The study we present here addresses the challenge of monitoring biodiversity across space and time by using remote acoustic monitoring techniques to assess acoustic activity across an urban–rural gradient on Okinawa-jima in Japan. We found effects of land-use on several soundscape indices, as well as on species’ vocal activity. Furthermore, we observed significant variation across a diurnal cycle and among sites. Daytime anthropophony tended to be higher at urban and suburban sites, which we believe may reflect an effect of urban noise and the diurnal anthropogenic cycle, as human activity is often highest during daylight hours (Fuller et al. 2007; Joo et al. 2011; Gage and Axel 2014). We also identified an increase in species detections along an urban to rural gradient, with stronger impacts on the endangered Okinawa rail and other disturbance-sensitive forest species than on common generalist species.
The soundscape indices reported here displayed systematic variation across sites, particularly along an urban–rural gradient. The Normalized difference soundscape index (NDSI) has been shown to accurately reflect anthropogenic noise when values are low (Gage and Axel 2014), and avian species richness when values are high (Fuller et al. 2015). We found that, on average, our urban site in Sueyoshi park had higher values than our suburban sites in Nago and Nakagusuku. However, the typical baseline NDSI at Sueyoshi was the lowest of all sites, indicating both a weak biophony and a persistent and constant noise from the city that was easily observable in spectrograms (NRF pers. obs.). In contrast, Nago and Nakagusuku had high baseline NDSI values with frequent incidents of high anthropophony, likely due to passing trucks or aircraft. This suggests that in a dynamic acoustic environment, complex temporal models may be necessary to better disentangle the effects of temporary and persistent acoustic disturbance (Botteldooren et al. 2006).
Acoustic diversity (ADI), which describes the diversity of 1 kHz frequency bands in a recording (Villanueva-Rivera et al. 2011), showed a strongly negative association with forest land cover and a strongly positive one with urban land cover. Given that bird diversity is highest at in the northern Yambaru forest, both in prior wildlife surveys (Itô et al. 2000; Biodiversity Center of Japan 2004) and in our species detections, we do not expect this ADI gradient to reflect species diversity. One explanation for this pattern is the constant broadband sound emitted by cicadas, which were recorded during most of the day throughout the study period. However, this pattern may also be explained by the prevalence of broadband anthropophony events in urban and suburban Okinawa. This result highlights the need for cross-validation of soundscape index values with estimates of local biodiversity, particularly birds and stridulating insects.
It is important to note some of the limitations inherent in drawing spatial conclusions from a small number of sites. Previous studies have shown that while soundscapes tend to be spatially auto-correlated (nearby areas sound similar), they can show important variation in sound amplitude, propagation, and diversity indices (Pekin et al. 2012; Rodriguez et al. 2014). Thus, further sampling is necessary to draw solid conclusions regarding the relationship between Okinawa’s soundscape and geography, and is indeed underway.
We identified several soundscape trends which were driven either solely or in part by weather conditions. The identified bands of lower acoustic diversity and complexity, and higher evenness roughly midway through our study correspond to a period of poor weather. During this time, high wind speed reduced acoustic diversity but increased evenness, whereas higher daily rainfall was associated with increased ADI and acoustic complexity (ACI). This seems intuitive, as it is widely accepted that geophony influences soundscape indices either directly through the impact of wind or rain on the soundscape (Farina 2014), or indirectly through the impact of geophony on the signaling behavior of sound-producing animal species (Davidson et al. 2017).
Automated species detection
Using an automated recognition approach, we were able to consistently detect vocalizations from all five focal species. The degree of accuracy varied for these detections between sites and species, with an average accuracy of 76.8% in locations where species were confirmed as present (Table 1). This accuracy level was generally sufficient to allow human confirmation of detection events. Furthermore, cluster assignment score cutoffs can be applied to enable conservative scoring of species presence or absence with minimal human interference. Ultimately, we were able to document a clear effect of geographic location—and potentially urbanization—on the focal species in our study. The two most common species in our study (Corvus macrorhynchos and Hypsipetes amaurotis; see Biodiversity Center of Japan 2004) were present at all five sites, and vocalization density of these species was least affected by our urban–rural gradient. We found that forest species (Halcyon coromanda and Otus elegans) showed a clear decline in vocalization density towards the more urban southern sites, suggesting greater sensitivity to disturbance. At the Yambaru forest site, Manabi no Mori, we were able to consistently detect the endangered Okinawa Rail, Gallirallus okinawae, whilst false positives for this species at other sites were minimal and exhibited poor clustering scores. Our finding that the detection rate of both G. okinawae and H. coromanda was affected by forest cover, with these culturally important species both being detected more frequently in forest sites, further highlights the value of Yambaru forest in supporting endemic, endangered and culturally significant biota (Itô et al. 2000).
Despite being in close proximity to roads and having large proportional surrounding urban land-use, the Nago forest site appears to be a local refuge for several of our focal species. Our common focal species, Hypsipetes amaurotis and C. macrorhynchos, were highly vocal at this site, as were our disturbance-sensitive focal species, Halcyon coromanda and O. elegans. This may suggest that the forest near Nago is an important site for biodiversity despite its urban setting, which could potentially support some of Okinawa-jima’s endemic species, were their ranges to expand further southwards. The Nakagusuku field site displayed high values of the bioacoustic index (BioA) and ACI, low NDSI and was a local hotspot for Hypsipetes amaurotis vocalizations, and to a lesser degree also Halcyon coromanda, despite the site’s southern location and mixed land-use cover. Along with Takiyamabaru, this site also exhibited a clear effect of diurnal cycle on soundscape indices, mainly for ADI and AEI. But unlike Takiyamabaru, at Nakagusuku we also observed high intensities of both anthropophony—mostly trucks, aircraft, and construction—and biophony—mostly cicadas and birds (SRP-JR and NRF, pers. obs.). This combination of intense biophony and anthropophony may also have contributed to the lower accuracy of our species detection models for Nago and Nakagusuku, particularly for C. macrorhynchos, H. coromanda and O. elegans (see Table 1).
We identified several patterns in our soundscape indices that appear to be driven by stridulating insects. Further, we found a clear effect of weather conditions on soundscape indices and in some cases species detection. Lastly, we observed a ‘dawn chorus’ effect in several indices, which we attributed to bird species vocalizing in the morning.
We found that Acoustic complexity (ACI) was highest at our suburban sites in Nago and Nakagusuku, likely due to the abundance and activity of cicadas (Graptopsaltria bimaculata, Platypleura kaempferi and P. kuroiwae) during the day and a repetitive orthopteran (Hexacentrus unicolor) during the night. Previous studies have found that ACI increases drastically in the presence of cicadas and other orthopterans that produce a broadband signal (Farina et al. 2011; Fuller et al. 2015). BioA was also highest at night in Nago and Nakagusuku, likely due to the persistent broadband signaling of several orthopteran species, especially Hexacentrus unicolor. However, the degree of diurnal differentiation in soundscape index values (particularly NDSI) appeared to be greater at suburban sites, potentially due to the presence of vehicular traffic noises during the day (dark blue lines in Fig. 3).
We also observed several notable temporal patterns that were concordant between our soundscape index and species detection results. Firstly, there was a general decrease in all species’ vocal activity during the period of inclement weather on Okinawa-jima. These low levels of vocalization detection across all species were concurrent with low soundscape values for NDSI and high values for ADI and ACI. This suggests an impact of inclement weather on species behavior, and also serves as a proof of concept by demonstrating the capability of both methods to detect it (Keast 1994). Secondly, we observed a general increase in diurnal species vocal activity during the “dawn chorus” at around 5:30 am. Three of our most abundant species: Hypsipetes amaurotis, C. macrorhynchos and Halcyon coromanda, began vocalizing around this time, and most detections of Halcyon coromanda were observed during the dawn chorus period (5:30–7:30). We found this effect to be correlated with several soundscape indices, with some indication of a dawn chorus being visible for ACI and ADI, but most noticeably for peaks of the Bioacoustic Index, which were a good temporal match with the onset of Halcyon coromanda and Hypsipetes amaurotis vocalizations. Our further recording of soundscapes from the winter supports the detection of a later dawn chorus in October through February (see Fig. 5). Despite the dawn chorus effect being well documented in studies of bioacoustics and soundscape ecology (Kacelnik and Krebs 1983; Wimmer et al. 2013; Towsey et al. 2014), future acoustic monitoring should explore the phenology of this event, and role of seasonal, weather, and biotic interference in determining its timing (Farina et al. 2015; Hart et al. 2015).
Taken together, our results indicate a weather-related decline in both soundscape indices and species detections, a detectable dawn chorus of individual species being visible in our soundscape results, and that several of our soundscape indices were saturated by insect activity for periods of our study. Overall, this is an encouraging sign that the soundscape approach succeeds in reflecting species’ behavioral phenology on Okinawa-jima (Farina et al. 2011; Davidson et al. 2017). Further, our findings suggest that future soundscape studies conducted across the summer season should recognize and treat differently periods of inclement weather and high cicada activity. However, it should be noted that perhaps poor weather conditions and broadband insect acoustic activity are equivalent insofar as they both reduce the signal efficacy of soniferous species due to a ‘filling up’ of acoustic niche space (Hart et al. 2015). We find it encouraging to note that this issue appears to be more manageable when comparing soundscape indices across longer duration recordings, as was the case for our winter recording period.