The data compiled here indicate the sex ratios of monarch butterflies at Mexican overwintering colonies have been changing over the three decades since their discovery, from generally female biased (approx. 53% female) in the 1970s, to largely male-biased in recent years (approx. 43% female). This discovery was certainly unexpected and is not readily explainable. At first glance, one might think that the thinning of the sanctuary's forest over the past three decades from illegal logging (Brower et al. 2002
) has gradually changed the microclimate, making it somehow less favourable for female survival in recent years. However, evidence to date does not indicate this species has any sex-related differences in cold tolerance to natural temperatures (i.e. per cent survival in relation to temperature) (Alonso-Mejia & Arellano-Guillermo 1992
) or to experimentally induced freezing (Anderson & Brower 1993
). Moreover, our own analysis (of the WWF data) provided no clear evidence of differential mortality throughout the overwintering period (i.e. percentage of females did not clearly decline from November to March).
A second possibility is that the clustering patterns have changed over time, making males somehow more likely to be sampled by researchers in recent collections. This also appears unlikely, considering what is known of overwintering behaviour in western North American monarchs. Frey & Leong (1993)
showed that overwintering monarchs in California have no sex-related differences in tree height preference, which would lead to sex biases in captures at clusters. It follows then that the sexes would not behave differently (in terms of clustering position) at Mexican colonies.
The cause of the decline in females may not even be related to the overwintering sites at all. After uncovering the overwintering trend, we examined published records of autumn migrants and found evidence that the proportion of female monarchs has been declining in this phase as well. Long before the Mexico destination was known, Beall (1948)
made a collection of 464 migrants in Ontario that was 55.6 per cent female. A collection of 266 migrants from Missouri in 1972 showed that 50.8 per cent were females (Brown & Chippendale 1974
). Herman (1988)
collected 1868 late-summer monarchs from 1976 to 1986 and 44 per cent were female. During 1998–2001, Borland et al. (2004)
captured migrating monarchs at more than 20 locations in Minnesota and Texas and the percentage that were female averaged 40 per cent across all sites. Most recently, Brindza et al. (2008)
captured 2224 migrants at two sites in Virginia from 2001 to 2006, of which 37 per cent were female. This decline in the proportion of female monarchs during the autumn migration provides further confirmation of the temporal trend we discovered at the overwintering sites and also indicates that the change in sex ratio is occurring at the breeding grounds, or at least in the late-summer migratory generation.
Breeding monarchs face a number of threats, such as anthropogenic habitat alterations, insecticides and other chemicals, and infections with parasites such as the protozoan Ophryocystis elektroscirrha
(OE). Interestingly, there is recent evidence of differential impacts of infection on males and females; infected females experience greater infection intensities (de Roode et al. 2008
) and larger parasite-induced reductions in body sizes than males (de Roode et al. 2007
). Furthermore, field collections made in the past five years at Mexican wintering colonies have shown higher prevalence than those from 30 years ago (S. Altizer 2009, personal communication). It follows then that if OE prevalence is increasing, and if it negatively affects females more so than males, it is possible that population-level sex ratios at the breeding grounds could become skewed towards males. On the other hand, if OE is not the cause of this phenomenon, it may be that equal numbers of males and females are indeed being produced in the summer, but for some reason fewer female monarchs are now undertaking the autumn migratory journey.
Clearly, the temporal trend found here is a phenomenon that deserves additional research to uncover the causative factor, but it also highlights the many questions that remain to be answered about the biology of this unique insect migration and overwintering phenomenon, which is at risk of disappearing in the near future because of habitat loss at overwintering sites (Brower & Malcolm 1991
) and along migration routes (Brower et al. 2006
). For now, the changing sex ratio of monarchs in eastern North America remains a fascinating discovery and one which we will continue to monitor in the future.