Mutualism is defined as an interspecific relationship among two or more species which obtain mutual benefits and improve their fitness relative to when they occur alone (Bronstein 1994). It is an important form of interaction, especially in tropical environments (Bronstein 2015). Ants, for example, have a high taxonomic and morphological diversity in the tropics (Brandão and Delabie 2012), which suggests a wide variety of behaviors and ecological functions, including an active involvement in mutualistic interactions (Rico-Gray and Oliveira 2007). There are many well-known examples of mutualism between ants and plants. In most cases, ants play a defensive role that can have direct effects on the fitness of a given plant species, since the presence of ants is directly related to a decrease in herbivory and increased vegetative growth and reproduction of the plant host (e.g., Rico-Gray and Oliveira 2007; do Nascimento and Del-Claro 2010). However, the effects of ants on plants are not always positive, (Rosumek et al. 2009), and can be neutral (Bronstein 1994) or negative (Jones et al. 2015).

Except for bees, reports of insect-plant interactions in Clusiaceae are few (e.g., Vlasáková et al. 2019), especially for arboreal and otherwise difficult-to-access genera, such as Lorostemon Ducke. Lorostemon is an Amazonian genus that comprises five species of trees: L. bombaciflorus Ducke, L. coelhoi Paula, L. colombianus Maguire, L. roseoviridis Ferr.-Silva & L. Marinho and L. stipitatus Maguire (Ferreira-Silva et al. 2023, 2024). The genus has solitary, apical or lateral inflorescences (rarely on the branches), and the flowers are large, glabrous, tubular, concave or straight, generally showy yellow-green to yellow-red, with very evident green to red bracts and sepals (Cabral and Marinho 2024). The flowers have a sweet aroma and nectaries that produce a large quantity of nectar. However, as trees of Lorostemon occur infrequently, and in very isolated populations, there is few information about ecological interactions or floral visitors (Ferreira-Silva 2023). Here we report the first observation of an insect-plant interaction in Lorostemon.

The reported observations were made in the context of a broader study on monitoring of floral visitors in Lorostemon species carried out every 1-2 weeks from December 2021 to June 2023 in the municipality of Manaus, Amazonas state, Brazil. Ants were identified through images taken in the field and hemipterans were collected and identified at Instituto Nacional de Pesquisas da Amazônia - INPA, and deposited in the entomological collection of the same institution. The observations were made on five individuals of L. coelhoi located at Ramal do Brasileirinho, km 5 (Sítio PANC, Sítio Karla and Sítio Santa Rita) in Manaus (3°01’21.0’’S, 59°52’37.2’’W). The trees were 3-4 m high and were located approximately 5 to 25 m apart from each other. On each monitoring occasion, the trees were observed by two people during 10 to 12 hours per day (during the day and during the night) on 15 days, with intervals of two to three days between each visit. The observations were only qualitative, with no behavior quantification, and made from the ground. A ladder was used for flowers placed higher up.

We observed that the five Lorostemon trees were visited by ants of Cephalotes sp., Camponotus atriceps Smith, 1858 and Dolichoderus sp., including nest construction by Camponotus atriceps and Dolichoderus sp. (Figure 1a). On one of the trees, we observed Corimelaena nymphs (Hemiptera: Thyreocoridae) at the base of the buds, feeding on the sap of flowers, fruits and petioles (Figure 1c). None of the ants was seen carrying pollen grains, but C. atriceps and Dolichoderus sp. were observed near the nectaries at the moment of opening of the flowers, probably searching for nectar (Figure 1b). We also observed C. atriceps and Dolichoderus sp. collecting a sugary honeydew excreted by the Corimelaena nymphs. No Cephalotes ants were observed on this tree. On the trees without Corimelaena nymphs, that ants bit flower buds in search of nectar, making holes in the flower (Figure 1d). Damaged flowers stopped development (Figure 1e), reducing pollination and fruit formation in these trees. The tree with hemiptera formed approximately 70 flowers and 29 developing fruits, while the four trees without hemiptera had less than 20 flowers and five fruits.

Figure 1
Ants and Hemiptera on Lorostemon coelhoi Paula (Clusiaceae). A - Ant nests among the leaves; B - Ant visiting flowers in anthesis; C - Ant grazing hemipteran nymphs (black arrowheads); D - Flower bud of L. coelhoi with holes caused by ants (white arrows); E - Non-viable flower bud after predation by ants. Credit: S.L. Ferreira-Silva.

Lorostemon does not bear extrafloral nectaries and, when floral nectar was unavailable (e.g., flowers were closed or absent), honeydew was an alternative food source for ants. Even not having observed ants carrying pollen grains, Camponotus atriceps and Dolichoderus sp., which were probably searching for nectar (Figure 1b), might be considered possible pollinators of L. coelhoi. Camponotus in particular do not have metapleural glands, which are responsible for secreting antibiotic substances, which could reduce pollen viability (Beattie et al. 1984).

Although the number of individuals monitored in this study was too small to be conclusive, we suggest that the presence of hemiptera and their interaction with various ant species contributed to the reproductive success of the trees through a reduction of damaging herbivory by the ants. The traditional theory highlights hemiptera as a resource for the plant to attract ants for plant defense (Campos and Camacho 2014), but our preliminary observations suggest a different hypothesis in that the hemipterans have a crucial role in preventing ants from attacking nectar producing flowers and being nectar-thieves. We understand that other parameters could influence plant reproductive success, such as abiotic factors and morphological characteristics of each individual, however, our observations suggest the occurrence of a tripartite mutualistic interaction among organisms of three trophic levels that possibly has a significant contribution to the reproductive success of Lorostemon and deserves further investigation.

ACKNOWLEDGMENTS

We thank Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the fellowship granted to the first author, and the graduate program in Botany at Instituto Nacional de Pesquisas da Amazônia (INPA/PPG-BOT) for logistical support.

REFERENCES

Data availability

The data that support the findings of this study are available, upon reasonable request, from the corresponding author [Silvia Larissa Ferreira-Silva].

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