Cretaceous Research 117 (2021) 104612

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Cretaceous Research
journal homepage: www.elsevier.com/locate/CretRes

Termite communities and their early evolution and ecology trapped in

Cretaceous Amber
Zhipeng Zhao a, b, Chungkun Shih b, c, Taiping Gao b, Dong Ren b, *
a
Fishery Resource and Environment Research Center, Chinese Academy of Fishery Sciences, Beijing, 100141, China
b
College of Life Sciences and Academy for Multidisciplinary Studies, Capital Normal University, Beijing, 100048, China
c
Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, DC, 20013-7012, USA

a r t i c l e i n f o a b s t r a c t

Article history: Termites are estimated to have originated in the Late Jurassic with an evolutionary radiation in the Early
Received 11 March 2020 Cretaceous. This rapidly evolved eusocial group, having close associations with the ecological commu-
Received in revised form nities and surrounding environments, established delicate microecosystems in the Cretaceous terrestrial
14 July 2020
ecosystems. Cretaceous amber with well-preserved clues of natural history provide a “time portal” for
Accepted in revised form 22 July 2020
Available online 18 August 2020
paleoentomologists to study the ecosystems in this geological age. Herein, we review the termites and
related inclusions reported from Cretaceous amber. Studies on fossil termites have been active in the last
two decades with the discoveries of diverse taxa, early eusociality, feeding habits, termitophiles, etc.
Keywords:
Termitoidae
Termite interactions have been demonstrated by either co-embedded specimens or specialized mor-
Cockroach phologies known from the extant evidence. The termites and associated communities in Cretaceous
Eusocial amber are significant for us to understand the termites’ early evolution, ecology and eusociality that had
Caste complicated interactions in their nests.
Termitophiles © 2020 Elsevier Ltd. All rights reserved.
Ecosystem

1. Introduction Amber is considered as the best fossil medium to preserve the

detailed morphologies of organisms in three dimensions, while
Eusocial termites live inside their nests together with a large providing better information regarding the behavior and paleo-
number of individuals of various castes in cooperation. In addition, ecology. The studies of termites in Cretaceous amber started from
ants (Tuma et al., 2019), termitophiles (Kistner, 1969; Kistner, 1998) Cockerell (1916), who reported Proelectrotermes swinhoei and
or fungi (Rouland-Lefevre, 2000; Matsuura, 2005; Matsuura, 2006; Kachinitermes tristis from Burmese amber (Cockerell, 1917). After-
Matsuura et al., 2009) can also be found in the termite nests, some wards, the study was stagnant for decades, until the revival since
hostile, but some symbiotic. The dead wood, plant debris, soil, 2000. Up to now, 23 genera and 26 species have been documented
termite saliva, faeces or even corpses constitute the abiotic nest from various Cretaceous amber deposits (Table 1) from Myanmar,
environment. On a smaller scale, one termite itself can also be Spain, Lebanon, France and New Jersey (Krishna and Grimaldi,
treated as a microecosystem, with various symbiotic protozoa and/ 2000; Delclo s et al., 2007; Engel et al., 2011; Sa
nchez-García
or bacteria located in the hind gut empowering the host termite to et al., 2020). Among these deposits, Lebanese amber is the oldest,
digest cellulose and get nourishment (Noirot and Noirot-Timothe
e, Lower Barremian or slightly older in age (Poinar and Milki, 2001;
1969; Iida et al., 2000; Brune and Ohkuma, 2011; Ballor and Azar et al., 2003; Maksoud et al., 2017). Besides, Burmese amber,
Leadbetter, 2012). Owing to termites’ huge biomass and high effi- with a geological age of 98.79 ± 0.62 Ma (Grimaldi et al., 2002;
ciency, they have made significant impact on the terrestrial eco- Cruickshank and Ko, 2003; Shi et al., 2012), is characterized by
systems by feeding on and degrading the fixed carbon in woods, abundant quantity and good quality. A geodynamic reconstruction
while regulating the soil properties and structure (Bignell and suggests that the Burmese amber biota lived in a Trans-Tethyan
Eggleton, 2000; Bignell, 2019). island arc near equator (Westerweel et al., 2019). In the latest
checklist of taxa from Burmese amber, 1159 insect species have
been documented up to April, 2020 (Ross, 2020), with many
endemic insect taxa of great importance (Bai et al., 2016; Liu et al.,
* Corresponding author. 2018; Gao et al., 2019; Yang et al., 2019).
E-mail address: [email protected] (D. Ren).

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2 Z. Zhao et al. / Cretaceous Research 117 (2021) 104612

Table 1
Termite species documented from Cretaceous amber.

Species Specimens condition Material (Age) Family

Proelectrotermes swinhoei Cockerell, 1916 alate Burmese amber (Cenomanian) Kalotermitidae

Kachinitermes tristis Cockerell, 1917 left hind wing Burmese amber (Cenomanian) Kalotermitidae
Archeorhinotermes rossi Krishna & Grimaldi, 2003 alate Burmese amber (Cenomanian) Archeorhinotermitidae
Proelectrotermes holmgreni Engel, Grimaldi & Krishna, 2007a, b forewing and hind leg Burmese amber (Cenomanian) Kalotermitidae
Mylacrotermes cordatus Engel, Grimaldi & Krishna, 2007a, b dealate Burmese amber (Cenomanian) Meiatermes grade
Dharmatermes avernalis Engel, Grimaldi & Krishna, 2007a, b alate Burmese amber (Cenomanian) Family incertae sedis
Tanytermes anawrahtai Engel, Grimaldi & Krishna, 2007a, b alate Burmese amber (Cenomanian) Family incertae sedis
Kachinitermopsis burmensis Poinar, 2009 alate Burmese amber (Cenomanian) Kalotermitidae
Krishnatermes yoddha Engel, Barden & Riccio 2016 alate, worker/pseudergate, Burmese amber (Cenomanian) Meiatermes-grade
soldier
Ginormotermes rex Engel, Barden & Riccio 2016 soldier Burmese amber (Cenomanian) Meiatermes-gradea
Anisotermes xiai Zhao, Eggleton & Ren, 2019a alate, worker/pseudergate, Burmese amber (Cenomanian) Mastotermitidae
soldier
Mastotermes monostichus Zhao, Eggleton & Ren, 2019a left wings Burmese amber (Cenomanian) Mastotermitidae
Pabuonqed eulna Vrsanský et al., 2019 alates, immatures Burmese amber (Cenomanian) Pabuonqedidae
Cosmotermes multus Zhao, Yin, Shih & Ren, 2020 colonies with immature, Burmese amber (Cenomanian) Stolotermitidae
workers/pseudergates, soldiers
Cosmotermes opacus Zhao, Yin, Shih & Ren, 2020 alate, colony with nymph, Burmese amber (Cenomanian) Stolotermitidae
workers/pseudergates, soldiers
Melqartitermes myrrheus Engel, Grimaldi & Krishna, 2007a, b alate Lebanese amber (Barremian) Meiatermes-grade
Lebanotermes veltzae Engel, Azar & Nel, 2011 alate Lebanese amber (Barremian) Family incertae sedis
Morazatermes krishnai Engel & Delclo s, 2010 alate Spanish amber, Pen~ acerrada I (Albian) Family incertae sedisb
Cantabritermes simplex Engel & Delclos, 2010 forewing Spanish amber, Pen~ acerrada I (Albian) Family incertae sedis
Aragonitermes teruelensis Engel & Delclos, 2010 forewing Spanish amber, San Just (Albian) Family incertae sedis
Ithytermes montoyai Sa
nchez-García et al., 2020 alates Spanish amber, Pen~ acerrada I (Albian) Meiatermes-gradec
Santonitermes chloeae Engel, Nel & Perrichot, 2011 alate French amber, Charentes (Cenomanian) Family incertae sedis
Syagriotermes salomeae Engel, Nel & Perrichot, 2011 alate French amber, Charentes (Cenomanian) Family incertae sedis
Lutetiatermes priscus Schlüter, 1989 forewing French amber, Bezonnais (Cenomanian) Family incertae sedis
Mastotermes sarthensis Schlüter, 1989 forewing French amber, Bezonnais (Cenomanian) Family incertae sedis
Termitotron vendeense Engel, 2014 alate French amber, Vende
e (Turonian) Meiatermes-grade
Carinatermes nascimbenei Krishna & Grimaldi, 2000 alate American amber, New Jersey (Turonian) Meiatermes-grade
undetermined; JZC Bu235 in Engel et al., 2016 worker Burmese amber (Cenomanian) Family incertae sedis
undetermined; AMNH Bu-SD001 in Engel et al., 2016 worker Burmese amber (Cenomanian) Family incertae sedisd
undetermined; TJ Bu002 in Engel et al., 2016 worker Burmese amber (Cenomanian) Family incertae sedis
undetermined; Bu935a in Engel et al., 2016 worker Burmese amber (Cenomanian) Family incertae sedis
undetermined; CES 552 in S
anchez-García et al., 2020 fragmentary wings Spanish amber, El Soplao (Albian) Family incertae sedis
undetermined; CES 446 in S
anchez-García et al., 2020 fragmentary alate Spanish amber, El Soplao (Albian) Family incertae sedis
undetermined; IGR.ARC-A2-385 in Engel et al., 2011 fragmentary wing French amber, Charentes (Cenomanian) Family incertae sedise
undetermined; Specimen 679 in Engel et al., 2011 wing Lebanese amber (Barremian) Family incertae sedis
undetermined; Specimen 732 in Engel et al., 2011 fragmentary wing Lebanese amber (Barremian) Family incertae sedisf
undetermined; Specimen 1283 in Engel et al., 2011 alate Lebanese amber (Barremian) Family incertae sedis
undetermined; CAS 111 in Engel & Delclo  s, 2010 partial imago Canadian amber, Grassy Lake (Campanian) Family incertae sedis
a
Much like Hodotermitidae sensu lato in view of the decurved mandibles.
b
The hind wing is incompletely preserved, but the venation looks like Mastotermitidae.
c
Much like the Mastotermitidae in view of the thicker and more sclerotized M vein comparing to CuA, a synapomorphy of Mastotermitidae.
d
Probably Anisotermes xiai, but with only two protibial spurs.
e
A cockroach wing.
f
Much like part of a forewing of Mastotermitidae, referring to Anisotermes xiai.

Some fossil termites reported from rock imprints were thought understanding of the ecology of termites as the alates can only be
to be the oldest known termites, but the latest calibrations indicate found outside the nest during nuptial flights. Our knowledge of the
that the age of Baissatermes lapideus, Mastotermes nepropadyom fossil termites of sterile castes, especially the soldiers and the
and Santonitermes transbaikalicus, from Baissa locality (Zaza For- communities, can benefit from amber which is capable of embed-
mation), is much younger than initially proposed, with a minimum ding the organisms inside the nests (Grimaldi and Engel, 2005;
age of 71.9 Ma (Engel et al., 2007a; Vrsanský and Aristov, 2014; Coty et al., 2014; Zhao et al., 2020). Besides, some trace fossils
Wolfe et al., 2016). Therefore, the oldest known termites hitherto provide information on termite nest structures (Rohr et al., 1986;
are alates of Melqartitermes myrrheus, Lebanotermes veltzae and Bordy et al., 2004, 2005; Genise, 2005; Francis and Harland, 2006).
some undescribed specimens from Lebanese amber (Engel et al.,
2007a, 2011). Besides, Valditermes brenanae and Meiatermes ber- 2. Termites in Cretaceous amber
trani from 130 million-year-old rocks of England and Spain,
respectively, are slightly younger in age (Jarzembowski, 1981; The classification of termites as monophyletic within the Blat-
Lacasa-Ruiz and Martínez-Delclo  s, 1986). Most of the imprint fossils todea is repeatedly verified and now well accepted (Lo et al., 2000;
of Cretaceous termites are preserved by wings only, thus, their Klass and Meier, 2006; Inward et al., 2007a; Wipfler et al., 2019).
taxonomy may not be precise. Moreover, the compression fossils While the taxonomic rank was discussed. Lo et al. (2007) tended to
hardly preserved the sterile castes or associated organisms, with continue using Isoptera up to now and Eggleton et al. (2007) pro-
one exception of the worker caste of Meiatermes bertrani docu- posed to use Epifamily Termitoidae for a more orderly rank. Both
mented from the Lower Cretaceous Spain (Grimaldi, 1990; Delclo s nomenclatures have been used in the subsequent literatures. An
and Martinell, 1995; Grimaldi et al., 2008). The alates are signifi- estimated age of the termite origin is in the Late Jurassic (Thorne
cant in the systematics but contribute limited information to our et al., 2000; Engel et al., 2009; Korb, 2010; Bourguignon et al.,
 Z. Zhao et al. / Cretaceous Research 117 (2021) 104612 3

2015). Diverse primitive termites reported by recent fossil studies basal position (second to Mastotermitidae) and early origination of
suggest an important stage of evolutionary radiation in the Creta- Porotermes about 115 Ma (Cameron et al., 2012; Bourguignon et al.,
ceous, and all documented termites in this period are non- 2015), while Cretaceous records are lacking. Similarly, other studies
Neoisoptera. The termites on the Cretaceous compression fossils, inferred Archotermopsidae is more basal (Inward et al., 2007b;
due to poorly preserved morphological characters, make it difficult Evangelista et al., 2019), also contradicted with the fossil records.
to get firm taxonomic positions and reconstruction of their early The recent study of two Cosmotermes species from the Cretaceous
evolution. More than half of these termites are family incertae Burmese amber gave the oldest fossil evidence of Stolotermitidae
sedis, and the phylogenetic positions of these termites are in the about 100 Ma and showed the castes in the colonies. The venation
comb paraphyly out of the known families. But termites from the of Cosmotermes is slightly different from the known extant stolo-
Cretaceous amber (Table 1), most with well-preserved body parts termitids, mainly the Rs vein of Cosmotermes terminating on the
and wings, provide relatively complete and accurate morphological costal margin anterior to wing apex (plesiomorphy, same with
information. As a result, the early evolution of termites became Mastotermitidae and Blattodea), while near wing apex in the extant
clearer and several species are assigned into the known families. Stolotermitidae and Archotermopsidae (Fig. 1D-F). Even so, the
body characters of the multiple castes support its phylogenetic
2.1. Mastotermitidae position in Stolotermitidae. There are some similarities between
Ginormotermes rex Engel, Barden, et Grimaldi, 2016 and Stolotermes
Although some suspected “mastotermitids” with large wings in the head shape and swollen femora, a synapomorphy of Stolo-
were reported from the Cretaceous (Thorne et al., 2000), their termes. Meanwhile, the pentamerous tarsomeres and massive
classifications cannot be supported due to poor preservation. They pronotum suggest it is more basal but restricted to Hodotermitidae
may be members of the Meiatermes-grade or morphological sensu lato, since the mandibles of Ginormotermes rex are bending
Hodotermitidae sensu stricto. The placement of Mastotermes sar- ventrally from the base to the apex, a synapomorphy of Hodo-
thensis, Schlüter, 1989 in Mastotermitidae is disputable, and Valdi- termitidae sensu lato.
termes brenanae, as well, is ambiguous to be mastotermitid
(Jarzembowski, 1981; Krishna, 1990; Grimaldi and Engel, 2005; 2.3. Kalotermitidae
Wappler and Engel, 2006). Comparing with the Euisoptera, Mas-
totermitidae are more cockroach-like, with large body size, gracile Kalotermitidae are the most diverse family among the basal
antennae, massive pronotum and primitive wings with dense veins groups, with four fossil records from Cretaceous amber, all from
and hind wing anal lobes. Zhao et al. (2019a) reported definite Myanmar. These kalotermitids include Proelectrotermes swinhoei
mastotermitids from Burmese amber, Anisotermes xiai and Masto- Cockerell, 1916; Kachinitermes tristis Cockerell, 1917 Pro-
termes monostichus, the former with multiple castes. The mor- electrotermes holmgreni Engel, Grimaldi & Krishna, 2007a, b and
phologies of A. xiai are quite similar with the relic mastotermitid Kachinitermopsis burmensis Poinar, 2009. They have broad prono-
Mastotermes darwiniensis Froggatt, 1897 and the dealate of Garmi- tum wider than head; Rs terminated on the costal margin anterior
termes succineus from Baltic amber (Engel et al., 2007b). The wings to the apex; M veins unbranched or with no more than four
of the Cretaceous mastotermitids are broader than those of the branches near the wing apex, located at the midway from Rs and
living species (Fig. 1A, B) and show more primitive plesiomorphies CuA. The extant kalotermitids, however, do not have the same
(e.g. the absence of distinct ocelli, the extra tibial spines on the venation pattern (Fig. 1I, J), commonly with the deformative M vein,
foreleg in A. xiai) that are shared with Cryptocercus which is the parallel and close to Rs, meanwhile away from the CuA (e.g. Neo-
acknowledged extant sister group of Termitoidae. Interestingly, termes), or sometimes very simple with superior veins conjunct to
regardless of the specialized head, the soldier of Anisotermes xiai is the Rs (e.g. Incisitermes). The conventional M vein of the Cretaceous
very “Cryptocercus-like” in dorsal view, showing a sizable prono- kalotermitids may be a primitive plesiomorphy shared with Mas-
tum with anterior margin strongly convex. The pronotum of Cryp- totermitidae, but degenerated in the subsequent evolution.
tocercus offers a shield covering and protecting the head
meanwhile acting as an excavating equipment (Nalepa, 2011), 2.4. Archeorhinotermitidae
maybe applying equally to the soldier of A. xiai. Moreover, both
Cryptocercus and A. xiai soldiers are wingless. These similarities A sole species has been assigned to this family. The alate of
may recall the idea that the transition from cockroaches to the Archeorhinotermes rossi from Burmese amber shows some primi-
termites and the origin of termite eusociality is a developmental tive characters, but the simplified wing venation is quite similar to
problem (Nalepa, 2015). the extant Rhinotermitidae (Krishna and Grimaldi, 2003), espe-
cially the specialization that C and Sc are fused, R1 and R2 are absent
2.2. Stolotermitidae and Rs and M are unbranched (Fig. 1K, L). Besides, Archeo-
rhinotermes rossi first evolved with fontanelle, and shared this
Stolotermitidae have been separated from Termopsidae sensu synapomorphy with monophyletic extant Neoisoptera. Phylogeny
lato, which once comprised showed it is the sister group of all the extant Neoisoptera (Fig. 2).
Stolotermitidae þ Archotermopsidae þ Termopsidae sensu stricto
(Engel et al., 2009). This small family comprises 15 species in four 2.5. Family incertae sedis
genera (symbol “y” means extinct): Porotermes (Porotermitinae)
Hagen, 1858, Stolotermes (Stolotermitinae) Hagen, 1858, The phylogenetic positions of most termites from Cretaceous
yChilgatermes Engel et al., 2013 and yCosmotermes Zhao, Yin, Shih & amber are indeterminate (Fig. 2). Some of these termites were
Ren, 2020. The extant stolotermitids are all dampwood termites, assigned to the Meiatermes-grade (Table 1), referred to as para-
with records from Oceania, South America and Africa. Fossil sto- phyletic between Mastotermitidae and all other families (Engel
lotermitids are rare, with three forewings from the Cenozoic and et al., 2009; Engel et al., 2016). As the most basal group of Eui-
two species from the mid-Cretaceous of northern Myanmar soptera, the Meiatermes-grade has many primitive characters
(Kaulfuss et al., 2010; Engel et al., 2013; Zhao et al., 2020). A similar to those of Mastotermitidae, e.g. large body size, pentam-
problem has not been resolved, that some of the molecular phy- erous tarsi, broad pronotum; but with reduced characters, e.g. the
logenetics with prediction of the divergent time suggest a quite simpler venation and the loss of hind wing anal lobes. Some of the
4 Z. Zhao et al. / Cretaceous Research 117 (2021) 104612

Fig. 1. Representative forewing venation patterns (without reticulated veins) of the termites in Cretaceous amber (left column) and extant relatives from families (right column),
not to the same scale. C, G, I, K, H, J redrawn from Engel et al. (2016); Engel et al. (2007a); Engel et al. (2011); Krishna and Grimaldi (2003) and Krishna et al., (2013), respectively.

species belonging to the Meiatermes-grade have the Rs vein ter- (Fig. 1D, H), the pronotum is larger, the tarsi pentamerous, etc.
minating at wing apex or exceeding or with inferior veins, e.g. Some wings of the Cretaceous termites from amber or compression
Meiatermes araripena, Mariconitermes talicei, Santonitermes chloeae, fossils (Jitermes tsaii, Yanjingtermes giganteus, Yongdingia opipara,
Krishnatermes yoddha (Fig. 1C, G) (but only in the paratype JZC- Huaxiatermes hungi, Asiatermes reticulatus Mesotermopsis in-
Bu1839b, conflict with the holotype). The wing venations of these completes, Mesotermopsis latus, Valditermes brennanae) show
termites are somewhat like those of the Archotermopsidae or similar venation pattern (Jarzembowski, 1981; Ren et al., 1995;
Hodotermitidae sensu stricto but the body characters are different Engel and Ren, 2003; Zhao et al., 2019b), but due to the missing
 Z. Zhao et al. / Cretaceous Research 117 (2021) 104612 5

Fig. 2. Phylogeny of the Termitoidae. Relationships of the basal termites, especially in Cretaceous amber, are based on Engel et al. (2016); Engel et al. (2009); Zhao et al. (2020)
(majority rule) and relationships of Neoisoptera are based on Bourguignon et al. (2015).
6 Z. Zhao et al. / Cretaceous Research 117 (2021) 104612

body structures, they had been thought to be hodotermitids. In worker, queen and king. The definite specialized termite soldiers in
short, the Cretaceous termites with outstretched Rs veins are the Cretaceous were unknown until the expanded studies of Bur-
probably transitional between Mastotermitidae and Hodotermiti- mese amber in the recent years. The reported termite soldiers are
dae sensu lato. Besides the Meiatermes-grade, some other termites all snapping soldiers with stout mandibles (Engel et al., 2016; Zhao
(e.g. Tanytermes, Dharmatermes) having a phylogenetic position et al., 2019a; Zhao et al., 2020). The soldiers of Krishnatermes yod-
close to Kalotermitidae and more basal, are shown as transitional dha and Anisotermes xiai had the mandibles bending dorsally, same
species but also diversified (Engel et al., 2007a; Engel et al., 2016; as Mastotermitidae, Kalotermitidae and Neoisoptera. The soldier
Zhao et al., 2019a). mandibles of Cosmotermes and Ginormotermes rex, however, bend
It is worth mentioning that a recent reported termite-like ventrally, same with all Hodotermitidae sensu lato. These primitive
cockroach: Pabuonqed eulna [Vrsanský et al., 2019] are with inter- soldiers were somewhat more armed than extant basal termite
esting phylogenetic position between conventional cockroaches soldiers. Anisotermes xiai and Ginormotermes rex were equipped
and termites. They show many plesiomorphies (e.g. massive pro- with massive pronotum, besides, Cosmotermes multus and Cosmo-
notum and tibial spines) that are more primitive than Masto- termes opacus had very sharp mandibular teeth. These mandible
termitidae but with some synapomorphies (e.g. simplified strengthenings may imply more dangerous environments for the
venation) similar with some derived termite families. Even so, the termites in the Cretaceous. However, the non-specialized worker
classification of Pabuonqed eulna are eusocial termites is dubious. caste found from Burmese amber mostly provides limited infor-
With more specimens found in the future, the transition from mation of the similar morphologies. Therefore, it is difficult to make
conventional cockroaches to termites will be clearer. sure if the worker castes are “true” workers or pseudergates. A
Some primitive characters can be only identified from termites feasible way for distinguishing the “true” workers or pseudergates
preserved in amber. For example, the procoxal ventral keels can be is to figure out their lifestyles. As we know, the living “OP (one-
found from the known Mastotermitidae and Meiatermes-grade, not piece)” basal termites, e.g., Stolotermitidae, Archotermopsidae and
only in alates but also in the workers/pseudergates and soldiers, Kalotermitidae, don't forage and don't have “true” workers. Instead,
furthermore, present in all cockroaches. Although this character is the nymphs which have the potential to develop into alates or
not observable from the compression fossil termites, it is obviously soldiers take on the “housekeeping” work as pseudergates (Abe,
shown as a plesiomorphy based on the parsimony. Besides, the hind 1991; Higashi et al., 2000).
wing anal lobe is acknowledged to be a plesiomorphy for Masto-
termitidae, inherited from cockroaches. However, the anal lobes are 3.2. Aggregation
smaller and thin, folded close to the abdomen, and with weak A
veins if present (invisible on compression fossils and barely visible Extant termites mostly appear in aggregations, inside the nests
under tricky angle in amber inclusions). Therefore, few of the giant or outside. The reproductive imagoes stay in the nest until the time
termites from the Cretaceous might be more primitive than for nuptial flight in union during the suitable season, to ensure the
expected. compatible time and space. When excavating a termite nest, the
first sight is major workers/pseudergates and minor soldiers, be-
3. Termites first possessed eusociality sides, the immatures (or larvae in many literatures) or nymphs also
appear. Each caste in the nests performs its own functions which
Although theories give explanations of the origin of eusociality are interdependent. The soldiers are responsible for the security,
(Wilson, 1971; Thorne, 1997; Wilson and Ho €lldobler, 2005; Nowak but the specialized mandibles counteract their capability of taking
et al., 2010), the fossil studies are evidential to understand the real food. Worker caste, without powerful anti-attack capability, take on
stages and environment stress. Among the known eusocial animals, the major “household duties”: care for the immatures or the queen,
termites show the earliest divergent time based on studies from the trophallaxis to transfer the nutrition, moreover, foraging for food. It
fossil records and molecular phylogenetics (Grimaldi and Engel, is difficult to extract information on ecosystems based on the
2005; Rust and Wappler, 2016). Termites are so extraordinary compression fossil termites from the Cretaceous, because almost all
with unified eusociality compared with the Hymenoptera that have are preserved only individually or even by deciduous wings
stages from solitary to eusocial. Due to the lack of intermediate taxa (Wappler and Engel, 2006; Grimaldi et al., 2008; Engel and Gross,
from subsocial cockroach (termite's ancestor) to the eusocial ter- 2009; Kaulfuss et al., 2010). On the other hand, the clusters
mites, it seems that the termites experienced one-stop evolution to contributing to the successful termite mating might have resulted
be eusocial although inconsequential. Moreover, it is well accepted in aggregated individuals trapped together by flowing resins which
that the transition of eusociality is “point of no return” (Wilson and later transformed into amber (Arillo, 2007; Lin et al., 2019).
Ho€ lldobler, 2005; Eggleton, 2011; Lo and Eggleton, 2011; Rust and However, even clusters of termite alates cannot directly reflect
Wappler, 2016), to find the clues is necessary to trace back eusocial colonies since solitary insects were also involved in the
further and subtler. Unfortunately, none of fossil Cryptocercus were preservation of nuptial flights (Boucot and Poinar, 2010; Lin et al.,
found for providing some symplesiomorphies from the common 2019). To explore the termite early eusociality, the individuals in
ancestor and none of wing characters provided from Cryptocercus the nest are crucial. Comparing to the swarm of alates, it is even
were treated as the closest outgroup. What is feasible is that to harder to find the fossil non-reproductives. The termite individuals
piece the existing evidence for the pathway of the early evolution of in the nests or the potentially existing colonies could hardly form
termite eusociality. So far, most of the evidence of the early euso- fossils within sediments before decomposition. That is also the
ciality were found from the Cretaceous Burmese amber. reason why there are suspected termite nest structures but without
any termites found inside (Rohr et al., 1986; Bordy et al., 2004,
3.1. Caste differentiation 2005; Genise, 2005; Duringer et al., 2007). Amber, on the other
hand, is more likely to preserve termites and their nest. In the
The reproductive division of labor is one of the requirements to studies of Mexican and Dominican ambers, several Nasutitermes
confirm the eusociality. The termites go further, with distinct soldiers and workers were embedded together, giving a glimpse of
morphological differentiation into castes including the soldier, the sterile castes in the Miocene nests (Grimaldi and Engel, 2005;
 Z. Zhao et al. / Cretaceous Research 117 (2021) 104612 7

Coty et al., 2014). However, they are higher termites in the Ceno- 4.3. Coprolites
zoic. Zhao et al. (2020) reported one cluster, preserved in Creta-
ceous Burmese amber, containing 89 individuals of different castes Cumulative fecal pellets are generally found in the termite nests,
as well as immature of instars. Compared with the simple swarm sometimes used as building materials (Stuart, 1969). The special
preservation, these wingless and sterile termites directly reveal the fecal pellets in hexagonal shape only happen in few insect groups,
scene of eusocial gregarious within Cretaceous termite colonies. e.g. termites and Anobiidae (Weidner, 1956; Colin et al., 2009). Zhao
The statistics about the proportion of each caste in the large ag- et al. (2020) reported the coprolites of Cosmotermes preserved in
gregation suggested “an early developmental stage of the colony Burmese amber. Different from the drywood termite fecal pellets
since no nymphs or reproductives were present”. Moreover, the with six convex lateral ridges, these coprolites are irregular or rice-
scene logically reflects the cooperative brood care and the over- shaped with unconspicuous lateral ridges, suggesting their food
lapping generations, thus, provides a compelling evidence of the sources were dampwood. Though there were kalotermitids which
eusocial lifestyle of Cretaceous termites. are known as drywood termites (Cockerell, 1916; Williams, 1968;
Engel et al., 2007a), the coprolites of drywood termites are not
present in the Burmese amber under our observation (based on our
4. Feeding and dwelling in woods collection).
[Vrsanský et al. (2019)] reported the coprolites of Pabuonqed
Eusocial termites dwelling in nests have protection against the eulna and the exterior of the fecal pellets additionally contribute to
negative factors from the terrestrial ecosystems (Ruxton et al., conclude the wood-boring habit and classification of P. eulna as
2014). As soil-feeding habit of the higher termites did not appear termites.
until the Cenozoic (Bucek et al., 2019; Engel, 2019), lower termites
are generally involved with wood-feeding, directly inherited from 4.4. Wood-dwelling
the termite ancestors and similarly to Cryptocercus. The wood-
feeding habit might be associated with the resin flows which The reported biota of Burmese amber suggested that they lived
trapped the Cretaceous termites, thus, suggesting complex in- under tropical forest climate (Selden et al., 2016; Xing et al., 2018; Li
teractions in the nest (Fig.3). et al., 2020). The humid broken trees or the rotting logs were
certainly basic components of the tropical forest and had potential
to be the food sources and the nests of termites. The primitive
4.1. Symbiotic microbes lifestyle of extant Cryptocercus, with parents and offspring in a
small colony, are similar to the known dampwood termites espe-
The lower termites have cellulose-degradative protozoa and cially the early stage. Besides, the wood fragment preserved with
bacteria located in the hind gut while higher termites, referring to primitive Pabuonqed eulna [Vrsanský et al., 2019] from Burmese
the family Termitidae, lack protozoa (Breznak and Brune, 1994; amber and the specialized forelegs also suggest the early wood-
Brune and Friedrich, 2000; Peterson and Scharf, 2016). The mi- boring habit. A Dampwood or rotting logs offered the hotbed for
crobes symbiose within the hind gut of termites are believed to give subsocial OP termite ancestor to evolve eusociality (Abe, 1987;
rise to the trophallaxis due to the acquired symbiosis, and then the Nalepa, 2003, 2015). With the evidence of the wood fragments,
behaviors drove the subsocial termite ancestors further to become debris, faeces and systematics, it is certain that the Cosmotermes
eusocial termites (Nalepa, 2015). Some peculiar specimens in were OP termites living in dampwood or rotting logs, and logically
amber open windows of the termite intestine and allow the the worker caste of Cosmotermes were pseudergates.
exploration of the symbiotic eukaryotes with the diameters about The scenes of termites trapped by sticky resin are different for
dozens of micrometres (mm). In the report of Kachinitermopsis reproductives compared to the sterile castes. It is likely that viscous
burmensis, ten new fossil flagellate species that attached on the resin flows creeped down along tree trunks while sticking the
imago intestine intima were described together (Poinar, 2009; swarming alates that fluttered wings (either sole or in groups), or
Engel and Delclo s, 2010). These flagellates show similar morphol- the resin flows dropped on the ground, entrapping the re-
ogies with the protozoa found from extant lower termites (Yamin, productives actively or passively. While for sterile individuals or
1979; Bignell, 2000; Ohkuma, 2008). colonies in the nest, there was a significantly lower probability of
entrapment as there is no evidence of the Cretaceous termites
foraged or lived in exposed nests. Entrapment could involve resin
4.2. Fossil woods drops on the dead stumps or rotting logs inhabited by wood ter-
mites, with the nests semi-opened, allowing the resin to pour in-
Termites are undoubtedly one of the main insects associated side and entomb sterile individuals.
with the ligneous plants, causing significant global economic losses
of more than 20 billion dollars per year (Govorushko, 2019). Several 4.5. Termitophiles
studies reported wood fragments in Cretaceous amber using the
optical microscope observation and/or the nuclear magnetic reso- The term termitophiles are generally used to refer to the obli-
nance (NMR) spectroscopy (Grimaldi et al., 2002; Perrichot, 2004; gate termitophiles with at least one full life cycle inside the termite
Poinar and Lambert, 2007). Some of the woods belongs to the nests (Kistner, 1969). While the non-obligate termitophiles only
family Araucariaceae, most similar to the Agathis, which is also temporarily stay in the nests as refuges. Favorable environments
speculated to be the source of Burmese amber. Another two studies with survivable temperature, humidity, food source, cleanness and
compared the fibres of two wood fragments co-embedded with the safeguard in the termite nests attract different kinds of arthropods,
non-reproductive termites (Zhao et al., 2019a, 2020). In amber with such as Arachnida, Diptera, or Coleoptera. These termitophiles are
the preserved part of a large colony of Cosmotermes multus, the able to avoid the exclusion by termite hosts by morphological
wood fibres binding aligned and transparent suggest the wood (Kistner, 1968), behavioral (Kistner, 1979) or chemical means
fragment was water-rich (Zhao et al., 2020). On the other hand, the (Howard et al., 1980). Cai et al. (2017) reported the recent limuloid
wood fragment co-embedded with a soldier of Anisotermes xiai rove beetles of Trichopseniini in Burmese amber with morpho-
shows matted, interlaced and dehydrated fibres (Zhao et al., 2019a). logical specialization, dating the earliest termitophiles back to the
8 Z. Zhao et al. / Cretaceous Research 117 (2021) 104612

Fig. 3. Diagram of the documented internal and external interactions with the OP (one-piece) termite colonies in the Cretaceous.

mid-Cretaceous, and speculated that this association had been living termites, and this may not fit well for the Cretaceous basal
established more than 100 million years ago. The potential hosts for termites which had higher diversity than extant basal termites
the Cretaceous limuloid rove beetles are restricted Mastotermiti- except for Kalotermitidae. With more transitional species and the
dae, Kalotermitidae and Meiatermes-grade of basal termites based improvement of systematic methods, the phylogeny of these
on field observation. Another solely preserved rove beetle of Mes- Cretaceous termites will be clarified. The Cretaceous was a key
oporini (Yamamoto et al., 2016), however, might not be obligate stage for the origin of eusociality, not only for termites, but also for
termitophiles since its extant relatives are not all termitophiles. We the ants, honey bees, vespid wasps, etc (Cao et al., 2020). The
speculate the termitophiles that symbiosed with the Cretaceous unified eusociality of these insects suggest a convergent evolution.
termites are underestimated since only few specimens reflect the But how did convergence of eusociality rapidly evolved in the
termite colonies in the nests, and the colonies all belong to Stolo- Cretaceous, stress from inorganic environment, competition, or
termitidae which have not been found to have association with evolutionary inherence? Besides, living termites have advanced
Trichopseniini. While morphologies are not strict direct evidence to group behaviors beyond the classic eusociality, that further
understand the symbiotic behaviors between the Cretaceous ter- improve survival and reduce the risk in the social living. Even the
mites and the termitophiles, more direct taphonomic evidence are primitive but extant Mastotermes darwiniensis and OP Hodo-
required. termopsis sjostedti of Archotermopsidae show such undertaking
behaviors for sanitation and produce vibration for alarm (Evans
et al., 2005; Sun et al., 2013; Sun and Zhou, 2013). These behav-
5. Future study directions iors are crucial in plague-resistance and group defence for eusocial
insects (Rosengaus et al., 2011). Did they originate parallelly with
The evolutionary radiation of termites in the Cretaceous gave the eusociality or independently? To answer these questions, future
rise to diverse morphologies such that it is difficult to find synap- studies will be needed to focus on the hard fossil evidence,
omorphies to unite these fossil termites. On the other hand, the
termite taxonomy uses classical standards mainly based on the
 Z. Zhao et al. / Cretaceous Research 117 (2021) 104612 9

especially Cretaceous amber inclusions co-embedded with non- Clarens Formation in the Tuli Basin, Southern Africa. (Bordy et al. 2004). PAL-
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found in Cretaceous amber are still family incertae sedis, it is not 
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their detailed and critical review and suggestion to improve the Northern Myanmar. Journal of Asian Earth Sciences 21, 441e455.
Delclo s, X., Martinell, J., 1995. The Oldest Known Record of Social Insects. Journal of
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Paleontology 63, 594e599.
National Natural Science Foundation of China [No. 31730087], the Delclo s, X., Arillo, A., Pen~ alver, E., Barro

n, E., Soriano, C., Valle, R.L.D., Berna

rdez, E.,
Program for Changjiang Scholars and Innovative Research Team in Corral, C., Ortun ~ o, V.M., 2007. Fossiliferous amber deposits from the Cretaceous
University [IRT-17R75], and Support Project of High-level Teachers (Albian) of Spain. Comptes Rendus Palevol 6, 135e149.
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in Beijing Municipal Universities [No. IDHT20180518]. The work New termite trace fossils: Galleries, nests and fungus combs from the Chad
was also supported by grants (T.P.G.) from the Beijing Natural Sci- basin of Africa (Upper MioceneeLower Pliocene). Palaeogeography, Palae-
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