Calibration of visually estimated distances to migrating seabirds with radar measurements Marı́a Mateos,1,2,4 Gonzalo M. Arroyo,1,2 Alejandro Rodrı́guez,3 David Cuenca,1 and Andrés de la Cruz2 1 Biology Department, Faculty of Marine and Environmental Sciences, University of Cádiz, Av. Republica Saharaui, s/n, 11510 Puerto Real, Cádiz, Spain 2 Fundación Migres, Complejo Huerta Grande, Ctra. N-340 Km 96.7, 11390 Pelayo, Algeciras, Cádiz, Spain 3 Department of Conservation Biology, Estación Biológica de Doñana, CSIC, Américo Vespucio s/n, Isla de la Cartuja, 41092 Sevilla, Spain ABSTRACT. Censusing seabirds from coastal areas requires reliable estimates of bird numbers and the distances of the birds from the coastline. Logistical constraints make visual estimation of distances the only feasible method in many studies. We tested the accuracy of visually estimated offshore distances of six migratory seabird species in the Strait of Gibraltar using simultaneous measurements obtained by radar. Most birds (91%) were detected within 3 km of the coast and we truncated our calibration at this distance. We found a strong correlation between radar and visual estimates (R 2 = 0.83, P < 0.0001). The magnitude of errors in visual estimates was moderate and ranged from 0.08 to 0.20 for different distances and observers. Among the factors potentially affecting the accuracy of visual estimates of distance to seabird in our study were observer identity, bird species, bird behavior, and weather; the most parsimonious model in our study included observer identity as the only predictor, and no model with more than one predictor had a smaller Akaike’s information criterion value. Radar can be used to help train observers and to reduce biases in visual estimates of distances by means of calibration. When no other methods are available to accurately measure distances to seabirds, visual estimates of distances, recorded by experienced observers and once calibrated with radar (or other ground-truthing methods), may be acceptable for different species under a wide range of environmental conditions. RESUMEN. Utilización de medidas de radar para la calibración de distancias a aves marinas migratorias estimadas visualmente Censar aves marinas desde áreas costeras requiere estimaciones fiables del nú mero de aves y de la distancia de estas a costa. Restricciones logı́sticas hacen que a veces las estimaciones visuales de las distancias sean el ú nico método factible para llevar a cabo estos estudios. Pusimos a prueba, en el Estrecho de Gibraltar, la exactitud de las estimaciones visuales desde costa, utilizando seis especies de aves marinas, concurrentemente, con medidas obtenidas por radar. La mayorı́a de las aves (91%) fueron detectadas dentro de un área de 3 km de la costa y ajustamos nuestra calibración a esta distancia. Encontramos una fuerte correlación entre las estimaciones visuales y las del radar (R 2 = 0.83, P < 0.0001). La magnitud de los errores visuales al estimar las distancias fue moderada y variaron de 0.08 a 0.20 para diferentes distancias y observadores. Entre los factores que afectaron a la exactitud de las estimaciones visuales, se encuentran el observador, la especie de ave, la conducta exhibida por el ave y las condiciones meteoroló gicas. El modelo con mayor parsimonia incluyó la identidad del observador como el ú nico vaticinador y ningún otro modelo, con más de un vaticinador, tuvo un valor de AIC menor. El radar puede ser utilizado para entrenar al personal y reduce el sesgo en las estimaciones visuales mediante la calibración. Cuando no hay disponible otros métodos para medir con exactitud la distancia a que se mueven las aves marinas, el uso de observadores experimentados y una calibración con radar (u otro método), pueden ser aceptables para trabajar con diferentes especies bajo una amplia gama de condiciones ambientales. Key words: coastal migratory routes, distance calibration, distance underestimation, seabird abundance, seaclutter, Strait of Gibraltar Distance sampling is a widespread method for estimating animal abundance (Buckland et al. 2001, 2004), and may be useful for estimating densities of marine birds (Komdeur 4 Corresponding author. Email: maria.mateos@ uca.es et al. 1992, Camphuysen et al. 2004). Along seabird migratory pathways or frequently used flight paths, such as between foraging areas and breeding colonies, surveys from stationary observation platforms are required to census birds (Camphuysen et al. 2004). These counts may yield abundance estimates with high accuracy provided that distances to birds can be measured without biases (Buckland et al. 2004). Different procedures have been used to obtain those distances, including visual estimates, optical range finders (Heinemann 1981), binocular reticules (Yen et al. 2004), radars (Petersen et al. 2006), and laser range finders (Ransom and Pinchak 2003). Characteristics of the surveyed populations, environmental conditions, and the accuracy required will dictate which methods should be used (e.g., Bibby et al. 1992). Estimating distance by eye has been criticized, but could be the only option under some circumstances (Bibby et al. 1992), and nearly all seabird census work, whether using shore-based or shipboard observers, relies on visually estimated distances. However, no assessment of the accuracy with which observers estimate these distances exists. Previous attempts to measure error in distance estimates to animals at sea, and the possible effects of factors such as weather on the accuracy of visual estimates of distance, have focused on cetaceans (Schweder 1997, Baird and Burkhart 2000, Williams et al. 2007). Because detection conditions and methods for estimating distances to cetaceans differ from those used for seabirds, calibrating distance estimates to birds at sea may require specific studies as well. However, to our knowledge, no study has assessed errors in distance estimates to seabirds or has examined the factors that may influence these errors. Different types of error may arise from visual estimation of distances, with biased distance estimates posing the main problem because they are difficult to detect and will transfer errors to the estimates of bird abundance. Such errors can be corrected either in the field through testing procedures and calibration (Marques 2004, Williams et al. 2007) or through statistical techniques employed during data analysis (Chen 1998, Marques 2004). Posthoc analytical approaches are less robust than field-testing programs (Marques 2004, Marques et al. 2006, Williams et al. 2007). Calibration of distance estimates to seabirds is therefore needed to improve estimates of bird abundance. Calibration will be further enhanced if errors in distance estimates could be predicted from factors such as bird size, bird behavior, weather conditions, or observer ability. We recorded and compared visual and radar estimates of distances to flying seabirds along a migratory pathway. Our specific aims were to: (1) test the accuracy of visually estimated off- shore distances to seabirds by means of radar measurements, and (2) determine the effect of bird size, bird behavior, weather, and observer skill on the accuracy of visual estimates. METHODS Our study was conducted from 5 March to 20 April and 16 October to 18 November 2006 at the Strait of Gibraltar (Fig. 1). This channel is 14 km wide at its narrowest point and is the only connection between the Atlantic Ocean and the Mediterranean Sea. Fieldwork was carried out at Tarifa Island (southwest Spain), the southernmost point of the north coast of the Strait of Gibraltar (Fig. 1). From this point, simultaneous observations of migrating seabirds were collected by an observer and a radar operator. The radar antenna and observers were at the same vantage point. Observers scanned the sea with and without the aid of binoculars (Victory FL 10 × 42 T; Zeiss, Oberkochen, Germany) and telescopes (Zeiss 20–60 × 85). Each seabird flock detected was identified to species level and its distance from the coast was estimated by the observer who then communicated the position of the flock and its flight direction to the radar operator. If the target was found on the screen, distance was also measured simultaneously by an Sband surveillance radar (FR-2137SBB, Furuno, Nishinomiya, Japan; peak power output 30 kW, variable pulse 0.07- 1.0 jis, transmitting at 3050 MHz) located on a platform 10 m above sea level. Distance estimates were made when targets crossed an imaginary line perpendicular to the coast at the observation point. At the beginning of each observation period, the radar operator adjusted the radar parameters (range, gain, and sea and rain filter) to optimize the radar picture. We combined both the range function and the off-center function, placing the origin (antenna position) in the lower part of the screen, to reach a scanning radius of either up to 4.5 km (short range) or 9.1 km (long range), with scanning radius alternated with each observation period. Gain, the receptor sensitivity to the energy reflected, was adjusted from 45 to 100, where 100 corresponded to the maximum sensitivity. Sensitivity was between 51 and 70 75% of the time, between 45 and 50 10% of the time, and between 71 and 100 15% of the time. The sea clutter filter reduced Fig. 1. Details of the African and Spanish coastline in the area of Tarifa. Note the characteristic narrow funnel-shape of the Strait of Gibraltar. Tarifa Island is the most efficient location for surveying seabirds the Strait of Gibraltar from the coast (Programa Migres 2009). the clutter produced by waves (0 = off; 100 = maximum). However, using this filter may result in the loss of weak echoes. The best setting was achieved when the size of the spots produced by sea clutter on the radar screen was minimized while weak echoes unequivocally produced by flying birds remained visible. During our study, the sea clutter filter was set at values ranging from 0 to 40, with the filter set between 11 and 30 75% of the time. The rain filter (range = 0– 100) reduced the clutter produced by the rain, and was always set at values <30 (and was set at zero 90% of time). Data were collected under a wide range of meteorological conditions, and visual observations were made by three experienced observers. All observers had censused seabirds for more than 4 years at the study site, were familiar with the bird species and environmental conditions occurring in the study area, and had worked with the radar for 4 months before the onset of this study. We restricted our analyses to the six most abundant seabirds, including Northern Gannets (Morus bassanus), Cory’s Shearwaters (Calonec- tris diomedea), Balearic Shearwaters (Puffinus mauretanicus), Atlantic Puffins (Fratercula arctica), Razorbills (Alca torda), and Great Skuas (Catharacta skua). Due to the difficulty of identification and the frequent occurrence of mixed flocks, Atlantic Puffins and Razorbills were considered together and referred to as auks. For each sighting, observers recorded species, flock size, flight direction, and estimated distance. Each hour, we recorded the speed and direction of wind at the observation site. After examining the frequency distribution of wind directions during 2006 at the Tarifa meteorological station, wind directions were categorized as either east or west because winds came from these directions 94% of time. Easterly winds (51.2% of records) had a mean direction (±1 SD) of 79.8 ± 22.2◦ , and westerly winds (42.8% of records) a mean direction of 271.0 ± 39.8◦ . All flying birds were observed heading either east or west. Flight directions were categorized as either with a headwind or tailwind (Spear and Ainley 1997). Visibility was assigned to one of three categories based on how clouds, haze, and light levels affected visibility of the African coast located 14 km away: (1) good, with the African coast clearly visible, (2) moderate, with only the silhouette of the coast visible, and (3) bad, with the African coast not visible, but the sea surface visible at a distance of about 7 km. No observations were made when boats, which typically follow a route along the center of the strait, could not be seen. Although radar records were used to calibrate visual estimates, radar measurements are not free from error. The technical specifications of our radar establish an inherent measurement error of 1%, with a maximum error of 30 m. Furthermore, birds appear on a radar screen as a two-dimensional echo instead of a onedimensional point, especially when in flocks. We measured the distance to the center of the echo. Thus, there might be a systematic error in these radar distances because the size of an echo on the screen could vary with the distance to the target due to the level of energy reflected. To test the magnitude of this error, we randomly selected a sample of 100 targets. We measured the echo size on the north–south axis on the radar screen with the aid of a geographical information system (ArcView 3.2.; Environmental Systems Research Institute 1999). We finally examined whether echo size varied with distance to the target as measured by radar. Statistical analyses. The error of the visual estimate of distance was calculated as Error = |radar estimate – visual estimate|/radar estimate. Only birds or flocks that were detected visually and had distances estimated with radar were included in the analysis. We did not assume that the relationship between visual estimates of distance, or their error, and the corresponding radar estimates were linear. Therefore, we analyzed this relationship with generalized additive models that may fit nonlinear, smooth functions (Hastie and Tibshirani 1990). Second, we examined whether observer identity, bird species, bird behavior (flock size and flight direction relative to wind direction), and meteorological conditions (wind speed and visibility) influenced the accuracy of visual estimates of distance. We used visually estimated distances as the dependent variable and included the distance estimated by radar as a covariate so that the effect of predictors was assumed to explain measurement errors. We built one model for each predictor and compared their fit to the data with the Akaike’s information criterion (AIC). We then examined whether the fit improved when two or more predictors were combined in the same model. We selected the most parsimonious model as that having the lowest AIC value (Burnham and Anderson 2002). Analyses were performed with the package “gam” in R 2.6.2 (R Development Core Team 2008). We built models assuming a gamma distribution, using the log-link function and thin plate regression splines as smooths functions. We allowed for a maximum of three degrees of freedom for the smooth functions. Values are reported as means ± 1 SD. RESULTS Observers made 1173 sightings that were subsequently located by radar, including 402 Northern Gannets, 375 Cory’s Shearwaters, 265 Balearic Shearwaters, 117 auks, and 14 Great Skuas. Overall, 42.4% of sightings were single birds and the rest were flocks. We made 3.4% of observations during calm conditions (wind speed < 0.5 m s−1 ), 44.9% during periods with easterly winds (range = 0.8– 15.8 m s−1 , mean = 3.9 ± 2.8 m s−1 ), and 51.7% during periods with westerly winds (range = 0.6–9.4 m s−1 , mean = 3.6 ± 2.4 m s−1 ). Visibility was good for 28.1% of the observations, moderate for 45.5%, and bad for 26.5%. Radar estimates of distance to bird sightings ranged from 183 to 6913 m (mean = 1559 ± 1009 m), and visually estimated distances ranged from 100 to 7000 m (mean 1438 ± 978 m). Most contacts (91%) were within 3000 m of the coast, as estimated by radar, and, for further analysis, we truncated our data at that distance. The estimated size of echoes varied from 9 to 33 m (mean = 17.9 ± 7.8 m, N = 100 flocks) for distances to the targets from 105 to 2950 m. Echo size on the radar screen did not vary with distance to the target (R 2 = 0.004, P = 0.65). The error in distance estimates attributed to the size of the echo was small, always <0.04, and, because most targets passed within 500 m, this error was often <0.02. Visual estimates of distance were correlated with the corresponding radar estimates (R 2 = 0.83, F = 1135, P < 0.0001, N = 1068; Figs. 2A and B). The absolute mean difference between visual and radar estimates of distance Fig. 2. Relationship between radar estimates of distance to flying seabirds and corresponding visual estimates in the range 0–3 km. The broken line indicates an unbiased relationship. (A) Data recorded by observer 1, the most accurate observer. (B) Data recorded by observer 3, the least accurate observer. increased with increasing distance, with differences of 141 m, 200 m, and 327 m for distances 0–1, 1–2, and 2–3 km, respectively. The error, however, decreased with distance, with error values of 0.20, 0.15, and 0.13 for the three distance intervals, respectively (overall mean error = 0.17 ± 0.15). Among the factors potentially affecting the accuracy of visual estimates of distance to seabird, the most parsimonious model included observer identity as the only predictor (Table 1), and no model with two or more predictors had a smaller AIC value. All observers tended to underestimate distances, and underestimation was higher at greater distances (>2 km; Figs. 2A and B). Errors in estimating distance were less for observer 1 (mean error = 0.13) than for observers 2 and 3 (mean error = 0.18 and 0.20, respectively) for all distances up to 3 km. Error differences between observers were exacerbated at greater distances. For the 2–3 km distance interval, mean errors were 0.08, 0.19, and 0.20 for observers 1, 2, and 3, respectively. DISCUSSION We found that observers could estimate distances with reasonable accuracy, as reflected by Table 1. Generalized additive models examining the effect of four types of predictors, namely visual observer, bird species, bird behavior (flock size and flight direction), and weather conditions (wind speed and visibility) on visual estimates of distances to seabirds. Distances estimated with radar were fitted as a covariate in all models, taking the form of a spline with 3 df. Predictors AICa AAICb Covariate only 14,785 91 2 Visual observer 14,694 0 3 Bird species 14,780 86 4 Flock size 14,781 87 5 Flight direction 14,784 90 6 Wind speed 14,781 87 7 Visibility 14,780 86 a Akaike’s information criterion. b Akaike differences. c Akaike weights. Model w ic 1.7 10−20 1 2.1 10−19 1.3 10−19 2.9 10−20 1.3 10−19 2.1 10−19 the significant correlation between radar and visual estimates. Furthermore, the error of visual estimates was relatively low (between 0.08 and 0.20, depending on the range of distances and observer) and similar to errors reported for visual estimates of distances to cetaceans (Williams et al. 2007). The required level of accuracy in distance estimates varies among specific ecological applications. However, Marques (2007) suggested that errors less than 10% are needed before applying estimates to distance sampling methodology. Errors in distance estimates produce errors of a similar magnitude in density estimates, that is, distance consistently overestimated by 10% underestimates densities by 9%, and distances underestimated by 10% produce densities overestimated by 11% (Buckland et al. 2001, 2004). Errors of visual estimates of distance in our study were on average higher than recommended for a reliable use of distance sampling methods, and may translate into unacceptably biased estimates of population size. However, a number of authors have suggested that such errors can be corrected through calibration, specifically by using regression equations obtained from the comparison of visual estimates of distances to seabirds with a ground-truthing method (Chen 1998, Williams et al. 2007). Observer identity affected the fit between visually estimated distances and distance measured by radar. As also reported in other studies (Baird and Burkhart 2000, Buckland et al. 2001), the three observers in our study tended to underestimate distances. Underestimation increased at greater distances, which was also observed in flagging experiments (Camp 2007). Moreover, we detected an observer-specific effect of underestimation that produced a systematic error that should be corrected before using data to estimate abundance (Buckland et al. 2001). In our study, the most parsimonious model (model 2, Table 1) may be used as a calibration model to correct the only source of bias we found (Mateos 2009). Differences in accuracy between observers may not be attributed to their degree of training or experience, which was similar among the three observers, but to variation in visual acuity or sharpness, perception of distance, or other aspects of their sensory abilities. Less experienced observers would likely have produced larger errors. Previous studies of the effect of training on the accuracy of distance estimation on land (Gibson and Bergman 1954, Gibson et al. 1955) and at sea (Oien and Schweder 1992, Schweder 1996, 1997) have clearly shown that training improves estimation of distance. Baird and Burkhart (2000) found a similar effect of experience when censusing whales. Calibration experiments involving the use of radar or other ground-truthing methods can be also useful for training observers and reducing differences in distance estimates. The accuracy of visual estimates might also be improved by specific training programs, where observers are told the distances measured with the radar after they estimate the distance to the target. Such training would help observers to better estimate distances (Camp 2007). For investigators without access to radarestimated distances, other methods are available for training observers when measuring distances (e.g., using buoys or floats placed at known distances from the observation point) and we encourage the implementation of training programs prior to field work (either with radar or other methods) for improving the accuracy of distance estimates. Furthermore, our results suggest that, when possible, selecting observers whose inherent ability to estimate distance is best among all potential candidates is advisable. Our results may be also useful for determining strip width when data are taken in the field only by distance intervals (Buckland et al. 2001). For example, in our case, because the highest error value was 0.2 within 3 km of the coast, trying to establish strip widths narrower than 600 m would not make sense. Distance estimates in our study were not species-dependent, even for species that varied considerably in size (e.g., 398 g and 549 mm wing span for Atlantic Puffins and 3010 g and 1850 mm wing span for Northern Gannets) and flight behavior (e.g., fast-flapping auks, intermediate flap-gliding Northern Gannets and glideflapping Balearic Shearwaters, and dynamicsoaring Cory’s Shearwaters). Similarly, the accuracy of distances estimated visually was not affected by weather conditions, flight direction, or wind direction. Consequently, we suggest that when no other method is practical, visual estimates could be reliably used for a wide range of seabird species and field conditions, provided that observers are sufficiently trained. Measuring distance with devices such as telemeters and radar in the field is not free from error and the possible consequences of this error on the estimation of bird abundance are rarely considered. Particularly when using radar, the signal on the radar screen appears as a spot that occupies a space generally larger than a bird or flock in the field. Nevertheless, the magnitude of this error in our study was low (generally <2%), and did not substantially affect the validity of distance measurements. To statistically address measurement errors, many observations are needed (Williams et al. 2007). On the other hand, collecting sufficient ground-truthing data to calibrate visually estimated distances could be costly (Chen and Cowling 2001). However, using radar, we found it possible to obtain a considerable amount of independent data, suitable for calibration, with relatively little effort, and large samples permit more reliable calibration than smaller samples. We conclude that, when no other methods are available to accurately measure distances in seabird studies, surveys by experienced observers can provide reasonably accurate distance estimates under a wide range of environmental conditions and for different species. Our conclusions could be applicable to at-sea surveys for seabirds when observers are on a moving ship, as long as landmarks located at known distances, measured with radar, are available. This might be the case for studies from boats close to the coast or where ship traffic is relatively common. Finally, the ability of radar to detect low-flying seabirds is limited when waves cause sea-clutter, but radar can be used to calibrate visual observations that, in turn, can be obtained under conditions when radar cannot be operated. ACKNOWLEDGMENTS This study was conducted within a collaboration agreement between the Migres Foundation and the University of Cádiz. 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