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Morphology Reveals the Unexpected Cryptic Diversity in Ceratophyllus Gallinae (Schrank, 1803) Infested Cyanistes Caeruleus Linnaeus, 1758 Nest Boxes

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Morphology Reveals the Unexpected Cryptic Diversity in Ceratophyllus Gallinae (Schrank, 1803) Infested Cyanistes Caeruleus Linnaeus, 1758 Nest Boxes Acta Parasitologica (2020) 65:874–881 https://doi.org/10.1007/s11686-020-00239-6 ORIGINAL PAPER Morphology Reveals the Unexpected Cryptic Diversity in Ceratophyllus gallinae (Schrank, 1803) Infested Cyanistes caeruleus Linnaeus, 1758 Nest Boxes Olga Pawełczyk1 · Tomasz Postawa2 · Marian Blaski3 · Krzysztof Solarz1 Received: 6 June 2019 / Accepted: 29 May 2020 / Published online: 8 June 2020 © The Author(s) 2020 Abstract Purpose The main aim of our study was to examine morphological diferentiation between and within sex of hen feas— Ceratophyllus gallinae (Schrank, 1803) population collected from Eurasian blue tit (Cyanistes caeruleus Linnaeus, 1758), inhabiting nest boxes and to determine the morphological parameters diferentiating this population. Methods A total of 296 feas were collected (148 females and 148 males), determined to species and sex, then the following characters were measured in each of the examined feas: body length, body width, length of head, width of head, length of comb, height of comb, length of tarsus, length of thorax and length of abdomen. Results The comparison of body size showed the presence of two groups among female and male life forms of the hen fea, which mostly difered in length of abdomen, whereas the length of head and tarsus III were less variable. Conclusion Till now, the only certain information is the presence of two adult life forms of C. gallinae. The genesis of their creation is still unknown and we are not able to identify the mechanism responsible for the morphological diferentiation of feas collected from the same host. In order to fnd answer to this question, future research in the feld of molecular taxonomy is required. Keywords Body size variability · Ceratophyllus gallinae · Fleas · Morphological diversity · Sexual size dimorphism Introduction Females and males of nearly all arthropods difer in their body size. This phenomenon is also widespread among insects and is called a sexual size dimorphism (SSD). SSD * Olga Pawełczyk [email protected] likely appears when growth patterns of females and males of the same species difer in their sensitivity to environmental Tomasz Postawa [email protected] conditions [1]. In addition, the larger size of body and par‑ ticular body parts is more desirable among insects. The main Marian Blaski [email protected] reasons of larger size selection may be the increase of mat‑ ing success in males and fecundity of females, what allows Krzysztof Solarz [email protected] to produce a bigger ofspring [1–8]. Moreover, seasonal changes of environment and presence of many diferences 1 Department of Parasitology, Faculty of Pharmaceutical between life forms during arthropods’ life cycle can cause Sciences in Sosnowiec, Medical University of Silesia, the phenotype variation among adult individuals [8, 9]. They Jedności 8, 41‑200 Sosnowiec, Poland 2 may difer in shape, behavior and their response to environ‑ Department of Vertebrate Zoology, Institute of Systematics mental factors. Heteromorphism—diferent forms at vari‑ and Evolution of Animals of the Polish Academy of Sciences, Sławkowska 17, 31‑016 Kraków, Poland ous periods of the male life cycle, is a phenomenon known among Acari, including groups of mites such as Astigmata 3 Department of Zoology, Faculty of Biology and Environmental Protection, University of Silesia, and Prostigmata [10–14]. It is often related to sexual behav‑ Bankowa 9, 40‑007 Katowice, Poland ior or male reproductive strategy and can lead to increased Vol:.(1234567890)1 3 Acta Parasitologica (2020) 65:874–881 875 reproductive success among heteromorphic males [11, 13]. hosts of C. gallinae belong blue (C. caeruleus) and great In turn, gynopolymorphism (sex carrying the polymorphism (Parus major) tits [28, 29]. Most of C. gallinae adults over‑ in female) was reported among representatives of order wintering in the cocoons and occur in relatively large num‑ Diptera (Drosophila melanogaster), Odonata (Coenagrion, bers in nests of their hosts during winter. In contrast to the Enallagma, Ischnura) and many species of Lepidoptera (e.g. birds breeding season, when feas disperse among birds gen‑ from Colias genus) [15–17]. erations [30, 31]. C. gallinae feas often occur with another Variability of ectoparasite population is caused by degree fea species—Dasypsyllus g. gallinulae (Dale, 1878) or with of host specifcity, the mode of parasite transmission and the blow fies of the genus Protocalliphora (Diptera: Calliphori‑ ability for adaptive phenotypic plasticity [18, 19]. Fleas are dae) in the same nest, which can afect bird reproductive obligatory external parasites of birds and mammals, thus performance [31, 32]. their more pronounced morphological variability can depend on their type of the host and the host living environment. Host Species Individual morphological characteristics of feas can be a result of host migration, its diet or condition [9, 20]. Exter‑ In this study, feas were collected from the blue tits C. caer- nal parasites are also subjected to a strong selection, which uleus nest boxes. Blue tits are common European passerine can lead to convergent evolved phenotypes among one or birds, which build their nests in natural tree‑holes and often more species. Furthermore, a strong selective pressure on inhabit nest boxes. Each spring, females lay around 10 eggs, loci, which controls morphological diferences in organisms, which are incubated and hatch 2 weeks later. C. gallinae can be caused by genetic isolation of the population of each infestation in nests and nest boxes signifcantly afects the host and the adaptation to a particular host [19, 21]. behavior of bird females [28, 33, 34]. Fleas demonstrate strong female‑biased SSD, what is a common trend among other groups of arthropods. Sexual Data Collection and Material Preparation size dimorphism decreases in larger species [22]. Further‑ more, feas do not demonstrate strong stable selection or The hen fleas C. gallinae were collected in the period strong constraints on female size. For example, egg produc‑ between 1998–2003 from blue tits (C. caeruleus) nest tion and egg size in feas are reported to be independent of boxes, which occurred in Panewniki Forestry Commission, body size [23, 24], but were explained well by the patterns land in the vicinity of Ruda Śląska (Upper Silesia, in the of relationships with their hosts. A high morphological vari‑ Southern Poland). Nest boxes were placed in deciduous for‑ ability between males and females was reported in Cera- est of Panewniki Forestry Commission, and systematically tophyllus hirundinis (Curtis 1826) collected from nests of examined throughout the year except for May, when tits lay Delichon urbica (Linnaeus 1758) (Upper Silesia, Poland) eggs and nestlings hatch. Nest boxes and feas were not col‑ [25]. Similar pattern was observed in a morphological vari‑ lected at that time, in order to protect birds. All feas were ability of Ceratophyllus gallinae (Schrank 1803) collected isolated from the nests and litter collected from nest boxes from Cyanistes caeruleus Linnaeus 1758 (before Parus by using Tullgren apparatus. All specimens were preserved caeruleus) nests. These results demonstrate that both males in 70% ethyl alcohol and preparated. Fleas were placed on and females manifested a high morphological variability [9]. microscopic permanent slides in Berlese solution. C. gal- Main aims of our study are to examine the morphological linae were determined according to Skuratowicz key [26]. diferentiation between and within sex of population col‑ All specimens were deposited in Department of Zoology at lected from Eurasian Blue Tits C. caeruleus inhabiting nest the University of Silesia (Katowice, Poland). A total of 296 boxes and to determine morphological parameters diferen‑ feas were collected, including 148 females and 148 males. tiating this population. To determine feas to species, sex and to measure morpho‑ logical features optical microscopy were used (Olympus CH40). The following characters were measured in each of Materials and Methods the examined feas: body length, body width, length of head, width of head, length of comb, height of comb, length of Ectoparasite Species tarsus, length of thorax and length of abdomen. The exam‑ ined material has been clustered into males and females, The hen fea C. gallinae is a common species in Europe, and after preliminary morphometric analysis into males North America and New Zealand, which has an extremely and females with a typical and smaller body size for exam‑ wide range of parasitizing hosts including 72 wild birds’ ined fea species. SSD‑related traits are length and height species and about 15 species of mammals. This fea regularly of comb. Moreover, the body length, body width, length of invades poultry and could cause the fatal iron defciency, thorax, length of abdomen, length of head and width of head anemia and allergic dermatitis of fowls [26–28]. To the main could be determined by SSD. These six features could be 1 3 876 Acta Parasitologica (2020) 65:874–881 also determined by the nutritional status of individual. The length of tarsus depends on physiological diferences, such as jumping performance [35]. Data Analysis Data were analyzed in several steps. Initially, sex determi‑ nation and morphological measurements specimens were performed. Due to presence of noticeable diferences in their size: normal type and smaller type, specimens were preliminary divided into two subgroups. The “small” and “typical” forms were previously marked by
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