Lonely males and low lifetime productivity in small populations


Email: paul.donald@rspb.org.uk

Perhaps because adult sex ratios (ASRs) in our own species are largely balanced (except in the oldest age cohorts, as a visit to any old people’s home will demonstrate), it is often assumed that the same holds true in populations of wild animals. This assumption is compounded by the difficulty of assessing ASRs accurately in the field, as simple counts of males and females are often confounded by huge differences in detectability between the sexes. However, with a significant increase in recent decades in detailed, long-term population studies in which numbers of males and females can be assessed with a fair degree of accuracy, it is becoming increasingly apparent that ASRs can be strongly unbalanced. In birds, for example, it seems that an ASR of one male to one female is unlikely to be the norm and that in many populations, indeed perhaps most, males outnumber females (Donald 2007). In some species, particularly those with small or declining populations, ASR in birds is often strongly skewed towards males, which might outnumber females by two or more to one. In the critically endangered Raso Lark Alauda razae, for example, up to 70% of the adult population may be males, although this fluctuates in time (Brooke et al. 2010). In mammals, the pattern appears to be in the opposite direction, females outnumbering males. Although sex ratios may vary from parity in the very earliest stages of life, even at the egg stage, the most likely cause of skewed ASRs is differences between the sexes in juvenile and adult survival rates (Breitwisch 1989, Donald 2007, Grüebler et al. 2008, Veran & Beissinger 2009). There are many reasons why female birds should live less long than males: for example, they invest much energy in laying eggs, they are at risk from predation during incubation, they tend to be the more dispersive sex and they tend to be smaller than males, which might compete with them for resources. Quite why small, isolated populations generally show more skewed ASRs than larger populations is still unclear but a number of reasons have been proposed (Donald 2007). In at least one well-studied population, it appears to be due to the fact that dispersing females essentially disappear from the population, unable to find other breeding populations, and for the same reason there is a lack of immigration of females from elsewhere (Steifetten & Dale 2006).

Greater understanding of the prevalence and degree of skewed ASRs is likely to influence our understanding of a wide range of ecological and demographic processes, including migration patterns, breeding behaviour, habitat selection, population viability, Allee effects and lifetime reproductive success (Engen et al. 2003, Bessa-Gomes et al. 2004, Calabrese & Fagan 2004, Donald 2007, Saino et al. 2010, Ewen et al. 2011, Lee et al. 2011). Empirical evidence of these effects is, however, rare. In a remarkable paper in the current issue of Ibis, Svein Dale (Dale 2011) presents data from his long-term study of the remnants of the much-depleted Norwegian population of Ortolan Bunting Emberiza hortulana to assess pairing success of males in this strongly male-skewed population. The observation that many males fail to find a mate in small populations with strongly skewed sex ratios is not new (Lawrence et al. 2008, Brooke et al. 2010), and indeed has already been reported in this Ortolan Bunting population (Dale 2001, Steifetten & Dale 2006), but this new paper adds greatly to our understanding of this issue by quantifying patterns of pairing success across the whole lifetime of male birds. In this population, around half the males remained unpaired in each breeding season, and for first-year birds, pairing success could be as low as 16%. As a result, the pattern of lifetime pairing success was highly skewed, the great majority of males never attracting a mate, or mating just once during their entire lifetimes. In this respect, the distribution of male pairing success resembles the distribution of lifetime reproductive fitness as measured by chick production (Newton 1989), the general pattern being that the bulk of one generation is parented by a small proportion of the previous generation. Even the older, most experienced males struggled to find mates and half the older males failed to attract a female in years following successful pairing. There was also a suggestion that the very oldest males had lower pairing success than less old males. It seems therefore that females preferentially selected more experienced males, with the youngest and perhaps the oldest birds missing out.

Although skewed ASRs clearly carry profound costs for males, they may actually bring benefits to females. Dale’s study of Ortolan Buntings did not assess female pairing success, but in this population and in others (Brooke et al. 2010) it is likely that most or all females were able to find a mate each year. In the Norwegian Ortolan Bunting population, females appeared to select the most experienced males, presumably thereby increasing their own breeding success. A recent study of Kentish (Snowy) Plovers Charadrius alexandrinus (Stenzel et al. 2011) has shown that in a population in which males outnumber females because of their higher annual survival, female reproductive output is actually enhanced, because they leave the care of the first brood to the male and immediately re-nest with a different mate. In this way, females are able to parent up to three successful broods in a breeding season, whereas males have time to father no more than two. Despite their shorter lifespans, therefore, females had greater overall lifetime productivity than males. However, an excess of males does not always play to the females’ advantage. In Nazca Boobies Sula granti and Humboldt Penguins Spheniscus humboldti, for example, aggressive nest intrusions by unpaired males often lead to loss of eggs or chicks (Taylor et al. 2001, Anderson et al. 2004). Although the costs of skewed ASRs to males can be assessed in the way that Dale demonstrates, estimating the costs and benefits to females is likely to be less straightforward.

Understanding the extent, causes and impacts of skewed ASRs could have profound implications for monitoring and conservation. For example, counts of the Norwegian Ortolan Bunting population based upon the usual method of recording singing males would greatly overestimate the functional population and its reproductive capacity, and so underestimate its extinction risk. As Dale concludes, it might be necessary to target conservation measures for small or isolated populations at females to achieve the maximum benefits. This is not mere rhetoric: there is growing evidence that males and females of the same species not only differ in size, structure and plumage (Owens & Hartley 1998) but also often behave in different ways, eat different foods, use different habitats, migrate in different ways, and perceive and respond to environmental stimuli differently (Recher & Holmes 2000, Insley et al. 2003, Lewis et al. 2005, Markman et al. 2006, Donald et al. 2007, Ball & Ketterson 2008, Palacin et al. 2009, Saino et al. 2010, Steinmeyer et al. 2010). Greater understanding of these differences may indeed one day show that, in a very wide range of attributes, sexual differences within species are often greater than interspecific differences within sexes. Small wonder, then, that numbers of males and females so often differ. The challenge facing conservationists now is how to use the results of this growing field of research.

I thank Jeremy Wilson for his comments on this article.