Monophagous Species Research Articles

Aphid populations are frequently infected with facultative endosymbionts.

The occurrence of facultative endosymbionts has been studied in many commercially important crop pest aphids, but their occurrence and effects in non-commercial aphid species in natural populations have received less attention. We screened 437 aphid samples belonging to 106 aphid species for the eight most common facultative aphid endosymbionts. We found one or more facultative endosymbionts in 53% (56 of 106) of the species investigated. This likely underestimates the situation in the field because facultative endosymbionts are often present in only some colonies of an aphid species. Oligophagous aphid species carried facultative endosymbionts significantly more often than monophagous species. We did not find a significant correlation between ant tending and facultative endosymbiont presence. In conclusion, we found that facultative endosymbionts are common among aphid populations. This study is, to our knowledge, the first of its kind in the Netherlands and provides a basis for future research in this field. For instance, it is still unknown in what way many of these endosymbionts affect their hosts, which is important for determining the importance of facultative endosymbionts to community dynamics.

Combinatorial Olfactory Signaling in Short-Distance Determines Host Plant Recognition in Locust

Selecting palatable plants matters for insect herbivores’ survival, especially for food-restricted oligophagous and monophagous species. However, the definite selection strategy to distinguish host plants from nonhost plants, as well as the underlying sensory basis, remains controversial. Here, we investigated the olfactory recognition of host plants in oligophagous migratory locusts. By establishing one novel behavioral paradigm that allowed the free-moving locusts to make olfactory choices in short-distance, we demonstrated that palps were required to differentiate host plants apart from nonhost counterparts sensitively. Specifically, the characteristic odors between the host plant and nonhost plant defined the behavioral differentiation of food sources, and this process required intact palps. Further, single nonhost odor suppressed the behavioral potency to host plant extraction, while single host odor attenuated the behavioral repulsion to nonhost plant. We also identified the palps odorant receptors (ORs) repertoire that modulated the short-range recognition of key volatiles from host plants and nonhost and demonstrated that combinatorial olfactory signaling controls food choice. Our results support a “pull–push” model in which olfactory signaling on locust palps acts as a key tuning modulator in host plant recognition, expanding the knowledge of insect chemosensation.

Pest categorisation of Nilaparvata lugens

The EFSA Panel on Plant Health performed a pest categorisation of Nilaparvata lugens (Hemiptera: Delphacidae), the brown planthopper, for the European Union. N. lugens is widespread in Asia where it is native; it also occurs in Oceania where it is naturalised. N. lugens is not known to be present in the EU and is not listed in Annex II of Commission Implementing Regulation (EU) 2019/2072. It is a monophagous species and a major pest of rice (Oryza sativa). High populations of planthoppers cause leaves to initially turn orange yellow before becoming brown and dry and this is a condition called 'hopperburn' that kills the plant. N. lugens can also transmit plant viruses. It can complete 12 generations per year in tropical areas, where it resides year-round. N. lugens can undertake long-distance migration of up to 500 km from tropical areas to form transient populations in sub-tropical and temperate areas but due to low temperatures and absence of rice plants during the winter it does not establish in such areas. Entry to the EU via migration is unlikely given the distance from tropical rice growing areas. A possible but unlikely potential pathway is the import of infested rice seedlings, although we have no evidence that such trade exists. In the EU, rice is mainly planted from seed; when transplanted, it is sourced locally. N. lugens is very unlikely to survive year-round in the EU due to unsuitable climate and lack of hosts during the winter. Consequently, the pest is very unlikely to become established in the EU territory. Nevertheless, there are measures available to further reduce the likelihood of entry, establishment and spread of N. lugens within the EU. N. lugens does not satisfy the criteria that are within the remit of EFSA to assess for it to be regarded as a potential Union quarantine pest.

Studies on the Frequency of Attack Produced by Obolodiplosis robiniae Haldeman in Black Locust Trees from Landscaped Spaces of Cluj-Napoca


 Obolodiplosis robiniae Haldeman (Diptera: Cecidomyiidae) is a monophagous species, the host plants being species of the genus Robinia. The species is native to the U.S.A., and in Europe, it was first reported in Italy, in 2003, from where it spread to all European countries. In Romania, it was reported in 2007. The attack of this species is produced by the larval stage and manifests leaves. After hatching, the endophytic and gregarious larvae cause changes in the parenchyma structure that lead to the appearance of characteristic galls located at the edge of the leaflet and rolled towards its lower part. In 2021, we monitored the frequency of attacked acacia leaves, the number of galls reported on a leaflet and the number of larvae in a gala in two locations in Cluj-Napoca: on the acacias in the Central Park of the city and on the acacias in some street alignments. In the case of acacias in Central Park, the frequency of attacked fruits was 15%, and in the case of acacias in the alignment, 7%. On the 50 attacked leaves taken from Central Park, there were 932 leaflets, of which 40% are with galls, and the leaves on the alignment had 1010 leaflets, of which 19.2% are with galls. The number of galas/leaflets was between 1 and 5 galas in Central Park, and on alignments between 1 and 4 galas. In both locations, most of the leaflets were with a single gala. The maximum larvae/gala was five specimens in Central Park and three larvae on the leaflets on the alignment.

Recovery of moth and butterfly (Lepidoptera) communities in a polluted region following emission decline.

Environmental pollution is one of the major drivers of the present-day decline in global biodiversity. However, the links between the effects of industrial pollution on insect communities and the underlying species-specific responses remain poorly understood. We explored the spatial pattern in insect communities by analysing 581 samples of moths and butterflies (containing 25,628 individuals of 345 species) collected along a strong pollution gradient in subarctic Russia, and we recorded temporal changes in these communities during the pollution decline that occurred from 1992 to 2006. In the 1990s, the diversity of the Lepidoptera community was positively correlated with the distance from the copper-nickel smelter at Monchegorsk. The overall abundance of Lepidoptera did not change along the pollution gradient, although the abundance of many species decreased with increasing pollution. The responses of each individual species to pollution were associated with its life history traits. The abundances of monophagous species that fed inside live plant tissues and hibernated as imagoes or pupae were not affected by pollution, whereas the abundances of oligophagous and polyphagous species that fed externally on plants and hibernated as larvae generally declined near the smelter. Substantial decreases in aerial emissions from the smelter between 1992 and 2006 resulted in an increase in the diversity of moths and butterflies in severely polluted habitats, whereas their overall abundance did not change. This recovery of the Lepidoptera community occurred due to the reappearance of rare species that had been previously extirpated by pollution and was observed despite the lack of any signs of recovery of the vegetation in the heavily polluted sites. We conclude that the recovery trajectories of insect communities following emission control can be predicted from studies of their changes along spatial pollution gradients by using space-for-time substitution.

Trophic relationships and mining seasons of the Nepticulidae of Lithuania: an updated survey

This study provides updated summarised data on host-plant preferences and mining seasons of the Nepticulidae of the Lithuanian fauna. It revealed that the Lithuanian Nepticulidae are trophically associated with 34 genera and 14 families of host plants. Four of these host-plant families stand out in a number of mining Nepticulidae species and all together host about 80% of the Lithuanian Nepticulidae. As regards feeding specialisation, the fauna of the Lithuanian Nepticulidae consists of three constituents: monophagous species (about 44%), narrow oligophagous species (about 48%), and true oligophagous species (about 8%). There are two distinctive peaks of mining: the summer peak from mid-June until mid-July and the autumn peak from early September until mid-October, when most species mine simultaneously.

Foliage-browsing Lepidoptera (Insecta) in deciduous forests of Ukraine for the last 70 years

As insect development depends on temperature, so the change in biology, behavior habits, frequency, and severity of outbreaks of foliage-browsing insects considered pests can follow the climate change. The reactions of species to the same climate changes can be specific, therefore, an unpredictable change in their ratio in the community will affect the consequences of climate change.
 The details of such changes must be studied to quantitatively assess future trends and the threats to deciduous forests. The aim of this research was to evaluate the representation in deciduous forests the foliage-browsing lepidopterous insects if different groups of size, lifestyle, voltinism, trophic relations, and ability to mass propagation in different periods of assessment for recent 70 years.
 In the analysis, we used a list of 118 lepidopterous species of foliage-browsing insects of deciduous forests, compiled on the basis of archival data from 1940–1975, and in the course of our own field research from 1975 to the present in the forests of Ukraine. Following trends were expected to be confirmed for these time intervals: to increase the number of species of small size, the number of species with hidden lifestyle, multivoltine species, polyphagous species, and so-called indifferent species. For each species, all these parameters were identified and proportions of species of each category for certain time intervals (1940–1950, 1960–1970, 1980–1990, and 2010–2020). Their distribution for size, voltinism, lifestyle, trophic features, and outbreak potential at these time intervals was compared using χ2-test.
 Among lepidopterous foliage-browsing insects of deciduous forests of Ukraine, the increase for recent 70 years was proved for the proportion of indifferent species (do not able to mass propagation), small species (with wingspan below 20 mm), as well as species with hidden (leaf-miners) and semi-hidden lifestyle (leaf-rollers). All trends are expressed the most obviously in 1940–1950 and further periods. The hypothesis about decrease the proportion of the univoltine and monophagous species for this period is not supported statistically.

LIPARTHRUM COLCHICUMSEMENOV (COLEOPTERA CURCULIONIDAE SCOLYTINAE) IN ITALY: INTRODUCED, ESTABLISHED OR NATIVE SPECIES?

Liparthrum colchicumSemenov (Coleoptera Curculionidae Scolytinae) is a relatively unknown monophagous insect species primarily associated with thin dried twigs (about 0.5-1cm in diameter) of Laurel (Laurus nobilis). After being caught in traps located at Italian ports, it was initially considered an intercepted species alien to the country. However, recent findings, suggest that this beetle may have a different origin. Several records from different sites of Tuscany and Latium showed that it could be relatively widespread in Italy. These observations strengthened the hypothesis that this scolytid, harmless to L. nobilis, might be already established or even native to the country. Therefore, we argue that it could have been easily overlooked thus far, as it thrives only in twigs already wilted due to different environmental factors. Moreover, field observations, carried out in the two Italian Regions, evidenced high frequencies of its infestations in Laurel twigs previously colonized by Xylosandrus compactus. Notes on the taxonomy and biology of this species are also reported in the present wo

The draft genome of the specialist flea beetle Altica viridicyanea (Coleoptera: Chrysomelidae)

BackgroundAltica (Coleoptera: Chrysomelidae) is a highly diverse and taxonomically challenging flea beetle genus that has been used to address questions related to host plant specialization, reproductive isolation, and ecological speciation. To further evolutionary studies in this interesting group, here we present a draft genome of a representative specialist, Altica viridicyanea, the first Alticinae genome reported thus far.ResultsThe genome is 864.8 Mb and consists of 4490 scaffolds with a N50 size of 557 kb, which covered 98.6% complete and 0.4% partial insect Benchmarking Universal Single-Copy Orthologs. Repetitive sequences accounted for 62.9% of the assembly, and a total of 17,730 protein-coding gene models and 2462 non-coding RNA models were predicted. To provide insight into host plant specialization of this monophagous species, we examined the key gene families involved in chemosensation, detoxification of plant secondary chemistry, and plant cell wall-degradation.ConclusionsThe genome assembled in this work provides an important resource for further studies on host plant adaptation and functionally affiliated genes. Moreover, this work also opens the way for comparative genomics studies among closely related Altica species, which may provide insight into the molecular evolutionary processes that occur during ecological speciation.

Characterization of microsatellite loci for three species of Tomoplagia (Diptera: Tephritidae) and absence of cross-species amplification

Tomoplagia (Diptera: Tephritidae) are endophagous herbivores on flowerheads of Asteraceae, with varying levels of host specialization. We isolated, characterized, and tested the heterologous amplification for sets of microsatellites of three species from this genus associated with native hosts in the Espinhaco mountain range, Brazil. We used two protocols to build microsatellite-enriched libraries and characterized 12 polymorphic loci for each fruit-fly species. The samples of T. grandis, a monophagous species, presented a lower number of alleles than the samples of the oligophagous species T. incompleta and T. bicolor. The average observed heterozygosity did not vary among species and the high values of Polymorphism Information Content suggest that the characterized microsatellite loci are quite informative. The primers developed for each Tomoplagia species failed to amplify the microsatellite loci for the other two species, which indicates a low conservation of the flanking nucleotide sequences in the three evaluated species. The sets of polymorphic microsatellites characterized for these species of Tomoplagia may be used in future ecological and evolutionary studies that aim to detect patterns of diversity on a fine scale.

Diversity and Host Plant-Use in North AmericanPhytomyzaHolly Leafminers (Diptera: Agromyzidae): Colonization, Divergence, and Specificity in a Host-Associated Radiation

AbstractInsects that feed on plants are widely used for studies of host-plant-associated speciation due to their diversity and tractability. The value of these studies necessarily depends upon an accurate understanding of the diet of the focal insects. In North America, the 12 Phytomyza Fallén (Diptera: Agromyzidae) leafmining fly species feeding on hollies (Ilex spp. (Aquifoliaceae: Ilex)) initially appeared to be primarily a host-plant-associated radiation of largely monophagous species. However, our increased collecting efforts found that a majority of the morphospecies are oligophagous, feeding on multiple Ilex species. Patterns of host-associations suggest that colonization of new hosts followed by host-associated speciation may be an important feature of diversification. Analyses of mitochondrial COI data in three oligophagous species found evidence of host-associated genetic structure consistent with processes of host-associated divergence. However, in one of these species, evidence of geographic divergence as well as host-associated divergence was detected, illustrating complexity in factors relating to speciation and host-use evolution in this radiation of leafmining flies.

Field screening of pigeonpea for their resistance against Melanagromyza obtusa (Diptera: Agromyzidae)

Melanagromyza obtusa (Malloch) has been recorded for the first time on pigeonpea at Nagpur, India and named as 'tur pod fly'. It is a monophagous species and devours the developing seeds of pigeonpea crop. It was reported to infest 12 to 100% pods causing losses of 2.4-95.0% on seed or grain (=250000 tonnes by weight) and are estimated at US $ 256 million annually. Therefore, a field experiment was conducted at Research Farm, Agricultural Research Station, Badnapur (VNMKV), India during kharif 2015-16 to source some promising pigeonpea genotypes against M. obtusa. The present investigations revealed the population of M. obtusa on 20 genotypes ranged from 0.00-277.64 maggots per 100 pods; pod and grain damage were ranging from 0.00-89.75 and 0.00-82.02%. The highest M. obtusa population, pod and grain damage was recorded in BRG-2 (277.64 maggots and 101.26 pupae per 100 pods; and 89.75 and 82.02%). On the basis of pod damage a total of five, two, eight, four and one genotypes were categorized as highly tolerant, tolerant, moderately tolerant, susceptible and highly susceptible; for grain damage these were seven, seven, three, two and one, respectively. The maximum yield was recorded from BDN-2010-1 (22.33 q/ha), followed by V-127 (21.61 q/ha). However, Cajanus scarabaeoides showed no maggot and pupal population, pod and grain damage by M. obtusa indicating its virtue of genetic resistance and it can be used in breeding programmes to develop resistant cultivars for farmer’s welfare.

Bacterial symbiosis in Bactrocera oleae, an Achilles' heel for its pest control.

Investigations on microbial symbioses in Tephritidae have increased over the past 30 years owing to the potential use of these relationships in developing new control strategies for economically important fruit flies. Bactrocera oleae (Rossi)-the olive fruit fly-is a monophagous species strictly associated with the olive tree, and among all the tephritids, its symbionts are the most investigated. The bacterium Candidatus Erwinia dacicola is the major persistent resident endosymbiont in wild B. oleae populations. Its relationship with B. oleae has been investigated since being identified in 2005. This endosymbiont is vertically transmitted through generations from the female to the egg. It exists at every developmental stage, although it is more abundant in larvae and ovipositing females, and is necessary for both larvae and adults. Studying B. oleae-Ca. E. dacicola, or other B. oleae-microbe interactions, will allow us to develop modern biological control systems for area-wide olive protection and set an example for similar programs in other important food crops. This review summarizes the information available on tephritid-microbe interactions and investigates relationships among fruit flies, bacteria and host plants; however, its focus is on B. oleae and its strict association with Ca. E. dacicola to promote environmentally friendly control strategies for area-wide pest management.

The Gut Microbiota Composition of the Moth Brithys crini Reflects Insect Metamorphosis.

Lepidoptera is a highly diverse insect order with major importance in agriculture as many species are considered pests. The role of the gut microbiota in insect physiology is still poorly understood, despite the research undertaken in recent years. Furthermore, Lepidoptera are holometabolous insects and few studies have addressed the influence of the changes taking place on the gut microbiome composition and diversity during metamorphosis, especially in monophagous species. The V3-V4 region of the 16S rRNA gene was sequenced to investigate the microbiota composition and diversity of the monophagous moth Brithys crini during three different life stages: egg, larvae (midgut and hindgut), and adult (gut). Our results showed that the microbiota composition of B. crini was stage specific, indicating that the developmental stage is a main factor affecting the gut microbiome in composition and potential functions. Moreover, the diversity of the gut microbiome reflected the developmental process, since a drop in diversity occurred between the larval and the adult phase, when the intestine is completely renewed. In spite of the changes in the gut microbiota during metamorphosis, 29 genera were conserved throughout the three developmental stages, mainly belonging to the Proteobacteria phylum, which define the core microbiome of B. crini. These genera seem to contribute to host physiology by participating in food digestion, nutrition, and detoxification mechanisms.

Molecular phylogeny and host‐plant use (Lamiaceae) of theThymogethespollen beetles (Coleoptera)

AbstractThe 24 members of the Euro‐Asiatic genusThymogethesare highly specialized pollen beetles associated as larvae with flowers of Lamiaceae Nepetoideae. All members of the genus were analysed in within the framework of an integrative taxonomy approach, which was aimed to reconstruct the phylogenetic relationships, as well as the possible pattern of evolution of their larval‐host‐plant association. Evidence from multiple molecular markers [COI; 16S; H3], combined with an estimation of divergence times using an average rate of 0.0177 substitutions/site/My among branches, placed the origin of the genus at a minimum of 9–10 Mya. This date of origin approximates the known evolution of the host plants in Euro‐Mediterranean areas. Evidence from combined molecular and cladistic morphological analyses resulted in suitable agreement with the previously established morphology‐based systematics of the genus, although members of theexilisspecies‐group were split into three clades. The only disagreement between results of this new combined phylogeny and previous classification is in the exclusion of “Thymogethes”grenieri. This species is herein positioned outside the genus, based on molecular evidence. Our analysis depicts severalThymogethesspecies differentiating in the last few Mys, specifically those included in theT. lugubrisspecies‐group. Combined evidence from DNA, morphology and ancestral state parsimony reconstruction of larval‐host‐plant associations suggests that subtribe Menthinae likely represents the ancestral host plants, with a series of independent host shifts during the radiation of the clade, in association first with Menthinae and subsequently with Lavandulinae and Nepetinae. Steno‐oligophagy is the most frequent (86%) condition, while strictly monophagous species are less numerous (14%).

Host Plant Selection in Phyllonorycter Species Living on Willows and Their Hybrids (Lepidoptera: Gracillariidae)

Own knowledge on host plants and on the breadth of the trophic specialization of central European species ofPhyllonorycterHübner, 1822 living onSalixspp. obtained over the past 60 years are presented. A total of 8 species were evaluated and divided into four groups after their trophic relationships; monophagous species:Phyllonorycter quinqueguttella(Stainton, 1851) onSalix repenss. l., andP. viminetorum(Stainton, 1854) onSalix viminalis(here only provisorly due to the small number of reared specimens); narrowly oligophagous species:P. dubitella(Herrich‑Schäffer, 1855) andP. salicicolella(Sircom, 1848), both onSalixspecies of the sectionCapreae; oligophagous species:P. hilarella(Zetterstedt, 1839) andP. salictella(Zeller, 1846) on manySalixspecies, each with different trophic preferences; broadly oligophagous species:Phyllonorycter connexella(Zeller, 1846) andP. pastorella(Zeller, 1846) developing onSalixandPopulusspecies. The hybrids are also used as host plants, and the laying females positively respond to them as well as to the biologicalSalixspecies, if at least one of the parental species is the usual host of the relevantPhyllonorycterspecies. The data on host plants reported by other authors are compared.

Temporal variation in bottom-up and top-down effects differ among herbivores with different seasonality

How variations in the strength of bottom-up and top-down forces are mediated by life-history trait differences of insect herbivores is an important but underexplored topic in ecology. Here, we implemented a factorial experiment manipulating plant quality by nitrogen fertilization and attack rates of parasitoids and spiders, respectively. We used sticky traps and mesh barriers in a salt marsh system to examine bottom-up and top-down effects on populations of three hemipteran sap-feeding monophagous species of Phragmites australis with different seasonality. The species included Chloriona alaica and Stenocranus matsumurai most abundant in spring and autumn, respectively, and Dimorphopterus pallipes abundant in both summer and autumn. Fertilization increased the density of S. matsumurai but had no effect on C. alaica and D. pallipes. Its negative effects on densities of the latter two species were even observed in earlier months. On the other hand, parasitoid removal not only increased abundance of all three herbivores, but also reduced the culm diameter, shoot height and biomass of P. australis, suggesting a trophic cascade. The main effects of parasitoid removal were greatest in months when those herbivores had their peak densities. In contrast, spider removal only affected the abundance of S. matsumurai with the greatest effect in September. Our results indicate that parasitoids have strong top-down effects on populations of insect herbivores in P. australis-dominated salt marshes and the strength of their effects is positively correlated with the host density. Furthermore, effects of plant quality and spider predation are more varied among herbivores with different seasonality.

Habitat structure and host plant specialization drive taxonomic andfunctional composition of Heteroptera in postfire successional habitats

Changes in habitat structure are the main driving forces for responses of animal assemblages to fire. According to the disturbance theory, generalist species are expected to outperform specialists in variable environments. Thus, we hypothesized that omnivorous and polyphagous species will become more abundant in unstable postfire successional vegetation, whereas monophagous (specialists), due to their strong dependence on host plants, are expected to respond according to the responses of plant hosts. We compared the responses of true bug (Heteroptera) assemblages in stable (unburnt) versus unstable (postfire successional) environments as this group shows a high diversity of feeding strategies. Redundancy analysis fitted our hypothesis as omnivorous and polyphagous bugs responded positively to fire whereas oligophagous bugs did not. Thus, the most generalized bugs in terms of diet were found in disturbed (burnt) habitats whereas specialized bugs were found in undisturbed (unburnt) habitats. Moreover, the most specialized bugs (monophagous species) responded to fire in accordance to the responses of their specific host plants. Although based on small bipartite networks, the lower modularity in burnt sites corresponded to a scenario of lower segregation of plant resources and fits the higher presence of generalist bugs in these sites. Our results suggest that plant?bug trophic interactions shape the response of Heteroptera to fire, and this response seems to be mediated by the degree of feeding specialization.

Bruchidius terrenus (Sharp, 1886) (Coleoptera: Chrysomelidae: Bruchinae): A New Invasive Species of Seed Beetles in the Fauna of Russia

Bruchidius terrenus (Sharp, 1886) (Coleoptera: Chrysomelidae: Bruchinae) is a new invasive East Palearctic species of seed beetles to the fauna of the Crimea and Russia was emerged in November 2017 from the seeds of Albizia julibrissin Durazzini, 1772 and A. kalkora (Roxburgh) Prain, 1897, that were collected in the Nikitsky Botanical Garden. B. terrenus is a monophagous species: larvae develop in the seeds of silk trees (Albizia Durazzini, 1772). The infestation levels of the seeds of A. julibrissin and A. kalkora were 45 and 78%, respectively. The species is monovoltine; emergence of imagoes was observed in November–December. The overwintering stage is imago.

BIOLOGIA DE <i>Montandoniola confusa</i> STREITO & MATOCQ (HEMIPTERA: ANTHOCORIDAE) EM PRESA NATURAL E ALTERNATIVA

O percevejo Montandoniola confusa Streito & Matocq tem sido citado como sendo o principal predador de Gynaikothrips ficorum Marchal, espécie monófaga que induz galhas em plantas de Ficus, como a espécie Ficus microcarpa L.f. (Moraceae). Estas espécies de fícus têm sido introduzidas em diversas partes do mundo, incluindo o Brasil, para utilização no paisagismo. Assim, este trabalho estudou o desenvolvimento e a reprodução do percevejo-predador usando o tripes, sua presa natural, comparado com ovos de Anagasta kuehniella (Zeller) e de Sitotroga cerealella Oliver, empregados como presas alternativas para a sua multiplicação. O percevejo-predador apresentou menor duração ninfal e superior viabilidade quando alimentado com o tripes e ovos de Anagasta kuehniella comparado a ovos de Sitotroga cerealella. A oviposição, no entanto, foi 2,37 e 3,71 vezes maior quando criados com o tripes em relação às presas alternativas Anagasta kuehniella e Sitotroga cereallea, respectivamente. Ovos das presas alternativas permitem a criação do predador, mas com desempenho inferior a presa natural.