Discussion
This experimental study investigated the effect of food availability on
the intensity of the anti-predator behaviour of breeding red kites.
Under experimentally enhanced food conditions, the intensity of
anti-predator behaviour was higher in red kite parents with old broods
than with young broods. This age-dependence disappeared in the
un-supplemented control group, where anti-predator behaviour was
constant over the entire nestling period. These results support the
previous theoretical prediction of Dale et al.
(1996)
that the “reproductive value of offspring” hypothesis has greater
relevance under favourable breeding conditions, while the
“harm-to-offspring” hypothesis becomes more relevant under poor
breeding conditions. These results suggest that food availability
affects parental anti-predator behaviour by changing the nestlings’ body
condition which represents a new pathway of how food conditions drive
parental investment.
Under a wide range of food conditions, food supplementation to parents
might mainly affect parental condition rather than vulnerability of the
brood
(Boutin
1990; Michel et al. 2022; Ruffino et al. 2014). However, in recent
studies we showed that enhanced food conditions due to our experimental
food supplementation increased nest and nestling survival, as well as
body condition of nestlings compared to control broods
(Catitti
et al. 2022; Nägeli et al. 2022). This confirms that food
supplementation reduces the harm that offspring suffer due to a period
of parental absence by increasing their baseline body condition – and
probably also increases the reproductive value of the brood due to
increased post-fledging survival probability of nestlings
(Naef-Daenzer
and Grüebler 2016).
The greater relevance of the “harm-to-offspring” hypothesis under
normal than enhanced food conditions suggests that also large species,
such as the red kite, can be affected by predator presence in the nest
area. Field observations during predator exposure trials support that,
even if mobbing intensity is low, red kite parents invest time in
supervising their brood and the predator; time that could otherwise be
spent in food provisioning
(Ghalambor
et al. 2013; Ibáñez-Álamo et al. 2015; Martin and Briskie 2009; Mutzel
et al. 2013). In this respect, parents of nestlings that are susceptible
to predation are faced with a trade-off between time invested in nest
guarding and time invested in foraging
(e.g.
Komdeur 1999; Rothenbach and Kelly 2012). The outcome of this trade-off
likely represents the underlying mechanism of adjustments in mobbing
intensity. During food shortages, when nestlings have more urgent food
requirements and are more susceptible to harm from starvation or
developmental stress
(see
Catitti et al. 2023), chasing away predators should expedite the return
to foraging. On the other hand, during favourable food conditions,
breeding pairs can spend more time passively guarding the nest and,
thus, can save energy and avoid risking themselves during active mobbing
behaviour. This might be true for bird species where nest guarding and
attendance can be efficient anti-predator strategies
(Catry
et al. 2006; Dewey and Kennedy 2001; Hu et al. 2017; Rothenbach and
Kelly 2012; Samelius and Alisauskas 2001). We suggest that nest guarding
and mobbing represent two different nest defence strategies that both
reduce nest predation
(Caro
2005; Montgomerie and Weatherhead 1988), but their cost-benefit ratio
changes with food availability and vulnerability of the brood.
As the two hypotheses show contrasting predictions for the effect of
nestling age on mobbing behaviour, we used nestling age to investigate
the relevance of the two hypotheses under different food conditions.
However, also brood size showed a clear effect on mobbing behaviour.
While the “harm-to-offspring” hypothesis does not give a clear
prediction regarding brood size, the “reproductive value of offspring”
hypothesis does
(Montgomerie
and Weatherhead 1988) and is supported by increased mobbing intensity in
parents with large versus small broods. We recently showed that large
brood sizes were associated with reduced body mass and increased
corticosterone levels in red kite nestlings
(Catitti
et al. 2022; Nägeli et al. 2022), illustrating the general life-history
trade-off between offspring number and offspring quality
(Stearns
1992). Since it is the body condition of the nestlings that is expected
to affect parental mobbing behaviour under the “harm-to-offspring”
hypothesis
(Dale
et al. 1996), these results suggest both, increased harm to offspring,
as well as increased reproductive value in large broods. Thus, increased
anti-predator investment into large broods suggests that the
reproductive value of an additional nestling is larger than the
increased costs of reduced body condition arising in a period of absence
no parental care. This might be a general pattern as increased parental
care investment into large broods, including anti-predator investment,
has been shown in many studies
(Clutton-Brock
1991; Lazarus and Inglis 1986; Royle et al. 2012).
Quantifying time-to-detection was important in this study because
differential detection could bias the investigation of capture
probability, which was used as proxy for mobbing intensity. Predator
detection time is not only a methodological issue, but is also likely
associated with nest predation risk, should low detection probability be
due to parental absence from the nest area
(Behrens
et al. 2019; Duncan Rastogi et al. 2006; Samelius and Alisauskas 2001;
Schmidt and Whelan 2005). Under poor natural food conditions, parents
detected the decoy predator later than under favourable food conditions
probably due to longer foraging trips. Supplementary feeding resulted in
earlier detection under poor natural food conditions, but later
detection under favourable food conditions. In addition, parents with
large broods detected the decoy predator earlier than parents with small
broods indicating a higher nest visitation rate. These results are in
line with recent studies showing that, in years with low food
availability, the home-range size of red kite pairs is considerably
larger than in years with high food availability
(Pfeiffer
and Meyburg 2015), and that prey delivery rate is elevated in large
versus small broods
(Andereggen
2020), but can be reduced under ad libitum food conditions.
Together, these results indicate that time-to-detection depends on
factors affecting movement behaviour within home-ranges and corroborates
that nest predation risk by avian predators can be increased in pairs
with large home-ranges
(Lameris
et al. 2018), in situations of low food availability
(Duncan
Rastogi et al. 2006), and in pairs with small brood-sizes
(Schmidt
1999), all being consequences of low habitat quality.
Finally, weather conditions during the predator exposure trial affected
time-to-detection probability, as well as time-to-capture. This was
expected for time-to-detection, because weather conditions are shown to
affect ranging behaviour
(Baucks
2018) and food delivery rates
(Andereggen
2020). However, while we added
weather variables mainly to account for potential biases in the analysis
of time-to-capture, our study is one of the very few showing that
weather conditions affect mobbing intensity
(but
see Fisher et al. 2004). Mobbing intensity strongly decreased i.e.
time-to-capture increased with high ambient temperatures and windy
conditions. When ambient temperatures are outside their thermal neutral
zone, birds face additional energy costs during activities, which could
affect their decisions regarding nest defence
(Fisher
et al. 2004). Also, windy conditions can affect control of swoops and,
thus, increase injury and predation risk of parent birds. This is also
supported by the fact that time-to-capture was increased when the
predator was placed closer to trees, impeding manoeuvrability. Both
underlying mechanisms, energetic trade-offs and increased threat of
injury, might be particularly relevant in large bird species exhibiting
predominantly soaring flight, such as red kites, where flapping flight
is energetically costly, and manoeuvrability limited
(Sapir
et al. 2010; Shepard et al. 2013; Shepard et al. 2016; Shepard et al.
2019).
In conclusion, we show that nest defence depends not only on predation
risk due to predator type and behaviour, but also on environmental
conditions. While, in general, parental anti-predator investment seems
to be adjusted to the reproductive value of the brood, this investment
is modulated by a multitude of factors associated with the brood, the
environment, and the approaching predator. In particular, this study
provides evidence that food availability affects anti-predator behaviour
by altering the body condition of nestlings. The vulnerability of the
offspring is therefore important for the choice of the nest defence
strategy. It represents a driver of mobbing intensity and is important
for the outcome of trade-offs between different forms of parental care.
Thus, low food availability might have mobbing-mediated consequences for
reproduction and reproductive costs beyond the consequences mediated
through changes in foraging behaviour, even if predation rate remains
unchanged. In addition to potential survival costs for the parents, the
additional parental effort due to frequent mobbing may even be a reason
for brood desertion under poor environmental conditions
(see
Nägeli et al. 2022). Ultimately, large-scale environmental factors
affecting investment into nest defence may have significant demographic
consequences.