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, 8 (1), 1924

Parasitised Feathered Dinosaurs as Revealed by Cretaceous Amber Assemblages

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Parasitised Feathered Dinosaurs as Revealed by Cretaceous Amber Assemblages

Enrique Peñalver et al. Nat Commun.

Erratum in

Abstract

Ticks are currently among the most prevalent blood-feeding ectoparasites, but their feeding habits and hosts in deep time have long remained speculative. Here, we report direct and indirect evidence in 99 million-year-old Cretaceous amber showing that hard ticks and ticks of the extinct new family Deinocrotonidae fed on blood from feathered dinosaurs, non-avialan or avialan excluding crown-group birds. A †Cornupalpatum burmanicum hard tick is entangled in a pennaceous feather. Two deinocrotonids described as †Deinocroton draculi gen. et sp. nov. have specialised setae from dermestid beetle larvae (hastisetae) attached to their bodies, likely indicating cohabitation in a feathered dinosaur nest. A third conspecific specimen is blood-engorged, its anatomical features suggesting that deinocrotonids fed rapidly to engorgement and had multiple gonotrophic cycles. These findings provide insight into early tick evolution and ecology, and shed light on poorly known arthropod-vertebrate interactions and potential disease transmission during the Mesozoic.

Conflict of interest statement

The authors declare no competing financial interests.

Figures

Fig. 1
Fig. 1
Cornupalpatum burmanicum hard tick entangled in a feather. a Photograph of the Burmese amber piece (Bu JZC-F18) showing a semicomplete pennaceous feather. Scale bar, 5 mm. b Detail of the nymphal tick in dorsal view and barbs (inset in a). Scale bar, 1 mm. c Detail of the tick’s capitulum (mouthparts), showing palpi and hypostome with teeth (arrow). Scale bar, 0.1 mm. d Detail of a barb. Scale bar, 0.2 mm. e Drawing of the tick in dorsal view indicating the point of entanglement. Scale bar, 0.2 mm. f Detached barbule pennulum showing hooklets on one of its sides (arrow in a indicates its location but in the opposite side of the amber piece). Scale bar, 0.2 mm
Fig. 2
Fig. 2
Confocal laser scanning microscopy images showing the hard tick morphology. a Habitus in ventral view of the Cornupalpatum burmanicum nymph associated with feathers. Scale bar, 0.2 mm. b Detail of the gnathosoma and coxal area in ventral view revealing the absence of genital pore. Scale bar, 0.1 mm. c Dorsal view detail of the gnathosoma and anterior part of the scutum (arrow indicates the lateral margin of the scutum). Scale bar, 0.1 mm
Fig. 3
Fig. 3
Morphology of the new tick family Deinocrotonidae. a Holotype (left) and paratype male in ventral view (arrows indicate the location of some entangled hastisetae of the beetle family Dermestidae). Scale bar, 1 mm. b Engorged paratype female in dorsolateral view. Scale bar, 1 mm. c Pseudoscutum (arrow) of specimen in b. Scale bar, 0.5 mm. d Paratype male in dorsal view. Scale bar, 0.5 mm. e Dorsal surface of the tarsus I from the holotype, showing Haller’s organ, an aggregate of chemoreceptors, mechanoreceptors, and hygroreceptors in ticks for locating hosts and mates (lines mark the length of the organ). Scale bar, 0.1 mm. f Transverse genital aperture between coxae II, coxal spurs, and basis capituli from the holotype. Scale bar, 0.5 mm. g Pitted dorsal integument without elevations in the pseudoscutum of the same specimen. Scale bar, 0.1 mm. h Engorged paratype female in ventral view with detail of the spiracle. Scale bar, 1 mm. i Genital aperture between coxae II of the paratype male. Scale bar, 0.2 mm. j Pulvillus and pretarsal claws of the holotype. Scale bar, 0.1 mm. k Lateral body margin showing the non-convoluted, mound-like elevations of the integument (arrows) between pits of the same specimen. Scale bar, 0.1 mm. l, m Anus and preanal groove of the paratype male and engorged paratype female, respectively. Scale bars, 0.1 mm. a, b, e, g, ik obtained with compound microscopy, the remainder with CT-scans
Fig. 4
Fig. 4
Photomicrographs showing some anatomical features of the new family Deinocrotonidae. Holotype (AMNH Bu-SA5a) (a, f, h); allotype (CM 63007) (b, c); paratype male (AMNH Bu-SA5b) (d, e). ab Right palp and right and left palpi in ventral views, respectively, with indication of the number of visible palpomeres. Scale bars, 0.1 mm. c Pseudoscutum and detail of the integument showing mound-like elevations between the pits (see inset). Scale bar, 0.5 mm. d Coxa II showing a row of three spurs (arrows). Scale bar, 0.1 mm. e Ruffled surface of the left genu III. Scale bar, 0.1 mm. f Articulations of the left leg III in ventral view. Note the notch-like processes (arrows). Scale bar, 0.1 mm. g Haller’s organ in dorsal surface of the tarsus I (bottom structure is the proximal capsule, in contact with the distal pit). Arrows point to sensilla. Scale bar, 0.05 mm. h Trochanterofemoral articulation of the right leg I. Note the notch-like processes (arrows). Scale bar, 0.1 mm
Fig. 5
Fig. 5
CT-scan images showing some anatomical features of the new family Deinocrotonidae. Holotype (AMNH Bu-SA5a) (a, c, d, f, g); paratype male (AMNH Bu-SA5b) (b, e); engorged paratype female (CM 63001) (h, i). a Pseudoscutum showing the cervical grooves (arrows). Note the abundant bubbles (bottom). Scale bar, 0.5 mm. b Pseudoscutum in anterodorsal view showing its posteriorly broadened anterior margin and the cervical grooves (right arrows). Scale bar, 0.5 mm. c Trochanterofemoral articulation of the right leg III (femur length ca. 0.5 mm). Note the notch-like processes (arrows). d Ruffled genual surface (genu length ca. 0.6 mm). e Right spiracle in frontal view. Scale bar, 0.2 mm. f Left spiracle in lateral view (arrow). Scale bar, 0.2 mm. g Post-genital, anteroventral depressed area (bold arrow) and genital groove medially divided in two sections (thin arrows). Scale bar, 1 mm. h Habitus showing the deformation of the body and the completely stretched integument due to engorgement (arrow indicates the spiracle). Scale bar, 1 mm. i Detail of the ventral surface showing the genital aperture extruded as a rounded protuberance (arrow). Scale bar, 1 mm
Fig. 6
Fig. 6
Hastisetae on the two deinocrotonid ticks preserved together and comparisons with extant Megatominae. a Hastiseta preserved with its spear-shaped head entangled in a leg of the paratype male (AMNH Bu-SA5b). Scale bar, 0.1 mm. b Detail of the spear-shaped head of the hastiseta from a. c Hastiseta with the spear-shaped head (arrow) entangled in the holotype (AMNH Bu-SA5a). Scale bar, 0.05 mm. d Hastiseta with the spear-shaped head photographed from above entangled in the base of the right femur I of the paratype male. Scale bar, 0.05 mm. e Spear-shaped head magnified from d showing its six knobs. f Multi-segmented portion of a hastiseta, without preserved head, on the posterior body margin of the holotype (segments to the right are distal). Scale bar, 0.05 mm. g Extant larval cast-off skin after molt in dorsal view of the Megatominae genus Anthrenus (arrows indicate two of the hastisetal tufts on abdominal segments), which can be found in bird nests. Scale bar, 0.5 mm. h Several hastisetae from a posterior tuft from g. Scale bar, 0.05 mm. i Basal (left), middle and distal (right) multi-segmented sections of one hastiseta from h. Scale bar, 0.02 mm
Fig. 7
Fig. 7
Reconstruction of the male and engorged female of Deinocroton draculi. Upper dorsal, ventral, frontal, and lateral views based on CT-scans of the holotype male (see Supplementary Movie 1) (Artist: Oscar Sanisidro). Lower lateral and ventral reconstructions based on CT-scans of the engorged paratype female (performed by the authors using elements from the male model performed by O. Sanisidro). Both reconstructions at the same scale and with modifications based on compound microscope observations. Scale bar, 1 mm
Fig. 8
Fig. 8
Amber drops attached to legs of the deinocrotonid paratype male (AMNH Bu-SA5b). a Dorsal view of the specimen (arrows indicate the amber drops). Scale bar, 1 mm. b Left tarsus I dorsally covered by an amber drop. Scale bar, 0.2 mm. c Right tarsus I coated by an amber drop with abundant bubbles inside (arrow indicates the claws). Scale bar, 0.2 mm
Fig. 9
Fig. 9
Reconstruction of the habitus of Deinocroton draculi on an immature feathered dinosaur. The reconstruction shows two unengorged males (left) and a female feeding to engorgement (right). Male body length ca. 3.9 mm. Colours of the ticks are conjectural but based on the colouration seen in the related nuttalliellid ticks. Performed by the authors using models of the males created by the artist Oscar Sanisidro
Fig. 10
Fig. 10
Ticks and their possible feathered hosts in deep time. Simplified phylogenies of parasitiform Acari (top) and tetanuran Dinosauria leading to the bird lineage (bottom). Although filamentous integumentary structures are known in some ornithischians and pterosaurs, the latter are not represented for not belonging to the bird lineage. Time ranges supported by the fossil record are depicted with thick lines; those inferred appear in thin lines. Asterisk marks the inferred origin of modern birds (Neornithes). Known fossil occurrences of parasitiform mites (all in amber; stars correspond to tick records that can be related to feathered dinosaur hosts, presented in this paper; quaternary records excluded): Lebanese amber—1, Mesostigmata indet.; Burmese amber—2, ?Opilioacarus groehni; 3 Cornupalpatum burmanicum, three specimens including the new one described herein entangled in a pennaceous feather; Compluriscutata vetulum, Amblyomma birmitum, and Amblyomma sp.; 4 Argasidae indet.; 5 Deinocroton draculi (herein); Raritan amber—6, Carios jerseyi; Baltic amber—7, Sejus bdelloides; Aclerogamasus stenocornis; Microgynioidea indet.; 8 Paracarus pristinus; ?Opilioacarus aenigmus; 9 Ixodes succineus and Ixodes sp.; Mexican amber—10, Dendrolaelaps fossilis; Dominican amber—11, Amblyomma sp.; 12 Ornithodoros antiquus. An unpublished, badly preserved specimen from Spanish amber (105 Ma) has been not included, but it could be assignable to Deinocrotonidae. See Supplementary Notes 3, 4, and 6 for inferred time ranges used, parasitiform records shown, oldest occurrences of dinosaur groups depicted, and discussion on feather evidence in non-avialan dinosaurs. Neog. + Q. Neogene and Quaternary, D.F.H. diverse feeding habits, S.F. solid feeders, F.F. fluid feeders

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