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Thrips species (Insecta: Thysanoptera) associated with flowers in a restinga fragment in northeastern Brazil/Especies de tripes (Insecta: Thysanoptera) associadas a flores em um fragmento de restinga no nordeste brasileiro.

1. Introduction

The world fauna of Thysanopotera includes approximately 6,000 species distributed in 800 genera (ThripsWiki, 2017). In the Neotropical Region, thrips have been relatively little studied, although this region has an enormous diversity of topography and flora, including mountains, large deserts and extensive tropical forests. According to Mound (2013), most thrips species recorded in South America are from Brazil.

According to Monteiro and Mound (2012), six of the eight families of thrips are found in Brazil (Uzelothripidae, Heterothripidae Merothripidae, Aeolothripidae, Thripidae and Phlaeothripidae) with a total of 576 species (Monteiro and Lima, 2011; Lima, 2017). However, thrips have been recorded from only a small part of the Brazilian territory, especially the states of Sao Paulo, Rio de Janeiro, Santa Catarina and Rio Grande do Sul (Monteiro and Mound, 2012; Lima, 2017). Santa Catarina and Sao Paulo alone account for more than half of the thrips fauna recorded in Brazil, mainly from studies carried out by Fritz Plaumann and J. Douglas Hood in the 1940s and 1950s (Monteiro, 2002; Lima, 2017).

In contrast, in northeastern Brazil, only a few studies of the Thysanoptera fauna have been conducted, mostly regarding cultivated plants, such as mango (Mangifera indica L.) in the state of Pernambuco (Oliveira et al., 2011); watermelon (Citrullus lanatus ((Thunb.) Matsum. & Nakai) in Rio Grande do Norte (Costa et al., 2015) and native and cultivated Fabaceae in Piaui and Maranhao (Lima et al., 2013a, b). In Ceara, there are also a few records of thrips species, mainly associated with zucchini squash (Curcubita pepo L.), onion (Allium cepa L.) and tomato (Solanum lycopersicum L.) (Lima et al., 2011).

It is essential to carry out studies involving the interaction of thrips and their hosts in their native areas, especially in neglected regions, in order to extend our knowledge of the Brazilian thrips fauna and the position that these insects occupy in different ecosystems. One of these native areas is the coastal forest habitat known as restinga, which exists in fragments that are severely threatened by human occupation along the entire Brazilian coast. So far, no thrips surveys in this type of environment have been conducted in the country, in contrast with the situation of other insect orders, such as Lepidoptera, Coleoptera and Diptera (Flinte et al., 2006; Monteiro et al., 2007; Silveira et al., 2008; Gostinski et al., 2016). The lack of such information impedes the development of conservation and management strategies for these and other organisms.

This study assessed the diversity of thrips in restinga remnants in the state of Ceara, Brazil, as an attempt to foster research on thrips in the Brazilian Northeast. Diversity was evaluated by means of diversity indices and a species-accumulation curve.

2. Material and Methods

2.1. Fieldwork

The collections were performed at points with flowering plants in a coastal forest (restinga) fragment in areas belonging to the Universidade Estadual do Ceara (UECE), Campus of Itaperi, Fortaleza, Ceara, Brazil (Figure 1). The UECE Itaperi Campus is located in the municipality of Fortaleza (03[degrees]47'45"S, 038[degrees]33'10"W, 38.4 m a.s.l.) and covers an area of 104 ha on the coastal plain, about 8 Km from the Ocean, with typical coastal vegetation (Esteves and Lacerda, 2000; IBGE, 2012), although heavily human-impacted (Brandao, 2003). This remnant is composed mainly (70%) of plants with a mean height of 6 meters that lose more than 30% of their leaves during the dry season. Aside from this, the vegetation near the campus buildings is herbaceous and shrubby, and remains green almost year-round.

A total of 86 plant species belonging to 34 families (Table 1) were sampled for thrips. Surveys were performed once a month in April, May, June and July 2011; February through August 2012; and February through August 2013. The plants were collected randomly, depending on the availability of flowers and inflorescences, typical habitats of common thrips (Lewis, 1973, 1997). Sampling was carried out between 7:00 and 9:00, and approximately 5 flowers from each species were placed in individual plastic bags and taken to the Laboratory of Insect-Plant Interaction, where the insects were screened under a stereomicroscope and the plant species were identified. The insects were stored in microtubes with AGA (10 parts of ethanol 60%, one part glycerin and one part glacial acetic acid) for preservation.

2.2. Identification

Adult thrips were mounted on permanent microscope slides and identified based on Mound and Marullo (1996). Plants were identified by comparison with herbarium specimens and using specialized literature (Bridson and Forman, 1998; Esteves and Lacerda, 2000; Brito et al., 2006; Moro et al., 2011). Vouchers of the thrips are deposited in the collection of the Laboratory of Insect-Plant Interaction (UECE).

2.3. Statistical analysis

A species-accumulation curve and species-richness estimators were calculated using the software EstimateS 9.1 (Colwell, 2013) in order to evaluate the sampling methods and to calculate the estimated richness ofthrips in the particular restinga fragment. Only nonparametric incidence-based estimators (ICE, Chao 2, Jackknife 1, Jackknife 2 and Bootstrap) (Gotelli and Colwell, 2001) were computed, using the classic model with 95% confidence intervals and 1000 randomizations. Also, the diversity indices of Shannon-Wiener (H') and Simpson (D) were calculated using the software DiVes 3.0.7 (Rodrigues, 2015). The Shannon-Wiener index was also calculated using data from plant families with higher richness of associated thrips to compare possible differences in diversity.

3. Results

A total of 456 thrips specimens belonging to 14 species were found in association with the coastal vegetation. Fifty-eight immatures (13 Tubulifera and 45 Terebrantia) were also found. The insects were associated with 36 of the 86 plant species sampled (Table 2). One probable new species of Treherniella was collected, and 46 new associations between thrips species and plants were established (Table 2), of which 13 are true host associations based on larvae collection (Table 2).

The accumulation curve did not reach an asymptote. The results obtained with the Chao 2, ICE and Jackknife 2 estimators indicate that at least ten more species may exist in the area. On the other hand, the resulting estimates of Bootstrap (17.88) and Jackknife 1 (22.58) are closer to the number of species effectively surveyed (Figure 2).

The Shannon-Wiener (H') and Simpson (D) indices for the sampled area were 1,7607 and 0.7769 respectively (Table 3). Thrips richness and abundance were concentrated in three plant families, Amaranthaceae, Caesalpiniaceae and Poaceae. Plant species of the three families harbored two-thirds of the thrips species collected, and about half of the thrips abundance sampled (Tables 1 and 2).

4. Discussion

This study established the first records of association between several thrips species and restinga plants in Brazil (Table 2). Fourteen species (seven of which, Androthrips ramachandrai, Frankliniella brevicaulis, F. gemina, F. insularis, F. tritici, Haplothrips gowdeyi, Heliothrips haemorrhoidalis, are new records) are added to the total known from state of Ceara, and the genus Treherniella is a new record in Brazil. This genus has been found on members of Poaceae in native vegetation in northern Italy (Marullo and Grazia, 2013), as well as in southern United States (Diffie et al., 2008) and in Paraguay and Argentina (ThripsWiki, 2017). Apart from Treherniella sp., all thrips species sampled in our study have been found in surveys conducted in different states of Brazil, i.e. Piaui and Maranhao (Lima and Zucchi, 2016), Rio Grande do Norte (Cavalleri et al., 2011) and Rio Grande do Sul (Pinent et al., 2005, 2006).

Most of these species are phytophagous, except for A. ramachandrai, a predator of Gynaikothrips spp. (Melo et al., 2013). The fiding 46 new associations of plant species with thrips in Brazil, along with the 13 true host associations demonstrates the importance of coastal vegetation in maintaining populations of thrips. Although the species identified are common on cultivated plants in other areas of Brazil, the failure to find other different species in the vegetation of this area is probably related to the degree of environmental alteration.

In southern Brazil, other studies in a natural area found a thrips richness in Itapua State Park (Cavalleri, 2005; Pinent et al., 2005, 2006) that is double the level observed in our study. However, the incomplete stabilization of the species-accumulation curve indicates that a higher richness of thrips species may be found in the fragments of coastal vegetation sampled. Moreover, the collection effort (number of surveys) and specimens collected was also higher in Rio Grande do Sul. Therefore, an increase in collection efforts may well demonstrate a higher richness of thrips species in the restinga fragment sampled here.

The diversity indices calculated in our study indicate that some species are more abundant in the area, thus leaving the diversity relatively low. The Simpson Index of the complete sample was close to 1 (Table 3), a result of the high abundances of a few species (mainly F. insularis and Microcephalothrips abdominalis). The diversity levels within the plant families with the highest richness of thrips species were slightly higher. This can be explained by the exclusion of species with low abundance collected from other plant families (Table 2). Cavalleri (2005), in Rio Grande do Sul, found a higher diversity (D = 0.211), as the species showed more uniform abundances.

The Shannon-Weiner index also indicated a low diversity. In Itapua State Park, the index value was 2.19 and there were differences between the plant family with the highest thrips richness (Asteraceae) and the other families (Cavalleri, 2005). Although the collection methods used by the author are different, these comparisons give an idea of the relative diversity of these different areas.

In Brazil, very few systematic surveys of thrips in natural ecosystems have been performed, and there are no assessments of the importance of preserving natural areas for conservation of these insects. Especially in the northeast region of this country, where the biodiversity of these insects is little known, efforts must be made to better understand the patterns and size of thrips populations. Restinga fragments in Brazil are fragile ecosystems threatened by human settlement. The area studied here is located near to built-up areas of one of the largest cities in northeastern Brazil, and is under environmental stress. The existence of a diverse fauna of insects harbored by many plant species is an important reason to carry out efforts for their conservation.

Acknowledgements

To the Programa de Extensao Universitaria (PROEX) and the Fundacao Cearense de Apoio ao Desenvolvimento Cientifico e Tecnologico (FUNCAP) for the research scholarships granted; to Gessiane da Silva Viana for the help in the sampling; and to Dr. Laurence A. Mound (ANIC/CSIRO, Australia) for his help in the identification of some thrips.

http://dx.doi.org/10.1590/1519-6984.169071

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I. M. B. Lima (a)*, M. A. Almeida-Filho (b), M. G. A. Lima (b), O. H. Bonilla (b) and E. F. B. Lima (c)

(a) Universidade Federal do Ceara--UFC, Avenida Mister Hull, s/n, Campus do Pici, CEP 60455-760, Fortaleza, CE, Brasil

(b) Laboratorio de Interacao Inseto-Planta--LABIIP, Universidade Estadual do Ceara--UECE, Avenida Dr. Silas Munguba, 1700, Campus do Itaperi, CEP 60740-000, Fortaleza, CE, Brasil (c) Universidade Federal do Piaui--UFPI, BR 343, Km 3,5, Campus Amilcar Ferreira Sobral, CEP 64800-000, Floriano, PI, Brasil

* e-mail: isabellymbl@hotmail.com

Received: September 9, 2016--Accepted: August 30, 2017--Distributed: February 28, 2019 (With 2 figures)

Caption: Figure 1. Location of the remnants of restinga vegetation in Fortaleza, Ceara, Brazil (UECE--Itaperi Campus) (03[degrees]47'45"S, 038[degrees]33'10"W, 38.4 m a.s.l.). (A) State of Ceara on Brazil's map; (B) Location of the municipality of Fortaleza, State of Ceara; (C) Sampling area in Universidade Estadual do Ceara, Campus Itaperi, Fortaleza, CE, Brazil.

Caption: Figure 2. Species accumulation curve and richness estimators for thrips species recorded in restinga fragment in the municipality of Fortaleza, Ceara, Brazil from 2011 through 2013.
Table 1. Plant species surveyed during thrips collections in resting
a fragment on the campus of State University of Ceara, Brazil.

Family            Species

Acanthaceae       Thunbergia erecta (Benth.) T. Anderson

Anacardiaceae     Anacardium occidentale L.

Amaranthaceae     Alternanthera brasiliana (L.) Kuntze
                  Amaranthus deflexus L.
                  Celosia cristata L.
                  Froelichia interrputa (L.) Moq.

Apocynaceae       Allamanda cathartica L.
                  Catharantus roseus L.
                  Nerium oleander L.

Asteraceae        Aspilia cearensis J.U. Santos
                  Bidens bipinnata L.
                  Blainvillea rhomboidea Cass.
                  Centratherum punctatum Cass.
                  Emilia coccinea (Sims) G. Don
                  Helianthus annuus L.
                  Tithonia diversifolia (Hemsl.) A. Gray

Bixaceae          Bixa orellana L.

Bombacaceae       Chorisia glaziovii (Kuntze) E. Santos

Boraginaceae      Cordia leucocephala Moric
                  Heliotropium indicum L.

Cactaceae         Opuntia cochenillifera (L.) Mill

Caesalpiniaceae   Aeschynomene viscidula Michx
                  Caesalpinia ferrea Martins
                  Caesalpinia leiostachya
                  Cicer arietinum L.
                  Clitoria fairchildiana R.A. Howard
                  Clitoria ternatea L.
                  Crotalaria incana L.
                  Macroptiliem lathyroides L.
                  Mimosa sp.
                  Senna obtusifolia (L.)
                  Senna sp.

Capparaceae       Cleome affinis D.C.

Commelinaceae     Commelina benghalensis L.

Convolvulaceae    Evolvulus anagalloides Meisn.
                  Ipomea asarifolia (Desr.)
                  Ipomoeapes-caprae (L.) R.Br.
                  Merremia aegyptia (L.) Urb.

Cucurbitaceae     Momordica charantia L.
                  Cucurbita moschata Duchesne ex Poir

Cyperaceae        Cyperus esculentus
                  Cyperus ferax (L.) Rich
                  Cyperus ligularis L.

Euphorbiaceae     Chamaesyce hyssopifolia L.
                  Croton Lobatus L.
                  Euphorbia hyssopifolia L.

Heliconiaceae     Heliconia sp.

Lamiaceae         Hyptis simulans Epling
                  Mesosphaerum suaveolens (L.) Kuntze

Malpigiaceae      Byrsonima crassifolia (L.) Rich

Malvaceae         Guazama ulmifolia Lam.
                  Hibiscus rosa-sinensis L.
                  Pavonia cancellata (L.) Cav.
                  Sida cordifolia L.
                  Sida galheirensis Ulbr
                  Sida micrantha A. ST. -Hill
                  Sidastrum micranthum A. ST. -Hil
                  Waltheria indica L.
Nyctaginaceae     Boerhavia diffusa L.

Oxalidaceae       Oxalis divaricata Mart. ex Zucc

Plantaginaceae    Angelonia campestris Nees & Mart
                  Scoparia dulcis L.

Poaceae           Cenchrus echinatus L.
                  Cynodon dactylon (L.) Pers.
                  Eleusine indica (L.) Gaertn
                  Melinis repens (Wild.) Zizka
                  Panicum maximum Jacq.
                  Paspalum plicatulum Michx
                  Paspalum urvillei Steud.
                  Pennisetum purpureum Schum
                  Setaria parviflora (Poir) Kerguelen

Rosaceae          Cydonia oblonga Mill.

Rubiaceae         Richardia grandiflora Steud
                  Spermacoce verticillata L.

Rutaceae          Citrus sinensis

Saxifragaceae     Philadelphus caucasicus Koehne

Solanaceae        Solanum asperum L. C. Rich.

Sterculiaceae     Guazuma ulmifolia Lamark

Turneraceae       Turnera subulata Sm.

Typhaceae         Thypa angustifolia L.

Verbenaceae       Clerodendrum splendens G. Don.
                  Duranta repens L. "aurea"
                  Lantana camara L.
                  Priva bahiensis A. DC.
                  Stachytarpheta coccinea Schauer

Zingiberaceae     Alpinia purpurata K. Schum

Table 2. Thrips species of thrips and their respective hosts in
fragment of restinga vegetation in the municipality of Fortaleza,
Ceara, Brazil.

Thrips species         Associated Plant species      Thrips individuals

                                                     [male]   [female]

Arorathrips            Eleusine indica                 --        1
mexicanus (Crawford)   Waltheria indica *              --        1

Frankliniella          Bixa orellana                   1         4
brevicaulis (Hood)     Celosia cristata *              --        6
                       Thunbergia erecta *             --        6

Frankliniella          Aspilia cearensis *             --        1
gardeniae (Moulton)    Cicer arietinum  *              --        1
                       Crotalaria incana               --        8
                       Guazuma ulmifolia *             --        1

Frankliniella gemina   Cicer arietinum *               --        6
(Bagnall)

Frankliniella          Bixa orellana +                 10        26
insularis (Franklin)   Caesalpinia leiostachya * +     3         15
                       Centratherum punctatum *        --        3
                       Clitoria fairchildiana * +      22        65
                       Clitoria ternatea *             --        2
                       Crotalaria incana               --        1
                       Mesospherum suaveolens *        --        1
                       Momordica charantia             --        7
                       Pennisetum purpureum *          --        2
                       Senna sp.                       --        1
                       Thunbergia erecta *             --        1

Frankliniella          Allamanda cathartica *          --        1
schultzei (Trybom)     Anacardium occidentale *        --        4
                       Celosia cristata * +            7         27
                       Clitoria ternatea *             --        5
                       Crotalaria incana               --        10
                       Froelichia interrupta *         --        8
                       Ipomoea pes--caprae *           1         1
                       Momordica charantica +          --        10
                       Pavonia cancellata *            7         --

Frankliniella          Crotalaria incana               --        1
tritici (Fitch)        Allamanda cathartica *          --        3
Microcephalothrips
abdominalis
(Crawford)

                       Aspilia cearensis *             --        3
                       Bixa orellana *                 --        6
                       Blainvillea rhomboidea *        --        1
                       Centratherum punctatum * +      --        12
                       Celosia cristata *              --        1
                       Citrus sinensis *               --        2
                       Clitoria ternatea *             --        1
                       Crotalaria incana * +           --        12
                       Helianthus annuus               --        1
                       Scoparia dulcis *               --        4
                       Setaria parviflora * +          --        13
                       Stachytarpheta coccinea *       --        4
                       Thunbergia erecta *             --        10
                       Tithonia diversifolia * +       --        29

Selenothrips           Anacardium occidentale +        --        2
rubrocintus (Giard)

Caliothrips phaseoli   Anacardium occidentale          --        1
(Hood)

Heliothrips            Bixa orellana *                           1
haemorrhoidalis
(Bouche)

Androthrips            Anacardium occidentale *        --        5
ramachandrai (Karny)   Cyperus esculentus              --        1

Haplothrips gowdeyi    Amaranthus deflexus             --        1
(Franklin)             Blainvillea rhomboidea *        --        3
                       Celosia cristata * +            --        11
                       Chamaesyce hyssopilia           --        1
                       Curcubita moschata              --        1
                       Cyperus esculentus *            --        4
                       Eleusine indica *               --        1
                       Euphorbia hyssopifolia *        --        1
                       Paspalum urvillei * +           --        18
                       Sida gatherensis * +            --        21
                       Waltheria indica *              --        2

Haplothrips trellesi   Waltheria indica *              --        2
(Moulton)

Treherniella sp.       Pavonia cancellata              --        1

TOTAL                                                  51       405

* New records of association with plant species in Brazil;
+ Host--associations based on larvae collection.

Table 3. Diversity indices of the thrips species in resting a
fragment in the municipality of Fortaleza, Ceara, Brazil.

Index                                      Values

Shannon-Wiener (H')    Sample              1,7607
                       Amaranthaceae       0.8723
                       Caesalpiniaceae     0.8366
                       Poaceae             1.0661
Simpson (D)            Sample              0.7769
                       Amaranthaceae       0.4852
                       Caesalpiniaceae     0.4019
                       Poaceae             0.5378
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Title Annotation:Original Article
Author:Lima, I.M.B.; Almeida-Filho, M.A.; Lima, M.G.A.; Bonilla, O.H.; Lima, E.F.B.
Publication:Brazilian Journal of Biology
Date:Feb 1, 2019
Words:3892
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