Optimal foraging shapes host preference of a polyphagous leafminer

Abstract.  1. Most research on host selection by arthropods is based on optimal oviposition theory. This theory, also called the oviposition preference–offspring performance hypothesis, predicts that a female will choose those hosts for oviposition on which larvae perform best. Recent studies suggested, however, that optimal foraging by adults, or the quality of the host for adult performance, might also influence host choice.
2. This study investigated whether host preference of the polyphagous leafminer Liriomyza trifolii is determined by optimal foraging and/or optimal oviposition.
3. Female realised fecundity correlated nearly perfectly with feeding and oviposition preference of L. trifolii . The relationships between host preference and the offspring performance measures were always weaker. Hosts optimal for adult nutrition were also optimal for offspring performance but not vice versa . Hence, it was concluded that optimal foraging shapes feeding and oviposition preference of L. trifolii as this is the best strategy in order to maximise female fitness.     

Host selection in insects: reproductive interference shapes behavior of ovipositing females

In nature, closely related species often utilize different host species, but it is still unclear what factors contribute to the evolution and maintenance of such diversified host selection. In this review, I describe how negative interspecific mating interactions (reproductive interference) can shape host selection by animals, focusing mainly on phytophagous and predatory insects. First, I explain an important premise of this hypothesis, which is that the adult reproductive site is the same as the feeding site for the offspring. Next, I describe several mathematical models and well-studied empirical systems to show that reproductive interference can sufficiently drive and maintain different host selection between phylogenetically related species. Then, I argue for the first time that reproductive interference can cause an oviposition preference in insects that is not optimal for the survival and development of the offspring, as a result of maternal adaptive behavior that maximizes the mother's own fitness. Furthermore, I argue that in insects, reproductive interference probably shapes oviposition behavior before the female alights on the host (e.g., habitat preference), without affecting post-alighting decision making. I would like to emphasize that these two arguments represent the novel approach to clarify the unrevealed pattern of complex insect oviposition behavior.     

Is a mango just a mango? Testing within-fruit oviposition site choice and larval performance of a highly polyphagous fruit fly

For fruit flies, fully ripe fruit is preferred for adult oviposition and is superior for offspring performance over unripe or ripening fruit. Because not all parts of a single fruit ripen simultaneously, the opportunity exists for adult fruit flies to selectively choose riper parts of a fruit for oviposition and such selection, if it occurs, could positively influence offspring performance. Such fine scale host variation is rarely considered in fruit fly ecology, however, especially for polyphagous species which are, by definition, considered to be generalist host users. Here we study the adult oviposition preference/larval performance relationship of the Oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae), a highly polyphagous pest species, at the “within-fruit” level to see if such a host use pattern occurs. We recorded the number of oviposition attempts that female flies made into three fruit portions (top, middle and bottom), and larval behavior and development within different fruit portions for ripening (color change) and fully-ripe mango, Mangifera indica L. (Anacardiaceae). Results indicate that female B. dorsalis do not oviposit uniformly across a mango fruit, but lay most often in the top (i.e., stalk end) of fruit and least in the bottom portion, regardless of ripening stage. There was no evidence of larval feeding site preference or performance (development time, pupal weight, percent pupation) being influenced by fruit portion, within or across the fruit ripening stages. There was, however, a very significant effect on adult emergence rate from pupae, with adult emergence rate from pupae from the bottom of ripening mango being approximately only 50% of the adult emergence rate from the top of ripening fruit, or from both the top and bottom of fully-ripe fruit. Differences in mechanical (firmness) and chemical (total soluble solids, titratable acidity, total non-structural carbohydrates) traits between different fruit portions were correlated with adult fruit utilisation. Our results support a positive adult preference/offspring performance relationship at within-fruit level for B. dorsalis. The fine level of host discrimination exhibited by B. dorsalis is at odds with the general perception that, as a polyphagous herbivore, the fly should show very little discrimination in its host use behavior.     

Choosing between good and better: optimal oviposition drives host plant selection when parents and offspring agree on best resources

Insect preferences for particular plant species might be subjected to trade-offs among several selective forces. Here, we evaluated, through laboratory and field experiments, the feeding and ovipositing preferences of the polyphagous leafminer Liriomyza?huidobrensis (Diptera: Agromyzidae) in relation to adult and offspring performance and enemy-free space. Female leafminers preferred laying their eggs on Vicia?faba (Fabaceae) over Beta?vulgaris var. cicla (Chenopodiaceae), in both laboratory and field choice experiments, although no oviposition preference was observed in no-choice tests. Females fed more often on B.?v.?var.?cicla (no-choice test) or showed no feeding preference (choice test), even when their realized fecundity was remarkably higher on V.?faba. Offspring developed faster, tended to survive better, and attained bigger adult size on the preferred host plant. Also, a field experiment showed higher overall parasitism rates for leafminers developing on B.?v.?var.?cicla, with a nonsignificant similar tendency in field surveys. According to these results, host plant selection by L.?huidobrensis appears to be driven mainly by variation in host quality. Moreover, the consistent oviposition choices for the best host and the labile feeding preferences observed here, suggest that host plant selection might be driven by maximization of offspring fitness even without a conflict of interest between parents and offspring. Overall, these results highlight the complexity of decisions performed by phytophagous insects regarding their host plants, and the importance of simultaneous evaluation of the various driving forces involved, in order to unravel the adaptive significance of female choices.     

Plant architecture affects periodical cicada oviposition behavior on native and non‐native hosts

Variation in plant quality provides a basis for oviposition site selection for a variety of insects. Of the plant traits that influence plant–insect interactions, plant architecture has received little attention despite its putative role in modulating oviposition behavior. In a common garden comprised of native and non‐native plant species, we assessed how host plant architecture and identity influenced the oviposition behavior of 17‐year periodical cicadas (Homoptera: Cicadidae: Magicicada). On each host, we quantified the availability of branches suitable for oviposition and compared those measures with the branches used by ovipositing cicadas. Using this approach, we determined how the structural attributes of plants (i.e. branch diameter, length and incline) affected oviposition site selection. We then related cicada oviposition preferences to offspring performance by quantifying egg hatching success. On each host species, cicadas selectively used broader and longer branches for oviposition, suggesting that branch architecture provides a basis for oviposition behavior irrespective of plant identity. Broader and longer branches were more abundant on native than on non‐native hosts in our study, contributing to greater oviposition loads among the native species. Egg hatching success was similar among native and non‐native hosts. However, it is possible that the use of native plants for oviposition could enhance offspring output because native hosts generally contained more viable eggs per egg nest and more egg nests per plant. While previous accounts of cicada oviposition preferences have focused on differences in oviposition loads among hosts, our evaluation of within‐host branch selection by ovipositing cicadas helps to clarify oviposition preferences at a higher resolution and demonstrates that plant architecture provides an important basis for oviposition behavior. Furthermore, because branch structure can differ substantially among host species, our results suggest that periodical cicadas may be sensitive to the changes in plant composition that often result from non‐native plant invasions.     

Oviposition site selection by herbivorous beetles: a comparison of two thistle feeders, Cassida rubiginosa and Henosepilachna niponica

In insects that feed on plants in both adult and larval stages, it is often difficult to distinguish oviposition preference from adult feeding preference, because oviposition can occur at or in proximity to feeding sites. In the present study, characteristics of oviposition site selection of two beetle species, Cassida rubiginosa Müller (Coleoptera: Chrysomelidae) and Henosepilachna niponica (Lewis) (Coleoptera: Coccinellidae), were investigated in the field and laboratory, with particular attention to relationships with adult feeding sites. In the field, distances between adult feeding scars and egg masses differed for C . rubiginosa and H . niponica , with the former being very small and the latter averaging 24.6 cm. The same tendencies for the distances between adult feeding scars and egg masses of the two beetle species were confirmed in cages in which only female beetles were released. Cassida rubiginosa restricted egg laying to host plants in the field and to leaves in laboratory assays. On the other hand, H . niponica placed 8% of egg masses on plants adjacent to host plants in the field and often placed eggs on artificial substrates rather than leaf discs in laboratory assays. These results suggest that oviposition and female feeding sites are virtually inseparable in the case of C . rubiginosa , while H . niponica females do not necessarily keep to host plant leaves as oviposition substrates and they tend to oviposit at some distance from their feeding sites. Results are discussed in relation to proximate and ultimate causes of host selection behavior.     

Relationship between adult and larval host plant selection and larval performance in the generalist moth, Trichoplusia ni

Adult oviposition preferences are expected to correlate with host plant suitability for the development of their offspring. For most lepidopteran species, this is particularly important as the hatching neonate larvae of many species are relatively immobile. Thus, the site of oviposition chosen by a female adult can greatly influence the probability of survival for her offspring. In the present study, we investigated the oviposition preference of adult Trichoplusia ni moths for six plant species to determine whether they could accurately rank the suitability of the plants for larval development. We also compared oviposition preferences to neonate larval acceptance and preference to determine whether the adult host range matched that of larval diet breath. Our results indicate that in two-choice and no-choice tests adult T. ni were able to rank the plants accurately, with the exception of anise hyssop. However, when given a choice of all six plants together, they laid more eggs on a plant that was not suitable for larval survival. Larvae accepted and fed on all plants in no-choice tests, and accurately ranked them according to larval performance. We conclude that neonate larvae are better able than adults to rank plants according to larval performance, and that larval diet breadth is wider than the range of plants accepted by adults. We also provide a discussion of the reduced accuracy of adult oviposition preference with increased plant choices.     

Oviposition site preference and developmental performance of a gall‐inducing leafhopper on galled and non‐galled host plants

Oviposition preferences of herbivorous insects affect offspring performance. Both positive and negative links between oviposition preference and offspring performance have been reported for many species. A gall‐inducing leafhopper, Cicadulina bipunctata Melichar (Hemiptera: Cicadellidae), feeds on various Poaceae plants and induces galls of enhanced nutritional value for their offspring. Although gall induction by C. bipunctata improves nymphal performance, the oviposition preference of females between galled and non‐galled host plants is still unclear. In this paper, the nymphal performance and oviposition and feeding‐site preference of C. bipunctata were investigated using galled wheat, Triticum aestivum L., and non‐galled barley, Hordeum vulgare L., as host plants. The survival rate of C. bipunctata on wheat was significantly higher than on barley. In the choice test, significantly more eggs were laid into barley, whereas the number of eggs deposited on both hosts was not significantly different in the no‐choice test. The number of settling individuals per leaf area was not significantly different between wheat and barley, suggesting no clear preference for oviposition between these plants. Experience as a nymph with a growing host did not affect oviposition preference as adult female. The inconsistent correspondence between offspring performance and oviposition preference of C. bipunctata may reflect the high mobility of nymphs and/or differences in leaf area between host plants. The results indicate that the previous finding that oviposition preference and offspring performance are not always positively correlated in herbivorous insects is applicable to gall‐inducing insects.     

Host selection and colonization strategies with evidence for a female-produced oviposition attractant in a longhorn beetle

In longhorn beetles and many other internally feeding insects, oviposition choice by females is critical to the survival of their offspring because their larvae are incapable of moving between hosts. Here we report on the complex host selection and colonization strategies of a longhorn beetle, Glenea cantor (F.) (Coleoptera: Cerambycidae), which is an important pest of kapok trees [Bombax ceiba L.=Gossampinus malabaricus (DC.) Merr.] in southern Asia. It attacks weakened trees, eventually killing them. The typical oviposition behavioral sequence in the laboratory includes the following: oviposition site search and recognition using antennae and palpi, oviposition slit preparation with mandibles, turning body direction 180°, egg deposition with the ovipositor, and oviposition wound covering with a jelly-like material from the ovipositor. Bark moisture content significantly increases from the upper to lower sections in kapok trees. In accordance with this variation female adults select the upper section of trees first for oviposition. As infestation continues and the host becomes more weakened, ovipositing females move further down the tree for oviposition. Consequently, the larvae kill the hosts from the top down. We show that the jelly-like material or eggs or both have an olfactory role in attracting females to oviposit nearby. Our findings are important in terms of increasing our understanding of host selection and colonization mechanisms of internally feeding insects, particularly cerambycids, and the development of environmentally friendly pest management measures.     

桔小实蝇和番石榴实蝇对6种寄主果实的产卵选择适应性

植食性昆虫对寄主植物的选择适应性是研究昆虫和植物协同进化关系的核心内容之一。评估寄主植物对植食性昆虫种群的适合度,需要综合分析昆虫对寄主的产卵选择性和寄主对昆虫的取食适合性。以桔小实蝇和番石榴实蝇为研究对象,分别测定了这两种实蝇对6种寄主果实:番石榴、香蕉、杨桃、木瓜、甜橙、番茄的产卵选择性以及幼虫取食后对其生长发育的影响。寄主产卵选择性实验分别采用完整寄主果实直接供试产卵和块状寄主果实气味引诱产卵两种处理方式;在生长发育适应性实验中,以幼虫和蛹的存活和生长发育等相关参数作为评价指标。实验结果表明,寄主的供试方式不同,两种实蝇的选择性均有明显差异;对寄主气味选择性强的寄主更适合于两种实蝇后代的生长发育。两种实蝇对6种寄主果实的产卵选择性和后代发育适合性两者相关性不显著,与许多文献报道单一地采用发育适合性(如发育历期、存活率或蛹重等)作为评价寄主选择性的结果不一致。两种实蝇之间对6种寄主果实的产卵选择和幼虫取食适合性既具相似性也具差异性,表明这两种实蝇在寄主生态位上既有重叠性又有分化性。     

Feeding Experience of Bemisia tabaci (Hemiptera: Aleyrodidae) Affects Their Performance on Different Host Plants

The sweetpotato whitefly, Bemisia tabaci biotype B is extremely polyphagous with >600 species of host plants. We hypothesized that previous experience of the whitefly on a given host plant affects their host selection and performance on the plants without previous experience. We investigated the host selection for feeding and oviposition of adults and development and survival of immatures of three host-plant-experienced populations of B. tabaci, namely Bemisia-eggplant, Bemisia-tomato and Bemisia-cucumber, on their experienced host plant and each of the three other plant species (eggplant, tomato, cucumber and pepper) without previous experience. We found that the influence of previous experience of the whiteflies varied among the populations. All populations refused pepper for feeding and oviposition, whereas the Bemisia-cucumber and the Bemisia-eggplant strongly preferred cucumber. Bemisia-tomato did not show strong preference to any of the three host palnts. Development time from egg to adult eclosion varied among the populations, being shortest on eggplant, longest on pepper, and intermediate on tomato and cucumber except for the Bemisia-cucumber developed similarly on tomato and pepper. The survivorship from egg to adult eclosion of all populations was highest on eggplant (80-98%), lowest on pepper (0-20%), and intermediate on tomato and cucumber. In conclusion, the effects of previous experience of whiteflies on host selection for feeding and oviposition, development, and survivorship varied depending on host plants, and host plants play a stronger role than previous experience. Preference of feeding and oviposition by adults may not accurately reflect host suitability of immatures. These results provided important information for understanding whitefly population dynamics and dispersal among different crop systems.     

Innate preference hierarchies coupled with adult experience,rather than larval imprinting or transgenerational acclimation,determine host plant use in Pieris rapae

The evolution of host range drives diversification in phytophagous insects, and understanding the female oviposition choices is pivotal for understanding host specialization. One controversial mechanism for female host choice is Hopkins’ host selection principle, where females are predicted to increase their preference for the host species they were feeding upon as larvae. A recent hypothesis posits that such larval imprinting is especially adaptive in combination with anticipatory transgenerational acclimation, so that females both allocate and adapt their offspring to their future host. We study the butterfly Pieris rapae, for which previous evidence suggests that females prefer to oviposit on host individuals of similar nitrogen content as the plant they were feeding upon as larvae, and where the offspring show higher performance on the mother's host type. We test the hypothesis that larval experience and anticipatory transgenerational effects influence female host plant acceptance (no‐choice) and preference (choice) of two host plant species (Barbarea vulgaris and Berteroa incana) of varying nitrogen content. We then test the offspring performance on these hosts. We found no evidence of larval imprinting affecting female decision‐making during oviposition, but that an adult female experience of egg laying in no‐choice trials on the less‐preferred host Be. incana slightly increased the P. rapae propensity to oviposit on Be. incana in subsequent choice trials. We found no transgenerational effects on female host acceptance or preference, but negative transgenerational effects on larval performance, because the offspring of P. rapae females that had developed on Be. incana as larvae grew slower on both hosts, and especially on Be. incana. Our results suggest that among host species, preferences are guided by hard‐wired preference hierarchies linked to species‐specific host traits and less affected by larval experience or transgenerational effects, which may be more important for females evaluating different host individuals of the same species.     

Temporal consistency and individual specialization in resource use by green turtles in successive life stages

For many insect herbivores, maternal host selection is a critical determinant of offspring survival; however, maternal fitness is also affected by adult resources such as food availability. Consequently, adult resources may promote oviposition in sub-optimal locations when measured in terms of offspring performance. We tested whether oviposition site preference is primarily shaped by proximity to adult food resources or offspring performance in the aspen leaf miner (Phyllocnistis populiella). Quaking aspen (Populus tremuloides) produce extrafloral nectaries (EFNs) on a subset of their leaves. EFN expression on leaves is associated with decreased P. populiella damage and larval performance; however, P. populiella adults feed from EFNs. We reduced extrafloral nectar availability on entire aspen ramets and excluded crawling predators in a full factorial experiment at two sites in interior Alaska, USA. Patterns of egg deposition by P. populiella appeared to be primarily affected by offspring survival rather than adult resource availability. While oviposition was unaffected by nectar availability, adult moths laid fewer eggs on leaves with than without EFNs. By avoiding leaves with EFNs, moths increased offspring survival. Both moths and predators distinguished between leaves with and without EFNs even when nectar and visual cues were obscured, and therefore may respond to chemical cues associated with EFN expression.     

Oviposition and feeding preferences of a flower-feeding weevil,Coelocephalapion aculeatum, in relation to conspecific damage to its host-plant

The oviposition and feeding preferences ofCoelocephalapion aculeatum Fall (Coleoptera: Apionidae), a host specific florivore ofMimosa pigra L. (Mimosaceae), were studied in relation to conspecific damage to its hostplant. Adults ofC. aculeatum cease ovipositing in inflorescences when the egg load reaches a number consistent with the larval carrying capacity of the inflorescence. The basis for this oviposition deterrence was examined by offering inflorescences damaged by adult feeding alone, larval feeding alone and a combination of adult feeding and oviposition. Adults preferred to oviposit on inflorescences which are not damaged by either adult feeding, larval feeding, or oviposition. No evidence for the existence of an oviposition deterring pheromone (ODP) was found. I suggest that the ability of a single host inflorescence to support the development of many larvae causes selection for the use of these oviposition deterring cues which can convey more quantitative information about the level of previous infestation than can ODPs. Adults fed a similar amount on damaged compared to undamaged inflorescences. These results assisted in the design of host range testing trials and allows predictions to be made about the effectiveness of this insect as a biological control agent.     

Cover Caption

Foliar nutrient content plays a key role in mediating the interaction of plants and insect herbivores within and across generations. Here, the weed biological control agent Neolema abbreviate is depicted feeding on its host Tradescantia fluminensis during trials measuring performance across generations on hosts with variable nitrogen content. Our study concluded that adult traits such as oviposition selection, weigh gain and longevity were largely unresponsive to parental diet. Instead, offspring diet was more important in determining performance (see pages 361–374). Photo provided Frank Chidawanyika.     

Selection of large host plants for oviposition by a monophagous leaf beetle: nutritional quality or enemy‐free space?

Abstract.  1. Oviposition site selection is crucial for the reproductive success of herbivorous insects. According to the preference–performance hypothesis, females should oviposit on host plants that enhance the performance of their offspring. More specifically, the plant vigour hypothesis predicts that females should prefer large and vigorously growing host plants for oviposition and that larvae should perform best on these plants.
2. The present study examined whether females of the monophagous leaf beetle Cassida canaliculata Laich. (Coleoptera: Chrysomelidae) prefer to oviposit on large host plant individuals of the meadow clary and whether large host plants are of higher nutritional quality than small host plants. Subsequently, it was tested whether the female preference correlates with offspring performance and survival.
3. In the field, females preferred large host plant individuals for oviposition and host plant quality, i.e. leaf nitrogen content, was significantly higher in leaves of large than of small host plants.
4. In the laboratory, larval development time was shorter on leaves of large host plant individuals than on small host plant individuals, but this could not be shown in the field.
5. However, a predator-exclusion experiment in the field resulted in a higher survival of larvae on large host plants than on small host plants when all predators had free access to the plants. On caged host plants there was no difference in survival of larvae between plant size categories.
6. It is concluded that females of C. canaliculata select oviposition sites that enhance both performance and survival of their offspring, which meets the predictions of the plant vigour hypothesis.     

The influence of prior experience on preference and performance of a cryptoparasitoid Scleroderma guani (Hymenoptera: Bethylidae) on beetle hosts

1. Numerous studies have reported the effects of learning or experience on parasitoid host preference and location. However, the integration of pre‐imaginal and adult experiences on the subsequent host preference and adult/offspring performance has been rarely tested in host–parasite interactions. 2. We present direct evidence that theses two kinds of experiences affect host preference and related fitness in the polyphagous parasitoid, Scleroderma guani. Two colonies of parasitoids were reared on Monochamus alternatus and Saperda populnea (Cerambycidae: Lamiinae). Individuals from the two colonies were given host‐switching experience for one generation (pre‐imaginal experience) while other individuals were given prior ovipositing experience on the two species, respectively (adult experience). 3. Scleroderma guani females demonstrated that their experiences determined adult behavioural responses and their subsequent performance to hosts. Females maximised both adult fitness (fecundity and longevity) and offspring fitness (survival and sex ratio) when they encountered hosts similar to their maternal hosts. Behavioural plasticity in host choice was affected by adult experience, resulting in improved adult feeding and ovipositing behaviour and further modifying adult fecundity and the offspring sex ratio. There was a positive correlation between oviposition preference and adult fecundity. 4. The results indicated that S. guani exhibited positive preference–performance correlations. This is most likely due to an adaptation to maternal hosts over multiple generations. However, foraging potential of adults to available cues from hosts may be driven quickly by an experience‐induced learning process rather than by natural selection processes shaped over many generations.     

Herbivore host choice and optimal bad motherhood

When theory predicts which phenotypes are well adapted to a given environment, the data do not always match the predictions. Host-plant selection by herbivorous insects is one such example. Herbivorous insects often appear to make poor choices about where their offspring should develop. New evidence presented by Scheirs et al. suggests that adult insects can choose oviposition sites that enhance their own long-term fitness at the expense of their individual offspring. This suggests that herbivorous insects might be genuinely bad mothers, that host choice is nonetheless adaptive, and that theory needs to incorporate new assumptions about host effects on adult performance.     

HERITABILITY OF OVIPOSITION PREFERENCE AND ITS RELATIONSHIP TO OFFSPRING PERFORMANCE WITHIN A SINGLE INSECT POPULATION

Within a population of the butterfly Euphydryas editha that oviposits predominantly on two host species, heritable variation in postalighting oviposition preference was found. In a separate experiment, oviposition preference of adult females was found to be correlated with offspring performance (growth). There was a significant tendency for offspring to perform better on the host species that their female parent preferred. Analysis of the data showed that no single factor, neither maternal preference nor the host species on which the offspring were raised, accounted for any significant variation in larval performance. However, the effect of the interaction between host species and maternal preference on offspring performance was highly significant. These findings imply specialization in both oviposition preference and offspring performance by individuals within a single population. With present evidence, this preference-performance correlation is likely to be genetic. However, as in previous studies, other interpretations cannot be excluded.     

Enemy-free space? Host preference and larval performance of a willow leaf beetle

To examine whether enemy-free space is an important factor determining the host utilization pattern of a leaf beetle Plagiodera versicolora, we investigated the relationship between adult preference and offspring performance on three co-occurring willow species, Salix sachalinensis, S. miyabeana and S. integra. Salix sachalinensis was by far the most preferred host plant of feeding adults, while both S. miyabeana and S. integra were rarely fed upon. The fact that most oviposition was observed on S. sachalinensis also suggested that P. versicolora preferred S. sachalinensis to other willows for oviposition. This adult preference did not correspond well to patterns of larval performance on the three willow species in the absence of enemies. Higher survivorship, shorter developmental time and larger adult size were achieved on S. sachalinensis and S. miyabeana than on S. integra. Performance as indicated by female adult size and development time on S. miyabeana were higher than on S. sachalinensis. In the presence of enemies, however, the survivorship of first-instar larvae on S. miyabeana was much lower than on other willows. Adults of P. versicolora apparently avoided S. miyabeana as an oviposition and feeding host and preferred S. sachalinensis as an enemy-free space. This was not because larvae had poorer performance on S. miyabeana, but because predation pressure on eggs and early instar larvae was more severe on S. miyabeana.