Tenuipalpus Sensu Lato Donnadieu (Acari: Prostigmata: Tenuipalpidae); New Species Groups, a New Species, and Keys to the World Species

Simple Summary Castro et al. divided the genus Tenuipalpus into two groups, i.e., Tenuipalpus sensu stricto and Tenuipalpus sensu lato. Four new species groups of the Tenuipalpus sensu lato group are proposed in this study, considering the total number of dorsal opisthosomal setae. Additionally, diagnostic keys to new species groups and the world species of Tenuipalpus sensu lato are developed. Abstract Four new species groups of the Tenuipalpus sensu lato group are proposed in the present study based on the total number of dorsal opisthosomal setae, namely, carolinensis with ten pairs of setae (214 species), dubinini with nine pairs of setae (33 species), granati with eight pairs of setae (29 species), and barticanus with seven pairs of setae (7 species) Additionally, diagnostic keys to species groups and 273 species of the Tenuipalpus sensu lato are provided. Three species, T. lustrabilis Chaudhri, T. guptai Sadana and Gupta, and T. solanensis Sadana and Gupta, are synonymized with T. punicae Pritchard and Baker. One species, T. rodionovi Chalilova, is suggested as a junior synonym of T. granati Sayed, and eight species, T. chiococcae De Leon, T. costarricensis Salas and Ochoa, T. ephedrae Livschitz and Mitrofanov, T. molinai Evans, T. santae Manson, T. simplychus Cromroy, T. tetrazygiae De Leon, and T. oxalis (Flechtmann), belonging to the carolinensis species group, are not included in the key. Furthermore, a new species of Tenuipalpus sensu lato, T. jazanensis sp. nov., is described and illustrated based on females collected from the Chamaerops spp. (Arecaceae).

Collyer [11] made the world key of 102 Tenuipalpus species.Additionally, some local keys were developed over time by Meyer [10], which included around 90 species from Africa; Baker and Tuttle [9] included 20 species from Mexico; Al-Gboory [12] included seven species from Iraq; Khanjani et al. [13] included nine species from Iran; Castro and Feres [14] included 12 species from Brazil; and Xu et al. [15] included 25 species from China.
For more than three decades, Tenuipalpus species groups, as proposed by Baker and Tuttle [9] and Meyer [10], were consistent.However, recently, Castro et al. [1] divided the genus into two groups by using a combination of characters: Tenuipalpus sensu stricto (36 species), with a pair of lateral projections associated with setae c3 and only one pair of setae 4a, and Tenuipalpus sensu lato (287 species), without a lateral projection associated with setae c3 and one to four pairs of setae 4a.Also, a world key to the species of Tenuipalpus sensu stricto was provided [1,16].However, no diagnostic key to the world species of Tenuipalpus sensu lato has been developed yet.
The aims of the present study were to (i) classify all species of Tenuipalpus sensu lato into new species groups based on distinct morphological characters; (ii) develop diagnostic keys to species groups and 273 species of the Tenuipalpus sensu lato; and (iii) examine specimens of Tenuipalpus species collected from different regions of Saudi Arabia.

Materials and Methods
The published taxonomic literature of all known 287 species belonging to the Tenuipalpus sensu lato group was collected using different resources: the Acarology Laboratory King Saud University, Google Scholar, ResearchGate, and different acarological journals, and through personal communication (Dr.Qing Hai Fan, Fujian Agriculture and Forestry University, China; and Dr. Elizeu B. Castro, São Paulo State University, São José do Rio Preto campus, São Paulo, Brazil).Diagnostic keys to species groups and 273 species are provided.All specimens of the genus that were collected by the Acarology lab have been examined.The mounted specimens of Tenuipalpus species were examined and identified under a phase contrast microscope (DM2500, Leica, Wetzlar, Germany).Different mite body parts were pictured using an Auto-Montage software system v4.0.1.1 (Syncroscopy, Cambridge, UK) and drawn with Adobe Illustrator v27.7 (Adobe System Inc., San Jose, CA, USA).All measurements are in micrometers.The terminology used in the research follows that of Mesa et al. [2].The specimens were deposited at the King Saud University Museum of Arthropods (KSMA, Acarology Section), Department of Plant Protection, College of Food and Agriculture Sciences, King Saud University, Riyadh, Saudi Arabia.

Results
The Tenuipalpus sensu lato group was divided into four species groups based on the total number of dorsal opisthosomal setae, namely, the carolinensis group-with ten pairs of setae (214 species), the dubinini group-with nine pairs of setae (33 species), the granati group-with eight pairs of setae (29 species), and the barticanus group-with seven pairs of setae (seven species).This proposed division did not consider whether a specific setae was absent or not (i.e., any setae among the opisthosomal setae can be absent).The diagnostic keys to those four new species groups and 273 species of Tenuipalpus sensu lato were also developed.

Remarks:
The new species, Tenuipalpus jazanensis sp.nov., belongs to the carolinensis species group.This species group is distinguished from other species groups of Tenuipalpus sensu lato by having ten pairs of opisthosomal setae.Tenuipalpus jazanensis sp.nov resembles T. pareriophyoides Meyer and Gerson and T. eriophyoides Baker by having more than three pairs of intercoxal setae 4a, one pair of setae 3a, dorsal setae lanceolate serrate and dorsum with irregular striate laterally.The new species differs from T. pareriophyoides and T. eriophyoides by the following characters; prodorsum medially with transverse striations; area in between setae c1, d1 and d3 with few reticulations (prodorsum medial area mostly smooth or punctate; area in between setae c1, d1 and d3 with rugose patten or striate); genu I with three setae (genu I with two setae); setae g and ag smooth (setae g and ag serrate in T. pareriophyoides; setae g and ag serrate in T. eriophyoides).
Different species groups were proposed based on the number of dorsocentral setae or dorsolateral setae [8][9][10].According to the number of dorsolateral setae, two species groups, caudatus and proteae, based on the presence and absence of setae f2 (with seven and six pairs of dorsolateral setae), respectively.Later, these two species groups were divided into species subgroups based on the number intercoxal setae 3a and 4a were recognized [9,10].Also, the character of dorsocentral and dorsolateral setae have been used as a first couplet in the different keys to classify the Tenuipalpus species (Al-Gboory [12]; Khanjani et al. [13]; Castro et al. [16]; Xu et al. [15]).The literature of 287 species of Tenuipalpus sensu lato signified the importance of dorsal opisthosomal setae as a prominent diagnostic morphological character.However, using the presence and absence of dorsolateral setae f2 (seven and six pairs of setae, respectively) could not be helpful, because some species (i.e., T. clematidos Wang, T. flechtmanni Mesa, Moraes, and Ochoa, T. isabelae Mesa, Moraes, and Ochoa, and T. salicis Al-Gboory) have six of dorsolateral setae (f2 present), but the dorsolateral setae (d3) is absent.Hence, those species can not be placed in any species groups that proposed Baker and Tuttle [9] and Meyer [10] because of these grouping caudatus and proteae is based on presence and absense of setae f2.However, some previous works are considering the number of dorsolateral setae to distinguish these two species groups, regardless of which dorsolateral seta is absent.For example, Mahdavi and Asadi [27] included two species (T.clematidos Wang and T. salicis Al-Gboory) in the proteae species group, which have setae f2 present.Therefore, we found that using the total number of opisthosomal setae is proper for dividing species groups, while the absence or presence of certain opisthosomal setae may be used for species differentiation in diagnostic keys.Hence, in this study, the four new species groups were proposed based on the number of opisthosomal setae.

Further Notes on the Poorly Described and Illustrated Species of the Species Group Carolinensis
The following remarks and additional notes are about those eight species belonging to the species group carolinensis, which were not included in the key due to poor/incomplete descriptions and illustrations.Their related species and a possible place in the diagnostic key are provided as follows: Tenuipalpus chiococcae De Leon The species T. chiococcae was originally described as close to T. pigrus Pritchard and Baker [17].The recent classification by Castro et al. [1] placed T. pigrus in Tenuipalpus sensu stricto since this species bears a pair of lateral body projections associated with setae c3.The result of our study placed T. chiococcae among five species in the diagnostic key, i.e., T. aurantiacus Wang, T. angolensis Meyer, T. nigerianus Meyer, T. spatulatus Wang, and T. obvelatus Wan.
Tenuipalpus costarricensis Salas and Ochoa Previously, T. costarricencis was considered close to T. granati Sayed [18].However, in our study T. granati is placed in the group granati, while T. costarricensis came closer to three species; T. eucleae Meyer, T. garciniae Meyer and Bolland, and T. indicus Maninder and Ghai in the species group carolinensis.

Tenuipalpus ephedrae Livschitz and Mitrofanov
For the species T. ephedrae, the morphological characters were obtained from a poor redescription [19], and the original description was not found.The taxonomic information available in the redescription only helped to place this species in the group carolinensis.

Tenuipalpus molinai Evans
The species T. molinai was originally described as close to T. pedrus Manson [20].The closely related T. pedrus Manson had been transferred to the genus Colopalpus Pritchard and Baker, previously [28].However, the available morphological characters indicate that the species T. molinai belongs only to the species group carolinensis, but could not be assigned in the key.

Tenuipalpus oxalis Flechtmann
The species T. oxalis is poorly described and illustrated, and the related species was not provided [21].The available morphological characters helped to designate the species only to the level of the species group carolinensis.

Tenuipalpus santae Manson
The species T. santae is morphologically close to T. celtidis Pritchard and Baker in the original description [22].Tenuipalpus santae could not be placed due to missing leg cheatotaxy and other diagnostic characters.

Tenuipalpus simplychus Cromroy
The species T. simplychus was described as closely related to T. knorri Baker and Pritchard in the original description [23].Due to missing leg chaetotaxy information, T. simplychus could not be assigned a certain place in the diagnostic key.

Tenuipalpus tetrazygiae De Leon
The species T. tetrazygiae, it was distinguished by the author from other described species of that time by the shape of dorsocentral setae and dorsum covered with irregular ridges [17].Although this species has been placed in the caroliensis group, no certain place could be identified in the diagnostic key.

Synonymy of Some Species of the Carolinensis Species Group
The species T. lustrabilis was previously reported as a suspected junior synonym of T. punicae Pritchard and Baker [2,13].We reviewed the original description and illustration [29] as well as the characters of T. lustrabilis in the published key by Meyer [8].T. lustrabilis is hereby synonymized with T. punicae based on the number of shared characteristics, i.e., leg chaetotaxy, palp segmentation, shape and number of dorsal setae, pattern of dorsal reticulations, as well as its geographic distribution (Pakistan) and host plant (Punica granatum).
Similarly, the species T. guptai Sadana and Gupta was also suggested as a junior synonym of T. solanensis Sadana and Gupta [2,13].We found that both species share most of their morphological features except for the number of setae on tarsi I-II (5-5 in T. guptai vs 7-7 in T. solanensis).This character has been commented to be a miscalculation [13], especially that T. guptai was described based on a single holotype female while T. solanensis only from three females.Moreover, both species were described based on specimens collected from the same host plant (P.granatum), the same type locality (India), on the same collection date (22-VI-1981), and have been mounted on the same slide (slide#91) [30].
Interestingly, the related species of T. solanesis is T. lustrabilis, which is declared as junior synonym of T. punicae.A detailed comparison of available description for both of these species show they are very similar; sharing leg chaetotaxy, palp segmentation, shape and number dorsal setae, pattern of dorsal reticulations, and host plant.Hence, the two species (T.guptai and T. solanensis) are also synonymized with T. punicae.
Tenuipalpus rodionovi Chalilova was described poorly without illustrations [31].Therefore, it is neither assigned to any of the four species groups and not placed in the diagnostic keys.However, it was mentioned in the original description that it resembles three species: T. granati Sayed, T. zhizhilashviliac Reck, and T. kobachidzei Reck.The latter two species belong to the species group carolinensis, while the former one belongs to the granati new species group.Pritchard and Baker [32] and Wainstein [33] suspected this species as a junior synonym of T. granati.There is a need to check the type specimens of this species to validate its status.Hence, T. rodionovi is considered as a suggested synonym of T. granati until further studies are made.

Figure 3 .
Figure 3. Tenuipalpus jazanensis sp.nov.Female.Palp.Scale bar: 25 μm.Males and immature.Unknown Type Materials.Holotype female, four paratype females, from Chamaerops sp.(Arecaceae) Wadi Baydh, Jazan, 17°37.559'N, 42°22.196'E, 10 October 2020, coll.J. H. Mirza, H.M.S. Mushtaq and E.M. Khan.Etymology: The specific epithet (jazanensis) is derived from the type region, Jazan.Remarks:The new species, Tenuipalpus jazanensis sp.nov., belongs to the carolinensis species group.This species group is distinguished from other species groups of Tenuipalpus sensu lato by having ten pairs of opisthosomal setae.Tenuipalpus jazanensis sp.nov resembles T. pareriophyoides Meyer and Gerson and T. eriophyoides Baker by having more than three pairs of intercoxal setae 4a, one pair of setae 3a, dorsal setae lanceolate serrate and dorsum with irregular striate laterally.The new species differs from T. pareriophyoides and T. eriophyoides by the following characters; prodorsum medially with transverse striations; area in between setae c1, d1 and d3 with few reticulations (prodorsum medial area mostly smooth or punctate; area in between setae c1, d1 and d3 with rugose patten or striate); genu I with three setae (genu I with two setae); setae g and ag smooth (setae g and ag serrate in T. pareriophyoides; setae g and ag serrate in T. eriophyoides).

Figure 3 .
Figure 3. Tenuipalpus jazanensis sp.nov.Female.Palp.Scale bar: 25 µm.Males and immature.Unknown Type Materials.Holotype female, four paratype females, from Chamaerops sp.(Arecaceae) Wadi Baydh, Jazan, 17 • 37.559' N, 42 • 22.196' E, 10 October 2020, coll.J. H. Mirza, H.M.S. Mushtaq and E.M. Khan.Etymology: The specific epithet (jazanensis) is derived from the type region, Jazan.Remarks:The new species, Tenuipalpus jazanensis sp.nov., belongs to the carolinensis species group.This species group is distinguished from other species groups of Tenuipalpus sensu lato by having ten pairs of opisthosomal setae.Tenuipalpus jazanensis sp.nov resembles T. pareriophyoides Meyer and Gerson and T. eriophyoides Baker by having more than three pairs of intercoxal setae 4a, one pair of setae 3a, dorsal setae lanceolate serrate and dorsum with irregular striate laterally.The new species differs from T. pareriophyoides and T. eriophyoides by the following characters; prodorsum medially with transverse striations; area in between setae c1, d1 and d3 with few reticulations (prodorsum medial area mostly smooth or punctate; area in between setae c1, d1 and d3 with rugose patten or striate); genu I with three setae (genu I with two setae); setae g and ag smooth (setae g and ag serrate in T. pareriophyoides; setae g and ag serrate in T. eriophyoides).

Table 1 .
List of species not included in the diagnostic key of the new species group carolinensis.