Gerromorpha (Hemiptera: Heteroptera) from the Metropolitan Region of Santarém, Brazil, including three new species of Microvelia Westwood, 1834 (Veliidae: Microveliinae)

Abstract Background Gerromorpha (Hemiptera: Heteroptera) comprises more than 2100 species of semiaquatic bugs, most of which have the ability to walk on the surface of the water. So far, 238 species have been recorded from Brazil, but several portions of the country remain poorly explored. The Metropolitan Region of Santarém (MRS), Pará State, Brazil, lacks faunistic and taxonomic studies concerning this group and the local fauna is under threat due to human actions. New information Aiming to fill gaps concerning the diversity and distribution of Gerromorpha in the Amazon, a survey of the semi-aquatic bugs from the MRS is presented. Collections were made in 33 aquatic ecosystems in the different phytophysiognomies within this area from July 2019 to October 2020. As a result, a checklist with 44 species recorded from the three municipalities of the MRS is presented. Furthermore, three new species of the genus Microvelia Westwood, 1834 (M.belterrensis sp. nov., M.hamadae sp. nov. and M.sousorum sp. nov.) are described, two species are recorded for the first time from Brazil (Microveliaaschnakiranae Makhan, 2014 and Rhagoveliagraziae Galindo-Malagón, Morales & Moreira, 2021), two from Pará State (Microvelialongipes Uhler, 1894 and Paraveliadilatata Polhemus & Polhemus, 1984) and 15 from the MRS (Brachymetralata Shaw, 1933, B.shawi Hungerford & Matsuda, 1957, Tachygerrisadamsoni (Drake, 1942), Microveliapulchella Westwood, 1834, Rhagoveliabrunae Magalhães & Moreira, 2016, R.evidis Bacon, 1948, R.jubata Bacon, 1948, Calliveliaconata (Hungerford, 1929), Oioveliacunucunumana Drake & Maldonado-Capriles, 1952, Paraveliabullialata Polhemus & Polhemus, 1984, Striduliveliaalia (Drake, 1957), S.stridulata (Hungerford, 1929), S.strigosa (Hungerford, 1929), S.tersa (Drake & Harris, 1941) and S.transversa (Hungerford, 1929)).


Introduction
Gerromorpha (Hemiptera: Heteroptera) is an infra-order of predatory, semi-aquatic bugs, most of which live on the surface of the water or amongst floating plants (Nieser and Melo 1997). Contrary to the Nepomorpha, or truly aquatic bugs, their antennae are long and plainly visible dorsally, inserted in front of the eyes. The body is 1.0 to 36.0 mm long and usually velvety, covered with a double layer of micro-and macrotrichia (Andersen 1982). The legs are usually narrow, with apical or pre-apical pretarsal claws (Ribeiro et al. 2019).

Notes
First records from the study area.

Notes
First records from the study area.

Notes
Described from Santarém (Drake and Harris 1934); first record from Belterra.

Notes
Previously recorded from Santarém (Drake and Harris 1930), but absent from our samples.

Notes
First record from the study area.

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Previously recorded from Santarém (Hungerford 1954), but absent from our samples.

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Previously recorded from Santarém (Moreira et al. 2008), but absent from our samples.

Notes
First record from Brazil.
Head covered with very short setae, longer on clypeus. Antenna covered with short setae. Antennomere I widest, slightly curved laterally, thickened towards apex; II wider than III-IV, thickened towards apex; III cylindrical, thinner than IV; IV fusiform, at middle subequal to II in thickness. Labium reaching base of mesosternum.
Thoracic terga densely covered with moderately long, light setae; sides of thorax, prosternum and acetabula with denser, longer setae; meso-and metasterna with short setae. Pronotum with lateral margins bowed; posterior margin sinuous, concave centrally, exposing two rounded lobes of the mesonotum laterally (Fig. 10C). Metanotum exposed as a short central stripe, with posterior margin widely concave. Legs covered with short setae, with some longer setae on dorsal surfaces of femora and tibiae. Femora without spines. Fore tibia straight, enlarged towards apex, with an obtuse, short spine at apex. Hind femur slightly thicker than middle femur. Hind tibia straight.
Abdominal mediotergites covered with moderately long setae. Mediotergites III-VI depressed; VI-VII with shiny median stripe; VII with posterior margin slightly concave.
Abdominal laterotergites elevated to about 90°. Abdominal sterna covered with short setae, posterior margins concave, without tubercles. Abdominal segment VIII slightly exposed, dorsally more than four times wider than long; dorsum with lateral margins convergent and posterior margin slightly concave ( Colouration and structure similar to apterous male, but larger and more robust (Fig.  12). Fore tibia straight, enlarged towards apex, without apical spine. Abdomen larger than in in males, as wide as pronotum (Fig. 12A). Abdominal segment VIII yellowishbrown dorsally and ventrally. Posterior margin of abdominal mediotergite VIII straight.
Abdominal laterotergites elevated to about 45º.

Diagnosis
This new species can be distinguished from other South American Microvelia Westwood, 1834 by the pronotum of the apterous form covering the mesonotum centrally, but exposing it laterally; the metanotum exposed centrally, with the posterior margin widely concave; the abdominal segment VIII of the males slightly exposed dorsally, more than four times wider than long, with the lateral margins convergent and the posterior margin slightly concave, ventrally deeply inserted into the pregenital abdomen, strongly sclerotised, with an evident central notch and three tufts of long setae on each side (only one tuft is visible before dissection); and the male proctiger    fig. 89) and M. hinei Drake, 1920 (Fig. 13d, e, f) are small species that share with M. belterrensis sp. nov. the general appearance and the male terminalia strongly inserted into the pregenital abdomen, although more deeply than in the new species and more weakly sclerotised. In contrast, M. venustatis displays a thicker antennomere IV and the abdominal sterna of the male bear tufts of setae medially (at least on segments V-VII; Fig. 13b Head black. Antenna dark-brown, proximal half of antennomere I yellowish-brown. Eye reddish-brown. Labium yellowish-brown, except for distal article dark-brown. Pronotum dark-brown with a medially interrupted yellowish-brown transverse band on anterior half (Fig. 14A). Metanotum black. Prosternum yellowish-brown, median groove dark. Meso-and metasterna black. Acetabula brown. Coxae, trochanters and proximal half and ventre of femora pale yellow; remainder of legs brown. Abdominal mediotergites black with whitish pruinosity; I with two darker longitudinal spots sublaterally; II-III darker at middle; IV-V dark with whitish pruinosity at median stripe and posterior third; VI-VII darker at one/two narrow median stripe(s). Abdominal laterotergites yellowishbrown, darker at anterior third and mesal and lateral margins. Abdominal sterna black (Fig. 14B). Terminalia yellowish-brown.
Head covered with short setae, longer on clypeus. Antenna reaching apex of metanotum; covered with short setae, longer and denser on article IV. Antennomere I widest, slightly curved laterally, thickened towards apex; II wider than III-IV, thickened towards apex; III cylindrical, thinner than IV; IV fusiform. Labium reaching middle of mesosternum.
Thoracic terga densely covered with very short setae; sides of thorax, prosternum and acetabula with longer setae. Pronotum long, covering mesonotum and most of metanotum; metanotum visible only as a very short central stripe (Fig. 14C). Circular punctures on a centrally interrupted transverse row adjacent to anterior margin of pronotum; another transverse row posterior to yellowish band; several sparse punctures posteriorly to latter row. Legs covered with short setae, with some longer setae on dorsal surfaces of femora and tibiae. Femora without spines. Fore tibia straight, enlarged towards apex, with an obtuse, short spine at apex. Hind femur thicker than middle femur. Hind tibia straight.
Abdomen covered with short setae. Posterior margin of abdominal mediotergite I with a slight concavity at middle; VII with a pronounced concavity (Fig. 14D). Abdominal laterotergites elevated to about 45º. Abdominal sterna II-IV moderately short, V-VI longer, VII twice as long as II; posterior margins concave, without tubercles, with many long setae (Fig. 14E). Abdominal segment VIII deeply inserted into pregenital abdomen; partially visible dorsally due to the concavity of mediotergite VII; faintly visible ventrally (Fig. 14D, E); posterior margin dorsally concave, ventrally with a weak median notch (Fig. 15A-D). Proctiger without lateral projections (Fig. 15E); parameres symmetrical ( Fig. 15G); shape as in Fig. 15F. Colouration and structure similar to apterous male ( Fig. 16A-C). Pronotum long, subpentagonal, completely covering meso-and metanota; posterior margin rounded. Fore wings dark brown, with a proximal pair of elongated whitish maculae, a distal pair of rounded whitish maculae and a median whitish macula close to apex; lateral margins with rows of white setae. Colouration and structure similar to apterous male, but larger and more robust (Fig. 16  D-F). Fore tibia straight, enlarged towards apex, without apical spine. Posterior margins of abdominal mediotergite VII and sternum VII straight. Posterior margin of abdominal tergum VIII rounded, with long setae. Abdominal laterotergites elevated to about 90º, slightly bowed on sides of mediotergites II-V, convergent and slightly reflected on sides of VI-VIII (Fig. 16D). Possibly fecundated females display expanded abdomen with differently shaped laterotergites (Fig. 16F).

Diagnosis
This new species can be distinguished from other South American Microvelia by the pronotum of apterous specimens long, covering the mesonotum and most of the metanotum; the metanotum visible only as a very short central stripe; the posterior margin of the male abdominal mediotergite VII with a pronounced concavity; the male abdominal segment VIII deeply inserted into the pregenital abdomen, with the posterior margin dorsally concave and ventrally with a weak median notch; the shape of the female abdomen, with abdominal laterotergites elevated to about 90º, slightly bowed on the sides of mediotergites II-V, convergent and slightly reflected on the sides of VI-VIII; and by the pattern of whitish maculae on the fore wings of macropterous specimens: a proximal pair of elongated maculae, a distal pair of rounded maculae and a median macula close to apex.

Notes
First records from the study area. Fig. 17d, e, f Head dorsally yellowish-brown, lighter on sides and anterior third, dark-brown on insertion of trichobothria; ventrally pale-yellow. Antenna dark-brown, except antennomere I yellowish-brown. Eye reddish. Labium yellowish-brown, except apex of article III and entire IV dark-brown. Pronotum yellowish-brown, lighter on transverse band on anterior third and at middle of posterior two-thirds, dark-brown around punctures adjacent to anterior margin and between anterior and posterior lobes (Fig.  18A, C). Metanotum pale-yellow, darker centrally. Ventre of thorax pale-yellow, anterior margins of meso-and metasterna dark-brown. Acetabula, coxae, trochanters and ventre of femora pale-yellow; dorsum of femora pale-yellow basally, dark-yellow towards apex; fore tibia yellowish-brown, dark-brown on apical third; middle and hind tibiae brown, lighter ventrally on proximal half; tarsi brown. Abdominal mediotergite I yellowish-brown, pale yellow on sides; II dark-brown, yellowish-brown on sides and anterior margin; III yellowish-brown, anterior margin dark brown, small pale-yellow patch at middle; IV yellowish-brown; V and VII yellowish-brown, each with longitudinal light-yellow band at middle; VI light-yellow. Abdominal laterotergite II pale-yellow, III-VI yellowish-brown on anterior half, pale-yellow on posterior half; VII yellowish-brown. Sides of abdomen yellow, dark-brown around opening of scent glands and on anterior margins of segments II-III. Ventre of abdomen yellow, dark-brown on sides of segments I-II (Fig. 18B). Terminalia yellowish-brown.

Photographs
Head with silvery pubescence adjacent to mesal margins of eyes and on posterior third; impressed median line inconspicuous; clypeus with long setae. Antenna long, reaching abdominal segment I; covered with short brown setae, with longer, lighter setae on antennomere IV. Antennomere I widest, slightly curved laterally, thickened towards apex; II wider than III-IV, thickened towards apex; III cylindrical, thinner than IV; IV fusiform, at middle subequal to II in thickness. Labium reaching middle of mesosternum.
Pronotum completely covering mesonotum, but not metanotum (Fig. 18C); anterolateral angles rounded; anterior third covered with silvery pubescence; circular punctures on a transverse row adjacent to anterior margin; another centrally interrupted transverse row posterior to yellowish band; two submedian punctures posteriorly displaced from latter row; posterior margin slightly concave at middle. Metanotum almost 1/3 as long as pronotum, unpunctured; posterior margin rounded. Propleuron with dense, short, light setae, many small punctures and a posterior row of larger punctures; meso-and metapleuron unpunctured, without depressions. Ventre of thorax without elaborated ornamentation, except two dark punctures on both pro-and mesosternum near coxae. Legs covered with short brown setae, with some longer setae on dorsal surfaces of femora and tibiae. Fore tibia straight, slightly thicker on apex than on base, without apical spine. Hind femur slightly thicker than middle femur, ventrally with a row of distally increasing spines on proximal two-thirds (Fig. 18E). Hind tibia straight.
Microvelia sousorum sp. nov. is most similar to M. novana (Fig. 21), known only from the type specimens from Santa Catarina State, southern Brazil. They can be separated by the shapes of the posterior margins of the pronotum (slightly concave at the middle in M. sousorum sp. nov. vs. rounded in M. novana), male abdominal mediotergite VII (slightly concave at the middle vs. straight) and male abdominal sternum VIII (straight vs. concave) and by the presence of spines on the hind femur of males in the new species, which are absent in M. novana.

Etymology
This species is named in honour of Carlos Sousa and Diego Sousa, colleagues who were both instrumental in our fieldwork. In addition, Carlos is SES' husband and gave all the necessary support for her to obtain her Master's degree, which resulted in this paper.

Notes
Previously recorded from Santarém (Moreira et al. 2011a), but absent from our samples.

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Previously recorded from Santarém (Polhemus 1997), but absent from our samples.

Notes
First records from the study area.

Notes
First records from the study area.

Notes
Previously recorded from Santarém (Bacon 1948; as R. perfidiosa); first records from Belterra and Mojuí dos Campos.

Notes
First record from the study area.

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Previously recorded from Santarém (Rodrigues et al. 2014a), but absent from our samples.

Notes
First record from the study area.

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First record from Pará State.

Notes
First records from the study area.

Notes
First record from the study area.

Notes
First records from the study area.

Notes
First records from the study area.

Discussion
Our survey of the semi-aquatic bugs from the MRS revealed the occurrence of 14 genera and 44 species belonging to the families Gerridae, Hydrometridae, Mesoveliidae and Veliidae in the study region (Table 2). This represents a 100% increase in relation to the specific diversity previously recorded from the area in literature (Champion 1898, Hungerford 1929b, Drake and Harris 1930, Kuitert 1942, Bacon 1948, Hungerford 1954, Neering 1954, Bacon 1956, Nieser 1970, Polhemus 1997, Moreira et al. 2008, Moreira et al. 2011a, Rodrigues et al. 2014a). Amongst the recorded species, Microvelia belterrensis sp. nov., M. hamadae sp. nov. and M. sousorum sp. nov. are described as new and, together with M. aschnakiranae, newly recorded from Brazil, increase the number of species of the genus known to occur in the country from 29 to 33 (Moreira 2021e). This contributes to fill a gap of knowledge about the genus in South America, where many species of Microveliinae remain undescribed (Polhemus and Polhemus 2007). Additionally, the recently-described Rhagovelia graziae is recorded from Brazil for the first time, increasing the distribution range of the species by more than 2000 km eastwards, from the Colombian Llanos to the Brazilian Amazon (Galindo-Malagón et al. 2021). Finally, M. longipes and Paravelia dilatata are recorded for the first time from Pará State. The former is quite common in temporary water bodies in South America and the new records fill a gap in its distribution between Roraima and Amazonas States and north-eastern Brazil ( Polhemus 1990, Moreira and Campos 2012, Rodrigues et al. 2012, Cordeiro and Moreira 2015, Rodrigues et al. 2021). The latter is a much rarer species, known from less than 10 localities in Guyana, Suriname and Brazil (Amazonas State) (Polhemus 2014, Polhemus and Polhemus 1984, Pereira and Melo 2007, Rodrigues et al. 2014b, Rodrigues and Moreira 2016. Our record extends the known distribution of the species by about 600 km to the east of the previous records in its southern edge, in Manaus, Amazonas State, Brazil (Polhemus and Polhemus 1984, Polhemus 2014, Rodrigues et al. 2014b, Rodrigues and Moreira 2016.  Table 2. Distribution of semi-aquatic bug species in the three Municipalities of the MRS, Pará, Brazil and references for the records. A single asterisk (*) indicates a new record from Pará State. Two asterisks (**) indicate a new record from Brazil.