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Ethology Ecology & Evolution
ISSN: 0394-9370 (Print) 1828-7131 (Online) Journal homepage: https://www.tandfonline.com/loi/teee20
Hunting lactating female ungulates deserves
caution: the case of the chamois
Luca Corlatti, Francesco Ferretti & Sandro Lovari
To cite this article: Luca Corlatti, Francesco Ferretti & Sandro Lovari (2019) Hunting lactating
female ungulates deserves caution: the case of the chamois, Ethology Ecology & Evolution, 31:3,
293-299, DOI: 10.1080/03949370.2018.1561526
To link to this article: https://doi.org/10.1080/03949370.2018.1561526
Published online: 26 Feb 2019.
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For u m
Hunting lactating female ungulatesdeservescaution:thecaseofthe
The Northern chamois R. rupicapra is one of the most abundant mountain-
dwelling ungulates in Europe and the Near East (Corlatti et al. 2011) and an iconic
symbol of mountain hunting. Despite its overall abundance, some populations of the
Alpine subspecies R. r. rupicapra lately showed a decreasing trend and other subspe-
cies are threatened (Corlatti et al. 2011). As hunting pressure is one of the major
drivers of population dynamics in game species, understanding the potential demo-
graphic consequences of different harvesting regimes is pivotal to ensure sustainable
wildlife management. In a paper on chamois population dynamics, Rughetti and
Festa-Bianchet (2014) adopted an individual-based modelling approach to explore
the consequences of different hunting regimes on several demographic parameters.
The theoretical rationale of this work is based on the potential demographic conse-
quences of hunting regulations and/or hunter preferences that, in many large mam-
mals, currently discourage harvesting of lactating females (Solberg et al. 2000; Bischof
et al. 2009; Mysterud 2011). In turn, this may cause a selective pressure on subadult,
non-lactating females (Rughetti & Festa-Bianchet 2011b) who may enjoy high natural
survival and high lifetime reproductive potential. It is thus suspected that removing
a relatively greater proportion of these young females could possibly lead to a severe
impact on population dynamics. Using varying levels of hunting pressure and of
relative survival probability of orphan vs non-orphan kids (0.5; 1), the authors mod-
elled the theoretical long-term effects of random hunting (i.e. harvesting of yearlings
and ≥2 years old females, irrespective of their reproductive status) and those of
selective hunting (i.e. harvesting of yearlings and ≥2 years old non-lactating females)
on chamois population size at equilibrium, age structure, hunting mortality of differ-
ent age classes and recruitment. The key result of this analysis is that “depending on
the effects of orphaning on juvenile survival, selective harvest may either increase or
decrease population growth rate compared to random harvest”(Rughetti & Festa-
Bianchet 2014). In the final part of the paper, the authors suggest that removing the
penalty of hunting lactating females “would have no effect on chamois population
dynamics, while leaving hunters with the opportunity to select a non-lactating female
if they wish”(Rughetti & Festa-Bianchet 2014). While we agree that that more infor-
mation on the effects of orphaning on juvenile survival is needed to elucidate the best
hunting strategy, in this article we argue that several other uncertainties should be
accounted for in future agent-based models, thus in the decision-making process, to
obtain generalizable recommendations.
Ethology Ecology & Evolution, 2019
Vol. 31, No. 3, 293–299, https://doi.org/10.1080/03949370.2018.1561526
© 2019 Dipartimento di Biologia, Università di Firenze, Italia
Uncertainties on short- and long-term consequences of orphaning
Data on the effects of orphaning on survival of chamois offspring are missing
(Rughetti & Festa-Bianchet 2014). Furthermore, as far as ungulates are concerned,
available information is scanty and contradictory (Festa-Bianchet et al. 1994; Andres
et al. 2013; see other references in Rughetti & Festa-Bianchet 2014). Understandably,
the authors decided to run a sensitivity analysis assuming two values for relative
survival probability of orphaned kids to test for the “best”and the “worst”scenario:
(i) equal survival between orphans and non-orphans, (ii) orphan survival is 50% of
Early growth and/or survival of offspring could be influenced by the condi-
tion of their mothers and the amount of maternal care (e.g. Clutton-Brock et al.
1984,1986; Festa-Bianchet 1988;Côté&Festa-Bianchet2001a). In turn, the
removal of mothers during the nursing period is likely to affect early growth,
hence survival of offspring. Thus, we may expect that the time of hunting will
play an important role in shaping survival probability of orphans. The analysis of
Rughetti and Festa-Bianchet (2014) does not explicitly state the time of hunting,
although it is likely assumed to occur in Autumn. However, chamois hunting
seasons vary greatly across regions and hunting districts, ranging between early
August and late February (Apollonio et al. 2011;Damm&Franco2014). Even if
we assume that offspring losing their mother near or after weaning might not
suffer increased mortality (Festa-Bianchet et al. 1994;butseeAndresetal.2013
and paragraphs above), consequences could be comparatively heavier for those
losing their mother over the summer. In turn, summer orphaning may greatly
impact on chamois kid survival, as long as some regulations allow hunting to
occur well within the period of intensive maternal care (i.e. until mid
September-early October, for chamois, Ruckstuhl & Ingold 1994; Scornavacca
et al. 2016,2018). Whether the currently used bounds 0–50% of orphan survival
are valid in these circumstances still has to be clarified: in mountain goats
Oreamnos americanus, for example, only one out of eight kids who lost their
mother during summer survived to 1 year of age (Côté & Festa-Bianchet 2001b).
If so, future agent-based models ought tousedifferentboundstomodelorphan
survival probabilities depending on the period of hunting.
Furthermore, in chamois, offspring stay with their mothers well after wean-
ing, until about 1 year of age. Beside lactation, juveniles benefit from bonding
with mothers by increasing protection against predators, defence from aggression
by conspecifics, social cohesion in herds, and by learning patterns of habitat use,
movements and food selection (e.g. Clutton-Brock et al. 1982; Green et al. 1989;
Andres et al. 2013). Ruckstuhl and Ingold (1999)foundthatinchamois–after
suckling frequency declined over summer –the mother-kid bond remained strong,
possibly to favour the synchronisation of activities (cf. Romeo & Lovari 1996,for
mountain goats). Thus, the consequences of maternal loss are unlikely to be
related solely to the cessation of milk supply, when orphaning will likely foster
an increase of kid vulnerability to starvation and/or predation (Apollonio et al.
Orphaning, however, may not only exert short-term effects but also far less
predictable long-term effects not included in the model. In mammals, conditions
experienced early in life influence conditions in adulthood (e.g. Lindström 1999;
Lummaa & Clutton-Brock 2002; Douhard et al. 2013) and affect life-history traits
such as individual reproductive success (e.g. Clutton-Brock et al. 1984,1986).
Although information on the long-term effects of orphaning are scarcer than those
available on short-term impacts, Festa-Bianchet et al. (1994) and Andres et al. (2013)
showed that, in males, body and horn/antler growth could be reduced. In some
species, these traits correlate directly or indirectly with male reproductive success
(Geist 1971; Clutton-Brock et al. 1982; Festa-Bianchet et al. 2000). Furthermore,
orphaning may exert negative effects in terms of stress response, reduced maternal
behaviour or augmentation of fear and aggression (for a review, see Apollonio et al.
2011). Rughetti and Festa-Bianchet (2014) mentioned potential long-term conse-
quences of orphaning on phenotypic quality (i.e. body mass and weapon growth)
and reproductive success of offspring. While we acknowledge the difficulty of incor-
porating such information in agent-based models, these potential effects on long-term
population dynamics are likely to increase model uncertainty.
What is a senescent chamois?
Rughetti and Festa-Bianchet (2014) assumed the occurrence of senescence in
females ≥9 years of age, yet large variations occur in the pattern of senescence in
chamois populations. From a reproductive point of view, breeding success in the Swiss
Alps declined only in females older than 16 years (Tettamanti et al. 2015). From
a survival point of view, Loison et al. (1994) did not find any significant decrease of
survival rate in Alpine chamois females until 13.5 years of age, whilst in different areas
of the Alps the onset of senescence may occur as early as 7 years or much later, at
about 12 years of age (Bleu et al. 2015). For example, Corlatti et al. (2012), for
a protected stable population of Alpine chamois, found out that females ≥8 years of
age enjoyed a survival rate of 0.92, much greater than the 0.70 value assumed by
Rughetti and Festa-Bianchet (2014). The effects of variation in female senescence
should thus be accounted for in future agent-based models.
Does a typical chamois hunting regime exist?
Although Rughetti and Festa-Bianchet (2014) assumed that the typical hunting
regulation implies separate harvest rates for adult and yearling females, harvesting of
yearlings and of ≥2 years old females is far from being the typical chamois hunting
system. Over the distribution range of this ungulate one can find quite a variety of
management regimes (Damm & Franco 2014). In parts of Italy, for instance, females
are grouped into four (1, 2–3, 4–10 and ≥11 years old) or three (1, 2–3, ≥4 years old)
age classes, whereas in Austria females are grouped into three age classes (1–3, 4–9, ≥
10 years of age) (Damm & Franco 2014). Moreover, despite the authors’assumption
that the absence of kid harvesting is typical of most hunted populations, hunting of
kids occurs in many chamois populations over the Alpine arch, e.g. in Austria and
Germany (that alone accounts for some 38% of the total Alpine chamois hunting bag
in Europe: Damm & Franco 2014), in Switzerland (Damm & Franco 2014) and in
France (Garel et al. 2009). This variability needs to be accounted for when evaluating
the performance of random vs selective harvesting. For example, it could be expected
that in hunting regimes in which fixed hunting quotas are assigned to more than two
female age-classes there would be less opportunity for overharvesting young and
productive females, while in hunting regimes where kids are allowed to be shot, the
removal of penalty for hunting lactating females and consequent kid orphaning could
possibly exert an over-impact on kid survival.
Random harvest…or not?
Given the very limited sexual dimorphism of chamois, especially before and after
the rutting season, in November (when males weigh 30–40% more than females; Garel
et al. 2009; Rughetti & Festa-Bianchet 2011a), if hunters are left with the choice to
hunt either lactating or non-lactating females, they may over-impact on females with
kids, to avoid the risk of culling males by error. This bias was anecdotally reported by
Italian hunters (i.e. in some districts of the Province of Brescia, where there are no
restrictions on lactating females). Furthermore, Corlatti et al. (2017) recently showed
that while in hunting regimes with restrictions on lactating females there is no selec-
tion for female trophies, in hunting regimes with no restrictions on lactation status
female chamois can become a target for trophy hunters –i.e. there is a strong negative
relationship between early horn growth and survival. This, in turn may have important
consequences for the dynamics of populations: as a matter of fact, female chamois
with rapid horn growth as yearlings reproduce earlier, and early horn growth proved
a reliable index of reproductive potential in young and senescent female chamois
(Rughetti & Festa-Bianchet 2011b). More generally, early primiparity positively associ-
ates with larger body mass, longer life expectancy and greater fitness in ungulates (cf.
Rughetti & Festa-Bianchet 2011b). By removing the penalty for hunting lactating
females, trophy hunters may thus preferentially remove long-horned, early primipar-
ous females at an early age, possibly making the random harvest, de facto, a non-
random regime targeted towards the most productive segment of the population. This
effect might be exacerbated by the occurrence of individual heterogeneity in female
reproductive performance (i.e. successful females chamois tend to be consistently
better than the unsuccessful ones in subsequent reproductive events; Tettamanti
et al. 2015). The level of individual heterogeneity may indeed play a major role when
evaluating the demographic consequences of different hunting regimes (i.e. negative
effects are most likely to occur when a random harvest regime is adopted in the
presence of strong individual heterogeneity) (Rughetti et al. 2017), and thus needs to
be accounted for in future agent-based models.
Agent-based models can be useful tools for preliminary evaluation of potential
effects of different options within the framework of adaptive management of wildlife
populations. The work of Rughetti and Festa-Bianchet (2014) represents a first
attempt to apply this approach to chamois. However, “uncertainty is pervasive in
ecological systems, and multiple types of uncertainty”such as stochastic variability,
sampling imprecision, observation errors and model errors may “affect the accuracy
and precision of modelling outputs”(Hoshino et al. 2014). Some real systems may be
irreducibly complex and, although they can still be treated by agent-based models, the
outcome may have fundamental limitations and, possibly, restricted range of validity
(Helbing 2012). We have argued that the model proposed by Rughetti and Festa-
Bianchet (2014) does not capture the great spatial heterogeneity in chamois life history
traits, variety of hunting regimes, and the potential selective consequences of random
female harvest. Consequently, we believe that the authors’suggestion that removing
the penalty for hunting lactating females, assuming kid orphaning “would have no
effect on chamois population dynamics, while leaving hunters with the opportunity to
select a non-lactating female if they wish”(Rughetti & Festa-Bianchet 2014) might
have local value, but deserves great caution if the readers wish to apply that to other
chamois populations. Further uncertainty components in the model parametrization
need to be carefully evaluated, to avoid misleading management recommendations.
Among the others: (i) the potential long-term effects on phenotypic quality and repro-
ductive success of orphans, (ii) the local variation of chamois hunting season, which is
likely to influence survival of orphans, (iii) the great variability of chamois hunting
regimes throughout the species’distribution range, (iv) the local variations in the
assumed senescence in chamois and (v) the potential demographic consequences of
trophy hunting when no restrictions on lactating females is imposed.
Agent-based models may be useful tools for the adaptive management of wildlife
populations: first steps have been taken towards the application of this approach to
chamois management by investigating the potential outcomes of different harvesting
regimes. Future modelling attempts should account for the diversity of hunting
regimes and for their interconnections with chamois life history traits, to obtain
more general and reliable insights into the long-term demographic consequences of
different chamois management options. Given the current uncertainties, we strongly
caution against the adoption of a hunting regime which includes kid orphaning, and
suggest that selective harvesting combined with the adoption of hunting quotas for
different female age classes may effectively reduce the pressure on young females with
high reproductive value, while avoiding the negative effects of trophy hunting and all
the uncertainties –ethical issues included –of orphaning.
No potential conflict of interest was reported by the authors.
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University of Natural Resources and Life Sciences Vienna, Gregor-Mendel Strasse 33,
A-1180 Vienna, Austria.
Research Unit of Behavioural Ecology, Ethology and Wildlife Management,
Department of Life Sciences, University of Siena, Via P.A. Mattioli 4, 53100 Siena,
Research Unit of Behavioural Ecology, Ethology and Wildlife Management,
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Italy. and Maremma Natural History Musem, Strada Corsini 5, 58100 Grosseto, Italy