Gallinaceous birds, including Western Capercaillies (Tetrao urogallus) and Black Grouse (Tetrao tetrix), are kept in aviaries and reintroduced to natural habitats as a part of ongoing measures to protect these endangered species. Although parasitic loads can immensely affect reintroduction success of these species, little is known about how the infestation level varies in birds reared with different methods. The aim of this study was to determine the prevalence of endoparasites in fecal samples collected from Galliformes kept in various types of aviaries and transported to reintroduction sites. Most parasitic infections in the examined birds were caused by protozoa of the genus Eimeria, including Eimeria lyruri and Eimeria procera in Western Capercaillies, and E. lyruri, Eimeria nadsoni, and Eimeria tetricis in Black Grouse, which also hosted nematodes of the Capillaria spp. and Ascaridia galli. The prevalence of parasites varied across different types of aviaries. In permanent aviaries, Eimeria spp. was detected in 36% and 35% of the fecal samples collected from Western Capercaillies and Black Grouse, whereas Capillaria spp. were identified in 41% and 69% of the samples, respectively. The prevalence of the identified parasites increased in permanent aviaries on the second sampling date. In contrast, birds kept in seminatural free-flight aviaries in line with the “born to be free” rearing method had a lower prevalence of these parasites. Galliformes housed in seminatural aviaries may be better prepared for reintroduction to their natural habitats.

Western Capercaillie (Tetrao urogallus) and Black Grouse (Tetrao tetrix) are critically endangered bird species of the family Phasianidae and are considered threatened species in 11 European countries (Głowaciński 2001). This designation of conservation concern obligates European Union members to fulfill specific goals aimed to protect these birds (Publications Office of the European Union 2009). Nevertheless, Western Capercaillie and Black Grouse populations continue to decline in Europe from a combination of adverse factors, including growing pressure from opportunistic predators, habitat fragmentation resulting from changes in land use, and intensive forest management (Angelstam 2004). Global climate change also significantly affects bird habitats around the world, but its effect is difficult to assess (Jetz et al. 2007; Bender et al. 2019). These adverse factors compromise the health status of birds, reduce reproduction, and increase bird mortality (Pautasso 2012). Strong geographic isolation and the small size of isolated populations contribute to inbreeding, loss of genetic diversity, and, consequently, range contraction in both species (Segelbacher et al. 2003; Storch 2007). Population size may be influenced by availability of food resources, environmental pollution, and infections caused by various pathogens, including parasites (Børset and Krafft 1973; Foster 1983; Höglund et al. 1992; Baines 1996). Parasitic infections can compromise bird health and decrease activity, thus impeding escape from predators (Temple 1987; Poulin 1994; Isomursu et al. 2010). Endoparasites also induce behavioral changes in birds. Infected birds may change their habitat preferences, thus becoming more vulnerable to predators and hunters (Hudson et al. 1992; Moore 2002). To mitigate the decline in population sizes of Capercaillie and Black Grouse, captive rearing systems have been established. Infections caused by parasites, mainly endoparasites, pose a serious challenge for rearing endangered species in captivity. According to Belleau (2006), human presence can cause stress in Black Grouse. Disturbed birds defecate more often, which can be responsible for increased prevalence of parasitic infections from contact with feces.

Currently, there is a lack of reports on parasitic loads of birds housed within these systems. Because the infestation level can affect the heath and reproduction of birds, a successful reintroduction can be supported by effective prevention and treatment of parasitic diseases. Therefore, our study aimed to evaluate the prevalence of endoparasites in Western Capercaillies and Black Grouse kept captive in various types of aviaries (permanent aviaries, adaptive aviaries, and seminatural free-flight aviaries) and in birds transported to reintroduction sites. This data might be valuable to improve captive rearing methods for these species.

Bird groups

In 2014–18, 320 fresh fecal samples were obtained from 18 female Capercaillies and 132 Black Grouse (56 females and 76 males) aged 6 mo to 2 yr, kept in different types of aviaries in southern and northeastern Poland. Fecal samples were collected from a permanent aviary for Capercaillies (group A); a permanent aviary for Black Grouse (group B); adaptive aviaries where Black Grouse are kept for 1 mo before reintroduction (group C); seminatural free-flight aviaries where a female Black Grouse and two to four young birds are kept (group D); and adaptive aviaries where Black Grouse are housed directly after transport (group E).

Capercaillie from group A were kept in a breeding station within Wisła Forestry in two partially roofed aviaries with nine compartments each (4×8 m). The birds were kept separately, with wooden walls between compartments. The remaining aviary sides were meshed and lined with pine and birch trees (Pinus sylvestris, Betula pendula). The floor was concrete, covered with gravel that was removed regularly. The station houses only female Capercaillie for reproduction and subsequent reintroduction of the offspring. Birds in our study were first introduced to the aviaries in 2012; no birds had been kept in the aviaries previously. Black Grouse from group B were kept in Spychowo Forestry in partially roofed aviaries (100 m2 each) that each housed up to 13 Black Grouse, both males and females. The concrete floor was bedded with gravel. Walls consisted of mesh fence and pine and spruce trees (P. sylvestris, Picea abies). The birds were introduced into the aviaries in 2017 when they were 1 yr old. Black Grouse from group C were kept in adaptive aviaries designed for forthcoming introduction into the natural habitat. Fully roofed aviaries (30×50 m) housed 12–20 birds each. Mesh fence enclosed the area with abundance of natural fauna and flora (blueberries, heather, anthills). Black Grouse from group D were kept in seminatural (“born to be free”) aviaries located in Wild Animal Park in Kadzidłowo. The aviaries were 20 m in diameter with a caged section for the mother in the middle. Exits in the meshed sides allowed young birds to leave the aviary and explore the surroundings. Black Grouse from group E were transported at night in a truck, in individual cardboard boxes lined with moss. Transit time was around 7 h.

In all aviaries, birds were fed available commercial diets for homing pigeons, supplemented with ant larvae and plants suitable for the season. In summer, birds received an additional supply of blueberries and, in late summer and early fall, cranberries and heather. Birds also had access to plants naturally growing in aviaries. Water was provided ad libitum in containers that were filled daily.

Sample collection and assessment

In each group, samples of fresh feces were collected from individual birds (10 g) or bulk samples were obtained directly from the aviary floor (100 g). In group A, individual samples were collected from 18 female Capercaillies in 2014 (A1) and from 16 of the same females in 2015 (A2). In group B, individual samples were collected from 17 Black Grouse (four males and 13 females). In group C, bulk samples were collected from 40 young Black Grouse (15 females and 25 males) on two dates: 7 d after caging (C1) and 3 d before release in reintroduction sites (C2). In group D, from four seminatural free-flight aviaries housing four permanently caged females and mothers and two to four young birds with unlimited contact with the isolated mothers and the external environment, individual samples were collected on two dates: 7 d after caging (D1) and 2 mo later (D2). In group E, individual samples were collected from cardboard boxes holding 59 young Black Grouse (27 females and 32 males) directly after transport to the reintroduction site. The sampling intervals are shown in Figure 1. Because of a lack of difference in parasitic loads between male and female birds, we present the results for both sexes combined.

Figure 1

Intervals between sampling dates of Black Grouse (Tetrao tetrix) and Capercaillie (Tetrao urogallus) feces that took place from 2014 to 2018 in Poland. In group A (Capercaillies in permanent aviaries), 18 samples were collected on the first sampling date and 16 samples 1 yr later. In group B (Black Grouse in permanent aviaries), 17 samples were collected. In group C (Black Grouse in adaptive aviaries), 40 samples were collected on the first date and 1 mo later. In group D (Black Grouse in seminatural aviaries), 16 samples were collected on the first date and 2 mo later. In group E (Black Grouse transported to reintroduction site), 49 samples were collected.

Figure 1

Intervals between sampling dates of Black Grouse (Tetrao tetrix) and Capercaillie (Tetrao urogallus) feces that took place from 2014 to 2018 in Poland. In group A (Capercaillies in permanent aviaries), 18 samples were collected on the first sampling date and 16 samples 1 yr later. In group B (Black Grouse in permanent aviaries), 17 samples were collected. In group C (Black Grouse in adaptive aviaries), 40 samples were collected on the first date and 1 mo later. In group D (Black Grouse in seminatural aviaries), 16 samples were collected on the first date and 2 mo later. In group E (Black Grouse transported to reintroduction site), 49 samples were collected.

Close modal

Fecal samples were examined by the Fülleborn floatation method and the decantation method according to Żarnowski and Josztowa (Gundłach and Sadzikowski 2004). The number of oocysts (OPG) or eggs per 1 g of feces (EPG; Ministry of Agriculture, Fisheries and Food 1986) was counted by the McMaster method (Gundłach and Sadzikowski 2004). Parasites in different developmental stages were identified with a guide (Hendrix and Robinson 2014), and they were classified from a morphometric analysis and taxonomic keys for identifying dispersive parasitic stages (Gundłach and Sadzikowski 2004) under a light microscope by Cell software (Olympus, Tokyo, Japan). Three replicates were obtained from each sample. We report the numbers found as a sample mean and SD.

Detected parasites

Microscopic analyses revealed two Eimeria spp. (Eimeria procera and Eimeria lyruri) in Capercaillies and three Eimeria spp. (E. lyruri, Eimeria nadsoni, and Eimeria tetricis) in Black Grouse. Eggs of the nematodes Capillaria caudinflata (Aonchotheca caudinflata) and Ascaridia galli were detected in both bird species. Eggs of the parasitic tapeworm Raillietina cesticillus was identified in Black Grouse group E.

Number of OPG or EPG

The mean number of OPG or EPG was counted for each parasite (Table 1). The occurrence of the parasites in birds is shown in Table 2.

Table 1

Mean number of oocysts and eggs per gram of Eimeria spp., Capillaria sp., Ascaridia galli, and Raillietina cesticillus found in fecal samples of Black Grouse (Tetrao tetrix) and Capercaillie (Tetrao urogallus) and kept in different types of aviaries between 2014 and 2018 in Poland. The SD is given in parentheses.a

Mean number of oocysts and eggs per gram of Eimeria spp., Capillaria sp., Ascaridia galli, and Raillietina cesticillus found in fecal samples of Black Grouse (Tetrao tetrix) and Capercaillie (Tetrao urogallus) and kept in different types of aviaries between 2014 and 2018 in Poland. The SD is given in parentheses.a
Mean number of oocysts and eggs per gram of Eimeria spp., Capillaria sp., Ascaridia galli, and Raillietina cesticillus found in fecal samples of Black Grouse (Tetrao tetrix) and Capercaillie (Tetrao urogallus) and kept in different types of aviaries between 2014 and 2018 in Poland. The SD is given in parentheses.a
Table 2

The number of Black Grouse (Tetrao tetrix) and Capercaillie (Tetrao urogallus) infested with parasites and housed in different types of aviaries between 2014 and 2018 in Poland and their prevalence in group A (Capercaillies in permanent aviaries) on the first sampling date (A1) and 1 yr later (A2), group B (Black Grouse in permanent aviaries), and group E (Black Grouse transported to reintroduction site). To measure the prevalence, fecal samples were collected from individual birds.

The number of Black Grouse (Tetrao tetrix) and Capercaillie (Tetrao urogallus) infested with parasites and housed in different types of aviaries between 2014 and 2018 in Poland and their prevalence in group A (Capercaillies in permanent aviaries) on the first sampling date (A1) and 1 yr later (A2), group B (Black Grouse in permanent aviaries), and group E (Black Grouse transported to reintroduction site). To measure the prevalence, fecal samples were collected from individual birds.
The number of Black Grouse (Tetrao tetrix) and Capercaillie (Tetrao urogallus) infested with parasites and housed in different types of aviaries between 2014 and 2018 in Poland and their prevalence in group A (Capercaillies in permanent aviaries) on the first sampling date (A1) and 1 yr later (A2), group B (Black Grouse in permanent aviaries), and group E (Black Grouse transported to reintroduction site). To measure the prevalence, fecal samples were collected from individual birds.

Parasites were detected in 11 samples collected from 18 female Capercaillies in group A (permanent aviary) in 2014 (A1), including Eimeria spp. oocysts (OPG 3,350±1,202.08) in two samples, Capillaria spp. eggs (EPG 385±91.92) in seven samples, and both parasites (OPG 4,060±622.25, EPG 282.5±81.32) in two samples. In the samples collected in 2015 (A2) from 16 female Capercaillies, parasites were detected in 13 samples, including Eimeria spp. (OPG 22,625±31,643.03) and eggs of Capillaria spp. (EPG 31.5±4.95) in eight samples; additionally, eggs of A. galli (EPG 27±28.28) were identified in five samples.

Parasites were detected in 12 out of 17 samples collected from group B. Eimeria spp. oocysts (OPG 11,733.33±7,503.92) were identified in three samples; Capillaria spp. eggs (EPG 280±120.83) were detected in four samples; both Eimeria spp. oocysts and Capillaria spp. eggs (OPG 10,580±7,010, EPG 300±110) in two samples; Eimeria spp. and A. galli eggs (OPG 6,450, EPG 370) in one sample; and coinfection of Eimeria spp., Capillaria spp. eggs, and A. galli eggs (OPG 12,950±9,450, EPG 335±15, EPG 250±110, respectively) in two samples.

In two adaptive aviaries (group C) that housed a total of 40 young (6-mo-old) Black Grouse over a period of 1 mo, 10 bulk samples were obtained. On the first sampling date (C1) Eimeria spp. oocysts (OPG 20,700) and Capillaria spp. eggs (EPG 230) were identified, whereas Eimeria spp. oocysts (OPG 45,300), Capillaria spp. eggs (EPG 280), and A. galli eggs (EPG 470) were detected on the second sampling date (C2).

In four seminatural free-flight aviaries (group D), samples were collected twice at a 2-mo interval. In the samples collected 7 d after caging (D1), Eimeria spp. oocysts (OPG 50,000±14,142.14) and Capillaria spp. eggs (EPG 225±21.21) were detected in the mothers, and Eimeria spp. oocysts (OPG 23,500±2,121.32) and Capillaria spp. eggs (EPG 260±14.14) were identified in the offspring. In the samples collected 2 mo later (D2), Eimeria spp. oocysts (OPG 66,500±37,376.66) and Capillaria spp. eggs (EPG 275±91.92) were detected in the mothers, whereas only a small number of Eimeria spp. oocysts (OPG 375±35.36) were identified in the offspring, with no eggs of Capillaria spp. observed.

Directly after transport to the reintroduction site, individual fecal samples were collected from cardboard boxes (group E) holding 59 (27 females and 32 males) young (around 6-mo-old) Black Grouse. Parasites were identified in 45 out of 59 samples (76.3%). Eimeria spp. oocysts (OPG 38,890.17±39,375) were detected in 42 birds; Eimeria spp. oocysts and Capillaria spp. eggs (OPG 6,691.25±6,166.26, EPG 410±56.57) were identified in eight birds; and R. cesticillus eggs (EPG 2,185±544.47) were detected in three birds.

Prevalence of parasites

Prevalence of parasites for groups A, B, and E is shown in Table 2. In group A (Western Capercaillies), the dominant parasites were Capillaria spp. (identified in 69% of the examined samples) and Eimeria spp. (36%) with occasional occurrence of Ascaridia spp. (15.63%). The prevalence of these parasites was determined at 50% (Capillaria spp.) and 22% (Eimeria spp.) in 2014 (A1) and at 50% for both parasitic genera accompanied by 31.25% prevalence of Ascaridia spp. in 2015 (A2).

In group B (Black Grouse), the dominant genus was Eimeria spp. (identified in 41% of the analyzed samples) followed by Capillaria spp. (20%) and Ascaridia spp. (12%). Mixed parasitic invasions were observed only in 36% of the examined samples.

In group E (Black Grouse), prevalence of Eimeria spp. (71.2%) was higher than prevalence of Capillaria sp. (13.56%).

The prevalence in the remaining groups (C and D) was not possible to calculate, because bulk samples had been collected.

The prevalence of parasites in the studied birds was typical of wild Galliformes, as well as Galliformes reared in seminatural conditions without antiparasitic treatments, excluding the prevalence of Eimeria spp. in birds transported to adaptive aviaries (group E). Similar results have been noted by other authors; for example, Eimeria spp. and Capillaria spp. were found in galliform birds kept in captivity (Tomczuk et al. 2017) and in wild birds (Millán et al. 2008).

In group E (birds transported to the reintroduction site), the prevalence of Eimeria spp. was high compared with other groups, at 71.2% (mean OPG 38,890.17±39,375), which can probably be attributed to transport-related stress. As a result, large amounts of fecal matter can be obtained for analysis of the parasitic fauna and prescription of any appropriate treatment before the birds are reintroduced to the natural habitat.

The prevalence of Eimeria spp. increased in Galliformes housed in aviaries (22.22% on the first sampling date, compared with 50% after 12 mo in group A). In contrast, the prevalence of Capillaria spp. remained stable. As most studies focus on one-time sampling of feces from wild birds held in captivity (Madsen 1952; Marco et al. 1999; Jankovska et al. 2012; Tomczuk et al. 2017), we were not able to compare our results with other reports. Further research into the change in prevalence of these parasites would provide an important insight into the efficiency of rearing methods in terms of parasite prevention. Capercaillie kept in solitary compartments (group A) had an overall higher prevalence of parasites than Black Grouse kept in collective aviaries (group B). Birds living in confined spaces have daily contact with feces, which can facilitate infection among cohabiting individuals from feces of other birds and their own excrements. Comparison between group A and B should be considered with caution because these were two different Tetrao species and the samples were not collected at the same time, which can immensely affect the results.

An analysis of the severity of parasitic infections revealed considerable differences between birds living in the same aviary. Notable differences were observed in group A, where OPG values for Eimeria spp. ranged from 250 to 4,500 in 2015. These findings indicate that parasitic invasions proceeded differently in birds kept in solitary compartments, regardless of identical environmental conditions and diet. The only preventive measure applied in the aviary against parasites was the regular exchange of gravel bedding. The drastic increase in the parasitic loads suggest that more definitive steps should be made to limit the parasitic invasion. Considerable differences in the severity of parasitic infections were also observed in group E, but these variations could be attributed to transport-related stress and the resulting higher defecation frequency (Belleau 2006) and immunosuppression (Applegate 1970; Mengert and Fehlhaber 1996; El-Lethey 2003; Jacobs et al. 2017).

Previous research into parasitic invasions has revealed the presence of Raillietina urogalli, R. cesticillus, Ascaridia compar, Heterakis gallinarum, C. caudinflata, and E. lyruri in Polish populations of Capercaillies and Black Grouse (Tomczuk et al. 2017). Our study demonstrated that in addition to E. lyruri, these species in Poland are also colonized by other species of the genus Eimeria, including E. nadsoni and E. tetricis (in Black Grouse) as well as E. procera (in Capercaillies). Madsen (1952) identified A. galli, Capillaria anatis, C. caudinflata, and Syngamus trachea in gamebirds (pheasants Phasianus colchicus, partridge Perdix perdix, and Black Grouse) in Denmark, whereas Marco et al. (1999) detected Heterakis tenuicauda and Corrigia spp. in Italian populations of Black Grouse. Eimeria lyruri, Hymenolepis spp., A. compar, Trichostrongylus tenuis, and feather mites Pterolichus obtusus were identified by Jankovska et al. (2012) in Black Grouse in the Czech Republic.

Depending on habitat, young Black Grouse appear to be more susceptible than older individuals to A. compar and C. caudinflata invasions; also, such parasite infections may affect the body weight of Black Grouse (Formenti et al. 2012). Parasitic infections are also more common in captive birds, which was confirmed in Capercaillies and Black Grouse in our studied aviaries, and the prevalence of parasites was higher in young birds, excluding young Black Grouse living in free-flight aviaries, than in adults.

Capercaillies kept in aviaries are characterized by smaller lungs and heart volume as well as longer intestines (Liukkonen-Anttila et al. 2000). Muscle glycogen levels are 10 times lower in captive birds. These changes impair take off and escape distance; therefore, captive birds are less likely to survive a predatory attack than are free-living birds (Liukkonen-Anttila et al. 2000).

Seminatural free-flight aviaries have been introduced as a way to protect endangered Galliformes and facilitate rearing of offspring both in close contact with the mother and in conditions similar to the birds' natural habitat (Krzywiński and Keller 2005; Krzywiński 2008; Krzywiński et al. 2009, 2011). Our study demonstrated that breeding females kept in captivity typically had persistent and severe parasitic infections caused by Eimeria spp. and Capillaria spp., which can be attributed to a small living space and the accumulation of feces in closed cage systems. Additionally, mothers that are deprived of contact with their offspring experience profound stress, which can lead to immunosuppression (El-Lethey et al. 2003). The observations made in young Black Grouse from group D suggest that unrestricted flight and independent search for food increase birds' ability to fight parasitic invasions. Oocyst counts were considerably lower, and Capillaria spp. were not detected in group D young birds (seminatural aviaries).

According to Krzywiński et al. (2011), captive breeding generates physiologic and behavioral problems that significantly increase mortality in Galliformes. Captive birds experience profound stress when they are reintroduced to their natural environment (Jenni et al. 2015). When released, most birds travel long distances, but the lack of antipredator adaptations makes them an easy target (Merta et al. 2015). The diurnal rhythm of activity and rest which is characteristic of wild populations is disrupted in captive birds. Maladapted birds do not express normal feeding behaviors, which compromises their health and increases mortality (Siano et al. 2006; Krzywiński et al. 2011). Merta et al. (2015) reported that in young Capercaillies reared according to the “born to be free” method, the mean survival time of females was more than five times longer, and males survived more than twice as long as control birds housed in closed cages before release. The health status of captive Galliformes, in particular breeding stock, should be regularly monitored during restoration and reintroduction programs to control parasitic infections and increase the birds' chances of survival. Our study highlights additional advantages of using seminatural aviaries in captive breeding of Black Grouse. In these aviaries, the birds’ parasitic loads diminished over time, whereas in other types of aviaries the infections intensified. As parasitic loads can immensely affect the performance and survival abilities of birds after reintroduction, maintaining low parasite loads in captive birds would be highly beneficial for the population sizes of these endangered species.

There is a regrettable dearth of scientific published information comparing parasitic loads in captive nondomestic birds reared in different designs of enclosures; this report addresses this data gap. Monitoring parasitic loads in captive birds should also serve as a basis for effective prevention and treatment. Care is needed when choosing parasiticides; Eimeria spp. colonizing the digestive tract of Black Grouse have been found to be resistant to toltrazuril, a popular broad-spectrum drug with anticoccidial activity (Sokół and Gałęcki 2018). Adequate housing conditions and effective treatment are the key success factors in programs aiming to reintroduce Galliformes to their natural environment.

The authors thank the employees and aviary staff of Spychowo and Wisła Forest Districts and A. Krzywiński of the Wildlife Park in Kadzidłowo for providing access to aviaries and assisting in the collection of fecal samples for the study. No live animals were directly handled in this study. Fecal samples for analyses were collected from the floor in aviaries and from transport boxes. This publication was financially co-supported by the Minister of Science and Higher Education in the range of the program entitled “Regional Initiative of Excellence” for the years 2019–22, project 010/ RID/2018/19.

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