1976; Bozzini and Chiaretti, 1999). According to Ghaouti et al. (2008), inbred lines are uniform, and uniformity was apparently appreciated by organic farmers. Line breeding varieties are developed under cages that exclude pollinators and enforce pure self-fertilization. There are conceptual criticisms that call into question the overall suitability of this strategy. Three major concerns may rise. First, it ignores that diversity based - on the heterozygosity of genotypes and on heterogeneity within cultivar contributes to higher and more stable yields (e.g. Link et al., 1994b). Secondly, the transition from outcrossing to high levels of self-fertilization may be accompanied by the evolution towards plants with lower pollinator attraction and altered morphology, which might reinforce pollinator decline (Fishman and Willis, 2008). It should not be forgotten that changes in flower structure under the pollinator-exclusion management strategies could result in mismatches between plant and pollinator, decreasing the ecological services provided by faba bean such as maintaining bee populations (Helenius and Stoddard 2007; Palmer et al., 2009). Finally, it appears that, in faba bean, breeding strategies which use and encourage open-pollinated conditions, with pollinator visitors and appropriate flowering patterns, result in cultivars with higher yield and resilience than breeding strategies for increased selfing (Maalouf et al., 2008; Suso and Río, 2015). The lack of adequate pollination is responsible for the poor results in breeding strategies and in developing cultivars. Maalouf et al. (2008) showed that, in faba bean, developing cultivars under open-pollination conditions (with local pollinators present) results in lower disease severity and higher number of resistant lines for chocolate spot and Ascochyta blight when compared to exclusion of pollinators (selfing conditions). Suso and Río (2015) developing cultivars under evolutionary breeding scheme showed that pollinators are crucial for achieving higher seeds per plant, a main predictor of crop yield. Thus, the proposed breeding strategy is to combine highly self-fertile genotypes which respond optimally to the presence of pollinators to produce high-yielding cultivars. Thus, the presence of pollinators allows the exploitation of heterosis potential but in absence of pollinators a minimum yield is achieved (Suso et al., 1996).

Controlling natural enemies by breeding for resistance

Enemies and beneficial fauna

In spite of the agronomic and economic importance of faba bean being well demonstrated, its cultivation is limited due to several factors that negatively affect, in an unreliable way, both its quality and yield performance. The abiotic factors (mainly drought and cold) and biotic ones (e.g. natural enemies, such as pests, diseases and parasites), to which this crop is susceptible, are of great importance (Rubiales et al., 2006; Torres et al., 2006; Kharrat and Ouchari, 2011; Pérez-de-Luque et al., 2010; Stoddard et al., 2010; Torres and Ávila, 2011).

Faba bean is adversely affected by numerous fungal diseases, such as Ascochyta blight (Ascochyta fabae Speg.), rust (Uromyces viciae-fabae (Pers.) de-Bary), chocolate spot (Botrytis fabae Sardina), downy mildew (Peronospora viciae (Berk.)) and foot rots (Fusarium spp.), which are considered to be major constraints to the crop (Torres et al., 2006; Stoddard et al., 2010; Kharrat and Ouchari, 2011). Importantly, broomrape (Orobanche sp.), a very aggressive parasitic angiosperm, is a relevant damaging and widespread enemy along the Mediterranean basin and Northern Africa (Rubiales et al., 2006; Pérez-de-Luque et al., 2010; Stoddard et al., 2010). There are also viruses (e.g. Bean leaf roll virus, BLRV, and the Bean yellow mosaic virus, BYMV) and nematodes (e.g. Ditylenchus sp.) as biotic constraints to this crop (Stoddard et al., 2010; Kharrat and Ouchari, 2011). These agents vary in incidence and severity on a regional basis.

In relation to pests, more than 70 arthropod species, from a wide diversity of taxonomic groups, have been reported attacking and damaging faba bean, at all stages of plant development, causing both direct and indirect damages, such as the transmission of pathogens (see for example Kamel, 1982; Makkouk and Kumari, 1989; Sadej and Ciepielewska, 2001; Nuessly et al., 2004; Ebadah et al., 2006; Mateus et al., 2007; El-Wakeil and El-Sebai, 2009; Stoddard et al., 2010; Mohapatra et al., 2015). Which pest species are present and their relative abundance are largely dependent on the geographic location of the faba bean crops. Comparing the species listed in different surveys it can be concluded that on a regional basis, insect pest complexes differ in their species composition rather than in the types or taxonomic groups of pests (Stoddard et al., 2010). However, it must be stressed that not all these enemies detected in the crop, damaging it, cause significant economic losses (Nuessly et al., 2004; Stevenson et al., 2007). According to Torres et al. (2006), pests like the black bean aphid (Aphis fabae Scopoly), sitona weevil (Sitona lineatus L.), and bruchid beetle (Bruchus rufimanus Boh.) limit yields if no pest control is employed. Aphids (several species) are probably the most important and damaging insect pests of faba bean world-wide, causing direct damages and also as virus vectors (Blackman and Eastop, 2000, 2007) and their control often dominates faba bean pest management programs.

Generally, faba bean offers a rich foraging habitat for several beneficial insects, both pest enemies (predators and parasitoids) and pollinators (Bugg et al., 1989; Koltowski, 1996; Osborne et al., 1997; Landis et al., 2000; Nuessly et al., 2004; Manning, 2006). One of the reasons is the presence of extrafloral nectaries located on the underside of the stipules, delivering nectar throughout the growing period of the crop, on which this beneficial fauna obtains food resources (Koreshkov, 1967). On the other hand, as referred in El-Wakeil and El-Sebai (2009), the natural susceptibility of faba bean to several pests, attracts a wide diversity of predators and parasitoids; this fauna, if well managed, may enhance the biological control on nearby crops or on those where faba bean is used as a groundcover (see examples in Landis et al., 2000). Faba bean is considered a substitute for the loss of habitat diversity as a result of agricultural intensification (Richards, 2001; Rebek et al., 2005) - this is an important ecological service provided by this crop.

Sources of resistance to faba bean natural enemies

The main focus of the faba bean breeding programs has been to improve yield, quality and reliability of production while minimizing the cost of inputs. Following this objective, efforts have been made to develop good quality lines with resistance to yield-reducing stresses, such as natural enemies. A large genetic variability has already been identified in faba bean in terms of resistance to several biotic and abiotic stresses, which has been collected and preserved in germplasm collections around the world (Torres et al., 2006).

Reviewing literature, it is evident that identification of disease resistance in existing varieties/ cultivars and breeding for disease resistance (or for avoiding high levels of susceptibility) has been a priority around the world. The use of genetic resistance is considered an economical and environmental friendly control method against crop enemies. Potential sources of disease resistance have already been identified (see, for example, Kohpina et al., 2000; Román et al., 2003; Bouhassan et al., 2004; Torres et al., 2006; Duc et al., 2010; Cubero, 2011; Kharrat and Ouchari, 2011; Paull et al., 2011; Villegas-Fernández and Rubiales, 2011; Mahmoud et al., 2015). The same for viruses, nematodes and parasites (Caubel and Leclercq, 1989; Román et al., 2002; Rubiales et al., 2006; Abbes et al., 2007; Duc et al., 2010; Pérez-de-Luque et al., 2010; Murphy-Bokern et al., 2014). However, it has been necessary to implement other disease control measures, because of several negative factors, such as the scarcity and/or complex nature of resistance sources found in faba bean (Rispail et al., 2010; Sillero et al., 2010). Additionally, according to Stoddard et al. (2010), few cultivars show resistance to more than one biotic stress.

Different types of resistance mechanisms can be considered for arthropod pests: (1) Antibiosis resistance affects the biology of the pest, causing increased mortality or reduced longevity and reproduction, and so pest abundance and plant damage is reduced; (2) Antixenosis resistance affects the behaviour of the pest and usually is expressed as non-preference for a resistant plant compared with a susceptible plant; on the other hand, (3) Tolerance is a plant response to a pest, in which a plant is able to withstand or recover from the damage it caused.

In relation to arthropds, references to resistance of faba bean cultivars/varieties are mainly focused on aphids, especially on the black bean aphid, A. fabae, but also on the cowpea aphid, Aphis craccivora (Koch) (Holt and Wratten, 1986; Prüter and Zebitz, 1991; Ebadah et al., 2006; Al-Antary et al., 2007; Shannag and Ababneh, 2007; Hansen et al., 2008; Béji et al., 2015). Other pests have received some attention, as it is the case of the leafminer Liriomyza congesta Becker and the broad bean bruchid B. rufimanus (Ebadah et al., 2006). These last authors’ study evidences that one cultivar may show some level of resistance to an insect pest, being however susceptible (or less resistant) to another species. A variety that exhibits resistance in one locality or environment may be susceptible in another, as a result of the influence of environmental conditions on the physiology of the plants and arthropods.

Conclusions

Faba bean has a relevant role in cropping systems contributing to sustainable alternatives to intensive commercial agriculture. The knowledge on the genetic diversity of faba bean germplasm, recently generated through different molecular markers, should be integrated on the selection of plants in order to develop more cost-effective and less time consuming breeding programs.

The pollination phenomenon was considered important for the production of local crops to promote sustainable development (Diaz et al., 2015). Faba bean is both a model plant for mating system analysis and an important crop for developing novel environmental services, such as pollinator population conservation. Full understanding of the mating system and pollination could answer a wide range of basic and applied questions in breeding. Examining faba bean mating system and pollination diversity is helpful to the choice of appropriate procedures to develop hybrid seed production technology that uses insect-aided natural crossing mechanisms of the crop to increase yield and yield stability heterosis-mediated. Additionally, it also has important significance for questions aiming the transformation towards autogamy for pure line breeding.

Faba bean crop is very susceptible to a high number of enemies, such as arthropod pests, diseases and parasites. Several control methods have been developed to increase yield, quality and reliability of production, which may be used in a complementary way, in an Integrated Pest Management (IPM) approach. Among them is the genetic control, using resistant varieties/ cultivars. Sources of resistance have already been identified for several of those natural enemies.

 

References

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Received/recebido: 2016.07.26

Accepted/aceite: 2016.12.14