Monocrotaline presence in the Crotalaria (Fabaceae) plant genus and its influence on arthropods in agroecosystems

Presença de monocrotalina em plantas do gênero Crotalaria (Fabaceae) e a sua influência sobre artrópodes nos agroecossistemas

Abstract

Crotalaria (Fabaceae) occurs abundantly in tropical and subtropical regions and has about 600 known species. These plants are widely used in agriculture, mainly as cover plants and green manures, in addition to their use in the management of phytonematodes. A striking feature of these species is the production of pyrrolizidine alkaloids (PAs), secondary allelochemicals involved in plant defense against herbivores. In Crotalaria species, monocrotaline is the predominant PA, which has many biological activities reported, including cytotoxicity, tumorigenicity, hepatotoxicity and neurotoxicity, with a wide range of ecological interactions. Thus, studies have sought to elucidate the effects of this compound to promote an increase in flora and fauna (mainly insects and nematodes) associated with agroecosystems, favoring the natural biological control. This review summarizes information about the monocrotaline, showing such effects in these environments, both above and below ground, and their potential use in pest management programs.

Keywords:
pyrrolizidine alkaloids; sunn hemp; arthropods; ecological interactions

Resumo

Crotalaria (Linnaeus, 1753) (Fabaceae) ocorre abundantemente em regiões tropicais e subtropicais e tem cerca de 600 espécies conhecidas. Estas plantas são amplamente utilizadas na agricultura, principalmente como cobertura e adubos verdes, além da sua utilização no manejo de fitonematoides. Uma característica marcante destas espécies é a produção de alcalóides pirrolizidinicos (APs), aleloquímicos secundários envolvidos na defesa das plantas contra os herbívoros. Nas espécies de Crotalaria, a monocrotalina é a AP predominante, que tem muitas atividades biológicas relatadas, incluindo citotoxicidade, tumorigenicidade, hepatotoxicidade e neurotoxicidade, além de uma vasta gama de interações ecológicas. Assim, estudos têm procurado elucidar os efeitos desse composto para promover um incremento na flora e fauna (principalmente insetos e nematoides) associados aos agroecossistemas, favorecendo o controle biológico natural. Esta revisão compila informações sobre a monocrotalina, mostrando tais efeitos nesses ambientes, tanto acima como abaixo do solo e a sua potencial utilização em programas de manejo de pragas.

Palavras-chave:
alcaloides pirrolizidínicos; crotalária; artrópodes; interações ecológicas

1. Introduction

Crotalaria is a genus of the Fabaceae family, it covering about 600 species that are divided into sections based on floral morphology (Flores et al., 2009). Representatives of this genus are well distributed in tropical and subtropical regions in which only a limited number of species occur in temperate regions (Palomino and Vázquez, 1991; Flores and Miotto, 2005; Flores et al., 2009).

Crotalaria species are known to contain non-protein amino acids and pyrrolizidine alkaloids (PAs) in their constitution, and the main compound is called monocrotaline (Mattocks, 1986; Hartmann and Witte, 1995; Wink and Mohamed, 2003; Flores et al., 2009; Schramm et al., 2019). Derived from such plants or in isolation, these PAs have biological activities previously reported, including cytotoxicity, tumorigenicity, hepatotoxicity, and neurotoxicity in humans and animals, and also influencing a wide range of ecological interactions (Culvenor et al., 1976; Boppré, 1990; Brown Junior and Trigo, 1995; Hartmann and Witte, 1995; Hartmann, 1999; Trigo, 2000; Nishida, 2002; Trigo, 2011).

The high concentration of PAs in Crotalaria is responsible for the low palatability and biosynthesis of sexual pheromones in the Utetheisa ornatrix (Linnaeus, 1758) (Lepidoptera: Archiidae) moth, for example (Eisner and Meinwald, 1995; Nishida, 2002; Ferro et al., 2006). Furthermore, Crotalaria species have demonstrated biological activity on phytonematodes (Wang et al., 2002), which has enabled these plants to manage populations of these organisms in agricultural production systems (Boppré and Thoden, 2010; Ntalli and Caboni, 2012).

The cultivation of Crotalaria is widely used in agriculture, mainly, due to the high biomass production and nutrient cycling, especially nitrogen (Lima Filho et al., 2014). In addition, these plants can be inserted in agroecosystems with greater intensity so that they can play an important role in integrated pest and disease management. Whether this effect by the PA content or by increasing the diversity of the local flora, which provides favorable conditions for the establishment and perpetuation of natural biological control, through the biological balance of the environment.

In this review, we analyze some characteristics of the Crotalaria species, especially its chemical composition, relating the influence exerted by such plants on the associated fauna, above and below ground, when inserted in agroecosystems, highlighting their potential use as a cultural management strategy in integrated pest management programs.

2. The Plant Genus Crotalaria: Description and Applications

The plant genus Crotalaria belongs to the Fabaceae family, Papilionideae subfamily and Crotalarieae tribe (Palomino and Vázquez, 1991), which comprises approximately 600 described species (Flores et al., 2009). Most species are native to India (Pacheco and Silva-López, 2010); however, eastern and southern Africa, Mexico, and Brazil can also be highlighted as they are important diversity hubs for these species (Palomino and Vázquez, 1991; Flores et al., 2009). In Brazil, the genus Crotalaria includes 31 native and 11 exotic species, popularly known as “xique-xique” or “guizo de cascavel” because of the rattling sound when the pod is shaken, similar to the rattle of Crotalus sp. (Reptilia: Viperidae) (Tokarnia et al., 2000; Flores et al., 2009; Scupinari et al., 2020).

In general, Crotalaria presents annual, erect, bushy, determinate-growing plants, with simple, alternate, lanceolate to obovate leaves, and a slightly hairy surface and a glabrous stem (Tokarnia et al., 2000; Andrade et al., 2008; Flores and Miotto, 2005; Flores et al., 2009). The flowers are usually yellow, sometimes streaked with red, arranged in showy racemes, calyx larger than the corolla, opening from the base to the top in a staggered fashion. They have an attractive scent and a high concentration of floral resources (nectar and pollen), widely available during the entire flower development, essential characteristics for attracting pollinators and natural enemies (Meagher Junior et al., 2019). The pods are cylindrical 4 to 6 cm in length, and propagation is by seeds, which are small and reniform in shape, with a variation in the color of the tegument (Andrade et al., 2008).

Crotalaria species are easily adaptable to sandy soils with low fertility and can provide increases of up to 100% in the crop yield implanted in succession (Wutke et al., 2014). Thus, they can be found in different environmental conditions, such as areas close to rivers, cliffs, restingas, forest edges, fields and savannas (Garcia et al., 2013). Furthermore, Crotalaria spp. are weeds, which are common in crops and altered locations, such as on roadsides and pastures (Flores and Miotto, 2005).

Crotalaria plants are mainly used in green manure and folk medicine. However, their medicinal use is restricted due to the high content of alkaloids in leaves and seeds, which plays a vital role in the chemical defense of these plants, as they are toxic to vertebrates and unpalatable to some herbivorous insects (Hartmann, 1999; Flores et al., 2009; Pacheco and Silva-López, 2010). However, despite the recognized toxic effect attributed to this class of alkaloids, in some countries (Colombia, for example), Crotalaria species are used in folk medicine (Peñaloza and Peláez, 2008; Pacheco and Silva-López, 2010).

In Brazil, Crotalaria is widely used in agriculture, especially in the Southeast, Northeast and Midwest, although there is a lack of technical information about this application. These plants are mainly used for coverage purposes for biomass production in a no-tillage system or mulching formation (Flores and Miotto, 2005; Garcia et al., 2013; Lima Filho et al., 2014). Furthermore, the use of Crotalaria spp. in consortium with crops of economic interest can be observed, whether for nematode control, pollinator attraction or increased nitrogen supply (Garcia et al., 2013; Lima Filho et al., 2014). In addition to the green manure and cover crop, Crotalaria species are widely used in agriculture to manage phytonematodes in revegetation areas contaminated with toxic substances (such as arsenic, for example) and to produce textile fibers (Garcia et al., 2013). In general, they stand out for their high strength and hardiness, high dry mass production, high nitrogen fixation rate and nutrient cycling (Lima Filho et al., 2014). However, the degree to which these characteristics are expressed varies with species, the planting season, management practices, edaphoclimatic conditions, growing season, and stand (Lima and Castro, 2017).

3. Chemical Composition of Crotalaria: Monocrotaline and Its Role in Defense Against Herbivory

The distribution and adaptability of legumes (Fabaceae) around the world suggests that some biological characteristics promote their establishment and evolutive success. In the most of these plants, distinct classes of chemical compounds can act against herbivores and help to the species establishment throughout the time (Lima et al., 2017).

Plant species of the Crotalaria genus, for example, are known to have high levels of PAs, which, besides being an important line of defense, are potentially hepatotoxic, neurotoxic, and carcinogenic to animals and humans. Generated after ingestion, the effects are characterized by liver and lung damage and clinical neurological signs (Culvenor, 1978; Kempf et al., 2010; Pacheco and Silva-López, 2010). The exact mechanism of the toxicity caused by monocrotaline is not yet determined, but it is known that its biotransformation by the liver into the reactive metabolite of hydromonocrotaline is necessary, which interferes with DNA synthesis and proteins (Butler et al., 1970; Honório Junior et al., 2010).

Phytochemical studies conducted with different Crotalaria species have allowed the identification, isolation and characterization of a large number of secondary metabolites, including several types of alkaloids, such as quinolizidines and pyrrolizidines, in addition to amines, flavonoids, polysaccharides, chalcones, condensed and catechin tannins, lectins, among other substances, such as protease inhibitors, defense peptides (Wink and Mohamed, 2003). Thus, pyrrolizidine alkaloids, chalcones, defense peptides, and protease inhibitors stand out concerning herbivory defense (Pacheco and Silva-López, 2010).

More than 50 PAs have so far been isolated in Crotalaria seeds, which made the occurrence of this class of compounds one of the taxonomic characteristics considered for the division of sections of species of the genus (Flores et al., 2009), that is, used as a chemotaxonomic marker (Table 1).

Table 1
Species belonging to each section of the genus Crotalaria in Brazil, the most abundant type of pyrrolizidine alkaloid (PA) and the degree of specialization of the flowers.

Section	Species	Predominant PA	Flower specialization
Calycinae	C. balanse	Monocrotaline	Standard appendages restricted to the blade and the keel nipple twisted in a spiral
	C. breviflora
	C. flavicoma
	C. grandiflora
	C. hilariana
	C. juncea
	C. martiana
	C. otoptera
	C. paulina
	C. pilosa
	C. stipularia
	C. tweediana
	C. velutiana
	C. vespertilio
Crotalaria	C. mucronata
	C. ochroleuca
	C. retusa
	C. spectabilis
	C. virgulata
Chrysocalycinae	C. harley	Senecionine	No specializations
	C. holosericea
	C. incana
	C. maypurensis
	C. micans
	C. miottoae
	C. reyipila
	C. vitellina
Hedriocarpae	C. lanceolata
	C. pallida
	C. trichotomata

• Adapted from Flores et al. (2009).

In general, Crotalaria species stand out as they produce large amounts of monocrotaline (Hartmann, 1999); however, some species can produce greater amounts of senecionine (Table 1) (Flores et al., 2009). Other PAs, such as junceine, tricodesmine, dehydropyrrolizine, and dicrotaline, may be present in smaller amounts, as in monocrotaline-predominant species, and senecionine and its derivatives may also be identified and vice versa (Mattocks, 1986; Pacheco and Silva-López, 2010). Thus, monocrotaline can represent up to 5% of the dry weight of seeds in some Crotalaria species (Martinez et al., 2014), and the structure of this compound is represented by a retronecine base linked to monocrotalic acid (Martinez et al., 2014).

The production of monocrotaline by Crotalaria can be influenced by some factors, such as water availability, plant nutrition and pest and/or pathogen attack (Schramm et al., 2019), as well as occurs in other species of Fabaceae that produce chemical defense compounds (Almeida-Cortez et al., 2004; Lima et al., 2017). The main site of production of this compound in these plants are the roots (Irmer et al., 2015) and it is known that the dry mass of decaying Crotalaria can release monocrotaline and other compounds present in these plants to the soil, interfering with the diversity of the edaphic fauna (Leal et al., 2018) and soil pests (Oliveira et al., 2007; Gill et al., 2010), in addition to providing the toxic alkaloid to neighboring plants that do not produce these compounds (Nowak et al., 2016).

The quantification of monocrotaline levels present in Crotalaria species has been under-documented. However, a recent study successfully quantified the amount of monocrotaline present in leaves and seeds of C. spectabilis using the HPLC/MS/MS method (Scupinari et al., 2020). The amounts of monocrotaline quantified by the authors in C. spectabilis leaves were 0.141 mg.g^-1 (5.88%), and in the seeds, it was 17.393 mg.g^-1 (3.037%)

Thus, it is known that C. spectabilis plants have a symbiosis with nitrifying bacteria (characterized by the presence of rhizobial nodules) and produce monocrotaline which is not considered functionally involved in symbiosis (Irmer et al., 2015; Schramm et al., 2019). In this study, the absolute amounts of PA per plant were higher in leaves, followed by nodules, roots and stems, while the concentration was higher in nodules (1.97 mg.g^-1 of dry weight), exhibiting a 10-fold concentration higher than in leaves (0.21 mg.g^-1 of dry weight). Despite this, it is known that the plant is the producer of PA and not the microbiont; however, transcripts of the gene responsible for its synthesis (HSS) were detectable only in nodules, indicating that they are the only site of alkaloid biosynthesis and the source from which monocrotaline and other PAs are transported above ground (Schramm et al., 2019). Thus, it is believed that the production of monocrotaline by Crotalaria species can be influenced by the establishment of symbiosis with nitrogen-fixing bacteria (Irmer et al., 2015), in which the amount of the compound is dependent on the plant organ.

In the specific case of monocrotaline in Crotalaria plants, the relationship of this compound with the U. ornatrix moth mentioned above can be cited. In this regard, monocrotaline is assimilated by the insect and used to repel natural enemies, and these compounds are transferred to offspring during copulation (Trigo, 2000; Cogni and Trigo, 2016).

3.1. Pyrrolizidine alkaloids and their effect on associated organisms: what is known so far?

Pyrrolizidine alkaloids are an important class of secondary metabolites (allelochemicals) biosynthesized by a large number of plant species (Martinez et al., 2014). These compounds are particularly found in specimens of Senecioneae and Eupatorieae, within Asteraceae, several genera of Boraginaceae, Apocynaceae, Fabaceae (mainly the genus Crotalaria) and some genera of Orchidaceae (Hartmann and Ober, 2000; Ober and Kaltenegger, 2009; Schramm et al., 2019). Furthermore, PAs are also found in species of Ranunculaceae, Convolvulaceae, Celastraceae, Proteaceae and Poaceae, where they occur in only a few or even a single species (Hartmann and Witte, 1995; Hartmann and Ober, 2000).

Generally, plants produce several types of PAs, usually within the same structural group, and the amount can vary greatly between species and between plants of the same species (plant-plant variation), depending on their physiological state, the environmental conditions, development stage, type of plant tissue, environmental conditions and procedures used for extraction and quantification (Hartmann and Witte, 1995; Flores et al., 2009; Schramm et al., 2019). Thus, reported concentrations of PAs vary greatly from trace amounts to 19% of dry weight (Schramm et al., 2019).

PAs have toxic action and are therefore feared in human and animal diets due to their structural characteristics. These alkaloids are the substrate for cytochrome P450-dependent enzymes, located in the liver in vertebrates, but also in insects (Ober and Kaltenegger, 2009; Schramm et al., 2019). Furthermore, the resulting pyrrolic intermediates exhibit cell toxicity and react with biological nucleophiles such as proteins and nucleic acids (Fu et al., 2004). Not all PAs are toxic, but those affecting human health particularly have esters and unsaturated 1,2-hydroxymethyl-dihydropyrrolizidine (HDP) in their structure (Mattocks, 1986). Potentially toxic PAs exhibit essential characteristics in their structure, such as: (i) an unsaturated pyrrole ring; (ii) one or two hydroxyl groups attached to the ring; (iii) one or two ester groups; and (iv) the branched acid molecule (Pacheco and Silva-López, 2010). Despite their rich diversity, they all share a common structure: they are alkaloids composed of necine esterified with one or more nectic acids (Pacheco and Silva-López, 2010; Schramm et al., 2019).

To date, more than 500 structurally different PAs are known and can be grouped according to the number of ester bonds or according to their base portion (Boppré and Thoden, 2010; Pacheco and Silva-López, 2010). Thus, almost all PAs can be classified into five different major structural groups (Kempf et al., 2010). Thus, toxic PAs comprise a large group of related compounds (about 160 already described) that occur in plants, mainly in species of the genus Crotalaria, Senecio, Heliotropium, Trichodesma, Symphytum, Echium and in other genera related to the Asteraceae and Boraginaceae families, which mainly biosynthesize monocrotaline, senecionine, triangularine, licopsamine and falaeonopsine (Pacheco and Silva-López, 2010).

Regarding the action of PAs on insects, it was shown that they are strong feeding deterrents for many herbivores, in addition to their genotoxic action (Hartmann, 1999) and have a broad defense function against herbivory in plants (Ober and Kaltenegger, 2009; Macel, 2011; Martinez et al., 2014; Schramm et al., 2019). Strong support for the defensive role of PAs includes the adaptations of specialized insects to PA-containing plants, allowing them not only to deal with these plant toxins but also to accumulate them in their body for their own defense (Hartmann and Ober, 2000; Ober and Kaltenegger, 2009). However, the importance of these effects is difficult to measure, and often the most specific observation is that generalist herbivores do not feed on a plant that contains some type of PA (Hartmann, 1999).

The general metabolism of PAs in insects is similar to the metabolism that occurs in humans, including adverse physiological effects (Schramm et al., 2019). Several studies on the effects of individual PAs and general PA content of a given plant in the feeding of specialist and generalist herbivores were conducted, and it was observed that the influence of such a compound on insects depends on the type and concentration of the most abundant PA in the plant tissue (Wei et al., 2015). Furthermore, it is known that generalist herbivores consume PA-containing plants only in times of scarcity of nutritionally adequate food, whereas adapted insects are believed to be attracted (Hartmann, 1999; Cheng et al., 2013).

In the same way, insects can convert and store this PA load, maintaining them in the form of non-toxic alkaloids, and this modification is carried out in the intestine, and the compounds from this process are adsorbed as tertiary alkaloids (Hartmann, 1999; 2004). These, in turn, are synthesized exclusively in the form of N-oxide, which is the specific molecular form for long-distance translocation and storage in the vacuole. In this form, N-oxide, are incorporated by insects (Hartmann, 1999; Brückmann et al., 2000).

Thus, herbivorous insects have evolved through numerous adaptations to overcome the defensive barrier of PA-protected plants and to overcome the defensive barrier of PA-protected plants and sequestrate them and use them for their own defense against predators (Hartmann and Witte, 1995). These alkaloids are accumulated and used by various insects in various processes, such as chemical defense in which they become deterrent food or acquire aposematic coloring against predatory invertebrates such as spiders, ants, coccinellids, and wasps (Nishida, 2002). Moreover, some males can convert their alkaloid charge through a signaling process, providing females with a way to discriminate between males that have the alkaloid and males without them (Trigo, 2011).

Concerning PA N-oxide storage, insects developed a strategy to use these allelochemicals for their own defense against predators. An example of this adaptation is the neotropical Ithomiinae butterflies which, unlike moths, do not feed on PA plants or sequester them from the larval stage but absorb PAs exclusively through nectar or dry twigs (Macel et al., 2005; Schramm et al., 2019). This habitat protects them from the Nephila clavipes (Linnaeus, 1757) (Aranae: Nephilidae) spider, eliminating butterflies that have already ingested PAs from their own net (Silva and Trigo, 2002; Schramm et al., 2019). Sequestered PAs play an important role in the mating process of some tribes of the Lepidoptera family because they serve as a precursor to male pheromones (Boppré, 1990). This is also the case of the African grasshopper, Zonocerus variegatus (Linnaeus, 1758) (Orthoptera: Pyrgomorphidae), which, due to N-oxidation and accumulation of PAs in its hemolymph, circumvents the chemical defense of plants and uses the compost to protect itself against predators (Kubitza et al., 2018).

Through the described mechanisms, specialized insects can take advantage of plants containing PAs (Joshi and Vrieling, 2005) through: (i) specific sensory recognition for a given PA in the host; (ii) biochemical mechanisms to ingest, maintain, metabolize, accumulate and transfer alkaloids under controlled physiological conditions and; (iii) alkaloid-guided mating behavior (Hartmann, 2004).

In addition to their contribution to defense against insects, PAs also influence plant interactions with fungi, with an inhibitory effect on Fusarium and Trichoderma (Hol and Van Veen, 2002). Plants that have beneficial interactions with microorganisms, especially mycorrhizal fungi, and nitrogen-fixing bacteria, influence the PA synthesis process, affecting the production and concentration of these compounds, which generally start to be produced in larger quantities released into the soil later (Schramm et al., 2019). From that moment, plants that do not produce PAs, when cultivated in the same place, can absorb and accumulate these compounds through the roots, either if they grow concomitantly with PA-producing plants or if they grow under their decomposing dry mass (Nowak et al., 2016).

4. Crotalaria in Agroecosystems: Effects on Associated Organisms

Regarding the influence of Crotalaria on the fauna associated with agricultural crops, four characteristics that are possibly related to its activity can be listed: (i) floral characteristics (Meagher Junior et al., 2019); (ii) the presence of monocrotaline above ground (Hartmann, 1999; Scupinari et al., 2020); (iii) the peculiarities of its root system (Wang et al., 2002; Irmer et al., 2015; Leal et al., 2018) and; (iv) and dry mass decomposition products (straw) (Oliveira et al., 2007; Gill et al., 2010; Nowak et al., 2016) (Figure 1). A summary of the main effects of the Crotalaria species on the associated fauna is shown in Table 2.

Figure 1
Influence of Crotalaria (Fabaceae) species on the associated fauna in agroecosystems: (a) inflorescence; (b) leaves and seeds; (c) roots; and (d) organic matter. According to ^[1]Meagher Junior et al. (2019); ^[2]Irmer et al. (2015); ^[3]Wang et al. (2002); ^[4]Leal et al. (2018); ^[5]Hartmann (1999); ^[6]Scupinari et al. (2020); ^[7]Nowak et al. (2016); ^[8]Oliveira et al. (2007) and Gill et al. (2010).

Table 2
Effects of Crotalaria species on the arthropods associated with agroecosystems.

Observed effect	Crotalaria species	Affected organisms			Reference
		Order	Family	Specie
Pollinator attraction	C. micans	Hymenoptera	Apidae	Apis melífera	Villalobos and Ramirez (2010)
				Xylocopa spp.
	C. juncea			Bombus morio	Krueger et al. (2008)
			Megachilidae	Megachile sculpturalis	Hall and Ávila (2016)
				Megachile lanata	Henson et al. (2019)
				Megachile bicolor	Meagher Junior et al. (2019)
				Megachile georgica
				Megachile mendica
			Apidae	Xylocopa virginica
				Xylocopa micans
	C. retusa			Xylocopa frontalis	Jacobi et al. (2005)
				Xylocopa grsescens
	C. spectabilis			Apis melífera	Marchini et al (2001)
				Xylocopa sp.	Henrique and Figueiredo (2018)
	C. vitellina		Halictidae	Augoclora sp.	Brito et al. (2010)
			Megachilidae	Megachile spp.
			Apidae	Trigona sp.
				Xylocopa brasilianorum
Increase of natural enemies populations	C. juncea	Hymenoptera	Trichogrammatidae	Trichogramma spp.	Manandhar and Wright (2016)
					Wright (2019)
				Trichogramma papilionis	Ali and Wright (2020)
		Dermaptera	Forficulidae	Doru luteipes	Tavares et al (2011)
		Coleoptera	Coccinellidae	Eriopis connexa
		Aranae	Nephilidae	Nephila clavipes
		Neuroptera	Chrysopidae	Chrysoperla externa	Venzon et al. (2006)
		Aranae	-	-	Lima and Castro (2017)
		Coleoptera	Coccinellidae	-
		Diptera	Asilidae	-
			Dolichopodidae	-
		Hymenoptera	Encyrtidae	-
			Vespidae	-
	C. lanceollata	Coleoptera	Coccinellidae	Hippodamia convergens	McSorley et al. (2009)
		Diptera	Asilidae	Neiotamus spp.
	C. ochroleuca	Hymenoptera	Trichogrammatidae	Trichogramma spp.	Wright (2019)
	C. spectabilis			Trichogramma spp.	Trisnawati and Azis (2017)
					Wright (2019)
		Hemiptera	Pentatomidae	Orus insidiosus	McSorley et al. (2009)
Pest attack/damage reduction	C. juncea	Lepidoptera	Noctuidae	Spodoptera frugiperda	Dias et al. (2016)
					Guera et al. (2020)
			Pyralidae	Elasmopalpus lignosellus	Gill et. al. (2010)
		Hemiptera	Aleyrodidae	Bemisia argentifolli	Manandhar et al. (2009)
		Coleoptera	Scarabeidae	Phyllophaga cuyabana	Oliveira and Garcia (2003)
					Oliveira et al. (2007)
			Vesperidae	Migdolus fryanus	Bento et al. (2020)
		Thysanoptera	Thripidae	Thrips tabaci	Quintanilla-Tornel et al. (2016)
		Hemiptera	Aphididae	-	Hinds and Hooks (2013)
					Manandhar and Hooks (2011)
	C. pallida	Lepidoptera	Noctuidae	Heliothis virescens	Cogni and Trigo (2016)
	C. spectabilis			Helicoverpa armigera	Reigada et al. (2016)
			-	-	Burkart (1952)
Sequestration of monocrolatine for defense	C. juncea	Lepidoptera	Arctiidae	Utetheisa ornatrix	Hartmann (1999)
	C. spectabilis				Schramm et al. (2019)
					Trigo (2000)
Reduction of nematode population	C. juncea	-	-	Heterodera glycines	Acharya et al. (2020)
		-	-	Pratylenchus brachyurus	Mathew and Opperman (2020)
		-	-	Meloidogyne incognita	Ferreira et al. (2020)
		-	-	Meloidogyne javanica
	C. spectabilis	-	-	Rotylenchulus reniformis	El-Deriny et al. (2020)

The floral characteristics of Crotalaria are an important factor for the attractiveness of pollinators and natural enemies as they have many flowers at different developmental stages, with vibrant and attractive yellow flowers, in addition to the high availability of pollen and nectar (Meagher Junior et al., 2019). Several pollinator species have been observed to occur in Crotalaria species, including Apis mellifera (Linnaeus, 1758) (Hymenoptera: Apidae) (Marchini et al., 2001; Villalobos and Ramírez, 2010; Henrique and Figueiredo, 2018), Xylocopa virginica (Linnaeus, 1771) (Hymenoptera: Apidae) and X. micans (Lepeletier, 1841) (Henrique and Figueiredo, 2018; Meagher Junior et al., 2019), X. brasilianorum (Linnaeus, 1767) (Brito et al., 2010), X. frontalis (Olivier, 1789) and X. grisesncens (Lepeletier, 1841) (Jacobi et al., 2005; Henrique and Figueiredo, 2018), Megachile mendica (Cresson. 1878) (Hymenoptera: Megachilidae), M. lanata (Fabricius, 1775) and M. sculpturalis (Smith, 1853) (Hall and Avila, 2016; Meagher Junior et al., 2019), M. bicolor (Fabricius, 1781) and M. georgica (Cresson, 1878) (Meagher et al., 2019), Augochlora sp. (Smith, 1853) (Hymenoptera: Halictidae) (Brito et al., 2010), Bombus morio (Swederus, 1787) (Hymenoptera: Apidae) (Krueger et al., 2008) and Trigona sp. (Jurine, 1807) (Hymenoptera: Apidae) (Brito et al., 2010; Henrique and Figueiredo, 2018). This increase in the population of pollinators has conditioned a significant increase in the production of agricultural crops intercropped with Crotalaria species. In this context, the increase in the number of soybean pods (Glycine max L., Fabaceae) (Sholahuddin et al., 2019) and coffee pods (Coffea spp. L., Rubiaceae) (Setyawati et al., 2018; Supriyad et al., 2019) when cultivated in consortium with Crotalaria juncea stands out, which is a factor attributed to greater abundance of pollinators.

The attractiveness of Crotalaria plants also extends to natural enemies, which was already observed for several species of the genus. For example, C. juncea caused attraction of natural enemies in some crops, such as cowpea (Vigna unguiculata L., Fabaceae), corn (Zea mays L., Poaceae) and a variety of fruit trees (Trisnawati and Azis, 2017). This increase in the population of natural enemies was also observed in other studies, which found a significant increase in the number of chrysopids (Chrysoperla externa Hagen, 1861 (Neuroptera: Chrysopidae)), earwigs (Doru luteipes Scudder, 1876 (Dermaptera: Forficulidae)), spiders (Nephila clavipes (Araneae: Nephilidae)) and stink bugs (Orius insidiosus Say, 1832 (Hemiptera: Anthocoridae)) in Crotalaria in the single cultivation and in the consortia (Venzon et al., 2006; Tavares et al., 2011). Moreover, in this context, another study pointed out that Trichograma papilionis (Nagarkatti, 1974) (Hymenoptera: Trichogrammatidae) preferred to parasitize Helicoverpa zea (Boddie, 1850) (Lepidoptera: Noctuidae) eggs deposited on C. juncea than on corn (Z. mays), suggesting that there may be interference from semiochemical volatiles released from the plants when the eggs are placed on the leaves (Ali and Wright, 2020).

In turn, the presence of monocrotaline in plants influences the establishment and development of pests associated with crops (Hartmann, 1999), whether in crop rotation/succession or in polycultures or intercrops, in which the roots were the main production site of this compound in plants (Irmer et al., 2015). The decomposing dry mass of Crotalaria can release monocrotaline and other compounds present in these plants into the soil, interfering with the diversity of the edaphic fauna (Leal et al., 2018) and soil pests (Oliveira et al., 2007; Gill et al., 2010), in addition to providing the toxic alkaloid to neighboring plants that do not produce these compounds (Nowak et al., 2016).

Regarding pest control, studies show that Crotalaria plants affect herbivores in different situations, affecting their biology and development, as well as the behavior of associated herbivores (Dias et al., 2016). When it consisted of the only food available, different Crotalaria species significantly reduced the survival of Spodoptera frugiperda (Dias et al., 2016), Helicoverpa armigera (Reigada et al., 2016), and Heliothis virescens (Fabricius, 1777) (Lepidoptera: Noctuidae) (Cogni and Trigo, 2016) in laboratory studies.

When cultivated in an intercropped way with crops of economic interest, Crotalaria reduced the occurrence of pests. In pumpkin (Cucurbita pepo L., Cucurbitaceae) crops, the consortia with C. juncea reduced the occurrence of aphids and beetle-pests and provided an increase in the population of predators such as spiders (Hinds and Hooks, 2013). Similarly, studies have shown that Crotalaria in consortia with pumpkin reduced the incidence of whitefly (Bemisia argentifolli Bellows & Perring, 1994 (Hemiptera: Aleyrodidae)), while also reducing the incidence of the pumpkin mosaic virus, which is transmitted by the aforementioned insect (Manandhar et al., 2009; Manandhar and Hooks, 2011).

In this context, Crotalaria plants can be used in push-pull systems, as in the study conducted by Guera et al. (2020), who associated C. juncea with corn. As a result, the authors observed that when in intercrop, C. juncea made corn less attractive to fall S. frugiperda (Smith & Abbot, 1797), under laboratory and greenhouse conditions.

Among other cultivation modalities, whether in intercropping or crop rotation/succession, Crotalaria plants can be used to form mulching, that is mulch for the soil. In this system, it was observed that C. juncea mulching reduced the damage caused by thrips (Thrips tabaci Lindeman, 1889 (Thysanoptera: Thripidae) and leafminer (Liriomyza spp. Mik, 1894 (Diptera: Agromyzidae)) in the onion (Allium cepa L., Amaryllidaceae) crop (Quintanilla-Tornel et al., 2016). Moreover, in that same study, there was an increase in the diversity and richness of associated species, especially in the population of predators and parasitoids, particularly spiders.

Another potential use for Crotalaria plants is as a trap crop, to attract or repel pests, natural enemies and other organisms in cropping systems (Santos et al., 2008). The attraction of some groups of insects is due to the characteristics of the plant, such as the architecture of the stems and high ground cover. These factors have favored populations of organisms by increasing humidity and reducing the temperature, providing areas of refuge and shelter for parasitoids and predators, in addition to mites and beneficial nematodes (McSorley et al., 2009).

The negative effect on insect pests can be direct (repellent effect) or indirect, by attracting natural enemies, which affect the herbivore population (Smith and McSorley, 2000). These effects were observed in citrus crops, where C. spectabilis plants were attractive to caterpillars (Burkart, 1952), and in tobacco (Nicotiana tabacum L., Solanaceae) crops, where C. juncea plants acted as a trap to attract natural enemies throughout the whole culture cycle (Trisnawati and Azis, 2017).

Regarding the specific effect of monocrotaline on insects, U. ornatrix stands out. Males of U. ornatrix have a court pheromone, which is derived from pyrrolizidine alkaloids ingested in the larval stage of the host plant, C. spectabilis (Trigo, 2000). U. ornatrix larvae sequester pyrrolizidine alkaloids (monocrotaline) and retain them during the developmental stages. When an adult, the alkaloid derivative is transferred to the female during copulation, via spermatophore, and in oviposition, it transfers the alkaloids to the eggs, serving as protection (Trigo, 2000; Cogni and Trigo, 2016).

Regarding the fauna that inhabits the soil, there was an increase in the number of insects captured in pitfall traps in C. spectabilis and C. ochroleuca cultivation sites (Leal et al., 2018). An increase in the mesofauna and a greater diversification of the macrofauna were also observed, in which the order Hymenoptera was the one with the most captured representatives (Leal et al., 2018). Thus, regarding soil pest control, studies show that Crotalaria plants act on rhizophagous pests, such as Phyllophaga cuyabana (Moser, 1918) (Coleoptera: Melolonthidae) white grubs, which prefer to feed on C. juncea instead of on other cultures, highlighting the importance of intercropping with cultures where this insect-pest occurs (Oliveira and Garcia, 2003; Oliveira et al., 2007). Furthermore, Crotalaria plants increased the mortality of Elasmopalpus lignosellus (Zeller, 1848) (Lepidoptera: Pyralidae) pupae in soil covered with C. juncea mulching (Gill et al., 2010).

In addition to these characteristics mentioned so far, it is worth noting that Crotalaria plants are the most used green manures for the management of phytonematode (Inomoto and Asmus, 2014), and the efficiency in controlling such pests can be explained by the high amounts of monocrotaline present in plants (Scupinari et al., 2020). Thus, several experiments demonstrate that Crotalaria of different species, in different arrangements (single cultivation or consortia) and conditions (field or laboratory), affected important species of phytonematodes, such as Meloidogyne incognita (Kofoid & White, 1919) and Meloidogyne javanica (Treub, 1885) (Rhabditida: Meloidoginidae) (Ferreira et al., 2020), Heterodera glycines (Rhabditida: Heteroderidae) (Ichinohe, 1952) (Acharya et al., 2020), Pratylenchus brachyurus (Godfrey, 1829) (Rhabditida: Pratylenchidae) (Mathew and Opperman, 2020) and Rotylenchulus reniformis (Rhabditida: Rotylencgulidae)(Linford & Oliveira, 1940) (El-Deriny et al., 2020).

Crotalaria interactions with phytonematodes can occur in the following ways: (i) as a non-host or poor host; (ii) producing toxic allelochemicals or inhibitors; (iii) providing a niche for antagonistic fauna and flora; or (iv) trapping the nematode (Wang et al., 2002). However, the resistance mechanism in Crotalaria varies between plant species and target nematodes (Wang et al., 2002; Boppré and Thoden, 2010; Ntalli and Caboni, 2012; Scupinari et al., 2020). In addition, the contribution of biomass provided by Crotalaria to the soil generates a large increase in organic matter, which is considered an ally in nematode management, as decomposing organic material favors an increase in the population of nematophagous fungi and bacteria, in addition to the incidence of predatory nematodes (Wang et al., 2002).

The information cited so far gives support to highlight the potential use of Crotalaria species in maintaining biological control in agricultural areas, called conservative biological control. Since, the increase in plant diversity in an agroecosystem, by itself, is able to assist in maintaining the population of natural enemies and, consequently, reduce the number of potential pests individuals (Freitas and Mantovani, 2018).

5. Conclusion

Plants of the Crotalaria genus have been used for various purposes in agriculture and industry. Considering the facts presented throughout this review, we highlight the potential use of Crotalaria species in agroecosystems, whether in crop rotation/succession, in intercropping systems or as a trap crop, in crops in large areas (conventional), or even in cropping systems of organic or agroecological production, especially as a cultural management strategy in integrated pest management programs. However, further studies are needed concerning the concentration of monocrotaline in Crotalaria species and the elucidation of the effects of this compound on the main pest insects affecting the crops to be protected.

Still, despite the high concentration of PAs, few studies have been conducted on the pharmacological and biotechnological applicability of those isolated substances of this genus. Therefore, the study of new molecules and those previously isolated from Crotalaria constitutes a new and wide field of investigation on the functions of these components and their potential application in therapeutic treatments and as an insecticide.

Acknowledgements

The authors would like to thank the anonymous reviewers for their helpful comments. This research was supported by the National Institute of Science and Technology – Semiochemicals in Agriculture (FAPESP and CNPq – grants #2014/50871-0 and #465511/2014-7, respectively).

References

• ACHARYA, K., YAN, G. and BERTI, M.T., 2020. Evaluation of diverse cover crops as hosts of two populations of soybean cyst nematode, Heterodera glycines. Crop Protection, vol. 135, pp. 105-205. http://dx.doi.org/10.1016/j.cropro.2020.105205
  » http://dx.doi.org/10.1016/j.cropro.2020.105205
• ALI, A.N. and WRIGHT, M.G., 2020. Behavioral response of Trichogramma papilionis in response to host eggs, host plants, and induced volatile plant cues. Biological Control, vol. 149, pp. 104-123. http://dx.doi.org/10.1016/j.biocontrol.2020.104323
  » http://dx.doi.org/10.1016/j.biocontrol.2020.104323
• ALMEIDA-CORTEZ, J.S., SHIPLEY, B. and ARNASON, J.T., 2004. Growth and chemical defense in relation to resource availability: tradeoffs or common responses to environmental stress? Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 64, no. 2, pp. 187-194. http://dx.doi.org/10.1590/S1519-69842004000200002 PMid:15462290.
  » http://dx.doi.org/10.1590/S1519-69842004000200002
• ANDRADE, D.A.V.D., ORTOLANI, F.A., MORO, J.R. and MORO, F.V., 2008. Aspectos morfológicos de frutos e sementes e caracterização citogenética de Crotalaria lanceolata (Papilionoideae-Fabaceae). Acta Botanica Brasílica, vol. 22, no. 3, pp. 621-625. http://dx.doi.org/10.1590/S0102-33062008000300003
  » http://dx.doi.org/10.1590/S0102-33062008000300003
• BENTO, J.M.S., ARRIGONI, E.B., DELLA LUCIA, T.M.C., VILELA, E.F. and LEAL, W.S., 2020. Migdolus In: J.R. SALVADORI, C.J. ÁVILA and M.T.B. SILVA, eds. Pragas de solo no Brasil Passo Fundo: Aldeia Norte Editora Ltda., pp. 309-330.
• BOPPRÉ, M. and THODEN, T., 2010. Plants producing pyrrolizidine alkaloids: sustainable tools for nematode management? Nematology, vol. 12, no. 1, pp. 1-24. http://dx.doi.org/10.1163/138855409X12549869072248
  » http://dx.doi.org/10.1163/138855409X12549869072248
• BOPPRÉ, M., 1990. Lepidoptera and pyrrolizidine alkaloids exemplification of complexity in chemical ecology. Journal of Chemical Ecology, vol. 16, no. 1, pp. 165-185. http://dx.doi.org/10.1007/BF01021277 PMid:24264905.
  » http://dx.doi.org/10.1007/BF01021277
• BRITO, V.L.G.D., PINHEIRO, M. and SAZIMA, M., 2010. Sophora tomentosa e Crotalaria vitellina (Fabaceae): biologia reprodutiva e interações com abelhas na restinga de Ubatuba, São Paulo. Biota Neotropica, vol. 10, no. 1, pp. 185-192. http://dx.doi.org/10.1590/S1676-06032010000100019
  » http://dx.doi.org/10.1590/S1676-06032010000100019
• BROWN JUNIOR, K.S. and TRIGO, J.R., 1995. The ecological activity of alkaloids. In: G.A. CORDELL, ed. The alkaloids: chemistry and pharmacology. London: Academic Press, pp. 227-354.
• BRÜCKMANN, M., TRIGO, J.R., FOGLIO, M.A. and HARTMANN, T., 2000. Storage and metabolism of radioactively labeled pyrrolizidine alkaloids by butterflies and larvae of Mechanitis polymnia (Lepidoptera: Nymphalidae, Ithomiinae). Chemoecology, vol. 10, no. 1, pp. 25-32. http://dx.doi.org/10.1007/s000490050004
  » http://dx.doi.org/10.1007/s000490050004
• BURKART, A., 1952. Las leguminosas argentinas silvestres y cultivadas 2nd ed. Buenos Aires: ACME Agency, 590 p.
• BUTLER, W., MATTOCKS, A. and BARNES, A., 1970. Lesions in the liver and lungs of rats given pyrrole derivatives of pyrrolizidine alkaloids. The Journal of Pathology, vol. 100, no. 3, pp. 169-175. http://dx.doi.org/10.1002/path.1711000305 PMid:5428936.
  » http://dx.doi.org/10.1002/path.1711000305
• CHENG, D., VAN DER MEIJDEN, E., MULDER, P.P., VRIELING, K. and KLINKHAMER, P.G., 2013. Pyrrolizidine alkaloid composition influences cinnabar moth oviposition preferences in Jacobaea hybrids. Journal of Chemical Ecology, vol. 39, no. 3, pp. 430-437. http://dx.doi.org/10.1007/s10886-013-0257-4 PMid:23435642.
  » http://dx.doi.org/10.1007/s10886-013-0257-4
• COGNI, R. and TRIGO, J., 2016. Pyrrolizidine alkaloids negatively affect a generalist herbivore feeding on the chemically protected legume Crotalaria pallida. Neotropical Entomology, vol. 45, no. 3, pp. 252-257. http://dx.doi.org/10.1007/s13744-016-0361-6 PMid:26830432.
  » http://dx.doi.org/10.1007/s13744-016-0361-6
• CULVENOR, C., 1978. Pyrrolizidine alkaloids-occurrence and systematic importance in angiosperms. Botaniska Notiser, vol. 131, pp. 473-486.
• CULVENOR, C., EDGAR, J., JAGO, M., QUTTERIDGE, A., PETERSON, J. and SMITH, L., 1976. Hepato-and pneumotoxicity of pyrrolizidine alkaloids and derivatives in relation to molecular structure. Chemico-Biological Interactions, vol. 12, no. 3-4, pp. 299-324. http://dx.doi.org/10.1016/0009-2797(76)90046-6 PMid:1253333.
  » http://dx.doi.org/10.1016/0009-2797(76)90046-6
• DIAS, A.S., MARUCCI, R.C., MENDES, S.M., MOREIRA, S.G., ARAÚJO, O.G., SANTOS, C.A. and BARBOSA, T.A., 2016. Bioecology of Spodoptera frugiperda (Smith, 1757) in different cover crops. Bioscience Journal, vol. 32, no. 2, pp. 337-345. http://dx.doi.org/10.14393/BJ-v32n2a2016-29759
  » http://dx.doi.org/10.14393/BJ-v32n2a2016-29759
• EISNER, T. and MEINWALD, J., 1995. The chemistry of sexual selection. Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 1, pp. 50-55. http://dx.doi.org/10.1073/pnas.92.1.50 PMid:7816847.
  » http://dx.doi.org/10.1073/pnas.92.1.50
• EL-DERINY, M.M., IBRAHIM, D.S. and MOSTAFA, F.A., 2020. Organic additives and their role in the phytoparasitic nematodes management. In: R. ANSARI, R. RIZVI and I. MAHMOOD, eds. Management of Phytonematodes: recent advances and future challenges. Singapure: Springer, pp 73-93. http://dx.doi.org/10.1007/978-981-15-4087-5_4
  » http://dx.doi.org/10.1007/978-981-15-4087-5_4
• FERREIRA, P.S., TORRES, J.L.R., SANTOS, M.A., PAROLINI, R.O. and LEMES, E.M., 2020. Host suitability of cover crops for Meloidogyne javanica and M. incognita. Nematology, vol. 22, no. 6, pp. 659-666. http://dx.doi.org/10.1163/15685411-00003329
  » http://dx.doi.org/10.1163/15685411-00003329
• FERRO, V.G., GUIMARÃES JUNIOR, P.R. and TRIGO, J.R., 2006. Why do larvae of Utetheisa ornatrix penetrate and feed in pods of Crotalaria species? Larval performance vs. chemical and physical constraints. Entomologia Experimentalis et Applicata, vol. 121, no. 1, pp. 23-29. http://dx.doi.org/10.1111/j.1570-8703.2006.00450.x
  » http://dx.doi.org/10.1111/j.1570-8703.2006.00450.x
• FLORES, A.S. and MIOTTO, S.T.S., 2005. Phytogeographic aspects of the Crotalaria L. species (Leguminosae, Faboideae) in Southern Brazil. Acta Botanica Brasílica, vol. 19, no. 2, pp. 245-249. http://dx.doi.org/10.1590/S0102-33062005000200006
  » http://dx.doi.org/10.1590/S0102-33062005000200006
• FLORES, A.S., TOZZI, A.M.G.A. and TRIGO, J.R., 2009. Pyrrolizidine alkaloid profiles in Crotalaria species from Brazil: chemotaxonomic significance. Biochemical Systematics and Ecology, vol. 37, no. 4, pp. 459-469. http://dx.doi.org/10.1016/j.bse.2009.06.001
  » http://dx.doi.org/10.1016/j.bse.2009.06.001
• FREITAS, J.R. and MANTOVANI, W., 2018. An overview of the applicability of functional diversity in biological conservation. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 78, no. 3, pp. 517-524. http://dx.doi.org/10.1590/1519-6984.09416 PMid:29069162.
  » http://dx.doi.org/10.1590/1519-6984.09416
• FU, P.P., XIA, Q., LIN, G. and CHOU, M.W., 2004. Pyrrolizidine alkaloids: genotoxicity, metabolism enzymes, metabolic activation, and mechanisms. Drug Metabolism Reviews, vol. 36, no. 1, pp. 1-55. http://dx.doi.org/10.1081/DMR-120028426 PMid:15072438.
  » http://dx.doi.org/10.1081/DMR-120028426
• GARCIA, J.M., KAWAKITA, K., MIOTTO, S.T.S. and SOUZA, M.C., 2013. O gênero Crotalaria L.(Leguminosae, Faboideae, Crotalarieae) na planície de inundação do Alto Rio Paraná, Brasil. Revista Brasileira de Biociências, vol. 11, no. 2, pp. 209-226.
• GILL, H.K., MCSORLEY, R., GOYAL, G. and WEBB, S.E., 2010. Mulch as a potential management strategy for lesser cornstalk borer, Elasmopalpus lignosellus (Insecta: Lepidoptera: Pyralidae), in bush bean (Phaseolus vulgaris). The Florida Entomologist, vol. 93, no. 2, pp. 183-190. http://dx.doi.org/10.1653/024.093.0206
  » http://dx.doi.org/10.1653/024.093.0206
• GUERA, O.G.M., CASTREJÓN-AYALA, F., ROBLEDO, N., JIMÉNEZ-PÉREZ, A. and SÁNCHEZ-RIVERA, G., 2020. Plant selection for the establishment of push–pull strategies for Zea mays-Spodoptera frugiperda pathosystem in Morelos, Mexico. Insects, vol. 11, no. 6, pp. 349. http://dx.doi.org/10.3390/insects11060349 PMid:32512789.
  » http://dx.doi.org/10.3390/insects11060349
• HALL, H. and AVILA, L., 2016. Megachile sculpturalis, the giant resin bee, overcomes the blossom structure of sunn hemp (Crotalaria juncea) that impedes pollination. Journal of Melittology, vol. 65, no. 65, pp. 1-11. http://dx.doi.org/10.17161/jom.v0i65.5887
  » http://dx.doi.org/10.17161/jom.v0i65.5887
• HARTMANN, T. and OBER, D., 2000. Biosynthesis and metabolism of pyrrolizidine alkaloids in plants and specialized insect herbivores. In: F. LEEPER and J. VEDREREAS, eds. Biosynthesis: topics in current chemistry Berlin: Springer, pp. 207-243. http://dx.doi.org/10.1007/3-540-48146-X_5
  » http://dx.doi.org/10.1007/3-540-48146-X_5
• HARTMANN, T. and WITTE, L., 1995. Chemistry, biology and chemoecology of the pyrrolizidine alkaloids. In: S. PELLETIER, ed. Alkaloids: chemical and biological perspectives Oxford: Pergamino, pp. 155-233.
• HARTMANN, T., 1999. Chemical ecology of pyrrolizidine alkaloids. Planta, vol. 207, no. 4, pp. 483-495. http://dx.doi.org/10.1007/s004250050508
  » http://dx.doi.org/10.1007/s004250050508
• HARTMANN, T., 2004. Plant-derived secondary metabolites as defensive chemicals in herbivorous insects: a case study in chemical ecology. Planta, vol. 219, no. 1, pp. 1-4. http://dx.doi.org/10.1007/s00425-004-1249-y PMid:15042370.
  » http://dx.doi.org/10.1007/s00425-004-1249-y
• HENRIQUE, M.O. and FIGUEIREDO, R.A., 2018. Ecologia reprodutiva de crotalária (Crotalaria spectabilis Roth, Fabaceae) em área de cultivo agroecológico. Revista Verde de Agroecologia e Desenvolvimento Sustentável, vol. 13, no. 3, pp. 385-391. http://dx.doi.org/10.18378/rvads.v13i3.5425
  » http://dx.doi.org/10.18378/rvads.v13i3.5425
• HENSON, K.A., CAMPBELL, J.W. and KAPLAN, D.A., 2019. Range extension of Megachile lanata (Hymenoptera: Megachilidae), a non-native sunn hemp pollinator, in Florida. The Florida Entomologist, vol. 102, no. 1, pp. 259-261. http://dx.doi.org/10.1653/024.102.0148
  » http://dx.doi.org/10.1653/024.102.0148
• HINDS, J. and HOOKS, C.R.R., 2013. Population dynamics of arthropods in a sunn-hemp zucchini interplanting system. Crop Protection, vol. 53, pp. 6-12. http://dx.doi.org/10.1016/j.cropro.2013.06.003
  » http://dx.doi.org/10.1016/j.cropro.2013.06.003
• HOL, W. and VAN VEEN, J., 2002. Pyrrolizidine alkaloids from Senecio jacobaea affect fungal growth. Journal of Chemical Ecology, vol. 28, no. 9, pp. 1763-1772. http://dx.doi.org/10.1023/A:1020557000707 PMid:12449504.
  » http://dx.doi.org/10.1023/A:1020557000707
• HONÓRIO JÚNIOR, J.E.R., SOARES, P.M., MELO, C.L., ARRUDA FILHO, A.C.V., SENA FILHO, J.G., BARBOSA FILHO, J.M., SOUSA, F.C.F., FONTELES, M.M.F., LEAL, L.K.A., QUEIROZ, M.G.R. and VASCONCÊLOS, S.M.M., 2010. Atividade farmacológica da monocrotalina isolada de plantas do gênero Crotalaria. Revista Brasileira de Farmacognosia, vol. 20, no. 3, pp. 453-458. http://dx.doi.org/10.1590/S0102-695X2010000300025
  » http://dx.doi.org/10.1590/S0102-695X2010000300025
• INOMOTO, M.M. and ASMUS, G.L., 2014. Adubos verdes das família Fabaceae e Mimosaceae para o controle de fitonematóides. In: O. LIMA FILHO, E. AMBROSANO, F. ROSSI and J. CARLOS, eds. Adubação verde e plantas de cobertura no Brasil: fundamentos e prática. Brasília: EMBRAPA, pp. 441-479.
• IRMER, S., PODZUN, N., LANGEL, D., HEIDEMANN, F., KALTENEGGER, E., SCHEMMERLING, B., GEILFUS, C.M., ZÖRB, C. and OBER, D., 2015. New aspect of plant–rhizobia interaction: alkaloid biosynthesis in Crotalaria depends on nodulation. Proceedings of the National Academy of Sciences of the United States of America, vol. 112, no. 13, pp. 4164-4169. http://dx.doi.org/10.1073/pnas.1423457112 PMid:25775562.
  » http://dx.doi.org/10.1073/pnas.1423457112
• JACOBI, C.M., RAMALHO, M. and SILVA, M., 2005. Pollination biology of the exotic rattleweed Crotalaria retusa L. (Fabaceae) in Northwest Brazil. Biotropica, vol. 37, no. 3, pp. 357-363. http://dx.doi.org/10.1111/j.1744-7429.2005.00047.x
  » http://dx.doi.org/10.1111/j.1744-7429.2005.00047.x
• JOSHI, J. and VRIELING, K., 2005. The enemy release and EICA hypothesis revisited: incorporating the fundamental difference between specialist and generalist herbivores. Ecology Letters, vol. 8, no. 7, pp. 704-714. http://dx.doi.org/10.1111/j.1461-0248.2005.00769.x
  » http://dx.doi.org/10.1111/j.1461-0248.2005.00769.x
• KEMPF, M., REINHARD, A. and BEUERLE, T., 2010. Pyrrolizidine alkaloids (PAs) in honey and pollen‐legal regulation of PA levels in food and animal feed required. Molecular Nutrition & Food Research, vol. 54, no. 1, pp. 158-168. http://dx.doi.org/10.1002/mnfr.200900529 PMid:20013889.
  » http://dx.doi.org/10.1002/mnfr.200900529
• KRUEGER, R., WANG, K.H., MCSORLEY, R. and GALLAHER, R.N., 2008. Artificial and natural pollination of sunn hemp in Florida. Proceedings of the Annual Meeting of the Florida State Horticultural Society, vol. 121, pp. 234-237.
• KUBITZA, C., FAUST, A., GUTT, M., GÄTH, L., OBER, D. and SCHEIDIG, A.J., 2018. Crystal structure of pyrrolizidine alkaloid N-oxygenase from the grasshopper Zonocerus variegatus. Acta Crystallographica. Section D, Structural Biology, vol. 74, no. 5, pp. 422-432. http://dx.doi.org/10.1107/S2059798318003510 PMid:29717713.
  » http://dx.doi.org/10.1107/S2059798318003510
• LEAL, G., MARASCA, I., RIBEIRO JUNIOR, L., GLADENUCCI, J. and CARMO, E., 2018. Propriedades biologicas do solo na cultura da Crotalaria. Agrarian Academy, vol. 5, no. 9, pp. 295-301. http://dx.doi.org/10.18677/Agrarian_Academy_2018a29
  » http://dx.doi.org/10.18677/Agrarian_Academy_2018a29
• LIMA FILHO, O.F.D., AMBROSANO, E.J., ROSSI, F. and CARLOS, J.A.D., 2014. Adubação verde e plantas de cobertura no Brasil: fundamentos e prática Brasília: Embrapa.
• LIMA, F. and CASTRO, M., 2017. Ocorrência de insetos-praga e inimigos naturais em plantio consorciado de pimenta-de-cheiro com adubos verdes. Biodiversidade, vol. 16, no. 3, pp. 40-48.
• LIMA, T.E., SARTORI, A.L.B. and RODRIGUES, M.L.M., 2017. Plant antiherbivore defense in Fabaceae species of the Chaco. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 77, no. 2, pp. 299-303. http://dx.doi.org/10.1590/1519-6984.12815 PMid:27599100.
  » http://dx.doi.org/10.1590/1519-6984.12815
• MACEL, M., 2011. Attract and deter: a dual role for pyrrolizidine alkaloids in plant–insect interactions. Phytochemistry Reviews, vol. 10, no. 1, pp. 75-82. http://dx.doi.org/10.1007/s11101-010-9181-1 PMid:21475391.
  » http://dx.doi.org/10.1007/s11101-010-9181-1
• MACEL, M., BRUINSMA, M., DIJKSTRA, S.M., OOIJENDIJK, T., NIEMEYER, H.M. and KLINKHAMER, P.G., 2005. Differences in effects of pyrrolizidine alkaloids on five generalist insect herbivore species. Journal of Chemical Ecology, vol. 31, no. 7, pp. 1493-1508. http://dx.doi.org/10.1007/s10886-005-5793-0 PMid:16222788.
  » http://dx.doi.org/10.1007/s10886-005-5793-0
• MANANDHAR, R. and HOOKS, C.R., 2011. Using protector plants to reduce the incidence of Papaya ringspot virus-watermelon strain in zucchini. Environmental Entomology, vol. 40, no. 2, pp. 391-398. http://dx.doi.org/10.1603/EN10229
  » http://dx.doi.org/10.1603/EN10229
• MANANDHAR, R. and WRIGHT, M.G., 2016. Effects of interplanting flowering plants on the biological control of corn earworm (Lepidoptera: Noctuidae) and thrips (Thysanoptera: Thripidae) in sweet corn. Journal of Economic Entomology, vol. 109, no. 1, pp. 113-119. http://dx.doi.org/10.1093/jee/tov306 PMid:26500338.
  » http://dx.doi.org/10.1093/jee/tov306
• MANANDHAR, R., HOOKS, C.R.R. and WRIGHT, M.G., 2009. Influence of cover crop and intercrop systems on Bemisia argentifolli (Hemiptera: Aleyrodidae) infestation and associated squash silverleaf disorder in zucchini. Environmental Entomology, vol. 38, no. 2, pp. 442-449. http://dx.doi.org/10.1603/022.038.0218 PMid:19389294.
  » http://dx.doi.org/10.1603/022.038.0218
• MARCHINI, L.C., MORETI, A.C.D.C.C., TEIXEIRA, E.W., SILVA, E.C.A.D., RODRIGUES, R.R. and SOUZA, V.C., 2001. Plantas visitadas por abelhas africanizadas em duas localidades do estado de São Paulo. Scientia Agrícola, vol. 58, no. 2, pp. 413-420. http://dx.doi.org/10.1590/S0103-90162001000200028
  » http://dx.doi.org/10.1590/S0103-90162001000200028
• MARTINEZ, S.T., PINTO, A.C., GLASNOV, T. and KAPPE, C.O., 2014. Chemistry of pyrrolizidine alkaloids revisited: semi-synthetic microwave and continuous-flow approaches toward Crotalaria-alkaloids. Tetrahedron Letters, vol. 55, no. 30, pp. 4181-4184. http://dx.doi.org/10.1016/j.tetlet.2014.05.055
  » http://dx.doi.org/10.1016/j.tetlet.2014.05.055
• MATHEW, R. and OPPERMAN, C.H., 2020. Current insights into migratory endoparasitism: deciphering the biology, parasitism mechanisms, and management strategies of key migratory endoparasitic phytonematodes. Plants, vol. 9, no. 6, pp. 671. http://dx.doi.org/10.3390/plants9060671 PMid:32466416.
  » http://dx.doi.org/10.3390/plants9060671
• MATTOCKS, A., 1986. Chemistry and toxicology of pyrrolizidine alkaloids London: Academic Press, 393 p.
• MCSORLEY, R., SEAL, D.R., KLASSEN, W., WANG, K.H. and HOOKS, C.R.R., 2009. Non-target effects of sunn hemp and marigold cover crops on the soil invertebrate community. Nematropica, vol. 39, pp. 235-245.
• MEAGHER JUNIOR, R.L., WATROUS, K.M., FLEISCHER, S.J., NAGOSHI, R.N., BROWN, J.T., BOWERS, K., MILLER, N., HIGHT, S.D., LEGASPI, J.C. and WESTBROOK, J.K., 2019. Documenting potential sunn hemp (Crotalaria juncea L.) (Fabaceae) pollinators in Florida. Environmental Entomology, vol. 48, no. 2, pp. 343-350. http://dx.doi.org/10.1093/ee/nvy190 PMid:30753472.
  » http://dx.doi.org/10.1093/ee/nvy190
• NISHIDA, R., 2002. Sequestration of defensive substances from plants by Lepidoptera. Annual Review of Entomology, vol. 47, no. 1, pp. 57-92. http://dx.doi.org/10.1146/annurev.ento.47.091201.145121 PMid:11729069.
  » http://dx.doi.org/10.1146/annurev.ento.47.091201.145121
• NOWAK, M., WITTKE, C., LEDERER, I., KLIER, B., KLEINWÄCHTER, M. and SELMAR, D., 2016. Interspecific transfer of pyrrolizidine alkaloids: an unconsidered source of contaminations of phytopharmaceuticals and plant derived commodities. Food Chemistry, vol. 213, pp. 163-168. http://dx.doi.org/10.1016/j.foodchem.2016.06.069 PMid:27451168.
  » http://dx.doi.org/10.1016/j.foodchem.2016.06.069
• NTALLI, N.G. and CABONI, P., 2012. Botanical nematicides: a review. Journal of Agricultural and Food Chemistry, vol. 60, no. 40, pp. 9929-9940. http://dx.doi.org/10.1021/jf303107j PMid:22973877.
  » http://dx.doi.org/10.1021/jf303107j
• OBER, D. and KALTENEGGER, E., 2009. Pyrrolizidine alkaloid biosynthesis, evolution of a pathway in plant secondary metabolism. Phytochemistry, vol. 70, no. 15-16, pp. 1687-1695. http://dx.doi.org/10.1016/j.phytochem.2009.05.017 PMid:19545881.
  » http://dx.doi.org/10.1016/j.phytochem.2009.05.017
• OLIVEIRA, L.J. and GARCIA, M.A., 2003. Flight, feeding and reproductive behavior of Phyllophaga cuyabana (Moser)(Coleoptera: Melolonthidae) adults. Pesquisa Agropecuária Brasileira, vol. 38, no. 2, pp. 179-186. http://dx.doi.org/10.1590/S0100-204X2003000200003
  » http://dx.doi.org/10.1590/S0100-204X2003000200003
• OLIVEIRA, L.J., GARCIA, M.A., HOFFMANN-CAMPO, C.B. and AMARAL, M.L., 2007. Feeding and oviposition preference of Phyllophaga cuyabana (Moser) (Coleoptera: Melolonthidae) on several crops. Neotropical Entomology, vol. 36, no. 5, pp. 759-764. http://dx.doi.org/10.1590/S1519-566X2007000500018 PMid:18060303.
  » http://dx.doi.org/10.1590/S1519-566X2007000500018
• PACHECO, J. and SILVA-LÓPEZ, R., 2010. Genus Crotalaria L.(Leguminoseae). Revista Fitos, vol. 5, no. 3, pp. 43-52.
• PALOMINO, G. and VÁZQUEZ, R., 1991. Cytogenetic studies in Mexican populations of species of Crotalaria L. (Leguminosae-Papilionoideae). Cytologia, vol. 56, no. 3, pp. 343-351. http://dx.doi.org/10.1508/cytologia.56.343
  » http://dx.doi.org/10.1508/cytologia.56.343
• PEÑALOZA, G.C. and PELÁEZ, C.A., 2008. Evaluation of biological activity of Crotalaria juncea extracts through a Drosophila melanogaster model. Vitae, vol. 15, no. 2, pp. 279-284.
• QUINTANILLA-TORNEL, M.A., WANG, K.H., TAVARES, J. and HOOKS, C.R., 2016. Effects of mulching on above and below ground pests and beneficials in a green onion agroecosystem. Agriculture, Ecosystems & Environment, vol. 224, pp. 75-85. http://dx.doi.org/10.1016/j.agee.2016.03.023
  » http://dx.doi.org/10.1016/j.agee.2016.03.023
• REIGADA, C., GUIMARÃES, K. and PARRA, J., 2016. Relative fitness of Helicoverpa armigera (Lepidoptera: Noctuidae) on seven host plants: a perspective for IPM in Brazil. Journal of Insect Science, vol. 16, no. 1, pp. 3. http://dx.doi.org/10.1093/jisesa/iev158 PMid:26798139.
  » http://dx.doi.org/10.1093/jisesa/iev158
• SANTOS, G.G., SILVEIRA, P.M.D., MARCHÃO, R.L., BECQUER, T. and BALBINO, L.C., 2008. Macrofauna edáfica associada a plantas de cobertura em plantio direto em um Latossolo Vermelho do Cerrado. Pesquisa Agropecuária Brasileira, vol. 43, no. 1, pp. 115-122. http://dx.doi.org/10.1590/S0100-204X2008000100015
  » http://dx.doi.org/10.1590/S0100-204X2008000100015
• SCHRAMM, S., KÖHLER, N. and ROZHON, W., 2019. Pyrrolizidine alkaloids: biosynthesis, biological activities and occurrence in crop plants. Molecules, vol. 24, no. 3, pp. 498-542. http://dx.doi.org/10.3390/molecules24030498 PMid:30704105.
  » http://dx.doi.org/10.3390/molecules24030498
• SCUPINARI, T., RUSSO, H.M., FERRARI, A.B.S., BOLZANI, V.S., DIAS, W.P., NUNES, E.O., HOFFMANN‐CAMPO, C.B. and ZERAIK, M.L., 2020. Crotalaria spectabilis as a source of pyrrolizidine alkaloids and phenolic compounds: HPLC‐MS/MS dereplication and monocrotaline quantification of seed and leaf extracts. Phytochemical Analysis, vol. 31, no. 6, pp. 747-755. http://dx.doi.org/10.1002/pca.2938 PMid:32428987.
  » http://dx.doi.org/10.1002/pca.2938
• SETYAWATI, A.I., SUPRIYADI., PARDONO, WIJAYANTI, R. and PUTRI, R.B.A., 2018. The role of flowering plants, Hibiscus sabdariffa and Crotalaria juncea in coffee ecosystem to diversity of insect pollinators and coffee fruit set. AIP Conference Proceedings, vol. 2014, 020027. http://dx.doi.org/10.1063/1.5054431
  » http://dx.doi.org/10.1063/1.5054431
• SHOLAHUDDIN, WIJAYANTI, R., ARNIPUTRI, R.B., SUPRIYA and WIDYANINGRUM, D., 2019. Pollinator diversity and soybean productivity with flowering plant (Crotalaria and Rosella). IOP Conference Series, vol. 250, 012113. http://dx.doi.org/10.1088/1755-1315/250/1/012113
  » http://dx.doi.org/10.1088/1755-1315/250/1/012113
• SILVA, K.L. and TRIGO, J.R., 2002. Structure–activity relationships of pyrrolizidine alkaloids in insect chemical defense against the orb-weaving spider Nephila clavipes. Journal of Chemical Ecology, vol. 28, no. 4, pp. 657-668. http://dx.doi.org/10.1023/A:1015214422971 PMid:12035917.
  » http://dx.doi.org/10.1023/A:1015214422971
• SMITH, H.A. and MCSORLEY, R., 2000. Intercropping and pest management: a review of major concepts. American Entomologist, vol. 46, no. 3, pp. 154-161. http://dx.doi.org/10.1093/ae/46.3.154
  » http://dx.doi.org/10.1093/ae/46.3.154
• SUPRIYAD, WIJAYANTI, R., ARNIPUTRI, B., PUSPITARINI, N. and DWIYATNO, M.H., 2019. The effect of Crotalaria juncea plant in coffee ecosystem to the diversity and abundance of predators and parasitoids insects. IOP Conference Series, vol. 250, 012018. http://dx.doi.org/10.1088/1755-1315/250/1/012018
  » http://dx.doi.org/10.1088/1755-1315/250/1/012018
• TAVARES, W., CRUZ, I., SILVA, R., FIGUEIREDO, M., RAMALHO, F., SERRÃO, J. and ZANUNCIO, J., 2011. Soil organisms associated to the weed suppressant Crotalaria juncea (Fabaceae) and its importance as a refuge for natural enemies. Planta Daninha, vol. 29, no. 3, pp. 473-479. http://dx.doi.org/10.1590/S0100-83582011000300001
  » http://dx.doi.org/10.1590/S0100-83582011000300001
• TOKARNIA, C.H., DÖBEREINER, J. and PEIXOTO, P.V., 2000. Plantas tóxicas do Brasil Rio de Janeiro: Helianthus. 646 p.
• TRIGO, J.R., 2000. The chemistry of antipredator defense by secondary compounds in neotropical Lepidoptera: facts, perspectives and caveats. Journal of the Brazilian Chemical Society, vol. 11, no. 6, pp. 551-561. http://dx.doi.org/10.1590/S0103-50532000000600002
  » http://dx.doi.org/10.1590/S0103-50532000000600002
• TRIGO, J.R., 2011. Effects of pyrrolizidine alkaloids through different trophic levels. Phytochemistry Reviews, vol. 10, no. 1, pp. 83-98. http://dx.doi.org/10.1007/s11101-010-9191-z
  » http://dx.doi.org/10.1007/s11101-010-9191-z
• TRISNAWATI, I. and AZIS, A., 2017. The effectiveness of habitat modification schemes for enhancing beneficial insects: assessing the importance of trap cropping management approach. AIP Conference Proceedings, vol. 1, pp. 020038. http://dx.doi.org/10.1063/1.4985429
  » http://dx.doi.org/10.1063/1.4985429
• VENZON, M., ROSADO, M.C., EUZÉBIO, D.E., SOUZA, B. and SCHOEREDER, J.H., 2006. Suitability of leguminous cover crop pollens as food source for the green lacewing Chrysoperla externa (Hagen) (Neuroptera: chrysopidae). Neotropical Entomology, vol. 35, no. 3, pp. 371-376. http://dx.doi.org/10.1590/S1519-566X2006000300012 PMid:18575698.
  » http://dx.doi.org/10.1590/S1519-566X2006000300012
• VILLALOBOS, S. and RAMÍREZ, N., 2010. Reproductive biology of Crotalaria micans Link (Fabaceae): pioneer species of wide geographical distribution. Acta Botanica Venezuelica, vol. 33, no. 1, pp. 67-81.
• WANG, K.H., SIPES, B. and SCHMITT, D., 2002. Crotalaria as a cover crop for nematode management: a review. Nematropica, vol. 32, pp. 35-57.
• WEI, X., VRIELING, K., MULDER, P.P. and KLINKHAMER, P.G., 2015. Testing the generalist-specialist dilemma: the role of pyrrolizidine alkaloids in resistance to invertebrate herbivores in Jacobaea species. Journal of Chemical Ecology, vol. 41, no. 2, pp. 159-167. http://dx.doi.org/10.1007/s10886-015-0551-4 PMid:25666592.
  » http://dx.doi.org/10.1007/s10886-015-0551-4
• WINK, M. and MOHAMED, G.I., 2003. Evolution of chemical defense traits in the Leguminosae: mapping of distribution patterns of secondary metabolites on a molecular phylogeny inferred from nucleotide sequences of the rbcL gene. Biochemical Systematics and Ecology, vol. 31, no. 8, pp. 897-917. http://dx.doi.org/10.1016/S0305-1978(03)00085-1
  » http://dx.doi.org/10.1016/S0305-1978(03)00085-1
• WRIGHT, M.G., 2019. Cover crops and conservation biocontrol: can the impacts of Trichogramma (Hymenoptera: Trichogrammatidae) be magnified? Annals of the Entomological Society of America, vol. 112, no. 4, pp. 295-297. http://dx.doi.org/10.1093/aesa/say061
  » http://dx.doi.org/10.1093/aesa/say061
• WUTKE, E.B., CALEGARI, A. and WILDNER, L.P., 2014. Espécies de adubos verdes e plantas de cobertura e recomendações para seu uso. In: O. F. D. LIMA FILHO, E. J. AMBROSANO, F. C. ROSSI and J. A. DONIZETI, eds. Adubação verde e plantas de cobertura no Brasil: fundamentos e práticas. Brasília: EMBRAPA, pp. 60-168.

Publication Dates

• Publication in this collection
  17 Jan 2022
• Date of issue
  2024

History

• Received
  02 Oct 2021
• Accepted
  06 Dec 2021