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One of the most comprehensive studies looking into the sex bias in natural history collections has found that among birds and mammals, males are more frequently collected.
The work reflects a growing awareness across all areas of science of underlying sex biases in data and their repercussions in the wider world.
The specimens held in natural history collections around the world represent the wealth, beauty and diversity of our planet. But rather than being an objective picture of life on Earth, these collections have long been the result of curatorial bias.
An example of this bias is that there is often an overrepresentation of mammals and birds in collections, despite the far more numerous and diverse invertebrates and plants. What's more, even within these groups there are certain biases in how they were collected.
By looking at the bird and mammal specimens held by five major natural history collections, including those at the Natural History Museum, researchers have been delving into whether there is an underlying sex bias - in others words, whether there were more male specimens in the collections than female ones.
'We looked at over two million specimen records from the American Museum of Natural History, the Field Museum, Muséum National d'Histoire Naturelle, the Smithsonian and the Natural History Museum London,' says Natalie.
'From that we found - perhaps unsurprisingly - that there was a bias towards male specimens. It is worse in birds than in mammals, with only about 40% of bird specimens being females, but around 48% female in mammals.'
Groups which show a particularly pronounced bias towards males are those which the males have ornamentations such as the birds of paradise, hummingbirds, carnivores and artiodactyls, like deer, antelope and cattle.
The disparity between the number of male and female specimens in the collections is not wholly unsurprising - it is often the males that have big, showy characteristics - but it might be expected that more recent scientific collections would try and redress this balance. The data, however, shows that this has not been the case.
This means that, for studies which have used natural history collections in everything - for example, biogeography, morphology, taxonomy, genetics and even parasitology - there is likely to be an underlying male bias in the data.
Showing that there is a skew in natural history collections is one thing, but figuring out where it comes from is just as important.
'We were then interested in trying to work out why there is this bias, because obviously curators don't just throw away the female specimens,' explains Natalie. 'It must be something to do with how they were collected.
'That could be either passive, so something to do with how male and female animals behave in the field, or it could be active whereby collectors are deliberately choosing to target males.'
Male and female animals can and do behave differently in the wild. In some species, for example, males may range more widely and so could be more likely to fall into traps, or maybe their more conspicuous nature means that males are more likely to be spotted.
'It is really hard to collate data on the passive explanations,' says Natalie. 'Although from what we can tell there are not more males in most natural populations. In fact, even though many wild populations are female-skewed, we still find lots more males in the collections, so it does seem like there is some active choice going on.'
The data showed that among mammals, collectors were more likely to select large individuals with some form or ornamentation or weaponry such as horns, antlers, mains or tusks. In birds, size was not as important as colouration, as it was the more brightly feathered individuals that were more likely to be collected.
Where you have birds in which the female is more colourful and bigger than the males, however, there are more females than males in the collections.
On the surface, a slight bias towards males in museum collections might not seem like much of an issue. But there are many aspects of a species' biology and behaviour that are affected by an animal's biological sex.
At a basic level, if a study is looking at the taxonomy of a species and there are significant differences between males and females in their morphology, any bias towards the males could result in it being difficult to identify females down to species levels, as females are underrepresented in collections.
These biases can go even deeper. For example, males can be more susceptible to parasites as testosterone inhibits the immune system. Where collections are sex-biased, research looking into infection and immunity within a species could be skewed.
As research is advancing into more technical analyses, these biases can cause significant differences. Stable isotope ecology can use the chemicals found in tissue to figure out where an animal may have been living or migrating based on what they were eating during their lifetime. But some species may have sex-segregated diets, meaning that you cannot draw inferences about a species in general if the underlying data is overrepresented by one sex.
'You'd like to hope that visiting researchers would come to the Museum and are selecting specimens with a mind to getting an equal number of males and females,' says Natalie.
'But often when people are doing big studies, they might not even consider the sex. They are more interested in getting as many species represented as possible, or in some cases they might not have a choice due to a limited number of specimens for some species that are available in the first place.'
In these situations, researchers simply need to be aware of the skews and build them into their analyses. This is something that is being seen more and more in science, from how crash test dummies have typically been based on the male body to how bulletproof jackets have been designed for men.
One of the most striking biases is seen when looking at type specimens. These are the individual specimens on which a species description is made, and so seen as a typical example of that particular species.
Of these, only 25% of bird and 39% of mammal type specimens were found to be female.
'This bias was found to be way more extreme,' says Natalie, 'but it is also funny because there is a way of fixing it and people don't seem to have bothered to take that option.
'You can have these things called paratypes, which are specimens collected at the same time as the type but will represent other parts of the species diversity. It would seem obvious to me to take an opposite-sex paratype, but people don't seem to be doing that.'
Natalie and her colleagues expected that there would be significant sex biases in the early 1800s as trophy hunters went out and selected the biggest and fiercest males, but the team assumed that it would get better over time. It didn't.
'It's exactly the same,' says Natalie. 'It's the most beautiful flat correlation that I've ever seen. It's glorious.'
Museums as whole, it turns out, are simply really bad at recording the sex of specimens in their collections. Of the two million that were looked at for this study almost half were unsexed, even in species where the sex is obvious. So one of the most basic things that could be done is to actually record the sex of an individual in the first place.