A Rare Cleptoparasitic Bee Tetralonioidella himalayana (Bingham, 1897) (Hymenoptera: Apidae) from India: Review and New Data

Abstract

Tetralonioidella Strand 1914 is a very rare apid genus globally, of which only two species, Tetralonioidella himalayana (Bingham, 1897) and Tetralonioidella tricolor (Lieftinck, 1972), are known from India. They are known to be cleptoparasitic on species of Habropoda Smith, 1854 and Elaphropoda Lieftinck, 1966. During hymenopteran survey in Arunachal Pradesh, we encountered Tetralonioidella himalayana (Bingham, 1897) and observed their behavioral regime, which is very poorly known. The identifying characteristics of both male and female, their foraging behavior, floral preference, distribution pattern, and possible host association have been studied. Exclusive floral association and host specialization are potential contributing factors to the rarity of T. himalayana. Such factors may limit the distribution range of the species. A priori sampling resolution with genetic and demographic exploration is required to evaluate the present status of such bee species.

Tetralonioidella Strand, 1914 is a member of the tribe Melectini, subfamily Apinae, and family Apidae (Hymenoptera: Apoidea). Tetralonioidella currently covers 19 described species exclusively from the Oriental region, ranging from Northern India, Nepal, and China to Thailand, Malaysia, Sumatra, and Java [1]. The representatives of the genus are 8.5–13.5 mm in body length with red, yellow, black, or brown thoracic hairs and orange hairs in tergal bands. Compared to other congeners of the tribe Melectini, they are comparatively slender with marginal cells extended typically just short of the combined length of three submarginal cells without lateral short, dense white pubescence on metasoma fulfilling in the presence of papillae on the distal part of the bare wing, which is characteristic of the tribe. Unlike most cuckoo bees, Tetralonioidella is drastically hairy and can be distinguished by the convex scutellum with a distinctive medial longitudinal carina, a pair of long spines hidden under the long hairs laterally, and a metasoma with uniform, short, appressed hairs [2, 3].

The species was first described from 1 ♀ holotype collected from Kumaon as Melecta himalayana by Bingham in 1897 [4]. Strand erected the genus Tetralonioidella, which was published a month earlier than that of the genus Protomelissa Friese [5]. Consequently, over nomenclatural priority, the valid species now stands as Tetralonioidella himalayana (Bingham, 1897). Lieftinck reported more information about the species in 1929, when he looked at samples from Darjeeling, Kurseong, Sikkim, and Shillong in Meghalaya [6]. T. himalayana was also reported in Nainital, Uttarakhand [7], and Kalimpong, West Bengal [8]. This study is the first to confirm the occurrence of Tetralonioidella himalayana (Bingham, 1897) in Arunachal Pradesh (Fig. 2a).

Fig. 2.

a Updated distribution of Tetralonioidella himalayana in India with new occurrence records from Tawang district, Arunachal Pradesh (present study), b Habropoda cf sinensis foraging on I. coetsa, c Habropoda sp. foraging on Crawfurdia speciosa, d Tetralonioidella. himalayana foraging on I. coetsa, e weighted interactions between the three bees with their respective plant species shows exclusive interactions between T. himalayana and I. coetsa plants. (Habcfsin = Habropoda cf. sinensis, Habsp = Habropoda sp. and Thima = Tetralonioidella himalayana)

The present study on recording bee-plant interactions in different altitudes (ranging from 1130 to 4200 m a.s.l.) and habitat gradients was undertaken in four different areas (Jang: 27.576°N, 91.997°E; Tawang: 27.586°N, 91.855°E; Lumla: 27.533°N, 91.715°E and Zemithang: 27.705°N, 91.739°E) of Tawang district, Arunachal Pradesh, India. The survey was done during April to May (pre-monsoon) and October to November (post-monsoon to pre-winter) in 2019 and 2021. Field studies during 2020 could not be executed due to the restrictions for COVID-19 outbreak. Fiducial timed observations were made on crop and non-crop plants for profiling bee foraging patterns on sunny days from 0800 to 1600 h. The cuckoo bee species, T. himalayana, is very rare in nature and its biology is practically unknown; the range of its geographic distribution and floral associations is still uncertain, and the identification of the species is riddled with several taxonomic emendations over time since most of the data are scatteredly distributed. This work is an effort to collate all the available information in the literature and observational findings from this study to contribute to the present updated knowledge of the species from India [2, 3, 7]. The present study is a contribution to studies on documenting the distribution of hymenopteran fauna from the region [9, 10].

Measurements as following: Full body length (13.18 mm ♂, 11.73 mm ♀); inter-tegular distance (4.12 mm ♂, 3.68 mm ♀); and fore wing length (10.43 mm ♂, 8.81 mm ♀). Both sexes are robust; males are bigger in size and have serrated antennae (Fig. 1a–b). The species exhibits black integument, with face longer than wide and long golden-brown pubescence particularly at the frontal area, upper part of the paraocular region. Clypeus, labrum, base of scape and legs are somewhat shorter. Thorax with comprehensive horizontal blackish or brown pubescent forms a stripe between the tegula (Fig. 1c–d). Scutum densely punctate. T1 and T2 (metasomal terga) sparsely pubescent but apical segments and margins are compactly pubescent without forming bands with median process of sternum 8 apically convex (Fig. 1e–f). Male genitalia is shown in Fig. 1g–h.

Fig. 1.

Tetralonioidella himalayana (Bingham, 1897): a head in frontal view of male, c habitus of male, e dorsal view of male and b head in frontal view of female, d habitus of female, f dorsal view of female, g male genitalia in ventral view, h male genitalia in dorsal view

Habropoda and Elaphropoda are known to be the hosts of Tetralonioidella in Java, Sumatra, Malaysia, and Thailand [6]. Habropoda is the most likely host of Tetralonioidella in Taiwan [2]. Lieftinck reported a common foraging niche for T. himalayana and five other Habropoda species in Uttarakhand, India; among which H. radoszkowskii (Dalla Torre) was the most abundant [7]. According to their pollen-collecting behavior, both the Habropoda species (Habropoda sinensis Alfken and Habropoda sp.) can be defined as flower-buzzing bees as they vibrate their thoracic muscle at a specific frequency clinging to the whole flower to dislodge pollen and hence are called buzz pollinators forming a very critical functional group for unique adaptation for pollination [11, 12]. In our present study, we found two potential hosts, Habropoda cf. sinensis Alfken, 1937 and Habropoda sp., in association with the cuckoo bee (T. himalayana) from Jang, Pangchen valley (Zemithang) and Lumla valley by their overlapping foraging dietary niche and occurrence in a shared altitudinal range.

A graphical representation on observed interactions between the focal bees and their conspecific visited plant species are depicted as in bipartite web from the study region (Fig. 2e). The nodes on the left indicates the bees and boxes on the right represent the visited plant species. The lines connecting the plants and bees (linkages) are the interactions weighted by abundance (no. of visits done by a bee species to their conspecific flowering plant species) (Fig. 2b–d). A combined observation of a total of 272 interactions of both the host and cleptoparasitic bee species among different plants was recorded. The bee species linkage density was frequent in Habropoda sp. (40.44%) followed by Habropoda cf. sinensis (33.82%) and T. himalayana (25.73%), while among plants, I. coetsa received the highest visits (69.11%) followed by S. scandens (18.38%), Crawfurdia speciosa (6.98%) and Impatiens sp. (5.51%). The overall network has a generalized pattern with degree of specialization (H2') 0.354 (the value ranges from 0 to 1, where integer 1 corresponds the highest specialized interaction), and the subjected nestedness metric based on overlap and decreasing fill (NODF) matrix value is 77.7 (where integer 100 denotes a perfectly nested interaction structure). The ecological network pattern for bee plant interactions were analyzed using R (version 4.2.2) statistical data process by using “Bipartite” package [13]. Habropoda bees are found foraging on plants like Crawfurdia speciosa Wall. (Gentianaceae), Impatiens sp. (Balsaminaceae), Isodon coetsa (Buch.-Ham. ex D.Don) Kudô (Lamiaceae) and Senecio scandens Buch.-Ham (Asteraceae); but, T. himalayana foraging is restricted exclusively on I. coetsa (Fig. 2e). Historical records based on the literature and observations from present study give predictive remarks on the host specificity of T. himalayana on I. coetsa. This fundamentally indicates plausible individual specialized fidelity for nectar, particularly sensitivity toward specific floral scents of the plant [14]. It is observed that T. himalayana shows a potential flight period from September to early December in Tawang and needs several Isodon populations for persistence throughout their activity period. The visiting vegetation is highly attractive to the local pollinators of diversified taxa, ranging from several species of hymenopterans, dipterans, and lepidopterans in different habitats and altitudes. T. himalayana, which depends on local plants, is in danger because of careless logging and clearing of weeds along the edges of fields to make room for more crops.

Unlike its hosts, T. himalayana has a shorter foraging bout and higher flower handling time ascending to peak during 1130–1300 h and gradually decreasing afterward in our study region. The only floral reward cleptoparasitic bees rely on is nectar since their development involves devouring the stored pollen for the host’s larvae [1]. The observed five T. himalayana populations across the study area found irrespective of their habitats, but the presence of the host plant species was critical for their occurrence. Cleptoparasitic bees are poorly understood, morphologically distinct from other bees, and account for approximately 20% of total bee species. The abundance and diversity of cleptoparasitic bees indicate a healthy bee community since they serve as an indicator guild and stabilizing factor to maintain bee alpha diversity because they are the first to respond to environmental disturbances; thus, it might be assessed as part of the bee monitoring regime [15].

Despite the lack of a baseline database for many species, combining the existing data with the latest tools allows for prioritizing environments for protection, identifying endemism gaps, and maximizing biodiversity. The present observations provide fresh insights into the knowledge of the natural history of T. himalayana which were hitherto unknown; further studies on the reproductive behavior and population status are required to comprehend the species. Because this is not only a single species, but also contributes to a network of ecological interactions of different groups where one missing link can trigger a domino effect in altering ecosystem services [16]. The discovery of the cuckoo bee species and relevant baseline information on its natural history could prove beneficial for stakeholders as native people play a critical role in the conservation of native pollinators and biodiversity [17]. The importance of studying interaction patterns of plants and pollinators and how parasitism, mutualism, and dominance of some species in ecological communities in natural habitats alter the distribution ranges concerning species at a micro-level is important in understanding the phenological shift and temporal mismatch at a spatiotemporal scale [18, 19]. Host–plant distribution modeling can subsidize targeted sampling regimes in future research on the distribution pattern of bees, and monitoring phenological shifts will be useful for climate change resilience studies [20]. The present study signifies the importance of studying specialized host–plant interactions at a local scale to address the Eltonian shortfall (addressing lack of knowledge on inter- or intraspecific interactions) and Wallacean shortfall (addressing the paucity of information on species distribution) as well as the relevance of contributing to the current effect of climate change on plant and pollinator communities.

Declarations

Conflict of interest

The authors declare no competing interest.