Mortality Causes in Captive Cantabrian capercaillie (Tetrao urogallus cantabricus) in Spain

Abstract

The Cantabrian capercaillie (Tetrao urogallus cantabricus) is one of the most severely threatened subspecies of capercaillie. Its current population range is restricted to a small area of the Cantabrian Mountains (northwestern Spain), with only around 200 individuals remaining. As part of the national strategy for the conservation of the subspecies, the Cantabrian capercaillie Captive Breeding Center of Sobrescobio opened in 2009. Here, we use the information provided by the necropsies performed in this facility on 29 individuals (11 males, 13 females and 5 undetermined; 16 chicks and 13 adults) in order to describe the main mortality causes of captive-bred Cantabrian capercaillies. After necropsy, tissue samples were taken for evaluation using standard methods in histology and microbiology. The majority of the captive animals (18/29, 62.07%) died due to infectious diseases, mainly due to Escherichia coli, Clostridium perfringens, or Aspergillus fumigatus infection. The remaining 11 animals died due to stress-related processes (i.e., rupture of the heart apex and cardiomyopathy or neurogenic shock) (8/29, 27.59%), duodenal obstruction and coelomitis (1/29, 3.45%), perforation of the proventriculus and heart with a briar branch (1/29, 3.45%) or euthanasia due to a valgus leg deformity that prevented proper animal welfare (1/29, 3.45%). Young animals (i.e., younger than 2 months) died mainly due to infectious diseases (14/16, 87.5%), while stress-related causes were responsible for most adult deaths (7/13, 53.85%). We additionally report that two free-ranging adult males died due to exertional myopathy. This study provides relevant information for reducing mortality in captive capercaillies and improving both living conditions in captivity and the adaptation of these animals to the wild.

Keywords: Cantabrian capercaillie; Tetrao urogallus cantabricus; aspergillosis; bacterial diseases; captivity; mortality causes; myopathy; pathology; valgus leg deformity.

Figure 1

Map showing the Cantabrian capercaillie, Tetrao urogallus cantabricus, distribution range. Approximate distributions for 1970 and 2020, based on [17] are shown in light gray and dark gray, respectively. The locations of the Cantabrian Capercaillie Breeding Centers of Sobrescobio (Sobrescobio CCBC, Asturias province) and Valsemana (Valsemana CCBC, León province) are also shown. The upper-left figure represents the entire distribution range of the species in Europe. Images of male (left) and female (right) Cantabrian capercaillies can be seen at the top.

Figure 2

Colibacillosis (A,B) and clostridiosis (C–F) in Cantabrian capercaillies. (A) Typhlitis due to Escherichia coli infection is observed, characterized by epithelial cell damage of the mucosa and inflammatory infiltrate. Hematoxylin-eosin stain. Inset: Gram-negative bacilli compatible with E. coli are present on the apical surfaces of mucosal epithelial cells. Gram stain. (B) Congestion and hemorrhage in kidney of an animal with colibacillosis. Hematoxylin-eosin stain. (C) Hemorrhagic enteritis is observed in a capercaillie with Clostridium perfringens infection. (D) Histological features in the intestine of a capercaillie with clostridiosis. Necrotic typhlitis is observed; stars indicate hemorrhages. Destruction of intestinal mucosa and network of fibrin are also detected. Hematoxylin-eosin stain. Inset: Presence of numerous Gram-positive bacilli adhered to the mucosal epithelium are shown. Gram stain. (E) Necrotic hepatitis with a focus of necrosis (star) in the liver parenchyma is observed. Hematoxylin-eosin stain. Inset: Multiple whitish-yellowish foci of necrosis (star) are observed in the liver. (F) Numerous Gram-positive bacilli compatible with Clostridium spp. are located in the focus of necrosis observed in (E). Gram stain.

Figure 3

Aspergillosis in a Cantabrian capercaillie. (A) Gross lesion (arrow) due to Aspergillus fumigatus in a capercaillie. (B) Numerous nodules (greenish-white granulomas, arrow) in air sacs of a capercaillie with acute aspergillosis are observed. (C) Lung. Severe pneumonia is observed, with a parabronchus containing numerous, dichotomously branched, septate fungal hyphae (stars), disclosed using PAS staining. Inset: Conidiophores (arrows) are seen in this severe pulmonary infection. PAS stain. (D) Kidney. Granulomatous nephritis with numerous hyphae and few conidiophores in the renal cortex (star) are observed. PAS stain.

Figure 4

Stress-related neurogenic shock in a Cantabrian capercaillie. Disseminated intravascular coagulation-DIC (i.e., microthrombi, arrows) in a renal glomerulus is observed.

Figure 5

Rupture of the heart apex and cardiomyopathy in a Cantabrian capercaillie. (A) Rupture of the heart apex with associated hemorrhage is observed (arrow). (B) Fragmentation of myocardial fibers, as well as prominent inflammatory infiltrate mainly made up of macrophages (star), can be observed. Hematoxylin-eosin stain. (C) Myodegeneration is highlighted using Mallory Azan staining. Only the unaffected fibers are stained in red. (D) Calcification (mineralization) (in black, arrows), hyalinization, necrosis of muscle fibers, and an infiltrate of macrophages are observed. Von Kossa stain.

Figure 6

Valgus leg deformity in a Cantabrian capercaillie. (A) The left leg is bent outwards at the hock joint (left image). The animal also shows lateral tilting of the distal tibiotarsal condyles (arrow, right image). (B) Myotonic dystrophy (stars) and fibrous cartilaginous metaplasia (asterisk) are observed in the region of the tendon and skeletal muscle associated with the femoral head. Hematoxylin-eosin stain. (C) Degeneration of muscle fibers that are atrophied (in red, arrows) and replaced by adipose tissue (stars) is observed using Masson´s trichrome stain. (D) Detail of the fibrous cartilage metaplasia, where chondrocytes are organized forming parallel rows between the collagen bundles (arrows). Masson´s trichrome stain.

Figure 7

Proventriculus perforation with a briar branch (A, arrow) and subsequent right heart ventricle perforation (B, arrow) in a capercaillie.

Figure 8

Severe exertional myopathy in a Cantabrian capercaillie in the supracoracoideus muscle. (A) Extensive segmental hyaline degeneration in the supracoracoideus muscle. Coagulative necrosis, areas of myofibrillar lysis (black arrow), as well as intensive inflammatory infiltrate mainly consisting of lymphocytes and macrophages (star) are observed. Hematoxylin-eosin stain. Inset: Gross appearance of the supracoracoideus muscle, which appears pale and dry (yellow arrow). (B) Hypercontracted, necrotic, and lysed myofibers are highlighted using Mallory Azan stain (arrow). (C) Segmental degeneration and inflammatory infiltrate in a longitudinal section of supracoracoideus muscle. Surviving myofibers can be seen in red (arrow). Mallory Azan stain. (D) Calcification (mineralization) (in black, arrows), hyalinization, and necrosis of muscle fibers are observed. Von Kossa stain.