An insight into the tribe Hexathrombiini (Actinotrichida: Trombidioidea, Microtrombidiidae, Eutrombidiinae) with new data on host-parasite interaction

Abstract

The status of the genera in the small microtrombidiid mite tribe Hexathrombiini is reevaluated. Type specimens representing all genera were studied and diagnostic characters for Hexathrombiini are reviewed, summarized, and new data and a key to the genera in the tribe are provided: Alhamitrombium, Beronium, Hexathrombium and Hoplothrombium. Hexathrombium is the most speciose genus in the tribe and species recorded from South America are compared, as well as those with a divided pygidial plate. A provisional key to species assigned to Hexathrombium is provided. Finally, Hexathrombium abirami was captured in Peru parasitizing a bright metallic tiger beetle (Tetracha fulgida). A total of 361 larvae were removed parasitizing a single carabid host; this is the highest load of parasites reported in terrestrial Parasitengona mites associated with arthropods. This capture represents a new record of Hexathrombiini mites for Peru. A redescription of He. abirami using all specimens available to date is included.

Keywords:

• Parasitengona
• Alhamitrombium
• Beronium
• Hexathrombium
• morphology

Introduction

The tribe Hexathrombiini Fain & Drugmand, 1993 (see Discussion section for authorship) was erected within Eutrombidiinae Thor, 1935 to accommodate Hexathrombium Cooreman, 1944, Beronium Southcott, 1986 and Hoplothrombium Ewing, 1925. Later, Mayoral & Barranco (2005a) described Alhamitrombium in Hexathrombiini. Fifteen species, variously distributed within the six zoogeographic regions, have been described in the tribe to date. All remain known exclusively from larvae that parasitize carabids (including formerly distinguished Cincindelidae) and staphylinid beetles. There are two exceptions: Hoplothrombium quinquescutatum Ewing, 1925 reported on a single specimen adhering to an Oribatida mite taken from the stomach of a toad (Ewing 1925), and Hexathrombium southcotti Zheng, 1997 captured from ichneumonid wasps (Zheng 1997; Felska et al. 2018). Haitlinger (1999) considered the latter to be probably an accidental host. Most species are known only from few specimens, and they have been recorded from single localities; as an exception, more than 40 specimens of Beronium laemostenis Mayoral & Barranco, 2005 have been collected from 10 different localities (caves) in Spain (Mayoral & Barranco 2005b; Mayoral 2013).

The most speciose genus is Hexathrombium and it contains the species: Hexathrombium cicindelae (Floch & Abonnenc, 1941), Hexathrombium abirami Haitlinger, 1997, and Hexathrombium marittae Haitlinger, 1994 – from the Neotropical region; Hexathrombium lubomirae (Haitlinger, 1994) – from the Afrotropical and Oriental Region; Hexathrombium fageli Fain & Drugmand, 1993 and Hexathrombium spatuliferum Cooreman, 1944 – from the Afrotropical region; Hexathrombium willisi Southcott, 1993 – with Nearctic distribution; Hexathrombium sorayae Haitlinger, 1994 and He. southcotti – with Palaearctic distribution; and Hexathrombium mamerti Haitlinger, 1999 – from the Australian region. Two other findings from South America refer to uncertain identifications of specimens assigned to He. cf. marittae and He. cf. cicindelae (Pérez-Espinoza & Moreno Salas 2016; Almada & Cédola 2017).

The genus Beronium Southcott, 1986 was erected by Southcott (1986) to accommodate Hoplothrombium coiffaiti Beron, 1973. This genus is known from the south-western Palaearctic, and comprises Beronium coiffaiti (Beron, 1973), Beronium veronicae Haitlinger, 1994 and B. laemostenis (Beron 1973; Haitlinger 1994; Mayoral & Barranco 2005b; Mayoral 2013). The monotypic genera Hoplothrombium Ewing, 1925, and Alhamitrombium Mayoral & Barranco, 2005 are known from the Nearctic and Palaearctic regions, respectively (Ewing 1925; Vercammen-Grandjean 1967; Mayoral & Barranco 2005a); they include the species Ho. quinquescutatum and Alhamitrombium tetraseta Mayoral & Barranco, 2005.

Welbourn (1983) listed Ho. quinquescutatum and Ho. coiffaiti under Hoplothrombium, in addition to the species Trombidium cicindelae Floch & Abonnenc, 1941 and He. spatuliferum. The generic affiliation of “coiffaiti”, “cicindelae” and “spatuliferum” was not followed by subsequent authors since those specimens do not comply with the generic diagnosis of the genus and Hoplothrombium has therefore remained monotypic.

Here, we redescribe Hexathrombium abirami from new specimens collected in Peru, parasitizing Tetracha fulgida (Klug, 1834) (Carabidae). The load of parasites reported here for T. fulgida is the highest infestation record of terrestrial Parasitengona mites associated with arthropods. The diagnostic traits for the four genera in Hexathrombiini were reviewed and representatives of the different genera were studied (except Hoplothrombium that we relied on published descriptions). An updated list of relevant characters, a key to the genera in Hexathrombiini and a provisional key to Hexathrombium species are provided.

Material and methods

A specimen of T. fulgida infested by larvae was collected in Peru (dept. Huánuco, Rio Yuyapichis, ACP Panguana, 9º37’S, 74º56ʹW, 230 m.a.s.l.), 01.05–21.05.2015, by S. Friedrich, F. Wachtel and M. Steinherr. The material was preserved in 80% Ethanol.

Larvae were detached from the host with an entomological pin and mounted on microscopic slides in Hoyer’s medium. The overall number of larvae attached to the host was counted and the measurements were taken using NIS-Elements Br software, under a Nikon Eclipse E600 microscope coupled with DS-Fi1 camera system. Photos were taken with a DS-Fi3 camera attached to a Nikon Eclipse 80i microscope and the images were stacked using Helicon Focus software (© Helicon Soft Ltd., 2000). All measurements are given in micrometers. The terminology follows Southcott (1993), Vercammen-Grandjean (1967) and Wohltmann et al. (2007). The material (slide-mounted and alcohol preserved larvae; host specimen) is deposited in the Department of Invertebrate Systematics and Ecology, Wrocław University of Environmental and Life Sciences, Poland (DISE WUELS). Five larvae (slide-mounted) are deposited at the Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Lima, Peru (MUSM).

For the purpose of comparison and re-appraisal of characters used in the diagnosis of Hexathrombiini, the type material of He. abirami, He. lubomirae, He. marittae, He. mamerti, B. veronicae, B. laemostenis and A. tetraseta was studied. The references to other members of the tribe are based on original descriptions.

Results

Hexathrombiini Fain & Drugmand, 1993Hexathrombiini Fain & Drugmand, 1993: 123.Hexathrombiini: Southcott 1993: 943.

Diagnosis

(after Fain & Drugmand 1993; Southcott 1993, verified).

Larva. Idiosoma constricted behind the level of coxae III, covered with scutum and four median shields, encompassing the bases of setae c₁, d₁, e₁ and h₁; the posterior-most shield may be divided into two separate sclerites. Eyes sessile, each composed of two lenses (Hexathrombium), one lens (Hoplothrombium and Alhamithrombium) or eyes reduced to ocular plates (Beronium). Scutum bearing non-sensillary setae (AM, AL, PL) and a pair of sensilla (S). fCx = 2-1-1 or 2-2-2. Medial coxala I (1a) simple. Setae on coxae II and III modified (short, thickened) or simple. Tarsi I and II terminated with two claws and empodium. Tarsus III highly modified, terminated with two claws and lophotrix (“penicala” sensu Southcott 1993). Inner (posterior) claw short and robust, median claw long, falciform. Lophotrix shifted to dorsodistal part of the segment. Gnathosoma with stephanostome. Hypostomalae thick, short.

Active postlarval forms. Not known.

Type genus. Hexathrombium Cooreman, 1944

Genera included

Hexathrombium Cooreman, 1944; Hoplothrombium Ewing, 1925; Beronium Southcott, 1986; Alhamitrombium Mayoral & Barranco, 2005.

Remarks

The position of seta 1a may indistinctly vary in all genera in question, as the seta is inserted close to the coxal plate margin and its actual location in the mounted specimens may be considered dubious. Vercammen-Grandjean (1967) considered 1a, observed within the coxal plate in Ho. quinquescutatum, a “migrated sternal seta”.

The chaetotaxy of terminal leg segments (Ge – Ta I, Ge – Ta II, Ge – Ta III), with special reference to specialized setae, has been variously interpreted due to the difficulties in their visualization, specially their actual nature and presence. The more detailed close-up to the setae, should be carried out to clarify their actual state in all members of the genus.

The highly modified termination of tarsus III is similar in all Hexathrombiini and differs to those observed in Eutrombidiini. Southcott (1993) described in Hexathrombiini the presence of a branched seta (“penicala” sensu Southcott 1993) on the dorsodistal projection of tarsus III, and also two claws located ventrodistally. From those, the median claw is long, falciform and simple, whereas the posterior claw (i.e. smilum) (anterior claw sensu Southcott 1993) is in the form of a short and thick hook with a dorsal spur-like process. In Eutrombidiini, there is a moustache-shaped seta about 3/4 along the dorsum of tarsus III (“cultala” sensu Southcott 1993), a multipronged seta with several large setules arising dorsally at the distal end of tarsus (“dumala” sensu Southcott 1993), and a thickened setae with setules in the ventrodistal portion of the tarsus (“calcanala” sensu Southcott 1993) (Southcott 1993). Husband and Wohltmann (2011) observed in Eutrombidium the presence of a scopa on tarsus III (“cultala” sensu Southcott, 1993) and lophotrix (“dumala” sensu Southcott 1993). Despite the different position of branched, pectinate seta in Hexathrombiini (seta shifted to a dorsodistal position), its structure is congruent with the lophotrix observed in Eutrombidiini and also in some other microtrombidiid mites. The short and thick inner claw located ventrodistal and covered with few bristles should be considered a smilum. Another modified seta, a scopa, is absent in Hexathrombiini.

Hexathrombium Cooreman, 1944Hexathrombium Cooreman, 1944: 1.Hexathrombium: Southcott 1993: 945.

Diagnosis

(after Southcott, 1993, verified).

Larva. The posterior-most shield on dorsal idiosoma (pygidial shield, Q5) entire (He. marittae, He. lubomirae, He. willisi) or divided into two separate sclerites (He. abirami, He. cicindelae, He. fageli, He. mamerti, He. sorayae, He. southcotti, He. spatuliferum). Eyes composed of two lenses inserted in ocular plates. Odontus bifid. fCx = 2-1-1. Medial coxala I (1a) simple (spike-like or slender, tapering). Lateral coxala I (1b), coxalae II (2b) and III (3b) bilobed, with diverged processes (in He. willisi – 1b, 2b, 3b - bilobed, with indistinctly diverged, rounded apically processes). Seta 3a shifted to intercoxal position or absent. Pre-anal tubercle present. fV = 12–16 (18–20 in He. southcotti); for comparison of character state in South American species see Table III. Hypostomala reniform.

Type species

Hexathrombium spatuliferum Cooreman, 1944

Species included and country records

He. abirami, Brazil, Peru; He. cicindelae, French Guiana; He. fageli, Ethiopia, Ivory Coast; He. lubomirae, Madagascar, Sumatra; He. mamerti, Australia; He. marittae, Chile; He. sorayae, China; He. southcotti, China; He. spatuliferum, Zaire; He. willisi, USA. Additional records: He. cf. cicindelae: Almada & Cédola (2017), Argentina; He. cf. marittae: Pérez-Espinoza & Moreno Salas (2016), Chile. Welbourn (1983) reported two presumably new species of Hoplothrombium from Ecuador; they were never formally described, however, they both should be placed in Hexathrombium (Cal Welbourn, pers. comm.).

Hosts

Coleoptera: Carabidae, Erotylidae, Staphylini- dae; Hymenoptera: Ichneumonidae (see also Table IV).

Redescription of Hexathrombium abirami Haitlinger, 1997Hexathrombium abirami Haitlinger, 1997: 81.

Diagnosis

Larva. Pygidial shield (Q5) divided. Coxalae 1a shifted to the margin of coxal plates, slender, tapering. Coxalae 1b and 2b bilobed, with horizontally diverged processes.

Description

Metric data provided in Table I (except for few dimensions given below).

Table I. Metric data for Hexathrombium spp. Species with divided pygidial shield Q5: He. abirami, He. cicindelae, He. fageli, He. mamerti, He. sorayae, He. southcotti, He. spatuliferum. Species with undivided pygidial shield: He. marittae, He. lubomirae. For He. willisi see Southcott (1993)

species	He. cicindelae (Floch & Abonnenc, 1941)	He. cf. cicindelae	He. spatuliferum Cooreman, 1944	He. fageli Fain & Drugmand, 1993	He. marittae (Haitlinger, 1994)	He. cf. marittae	He. sorayae (Haitlinger, 1994)	He. abirami Haitlinger, 1997	He. abirami Haitlinger, 1997	He. southcotti Zheng, 1997	He. mamerti Haitlinger, 1999	He. lubomirae (Haitlinger, 1994)
Source of data	Floch & Abonnenc (1941)	Almada & Cédola (2017)	Fain & Drugmand (1993)	Fain & Drugmand (1993)	Present study (type material)	Pérez-Espinoza & Moreno Salas (2016)	Haitlinger (1994)	Present study (type material)	Present study (new data)	Zheng (1997)	Haitlinger (1999)	Haitlinger (1994)
Distribution	[South America]	[South America]	[Afrotropic]	[Afrotropic]	[South America]	[South America]	[Palaearctic]	[South America]	[South America]	[Palaearctic]	[Australia]	[Sumatra, Magadascar]
Sample size/data layout	Sample size not known	Mean (range)^2 sample size not known	(range) n = 2	(range) n = 3	Mean (range) n = 7^1	Mean (range)^2 n = 25	(range) n = 3	Mean (range) n = 3^1	Mean (range) n = 10	n = 1	(range) n = 9	n = 7^7
IL	630–760^4	492 (545–610)^3	590–630	447–468	473 (417–563)	–	336–576^3	632 (581–667)	673 (564–761)	470	463–527^3	404–704^3
IW	280–430	287 (305–370)	300–302	195–222	236 (203–284)	–	192–328	353 (292–389)	388 (286–465)	250	216–266	208–408
IL/IW	–	–	2.0–2.1	–	2 (1.7–2.2)	–	1.7–2.0	1.8 (1.7–2.0)	1.7 (1.6–2.0)	1.9	–	–
Scutum L	–	[?]146 (132–150)	165–180	140–146	172 (166–178)	–	184–208	192 (187–195)	164 (145–175)	160	148–164	180–198
Scutum W	–	–	166–177	120–135	160 (158–165)	–	166–190	184 (182–187)	154 (138–168)	170	136–148	164–184
AM	–	–	–	30–39	32 (27–37)	–	30–34	32 (31–33)	35 (25–42)	27	28–36	34–44
AA	–	–	74–75	45–47	77 (75–80)	–	80–82	94 (91–98)	73 (67–82)	74	64–72	74–84
MA	–	87 (82–98)	85–99	66–74	74 (73–75)	72 (64–84)	96–104	106 (104–107)	93 (81–105)	98	76–84	98–114
AL	–	–	51–56 (broken)	30–45	44 (42–46)	–	28–32	54	43 (37–48)	30	40–46	32–38
AW	–	108 (102–113)	128–138	43–90	128 (125–132)	–	134–142	148 (145–153)	119 (104–132)	128	106–114	138–150
PL	–	25 (22–30)	32–36	25–38	24	–	18–20	31 (30–32)	30 (27–32)	20	24–30	14–16
PW	–	139 (130–147)	153–165	120–133	148	152 (142–167)	164–180	178 (169–186)	146 (133–162)	155	124–132	160–180
AP	–	34 (30–37)	42–45	39–45	58 (55–61)	59 (54–75)	28–32	49 (44–54)	39 (35–42)	32	38–44	28–32
S	–	–	76–85	65–75	84 (79–89)	–	–	–	106 (93–123)	116	82–96	100–116
SB	–	101 (92–107)^4 91 (75–108)^4	115–120	93–99	117 (110–121)	121 (116–136)	128–140	137 (132–140)	112 (94–126)	118	90–104	128–144
ASB	–	–	140–150	120–122	141 (130–148)	–	154–184	165 (164–166)	138 (120–151)	128	122–140	160–190
PSB	–	–	29–30	20–25	31 (26–36)	–	24–30	27 (21–31)	26 (22–32)	10	20–26	20–24
PSL (HS)	–	–	60–66	57–60	60 (55–70)	–	68–82	60 (56–63)	56 (49–65)	62	50–62	72–82
PSW (LSS)	–	–	150–171	128–130	169 (162–180)	–	170–192	177 (171–184)	145 (128–168)	120	124–154	172–202
PLN	–	29 (28–30)	18–30	36–39	23 (23–24)	–	–	29 (28–30)	31 (26–38)	25	–	19^7
QL (SL)	–	35 (35–40)^5 35 (30–40)^5	50–51	36–39	41 (39–44)	42 (39–49)	[?] 50	–	41 (38–44)	70	44–46	54–60
QW (SS)	–	50 (41–57)	57	42–52	64 (56–69)	32 (28–39)	76–78	72 (71–73)	60 (50–69)	65	46–64	80–100
L3	–	–	33–39	23–26	34 (28–41)	–	30	39 (39–40)	34 (28–38)	30	30–38	36–40
W3	–	–	103–118	75–86	107 (101–119)	–	106–120	118 (111–125)	95 (81–118)	110	72–86	112–126
PLN3	–	18 (18–20)	13–21	12–15	13 (12–14)	–	–	20 (19–20)	19 (15–22)	20	–	18^7
QL3	–	38 (35–43)	51–58	40–45	43 (39–48)	–	60	58	45 (36–51)	70	[?]52	68–74
QW3	–	–	45–50	30–48	47 (42–51)	–	44–60	57 (54–61)	43 (35–56)	50	36–44	54–68
L4	–	–	36–41	30-–32	40 (32–46)	–	34–36	39 (36–43)	41 (35–49)	35	36	36–44
W4	–	–	96–108	57–64	107 (100–111)	–	100–104	113 (100–126)	98 (82–111)	[?]30^8	[?]64–74	106–120
PLN4	–	21 (20–23)	15–19	16–18	13	–	–	18 (17–18)	20 (16–25)	22	–	25^7
QL4	–	41 (38–45)	51–56	42–48	51 (50–54)	–	[?]52–72	54	46 (41–52)	70	[?]54–56	80–90
QW4	–	–	47–48	24–35	61 (56–70)	–	66–72	57 (54–62)	54 (42–69)	30	36–52	78–94
L5	–	34 (33–38)	36	21–24	47 (44–50)	–	38–42	42 (39–44)	41 (36–47)	–	30–36	28–36
W5	–	–	21–24	15–18	57 (47–68)	–	54–60^5	28 (24–32)	23 (15–30)	40	–	44–52
PLN5	–	22 (20–25)	–	–	18 (17–20	–	–	23	23 (20–26)	–	–	16^7
QL5	–	67 (52–75)	70–75	45	53 (49–57)	54 (44–64)	82–90	84 (78–91)	68 (60–75)	90	70–78	102–114
QW5	–	31 (28–35)	35–36	25–28	26 (23–30)	–	24–26	36 (34–39)	42 (30–52)	25	24–28	22–26
DS	–	–	34–60	30–48	29–53	–	30–64	(33–67)	(28–60)	50–70	36–52	20–74
A lens	–	–	–	–	13	–	–	14 (13–15)	11 (8–12)	–	–	–
P lens	–	–	–	–	9	–	–	13 (12–14)	8 (6–10)	–	–	–
Ocular sclerite [L]	–	–	–	–	40	–	28–30	–	32 (29–37)	–	28–34	30–32
Cx I	–	62 (50–68)	–	–	49	–	68–76	69 (64–72)	68 (62–75)	–	58–72	70–80
Tr I	–	–	–	–	30 (25–33)	–	34–42	38 (34–41)	32 (29–39)	–	32–36	36–40
Fe I	–	47 (45–50)	50–54	47–51	49 (48–51)	–	48–54	59 (56–60)	54 (49–60)	–	42–50	50–60
Ge I	–	18 (18–20)	22–26	18–22	20 (18–22)	–	18–20	21 (21–22)	19 (17–22)	–	18–22	22–24
Ti I	–	31 (28–35)	36–39	31–35	29 (26–33)	–	32–36	40 (39–41)	36 (31–41)	–	32–36	34–40
Ta I	–	52 (50–53)	67–69	60–68	70 (64–77)	–	64–66	72 (69–73)	65 (60–69)	–	50–56	60–70
Leg I	–	–	–	–	254	–	266–288	298 (294–302)	275 (257–303)	290^6	244–268	–
Cx II	–	58 (55–60)	–	–	51 (50–52)	–	52–60	60 (57–62)	60 (53–70)	–	44–54	52–56
Tr II	–	–	–	–	31 (30–32)	–	34–42	38 (34–43)	30 (26–35)	–	28–32	34–44
Fe II	–	35	45–48	45	39 (38–40)	–	30–38	47 (44–49)	44 (39–47)	–	32–42	44–52
Ge II	–	16 (15–18)	17–18	15–16	14 (11–16)	–	14–18	15 (14–16)	15 (12–17)	–	16–18	16–20
Ti II	–	27 (25–30)	30–34	24–27	23 (20–25)	–	26–32	29 (26–31)	27 (22–30)	–	20–30	28–32
Ta II	–	43 (43–45)	49–51	42–48	49 (44–53)	–	44–48	53 (51–54)	49 (45–52)	–	40–50	48–56
Leg II	–	–	–	–	–	–	200–234	241 (238–243)	224 (212–233)	230^6	186–212	–
Cx III	–	53 (43–60)	–	–	58 (54–63)	–	52–60	59 (59–60)	55 (50–61)	–	48–56	50–54
Tr III	–	–	–	–	35 (30–39)	–	34–40	42 (41–43)	35 (30–41)	–	36–40	30–40
Fe III	–	38 (35–45)	45	42–45	35 (32–37)	–	32–36	43 (35–51)	41 (38–48)	–	32–40	38–48
Ge III	–	13	15–16	15	11 (9–13)	–	12–16	15 (15–16)	16 (14–18)	–	14–16	14–16
Ti III	–	17 (15–20)	21	20–23	18 (17–21)	–	18–22	24 (24–25)	23 (18–26)	–	18–26	18–22
Ta III	–	32 (30–33)	50–55	45	23 (22–23)	–	44–48	30 (28–32)	26 (23–30)	–	52–56	40–50
Leg III	–	–	–	–	177 (169–181)	–	198–212	216 (210–222)	196 (181–208)	230^6	210–216
IP	–	–	–	–	–	–	664–732	752 (751–754)	695 (650–735)	750^6	–

¹due to the condition of specimens from type series, the sample size for particular measurements varied (0–3 for He. abirami, 0–7 for He. marittae).

²rounded to integers (except for ratios); original data (Almada & Cédola (2017), Pérez-Espinoza & Moreno Salas (2016)) given with decimal values.

³measured with or without gnathosoma.

⁴provided twice (Almada & Cédola (2017: 1089), with different values.

⁵in He. sorayae (Q5 divided, plates not set apart) the actual width of Q5 s.hould equal half of the listed value.

⁶including claws.

⁷holotype and six paratypes from Sumatra; measurements of PLN, PLN3, PLN4, PLN5, based on one specimen, completed during present study.

⁸probably a mistake.

Gnathosoma (Figure 1(a,b)) compact, with well-sclerotized frames of subcapitulum, chelicerae and palps. Stephanostome present. Internal horseshoe-like sclerite inserted between inner and outer cuticular sheath. One pair of nude adoral setae (or). Subcapitular setae reniform. Cheliceral claws distinctly curved. Palps relatively small and robust. fP_p = 0-N-N-NNB2-BNNNNNωζ. Seta on palp femur and palp genu short, thorn-like. Two setae on palp tibia short, thorn-like, the third seta long, with 1–2 fine barbs. Odontus bifid. The longest, most proximal seta on palp tarsus with few (2–3) indistinct barbs only. Palpal supracoxalae (elcp) not detectable.

Figure 1. Hexathrombium abirami, larva. a) Gnathosoma (complete chaetotaxy of palp tibia and palp tarsus not shown). b) Details of palp tibia and palp tarsus

Supplementary measurements, not included in the Table I (format: mean (range)), for 10 specimens from Peru: GL = 101 (90–111), PaFe = 13 (11–15), PaGe = 9 (7–10), PaTi = 9 (8–11), PaTa = 7 (6–8), Odo = 6 (5–7), Ch base = 87 (77–104), Ch claw = 18 (13–24), bs = 10 (8–12).

Dorsal idiosoma (Figure 2) oval, slightly constricted behind the level of coxae III, rounded at anterior and posterior termination. Integument, except for sclerites, folded in lines. Scutum (Q1) (Figures 2 and 3) pentagonal in outline, rounded anteriorly, bearing paired, non-sensillary setae AM, AL, PL, and a pair of sensilla (S). Antero-lateral parts of scutum with linear pattern, medial part of the sclerite porous. Posterior margin almost straight, bordered with delicate lamellar band. Additionally, small octal-shaped or semi-oval mark, probably representing the less sclerotized part of the sclerite, present antero-laterally in lower layer of scutum (or [?] immediately under the scutum surface), on each side of symmetry axis. Bases of sensilla located between AL and PL bases, closer to PL and slightly shifted to medial position. AM smooth or with 1–2 barbs, AL, PL and S with few barbs along entire stem length. Paired eye lenses (Figure 2), each pair on a common, weakly sclerotized plate located close to the postero-lateral margins of the prodorsal sclerite (Q1). Scutellum (Q2) trapezoidal in shape, with a pair of c₁ setae. Second and third scutellum (Q3, Q4) with a pair of d₁ and e₁ setae, respectively (in one specimen (7802/13) with duplicated seta e₁ on Q4 sclerite); both sclerites rectangular in shape, with rounded corners. Setae e₁ located close to the anterior margin of Q4. The fifth shield (Q5) divided into two separated, oval plates, each bearing a h₁ seta. fD: (2)4-(2)4-(2)4-6-(1 + 1)2 = 28. Setae in rows C, D, E, F, except for c₁, d₁, e₁, located on small platelets; stems of setae in C-F rows only slightly narrowed at termination and covered with short barbs along the entire length. Setae c₃, d₃, e₃ slightly shorter than other setae in the respective rows C-E. Setae h₁ and h₂ longer than the preceding setae, distinctly narrowed apically; h₂ inserted in roundish plates (of diameter similar to the width of h₁ plates, i.e. Q5/2); shafts of h₂ slenderer than those of h₁ and with distinct setules.

Figure 2. Hexathrombium abirami, larva. Idiosoma, dorsal aspect

Figure 3. Hexathrombium abirami, larva. Scutum

Ventral idiosoma (Figure 4)

Coxal plates (I – triangular in outline, II – rectangular, rounded at base, III – square-shaped in outline) well sclerotized along the anterior border; the posterior border weakly marked or discontinuous. Anterolateral part of coxa I frame as well as its distal portion strongly sclerotized (Figure 4); sclerotization of the respective parts of coxae II and III less pronounced. Claparède’s organs (clp) present at posterolateral corner of coxa I. Coxa I with two setae, medial coxala (1a) normal, nude, tapering, placed on cuticular band forming the medial extension of the most sclerotized part of coxal frame; lateral coxala (1b) modified, bilobed (Figure 6(a)); coxa II and coxa III with one modified, bilobed seta each (2b and 3b, respectively); all modified coxalae (1b, 2b, 3b) with horizontally diverged processes (lobes); lobes indistinctly narrowing at termination and slightly extending beyond the setal base (widely diverging in 2b, making the seta the widest in comparison with 1b and 3b). Setae 3a (20 long) simple, slender, nude, and located between coxae III. Supracoxalae of coxae I (elc I) not detectable. fV: 4-4u-4-2 = 14. Ventral setae tapering, with thinner shafts than dorsal setae. Anal opening surrounded with membraneous valves, anal sclerites absent. Pre-anal protuberance (tubercle) present, circle-like, similar in diameter to the length of anus, and located anterior to excretory slit. The tubercle, slightly elevated above the idiosoma surface, surrounded with more sclerotized, porous sides.

Figure 4. Hexathrombium abirami, larva. Gnathosoma and idiosoma, ventral aspect

Legs (Figure 5(a–c))

Segmentation formula 6-6-6. For leg chaetotaxy see Table II. Normal setae on legs setulated to smooth. Robust, fan-like seta present in distal part of tarsus II. Tarsi I and II terminated with two claws and empodium. Claws similar in length, covered with onychotrichs. Empodium claw-like, slightly spatulate distally. Tarsus III highly modified at termination, with lophotrix in dorsodistal position and two claws located ventrodistal. Lophotrix composed of one branch, with one long, proximal, secondary branch on one side and with several, gradually shortening, secondary and tertiary branches on the other (Figure 7(a)). Inner claw short, robust, with small spurs; medial claw long, falciform.

Figure 5. Hexathrombium abirami, larva. Legs (trochanter – tarsus). a) leg I. b) leg II. c) leg III. Abbreviations: lo – lophotrix, sm – smilum

Figure 6. Lateral coxalae I (1b), II (2b), III (3b) in larvae of Hexathrombiini. a) Hexathrombium abirami, holotype. b) Beronium veronicae, holotype. c) Alhamitrombium tetraseta, holotype. Not to scale

Figure 7. Lophotrix in larvae of Hexathrombiini. a) Hexathrombium abirami. b) Hexathrombium lubomirae, holotype. c) Hexathrombium mamerti. d) Beronium veronicae, holotype. e) Alhamitrombium tetraseta, holotype. Not to scale

Table II. Leg chaetotaxy of Hexathrombium spp.¹ Species with divided pygidial shield Q5: He. abirami, He. fageli, He. mamerti, He. sorayae, He. southcotti. Species with undivided pygidial shield: He. marittae, He. lubomirae, He. willisi.

	He. fageli Fain & Drugmand, 1993	He. willisi Southcott, 1993	He. marittae (Haitlinger, 1994)	He. sorayae (Haitlinger, 1994)	He. lubomirae (Haitlinger, 1994)	He. abirami Haitlinger, 1997	He. abirami Haitlinger, 1997	He. southcotti Zheng, 1997	He. mamerti Haitlinger, 1999
Source of data	Fain & Drugmand (1993)	Southcott (1993)^Citation2	Present study (type series)	Haitlinger (1994)	Present study (type material)	Present study (type material)	Present study (new material examined)	Zheng (1997)	Present study (type material)
Cx I	2 [1a – normal, 1b – modified, with widely divergent lobes]	2 [1a – normal, 1b – modified, with not widely divergent lobes]	2 [1a – normal, 1b – modified, with widely divergent lobes]	2 [1a – normal, behind coxal plate, 1b – modified, with widely divergent lobes]	2 [1a – normal, 1b – modified, with widely divergent lobes]	2 [1a – normal, 1b – modified, with widely divergent lobes]	2 [1a – normal, 1b – modified, with widely divergent lobes]	2 [1a – normal, 1b – modified, with widely divergent lobes]	2 [1a – normal, 1b – modified, with widely divergent lobes]
Tr I	1n	1n	1n	1n	1n	1n	1n	1n	1n
Fe I	6n	5–6n	6n	6n	6n	6n	6n	6n	6n
Ge I	4n, 2σ	[?]n, 2σ	[?]4n, 2σ	5n, 1σ	5n, 1σ	5n, 1σ	5n, 1σ	6n	5n, 1σ
Ti I	6n, 2φ	4n, 1φ	6n, 2φ, 1κ	6n, 2φ, 1κ	6n, 2φ, 1κ	6n, 2φ, 1κ	6n, 2φ, 1κ	8n^4	6n, 2φ, 1κ
Ta I	[?]n, 1ω, 1ζ, 1ε	[?]14n, 1ω	[?]18n, 1ω, [?]2ζ^3, 1ε	[?]16n, 1ω, 1ε	c. 16n, 1ω, 2ζ, 1ε	[?]15n, 1ω, [?]2ζ^3, 1ε	18n, 1ω, 2ζ, 1ε	19n	[?]16n, 1ω, 2ζ, 1ε
Cx II	1 [2b – modified, with widely divergent lobes]	1 [2b – modified, with not widely divergent lobes]	1 [2b – modified, with widely divergent lobes]	1 [2b – modified, with widely divergent lobes]	1 [2b – modified, with widely divergent lobes]	1 [2b – modified, with widely divergent lobes]	1 [2b – modified, with widely divergent lobes]	1 [2b – modified, with widely divergent lobes]	1 [2b – modified, with widely divergent lobes]
Tr II	1n	1n	1n	1n	1n	1n	1n	1n	1n
Fe II	5n	5n	5n	5n	5n	5n	5n	5n	5n
Ge II	2n, 1σ	[?]n, 1σ	3n	3n	2n, 1σ	2n, 1σ	2n, 1σ	4n	2n, 1σ
Ti II	5n, 2φ	6n, 1φ	6n	5n, 2φ	5n, 2φ	5n, 2φ	5n, 2φ	7n^5	5n, 2φ
Ta II	[?]n, 1ω	[?]11n, 1ω	14n, 1ω	13n, 1ω	c.13n, 1ω, 1ε	[?]14n, 1ω, 1ε	14n, 1ω, 1ε	15n	[?]12n, 1ω, 1ε
Cx III	1 [3b – modified, with widely divergent lobes]	1 [3b – modified, with not widely divergent lobes]	1 [3b – modified, with widely divergent lobes]	1 [3b – modified, with widely divergent lobes]	1 [3b – modified, with widely divergent lobes]	1 [3b – modified, with widely divergent lobes]	1 [3b – modified, with widely divergent lobes]	1 [3b – modified, with widely divergent lobes]	1 [3b – modified, with widely divergent lobes]
Tr III	1n	1n	1n	1n	1n	1n	1n	1n	1n
Fe III	4n	4n	4n	4n	4n	4n	4n	3n	4n
Ge III	2n, 1σ	[?]n, 1σ	2n, 1σ	3n^7	2n, 1σ	2n, 1σ	2n, 1σ	3n^6	2n, 1σ
Ti III	5n	5n	5n	5n	5n	5n	5n	4n	5n
Ta III	[?]n	[?]9n	[?]10n	c. 10n	c. 11n	c. 11n	11n	14n	[?]12n

¹He. cicindelae and He. spatuliferum omitted due to the unavailability of data.

²data on He. willisi incomplete (see Southcott 1993), partly inferred from drawing.

³the presence of eupathidia on tarsi difficult to ascertain based on type material examined.

⁴the state 6n, 2φ or 6n, 2φ, 1κ cannot be excluded.

⁵the state 5n, 2φ cannot be excluded.

⁶the state 2n, 1σ cannot be excluded.

Material examined

Holotype and two paratypes, deposited in the Museum of Natural History, University of Wroclaw, Poland. Ten larvae collected on T. fulgida from Peru in 2015 (present study) and randomly selected from a sample of 361 specimens parasitizing one host (for details – see Material and methods).

Remarks

The new specimens collected in Peru and studied in this work were compared with the type material of He. abirami, and also with other species of Hexathrombium, with an emphasis on the South American species in the genus. A comparison of the metric data of the Peruvian specimens with the type series is included in Tables I and II. The differences observed in metric data between the type series of He. abirami and specimens collected in Peru (Table I) are attributed to intraspecific variations. These variations may be a result of the differences in geographic locations, ecological factors, and the mounting quality of the type material that may have affected the reliability of some measurements.

Based on the reexamination of the holotype and two paratypes of He. abirami Haitlinger, 1997, some characters redescribed here differ from those reported in the original description. A pair of eyes (each composed of two lenses placed on a common sclerite) are present at each side of scutum (original description, Figure 1, p. 82: one lens present at posterolateral margin of scutum, on each side of symmetry axis). Setae AL = 54 (original description: AL broken in all specimens); fn Fe = 6-5-4 (original description: fn Fe = 5-5-4); fn Ge = 5-2-2 (original description: fn Ge = 5-5-3); fn Ti = 6-5-5 (original description: fn Ti = 8-7-5); fsol Ti = 2-2-0 (original description: 2-1-0); vestigiala on tibia I, 2 eupathidia on tarsus I, famulus on tarsus II present. Preanal tubercle present.

Parasitism of specimens collected in Peru

Altogether, 361 larvae were found parasitizing a single carabid host, T. fulgida (Figures 8(a–d) and 9(a–d)). Eight were attached to the head (including labrum) (Figure 8(a–d)), 86 to the pronotum (Figure 8(a)), 183 to the elytra (22 under elytra) (Figure 8(a) and 9(a),(c)), 50 to the thorax and venter of abdomen (Figures 8(a–d) and 9(b)), and 26 were distributed among various leg segments (Figure 9(d)); for the remaining eight larvae the attachment sites were not recorded. Parasites seem to show a preference for the dorsal parts of the host and there was no preference for softer cuticle areas (including the dorsal abdomen), and instead the preference was for externally exposed areas that seem to be out of the reach of the host legs. Larvae were relatively firmly attached, and except for eight specimens, the detachment had to be performed with an entomological pin and forceps.

Figure 8. Tetracha fulgida with larvae of Hexathrombium abirami. a) dorsal habitus of the host. b) ventral habitus. c) head and anterior part of thorax, ventral view. d) head and anterior part of thorax, side view. Not to scale

Figure 9. Tetracha fulgida with larvae of Hexathrombium abirami. a) elytra. b) venter of abdomen. c) elytra (close-up). d) leg. Not to scale

Distribution

Neotropical (Brazil - original description, Peru - present data).

Supplementary data to the original descriptions of He. lubomirae, He. mamerti and He. marittae

Hexathrombium lubomirae (Haitlinger, 1994)Beronium lubomirae Haitlinger, 1994: 50.Hexathrombium lubomirae: Haitlinger 1997: 81.

Material examined

Holotype and six paratypes from Sumatra, mounted on one slide. For leg chaetotaxy see Table II.

Pygidial shield (Q5) undivided, with indistinct median incision at the posterior margin. Setae 1a shifted beyond the margin of coxa. Setae 3a absent. Setae 1b, 2b, 3b as in He. abirami. Preanal tubercle present. fn Fe = 6-5-4 (original description: fn Fe = 5-5-4); fn Ge = 5-2-2 (original description: fn Ge = 5-3-3); fsol Ge = 1-1-1 (original description fsol Ge = 0-0-0); fκ Ti = 1-0-0 (original description: fκ Ti = 0-0-0); fζ Ta = 2-0-0 (original description: 0-0-0); fε Ta = 1-1-0 (original description: 1-0-0). Lophotrix two-branched, each branch with several bristles (Figure 7(b)).

Hexathrombium mamerti Haitlinger, 1999Hexathrombium mamerti Haitlinger, 1999: 58.

Material examined

Holotype and eight paratypes mounted on one slide. For leg chaetotaxy see Table II.

Setae 1b, 2b, 3b as in He. abirami. fn Fe = 6-5-4 (original description: fn Fe = 5-5-4); fκ Ti = 1-0-0 (original description: fκ Ti = 0-0-0); fζ Ta = 2-0-0 (original description: 0-0-0); fε Ta = 1-1-0 (original description: 0-0-0). Tarsus I, tarsus II and femur III bearing a distinct seta, smooth or with few short barbs, much longer than the other setae in the segment. Lophotrix composed of two branches; the most proximal branch bifurcate at termination. The distal branch of the stem with several (c. 5) secondary branches (at least three of those as well as the main stem are bifurcate at termination (Figure 7(c)).

This species is similar to He. abirami, however it shows smaller measurements for most of the characters studied (see Table I).

Hexathrombium marittae (Haitlinger, 1994)Beronium marittae Haitlinger, 1994: 48.Hexathrombium marittae: Haitlinger 1997: 81.

Material examined

Holotype and four paratypes mounted on one slide and collected from Ceroglossus sybarita (now Ceroglossus buqueti sybarita); two paratypes mounted on another slide and collected from Ceroglossus darwini. Metric data are shown in Table I. For leg chaetotaxy see Table II.

Pygidial shield (Q5) undivided. fV = 14 (original description: fV = 20). Preanal tubercle present. Distal part of tarsus II with a fan-like seta, similar to one observed in He. abirami, but less robust.

Hoplothrombium Ewing, 1925Hoplothrombium Ewing, 1925: 263.Hoplothrombium: Vercammen-Grandjean 1967: 2.

Diagnosis

(after Vercammen-Grandjean 1967).

Larva. The posterior-most shield on idiosoma dorsum (pygidial shield, Q5) oblong, undivided. Eye composed of one lens inserted in an elongate ocular plate. Odontus simple. fCx = 2-2-2. Medial coxala I (1a) simple, elongate, smooth. Lateral coxala I (1b), medial and lateral coxala II (2a, 2b) and lateral coxala III (3b) spike-like. Medial coxala III (3a) barbed. fV = 18. Hypostomala in the form of a thick, short spine.

Type species

Hoplothrombium quinquescutatum Ewing, 1925

Species included and country record. Ho. quinquescutatum, Canada.

Hosts

[?] Oribatida (Ewing 1925).

Beronium Southcott, 1986Beronium Southcott, 1986: 62.

Diagnosis

(after Southcott 1986; Haitlinger 1994; Mayoral & Barranco 2005b, verified).

Larva. The posterior-most shield on idiosoma dorsum (pygidial shield, Q5) oblong, undivided. Eye lenses absent, ocular plate elongate. Odontus bifid. fCx = 2-1-1. Medial coxala I (1a) simple, thickened in anterior half, then acuminating or short, thin, setulose. Lateral coxala I (1b) short, stout either with blunt end or indistinctly bifid at termination, sometimes amorphic in anterior part. Lateral coxala II (2b) short, stout with rounded ends, slightly bifid. Coxala III (3b) short, peg-like, unilobed or indistinctly bifid. Setae 3a absent. Pre-anal tubercle present. fV 18–23. Setae around anal slit short, slightly thickened or thick, spine-like. Hypostomala reniform.

Type species

Hoplothrombium coiffaiti Beron, 1973

Species included and country records. B. coiffaiti, Morocco; B. veronicae, Spain (Canary Islands); B. laemostenis, Spain.

Hosts

Coleoptera: Carabidae (Platyninae: Sphodrini: Sphodrina).

Remarks

The absence of eyes, hitherto reported for Beronium, constitutes one of the main differences which allow to distinguish between Beronium spp., Alhamitrombium, spp. and Hexathrombium spp. In B. laemostenis and B. veronicae, ocular sclerites are present and they are elongated in shape, narrowing anteriorly and truncated posteriorly (Figure 10(a)); they are located adjacent to the posterolateral margins of the scutum, and in a similar location to the ocular plates observed in other trombidioid genera (including Hexathrombium). The plates are punctated over the entire surface and surrounded by folded in lines cuticle. The shape of these sclerotized structures resembles the plates surrounding the eye lenses in Hoplothrombium (Vercammen-Grandjean 1967: 5).

Figure 10. Beronium veronicae, holotype, larva. a) ocular sclerite. b) preanal tubercle. Alhamitrombium tetraseta, holotype, larva. c) ocular sclerite. Not to scale

Beronium veronicae Haitlinger, 1994Beronium veronicae Haitlinger, 1994: 50.

Material examined

Holotype and two paratypes mounted on one slide. For leg chaetotaxy see Table II.

Supplementary data to the original description of B. veronicae: pre-anal tubercle present (Figure 10(b)); coxalae 1b and 2b short, thick, indistinctly bifid, rounded lobes; coxalae 3b unilobed, peg-like and rounded terminally; fsol Ge = 1-1-1 (original description fsol Ge = 1-1-0). Setae on legs distinctly setulated. Lophotrix composed of two branches diverging from the main stem; one branch nude, the other one with several (c. 7) secondary branches (Figure 7(d)).

Mayoral & Barranco (2005b) in their key to Beronium spp., and followed by Mayoral (2013), referred to the presence of one solenidion on genu I and the lack of solenidia on genu III as characters to differentiate B. veronicae from the other two species in the genus. This was based on the original description of B. veronicae, in which Haitlinger (1994) described one solenidion on genu I and no solenidia on genu III. The present reexamination of the type material of B. veronicae allowed to confirm the presence of one solenidion on Ge I, but there is also a solenidion present on Ge III. Therefore, the presence of one solenidion on genu III should be treated as character shared by all three species assigned to Beronium. It is still possible to separate B. laemostenis from B. veronicae based on the number of solenidia on Ge I (2 vs. 1) (see Table V). Future reexamination of B. coiffaiti should help to verify the taxonomic status of this species.

Table III. Meristic traits related to idiosoma of Hexathrombium spp. Species with divided pygidial shield Q5: He. abirami, He. cicindelae, He. fageli, He. mamerti, He. sorayae, He. southcotti. Species with undivided pygidial shield: He. marittae, He. lubomirae. For He. willisi see Southcott (1993)

	He. cicindelae (Floch & Abonnenc, 1941)	He. fageli Fain & Drugmand, 1993	He. spatuliferum Cooreman, 1944	He. marittae (Haitlinger, 1994)	He. sorayae (Haitlinger, 1994)	He. lubomirae (Haitlinger, 1994)	He. abirami Haitlinger, 1997	He. southcotti Zheng, 1997	He. mamerti Haitlinger, 1999
Source of data	Floch & Abonnenc (1941)	Fain & Drugmand (1993)	Cooreman (1944)	Present study (type material)	Haitlinger (1994)	Haitlinger (1994)	Present study (type material and new material examined)	Zheng (1997)	Haitlinger (1999)
fV	14^1	16	16^2	14	14^3	12(14)	14	18–20	14

¹the presence 18 setae (including [?]3a and h2 stated in the original description by Floch & Abonnenc (1941); 14 setae present in He. cf. cicindelae by Almada & Cédola (2017) (one extra pair should be assigned to dorsal formula).

²setae h₂ drawn by Cooreman (1944) on ventral face of idiosoma should be excluded from fV formula.

³the presence of 12 setae reported by Haitlinger (1994) in the text and 14 setae (none of which is duplicated in the dorsal formula) provided in the drawing.

Table IV. Host and distribution data on Hexathrombium spp. recorded from South America

	He. cicindelae (Floch & Abonnenc, 1941)	He. cf. cicindelae	He. marittae (Haitlinger, 1994)	He. cf. marittae^1	He. abirami Haitlinger, 1997	He. abirami Haitlinger, 1997
Host	Coleoptera Carabidae	Coleoptera Carabidae	Coleoptera Carabidae	Coleoptera Carabidae	Coleoptera Erotylidae	Coleoptera Carabidae
	Odontocheila cajennensis (Fabricius)	Tetracha (Tetracha) brasiliensis brasiliensis (Kirky)	Ceroglossus buqueti sybarita Gerstaecker, Ceroglossus darwini Fabricius, Ceroglossus suturalis Hoppe, [?] “Ceroglossus valdiviae Hoppe”	Ceroglossus buqueti (Laporte)	Undetermined Erotylidae	Tetracha fulgida (Klug)
Distribution in South America	French Guiana	Argentina	Chile	Chile	Brazil	Peru
References	Floch & Abonnenc (1941), Felska et al. (2018)	Almada & Cédola (2017)	Haitlinger (1994), Felska & al. (2018)	Pérez-Espinoza & Moreno Salas (2016)	Haitlinger (1997)	This study

¹according to Pérez-Espinoza & Moreno Salas (2016) the length of setae, used as diagnostic character, is highly variable, and measures of QL setae do not correspond with the key; however, measures of setae QL5, AP and MA, correspond to the description of He. marittae by Haitlinger (1997).

Table V. Leg chaetotaxy of Beronium spp

	B. coiffaiti (Beron, 1973)	B. laemostenis Mayoral & Barranco, 2005	B. veronicae Haitlinger, 1994
Source of data	Beron (1973)	Mayoral & Barranco (2005b) and present study (type material)	Present study (type material)
Cx I	2 [1a – simple, 1b – modified, short, thick, indistinctly bifid]	2 [1a – simple, 1b – modified, short, thick, indistinctly bifid]	2 [1a – simple, 1b – modified, short, thick, indistinctly bifid]
Tr I	1n	1n	1n
Fe I	6n	6n	6n
Ge I	6n	4n, 2σ	5n^1, 1σ
Ti I	8^2	7n, 2φ, 1κ	6n, 2φ, 1κ
Ta I	16n, 1ω, 1ε^3	20n, 1ω, 1ε	c. 16n, 1ω, 2ζ, 1ε
Cx II	1 [2b – modified, indistinctly bifid]	1 [2b – modified, short, bifid]	1 [2b – modified, indistinctly bifid]
Tr II	1n	1n	1n
Fe II	5n	5n	5n
Ge II	3n^4	2n, 1σ	2n, 1σ
Ti II	7^5	5n, 2φ	5n, 2φ
Ta II	12n, 1ω	14n, 1ω, 1ε	c. 16n, 1ω, 1ε
Cx III	1 [3b – modified, indistinctly bifid]	1 [3b – modified, peg-like, unilobed]	1 [3b – modified, indistinctly bifid]
Tr III	1n	1n	1n
Fe III	4n	4n	4n
Ge III	2n, 1σ	2n, 1σ	2n, 1σ
Ti III	5n	5n	5n
Ta III	11n	14n	c. 11n

¹there are two setae which are smooth and their actual nature is difficult to ascertain.

²a total of eight setae reported by Beron (1973); the state 6n, 2φ cannot be excluded.

³presence of famulus inferred from the drawing provided by Beron (1973).

⁴the state 2n, 1σ cannot be excluded.

⁵a total of seven setae reported by Beron (1973); the state 5n, 2φ cannot be excluded.

The leg chaetotaxy of all three nominal species assigned to the genus is provided in Table V. The differences between the members of Beronium may pertain also to the number of setae in fV formula (B. coiffaiti – 19, B. laemostenis – 18–23, B. veronicae – 22(23)).

Alhamitrombium Mayoral & Barranco, 2005Alhamitrombium Mayoral & Barranco, 2005a: 111.

Diagnosis

(after Mayoral & Barranco 2005a, verified).

Larva. The posterior-most shield on idiosoma dorsum (pygidial shield, Q5) entire, oblong. Eye composed of one lens inserted in elongate ocular plate (Figure 10(c)). Odontus bifid. fCx = 2-1-1. Medial coxala I (1a) long, simple, slender. Lateral coxala I (1b) short, stout, distinctly bilobed, coxala II (2b) bilobed, with diverged rounded processes (fan-like), and coxala III (3b) short, peg-like, unilobed (Figure 6(c)). Setae 3a absent. fV = 21–23. Setae around anal slit long, robust, tapering and similar to 1a setae. Pre-anal tubercle present. Hypostomala reniform. Lophotrix composed of a main branch with 9 smaller secondary branches that shorten gradually towards distal end; a secondary long branch without ramifications is located anteriorly (Figure 7(e)).

Type species

Alhamitrombium tetraseta Mayoral & Barranco, 2005

Species included and country record

A. tetraseta, Spain.

Hosts

Coleoptera: Carabidae (Harpalinae: Lebiini).

Key to Hexathrombiini genera

[incl. Hoplothrombium - monotypic, Alhamitrombium - monotypic, Beronium, Hexathrombium]

Modified from Southcott 1993; Haitlinger 1994; 1997; Mayoral & Barranco 2005a, 2005b and based on the type material and material examined in this study (see: Material and methods)

• 1. fCx 2-2-2; lateral coxala I (1b) not modified, simple Hoplothrombium [Ho. quinquescutatum]

  - fCx 2-1-1; lateral coxala I (1b) modified, stout, peg-like or bifid 2

• 2. seta 3a absent; coxala III (3b) not bifid, with rounded or only indistinctly incised termination 3

  - seta 3a present or absent; coxala III (3b) bifid, with diverging or adjacent to each other processesHexathrombium [for the selection of species see provisional key below]

• 3. one eye on each side of prodorsum; ocular plate present; medial coxala (1a) slender, setulose, lateral coxala I (1b) stout, bilobedAlhamitrombium [A. tetraseta]

  - eyes absent; ocular plate present; medial coxala (1a) simple, lateral coxala I (1b) stout, indistinctly bifid or bluntBeronium [B. coiffaiti, B. laemostenis, B. veronicae]

Provisional key to Hexathrombium species

• 1. setae 3a present between coxal plates III [He. abirami, He cicindelae, He. fageli, He. mamerti, He. southcotti, He. spatuliferum, He. willisi] 2

  -. setae 3a absent [He. lubomirae, He. marittae, He. sorayae] 6

• 2. coxalae 1b, 2b, 3b with pointed, widely divergent lobes; pygidial shield (Q5) divided into two separate plates, each encompassing the base of one h₁ seta [He. abirami, He. cicindelae, He. fageli, He. mamerti, He. southcotti, He. spatuliferum] 3

  -. coxalae 1b, 2b, 3b with rounded, not widely divergent lobes; pygidial shield (Q5) undivided, encompassing the bases of paired h₁ setaeHe. willisi [USA, Oklahoma]

• 3. elongate, needle-shaped seta, much longer than other leg setae, present on tarsus I, tarsus II and femur IIIHe. mamerti [Australia]

  -. elongate, needle-shaped seta absent[He. abirami, He. cicindelae, He. fageli, He. southcotti, He. spatuliferum] 4

• 4. leg setae setulated He. fageli [Ethiopia, Ivory Coast]

  - leg setae barbed or nude[He. abirami, [?]He. cicindelae, [?]He. southcotti, He. spatuliferum] 5

• 5. setae PL levelled with SHe. southcotti [China]

  -. setae PL posterior of S [He. abirami [Brazil, Peru], [?]He. cicindelae*, He. spatuliferum*]

• 6. pygidial shield (Q5) undivided, at most with medial incision at posterior border[He. lubomirae, He. marittae]10

  pygidial shield (Q5) dividedHe. sorayae [China]

• 7. pygidial shield oblong; AP > 50; QL5 < 100He. marittae [Chile]

  -. pygidial shield incised posteriorly; AP < 35; QL5 > 100He. lubomirae [Madagascar, Sumatra]

*He. cicindelae [French Guiana] excluded from further key identification due to the insufficiency of data provided in the description; He. spatuliferum [Zaire]– re-examination of type necessary.

Discussion

Fain and Drugmand (1993) and Southcott (1993) erected, independently and within the same year (1993), the tribe Hexathrombiini within Eutrombidiinae to accommodate Beronium, Hexathrombium and Hoplothrombium. Due to the time coincidence, the authorship of the tribe has been assigned by different authors to either Fain and Drugmand (Fain & Jocqué 1996) or Southcott (Mayoral & Barranco 2005a). Fain and Drugmand published their paper on September 10^th, 1993, and Southcott’s paper was published on October 1^st, 1993. In accordance with the Article 24 and 50.6 of the International Code of Zoological Nomenclature (1999), we attribute the authorship of the tribe to Fain and Drugmand (1993); thus, Hexathrombiini Southcott, 1993 become an objective synonym of Hexathrombiini Fain & Drugmand, 1993.

Members of Hexathrombiini display relatively high consistency of character states, however the few differences observed at intratribal level seem to justify the independent status of genera hitherto assigned to this tribe. Among them, the presence/absence of eyes and the shape of coxal setae 1b, 2b, 3b (see also Figures 6 and 10(a,c)) are particularly important. On the other hand, a limited number of differences between nominal species assigned to Hexathrombium and Beronium poses the question of the actual species borders. This is accentuated by the limited number of known species for each of these two genera. The answer to the question should be reconsidered in the future when more species are described, taking in consideration larvae, active postlarval forms and molecular results when they are available. The status of the species assigned to Hexathrombium, with special reference to South American and African members, should be revised in the future when the redescriptions of He. cicindelae and He. spatuliferum become available.

The functional significance of pre-anal tubercle in Hexathrombiini should be elucidated. The presence of this structure, referred by Southcott (1993) as a “small near-circular structure”, was confirmed in the species He. willisi, He. cf. marittae and He. cf. cicindelae in Hexathrombium (Southcott 1993; Pérez-Espinoza & Moreno Salas 2016; Almada & Cédola 2017) and also in the species A. tetraseta, B. laemostenis and B. veronicae (see also Figure 10(b)) during our reexamination of these type specimens. The tubercle, due to its overall small size, may have been overlooked by some authors and thus omitted in their descriptions.

In Beronium Southcott, 1986, the shape of coxal setae, especially 1b, has been variously reported and there seems to be some variability in between specimens and species. Mayoral & Barranco (2005b) reported the presence of blunt and conical lateral coxala I in Beronium. In the current revision of the type material of B. laemostenis, it was possible to observe that there is some variation in the shape of this character among specimens. In this species, 1b seta is mostly thick and conical, but some specimens show a deformation of the seta and in some others, it looks slightly bifid. Haitlinger (1994) did not describe the seta 1b in B. veronicae, (except for referring to it as “thick seta”) but in the present re-examination of the holotype we can confirm the presence of 1b which is indistinctly bifid at termination (Figure 6(b)). This character (seta 1b) should be verified in B. coiffaiti, that according to the description of Beron (1973) is dilated.

There are very little data available about the biology and ecology of Hexathrombiini. The infestation of the bright metallic tiger beetle (T. fulgida) by the parasitic mite larvae He. abirami may have taken place on the ground – in wet sand or mud – with sparse or no vegetation. This is the natural habitat of adults of T. fulgida. Remarkably, this beetle has been proposed as a natural predator of the pest mole cricket in golf courses (T. fulgida in GBIF 2019). The number of mite larvae recorded (361) on a single host specimen reported in this study is the highest number of parasites recorded in arthropod-associated terrestrial Parasitengona mites. The next two highest values reported were also recorded for Eutrombidiinae larvae. Severin (1944) reported the presence of 175 larvae of Eutrombidium locustarum on Dissosteira carolina (Orthoptera), and Pérez-Espinoza & Moreno Salas (2016) reported 186 larvae of He. cf. marittae infesting Ceroglossus buqueti (Coleoptera: Carabidae). The preferred attachment site of Hexathrombium spp. larvae varied across different hosts, despite the similarities in the hosts’ body (they are closely related species). Around 50% of larvae collected in this study were attached to elytra. No larvae were attached to dorsal abdomen, which is consistent with the observations of Pérez-Espinoza and Moreno Salas (2016). Almada and Cédola (2017) reported that most larvae displayed a preference for the ventral thorax; in our study, only around 14% of larvae were attached to the thorax and venter abdomen.

Several morphological traits (presence of stephanostome facilitating a firm attachment to the host, relatively short legs), behavioral (preference to attachment sites with lower accessibility to hosts’ legs) and ecological (relatively narrow host spectrum) are of significant adaptive advantage and may reflect the relatively long co-evolution of Hexathrombium and other Hexathrombiini with their hosts.

Authors’ contributions

JMąkol and JMayoral contributed to the study design. SF performed the collection of T. fulgida with parasitic mites as well as the morphological identification of the host species. JMąkol performed the morphological analyses of new material of Hexathrombium collected from Peru and type material of Hexathrombium spp. and B. veronicae. JMayoral examined the type material of B. laemostenis and Alhamithrombium. JMąkol and JMayoral wrote the manuscript. All authors reviewed, read and approved the manuscript.

Acknowledgements

We thank Andreas Wohltmann (Ritterhude, Germany) for the discussion on homologies related to the modified termination of tarsus III in microtrombidiid mites. We thank Ryszard Haitlinger (Wrocław University of Environmental and Life Sciences, Poland) who made available to this study the type material of He. abirami, He. lubomirae, He. mamerti, He. marittae and B. veronicae. We thank Franz Wachtel (Grünwald, Germany) and Miriam Steinherr (Augsburg, Germany) for their assistance in collecting T. fulgida in Panguana, Peru.

Furthermore, we thank Diana Silva Dávila (Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Lima, Peru) for her cooperation and the Peruvian authority Servicio Nacional Forestal y de Fauna Silvestre (SERFOR) for issuing the collecting (# 007-2014-SERFOR-DGGSPFFS) and exporting (# 0001757-SERFOR) permits. We are thankful to Maciej Skoracki (Adam Mickiewicz University, Poznań, Poland) for bringing to Poland the Peruvian Hexathrombium from the collection in Germany. Finally, we thank Piotr Daszkiewicz (Muséum national d’Histoire naturelle, Paris, France), Jenny Foster (CSIRO Publishing, Australia) and Camille Locatelli (Royal Belgian Institute of Natural Sciences, Brussels, Belgium) for their help in determining the exact dates of publication of the journal issues containing the descriptions of Hexathrombiini.

Availability of data and material

All data generated or analysed during this study are included in this published article. The type material examined has been loaned from museum institutions. The non-type material of Hexathrombium abirami collected from Peru along with host specimen is stored in the collection of the Department of Invertebrate Systematic and Ecology, Wrocław University of Environmental and Life Sciences, Poland.

Disclosure statement

No potential conflict of interest was reported by the author(s).