Reproductive Traits of an Invasive Alien Population of Grey Squirrel (Sciurus carolinensis) in Central Italy

Abstract

The reproductive cycle of an invasive alien Italian grey squirrel population was studied to understand its adaptation and limit its spread, in order to conserve the autochthonous red squirrel. Female and male genital traits were evaluated throughout the reproductive cycle, including the ovary, uterus, testicle, epididymis, seminiferous tubule morphometry, and germinative epithelium histology. Moreover, individual female fecundity was determined by counting uterine scars. Ovary width and uterus weight, length, and width reached their highest values in the luteal and pregnancy phases. On conducting a histological evaluation of the testicular germinal epithelium, four morphotypes related to the different reproductive phases of the male squirrels were identified: immature, pubertal, spermatogenesis, and regressive. Testicle and epididymis weights and seminiferous tubule diameters reached their largest values during spermatogenesis. Uterine scar analysis showed that 69% of the females had given birth to one or two litters, while 31% had no uterine scars. Litters were larger in the first breeding period than in the second; annual fecundity was 4.52 ± 1.88 uterine scars/female. Umbrian grey squirrels have adapted to their non-native range, showing two annual mating periods at times similar to those in their native range, and high reproductive success.

Seasonal Expression of NGF and Its Cognate Receptors in the Ovaries of Grey Squirrels (Sciurus carolinensis)

“…202.5, Tomahawk Live Trap Co., Hazelhurst, WI, USA) in both breeding (n = 5) and nonbreeding (n = 5) seasons. The traps were sheltered against sunlight and set far from busy roads in order to minimize stress in the captured squirrels [29]. The squirrels were captured in compliance with regulations regarding wildlife control laid down in Art.…”

“…19 of the Italian Law 157/92 "Rules for the protection of wild animals and homeotherms and for hunting", Habitat Directive 92/43/CEE, and Regulation n. 1143/2014 (22 October 2014) of the European Parliament (on the prevention and management of the introduction and spread of invasive alien species). The trapped animals were surgically gonadectomized [29,34], which allowed the collection of their ovaries. Within a few minutes, the ovaries to be used for investigating the gene expression were washed in an RNase-free phosphate-buffered saline solution and then frozen at −80 • C [35], while the ovaries that were to undergo immunohistochemical evaluation were fixed in 4% (w/v) formaldehyde in PBS (pH 7.4) for 24 h at room temperature and then processed using routine tissue processing techniques [36].…”

“…In our recent study [29], it was observed that the grey squirrel females belonging to the Umbrian grey squirrel population (central Italy) have two mating seasons, one from December to February and the other from April to June, with two peaks of litter production [21,24,30]. This seasonal breeding activity is interrupted by anestrous phases that generally occur in March and from July to November [29].…”

“…In this context, a classic example in Europe of the competitive exclusion of a native species by an alien species is the replacement of the native red squirrel (Sciurus vulgaris) by the introduced grey squirrel in the United Kingdom and Italy [26][27][28]. In our recent study [29], it was observed that the grey squirrel females belonging to the Umbrian grey squirrel population (central Italy) have two mating seasons, one from December to February and the other from April to June, with two peaks of litter production [21,24,30]. This seasonal breeding activity is interrupted by anestrous phases that generally occur in March and from July to November [29].…”

“…Various authors have highlighted the importance of gaining a better understanding of the reproductive system of this invasive species since it adapts very well to new environments and is characterized by a greater reproductive success than the native species [29,31,32]. Therefore, the aim of this study is to investigate the ovarian presence, distribution, and gene expression of NGF, NTRK1, and NGFR, as well as plasma NGF levels, during both breeding and nonbreeding seasons.…”