The first flea with fully distended abdomen from the Early Cretaceous of China
© Gao et al.; licensee BioMed Central Ltd. 2014
Received: 11 April 2014
Accepted: 21 July 2014
Published: 27 August 2014
Fleas, the most notorious insect ectoparasites of human, dogs, cats, birds, etc., have recently been traced to its basal and primitive ancestors during the Middle Jurassic. Compared with extant fleas, these large basal fleas have many different features. Although several fossil species with transitional morphologies filled the evolutionary blank, the early evolution of these ectoparasites is still poorly known.
Here we report a new flea with transitional characters, Pseudopulex tanlan sp. nov., assigned to Pseudopulicidae, from the Lower Cretaceous Yixian Formation of Liaoning Province, China. Different from the previously described pseudopulicids, P. tanlan has relatively smaller body size but lacking any ctenidia on the tibiae or body, while the male with comparatively smaller and shorter genitalia. On the other hand, P. tanlan has some characters similar to the transitional fleas of saurophthirids, such as, a small head, short compacted antennae, small pygidium and many stiff setae covering the body.
Even though other possibilities can not be ruled out, the female specimen with extremely distended abdomen suggests that it might have consumed its last meal before its demise. Compared with other reported female flea fossils, we calculate and estimate that P. tanlan sp. nov. might have consumed 0.02 milliliter (ml) of blood, which is about 15 times of the intake volume by extant fleas. These new findings further support that fleas had evolved a broad diversity by the Early Cretaceous.
After Riek reported the first flea-like insect, Tarwinia australis, from the Early Cretaceous of Koonwarra, Australia in 1970 , Ponomarenko described a flea-like fossil, Saurophthirus longipes, in 1976 . In the past 36 years, there were no more fossil fleas described from the Mesozoic, even though thousands of other insect taxa have been reported from around the world -. Extinct Strashilidae have been described as flea relatives , but recently they are re-interpreted as aberrant Diptera . Since 2012, several flea fossils from the Mid-Mesozoic of northeastern China shed light on the origin and evolution of the basal and transitional fleas -. They were reported to live on diverse hosts such as coexisting feathered dinosaurs, pterosaurs, primitive birds and medium-sized mammals -. It has been proposed that fleas might have originated from an extinct clade of scorpionflies ,. Mesozoic fleas have been organized in three families . Pseudopulicidae, possessing large body sizes and very robust piercing-sucking mouthparts, are considered as the basal and stem group of fleas -. Monotypical Tarwiniidae differ from Pseudopulicidae and Saurophthiridae in having free maxillary palp (vs. no free palp), but similar to Pseudopulicidae in having tibial ctenidia . Saurophthiridae are more similar to extant fleas than pseudopulicids in the medium body size, short piercing suctorial stylet mouthparts and partially internal male genitalia (vs. completely external in Pseudopulicidae) ,. Up to now, 5 genera with 8 species have been assigned to these three flea families in the Mesozoic. They were reported to live on diverse hosts such as coexisting feathered dinosaurs, pterosaurs, primitive birds and medium-sized mammals -,.
Herein, we describe a new flea with transitional morphology from the Early Cretaceous, Yixian Formation of Liaoning Province, China. The new female flea has a fully distended abdomen, suggesting it might have consumed its last meal before its demise and subsequent fossilization. Comparing this female specimen with other known female fossil fleas, we calculate and estimate the volume of blood intake by this flea. These new findings support the notion that fleas had already a broad diversity by the Early Cretaceous.
The specimen was examined under a Leica MZ 16.5 dissecting microscope, and the photographs were taken with a digital camera system connecting with the Leica MZ 16.5. In some photos, ethanol (95%) was put on the surface of the specimen to improve clarity and contrast of details. Line drawings were prepared with CorelDraw X6 and Adobe Photoshop CS 6.0.
We summarize all known female fleas from the Mesozoic in Additional file 1: Table S1 (see in ). Based on the data from the Additional file 1: Table S1, the average ratio of the width of abdomen / body length is 0.28. We estimate that the abdominal width of the female of Pseudopulex tanlan is about 2.6 mm (9.26 * 0.28) without swelling. When it is fully distended, the abdomen width is 4.0 mm. To estimate the volume of blood intake, we select the 3rd to 7th segments (with a length of 4.46 mm) as the expandable parts, and calculate an ellipsoid volume for the abdomen (Additional file 2: Figure S1, see in ). We get two different ellipsoids (Additional file 2: Figures S1A and C), one has dimensions of radii of 2.23 mm, 2 mm and 2 mm (Additional file 2: Figure S1B), the other has radii of 2.23 mm, 1.3 mm and 1.3 mm (Additional file 2: Figure S1D). We calculate the change of the volumes between these two ellipsoids based on the following formula: V = 4/3 * π * a * b * c (a, b, c represent the three radii of the ellipsoid, π = 3.14). In our ellipsoids, the volume change is: V1 = 4/3 * 3.14 * 2.23 * 2 * 2-4/3 * 3.14 * 2.23 * 1.3 * 1.3 ≈ 22mm3. Therefore, we estimate the volume of blood intake by Pseudopulex tanlan is nearly 0.02 cc (ml). (see the Additional file 1: Table S1 and Additional file 2: Figure S1, are available at https://datadryad.org, doi: 10.5061/dryad.q4jv0, see in ).
This published work and the nomenclatural acts it contains have been registered in Zoobank (http://zoobank.org): Publication - urn:lsid:zoobank.org:pub:C9B16650-CFCD-4712-B3FD-F7986A91C472;new species - urn:lsid:zoobank.org:act:65C13577-AB40-4102-8970-8AB321BB70CC.
Description of the specimens
Insecta Linnaeus, 1758.
Siphonaptera Latreille, 1825.
Family Pseudopulicidae Gao, Shih & Ren, 2012.
Pseudopulex Gao, Shih & Ren, 2012
Pseudopulex tanlan Gao, Shih, Rasnitsyn & Ren sp. nov.
`Tanlan’ means `avaricious’ in Mandarin Chinese, referring to the fully distended abdomen and possibly voracious feeding.
Medium body size (about 10 mm long), head and thorax relatively small. Body covered with stiff, short bristles and setae. Tibia without ctenidia. Distal abdominal segments not sclerotized. Female with fore tibia about half as long as femur, cerci distinct, reaching end of abdomen. Male with relatively small and short genitalia. Mouthparts unknown.
Holotype female, No. CNU-SIP-LL2013002; paratype (allotype) male, No. CNU-SIP-LL2013003. Only a single plate exists for each specimen. They are housed in the Key Laboratory of Insect Evolution and Environmental Changes at the Capital Normal University (CNU).
Locality and age
Both holotype and paratype (allotype) were collected from the Early Cretaceous Yixian Formation, Dawangzhangzi Village, Lingyuan City, Liaoning Province, China, which was dated to be 124.6 ± 0.1 Myr ,.
The new species differs from P. jurassicus and P. magus in: small body size (about 10 mm long), short body vestiture, relatively short female fore tibia and small male genitalia. It differs from Hadropsylla Huang et al.  in presence of distinct cerci and small distinct pygidium in female (vs. invisible in Hadropsylla). Additionally, it differentiates from Tyrannopsylla Huang et al.  in apical abdominal segments not sclerotized and in female cerci reaching abdominal apex (vs. female Tyrannopsylla cerci not reaching abdominal apex, segment 8 sclerotized laterally and segment 9 at least dorsally, and male sterna 6-9 sclerotized).
Classification of Pseudopulex tanlansp. nov.
Although Pseudopulex tanlan sp. nov. does not have ctenidia on the tibiae or body, nor preserved mouthparts, we consider it belonging to Pseudopulicidae and hence to Siphonaptera based on its wingless body covered with many stiff setae, characteristic helmet-like head, short and slightly fusiform antenna comprising compact short antennomeres, highly simplified thorax with segments similar to abdominal ones in size and form, legs with long tarsi and long, thin and gently curved claws with characteristic small basal lobe, female abdomen soft and distensible with eight well-visible spiracles and external male genitalia. It differs from other known pseudopulicids in having smaller body and head and shorter vestiture, male with shorter and smaller genitalia, and female with distinct cerci reaching the end of abdomen. Four enigmatic ovate structures are revealed at the posterior part of heads of both female and male of P. tanlan (Figures 1C, D and 2D). Such structures have never been observed in other insects before, and their possible function is obscure.
Preliminary phylogeny of known fleas of Mesozoic
Behavior of Pseudopulex tanlansp. nov
The female P. tanlan is the first flea from the Mesozoic showing fully distended abdomen. All other known females of Mesozoic fleas are covered with dense setae on the abdomens, so it is difficult to identify the boundary between segments. Female P. tanlan is exceptional in having wide and clear segmental boundaries. Additionally, its ratio of the width of abdomen to the body length is about 0.43 vs. an average of 0.28 for other reported Mesozoic female fleas (Additional file 1: Table S1, see in ). Based on the ratio data above, we estimate the non-swelling abdominal width of the female P. tanlan is about 2.6 mm in contrast to 4.0 mm when fully distended. We consider that the most inflated 3rd to 7th segments of the distensible abdomen is a reservoir for holding its blood intake. Generally, examples of such broadly distended abdomens are very rare in the fossil record . Due to the well-preservation of this fossil specimen without any distinct signs of disarticulation, we consider decomposition as less probable as the cause of abdominal swelling. However, we can not rule out the inflation caused by carrying eggs, even though the effect of egg load on abdominal size is much less significant as evidenced by extant haematophagous insects like mosquitoes, biting midges and others.
This is the first time that two Mesozoic fleas of P. tanlan with bodies in partially lateral view but heads in dorsal view (Figures 1A and 2A) are described. It is of interest to note that all Mesozoic fleas (except for Tarwinia) are preserved in dorsoventral position implying more or less dorsoventral depressed body in contrast to laterally compressed extant fleas and, by inference, Tarwinia. The female holotype of P. tanlan is preserved in partially lateral position, with all legs to one side, while the male paratype, in half-lateral position with legs directed to both sides. For the male fossil, its position can be interpreted as a result of a lateral direction of its robust legs which make it difficult for the insect taking a true lateral position, and a cylindrical to slightly compressed body somewhat turned sidewise during burial. In fact, this inference might be at least partly applicable to the male fossil of Tarwinia as well . Unlike these, the fully distended body of female P. tanlan can be considered as near circular in section, and having comparatively weak legs, the insect was able to take almost any occasional position under the burial circumstances.
This inference that the female P. tanlan had a highly distensible abdomen which took nearly ovoid form under a complete blood load, make it possible for us to assess, even though roughly, the extent of its full diet. By calculating the volume changes from non-swelling to fully distended, we estimate an approximate volume of 0.02 cc (ml) of blood intake for P. tanlan (Additional file 2: Figure S1 see in ). This volume is 15 times of the volume that extant fleas are able to consume in a meal ,.
Up to date, no more than 10 specimens of basal and transitional flea fossils have been collected from about 300 thousands of fossil insects in the CNU Lab. They have diverse and different morphological characters supporting the notion that the Cretaceous might be a significant transitional period for fleas, during which several groups with relatively reduced body sizes and other transitional characters gradually appeared (Figure 3). All these early fleas might have lived and fed on coexisting feathered dinosaurs, pterosaurs, primitive birds or medium-sized mammals coexisting in northeastern China -. These diverse hosts and their various life styles during the Early Cretaceous might be a driving force to enhance the flourishing and diversification of fleas.
The authors declare that the study makes no uses of human, clinical tools and procedures, vertebrate and regulated animal subjects and/or tissue, and plants.
Availability of supporting data
TPG, CKS and APR collected, illustrated and analyzed the data. TPG and DR designed the research plan. XX and SW offered vertebrate host information. TPG, CKS, APR, XX and DR prepared the manuscript. All authors read and approved the final manuscript.
We thank Y.Z. Yao, Y.J. Wang, C.F. Shi for discussions, Q. Yang for suggestions and preparing the specimens. D.R. was supported by grants from the National Basic Research Program of China (973 Program; 2012CB821906), the National Natural Science Foundation of China (No. 31230065, 41272006), Great Wall Scholar and KEY project of Beijing Municipal Commission of Education Project (grant KZ201310028033), Program for Changjiang Scholars and Innovative Research Team in University (IRT13081); T.P.G was supported by the Beijing Natural Science Foundation (5144024) and the National Natural Science Foundation (31401993). X.X. was supported by the National Natural Science Foundation of China (grant 41120124002); and A.P.R. was supported by the Russian Academy of Sciences Presidium program “Biosphere Origin and Evolution of Geo-Biological Systems”.
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