Do thrips (Insecta: Thysanoptera) cause economic damage to Hancornia speciosa Gomes fruits?

ABSTRACT

The mangaba Hancornia speciosa Gomes (Apocynaceae) is more commercially viable than other native Cerrado fruit trees due to its nutritional properties and high production of fruit used in food products. Although thrips have been reported injuring mangaba, the identification of possible species of economic importance is not yet available. Thus, identifying species that may threaten mangaba plant health is a vital step in implementing management strategies. The aim of this present study was to survey thrips species during the reproductive stage of H. speciosa, determine the variety most susceptible to damage caused by these insects and to check whether the damage is economically important to this fruit tree. Thrips were collected from the ex-situ germplasm of the Agronomy School of the Federal University of Goiás, in Goiás state, Brazil. Twelve plants of three H. speciosa varieties (gardneri, cuyabensis and pubescens) were selected, from which 20 flowers and 20 fruits were assessed for the presence of thrips in September 2018 and 2019. A total of 1,306 thrips representing 13 species were collected from flowers. Of these, Frankliniella gemina was the most abundant. On the fruits, circular lesions were observed, initially as white spots that subsequently turned silver, possibly caused by Heliothrips longisensibilis. These injuries are superficial, rarely compromising large portions of the fruit, and do not cause economic damage. Therefore, thrips are not a primary threat to fruit production for fresh consumption or processing.

Keywords:
Apocynaceae; Frankliniella gemina; Heliothrips longisensibilis; Thripidae

Introduction

The mangaba, Hancornia speciosa Gomes (Apocynaceae), is widely distributed in Brazil and stands out among other fruit trees in the Brazilian Cerrado for its high fruit production. Mangaba fruits are mainly obtained from extractivism, practiced by traditional peoples (Silva Júnior and Lédo, 2016). In Brazil, 1849 tons of mangaba were produced in 2022, with emphasis on the northeastern states of Paraíba, Sergipe and Bahia (IBGE, 2022). The fruits consumption usually occurs in natura or in juices, ice creams, jellies and others (Oliveira and Aloufa, 2021). Flowering occurs from June to November, and the fruits are harvested from October to December (Silva et al., 2001), although some production can be obtained off-season. Despite the food production potential of this fruit tree species, information on its management remains scarce (Pereira et al., 2010).

Reports of insects associated with mangaba suggest their occurrence primarily in nurseries (Pereira et al., 2010). The most abundant insects associated on mangaba plants are aphids and leafcutter ants (Vieira Neto et al., 2002), as well as scale insects (Silva et al., 2021), caterpillars, irapuá bees, stink bugs (Michereff Filho and Michereff, 2006) and gall midges (Maia et al., 2023). Mites are also reported, albeit less frequently (Silva et al., 2020).

In addition to these groups, a few thrips species native to the Neotropics are abundant in H. speciosa: Coremothrips nubilicus (Hood, 1954) and Heliothrips longisensibilis Xie, Mound and Zhang, 2019 are predominantly found on leaves (Silva et al., 2019), whereas Frankliniella musaeperda Hood, 1952 is usually found on flowers (Alves-Silva et al., 2013). C. nubilicus is endemic to Brazil and has no economic importance (Lima, 2023). H. longisensibilis is recorded from Argentina and Brazil and introduced to China, causing harm to a few crops (Lima et al., 2020, 2021). F. musaeperda is reported from Brazil, Haiti and Dominican Republic and can injury bananas (Hood, 1952; Lima, 2023).

Thrips are abundant in the dry season and cause direct damage to mangaba due to feeding and oviposition (Silva et al., 2019). Direct observations allowed to describe these injuries as white spots that subsequently turn silver. These lesions are frequently observed, but their relative importance to production remains unknown. In addition, the species that cause such damage has not yet been identified (Pereira et al., 2010).

While studies have reported the presence of thrips on mangaba leaves and flowers, the relationship between these insects and the fruits is not yet understood. Thus, it is important to investigate whether mangaba varieties differ in terms of damage caused by thrips, and if thrips species associated with the leaves and flowers of these plants can also harm the fruits.

Given the potential of using H. speciosa in different industrial products or consuming its fresh fruit, studying the species associated with the reproductive parts of the plant and characterize the damage they cause is important. As such, this study aimed to survey the thrips population during the reproductive stage of H. speciosa and describe the damage that these insects cause to mangaba fruits.

Material and methods

Thrips were collected from the ex-situ germplasm of the Agronomy School (16º 35' 39'' S and 49° 17' 07'' W, altitude of 733 m) of the Federal University of Goiás, in Goiás state, Brazil. A randomized block design was used, with four repetitions and four H. speciosa varieties (speciosa, cuyabensis, gardneri and pubescens).

In order to assess thrips species associated with mangaba fruits and flowers, twelve plants of three varieties (gardneri, cuyabensis and pubescens) were selected. The variety speciosa was excluded from the study due to the small number of fruits and flowers during the assessment period. Collections were carried out during the reproductive stage of mangaba in September (full bloom) 2018 and 2019. For each plant, 20 flowers were collected and 20 fruits were assessed for lesions and thrips specimens. The specimens collected were mounted on permanent microscope slides, according to the methodology described by Monteiro (1994), and identified using the identification keys proposed by Mound and Marullo (1996) and Cavalleri and Mound (2012). Voucher specimens are deposited in the Natural History Collection of the Federal University of Piauí, Floriano, Brazil.

Lesions were visually assessed on fruits of the same age (peak fruiting for the different varieties) in October 2018 and 2019. The fruits were classified on a scale of 1 to 5, based on Goane et al. (2013), according to the level of damage, where 1 indicates no damage, 2 mild damage, 3 moderate, 4 severe, and 5 very severe (Fig. 1).

Figure 1
Hancornia speciosa fruits with damage caused by Thysanoptera. A- no damage, B- mild damage, C- moderate damage, D- severe damage and E- very severe damage.

Statistical analysis

A generalized linear mixed model (GLMM) with Gaussian distribution was used to assess thrips-related damage on fruits. Average fruit damage was used as a response variable, variety as a predictor variable for fixed effects, and plot and collection year as random effects variables. The analyses were performed using the lme4 package of R 4.0.2 software (Bates et al., 2015). The residuals obtained were checked for compliance with the assumptions of analysis of variance (ANOVA) using the Lilliefors and Levene’s tests, and then submitted to ANOVA via Tukey’s test, with Bioestat® software.

Results and discussion

A total of 1,306 thrips specimens were found on H. speciosa flowers (Table 1), belonging to the families Thripidae and Phlaeothripidae (Table 1). The variety gardneri exhibited the largest thrips population (p=0.039) (43.93%), followed by cuyabensis and pubescens (Fig. 2).

Table 1
Thrips associated with the flowers of Hancornia speciosa varieties from the ex-situ germplasm collection of the School of Agronomy – Federal University of Goiás, Goiânia, in 2018 and 2019.

Family	Species	2018	2019	Total
Phlaeothripidae	Haplothrips gowdeyi (Franklin, 1908)	1	7	8
Thripidade	Coremothrips nubilicus (Hood, 1954)	2	0	2
	Frankliniella brevicaulis Hood, 1937	0	1	1
	Frankliniella gardeniae Moulton, 1848	249	161	410
	Frankliniella gemina Bagnall, 1919	377	144	521
	Frankliniella insularis (Franklin, 1908)	3	13	16
	Frankliniella musaeperda Hood, 1952	36	25	61
	Frankliniella serrata Moulton, 1933	0	1	1
	Frankliniella schultzei (Trybom, 1910)	0	1	1
	Frankliniella tritici (Fitch, 1855)	35	33	68
	Heterothrips striatus Moulton, 1932	0	1	1
	Frankliniella sp.	0	2	2
	Frankliniella sp. n.	5	4	9
	Frankliniella spp. immatures	142	63	205
Total	-	850	456	1306

Figure 2
Abundance of thrips found on the flowers (mean + standard deviation) of Hancornia speciosa varieties from the ex-situ germplasm of the School of Agronomy – Federal University of Goiás. Means followed by the same letter do not differ according to Tukey’s test (p≤0.05).

Thirteen thrips species were identified on mangaba flowers, of which the most abundant were Frankliniella gemina Bagnall, 1919 and F. gardeniae Moulton, 1948 (Table 1). Frankliniella species (Fig. 3B) are commonly associated with flowers of several hosts (Cavalleri et al., 2018), and were the predominant group surveyed. This contrasts with the most abundant thrips species on leaves, C. nubilicus (Silva et al., 2019).

Figure 3
Hancornia speciosa flowers from an ex-situ germplasm, Goiânia, Goiás. A- flower with no thrips, B- Frankliniella sp. on the corolla of a mangaba flower.

Most of the Frankliniella species identified in the present study were previously reported in the Cerrado biome in different hosts (Lima, 2023). In studies conducted by Alves-Silva et al. (2013), F. musaeperda was observed on mangaba flowers in Minas Gerais state. The same insect species was also reported on Palicourea rigida Kunth flowers (Rubiaceae) (Cardoso et al., 2016). The present study is the first record of F. musaeperda in Goiás state, a species previously identified in states in southeastern (Minas Gerais and São Paulo) and southern (Paraná) Brazil (Lima and Miyasato, 2017; Lima, 2023).

Frankliniella species are reported in flowers of various plants (Lima et al., 2016), in which they can cause injuries characterized by light patches. For instance, on soybeans F. schultzei was observed feeding on pollen and causing premature flowers fall, resulting in a productivity reduction (Neves et al., 2022). In the present study, however, no thrips-related damage was observed on the mangaba flowers (Fig. 3A). On the other hand, Frankliniella species may also feed on H. speciosa flower pollen, as other congeneric species do on other plants (e.g. Danieli-Silva and Varassin, 2012). Pollen grains may adhere to the insects during feeding, possibly resulting in the indirect pollination of mangaba plants. However, specific research is needed to confirm this hypothesis. To date, moths from the families Sphingidae (Pereira et al., 2010), Hesperiidae and Nymphalidae (Darrault and Schlindwein, 2006) are reported as the main mangaba pollinators.

The lesions on the fruits may have been caused solely by H. longisensibilis (Fig. 4), since adults and larvae of this species were the only ones found associated with injury on cuyabensis and gardneri varieties. Lima et al. (2020) reported that other species of the subfamily cause similar lesions, including Heliothrips spp., but no other species were observed feeding on the fruits. Though most cuyabensis fruits presented mild damage, some exhibited severe lesions. The variety pubescens had the lowest number of damaged fruits, possibly the presence of trichomes may indicate antiherbivore defense.

Figure 4
Hancornia speciosa Gomes fruits with damage caused by Heliothrips longisensibilis. A- Adults and B- Larvae.

Silva et al. (2019) found a larger H. longisensibilispopulation on gardneri leaves, whose adaxial surface is glabrous, with pubescence along the central vein on the abaxial surface (Monachino, 1945). However, Scott-Brown and Simmonds (2006) reported that Heliothrips occurs in plants with smooth or coriaceous leaves. In mangaba, H. longisensibiliscauses whitish lesions on the leaves, beginning at the margin and progressing toward the center, typically associated with dark-colored droppings (Silva et al., 2019). The lesions observed on the fruits are similar to those that occur on leaves, characterized by white spots that subsequently turn silver, with no damage in the center (Fig. 4B). Fecal droplets associated with the above-mentioned lesions are also visible.

Despite the morphological differences observed on leaves and flowers of the three mangaba varieties, their fruits exhibited similar damage (Fig. 5). As a result, the lesions on the fruits were expected to differ between varieties. While cuyabensis has glabrous leaves and corollas, gardneri differs from the other varieties by presence of trichomes on the dorsal surface or midrib of its leaves. On the other hand, in pubescens, trichomes are located on the abaxial surface of leaves, with pubescent corollas, lobes and outer floral tube (Monachino, 1945). The flowers are white, hermaphroditic, tubular and fragrant. The inflorescence has seven flowers (Almeida, 1998). The fruits are generally rounded and berry-like, measuring 2.5 to 6 cm, and display a variety of shapes and colors, ranging from yellow to greenish, with or without red pigment (Silva et al., 2001).

Figure 5
Average score (+ confidence interval) on a scale of 1 to 5 for thrips-related damage to the fruits of Hancornia speciosa varieties from the ex-situ germplasm of the School of Agronomy – Federal University of Goiás, Goiânia, Goiás.

Different thrips-related damage is observed in other fruit species. In the peach Prunus persica L. (Rosaceae), F. occidentalis(Pergande, 1895) causes bronzing on the fruit surface and skin splitting (Tommasini and Ceredi, 2007), whereas damage to mangaba fruits is superficial. In mangaba, small populations of other Frankliniella species were observed only on the leaves, with no thrips-related damage to the fruits (Silva et al., 2019). Thrips-related damage in Vitis viniferaL. (Vitaceae) forms a whitish halo around small scars on the fruits (Moreira et al., 2014), similar to the lesions observed in H. speciosa. In lemon trees Citrus limon L. (Rutaceae), damage caused by the thrips species Pezothrips kellyanus (Bagnall, 1916) results in grayish or silver fruit or a ring at the peduncle base (Belaam-Kort and Boulahia-Kheder, 2017). Research conducted by Goane et al. (2013) in lemon orchards demonstrated that the density of Chaetanaphothrips orchidii (Moulton, 1907) was related to fruit phenology, with greater densities in ripe fruits and damage concentrated on those at the bottom of the trees.

No predator thrips were identified on fruits or flowers of H. speciosa. Studies on Thysanoptera are important because these arthropods can cause direct and indirect damage to a variety of plants. In mangaba plants, thrips damage only the fruits. Although lesions were observed in all the varieties analyzed, the scores attributed were low, indicating that the damage was not extensive. This means that the damage would not result in economic losses that might compromise fruit quality and use of the pulp. Moreover, the fruits might not be rejected by consumers for fresh consumption, despite the aesthetic damage.

Conclusions

A complex of Frankliniella species predominates on flowers of Hancornia speciosa, especially Frankliniella gemina. Despite the injuries observed on the fruits, thrips do not economically harm the fruits of H. speciosa.

Acknowledgments

The authors are grateful to the Coordination for the Improvement of Higher Education Personnel (CAPES) for the grant awarded to the first author, and to the curator of the mangaba collection, Rita Maria Devós Ganga, for the opportunity to study Hancornia speciosa.

The research data were obtained under a license granted by the Ministry of the Environment (MMA), Chico Mendes Institute for Biodiversity Conversation (ICMBio) and Biodiversity Information and Authorization System – SISBIO, Number: 66240-1, Authentication code: 0662400120181123.

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Edited by

Associate Editor:

Marcelo Picanço

Publication Dates

• Publication in this collection
  02 Aug 2024
• Date of issue
  2024

History

• Received
  10 Nov 2023
• Accepted
  15 May 2024