What are the impacts of human recreational activity on the distribution, nest-occupancy rates and reproductive success of breeding raptors? (systematic review)
One of the most common topics in environmental impact assessment is the effects of human disturbance on bird species, and particularly on birds of prey. However, scientific information available on this topic has never been properly synthesized so that decisions taken by managers can be based on evidence rather than on personal experience or on individual pieces of information which may be inconsistent with the whole.
To systematically collect and synthesize the available published and unpublished evidence in order to answer the question ‘what are the impacts of human recreational activities on nest-occupancy rates and reproductive success of breeding raptors?’
Seven electronic databases were searched using 19 sets of specific keywords. Unpublished information was sought by means of web-based search engines and by writing to individual experts and institutions involved in raptor study and protection.
We included studies that fulfilled the following criteria:
- Subject: breeding raptors (both diurnal and nocturnal)
- Intervention: human recreational activities performed close to nesting sites during the breeding period.
- Outcomes: changes in nesting-site location, nest-occupancy rate and breeding success parameters.
- Types of study: any field in situ study carried out in any part of the world involving wild-breeding raptors, comparing occupied nests (treatment) with random points in unoccupied areas suitable for reproduction or comparing nest location and performance before and after human disturbance took place (BACI experiments).
Data collection and analysis
Agreement between two independent researchers was assessed and a high degree of accordance was found for study inclusion, suggesting a repeatable procedure. Data (all original statistics from which an effect size could be calculated) were extracted following an a priori data extraction protocol regarding subject, intervention and outcome. Random-effects meta-analysis was performed by means of the software Metawin 2.1 on twenty-four independent data points, consisting of means, standard deviations and sample sizes of both control and treatment. The overall data set was divided into subgroups and meta-analysis was performed for each subgroup individually to account for heterogeneity. We modelled causes of heterogeneity by means of the software and environment R, taking individual effect sizes as the response variable, species and nesting site (tree vs. cliff-nesting) as factors and body size as a covariate (both as a continuous variable and as a dichotomous one). Models were built both for Hedge’s d and the log response ratio (lnR), as effect size metrics. Model selection was carried out taking into account the loss of Kullback-Leibler information by means of information theoretic criteria linking classical likelihood theory with theoretical information criteria (Akaike Information Criterion and Akaike weights).
A total of 3887 articles were detected by our specific searches. The final number of articles considered for data extraction was 52. The only outcome that we could meta- analyze was the displacement distance of nests from roads, compared to random points in suitable areas for breeding. Although the literature also provided comparable information on other anthropic variables, such as distance to unpaved tracks, we decided to consider only one of these variables (roads) as surrogate of human access to the countryside. A total of 24 studies were found to provide comparable information on this outcome.
A modest statistically significant effect of the presence of paved roads (as a proxy of human accessibility to the countryside) on raptor nest location was found after performing a random-effects meta-analysis on 24 independent data points (Pooled effect size (lnR)=0.22 (Bootstrap 95%CI 0.036 to 0.423; back-transformed ln Response Ratio 1.28; 1.07-1.57 bootstrap 95% CI). The mean absolute magnitude of nest displacement from roads, compared to random control points, was 663.46±389.23m.
Species negatively affected by roads included Cooper’s hawk, Spanish Imperial Eagle, Cinereous Vulture, Booted eagle, Eagle owl, Common buzzard, Bald eagle, and Peregrine falcon, some of them endangered species. Species which showed a tendency to be positively affected by roads included: Peregrine falcon, Booted eagle and Common Buzzard. The fact that some species such as Booted eagles and Common buzzards are present in both categories suggests that distance to roads is, to some extent, a population-specific trait, rather than a species-specific trait.
When exploring heterogeneity by means of Generalized Linear Mixed Models two explicative variables were considered: size of the raptor (body length), and nature of nesting substrate (tree-nesting vs. cliff-nesting) in addition to species which was incorporated as a random variable to prevent pseudoreplication. The longest displacement distances to roads were shown by big raptors breeding on trees, a group including many threatened species such as Cinereous vulture and Spanish Imperial eagle. Mean distance for this group of species was 1375±922.4m. In fact, model selection by means of information theoretic criteria indicated the influence of body size and nesting substrate on effect size was similar, especially when using Hedges’ d as an effect size metric.
Implications for management / policy / conservation: In countries where forested areas are very fragmented, the fact that big and tree-nesting raptors tend to nest far from roads can be a serious handicap for reproduction. Big raptors commonly nesting on trees (e.g. Booted eagle) which are found nesting on cliffs eventually, might reflect local human disturbance if trees are not scarce. Similarly, typically cliff-nesting raptors found breeding on trees (e.g. Golden eagle) might indicate low local human disturbance, if cliff availability is not a limiting factor locally.
Implications for research: Further empirical work (BACI experiments) to quantify the effect of human recreational activities on breeding raptors needs to be carried out if conservation decisions are to be based on evidence. No substantive progress on knowledge accumulation regarding this topic has been detected in the last 30 years.
The risk of impact of recreational human activities to breeding birds of prey is a common topic highlighted by many environmental impact assessments (EIA) worldwide. However, typically environmental impact studies fail to provide proper evidence on the impact of these activities on breeding success and breeding-site fidelity (dispersal) of individual pairs, and especially on the population and meta- population consequences of human activities (MartÌnez et al. 2003; Su·rez et al. 2003). Often managers use the precautionary principle to limit or ban these activities over sighting the previous step of systematically reviewing the information available to make a decision based on evidence.
When dealing with long-lived species such as raptors the survival of adult age classes is the parameter with a higher influence on the population growth rate. Hence, it is of little relevance to put a lot of resources into improving fecundity if causes of adult mortality owing to human activity (e.g. electrocution, drowning, food scarcity owing to human-facilitated diseases, etc) are operating. On the other hand, permanent breeding dispersal out of occupied territories, owing to human impact, can act as an equivalent of local mortality for the local dynamics of the population. However, in practice, many EIAs do not address the health of local raptor populations, but are only concerned with the fate of particular breeding pairs for which extant laws require protection.
Importantly we know from behavioural science that impact of humans on birds is, to a large extent, a matter of cultural habituation to human presence. Large penguins, living in isolated areas with few or no predators become naÔve and lose costly anti- predator behaviours, although not all such behaviour is affected (Blumstein & Daniel 2005). For example Humboldt penguins (Spheniscus humboldti), which are seldom exposed to human presence apparently do not fear the presence of humans in their breeding colonies, but are actually physiologically stressed (a person passing an incubating penguin at 150 m distance provokes a significant heart rate response), which translates into reduced breeding success (Ellemberg et al. 2006). Likewise Magellanic penguins (Spheniscus magellanicus) show typical adrenocortical responses to stressors when humans are present in their breeding grounds, but only if the colony has not been exposed to very high levels of ordinate human presence. Colonies exposed to moderate levels of disturbance do not show evidence of habituation over a period of a few years (Fowler 1999). Hence a usual management suggestion made by scientists is concentrating tourist visits in a small part of breeding colonies allowing birds in the visitation area to habituate (MartÌnez-AbraÌn et al. 2007).
Nevertheless, the degree and speed of habituation seems to be a species-specific trait as well as a site-specific trait (Blumstein et al. 2003). It also seems to be quite dependent on size and diet, with large predator species having less tolerance to human presence (Blumstein 2006). For example, although some habituation to pedestrians by Spanish Imperial Eagles was shown by Gonz·lez et al (2006) the same species, together with vultures, showed decreased local abundances during weekends associated to increased road traffic in these areas compared to week days (for a similar case with wintering Bald eagles consult Stalmaster & Kaiser 1998). However, the occurrence of other species did not change between working days and weekend days (Bautista et al. 2004). Habituation seems also to vary depending on age. Adult Bonelliís eagles (Hieraaetus fasciatus) may seek the proximity of human settlements during breeding, since they take advantage of human-associated fauna such as pigeons to forage (Sanz et al. 2005), but dispersing juveniles choose areas located farther from villages and roads than expected by chance alone (Balbotin 2005).
Regarding raptors, some wild-ranging species, which in the past were not associated with urban areas at all, are known to be colonising towns and cities as direct persecution by humans has decreased. This is the case of the common kestrels (Falco tinnunculus) breeding in Berlin (Kubler et al. 2005) and in many other large European cities. This is also the case as well of peregrine falcons (Falco peregrinus), re- introduced to many urban areas around the world, such as North America (Cade & Bird 1990; Holroyd & Banasch 1990, Italy (Serra et al. 2001), Per ̇ (Beingolea et al. 2003), Spain (Durany 2006) or Poland (Rejt 2003; 2004), to name just a few. Red- tailed hawks (Buteo jamaicensis) are also expanding into urban locations and seem to adjust well to urbanization (Stout et al. 1998; 2006). Raptors breeding in urban areas have high degrees of popular acceptance (Martell et al. 2000), show high plasticity in their diets to adapt to urban prey availability (eating mostly birds since urbanization increases bird biomass), and higher breeding success than their rural counterparts (Kauffman et al. 2003; 2004) or at least similar (Coleman et al. 2002), because they are often free from human persecution and have lower levels of nest predation and parasitism (Chace & Walsh 2006). In some instances, raptors can find safe places in urban areas to breed whilst moving to the rural outskirts to forage (op. cit.) or, on the contrary, breed in wild areas and move to urban or suburban areas to forage (Brambilla et al. 2006). However, sometimes urban environments act as ecological traps providing misleading cues of habitat quality to raptors such as Cooperís Hawks (Boal 1997).
Hence, not only colonial breeding birds can get used to human presence but also solitary breeders such as some falcons and hawks, since urban breeding entails habituation to humans. Some level of habituation to humans by raptors also occurs when humans frequent the breeding grounds of raptors breeding in wild areas (Gonz·lez et al. 2006). However habituation only can occur when two main requirements are met: a) lack of direct effect on birds by means of the proper ordination of human visits (McClung et al. 2004; Finney et al. 2005; Arroyo & Razin 2006) and b) high intrusion frequencies over a long time period (Gonz·lez et al. 2006; see Urios & MartÌnez-AbraÌn 2006 for a case of low habituation of a social raptor in an island colony with a low load of terrestrial visitation, but moderate levels of boat affluence during the breeding period). Raptors breeding in isolated sites are not used to human presence, and are most likely especially vulnerable to disturbance.
The question arises whether individual pairs (using either cliff, ground or forest breeding habits) can have their breeding success and fidelity to nesting sites affected by human recreational use of their breeding grounds. Breeding success can be influenced by a number of factors such as reduced nest attendance and consequent cooling or overheating of eggs, permanent clutch abandonment, absence of replacement clutches, lower success of replacement clutches, reduced chick brooding owing to temporal abandonment, permanent chick abandonment or reduced foraging success and hence reduced feeding rates to chicks. In turn, nest-site fidelity can be affected within a breeding season (nest abandonment with subsequent re-occupation) or between seasons (no nest re-occupation between seasons or permanent dispersal).
On the other hand it will also be important to keep in mind during the process of review of this question that human recreational uses could affect raptors more by reducing the quality of potentially good sites for breeding, which are presently unoccupied, than by affecting the normal development of breeding in presently occupied sites. Human occupation of potentially good sites may be the cause for density-dependent inter-specific competition among raptor species with increasing growth rates, owing to site limitation, with negative effects for the less aggressive species (see Ontiveros et al. 2004). This general scarcity of high-quality breeding sites could explain the earlier breeding calendar of some raptor species syntopic to other such raptor species, with more aggressive behaviours, when the more aggressive one or both are showing increasing trends.
Here we shall explore the literature on breeding-site fidelity and breeding success of diurnal raptors to find out whether there is scientific evidence of any effect of recreational activities on the components of fecundity and breeding dispersal as well as on the determinants of these effects, if they occur. To the best of our knowledge only Sidaway (1990) and Woodfield & Langston (2004) have made traditional reviews on the disturbance of human access on foot to birds. Likewise, an ongoing systematic review is now dealing with the impact of public access on ground-nesting birds (Dave Showler, pers. com.). A traditional review oriented to protecting raptors from human disturbance can also contain relevant information on the topic to review (Richardson & Miller 1997).