Helena C. Morais’s research while affiliated with Instituto de Ciências Farmacêuticas and other places

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Publications (64)


Ontogeny has a greater effect on defense and leaf nutritional status than fertilization in Stryphnodendron adstringens (Fabaceae)
  • Article

October 2024

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14 Reads

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1 Citation

Flora

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[...]

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Helena C. Morais

The role of leaf cutting and fire on extrafloral nectaries and nectar production in Stryphnodendron adstringens (Fabaceae, Mimosoideae) plants

May 2022

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73 Reads

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9 Citations

Plant Species Biology

Herbivory pressure is an important ecological aspect to determine quantitative variation in plant defenses, such as the number of extrafloral nectaries (EFNs) and their nectar amount and quality. Extrafloral nectaries can attract ants, which can be considered a type of induced plant defense. Besides, plants tend to invest more in defense when they are more vulnerable to herbivores. Therefore, we aimed to elucidate if Stryphnodendron adstringens (Fabaceae), a common Cerrado tree species, when subjected to damage (by manual leaf cutting and experimental fire) would produce a greater number of EFNs and changes its nectar quality on newly produced leaves in comparison with plants not subjected to these treatments. Leaf damage was performed artificially directly on the plant branches and at the entire plant canopy (by means of scissors or fire events). Extrafloral nectary density was higher in new leaves produced after the treatment application (artificial herbivory and fire) in comparison with plants under control treatment. The amount of nectar was also higher under treatments in comparison with control, with a significant change on nectar quality in plants subjected to the treatments of artificial herbivory. The results provided support for the hypothesis that EFNs are an inducible defensive strategy in S. adstringens, confirming the existence of phenotypic plasticity given environmental pressures.


Ordination of 72 traps sampled in four periods (beginning and middle of both rainy and dry seasons) through a nonmetric multidimensional scaling (NMDS), using the family abundance from a chewing and b sap-sucking herbivorous insects (p < 0.05). BRS beginning of rainy season, MRS middle of rainy season, BDS beginning of dry season, and MDS middle of dry season
Average a abundance and b richness of sap-sucking insect herbivores per trap on deciduous and evergreen trees sampled in four periods (beginning and middle of both the rainy and dry seasons) in a tropical dry forest (n = 72). The use of different letters upon bars indicates differences among periods, whereas the use of asterisk indicates differences between phenological groups (deciduous vs. evergreen) within the same period (p < 0.05). Error bars indicate one standard error. BRS beginning of rainy season, MRS middle of rainy season, BDS beginning of dry season, and MDS middle of dry season
Seasonal and diel variations in the activity of canopy insect herbivores differ between deciduous and evergreen plant species in a tropical dry forest
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August 2017

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500 Reads

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22 Citations

Journal of Insect Conservation

This study evaluated whether herbivorous insects can be expected to have particular adaptations to withstand the harsh dry season in tropical dry forests (TDFs). We specifically investigated a possible escape in space, with herbivorous insects moving to the few evergreen trees that occur in this ecosystem; and escape in time, with herbivores presenting an increased nocturnal rather than diurnal activity during the dry season. We determined the variation in the free-feeding herbivorous insects (sap-sucking and leaf chewing) between seasons (beginning and middle of both rainy and dry seasons), plant phenological groups (deciduous and evergreen trees) and diel period (diurnal and nocturnal) in a Brazilian TDF. We sampled a total of 5827 insect herbivores in 72 flight-interception traps. Contrary to our expectations, we found a greater herbivore diversity during the dry season, with low species overlap among seasons. In the dry season, evergreen trees supported greater richness and abundance of herbivores as compared to deciduous trees. Insects were also more active at night during the dry season, but no diel differences in insect abundance were detected during the rainy season. These results indicate that the strategies used by insect herbivores to withstand the severe climatic conditions of TDFs during the dry season include both small-scale escape in space and time, with evergreen trees playing a key role in maintaining resident insect herbivore populations in TDFs. Relatively more nocturnal activity during the dry season may be related to the avoidance of harsh climatic conditions during the day. We suggest that the few evergreen tree species occurring in the TDF landscape should be especially targeted for protection in this threatened ecosystem, given their importance for insect conservation.

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Host plants and general view of the vegetation of study areas of Strymon crambusa. (A) cerrado sensu stricto; (B) “campo sujo” (Cerrado grassland); (C) Oxalis cordata; (D) Oxalis densifolia.
Strymon crambusa, immatures and adult reared under laboratory conditions on Oxalis: (A) egg on the peduncle of inflorescences O. cordata; (B) first instar, (C) second instar, (D) third instar and (E) fourth instar on O. densifolia; (F) pupa; (G) adult male, dorsal view and (H) ventral view.
Biology of the immature stages of Strymon crambusa (Lycaenidae: Theclinae) on Oxalidaceae

November 2015

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183 Reads

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6 Citations

Revista Brasileira de Entomologia

ABSTRACT We document the biology and morphology of the egg, caterpillar, and pupa of Strymon crambusa (Hewitson, 1874), a Neotropical Eumaeini. In the Cerrado, the caterpillar feeds on the inflorescences and leaves of Oxalis L. S. crambusa has four larval instars, all of which are illustrated. The density of caterpillars on plants is higher than that recorded for leaf-feeding caterpillars and other flower-feeding Eumaeini, which suggests that the species is a specialist on Oxalidaceae in the Cerrado.


Fig. 1. Mean percentage of green leaves in the crown of deciduous and leaf-exchanger evergreen species (2007–2012) and average monthly rainfall (2007–2012) at the Mata Seca State Park (MSSP). Deciduous species: S. glandulosum , H. reticulatus and C. duar- teanum ; evergreen species: A. polyneuron , G. marginata and Z. joazeiro . The horizontal black bar corresponds to the dry season. 
Leaf traits and herbivory on deciduous and evergreen trees in a tropical dry forest

February 2015

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851 Reads

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62 Citations

Basic and Applied Ecology

Deciduous and evergreen trees coexist in tropical dry forests, but exhibit distinct leaf syndromes for resource-use efficiency and defenses against herbivores. Moreover, these functional groups may have contrasting patterns of temporal variation in leaf traits and herbivory along leaf ontogeny. We tested these predictions by comparing a set of leaf traits related to water stress and defense, and herbivory levels between young and mature leaves from evergreen leaf-exchanger and deciduous species. We evaluated deciduous and evergreen trees within the same habitat type: a tropical dry forest with 90-100% of leaf deciduousness during the dry season. We sampled 10 individuals of three deciduous and three evergreen species. Evergreen plants had greater leaf thickness and concentration of phenolics and tannins. On the other hand, deciduous plants had higher leaf nitrogen content and specific leaf area. Deciduous plants lost twice as much leaf area by herbivory as evergreen plants (6.48 versus 3.20%), and leaf damage was positively related to both phenolic compounds and nitrogen content. Mature leaves from both phenological groups had higher levels of tannins and phenolic compounds, and lower levels of nitrogen and herbivory increment than young leaves. Our results suggest an adaptive convergence on leaf traits primarily related to water stress for different species within each phenological group. Some of these traits also play a role in leaf palatability, although the fitness consequences of the absolute difference in leaf damage (approximately 3%) between evergreen and deciduous species remain unclear.


Fig. 1. (A) Study locales and the distribution of diet breadth for (B) Lepidoptera and (C) all other herbivores. Points on the globe are shown in orange for Lepidoptera study sites, green for other herbivore study sites, and red for study sites for both. Histograms in B and C illustrate counts of the numbers of herbivores associated with different numbers of host plant families; also shown is the shape parameter (α) from the discrete, truncated Pareto distribution. Tick marks under histograms indicate individual observations for visualization in the thin tail of the distributions. (D and E) Survival plots illustrate the fit of the Pareto (white circles), geometric (triangles), and Poisson (squares) distributions to the data (colored symbols). Log survival on the y axis is ln(P(X > x)), which is the natural logarithm of the probability of herbivores having a greater diet breadth (X) than the corresponding value (x) on the x axis. Note that most analyses focus on diet breadth at the scale of individual sites; for simplicity, diet breadth is shown here across sites.
Fig. 3. Diet breadth (DBR) comparisons for herbivore guilds from tropical and temperate communities for (A) family-level DBR and (B) species-level DBR. Higher values of the shape parameter (α) indicate more specialized diets. Means and SDs are based on rarefaction to the lowest number of host taxa sampled in each pairwise comparison connected by dotted lines. More than one community is represented by some but not all of the points (SI Appendix, section S1). Note that not all guilds could be analyzed for both species-and family-level DBR (Materials and Methods and SI Appendix contain more details).  
The global distribution of diet breadth in insect herbivores

December 2014

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1,461 Reads

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529 Citations

Proceedings of the National Academy of Sciences

Significance Dietary specialization determines an organism’s resource base as well as impacts on host or prey species. There are important basic and applied reasons to ask why some animals have narrow diets and others are more generalized, and if different regions of the Earth support more specialized interactions. We investigated site-specific host records for more than 7,500 species of insect herbivores. Although host specialists predominate, the proportion of specialists is affected by the diversity of hosts and shifts globally, supporting predictions of more exclusive tropical interactions. These results not only affect our understanding of the ecology of food webs, but also have implications for how they respond to environmental change, as well as for ecosystem management and restoration.


Figure 2: Figs. 9–13 Transmission electron microscope images of EFN from recently expanded Maprounea brasiliensis leaves. (9) Elongated cells that form the EFN. (10) Detail of plasmodesmata and vesicles. (11) Detail of two secretory cells. (12) Secretory cell. (13) The formation of vesicles at the apex of the secretory cell. GA Golgi apparatus, M mitochondria, N nucleus, n nucleolus, Pl plasmodesmata, V vacuole, ve vesicles, W cell wall. Scale bars (9) 5 μm. (10) 0.2 μm. (11–13) 0.5 μm
Figs. 9-13 Transmission electron microscope images of EFN from recently expanded Maprounea brasiliensis leaves. (9) Elongated cells that form the EFN. (10) Detail of plasmodesmata and vesicles. (11) Detail of two secretory cells. (12) Secretory cell. (13) The formation of vesicles at the apex of the secretory cell. GA Golgi apparatus, M mitochondria, N nucleus, n nucleolus, Pl plasmodesmata, V vacuole, ve vesicles, W cell wall. Scale bars (9) 5 lm. (10) 0.2 lm. (11-13) 0.5 lm 
Figs. 22-23 EFN and leaf traits of Maprounea brasiliensis produced at different times of the year: leaves flushed during the rainy season and leaves flushed during the dry season. (22) The number of EFNs per leaf. (23) The average of the largest diameter of EFN per leaf. Different letters indicate statistically significant differences, with P \ 0.05. Bars represent the standard deviation 
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Extrafloral nectary morphology and the role of environmental constraints in shaping its traits in a common Cerrado shrub (Maprounea brasiliensis A. St.-Hill: Euphorbiaceae)

September 2014

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222 Reads

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8 Citations

Brazilian Journal of Botany

This study aimed to elucidate the anatomy and morphology of extrafloral nectaries (EFNs) in Maprounea brasiliensis and whether environmental factors influence their traits of production and morphology. For this reason, we sampled leaves from individuals subjected to distinct fire and water regimes, and the anatomy and ultrastructures of EFNs as well as the chemical constitution of nectar were analyzed. EFN nectar production was associated with immature and recently expanded leaves. EFNs originate from the epidermis. At the end of ontogeny, secretory cells are surrounded by three or more layers of cells with secondary and lignified walls, isolating the EFN of vascular tissue. The ultrastructural analysis revealed mature EFNs with secretory activity. The experiments showed that EFN production was not influenced by the presence of frequent fires. However, during the rainy season, new produced leaves had nectaries in greater quantity and diameter than leaves produced during the dry season. The anatomical and ultrastructural changes demonstrated that nectar production is strongly influenced by the age of the nectaries which influence ant attendance to EFN since no ants were observed on leaves that did not secrete nectar. The seasonality experiment confirmed that EFNs of M. brasiliensis are resource dependent and evolutionary programed to appear in elevated number during the rainy season.


Larval Biology of Anthophagous Eumaeini (Lepidoptera: Lycaenidae, Theclinae) in the Cerrado of Central Brazil

July 2014

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1,988 Reads

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24 Citations

Journal of Insect Science

The biology and morphology of the early stages of 22 species of Eumaeini (Lepidoptera: Lycaenidae, Theclinae) are presented. Observations were collected through the inspection of inflorescences in the field and the rearing of 214 larvae in laboratory. Allosmaitia strophius (Godart) associated with Malpighiaceae species and the polyphagous Strymon mulucha (Hewitson) were the most frequently collected species. Detritivory was observed in two species, Electrostrymon endymion (F.) and Kisutam syllis (Godman & Salvin), and myrmecophily in four other species, A. strophius, Ministrymon azia (Hewitson), Parrhasius polibetes (Stoll), and S. mulucha. Cannibalism was observed in A. strophius; in addition, the pupa of this and of three other species produced audible sounds. Paiwarria aphaca (Hewitson) was highlighted because of the great difference observed between its first and last instars, as well as the marked difference between that species and the larvae of Paiwarria umbratus (Geyer) documented in Costa Rica. Larvae of Calycopis mimas (Godman & Salvin) displayed "bungee jumping" behavior when stimulated. Parasitoids (Diptera, Hymenoptera) attacked 21 larvae of eight species, A. strophius, K. syllis, M. azia, Pai. aphaca, P. polibetes, Rekoa marius (Lucas), S. mulucha, and Tmolus venustus (H.H. Druce). Illustrations of immatures and parasitoids are provided.


Lagartas do Cerrado - Guia de Campo

January 2013

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3,478 Reads

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13 Citations

O Guia de Campo Lagartas do Cerrado é o primeiro do gênero para qualquer bioma do Brasil. Será extremamente útil para profissionais e outros interessados na fauna de insetos, principalmente do Cerrado. Esse guia foi elaborado de forma simples e de maneira adequada para a utilização no campo, contém informações para cada espécie de lagarta e é fartamente ilustrado (lagartas e adultos) para facilitar a identificação das espécies. Contém a diagnose das lagartas de cada família e informações, quando possível, da descrição morfológica e das mudanças durante o seu desenvolvimento, da amplitude de dieta (especialista ou generalista), de espécies de plantas hospedeiras (somente aquelas restritas ao Cerrado de Brasília - DF, Pirenópolis e Chapada dos Veadeiros - GO), da aparência (coloração críptica ou aposemática), do comportamento (solitário ou gregário, desenvolvimento exposto na planta ou em abrigo), da ocorrência temporal e da abundância relativa em plantas do Cerrado de Brasília, Pirenópolis e Chapada dos Veadeiros (rara ou comum).


Fig. 1 Monthly proportion of sheltered and exposed caterpillars during the year (dry season, May-September) in the cerrado of the Distrito Federal, Brazil
Fig. 2 Proportion of sheltered and exposed caterpillars in the wet and dry seasons in the cerrado of the Distrito Federal, Brazil
Fig. 3 Proportion of sheltered caterpillars on plants with and without EFNs during the period of highest presence of new leaves (September-November) in the cerrado of the Distrito Federal, Brazil
Shelter-building caterpillars in the cerrado: Seasonal variation in relative abundance, parasitism, and the influence of extra-floral nectaries

December 2012

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331 Reads

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22 Citations

Arthropod-Plant Interactions

Caterpillar shelters provide protection against desiccation and natural enemies, whereas extra-floral nectaries (EFNs) may be an anti-herbivore adaptation that reduces herbivore abundance by attracting predators and parasites. We used a large, long-term dataset for caterpillars found in the Brazilian cerrado to examine temporal variations in the relative abundance of shelter-building caterpillars and exposed caterpillars, and to determine how much variation depends on the season and the presence of EFNs on host plants. We also compared the patterns of parasitism between sheltered and exposed caterpillars, between seasons, and between different host plants. The cerrado has a marked dry season, and its vegetation is a mixture of mostly deciduous shrubs and trees. Leaf production occurs mainly during the rainy season, and many plant species bear EFNs. Our results show that 60 % of cerrado caterpillars build shelters. These caterpillars were found to be proportionally more abundant during the dry season and less parasitized than exposed ones. The proportion of caterpillars building shelters was highest on plants with new leaves (functional EFNs), and parasitism of caterpillars on these plants was higher. Even though our study includes a taxonomically diverse suite of caterpillars that build many different types of shelter and a diverse set of plants and EFN types, our results suggest that EFNs play an important role in structuring caterpillar assemblages in the cerrado, and that the prolific use of shelters by caterpillars may be a result of their effectiveness in protecting caterpillars from natural enemies and desiccation.


Citations (47)


... Furthermore, even after ant-plants grow large enough to produce food rewards, ant defense in juvenile antplants is still less consistent than in mature plants because (i) there are lags as plants wait for ant queens to locate and colonize them (Bruna et al. 2011), and (ii) incipient ant colonies are less likely to survive in smaller plants (Nishi and Romero 2008). To survive without ant protection, young antplants have been hypothesized to employ chemical defenses or to have high tolerance to herbivory (Nomura et al. 2001;Heil and McKey 2003;Delgado et al. 2024). Some studies have indeed found higher levels of defensive chemistry in the leaves of unprotected juvenile ant-plants (Fonseca-Romero et al. 2019), though others have not (Del Val and Dirzo 2003;Ochoa-López et al. 2015). ...

Reference:

Challenges in the Early Ontogeny of a Mutualistic Plant: Resource Availability and Plant Defense in Juvenile Cecropia Ant-Plants
Ontogeny has a greater effect on defense and leaf nutritional status than fertilization in Stryphnodendron adstringens (Fabaceae)
  • Citing Article
  • October 2024

Flora

... However, any such changes are unknown. Finally, the effects of fire potentially occur through changes in nectar quantity or quality (Alves- Del-Claro 2013, 2014;Delgado et al 2022). The strongest effect of fire was on the incidence of ant-EFN interactions on Acacia, suggesting that the quantity and/or quality of extrafloral nectar was higher in burnt plots. ...

The role of leaf cutting and fire on extrafloral nectaries and nectar production in Stryphnodendron adstringens (Fabaceae, Mimosoideae) plants
  • Citing Article
  • May 2022

Plant Species Biology

... Despite the forest's size and context, it sustains various trophic guilds, indicating a valuable provision of ecosystem services offered by conserving such urban forest remnants. The entomofauna in our study area demonstrated a richness either equivalent or superior to those reported in other continental dry forests (Janzen & Schoener, 1968;Janzen, 1973a;Janzen, 1973b;Vasconcellos et al., 2010;Macedo-Reis, Quesada & Neves, 2019;Silva et al., 2017) and Caribbean islands (Janzen & Schoener, 1968;Janzen, 1973a;Janzen, 1973b). This richness, seen even in a limited area, highlights the conservation of a significant number of species and trophic guilds due to the presence of defined stratification. ...

Seasonal and diel variations in the activity of canopy insect herbivores differ between deciduous and evergreen plant species in a tropical dry forest

Journal of Insect Conservation

... This host plant supports a rich and diverse fauna of lepidopteran species within this biome, comprising 62 species in 22 families (Bendicho-López et al. 2006). These species are well known, including their degrees of specialization (Diniz & Morais 1995, 1997Diniz et al. 2001;Bendicho-López et al. 2003, 2006Bendicho-López & Diniz 2004). The specialization of these larvae is not a local event; for example, there are some species, like Stenoma cathosiota Meyrick (Depressariidae), that are specialists on R. montana in the Cerrado of Brazil (Diniz & Morais 1995, 1997Diniz et al. 2001;Bendicho-López et al. 2006), as well as in the dry forests, rainforests, and cloud forests of Costa Rica (Janzen & Hallwachs 2004). ...

Larvas de Lepidoptera e suas plantas hospedeiras em um cerrado de Brasília, DF, Brasil
  • Citing Article
  • January 1995

Revista Brasileira de Entomologia

... Corroborating our expectations, we found that richness of herbivorous insect species increases as the plant species richness in savanna areas increases. This result suggests that the higher the diversity of resources, the higher the richness of associated herbivorous insects (Marquis et al., 2002). Previous studies in the Brazilian Cerrado have also found a positive correlation between plant species richness and herbivorous species richness (Gonçalves-Alvim and Fernandes, 2001; Leal et al., 2016). ...

16. Interactions Among Cerrado Plants and Their Herbivores: Unique or Typical?: Ecology and Natural History of a Neotropical Savanna

... Un aspecto diferente muestra la oruga descripta por Dyar (1928), que se corresponde con la descripta e ilustrada por Schreiter (1943) bajo el nombre de M. nuda, y el de M. chacona (Bourquin, 1948;Orfila, 1967) que no presentan cresta dorsal, sino una densa cubierta de pelos claros aplanados sobre el cuerpo y dirigidos hacia posterior. Por su parte, las larvas de M. albicollis (Bourquin, 1941), M. braulio (Diniz et al., 2013) y M. dyari (Martínez, 2022) exhiben una densa cubierta pilosa con pelos muy largos y de aspecto esponjoso, que recubren todo el cuerpo y se unen en la línea media, mientras que las de M. hina serían más cortos, pero igualmente parejos y esponjosos (Sihezar, 2019). Realizando una comparación morfológica general de todo el estado larval, la especie estudiada se asemeja más a M. undalata vulpina (Bourquin, 1945a, b) que a cualquier otra especie del género con ciclo biológico conocido. ...

Lagartas do Cerrado - Guia de Campo

... Herbivorous insects exhibit a wide range of diets, from diets specializing on one plant species, genus, or family to diets that include host plants belonging to several families. However, most herbivorous insect species are specialists, and studies suggest that a high degree of specificity is characteristic of tropical herbivorous insects (Janzen 1988;Marquis 1991;Diniz & Morais 2002;Dyer et al. 2007). Several factors may affect the spatial variation of herbivorous insects (Roslin & Kotze 2005), including differences in landscape, communities of plants, soil types, diet breadth (Ødegaard 2006), variations in the chemical and physical quality of the host plant (Gaston et al. 2004;Murakami et al. 2008), composition and abundance of natural enemies (Denno et al. 2005;Gripenberg & Roslin 2007;Connahs et al. 2009), environmental structure, and the micro-and macro-climatic conditions of each area (Gripenberg & Roslin 2005). ...

Local pattern of host plant utilization by lepidopteran larvae in the cerrado vegetation

Entomotropica

... Resource availability is another potentially major driver for shaping arthropod stratification (Basset et al., 2003). Overall, knowledge on host plants of lepidopterans is sparse (Diniz et al., 2001). For Geometridae, species accumulation curves strengthen the impression of an understory group; we found 19 indicator species, four of these were Eois. ...

Host plants of lepidopteran caterpillars in the cerrado of the Distrito Federal, Brazil

Revista Brasileira de Entomologia

... In contrast with the florivorous habits of most species of Eumaeini (Robbins & Aiello 1982;Beccaloni et al. 2008;Morais et al. 2009;Silva et al. 2014), the caterpillars of Arawacus and other Zebra Hairstreaks are mostly folivorous (Table 1). Even the genera closer to Arawacus in the tribe Strymonina (sensu Robbins et al. 2022), such as Strymon Hübner, Rekoa Kaye, thereus, and Panthiades, feed mainly on flowers (e.g., Monteiro 1991;Beccaloni et al. 2008;Heredia & Robbins 2016;Ramírez-Fischer et al. 2016;Silva et al. 2016;Jorge et al. 2021). These natural history records suggest florivory as the ancestral condition in Strymonina but this hypothesis needs to be tested through comparative phylogenetic methods. ...

Biology of the immature stages of Strymon crambusa (Lycaenidae: Theclinae) on Oxalidaceae

Revista Brasileira de Entomologia

... Glucose, fructose and sucrose were found on the nectar of J. princeps. These sugars are present in the nectar of several plant species (Zanotti-Ávila, 2022, Nicolson, 2022 including other Euphorbiaceae species (Freitas et al., 2001;Papp, 2004;Delgado et al., 2014). As verified in J. princeps in this study, high levels of fructose in the nectar were described in seven species of Euphorbia (Euphorbiaceae) by Papp (2004). ...

Extrafloral nectary morphology and the role of environmental constraints in shaping its traits in a common Cerrado shrub (Maprounea brasiliensis A. St.-Hill: Euphorbiaceae)

Brazilian Journal of Botany