Year | Total number of nestboxes | Total number of boxes occupied | Box occupancy rate (%) | Number of boxes occupied by Varied Tit | Number of boxes occupied by Cinereous Tit |
2016 | 340 | 101 | 29.71 | 44 | 38 |
2017 | 451 | 171 | 37.92 | 67 | 58 |
2018 | 434 | 179 | 41.24 | 39 | 69 |
Citation: | Nyanasengeran Movin, Tatjana Gamova, Sergei G. Surmach, Jonathan C. Slaght, A.A. Kisleiko, James A. Eaton, Frank E. Rheindt. 2022: Using bioacoustic tools to clarify species delimitation within the Blakiston's Fish Owl (Bubo blakistoni) complex. Avian Research, 13(1): 100021. DOI: 10.1016/j.avrs.2022.100021 |
Although Blakiston's Fish Owl (Bubo blakistoni) is widely treated as a single species, marked differences in the structure of pair duets between continental and insular populations have been documented. However, no study has quantitatively assessed these vocal differences. We obtained 192 duets from 22 pairs of Blakiston's Fish Owl: 15 pairs of B. b. blakistoni from the Japanese island of Hokkaido and the Russian Kuril island of Kunashir, and seven pairs of B. b. doerriesi from Primorye on the Russian mainland. This is a sizeable dataset for such a large, retiring, and rare owl. We conducted bioacoustic examinations of 14 vocal parameters using principal component analysis and the Isler criterion to quantitatively test species boundaries within the B. blakistoni complex. We found that the insular populations on Hokkaido and Kunashir emerged as vocally similar to each other but markedly different from the continental populations of B. blakistoni, corresponding closely with presently accepted subspecies limits. Bioacoustic differences in the duets of the insular and continental groups are greater than the pairwise comparisons of territorial vocalisations between other sympatric owl species. Based on the reproductive importance of vocal duets in owl biology, we propose the taxonomic elevation of the continental subspecies to species level as Northern Fish Owl B. doerriesi. Our study corroborates the importance of bioacoustics in ascertaining species boundaries in owls and has important implications for the management of the two newly delimited species, each likely to be assessed as Endangered. Both species should be managed independently to optimise conservation outcomes.
There often is competition for limited resources when species live in the same area, especially in the breeding season. Individuals need suitable nest sites (Martin, 1993) and sufficient food resources for survival and reproduction (Martin, 1987). They also want to avoid losses caused by interference competition (Minot and Perrins, 1986; review in Dhondt, 2012).
A large number of experimental studies have shown that intra- and inter-specific competition can reduce breeding success and population size (Schoener, 1983; Finch, 1990; Gurevitch et al., 1992). House Wrens (Troglodytes aedon) that co-habit with Tree Swallows (Tachycineta bicolor) have lower reproductive success rate than wrens living in swallow-free plots (Finch, 1990). The first egg laying date of Eurasian Blue Tits (Cyanistes caeruleus) is affected by intra-specific and inter-specific interference, but no such relationship has been found in a closely related species, the Great Tit (Parus major, Møller et al., 2018). The reproductive output of the central nest is adversely affected by their short-distance neighbors containing conspecifics but not heterospecific ones (Deeming et al., 2017). Most studies have concentrated on the breeding behavior of conspecific or heterospecific neighbors to evaluate intra- and inter-specific competition. Breeding synchrony may also be an important environmental indicator as needs for resources vary hugely as nestlings grow. Competition might lead greater intervals among neighbors in terms of delay in breeding and might have effects on reproduction in neighbors.
Some species are sufficiently abundant and show no obvious spatial heterogeneity, while others are range-restricted and influenced by both habitat composition and local environment (Laube, 2011). Regarding the question of what affects the size of the distribution, most studies concentrated on non-behavioral environmental or spatial factors (e.g. Szabo et al., 2009; Boucher-Lalonde et al., 2014) but few have investigated behaviors. Zhang et al. (2019) attributed the difference in the distribution size of Cinereous (Parus cinereus) and Varied Tits (Sittiparus varius) to their personalities because the relatively wider-spread Cinereous Tit is more exploratory, active, and risk-prone than the Varied Tit, a locally distributed species, is. We predict that anti-interference capability of the narrowly-distributed Varied Tit may be weaker than that of the relatively widely-distributed Cinereous Tit.
Artificial nestboxes are widely used in studies of birds, particularly in field research, because they attract breeding birds. As a result, it is an effective tool to gather reproduction data (Møller et al., 2014) to study demographic shift, life history evolution, quantitative genetics, and sexual selection (Evans et al., 2002). To ensure sufficiency, usually large numbers of artificial nestboxes are provided, but only a small number are occupied every year (Mänd et al., 2005).
In this study, we measured intra- and inter-specific spatial distribution of used artificial nestboxes and investigated whether the intersection of neighbors’ living area affected the breeding outcome of the focal breeding pair. Two hole-nesting passerine species, Cinereous Tit and Varied Tit, were concentrated on. Based on which we proposed three hypotheses: (1) the distance of nests within species is longer than that between them, (2) conspecific and heterospecific neighbors both have a negative impact on the focal nest, and (3) the range-restricted species, Varied Tits, are more vulnerable to neighbor influence than the relatively wider-spread Cinereous Tits.
Starting from 2016, this study was carried out every year from early April through mid-July for three consecutive years in Liaoning Xianrendong National Nature Reserve (39°54ʹ‒40°03ʹ N, 122°53ʹ‒123°03ʹ E). Yet ten years before this study began artificial nestboxes had already been installed and supplemented or replaced every year. All boxes had a base dimension of 15 cm × 15 cm and a height of 30 cm. The opening was round, with a diameter of 3 cm or 3.5 cm, and located about 7 cm below the box cover. The artificial nestboxes were hung mainly on Pinus densiflora, Quercus mongolica and Pinus koraiensis, at a height of 2–3 m from the ground.
All boxes were hung randomly on both sides along infrequent paths in the reserve. Their locations were recorded using OvitalMap (Beijing Ovital Software Co. Ltd. 2016). The average distance between two nearest ones was around 30 m. Weekly recording included the laying date, the species (available since incubation) and reproductive parameters such as clutch size, the number of hatchlings, ten-day-old nestlings and fledglings. We then calculated the hatching rate (the number of hatchlings/clutch size) and reproductive success rate (the number of fledglings/clutch size). The distances from the central nestbox to (1) the nearest ones, (2) the nearest nestbox occupied by a conspecific, and (3) the nearest nestbox occupied by a heterospecific were all measured using OvitalMap.
The data was analyzed in SPSS version 21.0 (IBMCorp. Armonk, NY). An index of dispersion (Fowler et al., 1997) was calculated to ascertain the box distribution pattern. Mixed effect regression was used to test factors (the explanatory variable: neighbor type; and the random factors: box number and year) that affected the intra- and inter-specific nest spacing (the response variables: the distance between the focal nest and its nearest conspecific/heterospecific nest). We used mixed effect models to explore the influence of spatial distribution on the hatching rate of the focal nest (the explanatory variables: conspecific distance, heterospecific distance; and the random factors: box number and year) and linear models to explore the influence of spatial distribution on the reproductive success rate of the focal nest (the explanatory variables: conspecific distance, heterospecific distance). We used mixed effect models to explore the influence of breeding behavior on the hatching rate of the focal nest (the explanatory variables: neighbor type, neighbor hatching rate, and breeding synchrony; and the random factors: box number and year) and linear models to explore the influence of breeding behavior on the reproductive success rate of the focal nest (the explanatory variables: neighbor type, neighbor reproductive success rate and breeding synchrony). All analyses were considered significant at a probability value of <0.05.
In total, 340, 451 and 434 nestboxes were investigated in 2016, 2017 and 2018, respectively. Each year less than half were occupied (Table 1) mainly by Cinereous Tits and Varied Tits, while few were occupied by other species such as Marsh Tits (Poecile palustris) and Daurian Redstarts (Phoenicurus auroreus). Over the 3 years, 20 boxes were used twice by Cinereous Tits, 17 boxes were used twice by Varied Tits, and 1 box was used thrice by each. All boxes were randomly dispersed within 500 m on both sides of the path (e.g., Fig. 1, dispersion indices χ2 = 13.46, df = 19), as were those occupied by both Varied Tits (χ2 = 8.68, df = 19) and Cinereous Tits (χ2 = 18.02, df = 19).
Year | Total number of nestboxes | Total number of boxes occupied | Box occupancy rate (%) | Number of boxes occupied by Varied Tit | Number of boxes occupied by Cinereous Tit |
2016 | 340 | 101 | 29.71 | 44 | 38 |
2017 | 451 | 171 | 37.92 | 67 | 58 |
2018 | 434 | 179 | 41.24 | 39 | 69 |
The distance between breeding nests was significantly affected by neighbor type (F = 29.652, P < 0.001), but not species (F = 1.304, P = 0.254). The distance between intraspecific breeding nests of Varied Tits was significantly longer than that between interspecific nests (Fig. 2A). For Cinereous Tits, the same was true (Fig. 2B). However, reproduction of Varied and Cinereous Tits was not significantly relevant to the distance from their neighbor’s nest (Table 2).
Hatching rate | Reproductive success | |||
t-value | P | t-value | P | |
Cinereous Tit | ||||
Conspecific distance | 1.81 | 0.075 | 0.041 | 0.968 |
Heterospecific distance | 0.30 | 0.765 | −0.488 | 0.633 |
Varied Tit | ||||
Conspecific distance | −0.267 | 0.791 | −0.193 | 0.849 |
Heterospecific distance | 1.241 | 0.219 | 0.600 | 0.557 |
The hatching rate of Varied Tits (n = 144, r2 = 0.892) was not related to recorded breeding behavior of their neighbors (hatching rate, t = 0.773, P = 0.982; and breeding synchrony, t = −0.419, P = 0.333). Its reproductive success rate (n = 38, r2 = 0.270, F5,32 = 2.362, P = 0.062) was negatively related to that of their neighbors (t = −2.677, P = 0.012) and positively related to the interaction between neighbor type and the reproductive success rate of the neighbor (t = 2.142, P = 0.040). Separate analyses on intraspecific neighbor and interspecific neighbor showed that the reproductive success of Varied Tits was negatively related to that of intraspecific neighbor (t = −2.889, P = 0.011, Fig. 3) and not significantly related to that of interspecific neighbor (t = −0.086, P = 0.932, Fig. 3). The reproductive effect of Cinereous Tits (hatching rate, n = 140, r2 = 0.758; and reproductive success rate, n = 34, r2 = 0.201, F5,28 = 1.404, P = 0.253) was not significantly affected by the recorded breeding behavior of their neighbors.
There was spatially separated nest sites selection for Varied Tits and Cinereous Tits. The distance between nests was longer within than between species. While both inter- and intra-specific competitions affect site selection (Tarjuelo et al., 2017) and food abundance (Teather, 1992), intraspecific competition in particular also impacts mate choice (Martínez-Rivera and Gerhardt, 2008) and extra-pair mating (Birkhead et al., 1985). To reduce such competition, individuals of the same species may space each other's nesting sites farther apart. Thus, intra-specific nests were more sparsely spaced. Deeming (2017) also shows that the conspecific nest distance is longer than the heterospecific one for Blue Tits and Great Tits. These results support that intraspecific competition in nest selection is more intense than interspecific competition.
Regarding spatial distribution, Varied and Cinereous Tits showed a similar pattern. The distance to their neighbor’s nest was not significantly relevant to reproduction. But intense competition arises from the relatively short distance between two nests of the same species, which may adversely affect the reproduction of the breeding nest (Deeming et al., 2017). In our study, fewer than half of the installed boxes were occupied. The average distance between two nearest nestboxes was around 30 m, about twice the distance between two nearest neighbors. The space interval was relatively sufficient, and that was not so drastic to affect the reproductive success.
The breeding success of Varied Tits may or may not be affected by that of their neighbors. The type matters. Between conspecific neighbors there is a negative correlation whereas between heterospecific ones, no identifiable correlation. Competition can reduce the number of offsprings (Gurevitch et al., 1992). In resource-restricted habitat, we are likely to detect the effect of density-dependence on reproduction in territorial species (Dhondt, 2010). When the conspecifics reproduce in the same area, there will be severe competition for food (Krüger et al., 2012). Food shortage is known to disrupt reproduction.
However, Cinereous Tits did not show significant correlation to any recorded reproductive behavior of their neighbors. The results are supported by Møller’s (2018) finding that the breeding behavior of Blue Tits is affected by conspecifics but not Great Tits. In other words, the effect of competition on demographic variables has interspecific divergence. This may result from the either the scramble or exploitation-type competition for food both within and between species, and interference competition between different body sizes (Dhondt, 1977, 2010), as Cinereous Tits are larger than Varied Tits. Interspecific divergence may be related to the variances in clutch size of the two species. In our research site, the clutch size of Varied Tits is mostly 7–9, and the clutch size of Cinereous Tits is 7–13. Flexible adjustment of clutch size might be one of the ways for big tits to reduce competition. Behavioral differences may also contribute to the divergence. Active individuals can get more food resources under the same circumstance (David et al., 2011). So Varied Tits, which are less exploratory, active, and risk-taking than Cinereous Tits (Zhang et al., 2019), get less. Reproductive success of Cinereus Tits is not significantly affected.
This study focused on one option of breeding site, namely through artificial nestboxes, rather than exhausting all possibilities. For example, nests in natural cavities are not considered. This is because on the reserve, where dead wood is removed in a timely manner, natural cavities are in insufficient supply. Before the breeding season, in March, we ringed the birds on the experimental site. During the entire breeding test period, unringed individuals were rarely spotted. Therefore, we assume that, at least in the area where artificial nest boxes were hung, natural nests were negligible.
Boxes that are too densely distributed can even negatively affect the breeding behavior of birds, especially in areas where natural nests are extremely scarce. Thus, artificial nestboxes usually have low occupancy rate (Mänd et al., 2005; Deeming et al., 2017). This knowledge can be applied to the arrangement of nestboxes for bird study and conservation.
Our results show that intra- and inter-specific competition affects the nest distribution of two hole-nesting species. The effect on reproductive outcome has interspecific divergence. The reproductive outcome of Varied Tits is significantly affected by its conspecific and heterospecific neighbors, but that of Cinereous Tits is not affected.
YJ conceived the experiments, analyzed the data, wrote the manuscript, and reviewed the drafts; YB conceived and designed the experiments, performed the experiments, analyzed the data, and wrote the manuscript; RM analyzed the data; JZ performed the experiments; DW conceived and designed the experiments, and reviewed drafts of the paper. All authors read and approved the final manuscript.
All our study procedures were approved by Liaoning Xianrendong National Nature Reserve.
The authors declare that they have no competing interests.
Thanks for the support of Liaoning Xianrendong National Nature Reserve. This work was supported by the National Natural Science Foundation of China (No. 31872231 to DW, No. 32000316 to YJ).
Bardin, A.V., 2006. Autumn encounter with a Blakiston’s fish owl Ketupa blakistoni on Sakhalin. Russkii Orn. Zhurnal Ekspress-vypusk. 15, 738-739 (in Russian)
|
Berzan, A.P., 2005. Analysis of modern distribution and population size of Blakiston’s fish owls in the southern Kuril Islands and Sakhalin. In: Volkov, S.V., Morozov, V.V., Sharikov, A.V. (Eds.), Owls of Northern Eurasia. Working Group of Birds of Prey and Owls, Moscow, Russia, pp. 447–449 (in Russian with English summary).
|
Brazil, M.A., Yamamoto, S., 1989. The behavioural ecology of Blakiston’s Fish Owl Ketupa blakistoni in Japan: calling behaviour. In: Meyburg, B.-U., Chancellor, R.D. (Eds.), Raptors in the Modern World: Proceedings of the III World Conference on Birds of Prey and Owls. World Working Group on Birds of Prey and Owls, Berlin, Germany, pp. 403–410.
|
Courtin, J., Andreev, A.A., Raschke, E., Bala, S., Biskaborn, B.K., Liu, S., et al., 2021. Vegetation changes in southeastern Siberia during the Late Pleistocene and the Holocene. Front. Ecol. Evol. 26, 9
|
del Hoyo, J., Collar, N.J., 2014. HBW and BirdLife International Illustrated Checklist of the Birds of the World. Non-passerines, vol. 1. Lynx Edicions, Barcelona.
|
Dykhan, M.B., Kisleiko, A.A., 1988. Number and distribution of Blakiston's fish owls on Kunashir Island during the breeding period. In: Litvinenko, N.M. (Ed.), Rare Birds of the Russian Far East and Their Protection. Dalnevostochnoe Otdeleniye Akademii Nauk SSSR, Vladivostok, Russia, pp. 29–32 (in Russian).
|
Howell, S.N.G., Robbins, M.B., 1995. Species limits of the least pygmy-owl (Glaucidium minutissimum) complex. Wilson Bull. 107, 7-25
|
Isler, M.L., Chesser, R.T., Robbins, M.B., Cuervo, A.M., Cadena, C.D., Hosner, P.A., 2020. Taxonomic evaluation of the Grallaria rufula (Rufous Antpitta) complex (Aves: Passeriformes: Grallariidae) distinguishes sixteen species. Zootaxa 4817, zootaxa-4817
|
King, B. 2002. Species limits in the Brown Boobook Ninox scutulata complex. Bull. Br. Ornithol. Club 122, 250-256
|
Krabbe, N.K. 2017. A new species of Megascops (Strigidae) from the Sierra Nevada de Santa Marta, Colombia, with notes on voices of New World screech-owls. Ornitol. Colomb. 16, 1-27
|
Lovette, I.J., 2004. Mitochondrial dating and mixed support for the “2% rule” in birds. Auk 121, 1-6
|
Mayr, E., Ashlock, P.D., 1991. Principles of Systematic Zoology, second ed. McGraw-Hill Inc, Now York, p. 475.
|
Nechaev, V.A., 1991. Birds of Sakhalin Island. Amur-Ussuri Center for Avian Biodiversity, Vladivostok (in Russian).
|
Pukinskii, Y.B., 1973. Ecology of Blakiston’s Fish Owl in the Bikin river basin. Byull. Mosk. O-va Ispyt. Prir. Otd. Biol. 78, 40-47 (In Russian with English summary)
|
Pukinskii, Y.B., 1974. Blakiston’s Fish Owl vocal reactions. Vestn. Leningr. Univ. 3, 35-39 (In Russian with English summary)
|
Pukinskii, Y.B., 1993. Blakiston’s fish owl – Ketupa blakistoni. In: Numerov, A.D. (Ed.), The Birds of Russia and Contiguous Regions: Pterocliformes, Columbiformes, Cuculiformes, Strigiformes. Nauka, Moskow, pp. 290–302 (in Russian).
|
Rasmussen, P.C., Allen, D.N.S., Collar, N.J., DeMeulemeester, B., Hutchinson, R.O., Jakosalem, P.G.C., et al., 2012. Vocal divergence and new species in the Philippine Hawk Owl Ninox philippensis complex. Forktail 28, 1-20
|
Sangster, G., Rozendaal, F.G., 2004. Systematic notes on Asian birds. Territorial songs and species-level taxonomy of nightjars of the Caprimulgus macrurus complex, with the description of a new species. Zool Verh Leiden. 350, 7-45
|
Seebohm, H., 1895. Bulletin of the British Ornithologists’ Club. Ibis 5, 4
|
Slaght, J.C., Takenaka, T., Surmach, S.G., Fujimaki, Y., Utekhina, I.G., Potapov, E.R., 2018. Global distribution and population estimates of Blakiston's Fish Owl. In: Nakamura, F. (Ed.), Biodiversity Conservation Using Umbrella Species. Ecological Research Monographs. Springer, Singapore, pp. 9–18.
|
Taczanowski, L., 1891. Faune Ornitologique de la Siberie orientale. Premiere partie. Memoris de l’Academie Imperiale des Sciences de St Petersbourg. Serie 7, 1278 (in French)
|
Takenaka, T., 1998. Distribution, Habitat Environments, and Reasons for Reduction of the Endangered Blakiston’s Fish Owl in Hokkaido, Japan. Ph.D thesis. Hokkaido University, Sapporo, Japan.
|
Takenaka, T., 2018. Ecology and conservation of Blakiston's fish owl in Japan. In: Nakamura, F. (Ed.), Biodiversity Conservation Using Umbrella Species. Ecological Research Monographs. Springer, Singapore, pp. 19–46.
|
Turner, D.A., Pearson, D.J., 2015. Systematic and taxonomic issues concerning some East African bird species, notably those where treatment varies between authors. Scopus 34, 1-23
|
Yakovlev, B.P., 1929. Animal world of Manchuria: birds. Obshchestvo Izucheniya Manchzhurskovo Kraiya, Kharbin. Serie A. 33, 1-51 (in Russian)
|
Yamamoto, S., 1999. The Blakiston's Fish Owl. Hokkaido Shinbun Press, Japan (in Japanese).
|
Yoshii, C., Yamaura, Y., Nakamura, F., 2018. Predicting future range expansions of Blakiston's fish owl subject to conservation efforts. In: Nakamura, F. (Ed.), Biodiversity Conservation Using Umbrella Species. Ecological Research Monographs. Springer, Singapore, pp. 221–236.
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Year | Total number of nestboxes | Total number of boxes occupied | Box occupancy rate (%) | Number of boxes occupied by Varied Tit | Number of boxes occupied by Cinereous Tit |
2016 | 340 | 101 | 29.71 | 44 | 38 |
2017 | 451 | 171 | 37.92 | 67 | 58 |
2018 | 434 | 179 | 41.24 | 39 | 69 |
Hatching rate | Reproductive success | |||
t-value | P | t-value | P | |
Cinereous Tit | ||||
Conspecific distance | 1.81 | 0.075 | 0.041 | 0.968 |
Heterospecific distance | 0.30 | 0.765 | −0.488 | 0.633 |
Varied Tit | ||||
Conspecific distance | −0.267 | 0.791 | −0.193 | 0.849 |
Heterospecific distance | 1.241 | 0.219 | 0.600 | 0.557 |