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.

Keywords: alien invasive species; competitive exclusion; grey squirrel; morphometry; red squirrel; reproduction; uterine scar.

Figure 1

(a) An ovary with a corpus luteum (arrow) on the surface. (b) A reproductive apparatus, after cutting the broad ligament and stretching, composed of the ovaries and fallopian tubes (arrows), uterine horns (arrowhead), and vulva (v); two uterine horns placed side by side in their distal end (bold arrow). The broad ligament infiltrated by adipose bodies (*) can be observed. The dashed line indicates that the length of the uterus was measured between the two proximal ends. (c) A white, small, ribbon-like and quite relaxed uterus belonging to an immature squirrel. (d) Two embryonic vesicles (arrows) are contained within a uterus strongly folded back on itself and forming spiral loops. Bladder (*) and vulva (v) are shown. (e) Dorsal surface with a transverse groove (arrow) defining the border between the cervix and the vagina. The bladder (*) can be observed below the vagina. (f) Distal and medial portion of the two uterine horns opened to show longitudinal folds of the mucosa. The arrows indicate the two external orifices of the uterus.

Figure 2

A uterus after the treatment to evidence uterine scars. The arrows highlight more recent darker scars, while the arrowheads indicate older, lighter-coloured scars.

Figure 3

Testicles belonging to squirrels of different ages and breeding status.

Figure 4

Images of testicles in different reproductive phases. (a) Immature phase: germinal epithelium where tubules are small and devoid of lumen; the epithelium consists of numerous Sertoli cells located at the base and some spermatogonia with abundant cytoplasm in a more central position. (b) Pubertal phase: some tubules have large lumen and the epithelium consists mainly of basal Sertoli cells and primary spermatocytes in the luminal compartment; round spermatids and a cluster of Leydig cells can also be observed. (c) Spermatogenesis phase: all tubules show a large lumen; epithelium is completely formed and is in active spermatogenesis with elongated spermatids. (d) Regression phase: testicles with degenerated germinal cells occupying the lumen.

Figure 5

Images of epididymis in different reproductive phases. (a) Immature phase: the diameter of the epididymis is small and the lumen is empty. (b) Spermatogenesis phase: the diameter of the epididymis is larger and it is full of spermatozoa. (c) Regressive phase: cell debris and squamous cells can be observed in the epididymis lumen.