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A predation paradox for tropical birds?

Blog written by Suzanne Austin & Doug Robinson. Read the full paper here.

Why do lowland tropical birds have longer incubation periods than temperate species? This question has received substantial attention in recent decades with a large amount of research on a hypothesis known as the predation paradox. This hypothesis suggests that the longer tropical incubation periods are a consequence of parents reducing their own time at the nest to reduce chances predators will find the nests by seeing the parents coming and going. Nests of tropical songbirds are, on average, lost to predators more often and more quickly than those of temperate songbirds. For example, an average songbird nesting in the humid lowlands of Panama will have to nest about four times before they fledge offspring whereas a typical temperate songbird may need to nest only once or twice to fledge kids.

As a consequence of less parental time at the nest, egg temperatures drop, which then increases the time required for embryos to develop. Despite these ideas, there have been few data gathered on actual time spent incubating by most species of tropical birds. We documented incubation behavior by 112 species of tropical and temperate songbirds with video cameras plus some data from the existing literature.

Dusky antbird. Image at top of the blog shows a white-billed antbird. Both photos by Lisa Miller.

To understand how adults were allocating time to incubation of eggs, we compared multiple variables that described adult incubation behavior including constancy (the total proportion of time that adults spend incubating), visit rate (the number of trips by parents to the nest in an hour), on-bout length (the amount of time parents spent incubating their eggs in an individual visit), and off-bout length (the time parents spent off of the eggs during an individual recess). We also compared each parental attendance variable to a set of environmental, natural history and life-history characteristics, such as nest predation rate, egg mass, adult mass, clutch size, adult incubation strategy (uni-parental or bi-parental), nest height, and nest type (open-cup, enclosed-cup, or cavity).

Despite longer tropical incubation periods, we found that the proportion of time (constancy) spent incubating was not different for tropical and temperate birds.  When we adjusted constancy to reflect the differences in day length between Michigan and Panama, we still found no difference associated with latitude in constancy. This result indicates that birds were spending a similar proportion of time incubating regardless of latitude (median= 71-75%).

However, when we investigated how birds allocated their incubation time, we found that tropical songbirds typically stayed longer on their eggs during each incubation bout (on-bout length), took longer recesses away from their eggs (off-bout length) and made fewer trips to their nests (visit rate). Lowland tropical species were engaging in a different incubation strategy than temperate songbirds.

Field sparrow nest. Photo by Suzanne Austin.

While our finding of similar constancy across latitudes was inconsistent with the predation paradox, our data indicated that visit rate and off-bout length followed the pattern predicted by the predation paradox, but on-bout length didn’t. The expectation of lower constancy and shorter on-bout length, which were proposed to explain the longer tropical incubation periods, did not occur in our sample of tropical birds.  

Our data did reveal that nest predation was related to several attendance variables, but in directions inconsistent with those suggested by the predation paradox. Instead, birds subject to higher nest predation rate tended to spend more time on the nest rather than less time. We also found that incubation period was not related to any of our attendance variables, which suggests that how eggs were incubated didn’t explain the variation in incubation period length in the songbird species in our dataset.

We suggest that parents have optimized their incubation strategy to limit fitness costs to their offspring and to themselves, which may explain why constancy is fairly consistent within species. Yet, how birds allocate their time incubating their eggs varies across latitude. We suggest that there is an interaction between the environment and the needs of the embryo, which influences the strategy parents use to incubate their eggs. For example, the higher, more stable ambient temperatures of the lowland tropics likely allow parents to spend longer away from their eggs than temperate parents because the cooling rate of eggs is lower. These data add to the growing body of literature that suggests nest predation does not explain the observed differences in embryonic development across latitudes. Instead, much of the variation might be influenced by intrinsic differences in embryos during development, such as latitudinal differences in construction of immune systems, morphological attributes and degree of maturity at hatch.

Menopause with the in-laws: Why living with your husband’s family may make your menopause worse

Blog written by Megan Arnot. Read the full paper here.

The menopause generally occurs in women at around the age of 50 (Laisk et al., 2019), and for many, this process is accompanied by many negative symptoms, such as brain fog, hot flashes, and anxiety. In Western societies, it is often taken as read that these symptoms are a normal part of the menopausal transition; however, cross-cultural research is beginning to demonstrate an unpleasant experience is not an inevitability (Avis et al., 2001).

For example, Japanese women are less likely to report hot flashes compared to Western women (Thurston et al., 2008). Similarly, women who smoke are at a greater risk of a turbulent menopausal transition and an earlier menopause than non-smokers (Gold et al., 2006). As a result, researchers have begun to focus on what behavioural and lifestyle factors might influence the severity of symptoms throughout the menopausal transition.

In our new paper, we consider whether living arrangements influence menopause symptoms, and our results were surprising: women living with their genetic family reported less severe menopause symptoms than those who lived with their husband’s family.

Family matters?

As anthropologists, we are interested in how different levels of relatedness within households can have behavioural and physiological implications.  In the case of the menopause, we were interested to see whether these varying levels of relatedness had any bearing on the symptoms experienced throughout the menopausal transition. To do so, we travelled to south-west China to collect data. 

In this region of China, there are different ethnic groups with distinct living arrangements, which lends itself to easy comparison of different levels of relatedness between households. Firstly, the Han and Yi are ‘patrilocal’, which means women typically leave their family following marriage to live with that of her husbands. Secondly, the Mosuo and Zhaba display a more uncommon ‘duolocal’ residence pattern. This means that even when married the husband and wife live separately, each residing in their family households, partaking in the practice of zou hun (‘walking marriage’), in which they only visit one another at night (Wu et al., 2013).

It turned out that the duolocal women who lived with their own families reported significantly less symptoms than the patrilocal women who lived with their husband’s family following marriage.

Living arrangements and conflict

While this results was initially slightly perplexing, we think that this may be due to the differing levels of conflict and support within the households, which is contingent upon the post-marital residence pattern of the group.

If a woman moves to live with her husband’s family (i.e. is patrilocal), then until she has children, she is not biologically related to anyone in the household. This lack of relatedness may cause tension between the new wife and her husband’s relatives, as they have little genetic interest in her (Danielsbacka et al., 2018).  Additionally, it has been observed elsewhere that women who live with their husband’s family argue with their partners more and are more likely to get divorced. More extremely, rates of domestic violence are higher for women who live away from their family (Borgerhoff Mulder & Rauch, 2009). 

In the context of menopause symptom severity, increased levels of household conflict would likely make the woman more stressed, and stress has been observed in previous research to worsen pain perception (Ahmad & Zakaria, 2015). Therefore, household conflict may exacerbate any menopause symptoms the woman is experiencing.

In addition to there being decreased levels of household conflict when women reside with their own family following marriage; these households may also provide higher levels of social support. A household in which there are plenty of people willing to help you out – both in terms of emotional and physical support – would contribute to a less stressful environment, which may soften the physiological and psychological burden of the menopausal transition. 

Within the study sample, the Mosuo are widely regarded to be an extremely peaceful group, with arguments between family members being consciously avoided and rarely observed. On the other hand, in in ethnographic literature there is a greater number of reports of social conflict within the Han and the Yi, lending support for our hypothesis that conflict and support are influential in determining how symptomatic the menopausal transition is.  

Global perspectives

While our research was conducted in China, globally, we see a wide range of living arrangements which would provide various levels of conflict and social support. In the West, women typically live away from their families, which may mean they have decreased levels of social support, perhaps contributing to more turbulent menopause symptoms.

These results aren’t an excuse to visit your in-laws less! However, they do demonstrate that menopause symptoms are not simply the inevitable result of hormonal irregularities. To an extent, they are the product of your social environment, which should be worth bearing in mind when approaching and going through the menopause.

References

AHMAD, A. H. & ZAKARIA, R. 2015. Pain in Times of Stress. The Malaysian Journal of Medical Sciences, 22(Special Issue), 52-61.

AVIS, N. E., STELLATO, R., CRAWFORD, S., BROMBERGER, J., GANZ, P., CAIN, V. & KAGAWA-SINGER, M. 2001. Is there a menopausal syndrome? Menopausal status and symptoms across racial/ethnic groups. Social Science & Medicine, 52(3), 345-356.

BORGERHOFF MULDER, M. & RAUCH, K. L. 2009. Sexual conflict in humans: Variations and solutions. Evolutionary Anthropology, 18201-214.

DANIELSBACKA, M., TANSKANEN, A. O. & ROTKIRCH, A. 2018. The “Kinship Penalty”: Parenthood and In-Law Conflict in Contemporary Finland. Evolutionary Psychological Science, 4(1), 71-82.

GOLD, E. B., COLVIN, A., AVIS, N. E., BROMBERGER, J., GREENDALE, G. A., POWELL, L., STERNFELD, B. & MATTHEWS, K. A. 2006. Longitudinal analysis of the association between vasomotor symptoms and race/ethnicity across the menopausal transition: Study of Women’s Health Across the Nation. American Journal of Public Health, 96(7), 1226-1236.

LAISK, T., TŠUIKO, O., JATSENKO, T., HÕRAK, P., OTALA, M., LAHDENPERÄ, M., LUMMAA, V., TUURI, T., SALUMETS, A. & TAPANAINEN, J. S. 2019. Demographic and evolutionary trends in ovarian function and aging. Human Reproduction Update, (dmy031), 1-17.

THURSTON, R. C., BROMBERGER, J. T., JOFFE, H., AVIS, N. E., HESS, R., CRANDALL, C. J., CHANG, Y., GREEN, R. & MATTHEWS, K. A. 2008. Beyond frequency: who is most bothered by vasomotor symptoms. Menopause, 15(5), 841-847.

WU, J. J., HE, Q. Q., DENG, L. L., WANG, S. C., MACE, R., JI, T. & TAO, Y. 2013. Communal breeding promotes a matrilineal social system where husband and wife life apart. Proceedings of the Royal Society B: Biological Sciences, 280(1758).

The shortest way from Belgium to Congo leads through Prague

Blog written by Karolína Brandlová. Read the full paper here.

It’s amazing to see my students getting their education in Prague, professionally growing and becoming part of the research and conservation teams across Africa. Our faculty is a sort of surprise, being situated in the heart of Europe and focused on tropical regions – Faculty of Tropical AgriSciences of the Czech University of Life Sciences Prague.

When I graduated (decades ago) our faculty was almost fully oriented to agriculture in the tropics. Fifteen years ago, we decided together with my colleagues concerned about wildlife to open a new study branch focused on wildlife management, currently named Wild and Domestic Animal Production, Management and Conservation. Step by step we have developed a team able to combine extensive fieldwork across Africa with teaching specific subjects focused both on wildlife management and conservation and on sustainable animal production. We’ve always been teaching in English and have acquired students from different parts of the world, passionate to join our projects and become wildlife management and conservation professionals. The first author of this paper, Mathias D’haen, is one of them.

Fieldwork surrounded by elephant grass in Garamba National Park. Photo copyright – African Parks.

He came to Prague from Belgium, with a clear idea to work on a conservation project in Africa. It was not easy at the very beginning to find a place where he could go to fulfil his idea for his master thesis, with results which would have clear applied conservation impact. He finally decided to join the team at African Parks, managing the extremely challenging Garamba National Park in the Democratic Republic of Congo, where he spent a year as a trainee and became responsible for giraffe research, monitoring and conservation.

Garamba National Park is really remote. The last remnant of a once widespread Kordofan giraffe population is now completely isolated, with the nearest neighbouring population hundreds of kilometres away in South Sudan – and it is unsure if those giraffe even still exist there . Garamba is also the southernmost part of the Kordofan giraffe area of distribution, with considerably higher humidity than the rest of its range, resulting in different vegetation conditions and composition.


Kordofan giraffe standing up after immobilisation, fitted with a harness satellite collar. Photo copyright – African Parks.

Mathias became part of the team and, supported by experts from Giraffe Conservation Foundation, searched for answers to many crucial questions which may help set up effective conservation measures for this population. How many giraffe are, in fact, in Garamba? Where do they live and how they use the challenging environment? What should be done to ensure their long-term survival?

Kordofan giraffe in Garamba Nationa Park. Photo copyright – African Parks.

You can find some of the answers in the paper, and also some more questions which emerged during the data processing and result interpretation. We are all aware of the fact that the paper itself will not save the giraffe. However, the results of our study can be used to design dedicated conservation actions and make informed decisions. I am proud of Mathias who is still working with African Parks, and proud of many other students who are becoming conservation professionals able to conduct sound research which may be applied to effectively protect species and prevent species extinctions.

Friend or Foe? What if we could predict the impact of non-native insects before they arrived?

Blog written by Angela M. Mech, Matthew P. Ayres, and Daniel A. Herms. Read the full paper here.  

When we hear the word ‘Alien’, most of us conjure up images of extraterrestrials: terrifying, sharp-toothed, drooling, ugly creatures from outer space that are out to destroy us. The truth of the matter is that our fear regarding these aliens is not completely irrational – we don’t know what they would want, we don’t know how dangerous they could be, and we don’t know if we have any weapons that could stop them if they did turn out to be dangerous. When it comes to alien (non-native) herbivorous insects, we have the same fears for the same reasons. We don’t know if they will wipe out our native plants or permanently alter our ecosystems, we don’t know how much they will cost us, and we don’t know if we’ll be able to stop them. This fear exists even though we know that only a small percentage (~15%) of non-native insects actually damage our forests. One of the greatest challenges we face is that we don’t know whether a newly established insect will be harmless or a high-impact invader that causes widespread tree mortality. Our fears may be alleviated if we could somehow predict how much damage a non-native insect would cause before it even gets here. Towards that end, we need to understand what factors drive insect impact. In other words, what ingredients are in the recipe for destruction?

Approximately 450 non-native herbivorous insects have established in North American forests (Aukema et al. 2010). Since the late 1800’s, researchers have been trying to find a recipe that predicts their impact, with most hypotheses assuming that evolutionary history is probably one of the main ingredients. In our study, we evaluated multiple ingredients as potential predictors of insect impact, including those related to the evolutionary relationships between insects and trees. We examined four main categories: 1) insect traits such as the number of eggs laid, feeding method, and reproductive strategy; 2) host traits such as tree growth rate, wood density, and shade tolerance; 3) evolutionary history between the novel and coevolved hosts (i.e., how many million years ago the non-native insect’s new host and native host shared a common ancestor), and; 4) evolutionary history between the non-native insect and the species that coevolved with the new host tree (i.e., what is the closest insect relative that coevolved with the novel host?).

Eastern hemlocks (Tsuga canadensis) killed by the hemlock woolly adelgid (Adelges tsugae) in the Great Smoky Mountains National Park, Tennessee. Photograph by Scott Salom, Virginia Polytechnic Institute and State University.

For our study, we focused on non-native insects that feed exclusively on conifer trees (conifer specialists). Conifers made a good model system because they are well studied (including evolutionary history) and of great importance ecologically and economically; 58 non-native insects in North America are considered conifer specialists. We found that divergence time to the most recent common ancestor between the insect’s native and new conifer host was a strong predictor of insect impact. For example, sap-feeding conifer specialists are more damaging on trees that diverged ~12-17 million years ago, with a 27% chance that they will cause widespread tree mortality, but that probability drops to as low as 1 in 650 million as the trees become more distantly related. In regards to host traits, we found that trees that were both shade tolerant and drought intolerant have a higher chance of experiencing mortality from a non-native insect than trees without these traits (26% versus 1.4% respectively). We also found that the chances of the non-native insect causing high impact was ten times lower if there was a North American insect in the same genus already utilizing the host tree. Surprisingly, there was no relationship between insect traits, singularly or in combination, and the probability that a non-native insect would be high-impact. Our research is the first that we know of to quantify the risk that a non-native insect will become a high-impact pest based on evolutionary history.

Example of high-impact damage caused by a non-native insect: Red pines (Pinus resinosa) killed by the red pine scale (Matsucoccus matsumurae)near Myles Standish State Forest, Massachusetts. Photograph by Jeff Garnas, University of New Hampshire

Most recipes typically have more than one ingredient, and we hypothesized that the same was probably true with predicting impact. In fact, we found that combining the three predictive models into a single model increased the strength of predictability beyond any of the individual models. From random selections of insect species that were high impact and not high impact, our composite model correctly identified the high-impact species 91% of the time. For example, one of the most damaging non-native conifer specialists in North America is the balsam woolly adelgid (Adelges piceae), which is causing mortality of a number of native fir species. These insect-tree combinations have the following category traits: 1) North American fir trees are shade tolerant and drought intolerant, 2) North American fir trees diverged from the European silver fir 13.6 – 16.8 million years ago, and 3) none of the North American fir trees coevolved with an Adelges species; the perfect recipe for mass destruction.

Our model provides a practical means for managing environmental security in the age of globalization. We can now better predict the impact that a non-native forest insect would have before it invades North America. Specifically, our combined model predicts whether a non-native, conifer specialist insect will have a one in 6.5 to a one in 2,858 chance of becoming high impact. This could have practical value in our struggles to limit high-impact non-native invasions. For example, we can now produce more quantitative and reliable watch lists of potential new pests, which could let us prevent their arrival in the first place. This knowledge will hopefully be a powerful weapon to help keep the next high-impact alien insect from becoming our next nightmare.  

Literature Cited

Aukema, J. E., McCullough, D. G., Von Holle, B., Liebhold, A., Britton, K., & Frankel, S. J. (2010). Historical accumulation of nonindigenous forest pests in the continental United States. Bioscience,60, 886-89. doi: 10.1525/bio.2010.60.11.5

Behind the paper: returning home to study how box-nesting birds fend off their parasites

Blog written by Sarah A. Knutie, Assistant Professor at the University of Connecticut, USA. Read the full paper here.

As a first generation college student, I had little knowledge of the college process and what it entailed. At the University of Minnesota, I started as a computer science major because my mother showed me a newspaper article promoting women in the field of Information Technology (IT) and I enjoyed using HTML to create unofficial fan websites for celebrities (you’re welcome Leonardo DiCaprio).

After several years of coursework, I decided that computer science was not my passion so I started exploring all other possible majors. I enrolled in a few ecological field courses at the UMN’s Itasca Biological Station in northern Minnesota and after a few days of the courses, I had found my career path. Over the next decade, I decided that I wanted to return to Minnesota someday to establish a long-term research program to inspire and train undergraduates just like myself. Therefore, while pursuing my graduate degrees on unrelated projects, I spent all my “free time” during the summer months building connections with local residents, including Christmas tree farmers, at and near Itasca Biological Station.

Banding birds in northern Minnesota in 2008. Photo by Erin Feichtinger.

After finishing my PhD, for which I studied the effect of introduced parasitic nest flies on birds in the Galapagos Islands, I wanted to find a local system in the US to understand the variation in host defenses against native parasites. The perfect system finally caught my eye: box-nesting birds and their parasitic nest flies Protocalliphora sp.

Nest box in a field in northern Minnesota. Photo by Sarah Knutie.

Not only are these flies similar to the parasites that I studied in the Galapagos (they live in the nests and the larval (maggot) stage feeds on the baby birds), but I also could experimentally manipulate the parasites and environmental conditions to establish links among host, parasites, and their environment in Minnesota. Protocalliphora flies parasitize a wide range of bird species, but some of the most commonly-studied bird hosts are the eastern bluebirds and tree swallows.

Adult eastern bluebird. Image at the top of the blog shows an adult tree swallow. Both pictures by Jeremy Cohen.

In 2014, my father and I started building wooden bird nest boxes for eastern bluebirds and tree swallows. Over the next 4 years, we built and established close to 150 new nest boxes near Itasca Biological Station, which added to the existing 50 or so boxes that had already been set up by local residents.

My father, Steve Knutie, with the first few nest boxes that he built in my grandmother’s garage. Photo by Sarah Knutie.

The first step of the project was to determine the effect of the parasite on hosts and whether hosts could defend themselves against the parasite. I had already established working relationships with local residents, including co-author John Hurlbert from Bemidji’s Christmas [Tree] Forest. I recruited University of Minnesota undergraduate students, including first author Kirstine Grab and co-authors Allie Parker and Dasha Pokutnaya, to help with the fieldwork. I also collaborated with Dr. Brian Hiller from Bemidji State University and his undergraduate student McKenzie Ingram. I was fortunate to receive two small grants from the Minnesota Ornithologists’ Union and North American Bluebird Society to get this work started.

Former Christmas tree farmer John Hurlbert shows his granddaughter the tree swallows in his nest box. Photo by Sarah Knutie.
Dr. Brian Hiller and McKenzie Ingram at a bluebird nest box. Photo by Sarah Knutie.

My team first reviewed published studies on the relationship between the parasitic nest fly and bluebirds and swallows. We found that across space and time, bluebirds had over twice as many parasites compared to swallows but both bird species did not suffer a negative consequence of the parasite on their survival. These results suggested that bluebirds and swallows are both well defended against the parasite, but might defend themselves in different ways.

Recently hatched tree swallow nestlings. Photo by Sarah Knutie.

Two field seasons went by in Minnesota before we had enough pairs of birds occupying the boxes for the study. In 2016-2017, we started our study by experimentally manipulating the nest parasite (in other words, hosts were either parasitized or not) to determine the effect of the parasite on the growth and survival of the nestling birds. We found that the parasite did not affect the survival of either species. Therefore, both hosts were tolerant to the effect of the parasite at their respective parasite numbers. However, swallows had half as many parasites as the bluebirds. These differences were likely because swallow nestlings produced an immune response to the parasite, which reduced parasite numbers; in contrast, bluebird nestlings did not produce a detectable immune response to the parasite. We could not identify the specific way that bluebirds defend themselves against the high number of parasites to which they are exposed, but the birds are likely investing in tolerance measures to compensate for energy lost to the parasite or effectively repair damage caused by the parasite.

Tree swallow parent visiting a nest box. Photo by Jeremy Cohen.

After gathering these two years of data, I decided that it was time to publish the work. Since undergraduate education continues to be a theme in this research, I invited Kirstine Grab to spearhead the paper, from analyzing the data to writing the first and final drafts. This was Kirstine’s first scientific paper, and writing the paper with her was an incredibly rewarding experience for both of us. I am so proud of and encouraged by these early-career scientists.

First author Kirstine Grab holding baby bluebirds. Photo by Sarah Knutie.

Since 2017, my team has continued monitoring the effect of the parasite on bluebirds and swallows to determine whether there is annual variation in host-parasite relationships over a long time scale. The team has also been working hard to determine what environmental factors, such as food availability or temperature, affects host defenses against parasites. We have also established a citizen science project to determine the spatial distribution of nest parasites across the entire range of bluebirds and swallows throughout the United States. Please get in touch if you are interested in participating (nestparasitestudy@gmail.com).

University of Connecticut undergraduate Alyssa Addesso with a nest from a citizen scientist. Photo by Sarah Knutie

I am very fortunate that I have been able to come full circle in my career. The past 15 years – from taking classes at the Itasca Biological Station as an undergraduate to mentoring students of my own at that same station – has been a long, but extremely rewarding, journey. My advice to those who are interested in pursuing a career in field research is to think long term. Where do you see yourself in 10-15 years? Can you start setting up your system now? Often times, these side projects just need a few small steps at a time but once you’ve taken enough of these steps, you might just create the center piece of your research program!

Sunset over Lake Itasca at Itasca Biological Station. Photo by Laura Domine.

I would like to respectfully acknowledge that the fieldwork was conducted on the ancestral territory of the Chippewa Nationwhere Clearwater and Beltrami counties, Minnesota, are located.

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