8.7: Problems of Small Populations
While some small populations have persisted against the odds, sufficiently large populations are generally needed to prevent eventual extinction (Halley et al., 2016, see also Section 9.2). Small populations—which include species that have always had small populations and previously large populations that have been reduced to a few individuals—face three additional inherent and unavoidable pressures beyond the threats discussed in Chapters 5–7. These three additional pressures are: (1) loss of genetic diversity; (2) demographic stochasticity; and (3) environmental stochasticity and natural catastrophes. We will now examine how each of these pressures can lead a small population to eventual extinction. Much of this discussion is based on a ground-breaking manuscript by New Zealand ecologist Graeme Caughley, which discusses at length the threats faced by small and declining wildlife populations (Caughley, 1994).
Loss of genetic diversity
Small populations are at risk of losing genetic variation much faster than large populations.
Species with high genetic diversity are generally more able to adapt to and reproduce under new conditions such as those brought by environmental changes (Section 3.2). These adaptations can occur at both individual and population levels. For example, under climate change, some genes may allow some populations to adapt their ranges faster or better tolerate warmer and wetter environments, while phenotypic plasticity —the ability of one gene to express itself differently under different conditions—may allow certain individuals to better adapt to a changing environment. One species that displays remarkable phenotypic plasticity is the crystalline iceplant (Mesembryanthemum crystallinum); by regulating its photosynthetic pathways, an individual plant can adjust its water needs based on the amount of salt and moisture available in the environment (Tallman et al., 1997). Such flexibility may explain why this species, native to southwestern Africa, North Africa, and Europe, has been a successful invader in environments as diverse as those in South America, North America, and Australia.
While populations with many individuals usually also have high levels of genetic diversity, small populations regularly suffer from low levels of genetic diversity. This low genetic diversity not only leaves those populations unable to adapt to changing conditions, but also makes them more susceptible to a variety of deleterious genetic effects (Caughley, 1994). Each of these effects leads to even greater loss of fitness and genetic diversity, hence even larger population declines, and eventually extinction. In the next sections, we discuss further why these deleterious genetic effects are so harmful to small populations.
Genetic drift
In wildlife populations, there are always some alleles that are relatively common, and others that are relatively rare. The relative abundance of any of these alleles may however change from one generation to another purely by chance. While common alleles generally tend to stay common, rare alleles have a high chance of being randomly lost in subsequent generations. Consider how each parent only passes on half of their genetic code to each offspring; this means that the ability of a rare allele to persist is dependent on how many individuals carry it, which individuals produce offspring, and how many offspring those individuals produce. Another important factor is population size (Figure 8.8): in any small population, only a limited number of individuals can carry any single allele, so the smaller the population, the higher the likelihood that alleles are lost to the next generation. This loss of alleles is called genetic drift.
While genetic drift equates to a loss of genetic diversity, there are some cases where populations show no obvious ill effects. Such may have been the case for female elephants in South Africa’s Addo Elephant National Park. Hunting once nearly killed off this entire population; by the time they were adequately protected in 1931, only 11 animals remained, eight of which were female. Of those eight females, at least four were tuskless, while only two, maybe three, females carried both tusks. Over the next decades, Addo’s female elephants have shown increasing degrees of tusklessness; by 2002, only 2% of females had tusks (by comparison, 96–98% of elephant females are normally expected to develop tusks, Maron, 2018). One can therefore postulate that the allele responsible for the tusk development in female elephants became rare, and that the progressive loss of tusked females is a sign of genetic drift (Whitehouse, 2002). While Addo’s female elephants do not show any known limitations from being tuskless, the loss of alleles can also be devastating to the population suffering from genetic drift if, for example, the lost allele(s) coded for traits that would have allowed a species to adapt to a changing environmental condition.
It is important to note that genetic drift is distinct from natural selection. That is, genetic drift involves random changes in the frequency of alleles, whereas natural selection involves changes in traits in response to sexual selection or specific environmental conditions. For example, reduced tusk size in some heavily-hunted elephants in Africa (e.g. Chiyo et al., 2015) is a selective pressure in response to hunting that favour large tusks—this is distinct from Addo’s female elephants that have lost their tusks even in the absence of selective hunting pressure.
Mating among closely related individuals, which occurs in small populations, often results in lower reproductive success and weaker offspring.
Inbreeding depression
In large populations, a variety of instinctive mechanisms are in place to promote heterosis, which occur when offspring have a level of genetic variation that improves their individual evolutionary fitness. Some species are predisposed to disperse from their place of birth to prevent sibling–sibling or parent–offspring mating, while others are restrained from mating with close relatives through sensory cues such as individual odours. Many plants have morphological and physiological traits that facilitate cross-pollination and reduce self-pollination.
However, in small populations with few unrelated mates, the urge to breed might be stronger than the mechanisms that promote heterosis. Under these conditions, rather than forgoing reproduction, breeding among closely-related individuals (or inbreeding) can occur. This breeding among close relatives might result in inbreeding depression, which can occur when closely-related parents give their offspring two copies of a deleterious allele. Individuals suffering from inbreeding depression typically have fewer offspring or have offspring that are weak or fail to reproduce. Such is the case for some mountain gorillas (Gorilla beringei beringei, EN): genetic studies have shown how birth defects in several small populations can be attributed to inbreeding depression (Xue et al., 2015). Inbreeding depression has also been identified as the reason why some small lion populations are more susceptible to diseases (Trinkel et al., 2011). Inbreeding depression can result in a vicious cycle for declining population sizes, where such declines can lead to even more inbreeding depression, and eventually extinction (see Section 8.7.4).
Outbreeding depression
Large populations have many ecological, behavioral, and physiological mechanisms that prevent hybridisation, the production of offspring among genetically distant taxa, whether they be individuals of different species, or individuals of the same species but with different adaptations (the latter being intraspecific hybridisation). As with inbreeding depression, these mechanisms may fail in small populations, leading to outbreeding depression (Frankham et al., 2011). Because offspring that result from outbreeding depression have traits that are intermediate to their parents, they may not be adapted to either of the parents’ ecosystems. For example, one study found that plants suffering from outbreeding depression have weakened defences against herbivory (Leimu and Fischer, 2010). Outbreeding depression may also lead to a breakdown in physiological and biochemical compatibility between would-be parents—hybrid sterility is a well-known consequence of this breakdown. Consequently, species and populations suffering from outbreeding depression often show similar symptoms to inbreeding depression, including lower fitness, weakness, and high rates of mortality.
The opposite of outbreeding depression is hybrid vigour. Under these conditions, the hybrid offspring can be quite strong in an evolutionary sense; they may even outcompete their parent species. Such is the case with the South African endemic black wildebeest (Connochaetes gnou, LC); having recovered from near-extinction, poorly planned translocations are now threatening this species, which readily hybridises with the widespread common wildebeest (Connochaetes taurinus, LC) in areas of contact (Grobler et al., 2011).
Population bottlenecks
In some taxa, such as butterflies, annual plants, and amphibians, population size varies dramatically from generation to generation. During some years, populations can be so large that they appear to face little risk of extinction. However, abundant years can be misleading when followed by successive years of low abundance. Generally, in a population that undergoes extreme size fluctuations, the population size required to ensure continued persistence (i.e., the minimum viable population (MVP), Section 9.2) is in effect much nearer the lowest than the highest number of individuals in any given year. However, during years with low abundance, a phenomenon known as a population bottleneck may occur—that is, the small population size may lead to the loss of rare alleles from one generation to the next. Population bottlenecks may lead to more inbreeding depression which, in turn, reduces reproductive success (Heber and Briskie, 2010) and increases vulnerability to diseases (Dalton et al., 2016). Low genetic diversity in great white sharks (Carcharodon carcharias, VU) living in South Africa’s Indian Ocean is thought to be the result of a population bottleneck (Andreotti et al., 2015).
Populations founded by only a few individuals by definition start off with low genetic diversity, having lasting effects in the population through time.
New populations founded by only a few individuals are vulnerable to a special type of population bottleneck, the founder effect. The founding individuals of a new population by definition start off with low genetic diversity, much less than the original population that the founders left behind. This low genetic diversity puts the new population at risk of further genetic diversity declines, which have lasting effects through time. This situation can occur naturally when only a small number of individuals disperse to establish a new population or when founder individuals come from a small population that already suffered from low genetic diversity. Being mindful of these concerns is especially important for translocation (Section 11.2) or captive breeding (Section 11.5) projects. For example, to prevent extinction of the world’s smallest gazelle, the Speke’s gazelle (Gazella spekei, EN), a captive population of this species, almost entirely restricted to Somalia, was established in the USA. The founder population for this captive breeding project consisted of only one male and three females, leading to severe levels of inbreeding depression and high mortality rates in offspring (Kalinowski et al., 2000). Understanding the importance of managing for genetic diversity can help avoid these and other challenges that can threaten the success of translocation projects.
Demographic stochasticity
Demographic stochasticity (also known as demographic variation) refers to random variations in a population’s demographic traits (e.g. sex ratios, birth rates, death rates), the cumulative effect of variation in individual organisms’ fitness. In any natural population, some individuals will produce fewer offspring than average, while others will produce more than average; some individuals will produce no offspring at all. Similarly, some individuals die younger than average, while others live longer than average. For populations that are sufficiently large, average birth and death rates provide relatively stable descriptions of key aspects of that population’s demography. However, when a population’s size decreases to below a certain threshold, variations in fitness of a small number of individuals can have a large impact on the overall populations’ demographic parameters, causing population size and other characters to fluctuate up or down unpredictably (Schleuning and Matthies, 2009). Consider, for example, an isolated population of crocodiles with only a few females. As with many other reptiles, offspring sex ratios of crocodiles are determined by the environmental temperature during incubation (Hutton 1987). If, by chance, the population experiences two years of high temperatures, which favour male offspring, and the few females die by chance, the all-male population may be doomed for extinction unless some female crocodiles immigrate from elsewhere.
The social systems of group-living animals can easily be disrupted when their population size or density falls below a critical level.
Small population sizes or low densities can also disrupt social interactions among individuals—especially interactions that affect reproduction—which can cause populations to become demographically unstable. This situation, referred to as the Allee effect, can result in further declines in population size, population density, and population growth rate. Obligate cooperative breeders, such as African wild dogs (Lycaon pictus, EN), are especially vulnerable to the Allee effect (Courchamp et al., 2000) since they need a certain number of individuals to protect their territories and obtain enough food for their offspring (Figure 8.9). Allee effects might also prevent impact group-living species that are not cooperative breeders—recalling the “safety in numbers” mantra, Allee effects seem to prevent the recovery of locally-rare sable antelope (Hippotragus niger, LC) populations in South Africa’s Kruger National Park, as reduced herd sizes increases their exposure to predation (Owen-Smith et al., 2012). But even solitary species that live at low densities are susceptible to Allee effects, since they may find it hard to locate mates once the population density drops below a certain level.
Environmental stochasticity and catastrophes
Environmental stochasticity, the unpredictable variation in environmental conditions, can cause dramatic population size fluctuations over time, and hence, substantially increase the risk of extinction. Consider, for example, how the development rate of many insects is strongly temperature-dependent (e.g. Rebaudo and Rabhi, 2018). In an average or warm year, young insects that hatch on time and feed well may result in ecologically fit adults that produce many young, whereas unusually cold years might reduce hatching success and larval activity, which could also reduce adult fitness (Gibert et al., 2001). So, highly unfavourable conditions in any one year can cause dramatic population declines, or even push a species to extinction if conditions persist over successive years across its range.
Even though a small population may appear to be stable or increasing, an environmental catastrophe can severely reduce population size or even cause extirpation or extinction.
The increased risk of extinction from environmental stochasticity also applies to natural catastrophes that can occur at unpredictable intervals (e.g. droughts, storms, earthquakes, and fires). Range-restricted species are particularly vulnerable to this kind of threat. For example, the biodiversity living in and around several African crater lakes are vulnerable to a rather unique natural phenomenon called “lake burping”. Volcanic chambers underneath some of these lakes are rich in CO 2 . Small amounts of CO 2 may sometimes (or constantly, in some cases) seep up through the lake bed into the surrounding water. Because these lakes are thermally stratified—layers of cold, dense water settle near the bottom while warm, less dense water floats near the top—the CO 2 -saturated water remains near the bottom of the lake. However, when there is a geologic disturbance, such as a landslide or earthquake, massive amounts of CO 2 may suddenly be released, first saturating the warmer water at higher levels with CO 2 (killing fish and other oxygen-dependent species in the process), before displacing the breathable surface air in and around the lake. In 1986, one such CO 2 eruption killed 1,800 people and 3,500 heads of livestock near Cameroon’s Lake Nyos (Krajick, 2003). Some scientists fear that increased deforestation (which may trigger erosion and landslides) and hydraulic fracturing (which may trigger earthquakes, Section 7.1.1) could trigger similar events at other crater lakes in the region.
Environmental stochasticity tends to increase the probability of extinction more than does demographic stochasticity. As discussed, this is especially true for small populations and range-restricted species.
The extinction vortex
As populations decline in size, they become increasingly vulnerable to the combined impacts from the loss of genetic diversity, inbreeding depression, Allee effects, environmental stochasticity, and demographic stochasticity. All these factors tend to lower reproduction, increase mortality rates, and reduce population size even more, in turn driving populations to extinction at increasingly faster rates over time (Fagan and Holmes, 2006). Conservationists sometimes compare this phenomenon to a vortex, spiralling inward, moving faster (or declining faster in the case of a population) as it gets closer to the centre. At the centre of this extinction vortex (Gilpin and Soulé, 1986) is oblivion—the extinction of the species (Figure 8.10).
The demise of the bluebuck—the first large mammal of Africa to face this fate after European colonisation—may have been the result of an extinction vortex. When European colonists first arrived in South Africa, this ungulate already persisted as a single, small population of an estimated 370 individuals (effective population size at 100 individuals) and a highly restricted (4,300km 2 ) distribution. Considering this small and restricted population’s vulnerable to deleterious genetic factors and demographic stochasticity, a recent study showed that this species was probably caught in an extinction vortex by the time the first colonist shot the first bluebuck (Kerley et al., 2009). This species would thus likely have gone extinct even in the absence of hunting and habitat loss, which only hastened its departure.
Is there any hope for small populations?
Despite the odds and the many threats facing Africa’s wildlife, many species that were once on the brink of extinction have clawed their way back from the abyss towards stable, and sometimes even growing populations. Prime examples include the Pemba flying fox (Pteropus voeltzkowi, VU); considered Critically Endangered in 1996, conservation education programs raised awareness of this unique bat, which now has considered Vulnerable, having recovered to more than 28,000 individuals (Entwistle and Juma, 2016). Similarly, because of habitat destruction and introduced predators, the future of the Seychelles magpie-robin (Copsychus sechellarum, EN) looked rather bleak in 1970, when only 16 individuals remained, all on one island. Today, thanks to habitat restoration efforts, supplemental feeding, invasive species eradication, provisioning of nest boxes, and a translocation program, there are more than 280 Seychelles magpie-robins scattered across five islands (Burt et al., 2016). Another remarkable conservation success story involves the rescue of the southern white rhinoceros (Ceratotherium simum simum, NT), which was reduced to about 20 individuals in a single protected area in the late 1880s. Dedicated conservation efforts since then have seen this iconic species recover to more than 20,000 individuals, with individuals introduced and reintroduced all over Africa and zoos throughout the world. None of these species would have been alive today if it wasn’t for intensive multi-year efforts by dedicated conservation biologists to pull them out of their individual extinction vortices.
Bringing species with small populations back from the edge of extinction requires dedication, careful planning, and significant amounts of resources.
Bringing species with small populations back from the edge of extinction requires dedication, careful planning, and significant amounts of resources. It also requires careful population management to mitigate the negative impacts of founder effects and both demographic and environmental stochasticity (Box 8.4; see also Chapter 11). As these examples show, it can be done. But, given the challenges, it should always be a priority to prevent a species from declining to very low numbers in the first place.
Kelly Marnewick 1,2
1 Carnivore Conservation Programme,
Endangered Wildlife Trust,
Johannesburg, South Africa.
2 Current address: Department of Nature Conservation,
Tshwane University of Technology,
Pretoria, South Africa.
South Africa is one of the few countries in Africa where numbers of many large carnivore species are stable and, in some cases, increasing. Much of this success can be attributed to the managed metapopulation approach, which involves the reintroduction and subsequent translocation and management of populations in geographically isolated fenced reserves, between which natural dispersal is highly unlikely. As of 2016, more than 300 cheetahs are being managed in 51 reserves encompassing 10,995 km 2 (mean: 195 km 2 range: 20–1,000 km 2 ) and nearly 250 African wild dogs in 11 reserves encompassing 5,086 km 2 (mean: 216 km 2 range: 19–1,000 km 2 ). The reserves are situated across the country within a variety of land tenure systems including state and provincial protected areas and privately owned and community-run game reserves. Most reserves derive income primarily from ecotourism.
Each reserve forms part of the national network. Animals are moved between reserves to maintain the genetic integrity and demographic balance of individual subpopulations, but also to minimise direct management in the long term. Translocations are planned to mimic natural processes as far as possible but, due to the intricacies involved in managing animals between several reserves, this is not always possible. For wild dogs, small groups of unrelated adult males and females are artificially bonded to form packs, which mimics natural pack formation in the wild. For cheetahs, sub-adults are removed once they disperse from their maternal range. The animals are generally immobilised in the field and transported awake in crates on vehicles to their new reserves. Soft releases (Section 11.2.1) are preferred: these involve the animals being kept in temporary holding bomas of approximately 1 ha in size for about three months. The formation of artificial social groups is also done during this period. Intensive post-release monitoring is done at intervals reliant on reserve resources, but daily monitoring is recommended. The success rate of reintroductions has been high and, for wild dogs, has been strongly linked to the social cohesion of released groups (Marneweck et al., 2019), and the integrity of perimeter fences (Gusset et al., 2008).
This highly collaborative process involves multiple stakeholders, including conservation NGOs, provincial government conservation departments, private reserve owners and managers, researchers, local communities, and tourists. Effective and responsible population management tools help to prevent local populations growing too large or too small, and best practice guidelines ensure the ethical handling and management of animals. Individual reserves are responsible for providing infrastructure and other requirements including managing sustainable prey populations, perimeter fences, bomas and post release monitoring, as well as ensuring that a management plan is in place and adhered to. In many cases, students or volunteer organizations conduct post-release monitoring. National, high-level management is coordinated by the Endangered Wildlife Trust (EWT) and is funded through donations from corporations, individual philanthropists, conservation trusts, and foundations.
The managed metapopulation approach to carnivore conservation has increased the number and distribution of both cheetahs and African wild dogs in South Africa and built technical capacity in the country for metapopulation management (Davies-Mostert and Gusset, 2013), which has also been applied to species, such as lions, elephants, and black rhinoceros (Diceros bicornis, CR). Opportunities abound in other countries to use lessons learned in South Africa for the recolonisation of other areas where large mammals have been locally or regionally extirpated. Additionally, projected human population expansion, and the habitat fragmentation that comes with it, means that this approach is likely to become an indispensable tool in maintaining the viability of populations in disconnected landscapes.