Territoriality is one of the most decisive aspects in ecology and behavior of animals, humans included, with important evolutionary implications. Hence, the study of territoriality in long-lived vertebrates might be a good proxy for this purpose. In this study we propose a new view in spatial ecology of large vertebrates by which territories exist by themselves and are independent of the individuals occupying them. To the best of our knowledge, this had not been taken into account in studies of territoriality to date. To this end, we have taken advantage of a large sample size either in terms of number of locations (4791080 GPS locations), number of territories occupied by different individuals (22 territories), and in terms of study duration (seven years).
Annual territorial overlap between individuals within the same territory
Our results show that the area and delimitation of territories remain the same over the years regardless of the individuals inhabiting them, with a high mean percentage of overlap between individuals occupying the same territory (80.95 ± 13.44%). This means that the territory remains constant regardless of whether it is used by one pair, by a new pair or by a pair formed by a previous and a new individual. Our result of the overlap between different occupants of a territory has never been studied before, neither in Bonelli's eagle nor in other vertebrate species. Instead of that, there are previous studies that measured the inter-annual fidelity by each individual or overlap between sexes. The overlap percentage of the occupants of a territory recorded in our study is higher in comparison to these previous studies in Bonelli's eagle of individual overlap percentage recorded by GPS (30.3%, n = 7, Pérez-García et al., 2013; 76.8%, n = 8, Martínez-Miranzo et al., 2016), but lower than the percentage of overlap between sexes recorded by radio-tracking (98.6%, n = 10, Bosch et al., 2010). The overlap percentage is also higher than the percentage of individual inter-annual fidelity overlap described in other raptor species such as the Golden eagle (Aquila chrysaetos) (60%, n = 8, radio-tracking, Marzluff et al., 1997; 70% (99% kernel), n = 17, GPS, Watson et al., 2014), and Spanish imperial eagle (Aquila adalberti) (75%, n = 8, radio-tracking, Fernández et al., 2009). The higher percentage recorded in this study is probably due to the larger sample size (n = 51 individuals) and the higher precision of the raw data (GPS/GSM telemetry versus combined Argos/GPS telemetry or radio-tracking). Therefore, our results show the fidelity and similarity between individuals occupying the same territory and the definition of territorial limits do not change over time.
Interestingly, our results also show that space use could also be oppressed by neighboring territorial pairs. Our overlap analysis shows that the shape of the territory is also maintained in addition to its extension. Moreover, the topology of the territory is not similar between neighboring pairs; whereas some are elongated, others are rounded; others are more irregular, adapting to the physiognomy of the terrain and maintaining these limits and this differentiated shape across individuals and time.
The invariability of the territories is also supported by the statistical results of the GLMM in the sense that the limits of the total home-range size (K95%) do not vary significantly either over time or by the different occupants. In fact, both the extension of active use areas (i.e. feeding and resting; K75%) and the core areas of the territory (K50%) are invariant between years and between individuals within the same territory. Smaller home-range size of females (K95%, K75% and K50%) is explained by incubation tasks during the breeding season (López-López et al., 2021).
Territory eccentricity
The invariance in eccentricity within each territory corroborates the stability of territory physiognomy. Eccentricity has been previously studied in Bonelli's eagles between breeding and non-breeding periods (Bosch et al., 2010), finding a significant eccentricity value for breeding areas in relation to the global home range. In other species such as the booted eagle (Aquila pennata), eccentricity has been also studied without finding differences between sexes and between breeding and non-breeding seasons (López-López et al., 2016a).
The location of the nest in the different topologies of the territories can also vary, either centrally or eccentrically. Despite these differences, the distance between the centroid and the nest remains constant among the different individuals occupying each territory over time. These results suggest that territory use is similar for different individuals regardless of nest location and the maintenance of territories independent of time and owners is once again reaffirmed.
Simple and double replacement cases
To further demonstrate our hypothesis, we now discuss the cases of territories where single or double substitution occurred. The members of the pairs occupying the territories in most cases of replacement had died or disappeared and the new member maintained the same territory as the previous one. How does the fact that both members of the pair disappear at the same time affect the physiognomy and boundaries of the territory?
Our hypothesis on the invariability of the territory is shown again. For example, in the first case of a double turnover, despite the disappearance of the pair, the neighbors did not occupy a part of the territory by extending the boundary of their territory in that direction. Instead, they maintained their boundaries with the same configuration and eccentricity. In a second case, two neighboring pairs did not extend their territorial boundaries into the territory of the pair that had disappeared. The pair that did so inhabited practically all of the new territory, maintaining their original territory with pre-existing boundaries in the occupied territory and did not extend the area of the occupied territory nor its shape. This could happen because the territory of the missing pair was surrounded by marked pairs except on one side, which overlooks an orange grove and urban territories that were not occupied by any Bonelli's eagle pair. In successive years, this pair that occupied two territories, gradually reduced its extension but maintained the core area of both territories, and the neighbors did not occupy part of the abandoned territory. In the case of simple replacements, our results show that the new member of the pair adapts the limits of its home-range to the previous one, also similar to the other member of the pair (the non-substituted one).
To date, it was thought that territory boundaries were maintained by pressure from neighbors (Fryxell, and Lundberg, 1997; Adams, 2001; López-Sepulcre and Kokko, 2005) and disappeared when the defending pair died, disfiguring the boundaries and shape of the territory, resulting in the eventual occupation by neighboring pairs. The boundaries of the territories of the pair inhabiting the empty territory would also be disfigured.
Evolutionary implications
The turnover events recorded in this study by means of accurate GPS/GSM telemetry have made possible to assess the outcome of individual turnover from established territories in long-lived vertebrates. To the best of our knowledge, this is the first time the pre-existence of territories with their entity, regardless of the individuals that occupy them, has been supported by field information.
In many animal strategies, the evolution of territoriality reflects the balance between benefit and cost (Ord, 2021). Species whose males use territories to monopolize access to females appear to incur higher costs than those that defend only food resources (Adams, 2001; Ord, 2021). On the other hand, Wilson (1975) considered that territory could change in time and space, that it may not be a fixed space. On the contrary, other argued that territories are fixed spaces (Brown, 1975; Kauffmann, 1983). We consider that the existence of stable territories regardless of the individuals occupying them may represent an evolutionary advantage that we could divide into the following points: 1) territoriality increases population stability and floating individuals form a buffer against fluctuations (López-Sepulcre and Kokko, 2005); 2) the age and the quality of a territory (measured as reproductive success) are correlated (Ferrer and Bisson, 2003). We, therefore, distinguish a constant struggle in the floating population to reach the best territories, usually replacing agonistically a member of the pair or, in the case of a natural loss, by occupying the vacant in the territory as soon as possible. In fact, our field observations show that replacement after a vacancy takes place usually in less than few weeks. In contrast, the formation of new territories by tracked animals has not been recorded throughout the study period. In this continuous struggle, the best specimens settle in the best territories, which are the ones that favor the continuity of the population. The main evolutionary advantage is that no energy is wasted in founding, exploiting and defending new territories with limited chances of success. We have proposed this territorial strategy for Bonelli's eagles, it remains to be seen which other animal groups or species are also partially or adapted to this strategy.
Implications for conservation
The assessment of the independent pre-existence of territories is of great value for the conservation of territorial species. Hence, the identification of territories regardless of the state of occupancy and its preservation in an adequate state of conservation will facilitate their occupation when an eventual recovery of the species could take place. Finally, this study highlights the role of modern telemetry techniques to get a better understanding of the exact delimitation of territories. This tool makes possible to act with the greatest precision, for example, in the delimitation of protected areas or for taking management actions for endangered species.