New records and update on the geographic distribution of fifteen species of Lincus Stål , 1867 ( Insecta : Hemiptera : Pentatomidae ) associated with palms and coconut trees in the Neotropics

The Neotropical genus Lincus Stål, 1867 is frequently associated with the transmission of diseases to palms and coconut trees (Elaeis guineensis and Cocos nucifera) in commercial plantations in South America. Here we update the geographical distribution of 15 species of Lincus collected in E. guineensis and C. nucifera in the Neotropics. The geographical range of five species is expanded with new countries recorded for L. malevolus and L. styliger, and detailed geographic information is given for the first time for L. lobuliger and L. securiger.

The distribution of phytophagous insects is deeply related to the availability of vascular plants for their feeding.The insects' piercing-sucking feeding mode can be related to the transmission of many plant diseases.Among the hemipterans, insects potentially vectors of microbial plant pathogens, the heteropterans have been significantly reported as disease transmitters in the Neotropical Region.Among a diversity of plants serving as shelter and food source for many stink bugs (Pentatomidae), the coconuts and palms frequently receive microorganisms transmitted through the bugs' saliva.Diseases such as the Marchitez sorpresiva in palms (Elaeis guineensis) and the hartrot in coconut (Cocos nucifera) can affect large plantations, harming the production of a great diversity of natural products that maintain the economy in Neotropical countries, especially in the Amazon region (Howard 2001;Araújo et al. 2003;Mitchell 2004).The trees usually die two months after the first symptoms of the disease, which includes the progressive browning and desiccation of the leaves, rot of roots and tissues, and the drying and fall of fruits in mature plants (Camargo 1999;Araújo et al. 2003).The causal agent of hartrot and Marchitez is a protozoan of the family Trypanosomatidae, Phytomonas staheli McGhee & McGhee, 1979.This pathogen can be transmitted by pentatomids of the tribe Ochlerini as Macropygium Spinola, 1837, Ochlerus Spinola, 1837, and mainly Lincus Stål, 1867 (Couturier & Kahn 1989, 1992;Camargo 1999;Howard 2001;Mitchell 2004;Di Lucca et al. 2013).
In this work we update the known distribution of the 15 species of Lincus that occur in palms and coconut trees.The data were reviewed from literature, and complemented by the specimen data available in the entomological collection of the Federal University of Rio Grande do Sul (UFRG), Brazil.Voucher specimens of all species with new distribution data are deposited in UFRG (numbers LES0001/16 to LES0053/16).Additionally, five males and five females of Lincus curvatus Campos & Roell, 2017 are deposited in the Pontificia Universidad Católica del Ecuador (PUCE) (vouchers are not numbered in this collection).We also received images of type specimens and their labels from the following collections: American Museum of Natural History, USA (AMNH); California Academy of Sciences, USA (CASC); David A. Rider collection, USA (DARC); Natural History Museum of London, United Kingdom (NHMUK); Senckenberg Deutsches Entomologisches Institut, Germany (SDEI).
The geographic coordinates are in decimal degrees and were taken from software Google Earth (version 7: https:// www.google.com/earth/)and the map (Figure 2) was made using the software ArcGIS Desktop (version 10.4.1: http:// desktop.arcgis.com).Dolling, 1984 Figures 1A, 2, 3A; Tables 1, 2 Body brown, length between 10.2-10.9mm, with 1 + 1 yellowish spots on humeral angles, and on apex of radial veins.Mandibular plates longer than clypeus; apex of mandibular plates and clypeus light brown, slightly translucent on apex.Pronotal lobes subtriangular, anterior margins sinuous, directed anteriorly, surpassing the lateral limit of eyes (fig.3A, pl).Ventral rim of pygophore V-shaped, its sides straight.Segment X conical, not expanded at apex.

Lincus apollo
As mentioned by Dolling (1984), the female of L. apollo runs to L. styliger Breddin in Rolston's (1983) key, but they can be differentiated by the smaller dimensions of L. apollo.In addition, the posterolateral angles of the pygophore are apically emarginate in L. apollo, and obtuse in L. styliger.

Lincus bipunctatus
Lincus bipunctatus is included in Rolston's (1983) key as L. croupius Rolston.This species was compared to L. fatigus Rolston by Rolston (1983) because both have deflected pronotal lobes; however, the pronotal lobes of L. bipunctatus are broad and convex anteriorly, while in L. low spots on apex of radial veins.Distal two antennomeres, labium and tarsi yellowish.Mandibular plates slightly longer than clypeus, not convergent.Pronotal lobes broad, deflexed toward apex, surpassing the lateral limit of eyes about one-half width of each eye, anterior margins convex (Fig. 3B).Ventral rim of pygophore V-shaped, setose, and  Table 1.List of the species of Lincus associated with palms and coconut trees in the Neotropical Region.

Lincus curvatus
As mentioned by Campos & Roell (2017), this species can be misidentified as L. lamelliger Breddin or L. subuliger Breddin in Rolston's (1983) key; however, L. curvatus can be distinguished by the the asymmetrical segment X of males.

Lincus dentiger
Lincus dentiger is included in Rolston's (1983) key, identified on step 28 through characteristics of male genitalia, or on step 32 through characteristics of the pronotal lobes.Besides that, this species is included in the "big-eyed" convenience group (Rolston 1983) along with L. breddini Rolston, L. lamelliger, L. laminatus Rolston, L. lobuliger Breddin, L. rufospilotus (Westwood), L. styliger, L. substyliger Rolston and L. vallis Rolston.The main difference between L. dentiger and the other species of this group is the lyreshaped ventral rim of phygophore.
We examined the labels of the female holotype through images received from SDEI.In addition, we examined one female in the collection of UFRG, which is from a new locality in Ecuador.Rolston, 1983 Figures 1E, 2, 3C; Tables 1, 2 Body dark brown, measuring about 9.20-11.30mm, yellow stained on humeral angles, discal corium, and on middle of each connexival segment.Mandibular plates slightly longer than clypeus, not convergent, vertex of head slightly tumescent.Eyes small, width of each eye no more than half of interocular distance.Pronotal lobes subrectangular, apically expanded, truncate, anterior margins straight, surpassing the lateral limit of eyes more than width of each eye (Fig. 3C) (Rolston 1989).Ventral rim of pygophore V-shaped, with setae along the margin, medially carinated.Segment X expanded, longer than pygophore, apex rounded (Rolston 1989, figs. 1, 2, 3 and 4).

Lincus hebes
Lincus hebes was described after the review of Lincus (Rolston 1983) and placed in the "little eyed" convenience group (Rolston 1983(Rolston , 1989)).Although this species runs to L. armiger Breddin in Rolston's key, these two species can be distinguished by the pronotal lobes: rectangular in L. hebes and digitiform in L. armiger.
We examnied the labels of a male paratype through images from CASC.We also examined two specimens at UFRG from the same locality as the paratype.Rolston, 1983 Figures 1F, 2, 3D; Tables 1, 2 Body dark brown, measuring between 12.55-12.80mm, Table 2. Distribution records for the species of Lincus associated with palms and coconut trees in the Neotropical Region.New collection sites located in previously registered countries or states/provinces are referred to as "new locality", whereas new collection sites located in also new registered countries or states/provinces are referred to as "new record".yellow stained on humeral angles, base and apex of scutellum, apex of each radial vein and on middle of each connexival segment.Mandibular plates longer than clypeus, convergent.Eyes large, width of each eye more than half of the interocular distance.Pronotal lobes apically expanded, hatchet-shaped, surpassing the lateral limit of eyes (Fig. 3D) (Rolston 1983).Pygophore subrectangular, ventral rim concave with setae along the margin, medially carinated.Apex of segment X expanded and flattened (Maciel et al. 2015, figs. 11 and 12).Lincus incisus is included in Rolston's (1983) key.Recently, the male of L. incisus was described by Maciel et al. (2015) who presented new distribution records for the species.Dolling, 1984 Figures 1G, 2, 4B; Tables 1, 2 Body ocher to dark brown, measuring between 9.70-10.60mm, basal half of head and pronotum darker than apex, three yellow spots on base of scutellum, 1 + 1 on apex of each radial vein, and one on middle of each connexival segment.Mandibular plates slightly longer than clypeus, not convergent.Pronotal lobes subtriangular, longer than wide, surpassing the lateral limit of eyes (Dolling 1984, fig. 1).Ventral rim of pygophore U-shaped, with a medial obtuse projection at level of apex of segment X. Segment X globular, expanded, deflexed and spatulated apically (Fig. 4B) (Dolling 1984, fig. 2).Gonocoxitos 8 tetragonal (Dolling 1984, fig. 4).

Lincus lethifer
Lincus lethifer was compared to L. anulatus Rolston by Dolling (1984) who claimed the shape of gonocoxites 8, tetragonal in L. lethifer and rounded in L. anulatus, is sufficient to distinguish the two species.

Lincus lobuliger
Lincus lobuliger is included in Rolston's key (1983) and placed in the "big-eyed" convenience group (Rolston 1983).The characteristics that distinguish this species from the others in this group are: mandibular plates not convergent (convergent in L. vallis); pronotal lobes longer than wide and surpassing the lateral limit of eyes (not surpassing in L. breddini, and as long as wide in L. lamelliger); ventral rim of pyogophore U-shaped (V-shaped in L. dentiger, L. laminatus, and L. styliger), and pygophore subrectangular (oval in L. rufospilotus and L. substyliger).
Through the examination of the specimens in the collection of UFRG we expand the distribution of L. lobuliger to two states in Brazil (Pará and Paraíba) and one new locality in the state of Bahia, Brazil.Rolston, 1989 Figures 1I, 2, 4D; Tables 1, 2 Body dark brown, measuring between 9.60-11.30mm, with one yellow spot on base of pronotum, one on base of scutellum, and 1 + 1 on apex of each radial vein.Mandibular plates little longer than clypeus, not convergent.Pronotal lobes digitiform, rounded at apex, anterior margins straight, anterolateral directed, surpassing the lateral limit of eyes.Ventral rim of pygophore V-shaped, with setae along the margin, medially carinated (Fig. 4D).Apex of parameres visible from posterior view.Segment X subrectangular, moderately expanded, but not surpassing the postero-lateral angles (Rolston 1989, figs. 12-14).Rolston (1989) compared L. malevolus to L. spurcus Rolston by the similar coloration and general morphology, indicating the male genitalia as the best character to differentiate them.The ventral rim of pygophore is more straight in L. malevolus than L. spurcus, and the segment X is more expanded in L. spurcus than L. malevolus.

Lincus malevolus
Through the examination of the specimens in the collection of UFRG we expand the distribution of L.lobuliger to a new record for Colombia.Breddin, 1904 Figures 1J, 2, 3E; Tables 1, 2 Body dark brown, measuring between 12.60-12.80mm, yellow stained on humeral angles, base of scutellum, apex of each radial vein, and on middle of each connexival segment.Mandibular plates little longer than clypeus, not convergent.Pronotal lobes expanded, hatchet-lobed, surpassing the lateral limit of eyes about 1/2 width of each eye (Rolston 1983, fig. 25).Ventral rim of pygophore V-shaped, with setae on the apical third, medially carinated.Segment X tubular, not expanded (Fig. 3E) (Rolston 1983, figs. 26-29).

Lincus singularis
Lincus singularis is included in Rolston's (1983) key and is identified on the twelfth step.The female genital plates are quite distinct from the other Lincus species, showing gonocoxites 8 with produced lateral margins, while in other species of Lincus the lateral margins of gonocoxites 8 are straight.The pygophore is also peculiar, with posterolateral angles rounded and dorsally depressed, distinctly projected beyond the ventral rim.

Lincus spathuliger
Lincus spathuliger was compared to L. vandoesburgi Rolston by Rolston (1983) because it has expanded pronotal lobes and short second antennomeres.The difference between the two species is the absence of a subapical projection on the anterolateral pronotal margins in L. spathuliger, present in L. vandoesburgi.

Lincus tumidifrons
Lincus tumidifrons is included in Rolston's (1983) key.The species is placed in the "swollen head" convenience group (Rolston 1983) along with L. parvulus and L. singularis.The species can be distinguished by pronotal lobes subtriangular in L. tumidifrons while rounded in L. parvulus and L. singularis.The female and male genitalia are also distinctive in L. tumidifrons in comparison with L. parvulus and L. singularis.
Distribution data (Table 2) are from Rolston (1983) and Dollet et al. (1993), and from labels of two paratypes from Panama in DARC.This is the first compilation of the geographic distribution of the Lincus species recorded on palm and coconut trees, since the first reports associating the genus with the transmission of Phytomonas were published in the 1980s (e.g., Desmier de Chenon 1984;Couturier & Khan 1989).The previous list accounting for 11 species of Lincus collected on palm and coconut trees (Howard 2001) is updated to the 15 species identified here.The geographical ranges of five species are expanded with new countries recorded for L. malevolus and L. styliger, representing a linear range expansion of 1,200 and 1,500 km respectively.Also, detailed geographic information has been retrieved for L. lobuliger (new records in Pará and Paraíba, Brazil) and L. securiger since these species were previously referred only generically to their presence in the respective countries of occurrence.Both L. lobuliger and L. securiger have the largest distribution ranges among the species studied, occurring in the Brazilian Amazon and Atlantic Forest regions.

Figure 2 .
Figure 2. Geographic records of the species of Lincus associated with palms and coconut trees in the Neotropical Region.