Japanese tits discriminate between diurnal and nocturnal raptor predators

doi:10.21203/rs.3.rs-7085308/v1

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Japanese tits discriminate between diurnal and nocturnal raptor predators

https://doi.org/10.21203/rs.3.rs-7085308/v1

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Diurnal and nocturnal raptors exhibit significant differences in foraging times and predatory behavior, yet little is known about their nesting defense responses of parent birds to these raptors during the breeding season. This study focuses on the Japanese tits Parus minor using taxidermic experiments to assess whether they discriminate between sparrowhawk Accipiter nisus and Indian scops owl Otus bakkamoena. Our results show that the nesting defense behavior of Japanese tits towards sparrowhawks is significantly lower than that towards owls. Specifically, Japanese tits predominantly engage in distant observation behavior when encountering sparrowhawks, whereas they display more aggressive behavior toward owls. Overall, we propose that Japanese tits discriminate between sparrowhawks and owls, with the latter posing a lesser threat to adult birds.

nest defense behaviors

Japanese tits

sparrowhawk

owl

Birds can assess the risk that various predators present (Saavedra et al., 2020). Studies have shown that birds demonstrate different anti-predator behavior when confronted with one predator vs. another. For instance, cinereous tits Parus cinereus observe an aerial predator like the sparrowhawk at long-distances, whereas they are aggressive towards a ground predator, such as the chipmunk Tamias sibiricus (Shen et al., 2023). However, threats posed by predators of the same type can still vary significantly. Red-backed Shrikes Lanius collurio, for instance, exhibit a higher frequency of mobbing behavior toward the common kestrel Falco tinnunculus, which primarily preys on small mammals, compared to the Eurasian sparrowhawk, which mainly targets small birds (Strnad et al., 2012). Accurately assessing the risk for different predators is crucial for the survival of the bird (Mutzel et al., 2013; Thys et al., 2019).

The raptor is one primary predator of small birds. The raptor foraging time can indicate their predatory habits, thereby influencing the defensive behavior of their prey. Falconiformes, such as hawks and falcons, are primarily active during the day, whereas Strigiformes, such as owls, are mainly active at night (Arnold et al., 2006). Balbontín et al. (2020) found that the barn swallow Hirundo rustica recruits more swallows and makes more attacks when confronted by the small owl Athene noctua compared to engaging the falcon Falco peregrinus. This may be due to the greater survival pressure by nocturnal predators on adult barn swallows (Balbontín et al., 2020). Previous studies have shown that during the breeding season, the great tit Parus major, a close relative of the Japanese tit, exhibits different anti-predator behavior toward owls compared to sparrowhawks (Curio et al., 1983; E et al., 2024). However, there is limited research available on the anti-predator behavior of parent birds in response to diurnal and nocturnal raptors during breeding seasons.

Japanese tits, a common cavity-nesting bird, have the ability to discriminate raptors from rodents based on their size; this allows the birds to assess the threat to their offspring (Dunn et al., 2021; Yu et al., 2021). Our present study has focused on Japanese tits and conducted field dummy experiments to assess their ability to discriminate between sparrowhawks and Indian scops owls. The owl primarily preys on rodents and is a secondary cavity-nesting birds, whereas the sparrowhawk mainly targets birds and is an open-nesting species. This niche difference results in the owl exerting significantly lower predation pressure on adult Japanese tits compared to the sparrowhawk, although it may impose higher predation pressure on nestlings (Galeotti et al., 1991; Zawadzka et al., 2001). Therefore, we proposed that Japanese tits can distinguish between sparrowhawks and owls, thereby exhibiting stronger anti-predator behavior toward owls which pose a lower predation risk to themselves, albeit a higher risk to their nestlings.

The study was conducted in the Zuojia Nature Reserve (44°01′–45°00′N, 126°00′–126°08′E) of Jilin Province, Northeast China. Both sparrowhawks and owls are distributed in this region, although they exhibit significant differences in their activities and dietary preferences. The sparrowhawk is primarily diurnal, whereas the owl hunts during twilight and night. The oriental turtle dove Streptopelia orientalis was also part of this study and served as a control species (Yu et al., 2017).

Prior to the breeding season, artificial nest boxes were placed in the Zuojia Nature Reserve to attract Japanese tits for nesting. Starting in mid-April, nest boxes within the study plots were monitored weekly. Upon detecting signs of nest occupation, the observational frequency was increased to every 2–3 days. Breeding parameters were recorded, including the date of the first-egg laying, their number, clutch size, as well as incubation and hatching times.

Experimental trials with dummy sparrowhawks, owls and doves were performed during nesting periods from May 18 to June 18, 2022, and when nestlings were 5 to 10 days old. Experiments were performed on clear, windless days between 8:00 am and 5:00 pm. The presentation of these dummies was randomized with at least 1-hour intervals between trials. Upon confirming the absence of adult Japanese tits near the nest, dummies were promptly positioned on the nest box lids. The human observer was hiding about 10 to 15 m from the nest and recorded responsive behavior for 5 minutes following the appearance of birds within 10 m of the nest. All trials were recorded using a video-recorder (SONY TD20E, Sony Corporation, Tokyo, Japan) for subsequent behavioral analysis. Dummy birds were maintained in natural standing postures, with two dummies per species randomly selected for trials to minimize posture-related experimental bias. Trials were aborted if adult birds failed to return within 30 minutes post-placement, with subsequent attempts at ~1-hour intervals. All dummy trials were completed in a single day in order to control for meteorological variations.

The researcher assessed the birds' responsive behavior using a 5-point scale with the following scoring criteria: 1 point, the tit ignored the dummy and continued feeding nestlings; 2 points, the tit remained stationary while monitoring the dummy; 3 points, the tit exhibited vigilance behavior, such as hopping or wing-flashing; 4 points, the tit approached the dummy, spread its wings and tail, displayed body swaying (accompanied by hissing calls), and/or made aggressive postures without physical encounter (e.g., hovering), and 5 points, the tit directly engaged using physical aggression toward the dummy. If multiple behaviors were observed during a given trial, the highest recorded score was recorded (Møller et al., 2015; Yu et al., 2017)).

Statistical analysis

The Cumulative Linear Mixed Model (CLMM, clmm in R package ordinal) was used to analyze significant differences in the response behavior scores. The 2-tailed likelihood ratio test was used to obtain P-values. In this model, the response score was set as the dependent variable, whereas the dummy type, brood size, and nestling age were included as fixed independent terms. Nest box number and presentation order were treated as random independent terms. When significant differences were detected in multiple comparisons, post-hoc pairwise comparisons were conducted using the same method, with P-values adjusted by the false discovery rate correction.

There were significant differences in the response behavior scores of Japanese tits (n = 24 nests) to three kinds of dummies (CLMMs, x² = 15.26, df = 2, P < 0.001), but brood size (x² = 0.46, df = 1, P = 0.498) and nestling age (x² = 0.08, df = 1, P = 0.774) had no effect on dummy response scores. Comparative analysis revealed that Japanese tits had significantly higher nest defense scores against owls than against sparrowhawks (adjusted P < 0.01). However, the defense response scores toward owls were significantly higher than those toward doves (adjusted P = 0.030). While the Japanese tit response was similar to that of sparrowhawks and doves (adjusted P = 0.091), Japanese tits displayed predominantly vigilant or intimidating behavior towards owls. On the other hand, when confronted with doves, Japanese tits exhibited more vigilant behavior, yet when facing sparrowhawks, most Japanese tits displayed stationary observational behavior showing the lowest average response score (Fig. 1).

Consistent with our predictions, Japanese tits exhibited significantly different anti-predator behavior when confronted with diurnal vs. nocturnal raptors. Basically, they demonstrated stronger nest defense responses toward owls than sparrowhawks. During the breeding season, when birds detect perched raptors, their nest defense strategies generally fell into two categories: 1) parents adopted active anti-predator behavior, such as hopping around or directly attacking the predator in order to drive it away, or 2) parents maintained a certain distance from the predator, simply observing its movements to reduce the risk of exposing the exact location of the nest and their own position(Montgomerie et al., 1988). Sparrowhawks primarily prey on birds, including adult birds and larger nestlings active near the nest entrance༈Zawadzka et al., 2001༉.

In this study, experiments were conducted when nestlings were 5 to 10 days old, a stage during which nestlings are too small to move near the nest entrance. Therefore, we predicted that Japanese tits would choose to observe sparrowhawks from a distance to minimize their own predation risk. In contrast, owls primarily prey on small mammals in woodland habitats(Galeotti et al., 1991), resulting in a relatively lower predation frequency. Given the lower actual threat posed by owls to adult birds, Japanese tits adopted relatively proactive anti-predator behavior, such as close-range intimidation, to drive them away. We propose that Japanese tits discriminate raptor sparrowhawks from owls, and adjust their anti-predator behavior based on the threat level posed by raptors.

Both sparrowhawks and owls exhibit daytime activities, and their primary activity periods show distinct diel segregation(Curio et al., 1983). We speculate that this activity difference may be an important reason for their different defense behavior of Japanese tits against different raptors. In addition, the owl, as a secondary cavity-nesting bird, may enter tree holes or artificial nest boxes to prey on Japanese tits' eggs and nestlings and thus pose a serious threat to the offspring of Japanese tits༈Шохрин В П et al., 2019༉. In comparison, sparrowhawks build open nests, with its predation strategy relying on fast surprise attack flights, mainly targeting birds in the open nest. Since the nest structure of Japanese tits provides a natural physical barrier, the threat of sparrowhawks to its nestlings is relatively small༈Panter et al., 2021༉. The ecological differences in nest site selection of raptors may lead to Japanese tits facing different degrees of nest predation pressure, which in turn affects the strategy and intensity of their anti-predator behavior.

Acknowledgements

The authors would like to express their deep gratitude to all of the contributing bird ringers from Chao Shen, to Jiangping Jin for field assistance, to Jiaru Zhang for his advice about statistical methods. The authors also highly appreciate that Prof. Kevin H. Mayo checking the text for English language.

Authors’ contributions

ME and DL conceived and designed the study. CS and JJ conducted the investigation in the field, analyzed the data and drafted the manuscript. JZ and JJ assisted the field work. All authors read and approved the final manuscript.

Funding

Financial support has been provided by National Natural Science Foundation of China (32272650 to DL), the Open Project of Ministry of Education Key Laboratory for Ecology of Tropical Islands, Hainan Normal University, China (No. HNSF-OP-202301).

Data availability

The data presented in this study are available on request from the corresponding author.

Competing interest

We declare that we have no competing interests.

Ethics approval and consent to participate

The experiments comply with the current laws of China, where they were performed. Fieldwork was carried out with permission from the Zuojia Nature Reserve and the Forestry Bureau of Jilin Province of China (approval number: 2006178). The National Animal Research Authority approved experimental procedures in Changchun Normal University, China.

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No competing interests reported.

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Japanese tits discriminate between diurnal and nocturnal raptor predators

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