Entomobrya paroara Arlé & Guimarães, 1978

Viana, Stéphanie Dos Santos, Morais, José Wellington De & Cipola, Nikolas Gioia, 2024, Taxonomic revision of Entomobrya Rondani, 1861 (Collembola: Entomobryidae: Entomobryinae) from the Brazilian Amazon, Zootaxa 5452 (1), pp. 1-110 : 30-39

Entomobrya paroara Arlé & Guimarães, 1978

Figs 21–28 , Table 2

Entomobrya paroara Arlé & Guimarães, 1978: 2 , figs 1–23, Brazil, Pará state, Ananindeua municipality (original description).

Typological note. The type material of E. paroara deposited at MNRJ was destroyed in the fire of September 2018, while the paratypes deposited at MPEG were lost (Orlando T. Silveira, personal communication). The neotype is herein designated from specimens collected in type locality ( Fig. 28 ) (ICZN 2000, chapter 16, article 75.3.4 and 75.3.6. and article 76). The specimens fit all morphological characteristics presented in the original description ( Arlé & Guimarães 1978).

Examined type material. Neotype female designed on slide ( INPA-CLL 0000272 ): Brazil, Pará state, Ananindeua municipality, “Águas Brancas” neighborhood, “II de Junho” street, forest “II de Junho” street, 01°23’35”S, 48°22’25”W ( Fig. 28 ), 25 m, 13–15.viii.2021, pitfall-trap, SS Viana coll.

Other examined material. One male on slide ( INPA): Brazil, Pará state, Belém municipality, forest of the Museu Paraense Emílio Goeldi , 01°27’07”S, 48°26’38”W, 39 m, 9–13.i.2014, pitfall-trap, RS Sovano coll. Three females on slides and 7 specimens in alcohol ( INPA): Santarém municipality, “Alter do Chão” district, “Norato” island, 02°30’S, 54°57’W, 2 m, 27.iv.2002, pitfall-trap, D Rodrigues coll. Two females on slides and 6 specimens in alcohol ( INPA): Capitão Poço municipality, Ecological reserve of “São Geraldo Magela”, 01°47’57.47”S, 47°05’32.94”W, 73 m, 07–27.ix.2019, malaise-trap, Fj Sosa coll. One specimen in alcohol ( INPA): idem, except 14–21.vii.2019 . One juvenile on slide and 2 specimens in alcohol ( INPA): Acre state, Manoel Urbano municipality, State Park of “Chandless”, 09°23’52”S, 69°54’58”W, 215 m, 05–13.x.2016, pitfall-trap, IPS Santos coll. One female on slide and 1 specimen in alcohol ( INPA): idem, except, 09°23’26”S, 69°55’15”W, 208 m . One female on slide ( INPA): idem, except, 09°24’21”S, 69°53’52”W, 234 m . One male on slide ( INPA): Bujari municipality, “Antimary” State Forest , near to river, 09°20’02.3”S, 68°19’21.6”W, 216 m, 22–26.ix.2020, manual collect, N Hamada, JMC Nacimento & JO Silva coll. One female on slide and 1 specimen in alcohol ( INPA): Amazonas state, Ataláia do Norte municipality, Natural reserve of “Palmari”, 04°17’21”S, 70°16’36.8”W, 90 m, 09.iv.2014, sweep, JT Câmara, FF Xavier F & A Plant coll. One female on slides ( INPA): Barcelos municipality, National park of “Jaú”, “Papagáio” river, 02°00’03”S, 62°43’54”W, 46 m, 16–19.vi.2001, pensilvânia-trap, A Henriques, J Vidal & A Filho coll. One female and 1 male on slides and 3 specimens in alcohol ( INPA): Careiro Castanho municipality, Biodiversity Research Program ( PPBIO), 03°40’42”S, 60°19’41”W, 45 m, 11–13.xii.2013, malaise-trap, JA Rafael, JT Câmera & FF Xavier coll. Two males on slides and 10 specimens in alcohol ( INPA): Maués municipality, “ Santa Helena ” farm, forest near to “Morais” street, 03°27’13”S, 57°39’01”W, 27 m, 25–28.iv.2017, malaise-trap, A Somavilla coll. Twenty-two specimens in alcohol ( INPA): idem, except 28.iv–09.v.2017 . One female on slide ( INPA): Novo Airão municipality, National park of “Anavilhanas”, left margin of “Negro” river, 02°37’09”S, 60°56’58”W, 27 m, 27.xi–06.xii.2021, malaise-trap, RA Azevedo, RNM de Morais-Junior & IO Fernandes coll. One female on slide ( INPA): Presidente Figueredo municipality, “AM-270” road margin, km 18, 02°02’48”S, 59°52’01”W, 143 m, 30.viii.2014, plate-trap, NG Cipola & FGL Oliveira coll. Two specimens in alcohol ( INPA): Rio Preto da Eva municipality, “Flor do Campo” farm, “AM-010” road margin, km 57, 02°43’33.1”S, 59°51’05.7”W, 117 m, 19–21.vi.2023, pitfall-trap, BM Medeiros & SS Viana coll. Two specimens in alcohol ( INPA): Tefé municipality, “Emade” road, km 08, 03°26’53.8”S, 64°40’57.9”W, 76 m, 12–15.i.2013, pitfall-trap, AM Pereira Jr. coll. Two females on slides and 2 specimens in alcohol ( INPA): Manaus municipality, “Embrapa Amazônia Ocidental”, in cultivation of organic Guaraná , 02°53’29.14”S, 59°58’45.80”W, 97 m, 28.ix.2012, Möerick-trap, K Schoeninger coll. One specimen in alcohol ( INPA): idem, except 23.ix.2012 . One female on slide and 1 specimen in alcohol ( INPA): idem, except cultivation of conventional Guaraná , 02°53’42.18”S, 59°59’10.58”W , 98 m. One specimen in alcohol ( INPA): idem, except 26.x.2012 . Three females on slides and 3 specimens in alcohol ( INPA): forest of the Nacional Research Institute of the Amazon , “Bosque da Ciência”, 03°05’54”S, 59°59’09”W, 92 m, 21.v.2012, yellow plate-trap, P Bartholomay coll. One specimen in alcohol ( INPA): idem, except 03°05’56”S, 59°59’04”W, 54 m, 12.v.2014, suspended-trap, R Klepper coll. One female on slide and 1 specimen in alcohol ( INPA): idem, except Department of Entomology , 03°05’42”S, 59°59’23”W, 97 m, 22.iv.2012, AMO Pes coll. One male and 6 females on slides and 14 specimens in alcohol ( INPA): idem, except 03°05’49”S, 59°59’19”W, 95 m, 01–03.vi.2013, malaise-trap, GC Tavares coll. One female on slide ( INPA): idem, except 03°05’45”S, 59°59’21”W, 02.xii.2013, entomological aspirator, DDR Fernandes coll. Two females on slides and 18 specimens in alcohol ( INPA): idem, except 03°05’48”S, 59°59’23”W, 79 m, 31-vii–13.ix.2021, malaise-trap, E Viegas & M Soares coll. Ten specimens in alcohol each institution ( CC / UFRN, MNRJ, MZUSP): idem, except 12–15.viii.2022, pitfall-trap, NG Cipola & SS Viana coll. One female on slide ( INPA): Reserva Ducke, L 3-4500 grid, 02°56’21”S, 59°55’35”W, 101 m, 25–27.iii.2013, yellow plate-trap, NG Cipola & MB Graça coll. One female on slide and 1 specimen in alcohol ( INPA): idem, except headquarters, 02°55’S, 59°58’W, 83 m, 01–15.x.2014, malaise-trap, AM Silva-Neto coll. One specimen in alcohol ( INPA): idem, except 02°55’48”S, 59°58’30”W, 73 m, 17–18.x.2019, white plate-trap, TM Almeida coll. Two females on slides and 2 specimens in alcohol ( INPA): tower of Reserve “ZF-02”, road BR-374, km 14, 02°35’20.7”S, 60°06’55.3”W, 122 m, 01–05.xii.2013, malaise-trap, JA Rafael, JT Câmera & FF Xavier coll. One female on slide ( INPA): Maranhão state, São Luís municipality, “Maracanã” neighborhood, “Mangalho” farm, Ombrophilous forest of solid ground, 02°36’11”S, 44°17’50”W, 11 m, 08–09.i.2014, pitfall-trap, VJC Bastos & AC Nascimento-Pereira coll. One female on slide ( INPA): Roraima state, Amajari municipality, mountain of “Tepequém”, 03°46’33”N, 61°43’35”W, 32 m, 15–31.vii.2015, malaise-trap, PCS Barroso & Boldrini coll. One specimen in alcohol ( INPA): idem, except 03°45’20.7”N, 61°42’52.8”W, 678 m, 03–08.xi.2021, R Ale-Rocha, M Soares, L Barros & S Nascimento coll.

Diagnosis. Head laterally with a longitudinal stripe, Th II–Abd III with two longitudinal stripes which usually unite into another irregular spot on Abd IV, femur distally and tibiotarsus III always with 1 and 2 spots, respectively ( Figs 21–22 ); Ant IV without the apical bulb; pl1–2 smooth, normal or bifurcated ( Fig. 23C ); head macrochaetotaxy with 7–9 ‘ An ’, 3 ‘ A ’, 3–4 ‘ M ’, 6–9 ‘ S ’, 0–1 ‘ Ps ’, 4 ‘ Pa ’, 1–2 ‘ Pi ’, 2 ‘ Pm ’, 0–1 ‘ Pmp ’, 5 ‘ Pp ’, 1 ‘ Ppe ’ and 3–4 ‘ Pe ’ mac, respectively ( Fig. 23D ); labral inner papillae with 3–4 projections, outer with 2 projections ( Fig. 24A ); labial papilla E l.p. conical and almost reaching the base of a.a. ( Fig. 24B ); sublobal plate with 3 inner appendages; Th II internally with 9–10 anterior, 5–12 median and 15–22 posterior mac; Th III–Abd I with 19–24 and 8–12(13) mac, respectively; Abd II–III with 3–5 and 0 inner mac, respectively; Abd IV with 18–26 inner and 15–21 outer mac ( Fig. 25 ); unguiculus III ai lamella acuminate and pe serrated ( Fig. 26E ); collophore anteriorly generally with 4 distal mac ( Fig. 27A ); dens distally with only regular chaetae; mucro proximal tooth larger than the distal one, basal spine surpassing the apex of the proximal tooth ( Fig. 27D ).

Redescription. Total length (head + trunk) of specimens 1.97–2.13 mm (n=4), neotype 2.13 mm. Specimens pale yellowish or whitish, with or without bluish or blackish pigments weakly distributed over the distal half of Ant IV–III, Ant II–I variably pigmented; head dorsally with 2 irregular spots strongly or weakly pigmented; speckled or uniform pigments on head laterally, forming a longitudinal stripe up to the Abd III, plus other two longitudinal stripes from the Th III to the Abd III, with both stripes united irregularly on Abd IV laterally, in an irregular spot; Abd IV posteriorly, Abd V–VI, coxa I–III and collophore irregularly pigmented; femur I–III eventually with a longitudinal stripe, but always with 1 distal spot; tibiotarsus I–III with 1 proximal and 1 distal spot; eyepatches black ( Figs 21–22 ).

Head. Antenna shorter or subequal to the trunk length ( Figs 21E–H , 22G–L ), ratio antennae: trunk = 0.94–0.71: 1 (n=4), neotype 0.74: 1; antennal ratio as I: II: III: IV = 1: 1.39–1.49: 1.32–1.44: 1.90–2.11 (n=4), neotype 1: 1.46: 1.35: 2.11. Ant IV weakly annulated on its distal 3/4 and devoid of apical bulb, with 3 apical finger-shaped sens, and numerous sens of different sizes. Ant III organ with 2 finger-shaped sens, 3 guard sens, 2 elongated sens and at least 4 sens of different sizes ( Fig. 23A ). Ant II dorsally with about 18 elongated sens and 4–5 dorsal mac, without ventral mac ( Fig. 23B ). Ant I dorsally with 6 elongated sens, 7–8 mac and 3–4 smooth mic at the base ( Fig. 23B ). Eyes A and B larger, G and H slightly smaller than the others, and with 5–6 interocular mes (q, v, s, p, r, t); head dorsal chaetotaxy ( Fig. 23D ) with 7–9 ‘ An ’, 3 ‘ A ’, 3–4 ‘ M ’, 6–9 ‘ S ’, 0–1 ‘ Ps ’, 4 ‘ Pa ’, 1–2 ‘ Pi ’, 2 ‘ Pm ’, 0–1 ‘ Pmp ’, 5 ‘ Pp ’, 1 ‘ Ppe ’ and 3–4 ‘ Pe ’ mac, respectively. Clypeal formula with 4 (l1–2), 15–21 (f, 1 unpaired), 3–5 (pf0–2) ciliate chaetae, l1–2 longer, ciliate and apically acuminate, 4 f and pf0–1 subtly larger, 2 f and pf2 smaller than the others, others subequal ( Fig. 23C ). Prelabral chaetae smooth, pl1–2 normal or bifurcated, equally or unequally ( Fig. 23C ). Labral inner papillae with 3–4 projections, outer papillae with 2 projections smaller than the inner papillae ( Fig. 24A ). Labial papilla E l.p. conical and almost reaching the base of a.a. ( Fig. 24B ). Maxillary palp b.c. 1.32 longer than t.a.; sublobal plate with 3 inner appendages (sb1–3). Basolateral and basomedian labial fields with M1–2, R, E, L1–2 ciliate, M2 subtly smaller than the others, present or absent ( Fig. 24C ). Cephalic groove with 9 ciliate chaetae of different sizes; postlabial formula with 4 (G1–4), 4 (X2–4), 4 (H1–4) chaetae plus 1 chaeta between the series ( Fig. 24D ).

Thorax chaetotaxy ( Fig. 25A ). Th II a, m and p series (excluding the anterior collar) with 9–10, 5–12 and 15–22 mac (1 mac or mes rarely present), respectively. Th III a, m and p series with 6–7 (1 mac rarely absent), 4–5 and 9–12 (1 mac rarely absent) mac, respectively. Ratio Th II: III = 1.65–36: 1 (n=4), neotype 1.36: 1.

Abdomen chaetotaxy ( Figs 25B–C ). Abd I a, m and p series with 0–3 (2 mac rarely absent), 4–9 (1 mac rarely absent) and 1 mac, respectively. Abd II a, m and p series with 0–2, 5 and 1–2 mac. Abd III a, m and p series with 1, 1–3 and 1 mac, respectively, plus 2 extra mac or mes laterally. Abd IV with 18–26 (1 unpaired and 1 extra mac) inner mac of A–C series and 15–21 outer mac of T–Fe series (1–3 extra mac); 11 sens (ps type I and others type II) and 21 posterior mes. Abd V a, m and p series with 4, 3, and 5 mac, respectively. Ratio Abd III: IV = 1: 4.06–8.13 (n=4), neotype 1: 5.51.

Legs ( Figs 26A–E ). Subcoxa I with 3 chaetae and 2 psp; subcoxa II with an anterior row of 8 chaetae and about 9 anterior chaetae; posterior row of 5 chaetae, 2 anterior chaetae and 2 psp; subcoxa III with one row of 11 chaetae, about 16 anterior chaetae and 2 psp ( Figs 26A–C ). Trochanteral organ with 37 spine-like chaetae, 4 anterior, 7 posterior, 19 internal, 1 apical and 6 on the distal arm ( Fig. 26D ). Tibiotarsus I–III with 9–12 inner finely ciliate mac. Unguis b.t. on proximal 2/4, m.t. on distal 1/3 and smaller than b.t., a.t. minute and on distal 1/8. Unguiculus I–III lamellae (ae, ai, pe, pi) smooth and acuminate, except pe serrated and with a small proximal tooth; ratio unguis: unguiculus = 1: 0.55. Tibiotarsus III smooth chaeta 1.17 longer than the unguiculus; tenent hair 0.91 shorter than the unguis ( Fig. 26E ).

Collophore ( Fig. 27A ). Anterior side with about 28–29 ciliate chaetae, 3–4 distal mac (1 rarely absent), and about 25 chaetae of different sizes widely distributed on the corpus; posterior side with about 48 ciliate chaetae of different sizes widely distributed on the corpus (8 unpaired), and distally with 1 smooth chaeta; lateral flap with 16–21 chaetae, 6–8 smooth and 9–14 ciliate.

Furcula ( Figs 27B–D ). Manubrium ventrally with 2 subapical and about 35 distal ciliate chaetae of different sizes. Manubrial plate dorsally with 6–9 chaetae of different sizes and 3 psp. Dens dental lobe with 2 (bs1 and bs2) thicker ciliate chaetae, bs1 subequal to bs2. Dens tightly crenulate on its distal 1/4 distally only with regular chaetae. Mucro proximal tooth larger than the distal one, mucronal spine surpassing the proximal tooth apex.

Variations. Specimens of E. paroara from different localities mostly show similar variations, principally on the body color pattern and polymorphisms (mac or mes, mac present or absent) in the dorsal chaetotaxy of the head and Th II – Abd IV ( Figs 21–22 , 23D , 25A–C ). However, some variations are uncommon in some populations, like in 3 females from Santarém municipality, “Alter do Chão” district, “Norato” island, 02°30’S, 54°57’W ( INPA), which have Th II p4 mac on both sides (generally absent on some side) and Th III a2 and p2 mac absent only in these specimens ( Fig. 25A ). A specimen from Maués municipality lacks Abd I a3 and a5 mac, as well as 1–2 extra outer mac on Abd IV anteriorly ( Figs 25B–C ). Other rare variations were also observed in a specimen from Manaus municipality, with the collophore anteriorly with 3 distal mac (usually 4) and Abd I m4e and a5 mac absent (usually present) ( Figs 27A , 25B ) .

Distribution. Entomobrya paroara was originally known from seven municipalities of Pará state ( Arlé & Guimarães 1978), but its distribution is herein expanded to four other states (Acre, Amazonas, Maranhão and Roraima) from the Brazilian Amazon ( Fig. 28 ).

Remarks. Entomobrya paroara resembles E. tupiana Arlé, 1959 from Rio de Janeiro state by body longitudinal stripes of pigment and unguiculus III ai lamella acuminate ( Figs 21A–D , 22A–F , 26E ). However, E. paroara differs from E. tupiana by mucronal spine surpassing the apex of the proximal tooth (not reaching in E. tupiana ) ( Fig. 27D ) and Th II–Abd IV with two paired longitudinal stripes ( Figs 21–22 ), while E. tupiana has medially an unpaired extra stripe (see Arlé 1959: 27 figs 10–13).

E. paroara also resembles Entomobrya murreensis Yosii & Ashraf, 1965 from Pakistan due to body with longitudinal stripes of pigment, inner tibiotarsus III with finely ciliate mac, and unguiculus ai lamella acuminate (see Yosii & Ashraf 1965: 155). However, E. paroara differs from this species by labral inner papillae with 3–4 projections (1 in E. murreensis ) ( Fig. 24A ).

The dorsal chaetotaxy of E. tupiana and E. murreensis is unknown, but it is possible to differentiate E. paroara from these species based on the characteristics mentioned above, including others such as Ant. IV apical bulb absent (apically unilobed in E. tupiana and bilobed in E. murreensis ), unguiculus III pe lamella serrated (smooth in E. tupiana and E. murreensis ), and mucro proximal tooth larger than the distal one (subequal in E. tupiana and E. murreensis ) ( Figs 23C , 26E , 27D ). Differences between the Brazilian species are summarized in Table 1.

Figures

FIGURE 21. Entomobrya paroara habitus of fixed specimens in ethanol: (A–D, dorsal view; E–H, lateral view); A and E, specimens from Santarém municipality, Pará state; B–C and F–H, specimens from Maués municipality, Amazonas state; D and H, specimens from Novo Airão municipality, Amazonas. Scale bars: 1 mm.

FIGURE 22. Entomobrya paroara habitus of fixed specimens in ethanol from Manaus municipality, Amazonas states: A–F, dorsal view; G–L, lateral view. Scale bars: 1 mm.

FIGURE 23. Entomobrya paroara antennae and dorsal head: A, Ant III distally (dorsal view); B, chaetotaxy of left Ant II–I (dorsal view) respectively, arrows indicate elongated sens, dorsal apically foot-shaped mac, and smooth mic present or absent in Ant I; C, clypeal and prelabral chaetotaxy, arrow shows pl1–2 chaeta bifurcated or normal; D, head chaetotaxy (left side).

FIGURE 24. Entomobrya paroara ventral head: A, labral papillae; B, labial papillae E (left side); C, proximal chaetae and basomedian and basolateral labial fields, arrow indicates M2 chaeta present or absent; D, cephalic groove and anterior part of the postlabial chaetotaxy.

FIGURE 25. Entomobrya paroara dorsal chaetotaxy (left side): A, Th II–III; B, Abd I–III; C, Abd IV–V.

FIGURE 26. Entomobrya paroara legs: A–C, chaetotaxy of subcoxa I–III respectively (outer side); D, trochanteral organ (posterior view); E, distal tibiotarsus and empodial complex III (posterior view).

FIGURE 27. Entomobrya paroara abdominal appendages: A, collophore chaetotaxy (lateral view), arrow on lateral flap indicates a ciliate or smooth chaeta; B, distal manubrium (ventral view); C, manubrial plate (dorsal view), arrows show the chaetal representation, including chaetae present or absent; D, dens distally and mucro (outer view).

FIGURE 28. Map depicting the distribution of E. paroara in the Brazilian Amazon, the star represents its type locality, yellow circles new records, and red circles additional localities reported in the original description (Arlé & Guimarães, 1978).