Potential functional and numerical response in a large sized raptor may be mediated by the abundance of an exotic lagomorph

1 Introduction

Predators that rely on a particular prey as their main food source may be affected in different ways according to shifts in the abundance of such prey (Jaksić, 1989; Marti et al., 1993; Dupuy et al., 2009). Generally, when the abundance of the most consumed prey decreases predators show a functional response adjusting their diet. According with the alternative prey hypothesis (Angelstam et al., 1984), predators may adapt their diet according to fluctuations in the abundance of their main preys. When this functional response fails to compensate the shortage of resources, a numerical response may take place altering different population parameters (Solomon, 1949; Redpath and Thirgood, 1999). For instance, predators that relied on native European rabbits (Oryctolagus cuniculus) in Spain suffered significant changes when an outbreak of the rabbit hemorrhagic disease (RHD) reduced rabbits population in the early 1980’s (Moreno et al., 2008; Lees and Bell, 2008; Moleón et al., 2009). Most predators changed their diets to cope with the lack of prey (Fernández, 1993; Moleón et al., 2009, 2012). The decrease of rabbits reduced the breeding performance of some species (Fernández, 1993), and produced the loss of breeding territories (Martínez and Zuberogoitia, 2001).

A large number of foreign species have been introduced in many ecosystems worldwide, causing impacts of different magnitudes (Vitousek et al., 1996; Lowe et al., 2000). Some of these alien species adapted fast to their new environments becoming primary prey for the native predators of the invaded community (Tylianakis et al., 2008). When a new prey decreases, this may impact native predators’ assemblages that currently rely on it strongly (Tablado et al., 2010).

In Patagonia, southern South America, the food source for the predator assemblage has been modified in the last century by the introduction the European hare (Lepus europaeus). It constitutes an abundant, relatively easy to hunt and rich in biomass prey for the medium-to-large sized carnivore assemblage extant in Patagonia. It was introduced in 1888 and by 1980 it was already present in most of the Argentinean territory (Grigera and Rapoport, 1983). Currently hares are consumed by several Patagonian raptors (Hiraldo et al., 1995; Monserrat et al., 2005; Lambertucci et al., 2009; Barbar et al., 2016a,b), as well as other terrestrial predators (Novaro et al., 2000). However, there are almost no studies evaluating the long-term effect of the hare population fluctuations on the predator populations from South America.

One of the predators that strongly feed on the European hare is the black-chested buzzard-eagle (Geranoaetus melanoleucus, hereafter “eagle”, Hiraldo et al., 1995). This is a large raptor that inhabits open areas from Venezuela to southern Argentina (Ferguson-Lees and Christie, 2001). In Patagonia it presents one of the highest densities of breeding territories for any eagle species (Hiraldo et al., 1995; Barbar et al., 2018). It is a generalist that consumes small mammals, birds, reptiles and arthropods. The European hare is the most important item consumed in northwestern Patagonia by both territory holding adults and non-reproductive immatures. Furthermore, immature eagles select patches where the density of hares is particularly high (Bustamante et al., 1997).

Here we evaluate how eagles respond to decreases in the population of the introduced hare, and if this response is similar to that of native predators when their native most important prey decrease in other systems. We hypothesized that the response of a predator before fluctuations of an established alien species will be similar to that shown by native predators and preys that had evolved together. We predict that a decrease in hare abundance will produce different effects on eagle’s population depending on the intensity of the decrease. First, we expect a decrease in the consumption of hares by the eagles when hares are less abundant. Then we expect a numeric response (Rohner, 1996), as follow: 1) as immature eagles are not attached to a territory, we expect a change in age structure of the local population, with less immature when hares are scarce, 2) a decrease in the breeding performance, with lower numbers of pairs attempting to breed and/or an increased nestling mortality, and 3) ultimately, a reduction of the adult abundances with its consequent loss of breeding territories.

2 Methods

3 Results

3.1

3.1 Food habits

In 1991/92 we collected 1097 pellets from 26 territories, in 2006 228 from 12 territories, and in 2011 96 from 9 territories. Hares represented 58.29% of the diet in 1991/92, 51.36% in 2006, and 41.26% in 2011 (Table 1). We were able to collect pellets for all years in the same 9 territories in 1991/92, 2006 and 2011. Therefore, we used those territories to make comparisons between years to avoid biases due to the differences in sampling size. Interaction links between territories and prey items varied over the years, with a reduction of 17% in the consumption of hares between 1991/92 and the formation of new links in 2006 and 2011 with the arrival or increase in numbers of European rabbits (Oryctolagus cuniculus) and the red deer (Cervus elaphus, Fig. 1).

Table 1 Black-chested buzzard-eagle diet in Northwestern Patagonia during the breeding seasons of 1991/92 (26 territories, 1097 pellets), 2006 (12 territories, 228 pellets) and 2011 (nine territories, 96 pellets).

Species	1991/92		2006		2011
	Frequency of appearance	Percentage of pairs	Frequency of appearance	Percentage of pairs	Frequency of appearance	Percentage of pairs
Mammals
Lepus europaeus	58.29	100	51.36	100	41.26	100
Oryctolagus cuniculus	0	0	13.21	38	23.3	22
Rodents	19.16	85	25.85	72	30.3	22
Other mammals	3.36	40	11.46	30	30	33
Birds	16.43	100	31.2	100	35.16	100
Reptiles	1.84	40	1.38	25	1.56	22

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Fig. 1

Trophic interactions of nine territories of black-chested buzzard-eagles during the breeding seasons of 1991/92 (1992), 2006 and 2011. The sizes of boxes represent the percentage of the diet in each year, for every territory. Thickness of interaction lines between each territory and the different prey items represents the strength of each predator prey interaction. The two exotic lagomorphs are in brown boxes.

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3.3

3.3 Relationship between eagle and hare abundance

The abundance of hares decreased over the years, as well as the total abundance of eagles (Table 3). There was a significant decrease of hares as well as immature eagles over the years (Table 3). There was a positive relationship between the abundance of adult eagles and the abundance of hares. This pattern of decreasing abundances over the years is evident when comparing the abundance of eagles and with the abundance of hares (Fig. 1). Overall, the total abundance of eagles decreased over time but this is mainly driven by the decrease in immature eagles (Table 3; Fig. 2). We found no activity in 2011 in the communal roosts found by Hiraldo et al. (1995) and Bustamante et al. (1997) in 1991.

Table 3 Generalized Linear Mixed Models for European hare and black-chested buzzard-eagles abundances over the years. Models tested the effects of the years over hares and eagles abundances, and the effect of hares’ abundance over eagles abundance.

Modeled variable	Fixed effects	Estimate (±S.E.)	p	Random variables
Hare abundance	Year	−0.07 (±0.19)	<0.01	Site
Total eagle abundance	Year	−0.02 (±0.01)	n.s.	Site, hare abundance
Adult eagle abundance		−0.01 (±0.01)	n.s.
Immature eagle abundance		−0.15 (±0.03)	<0.01
Total eagle abundance	Hare abundance	0.13 (±0.05)	0.01	Site, year
Adult eagle abundance		0.11 (±0.06)	0.01
Immature eagle abundance		0.12 (±0.12)	n.s.

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Fig. 2

Abundance of adult and immature black-chested buzzard-eagles, abundance of European hares and number of sites with hares in the years 1992, 2006, 2011 and 2012.

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4 Discussion

We found an apparent reduction in hare consumption by eagles over time suggesting that a functional response may have taken place. This is reflected in a decrease in frequency of occurrence of hares in the diet, but is more evident in the reduction of strength of interaction links in the diets of each territory (Fig. 2). However, in 2006 and 2011, it seems that there was a replacement of hares by rabbits. There was also a sustained consumption of carrion (large mammals that cannot be hunted by the eagle) through time, which was more intense in 2011 possibly as a response to a decrease of their main prey availability. The difference in sample size between the years (especially between 1991/92 and 2011) was a consequence of the lack of pellets in the territories in the later years. The season of 2011 was the one with the lowest abundance of hares we recorded, so it is possible that eagles may have had to move larger distances to forage and therefore pellets were no longer concentrated nearby nests as in 1991/92, when hares were more abundant. The Spanish Imperial eagle (Aquila adalberti) which is considered a specialist in catching rabbits showed a similar response we found with the black-chested Buzzard-eagles, when the RHD affected rabbits in the 80′s (Sánchez et al., 2009).

Paired with the apparent decrease in hare consumption over the years, we found a decrease in the abundance of immature suggesting a numerical response, affecting population age structure. The abundance of immature birds decreased over the years while adults remained constant. Furthermore, in 2011 we visited the places that were used as communal roosts by immature individuals in 1991/92 (Hiraldo et al., 1995), but we found no eagles nor any evidence suggesting any kind of use (i.e. pellets or feathers). This could be because adults took advantage of other exotic alternative preys as rabbit and they scavenge on large mammals. These responses differ from those shown by other raptors which drastically decrease the numbers of adults when their main prey became scare. For instance, around half of the breeding territories of the eagle owl (Bubo bubo) in the Iberian Peninsula where lost in two consecutive seasons when the RHD strongly diminished the abundance of rabbits (Martínez and Zuberogoitia, 2001). However, a generalist species as the black kite (Milvus milvus) had shown similar responses as eagles, since breeding parameters decreased, but not adult density (Viñuela and Veiga, 1992).

Immature and adult eagles differ in their patterns of habitat selection. Immature may have more freedom of movement and can adjust their spatial distribution according to density of their main prey (Bustamante et al., 1997), while adults behave as central place foragers and are attached to their territory. Our results suggest that this pattern maybe evident also at a time scale, with immature present only in periods when hares were abundant. On the other hand adults remained in the area tolerating changes in hare abundance. It seems that adults are more tolerant to a shortage of prey in order to maintain their territory. Non territorial immature could select patches where preys are abundant and abandon these areas. This pattern was found in raptors from the Northern Hemisphere as the great horned owls (Bubo virginianus) in which immature non-territorial members of the population coexist with territorial breeding adults, while the abundance of snowshoe hares (Lepus americanus) was high. When hares abundance decreased, adults remained in their territory while immature abundance decreased (Rohner, 1996).

The decrease in immature abundance could be due to an increase of mortality or because they are moving to areas with more prey. If an increased mortality is the case, the area may be working as an ecological sink in which case recruitment is limited and the population is maintained due to the arrival of individuals from other areas. However, raptors use to move long distances during the natal dispersal period (Penteriani and Delgado, 2009). Eagles reach maturity at 4–5 years of age, therefore they have a long natal dispersal period in which they could move and establish somewhere else. Dispersal of immature individuals may also be a consequence of increased intra-specific competition with adults associated to the shortage of prey (Bustamante and Hiraldo, 1988; Negro et al., 1997). Furthermore, unusual concentrations of dispersal immature individuals have been recorded in areas were nesting activity is low in the center of Argentina, suggesting that individuals born in other areas may travel long distances searching for prey (López et al., 2017). The patterns of dispersal movements of immature remain unknown. In any case it seems that the abundance of their main prey produces changes in the presence and use of the area.

Although there is a slight decrease in territory density and NND, active territories remain abundant in the area with some pairs breeding less than 1000 m from their nearest active neighbors. Therefore, this does not reflect a numerical response at the level of breeding pairs. Such density remains between the highest recorded for this kind of species worldwide (Hiraldo et al., 1995; Barbar et al., 2018). However, we recorded a decrease in breeding performance when hare abundance was the lowest (during the year 2011). According to our hypothesis, this could be indicating that the disturbance caused by the shortage of hares affected breeding success and the abundance of immature individuals, but it was not strong enough to affect neither the abundance of adults nor the density of breeding territories. Alternatively, the disturbance caused by the eruption of the Puyehue-Cordón Cauye volcanic complex during 2011 (Gaitán et al., 2011) may have indirectly affected eagles. Ashes deposition affects plant productivity by accumulation and abrasion by the finest particles. Then herbivores may suffer from starvation, among other impacts (Wilson et al., 2011). This may eventually affect predators and produce a decrease in breeding performance as recorded in 2011. This is reinforced by the fact that in 2012, after some recovery of the eruption impact, breeding performance was higher. However, there is a need of more information to evaluate the effect volcanic ashes deposition may have on eagles.

There are, however, other factors different from hares abundance that may impact eagles population. For instance an unusual aggregation of black-chested buzzard-eagles (mainly immatures), possibly associated with fluctuation in prey abundance in central Argentina (López et al., 2017), may have favored recent events of large mortalities due to electrocution in that area, which show that those eagles are highly susceptible to this disturbance (Sarasola and Zanon Marínez, 2017). Electrocution in our study area could also have an impact on eagles, and more data in this regard is needed. However, even though we did not perform any systematic surveys under electric pools, neither new electric lines nor unusual congregation of eagles have been recorded in the study area. During our study period we only found one juvenile eagle dead under an electric line. This was one of two fledges that had recently left the nest constructed in a concrete made electric pool Therefore we have no evidence suggesting that electrocution as recorded by Sarasola and Zanon Marínez (2017) could be the explanation for our numerical response in juvenile eagles, although this subject merit special attention and specific studies.

Persecution by humans is another factor that may have a negative impact on eagles and could also be an alternative explanation to our findings. However, the fact that adult abundance and NND did not vary over the years suggests that if there is persecution towards this species it is mainly affecting immature individuals. This has been reported for similar species in other regions of Argentina (i.e. Sarasola and Maceda, 2006; Barbar et al., 2016a,b). We cannot discard this alternative hypothesis, however owners of two of the most extensive properties in the study area, were several of the count points and active nests were surveyed, claim that there is no persecution to this species in their land.

The European hare altered the community in South America since its arrival by being an abundant food resource for many predators and a competitor for native herbivores (Grigera and Rapoport, 1983; Novaro et al., 2000; Barbar et al., 2018; Barbar and Lambertucci, 2018, 2019). In our study system hares had temporal and spatial fluctuations including important local decreases. Eagles seem to have responded by adjusting the diet and changing the proportion of age classes, with adults remaining in the area and immature decreasing in abundance. Further studies on the effect of exotic European hares on the demography of their consumers should be carried out since our results suggest that their fluctuations may produce numerical responses in a top predator population.

Conflict of interest

The authors declared that there is no conflict of interest.