The Wasps (Hymenoptera) from Lower Cretaceous Lebanese and Spanish Ambers

Abstract

Hymenoptera is the fourth-most diverse insect order today, including wasps, bees, bumblebees, and ants. They show a wide panoply of modes of life, such as herbivory, predation, parasitoidism, pollination, and eusociality. This group also includes a great number of extinct species from both amber and compression outcrops. Hymenopterans probably originated in the Paleozoic, although their oldest record is from the Middle or Late Triassic, and their diversity expanded since the Cretaceous. Here, we present a review of the Hymenoptera in Lower Cretaceous ambers from Lebanon (Barremian) and Spain (Albian), which is pivotal for the study of hymenopteran evolution. Hymenoptera in Lebanese ambers are represented by 32 species in 22 genera within 15 families, while in Spanish ambers, they correspond to 49 species in 40 genera within 18 families. Most of these species belong to the ‘Parasitica’, and only a few species have been assigned to the Aculeata. The group ‘Symphyta’ is represented by one species in Spanish amber. The paleobiogeography and possible paleobiologies of the species in these ambers are reviewed. Furthermore, checklists for all Hymenoptera species in Lebanese and Spanish ambers are provided.

1. Introduction

Hymenoptera are holometabolous insects, including wasps, bees, bumblebees, and ants [1], corresponding to the fourth-most diverse insect order, accounting for more than 150,000 living species [2]. The presence of hamuli, tiny hooks on the anterior margin of hind wings that allow their coupling with the forewings, is the main anatomical characteristic of Hymenoptera [3]. The ovipositor in some groups representing the Aculeata has evolved into a venomous sting [3,4]. Hymenopterans have a wide distribution and show a panoply of biologies, such as herbivory, predation, parasitoidism, pollination, and eusociality [1]. Phylogenetic studies have placed Hymenoptera as a sister group to the rest of the holometabolous insects [5]. The groups ‘Symphyta’ and Apocrita have been historically differentiated, the latter characterized by a narrowing (called petiole) between the first (fused to the thorax) and second segments of the abdomen [6]. Within Apocrita, ‘Parasitica’ and Aculeata have been distinguished, the latter characterized by the presence of a sting in the females [6]. However, both ‘Symphyta’ and ‘Parasitica’ have been recognized as paraphyletic groupings [6]. The ‘Parasitica’ were grouped together due to their parasitoid biology; however, not all members are parasitoids, and some groups of Aculeata also show this peculiar lifestyle [7].

With more than 3,500 known extinct species, Hymenoptera is one of the insect groups with a greater fossil diversity [3]. The oldest representative dates back to the Middle or Late Triassic, although molecular analyses point out that the group could have originated in the Carboniferous and diversified before the Triassic [7]. Hymenoptera are one of the most abundant and diverse groups of insects found in amber, probably linked to their small size and habitats close to resiniferous trees, thus facilitating their entrapment in resin. Bees and ants, keystone insects in current ecosystems, probably emerged during the Early Cretaceous and diversified during the Late Cretaceous, simultaneously with the radiation of angiosperms [1,7], but still relatively rare in Cretaceous ecosystems [8]. The evolutionary history of the panoply of modes of life present in Hymenoptera is hitherto mostly unknown, and the study of extinct families is crucial to better understanding their present diversity. Cretaceous ambers are an excellent source of information for fossil hymenopterans, providing keys to a changing world that transitioned from ecosystems dominated by gymnosperms to angiosperms during the so-called Angiosperm Terrestrial Revolution [9].

Cretaceous ambers, linked to the Cretaceous Resinous Interval [10], are an important source of information on fossil Hymenoptera as they have provided numerous specimens belonging to diverse families [11,12]. Several Upper Cretaceous ambers have yielded abundant hymenopterans, such as the lower Cenomanian Kachin Burmese amber [13]. However, information on wasps from the Early Cretaceous is more restricted. They are represented from several compression outcrops, limiting the anatomical observations due to preservation [14,15]. Their record in Lower Cretaceous ambers is present in small number in ambers from Congo, Myanmar (Hkamti), and Japan [16,17,18]. In contrast, hymenopterans are highly numerous and diverse in Lebanese and Spanish ambers, highlighting their relevance and making them fundamental for the study of hymenopteran evolution. Here, we present a review of the Hymenoptera in both Lebanese and Spanish ambers, including checklists of described species and discussing the paleodiversity, paleobiogeography, and paleobiology.

2. Geological Settings

Amber has been found in more than 450 outcrops in Lebanon, with a timespan ranging from the Late Jurassic (Kimmeridgian) to the Late Cretaceous (Cenomanian), but bioinclusions have been only discovered in amber of 30 outcrops, all of them from the Barremian [19,20,21]. Most Lower Cretaceous ambers from Lebanon are found in the Sandstone of the Lebanon Unit, also known as the “Grès du Liban” Alloformation [19]. Amber (of the same early Barremian age) is found in thin levels of dark shales together with lignite and plant remains in three depositional intervals of the “Grès du Liban” [19,22]. The dating of these depositional intervals ranges from early to late Barremian based on charophytes, foraminifers, rudists, and echinoids [22]. It is considered that the resin pieces from the lower depositional interval underwent short-distance transport before burial [19], i.e., parautochthony. The remaining amber material found in mid- and upper depositional intervals was reworked in estuarian or margin-littoral shelves. The paleoenvironment of the amber outcrops has been inferred as dense resiniferous forests in a fluvial system with a marine influence under a warm and humid climate [19,22]. Until now, hymenopterans have been identified in amber from 17 outcrops in Lebanon (Figure 1A), being abundant in ambers from Bcharreh, Baskinta, Bouarij, Hammana-Mdeyrij, Ain Dara, and Jezzine. The relative rarity of hymenopteran from the remaining fossiliferous outcrops is certainly due to undersampling, as most of these outcrops have been visited once or a few times.

The Iberian Peninsula is also rich in amber outcrops. More than 150 possible amber deposits have been reported, but the presence of amber has been only confirmed in 67 outcrops from Spain and nine from Portugal. The oldest amber from the Iberian Peninsula is from the Triassic (Ladinian–Rhaetian) of Alicante Province [23]. There are a few Upper Cretaceous ambers from Spain, although most of the amber-bearing outcrops are dated as Early Cretaceous [23]. The Cretaceous amber outcrops from the Iberian Peninsula correspond to the western (Lusitanian Basin), northern (Central Asturian Depression and Basque Cantabrian Basin), and eastern (Maestrazgo Basin) coasts of the ‘mid’-Cretaceous Iberia Island. They are considered parautochthonous, and the resin depositional environments are inferred as deltas, estuaries, or coastal swamps ranging from humid to arid climatic contexts [23,24,25]. Bioinclusions have been found in amber from 12 outcrops of the Iberian Peninsula from the early Albian to the early Cenomanian [23,24,25,26,27]. Among them, the richest in bioinclusions are El Soplao, Peñacerrada I, San Just, and Ariño [23,26]. Hymenopterans have been found in ambers from nine outcrops so far (Figure 1B).

3. Hymenoptera Paleodiversity in Lebanese and Spanish Ambers

3.1. Lebanese Ambers

Hymenoptera in Lebanese ambers are represented by 32 species in 22 genera within 15 families (Appendix A). Eight of the recorded families are extinct and restricted to the Cretaceous: †Protoitidae, †Spathiopterygidae, †Gallorommatidae, †Archaeoserphitidae, †Serphitidae, †Maimetshidae, †Stigmaphronidae, and †Holopsenellidae. Most of the species belong to the ‘Parasitica’ (78%), and Aculeata only correspond to seven species (Figure 2A, 3). The outcrops providing a higher number of species are Hammana-Mdeyrij and Bcharreh. Interestingly, all of the recorded species are only present in their type locality; therefore, there are no co-occurrences at the species level. There is only one genus identified from two outcrops, the genus Protoita from Hammana-Mdeyrij and Roum-Aazour-Homsiyyeh [28]. The most diverse family is the group of tiny chalcidoid wasps †Protoitidae (35% of the total species), followed by Evaniidae, †Serphitidae, and Scolebythidae.

The taxonomy of the hymenopterans from Lebanese ambers is mostly stable, and only a few taxonomic changes have been applied. The species Cretaxenomerus jankotejai Nel and Azar, 2005 was originally placed in the family Scelionidae [29], but an extensive study on chalcidoid wasps from Lebanese ambers has allowed transferring this species to the recently erected family †Protoitidae [28]. The monotypic genus Eovernevania was considered to be a junior synonym of Cretevania based on the lack of important anatomical differences [30], thus resulting in the species Cretevania cyrtocerca (Deans, 2004) being derived from Hammana-Mdeyrij amber. The species Aphelopus palaeophoenicius Olmi, 2000 was transferred to a new genus in its own new subfamily, turning into Archaeodryinus palaeophoenicius (Olmi, 2000) based on its anatomical differences with the rest of the dryinids [31]. The species Holopsenella primotica Engel, Ortega-Blanco and Azevedo, 2016 was first considered the only member of its own subfamily within Bethylidae [32], the holopsenellines probably being the earliest diverging bethylids [33]. However, the status of this subfamily was raised into a family, †Holopsenellidae, and placed as Incertae sedis in Aculeata [34].

Apart from the mentioned families, new specimens under study have been preliminarily assigned to the families †Baissidae, Braconidae, Megaspilidae, Mymarommatidae, and Chrysididae.

3.2. Spanish Ambers

Hymenoptera in Spanish ambers correspond to 49 species in 40 genera within 18 families (Appendix B). Among them, there are eight extinct families whose record is limited to the Cretaceous: †Spathiopterygidae, †Alavarommatidae, †Gallorommatidae, †Proterosceliopsidae, †Serphitidae, †Maimetshidae, †Radiophronidae, and †Stigmaphronidae. Similarly to Lebanese amber, most of the species belong to the ‘Parasitica’ (88%), while only five species form part of the Aculeata (Figure 2B, 3). Interestingly, there is one species, represented by the holotype, belonging to the sawfly family Anaxyelidae [35]. The ambers that have yielded the highest number of specimens are Peñacerrada I (782 specimens), El Soplao (276), San Just (111), and Ariño (34), although most of them are pending to be studied. Peñacerrada I is the type locality of 39 species, followed by San Just, type locality of 7 species. It is important to note that there are five co-occurrences at the species level among Spanish ambers: Megalava truncata Perrichot, 2009 (Megalyridae, in Peñacerrada I and El Soplao, [36,37]), Alavaromma orchamum (†Alavarommatidae, in Peñacerrada I and San Just, [38]), Cretaceomma turolensis (Ortega-Blanco, Peñalver, Delclòs and Engel, 2011) (†Gallorommatidae, in San Just and possibly in Ariño, [26,38]), Archaeromma hispanicum Ortega-Blanco, Peñalver, Delclòs and Engel 2011 (Mymarommatidae, in Peñacerrada I and El Soplao, [38]), and Burmaphron jentilak Ortega-Blanco, Delclòs and Engel, 2011 (†Stigmaphronidae, in Peñacerrada I and San Just, [39]). Furthermore, the genus Cretevania (Evaniidae) is present in the ambers from El Soplao, Peñacerrada I, San Just, and Arroyo de la Pascueta [30,40], and the genus Serphites (†Serphitidae) has been identified in the ambers from Peñacerrada I, San Just, and Ariño [26,41]. The most abundant and diverse wasp family in Spanish ambers is Scelionidae, accounting for 17% of the total species. The families †Stigmaphronidae, Evaniidae, and †Serphitidae are also highly diverse.

Some hymenopteran taxa from Spanish ambers have undergone taxonomic changes. The species Iberopria perialla Engel, Ortega-Blanco, and Delclòs, 2013 was originally assigned to Diapriidae [42], later it was transferred to †Cretacoformicidae [43], and subsequently, this family was synonymized under †Trupochalcididae, although returning I. perialla to Diapriidae [44]. The species Galloromma turolensis Ortega-Blanco, Peñalver, Delclòs and Engel, 2011 (†Gallorommatidae) [38] was transferred to the new genus Cretaceomma and is also present in Lebanese amber [45]. The genus Proterosceliopsis, described from a specimen of Peñacerrada I amber, was first considered to be a member of Scelionidae [46] but was later placed in its own family, †Proterosceliopsidae, based on their differential anatomical characteristics [47]. Both families †Radiophronidae and †Stigmaphronidae, the former described from specimens in Peñacerrada I amber, were placed in the superfamily Ceraphronoidea [39,48], although their relationships with this superfamily have been questioned, and they might belong to Aculeata [49]. The species Lancepyris alavaensis Ortega-Blanco & Engel, 2013 (Bethylidae) was transferred to the new genus Zophepyris, similarly to the species Embolemus periallus Ortega-Blanco, Delclòs and Engel, 2011 (Embolemidae), which was assigned to the genus Ampulicomorpha, clarifying the relationships within their corresponding families [32,50,51].

The families Baeomorphidae, Chrysididae, Sapygidae, Sierolomorphidae, and Tiphiidae have been preliminarily identified and the study of the specimens is in progress.

4. Discussion and Conclusions

Lebanese and Spanish ambers are among the most important sources of knowledge of fossil Hymenoptera based on the exceptional preservation of the specimens and their dating as Early Cretaceous (Figure 3), providing information from a crucial epoch for the Hymenoptera just prior to the Angiosperm Terrestrial Revolution [9,52]. ‘Symphyta’ are rare in Cretaceous ambers in comparison to the Apocrita. These wasps are not present yet in Lebanese ambers, and they are represented in Spanish ambers by only one species [35]. Most of the species in Lebanese and Spanish ambers are ‘Parasitica’, and the Aculeata correspond to only a few specimens (Figure 2). Wasps belonging to this group are represented by limited species in New Jersey, Taymyr, and Canadian ambers. This is surprising in comparison to Kachin amber, where Aculeata include more than half of the whole studied hymenopteran diversity [13,34]. This fact may be explained by a research bias in which the study of hymenopterans from Kachin amber is focused on Aculeata, where the families Bethylidae, Dryinidae, Embolemidae, Formicidae, and Vespidae are highly diverse [13]. However, it is also possible that the differential diversity is linked to paleoenvironmental or paleobiogeographical factors, resulting in different wasp communities. Regarding the most diverse hymenopteran families today, Ichneumonidae are absent in Lebanese and Spanish ambers, while Braconidae are only represented by a few species [53].

Five co-occurrences of hymenopterans at the species level between Spanish amber outcrops have been reported. The same species in different Spanish ambers have also been noticed for other insect groups, such as barklice, beetles, and midges [54,55,56]. These taxonomical coincidences may be linked to a great extension of the resiniferous forests along the northern and eastern coasts of the Iberia Island during the Albian, allowing entomofaunal dispersal. Interestingly, no hymenopteran species co-occurrences have been reported from Lebanese amber despite their close geographical and temporal distances, probably due to a research bias. In Lebanese and/or Spanish ambers, wasp genera with a wide distribution during the Cretaceous have been described, such as Cretevania, Archaeromma, and Serphites, all of them present in ambers from several distant provenances [30,38,41]. The genera Eosyntexis, from Spanish amber, and Cretevania, from both Lebanese and Spanish ambers, are also present in compression outcrops [30,35], evidencing that they thrived in diverse paleoenvironments and regions.

As discussed in previous articles, the entomofaunas from Lebanese and Spanish ambers shared similarities, as 20 insect genera co-occurrences have been reported [57,58,59]. In the case of the Hymenoptera, five genera have been identified from both provenances (

Table 1. Co-occurrences at the genus level of Hymenoptera between Lebanese and Spanish ambers with other Cretaceous ambers. Lebanon–Barremian, Congo–Aptian, Spain–Albian, Myanmar (Hkamti)–Albian, Myanmar (Kachin)–Cenomanian, France (Charentes)–Cenomanian, Russia (Nizhnyaya Agapa)–Cenomanian, USA (New Jersey)–Turonian, Japan (Iwaki)–Coniacian, Japan (Kuji)–Coniacian/Santonian, Russia (Yantardakh)–Santonian, Canada–Campanian.

Family	Genus	Lebanon	Congo	Spain	Myanmar (Hkamti)	Myanmar (Kachin)	France(Charentes)	Russia (Nizhnyaya Agapa)	USA (New Jersey)	Japan (Iwaki)	Japan (Kuji)	Russia (Yantardakh)	Canada
†Spathiopterygidae	Mymaropsis	X		X
Evaniidae	Cretevania	X	X	X		X		X				X
	Iberoevania			X		X
†Gallorommatidae	Cretaceomma	X		X
	Galloromma			X		X	X	X
Mymarommatidae	Archaeromma			X		X			X	X	X	X	X
†Proterosceliopsidae	Proterosceliopsis			X		X
Scelionidae	Proteroscelio	X				X							X
†Archaeoserphitidae	Archaeoserphites	X				X
†Serphitidae	Aposerphites			X								X
	Microserphites	X		X				X
	Serphites			X		X	X		X			X	X
†Maimetshidae	Iberomaimetsha			X								X
†Stigmaphronidae	Burmaphron			X		X
	Elasmophron			X					X
	Hippocoon			X								X
	Tagsmiphron			X					X				X
	Libanophron	X		X
Embolemidae	Ampulicomorpha			X	X	X
†Holopsenellidae	Holopsenella	X			X	X

): Cretaceomma, Cretevania, Libanophron, Microserphites, and Mymaropsis. This is surprising based on the geographical distance and the temporal separation of about 20 myr. Similar paleoenvironmental factors in these regions might explain the taxonomic coincidences, and land ‘bridges’ in western Tethys could facilitate the displacement of insect fauna, usually with low dispersal abilities [59]. The high co-occurrence of genera between Lebanese (four genera) and Spanish (eight genera) ambers with Kachin amber (Table 1) is thought-provoking. Furthermore, the presence of the same genera in Spanish ambers and New Jersey (four genera) and Yantardakh (six genera) ambers would not be expected, considering the great geographical and temporal separation (Table 1). However, Cretaceous hymenopteran biogeography is still not well known, and more information is required to understand the factors facilitating or hindering the long-distance movement of wasps during this period.

Hymenoptera were abundant and diverse in the Early Cretaceous resiniferous forests of Iberia Island and Levantine regions, occupying key ecological niches and showing a panoply of modes of life, probably mirroring those living in present-day ecosystems. The only representative of ‘Symphyta’ in Spanish amber, Eosyntexis parva Ortega-Blanco, Rasnitsyn and Delclòs, 2008, could lay eggs in burnt wood, similar to the living species of the family [35]. The rest of the extant families present in Lebanese and Spanish ambers are parasitoid, including the few aculeate families. Therefore, it is possible that their members in these ambers were also parasitoid. However, the wide diversity of modes of life present in Hymenoptera [1,7], and considering the high number of different types of parasitoidism behaviors and secondary reversals [60], makes it risky to assume a certain lifestyle for extinct species. Most of the extinct hymenopteran families, such as †Spathiopterygidae, †Serphitidae, †Radiophronidae, and †Stigmaphronidae, have been considered parasitoid based on phylogenetic inference [39,41,48,61], but an extensive morphological study is still required to better understand their possible paleobiologies.