Introduction
The Anthropocene is characterized by an unprecedented rate of
biodiversity loss driven by a number of anthropogenic stressors
including climate change, pollution, habitat loss, overexploitation and
the transmission of invasive species (Young et al. 2016). As populations
decline in the face of these stressors the need for conservation
intervention becomes increasingly important. However, conserving small
populations is complicated as declining population size increases the
risk of detrimental demographic processes driving populations inexorably
towards extinction (Fagan & Holmes 2006). For example, individual
fitness in many species is expected to decrease with population size due
to Allee effects (Berec et al. 2007) and a loss of genetic diversity
(Saccheri et al. 1998; Blomqvist et al. 2010); demographic stochasticity
influences small populations by increasing the annual variability in
population growth rate (Fagan & Holmes 2006), which is particularly
problematic in small populations as major fluctuations could lead to
their extinction (Gilpin & Soulé 1986; Caughley 1994); moreover, small
populations are also especially vulnerable to direct extirpation from
external drivers of mortality, such as environmental stochasticity and
random catastrophes (Caughley 1994). The concurrent presence of these
processes is thought to lead to self-reinforcing, rapid and catastrophic
downward spirals to extinction, so-called ‘extinction vortices’ (Gilpin
& Soulé 1986), during which there may be little prospect of the
population recovering even with intense conservation effort (Palomares
et al. 2012). To identify the populations most at-risk and to make
informed conservation decisions, we need to understand the factors that
determine the robustness of a population to extirpation by the
extinction vortex.
Fagan and Holmes (2006) empirically corroborated, albeit with a small
database of population extirpations, several preexisting hypotheses of
the extinction vortex; specifically, that (i) time to extinction scales
to the logarithm of population size, indicating that as a population
declines its time to extinction decreases at an increasing rate, (ii)
geometric growth rate declines as extinction nears, due to declining
individual fitness and (iii) annual variability in population change
increases as extinction nears, attributable to an increasing influence
of stochastic factors.
A species’ intrinsic and ecological traits are often key predictors of
extinction risk (Gaston & Blackburn 1995; Purvis et al. 2000; Cardillo
et al. 2008), with geographic range size, life-history speed, and degree
of specialization emerging as persistent indicators (Chichorro et al.
2019). However, with few exceptions (Duncan & Young 2000; Brashares
2003; Koh et al. 2004), real-life extinctions have rarely been used to
infer extinction proneness in relation to biological traits (Brook et
al. 2008). Similarly, using a lab-based experiment, Godwin et al. (2020)
were the first to explicitly investigate how variation in a specific
behavioral trait (mating pattern) can result in differential population
vulnerability to the extinction vortex; though analogous studies have
not been carried out on real-life population data.
Unfortunately, many of the traits identified as important predictors of
extinction risk are difficult to measure, particularly in populations
which are already severely reduced, meaning that it is necessary to use
proxy measures of these intrinsic ecological traits. Body size is a
particularly important trait, associated with a suite of intrinsic,
ecological and anthropogenic factors that are frequently invoked in
studies relating to extinction risk such as life-history speed (Johnson
2002), population density (Fa & Purvis 1997; Davidson et al. 2009), and
the level of exploitation by humans (Owens & Bennett 2000; Ripple et
al. 2016, 2019). Furthermore, because of the ease of obtaining body size
data and the significance of body size as a correlate of many
hard-to-record population traits, it is arguably the most readily
available trait available among taxa. This enhances the potential
utility in predicting how small populations will respond without having
to obtain more cryptic information with time-consuming and expensive
data-collection procedures.
Smaller-bodied species are generally more fecund with greater intrinsic
rates of growth, meaning they can recover from perturbations more
quickly (Brook & Bowman 2005) and spend less time at small population
sizes where there is a large threat of extirpation (Allen et al. 2017).
However, slower life history speed in larger-bodied species is linked to
greater resistance to both environmental (Millar & Hickling 1990;
Peltonen & Hanski 1991; Sinclair 2003; Saether et al. 2013; Yeakelet al . 2018) and demographic (Jeppsson & Forslund 2012; Saether
et al. 2013) stochasticity. Greater susceptibility to stochastic
processes implies that populations of smaller-bodied species can be
abruptly reduced to a point where the risk of extinction is acutely high
(Schoener et al. 2003; Allen et al. 2017). The relationship between body
size and robustness against the extinction vortex thus depends on the
relative importance of population growth rate versus susceptibility to
stochastic elements.
Here, we assess – for the first time – whether body size can interact
with underlying demographic processes to influence the dynamics of a
population in the region of an extinction event, building upon the
analysis of Fagan and Holmes (2006) but with a much larger database. To
do this requires cases of populations monitored through to extirpation,
negating the need to designate quasi-extinction thresholds, which could
result in erroneous interpretations of extinction dynamics (Fagan &
Holmes 2006). We use a global database of vertebrate population time
series, supplemented with body size data from various life history
databases to identify 55 populations where extirpation has been
observed. We find support for the three aforementioned predictions of
the extinction vortex (Gilpin & Soule 1986; Fagan & Holmes 2006) and
evidence that deterioration in population dynamics, due to the
extinction vortex, takes place at a faster rate in smaller-bodied
species.