Associations Between Fossil Beetles and Other Organisms

geosciences

Review Associations between Fossil Beetles and Other Organisms

George Poinar

Department of Integrative Biology, Oregon State University, Corvallis, OR 97331, USA; [email protected]

Received: 26 February 2019; Accepted: 18 April 2019; Published: 21 April 2019

Abstract: The present work reveals plant and animal associates of 16 families and subfamilies of fossil beetles that have been preserved in amber from Mexico, the Dominican Republic, and Myanmar. The associates include mites, pseudoscorpions, spiders, insect parasites and predators, fungi, angiosperm parts, vertebrates, and nematodes. The presence of these fossil associates can be attributed to the rapid preservation of organisms in resin, thus maintaining natural associations almost “in situ”. Examples of present-day associations similar to those of the fossils show that speciﬁc behavioral patterns are often far more ancient than the speciﬁc lineages involved.

Keywords: fossil beetles; fossil associates; Myanmar amber; Dominican amber; Mexican amber

1. Introduction Beetles, being the most successful animals on Earth and displaying a range of colors, shapes and sizes, form many associations with other organisms [1]. While a multitude of fossil beetles have been described, very few of them have left any physical or biological evidence of organisms that shared their environment. The present work shows a range of plants, fungi and animals that were found associated with various fossil beetles. Such examples are rare, and the majority of cases occur in amber [2,3]. Preservation in this media is not only due to the rapid entombment of the organisms, thus maintaining any natural associations “in situ”, but also to the preservative properties of amber [4].

2. Materials and Methods Examples of beetles associated with animals and plants were obtained from inclusions in Dominican, Mexican, and Burmese amber. Some cases were taken from the literature while others were selected from the Poinar amber collection at Oregon State University. Many of these associations are new and have not been examined by experts so taxonomic details are limited or unavailable. In some cases, the associated organisms are described but not the beetles and vice versa. Attempts were made to include all previous published cases of fossil beetles with associates. Ages of the amber sites containing specimens used in this work are 15–45 Mya for Dominican [5,6], 22.5–26 Mya for Mexican [7] and 97–110 Mya for Burmese [8,9].

3. Results The associations between fossil beetles and other organisms are arranged under the associated organisms. Table1 summarizes the fossil beetle groups with their various associates while Table2 indicates the present location and accession numbers of the various specimens.

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Table 1. Beetle groups with associated organisms included in the present work.

Beetle Group M P S P+PFAVN Brentidae +D Cantharidae +B Chrysomelidae +D +D Colydinae +D Curculionidae +D +D +D Dermestidae +B Dryophthoridae +D Elateridae +D +B Histeridae +D Ithyceridae +B Lampyridae +D Meloidae +D Platypodinae +D +D +D +D +B +D Pselaphinae +D Ptilodactylidae +Me Staphylinidae +D +D +D Associates: M = mites; P = pseudoscorpions; S = spiders; P + P = parasites and predators; F = fungi; A = angiosperms; V = vertebrates; N = nematodes. Amber sources: B = Burmese, D = Dominican, Me = Mexican.

Table2. Location of specimens ﬁgured in the present review. PAC = Poinar amber collection, maintained at Oregon State University, Corvallis, Oregon, USA.

Figure Number and Subject Type of Amber Location of Specimen 1. Mites on beetle Dominican PAC-Sy-1-5 2. Mites on beetle Dominican PAC-Sy-1-164 3. Mites adjacent to beetle Dominican PAC-Sy-1-5 4. Mite holding beetle leg Dominican PAC-Sy-1-5 5. Mites on weevil Dominican PAC-C-7-413 6. Mites on beetle larva Dominican PAC-Sy-1-27 7. Mites on beetle larva Dominican PAC-Sy-1-27 8. Pseudoscorpion on beetle Dominican PAC-Sy-1-15 9. Pseudoscorpion on beetle Dominican PAC-Sy-1-15 10. Beetle in spider cocoon Dominican PAC-Sy-1-58 11. Beetle in spider web Dominican PAC-Sy-1-58 12. Beetle in spider web Dominican PAC-Sy-1-58 13. Beetle with termite Dominican PAC-Sy-1-24 14. beetle and moth Dominican PAC-Sy-1-186 15. Parasitized weevil Burmese PAC- B-C-48B 16. Parasitized click beetle Dominican PAC-Sy-1-131 17. Wasp cocoons Dominican PAC-Sy-1-131 18. Fly egg on beetle Dominican PAC-C-7-305F 19. Bug attacking beetle Dominican PAC-Sy-1-135 20. Beetle on stingless bee Dominican PAC-Sy-1-14 21. Chemical warfare Burmese Buckley collection ABS66 22. Beetle with fungus Burmese PAC-B-F-7 Geosciences 2019, 9, 184 3 of 24

Table 2. Cont.

Figure Number and Subject Type of Amber Location of Specimen 23. Fungus on beetle Burmese PAC-B-F-7 24. Beetle mycangium Burmese PAC-B-F-7 25. Fungus on click beetle Burmese PAC-B-F-9 26. Weevil with orchid Dominican PAC-C-1-191 27. Beetle with orchid Mexican PAC- C-1-156 28. Beetle larva with case Dominican PAC-C-7-52 29. Beetle larva by bird Burmese PAC-B-V-3 30. Nematode on beetle Dominican PAC-N-3-19 31. Nematode parasite Dominican PAC-N-3-60 32. Nematode parasite Dominican PAC-N-3-41 33. Nematode parasite Dominican PAC-N-3-9 34. Nematode parasite Dominican PAC-N-3-17 Geosciences 2019, 8, x FOR PEER REVIEW 3 of 24

3.1. Associations with Mites (Arachnida: Acari) Acari) Mites are ubiquitous and it is likely that during their lifetime all extant beetle species encounter these small arachnids. In In fossil fossil beetles, beetles, it it is is usually usually the the phoretic phoretic stages stages of of mites mites that that are are ass associates.ociates. This isis especiallyespecially evidentevident in in wood wood inhabiting inhabiting beetles beetles that that often often share share their their habitats habitats with with mites. mites. When When the adultthe adult beetles beetles are ready are ready to ﬂy to to fly another to another location, location, the mites the attach mites themselvesattach themselves to the beetles to the [ 10beet]. Phoreticles [10]. mitesPhoretic in Dominican mites in Dominican amber display amber diﬀ displayerent methods different of attachment. methods of Some attachment. mites simply Some hold mites on simply to the carrier’shold on to body the (Figurescarrier’s1 body and2 ),(Figures sometimes 1 and detaching 2), sometimes when enteringdetaching the when resin entering (Figure3 ).the Others resin secure(Figure themselves3). Others secure to the cuticle themselves of the to beetle the cuticle by their of mouthparts the beetle (Figureby their4 ). mouthparts A more specialized (Figure 4). method A more of attachmentspecialized occursmethod when of attachment the mite forms occurs a thinwhen strand the mite of hardened forms a “glue”thin strand that isoffastened hardened to “glue” the beetle’s that cuticleis fastened (Figures to the5– beetle’s7)[11]. cuticle (Figures 5–7) [11].

Figure 1. Mites ( (Arachnida:Arachnida: Acari Acari)) clinging clinging to to the the underparts of a platypodine beetle ( (Coleoptera:Coleoptera: Curculionidae: Platypodinae Platypodinae)) in Dominican amber. Scale bar = 3030 µm.µm.

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Figure 2. 2. TwoTwo mites mites (Arachnida: (Arachnida: Acari) Acari) Acari) (arrowheads)(arrowheads) (arrowheads) attached attached attached to to to the the the underparts underparts of of a a histerid ((Coleoptera:(Coleoptera: Histeridae) beetle in Dominican amber. Note also associated nematodes (arrows).(arrows). Scale bar = 580580 µm.µm.

Figure 3. 3. LargeLarge mites mites (Arachnida:(Arachnida: Acari) Acari) Acari) thatthat that detached detached detached from from from a a a platypodine platypodine beetle beetle (Coleoptera: (Coleoptera: Curculionidae: Platypodinae) in in Dominican Dominican amber. amber. Scale Scale bar bar == 780780780 µm.µm.µm.

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Figure 4. 4. MiteMite (arrow (arrow)) (Arachnida: (Arachnida: Acari) Acari) holding holding a a leg leg of of a a staphylinid staphylinid beetle (Coleoptera: Staphylinidae) by its mouthparts in Dominican amber. Scale bar = 435 µm.µm.

FFigureigure 5. 5.Mites Mites (Arachnida: (Arachnida: Acari) Acari) attached attached to a dryophthorid to a dryophthorid weevil, Bicalcasura weevil, maculataBicalcasura, (Coleoptera: maculata, (Coleoptera:Dryophthoridae) Dryophthoridae) by hardened by glue hardened sticks in glue Dominican sticks in amber. Dominican Scale amber. bar = 770 Scaleµm. bar = 770 µm.

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Figure 6.6. Deuteronymph uropodid mites (Arachnida: Acari)Acari) attached attached to to a beetle larva by hardened glue sticks in Dominican amber. Scale bar = 450450 µm.µm.

Figure 7. 7. DetailDetail of of hardened hardened glue glue sticks sticks attaching attaching phoretic phoretic mites mites (Arachnida: (Arachnida:(Arachnida: Acari) Acari) Acari) to the toto beetle thethe beetle larva larvainlarva Figure inin Figure6. Scale 6. barScale= bar75 µ =m. 75 µm.

3.2. As Associationssociations with with Pseudoscorpions Pseudoscorpions (Arachnida: Pseudoscorpiones) Pseudoscorpiones) Pseudoscorpions in in Dominican Dominican amber amber also also use beetles use beetles for transport for transport [12]. These [12]. arachnids These arachnids normally normallygrasp the grasp posterior the portionposterior of portion the beetle’s of the abdomen, beetle’s abdomen, usually with usually one chela with (Figureone chela8) but (Figure sometimes 8) but withsometi twomes (Figure with 9two). Silken (Figure threads 9). Silkenilken are apparently threadsthreads areare secreted apparently from glandssecreted in theirfrom clawsglands that in attachtheir claws their thatchelathat attachattach to the theirtheir beetle chelachela [1]. toto thethe beetlebeetle [1].[1].

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Figure 8. 8.Adult Adult pseudoscorpion pseudoscorpion (Parawithius (Parawithiussp.: Pseudoscorpiones: sp.: Pseudoscorpiones: Withiidae) Withiidae) clasping a platypodine clasping a beetleplatypodine (Cenocephalus beetle (Cenocephalus rhinoceroides : rhinoceroides Coleoptera:: Coleoptera: Curculionidae: Curculionidae: Platypodinae) Platypodinae with one) wit chelah one in Dominicanchela in Dominican amber. Arrowsamber. Arrows show phoretic show phoretic nematodes nematodes that became that became detached detached from the from beetle. the beetle. Scale barScale= bar990 =µ 990m. µm.

Figure 9. 9. AdultAdult pseudoscorpion (Arachnida: Pseudoscorpiones) Pseudoscorpiones) clasping clasping a a platypodine beetle (Coleoptera:(Coleoptera: Curculionidae: Platypodinae Platypodinae)) with bothboth chelae in Dominican amber.amber. ScaleScale barbar == 950 µm.µm.

3.3. Associations with Spiders (Arachnida: Araneae) Araneae) Spiders areare anan arachnid arachnid group group that that determine determine the the fate fate ofmany of many beetles. beetles. Their Their webs webs in amber in amber often captureoften capture various vario insects,us insects, including including beetles. beetles. One spider One spider cocoon cocoon was wrapped was wrapped around around an ant-like an ant stone-like beetlestone beetle (Staphylinidae: (Staphylinidae: Scydmaeninae) Scydmaeninae in Dominican) in Dominican amber amber (Figure (Figure 10). Further 10). Further evidence evidence of spider of websspider capturing webs capturing beetles beetles in Dominican in Dominican amber amber are an are enmeshed an enmeshed platypodine platypodine beetle beetle (Figure (Figure 11) and 11) a colydiineand a colydiine beetle beetle (Figure (Figure 12). 12).

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Figure 10. AntAnt-like--likelike stone stone beetle ( (Coleoptera:Coleoptera: Staphylinidae: Scydmaeninae Scydmaeninae))) wrappedwrapped in in a a spider spider web web “cocoon”“cocoon” ininin DominicanDominicanDominican amber. amber.amber. ScaleScale barbar == 1.2 mm.

Figure 11. Platypodine beetle (Coleoptera: (Coleoptera: Curculionidae:Curculionidae: PlatypodinaePlatypodinae Platypodinae))) inin spiderspider web web in in Dominican Dominican amber. Scale bar = 950950 µm.µm.

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Figure 12. Colydiine beetle (Coleoptera: Zopheridae) in spider web in Dominican amber. Scale barbar == 1.0 mm.Figure 12. Colydiine beetle (Coleoptera: Zopheridae) in spider web in Dominican amber. Scale bar = 1.0 mm. 3.4. Associations with Termites (Blattodea: R Rhinotermitidae)hinotermitidae) 3.4. Associations with Termites (Blattodea: Rhinotermitidae) Staphylinids (Coleoptera: Staphylinidae) Staphylinidae) show show a a great morphological diversity related to their life habits. Staphylinids One One subfamily, subfamily, (Coleoptera: the Trichopseniin Trichopseniinae, Staphylinidae)ae , showare shaped a great like morphological horseshoe diversity crabs, and and related being being to flightless, ﬂightless,their requirelife assistance assistanchabits. Onee insubfamily, reaching reaching the new new Trichopseniin habitats. habitats.ae Dominican Dominican, are shaped like amber amber horseshoe specimens crabs, showand show being that flightless, when these require assistance in reaching new habitats. Dominican amber specimens show that when these beetles areare readyready to to leave leave their their termite termite colonies, colonies, they they crawl crawl on wingedon winged termites termites (Figure (Figure 13) or 13) on tineidor on beetles are ready to leave their termite colonies, they crawl on winged termites (Figure 13) or on (Lepidoptera: Tineidae) moths that also inhabit the termitaria (Figure 14). In both cases, the beetles tineidtineid (Lepidoptera: (Lepidoptera: Tineidae) Tineidae) moths moths that that also also inhainhabit thethe termitaria termitaria (Figure (Figure 14). 14). In bothIn both cases, cases, the the do not appear to be attached to the carrier by any special device since they were free in the resin. beetlesbeetles do not do appearnot appear to beto beattached attached to to the the carrier carrier by anyany special special device device since since they they were were free freein the in the Theseresin.resin These trichopseniine. These trichopseniine trichopseniine rove beetles rove rove beetles datebeetles back date date to b back theack mid-Cretaceousto the midmid-Cretaceous-Cretaceous [13]. [13]. [13].

FigureFigure 13. 13.Prorhinopsenius Prorhinopsenius alzadae alzadae(Coleoptera: (Coleoptera: Staphylinidae) Staphylinidae) adjacent adjacent to a to termite a termite (Blattodea (Blattodea:: Rhinotermitidae)Rhinotermitidae) in Dominican in Dominican amber. amber. Scale Scalebar bar == 750 µm.µm. Figure 13. Prorhinopsenius alzadae (Coleoptera: Staphylinidae) adjacent to a termite (Blattodea: Rhinotermitidae) in Dominican amber. Scale bar = 750 µm.

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Figure 14. A member of the TrichopseniinaeTrichopseniinae (Coleoptera:(Coleoptera: Staphylinidae) adjacent to a tineid moth (Lepidoptera: Tineidae) inin DominicanDominican amber.amber. ScaleScale barbar = 750 µm.µm.

3.5. Associations with Insect Parasites and Predators Euphorinae wasps wasps (Hymenoptera: (Hymenoptera: Braconidae Braconidae)) are are well well known known for for attack attackinging various various stages stages of ofbeetles. beetles. In In amber amber there there is is evidence evidence of of a a euphorine euphorine wasp wasp attacking attacking the the adult adult weevil, Habropezus plaisiommus (Coleoptera:(Coleoptera: Ithyceridae: Ithyceridae: Carinae) Carinae) in in Burmese Burmese amber amber (Figure (Figure 15)15)[ [14].14]. Cocoons Cocoons and a mature pupa or newly hatched adult of anotheranother probable euphorine were attached to the body of an adult click beetle (Coleoptera:(Coleoptera: Elateridae) in DominicanDominican amber (Figures 16 and 1717).).

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Figure 15. 15. AA parasitized parasitized weevil, weevil, HabropezusHabropezus plaisiommus plaisiommus (Coleoptera:(Coleoptera: Ithyceridae:Ithyceridae: Carinae), Carinae), with with a euphorine braconid cocoon (arrow) (Hymenoptera:(Hymenoptera: Braconidae) in Burmese amber.amber. Scale bar == 800 µm.µm.

Figure 16. 16. AA click click beetle beetle ((Coleoptera:Coleoptera: Elateridae) Elateridae) with with attached attached probable probable euphorine cocoons ((Hymenoptera:Hymenoptera: B Braconidae)raconidae) (arrow (arrow)) in Dominican amber. Scale bar = 1.31.3 mm. mm.

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FigureFigure 17. 17. DetailDetail ofof cocooncocoon cocoonsss shown shown in in Fig FigureFigureure 16.1616.. Arrow Arrow showsshows maturemature waspwasp pupa pupa or or newlynewly emerged emerged adult.adult. ScaleScale barbar == 280280280 µm.µm.µm.

TachinidTachinid ﬂiesfliesflies (Diptera: (Diptera:(Diptera: Tachinidae) Tachinidae)Tachinidae) also alsoalso attack attackattack beetles beetlesbeetles and andand the thethe presence presencepresence of aofof hatched aa hatchedhatched tachinid tachinidtachinid egg eggonegg the on on pronotum the the pronotum pronotum of the leafof of thethe beetle, leaf leaf Stenaspidiotus beetle, beetle, StenaspidiotusStenaspidiotus microptilus microptilusmicroptilus(Coleoptera: ((Coleoptera:Coleoptera: Chrysomelidae) Chrysomelidae)Chrysomelidae) in Dominican in in Dominicanamber,Dominican is fossil amber,amber, evidence isis fossilfossil of evidenceevidence parasitism ofof by parasitismparasitism this group byby [ 15thisthis] (Figure groupgroup [15]18[15]). (Figure(Figure 18).18).

FigureFigure 18. 18. TachinidTachinid egg egg (Diptera: (Diptera: Tachinidae)Tachinidae) (arrow(arrow (arrow))) attachedattached toto thethe pronotum pronotum of of the the leaf leaf beetle beetle StenaspidiotusStenaspidiotus microptilus microptilus ((Coleoptera:(Coleoptera:Coleoptera: Chrysomelidae) Chrysomelidae) in Dominican amber. Scale Scale bar bar == 750750 µm.µm.µm.

FossilFossil evidence evidence of of beetle beetle predation predation is is quite quite rare rare,rare,, so so it it was was a a surprise surprise to to find ﬁndfind a a platypodine platypodine under under attackattack by by a a reduviid reduviid bug bug (Hemiptera: (Hemiptera: Reduviidae) Reduviidae) in in Dominican Dominican amber amber (Figure (Figure 19)1919))... Another case of predationpredation involvedinvolvinvolveded the thethe beetle beetlebeetle as asas the thethe predator. predator.predator. This ThisThis was waswas a meloid aa meloidmeloid (Coleoptera: (Coleoptera:(Coleoptera: Meloidae) MMeloieloidae)dae) triungulin triungulintriungulin just justjust aboveabove thethe “neck”“neck” ofof aa stinglessstingless beebee (Hymenoptera:(Hymenoptera: Apidae)Apidae) inin DominicanDominican amberamber (Figure(Figure 20).20). WhenWhen carriedcarried bbackack toto thethe hive,hive, thethe triungulintriungulin willwill devourdevour tthehe developingdeveloping beebee stagesstages [16].[16].

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Figure 19.19. Reduviid (Hemiptera: Reduviidae) attacking a platypodine (Coleoptera: Curculionidae: PlatypodinaePlatypodinae)) in Dominican amber. Scale bar = 1.01.0 mm. mm.

Figure 20. 20. MeloidMeloid triungulin triungulin (Coleoptera: (Coleoptera: Meloidae) Meloidae) (arrow) (arrow) on a stingless on a stingless bee (Hymenoptera: bee (Hymenoptera: Apidae) Apidae)in Dominican in Dominican amber. Scale amber. bar Scale= 400 barµm. = 400 µm.

An unusual example of defensive behavior in in response to to a potential predator was was found in a cantharid beetle (Coleoptera: C Cantharidae)antharidae) in in Burmese Burmese amber. amber. Based Based on on the the tactile stimulus of the antennae of a potential blattid predator, the beetle extruded chemical vesicles from its abdomen, one of which released a secretion secretion that that covered covered a a portion portion of of the the potential potential predator’s predator’s antenn antennaa [17] [17 (Figure] (Figure 21). 21 ).

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Figure 21. Soldier beetle ( (Coleoptera:Coleoptera: Cantharidae) Cantharidae) displaying chemical defense behavior in Burmese amber. G = extruded glandular vesicle. A A = antennaantenna of predatory blattid (Blattodea:(Blattodea: Blattidae) in contact with the beetle.beetle. Scale bar = 1.21.2 mm. mm.

3.6. A Associationsssociations with Fungi Fungi represent another ubiquitous group and the many diverse roles they have with insects are only now now beginning beginning to to be be understood. understood. When considering fungal-beetlefungal-beetle associations, the ﬁrstfirst image that comes to mind are the beetles thatthat feed on various fungi [[18].18]. One such fungal group that furnished nutritionnutrition forfor thethe developingdeveloping stages stages of of wood-boring wood-boring beetles beetles are are ambrosia ambrosia fungi fungi that that occur occur in thein the tunnels tunnels of barkof bark beetles beetles and and are are carried carried by theby the beetles beetles in mycetangia in mycetan fromgia from one one site tosite another to another [19]. Evidence[19]. Evidence in Burmese in Burmese amber amber of an ambrosiaof an ambrosia fungus fungus associated associated with a platypodinewith a platypodine beetle shows beetle that shows this isthat an ancientthis is associationan ancient (Figures association 22 and (Figures 23)[20 ]. 22 Hyphal and 23) fragments [20]. Hyphal and yeast-like fragments propagules and yeast within-like mycetangiapropagules within on the myc femoraetan ofgia the on beetlethe femora show of that the a beetle close associationshow that a with close these association fungi had with already these beenfungi establishedhad already in been platypodines established (Coleoptera: in platypodines Curculionidae: (Coleoptera: Platypodinae) Curculionidae by the: Platypodinae mid-Cretaceous) by (Figurethe mid 24-Cretaceous)[21]. (Figure 24) [21].

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Figure 22. The platypodine,platypodine, PalaeotylusPalaeotylus femoralisfemoralis (Coleoptera:(Coleoptera: Curculionidae:Curculionidae:: Platypodinae Platypodinae)Platypodinae) covered with mycelium, conidiophores and conidia of the ambrosia ambrosia fungus,fungus ,, PaleoambrosiaPaleoambrosia entomophila ((Ophiostomatales:Ophiostomatales: Ophiostomataceae) Ophiostomataceae) in Burmese amber. Scale bar = 430430 µm.µm.

Figure 23. 23. ConidiophoreConidiophore of of the the ambrosia ambrosia fungus, Paleoambrosia entomophila (Ophiostomatales: Ophiostomataceae) on Palaeotylus femoralis femoralis (Coleoptera:(Coleoptera: Curculionidae: Platypodinae Platypodinae)) in in Burmese Burmese amber. Scale bar = 66 µm.µm.

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Figure 24. Portion of the femoralfemoral mycetangiummycetangium ofof PalaeotylusPalaeotylus femoralis (Coleoptera:(Coleoptera: Curculionidae: PlatypodinaePlatypodinae)) showing hyphal fragments and yeast yeast-like-like propagules (arrow) of the the ambrosia ambrosia fungus, Paleoambrosia entomophilaentomophila(Ophiostomatales: (Ophiostomatales: Ophiostomataceae) Ophiostomataceae) in in Burmese Burmese amber. amber. Scale Scale bar = bar14 =µ m. 14 µm. Other associations involve fungi that utilize beetles for nutrition. Members of the Trichomycetes are associatedOther associations with the digestive involve tract fungi of that arthropods, utilize including beetles for beetles nutrition. [22]. TheseMembers fungi of obtain the nourishmentTrichomycetes from are digestedassociated food with in the the digestive alimentary tract tract of of arthropods, the host and including normally beetles cause [22]. little These or no physicalfungi obtain damage. nourishment A rare examplefrom digested of a trichomycete food in the alimentary growing out tract of of the th orale host cavity and ofnormally a click beetlecause (Coleoptera:little or no physical Elateridae) damage. was A found rare inexample Burmese of a amber. trichomycete It is typical growing for trichomycetesout of the oral tocavity establish of a themselvesclick beetle in(Coleoptera: the hindgut Elateridae) of the host, was however foundPriscadvena in Burmese corymbosa amber.(Priscadvenales: It is typical for trichomycetes Priscadvenaceae) to couldestablish have themselves established in itself the hi inndgut the foregut of the since host, it however is attached Priscadvena to the oral corymbosa cavity of(Priscadvenales: the beetle [23] (FigurePriscadvenaceae) 25). could have established itself in the foregut since it is attached to the oral cavity of the beetle [23] (Figure 25).

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FigureFigure 25. A trichomycete, PriscadvenaPriscadvena corymbosa corymbosa(Priscadvenales: (Priscadvenales: Priscadvenaceae) Priscadvenaceae) emerging emerging from from the theoral oral cavity cavity of anof elateridan elaterid beetle beetle (Coleoptera: (Coleoptera: Elateridae) Elateridae) in Burmesein Burmese amber. amber. Scale Scale bar bar= 1.0 = 1.0 mm. mm.

3.7.3.7. Associations Associations with with Flowering Flowering Plants Plants OrchidsOrchids have have a a unique unique method method of of pollination pollination t thathat involves involves dispersing dispersing their their pollen pollen in in little little sacs sacs calledcalled pollinia. pollinia. Pollinia Pollinia are are usually usually attached attached to to pollinators pollinators by by adhesive adhesive pads pads (viscidia) (viscidia) with with the the entire entire pollinationpollination unit unit called called a a pollinar pollinarium.ium. Beetles Beetles have have various various associations associations with with orchids. orchids. They They visit visit the the flowersflowers for for pollen pollen and and nectar nectar and and consequently consequently serve serve as as pollinators pollinators and and also also use use floral floral flowers flowers and and vegetativevegetative parts parts for for rearing their young. A A cryptorhynchid weevil weevil (Coleoptera: (Coleoptera: Curculionidae) Curculionidae) in in DominicanDominican amber amber had had the the pollinarium pollinarium of Cyclindrocites of Cyclindrocites browni b(Angiospermae:rowni (Angiospermae: Orchidaceae) Orchidaceae) attached attachto itsed pronotum to its pronotum (Figure 26(Figure). In Mexican 26). In Mexican amber, amber, a ptilodactylid a ptilodactylid (Coleoptera: (Coleoptera: Ptilodactylidae) Ptilodactylidae) beetle beetle had the pollinarium of Annulites mexicana (Angiospermae: Orchidaceae) attached to its mouthparts (Figure 27) [24].

Geosciences 2019, 9, 184 18 of 24 had the pollinarium of Annulites mexicana (Angiospermae: Orchidaceae) attached to its mouthparts

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Figure 26. 26. Cryptorhynchid weevil (Coleoptera: Curculionidae) Curculionidae) with with attached orchid pollinarium pollinarium (arrow) of Cyclindrocites browni (Angiospermae: Orchidaceae) Orchidaceae) inin DominicanDominican amber.amber. Scale bar = 1.01.0 mm. mm.

Figure 27. Ptilodactylid (Coleoptera: Ptilodactylidae) Ptilodactylidae) beetle beetle with with attached attached pollinarium pollinarium (arrow) (arrow) of Annulites mexicana (Angiospermae: Orchidace Orchidaceae)ae) in in Mexican Mexican amber. amber. Scale bar = 250250 µm.µm.

CaseCase-bearing-bearing chrysomelid chrysomelid larvae larvae (Coleoptera: (Coleoptera: Chrysomelidae) Chrysomelidae) in Dominican in Dominican amber are amber included are includedhere since here the casessinceare the often cases constructed are often constructed with digested with angiosperm digested remainsangiosperm (Figure remains 28). The (Figure ability 28). to Theconstruct ability these to construct cases and these continually cases and enlarge continually them to enlarge ﬁt their them growing to fit bodies their is growing an amazing bodies example is an amazingof insect behaviorexample of [25 insect]. behavior [25].

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Geosciences 2019, 8, x FOR PEER REVIEW 19 of 24

Figure 28. CaseCase-bearing-bearing chrysomelid chrysomelid beetle beetle larva larva (Coleoptera: (Coleoptera: Chrysomelidae) Chrysomelidae) in in Dominican Dominican amber. amber. ScaleFigure bar = 1.028.1.0 Casemm. mm.- bearing chrysomelid beetle larva (Coleoptera: Chrysomelidae) in Dominican amber. Scale bar = 1.0 mm. 3.8. Associations Associations with with Vertebrates Vertebrates 3.8. Associations with Vertebrates An association of a fossil dermestid dermestid beetle beetle (Coleoptera: (Coleoptera: Dermestidae) Dermestidae) with with a a vertebrate is An association of a fossil dermestid beetle (Coleoptera: Dermestidae) with a vertebrate is represented by a larva that was scavenging bird remains in Burmese amber (Figure 2929).). Dermestids represented by a larva that was scavenging bird remains in Burmese amber (Figure 29). Dermestids are well known for feeding on vertebrate remains and experimenters remove remove tissue tissue from from skulls skulls by by are well known for feeding on vertebrate remains and experimenters remove tissue from skulls by placing them in an enclosed container with these beetles. placingplacing them them in an in enclosedan enclosed container container with with thesethese beetles.

FigureFigure 29. Larva29. Larva of dermestidof dermestid beetle beetle (Coleoptera: (Coleoptera: Dermestidae) Dermestidae) adjacent adjacent to bird to bird remains remains (arrow) (arrow) in in Burmese amber. Scale bar = 1.5 mm. Burmese amber. Scale bar = 1.5 mm. Figure 29. Larva of dermestid beetle (Coleoptera: Dermestidae) adjacent to bird remains (arrow) in

Burmese amber. Scale bar = 1.5 mm.

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Geosciences 2019, 8, x FOR PEER REVIEW 20 of 24 3.9.3.9. Associations Associations with with Nematodes Nematodes (Nematoda)(Nematoda) 3.9.NematodesNematodes Associations are arewith another another Nematodes ubiquitous ubiquitous (Nematoda) group group that have formed formed diverse diverse associations associations with with plants plants andand animals. animalsNematodes. Nematodes Nematodes are another use use beetles ubiquitousbeetles for group development that have of of formed their their young youngdiverse as asassociations well well as as for for with phoresis phoresis plants [26] [26 ] (Figures(Figuresand2 animals and 2 8and).. A Nematodes8 case). A of case the use of latter thebeetles in latter Dominican for in development Dominican amber of is amber theirshown young is with shown as the well withmycetophilous as the for phoresis mycetophilous nematode, [26] Cryptaphelencusnematode,(Figures 2Cryptaphelencus and dominicus 8). A case(Nematoda: dominicus of the latter (Nematoda: Aphelenchoidea), in Dominican Aphelenchoidea), amber whose is shown dauer whose with (resistant dauer the mycetophilous (resist stageant juveniles) stage werejuveniles)nematode, released were fromCryptaphelencus released the body from of dominicus their the body platypodine (Nematoda: of their carrier platypodineAphelenchoidea), (Coleoptera: carrier whose Curculionidae:(Coleoptera: dauer (resist Curculionidae Platypodinae)ant stage : (FigurePlatypodinaejuveniles) 30). Under were) (Figure normal released 30). conditions, from Under the normal bodywhen of the conditions, their platypodine platypodine when arrived carrier the atplatypodine its(Coleoptera: new habitat, arrived Curculionidae these at nematodes its new: wouldhabitat,Platypodinae leave these the nematodes beetle) (Figure and 30). developwould Under leave on normal fungi the beetle withinconditions, and the develo beetle’s whenp theon tunnels. platypodinefungi within Bacteria- arrived the feeding beetle’s at itsnematodes, tunnels. new habitat, these nematodes would leave the beetle and develop on fungi within the beetle’s tunnels. suchBacteria as the- diplogastrid,feeding nematodes,Scolytonema such dominicana as the diplogastrid,(Nematoda: Diplogastroidea),Scolytonema dominicana in Dominican (Nematoda: amber, Diplogastroidea),Bacteria- feeding in Dominican nematodes, amber, such asalso the used diplogastrid, platypodines Scolytonema for transport dominicana (Figure 31).(Nematoda: also usedDiplogastroidea), platypodines in Dominican for transport amber, (Figure also used31). platypodines for transport (Figure 31).

Figure 30. Dauer stages of the fungivorous aphelenchoidid nematode, Cryptaphelencus dominicus FigureFigure 30. 30.Dauer Dauer stages stages of of the the fungivorous fungivorous aphelenchoidid aphelenchoidid nematode, nematode, CryptaphelencusCryptaphelencus dominicus dominicus (Nematoda: Aphelenchoidea) that were phoretic on a platypodine (Coleoptera: Curculionidae) beetle (Nematoda:(Nematoda: Aphelenchoidea) Aphelenchoidea) that that were were phoreticphoretic on a platypodine platypodine (Coleoptera: (Coleoptera: Curculionidae Curculionidae)) beetle beetle in Dominican amber. Scale bar = 460 µm. inin Dominican Dominican amber. amber. Scale Scale bar bar= = 460460 µµm.m.

Figure 31. Two diplogastrid nematodes (Scolytonema dominicana (Nematoda: Diplogastroidea) adjacent to a platypodine beetle (Coleoptera: Curculionidae: Platypodinae) in Dominican amber. FigureFigureScale 31. bar 31.Two = Two140 diplogastrid µm. diplogastrid nematodes nematodes (Scolytonema (Scolytonema dominicana dominicana(Nematoda: (Nematoda: Diplogastroidea) Diplogastroidea) adjacent toadjacent a platypodine to a platypodine beetle (Coleoptera: beetle (Coleoptera: Curculionidae: Curculionidae Platypodinae): Platypodinae in Dominican) in Dominican amber. amber. Scale

barScale= 140 barµ m.= 140 µm.

Geosciences 2019, 8, x FOR PEER REVIEW 21 of 24 Geosciences 2019,, 98,, 184x FOR PEER REVIEW 2121 of of 24 Beetles are also parasitized by nematodes that develop in their body cavity and sometimes juvenileBeetles stages are of also these parasitized parasites by emerge nematodes when that the develop host enters in thei ther body resin. cavity One and such sometimes parasitic Beetles are also parasitized by nematodes that develop in their body cavity and sometimes juvenile nematodejuvenile stages is the of allantonematid, these parasites Palaeoallantonema emerge when the apionae host enters(Nematoda: the resin. Allantonematidae), One such parasitic that stages of these parasites emerge when the host enters the resin. One such parasitic nematode is emergednematode from is the its allantonematid,apionine (Coleoptera: Palaeoallantonema Brentidae) weevil apionae host (Nematoda: in Dominican Allantonematidae), amber (Figure that 32). the allantonematid, Palaeoallantonema apionae (Nematoda: Allantonematidae), that emerged from its Juvenilesemerged from of its another apioni ne parasitic (Coleoptera: allantonematid, Brentidae) weevilPalaeoallantonema host in Dominican dominicana amber (Nematoda: (Figure 32). apionine (Coleoptera: Brentidae) weevil host in Dominican amber (Figure 32). Juveniles of another Allantonematidae)Juveniles of another emerged parasitic from their allantonematid, rove beetle host Palaeoallantonema (Coleoptera: Staphylinidae) dominicana in (Nematoda:Dominican parasitic allantonematid, Palaeoallantonema dominicana (Nematoda: Allantonematidae) emerged from amberAllantonematidae) (Figure 33) [26, emerged27]. from their rove beetle host (Coleoptera: Staphylinidae) in Dominican theiramber rove (Figure beetle 33 host) [26, (Coleoptera:27]. Staphylinidae) in Dominican amber (Figure 33)[26,27].

Figure 32. Parasitic nematode, Palaeoallantonema apionae (Nematoda: Allantonematidae) (arrow) that emergedFigure 32. from Parasitic its apioni nematode,d weevil Palaeoallantonema host (Coleoptera: apionae Brentidae) (Nematoda:(Nematoda: in Dominican Allantonematidae) amber. Scale (arrow) bar = that420 µm.emerged fromfrom itsits apionid apionid weevil weevil host host (Coleoptera: (Coleoptera: Brentidae) Brentidae) in Dominicanin Dominican amber. amber. Scale Scale bar =bar420 = µ420m. µm.

Figure 33. ParasiticParasitic juveniles juveniles (arrow) (arrow) of the nematode, Palaeoallantonema dominicana (Nematoda: Allantonematidae)AllantonematiFigure 33. Parasiticdae) thatthat juveniles emerged emerged (arrow) from from their of their therove nematode, beetle rove (Coleoptera: beetle Palaeoallantonema (Coleoptera: Staphylinidae) Staphylinidae) dominicana host in (Nematoda: Dominican host in Dominicanamber.Allantonemati Scale amber. bardae)= 900Scalethatµ m.bar emerged = 900µm. from their rove beetle (Coleoptera: Staphylinidae) host in Dominican amber. Scale bar = 900µm.

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Mermithid nematodes nematodes parasitize parasitize terrestrial terrestrial and freshwater and freshwater insects as insects well as as other well invertebrates. as other Afterinvertebrates. developing After in the developing hemocoel in of the terrestrial hemocoel hosts, of theterrestrial post-parasitic hosts, the juveniles post-parasitic emerge and juveniles enter theemerge soil and where enter they the maturesoil where to thethey adult mature stage. to the One adult rare stage. fossil One shows rare fossil the mermithid,shows the mermithid,Heydenius lamprophilusHeydenius lamproph(Nematoda:ilus (Nematoda: Mermithidae) Mermithidae) that emerged fromthat a emerged lampyrid (Coleoptera:from a lampyrid Lampyridae) (Coleoptera: beetle inLampyridae) Dominican beetle amber in [26 Dominican] (Figure 34 amber). [26] (Figure 34).

Figure 34.34. AA mermithidmermithid nematode,nematode, HeydeniusHeydenius lamprophiluslamprophilus (Nematoda:(Nematoda: Mermithidae) that emergedemerged from its lampyrid (Coleoptera:(Coleoptera: Lam Lampyridae)pyridae) beetle host in Dominican amber. Scale bar = 1.9 mm.

4. Discussion The great great majority majority of of the the fossil fossil associations associations depicted depicted here here have have continued continued to the topresent. the present. Mites Mitesphoretic phoretic on weevils on weevils [10] and [10 bark] and bee barktles beetles[28] are [widespread28] are widespread today. Pseudoscorpions today. Pseudoscorpions have phoretic have phoreticassociations associations with extant with beetle extants and beetles other and insect other groups insect [12]. groups [12]. The interesting interesting modiﬁcation modification of of the the body body of extant of extant Trichopseniinae Trichopseniinae (Staphylinidae) (Staphylinidae) living in living termite in coloniestermite colonies is well knownis well todayknown and today specimens and specimens from Dominican from Dominican amber haveamber been have compared been compared to extant to formsextant informs Australia in Australia [29]. [29]. What is also interesting is that one of the Dominican specimens was found adjacent to an adult tineid moth. moth. Tineid Tineid moths moths are are known known associates associates of termite of termite colonies colonies in Africa in Africa and it and is likely it is thatlikely similar that associationssimilar association occur ins occur the Neotropics in the Neotropics [30]. [30]. Extant female female euphorine euphorine braconids braconids that that attack attack adult adult beetles beetles insert inserttheir ovipositor their ovipositor either through either thethrough intersegmental the intersegmental membrane membrane in the abdominal in the abdominal region (as region with Perilitus (as withspp.), Perilitus at the spp.), base at of the the base elytra of (asthe in elytraSyrrhizus (as inspp.) Syrrhizus or in thoracicspp.) or sutures in thoracic (as with suturesCosmophorus (as withspp.) Cosmophorus [31]. When spp.) development [31]. When is ﬁnisheddevelopment the mature is finished larvae the formmature a cocoonlarvae form in the a cocoon surroundings in the surroundings or attached toor theattached host asto thethe host case illustratedas the case here illustrated with the here host with beetle, theHabropezus host beetle, plaisiommus Habropezus. Euphorinesplaisiommus do. Euph not alwaysorines do kill not their always hosts uponkill their emergence hosts upon and thereemergence are records and there of some are largerecords hosts of recovering,some large whichhosts recovering, may have been which the may case withhave thebeen parasitized the case with elaterid the parasitized in Dominican elaterid amber in [ 31Domini]. can amber [31]. The tachinid egg on the thorax of the leafleaf beetlebeetle StenaspidiotusStenaspidiotus microptilus in DominicanDominican amber resembles the eggs of extant members of the Neotropical genus Strongygaster that deposits eggseggs on adult leaf beetles [[15].15]. Meloe triungulins are well known to have phoretic associations with extant bees and the biology of some species has been elucidated. When the triungulins are carried into bee nests, they devour bee eggs and larvae as well as any provisions, such as pollen and honey [31].

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Meloe triungulins are well known to have phoretic associations with extant bees and the biology of some species has been elucidated. When the triungulins are carried into bee nests, they devour bee eggs and larvae as well as any provisions, such as pollen and honey [31]. The cantharid beetle that was displaying a chemical defense response to a potential predator in Burmese amber is the earliest fossil record of a chemical defense response and shows that such responses, which occur today in these and other beetles, were present some 100 Mya [17]. Fungi can be a nutritional source for beetles. There are many studies on ambrosia fungi and their symbiosis with bark beetles [19]. There are also fungi that use beetles as hosts, including the trichomycete, Priscadvena corymbosa, that was emerging from the mouth of an elaterid beetle [23]. Records of nematodes associated with fossil beetles also have associations with contemporary family members. For instance, there are many cases of extant aphelenchoidid and diplogastrid nematodes associated with members of the Platypodinae [32]. There are also records of allantonematids parasitizing apionine weevils and rove beetles [32]. However, there does not appear to be any extant record of mermithid parasites of Lampyridae [32]. At this point, with 21 records from Dominican amber, four from Burmese amber and a single one from Mexican amber, it would appear that the number of beetles with associates from the three amber deposits are correlated with the availability of fossils from those three sites. Dominican amber specimens have been the easiest to obtain over the past 30 years. There must be examples of beetles with associates in Baltic amber, however that material has been diﬃcult for collectors to acquire.

5. Conclusions The many fossil associations depicted here that have continued to the present support the principle of behavior fixity or constancy [2,3]. In brief, this principle states that once successful associations between two or more separate lineages are established, they will continue as long as environmental conditions are favorable. Even if the partners of such associations become extinct at the specific or generic level, they are replaced by new lineages that continue the established alliances with little modification. Thus, specific behavioral patterns are often much more ancient than the specific lineages involved.

Funding: This research received no external funding. All photographs were taken by the author. Conﬂicts of Interest: The author declares no conﬂict of interest.

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