AUTHOR BLOG: Are All Eggs Created Equal? Saltmarsh Sparrows Support Gender Equality

Bri Benvenuti and Adrienne Kovach

Linked paper: Annual variation in the offspring sex ratio of Saltmarsh Sparrows supports Fisher’s hypothesis by B. Benvenuti, J. Walsh, K.M. O’Brien, M.J. Ducey, and A.I. Kovach, The Auk: Ornithological Advances 135:2, April 2018.

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Three Saltmarsh Sparrow chicks banded as part of a study on offspring sex ratios. Photo: B. Benvenuti

In birds, females have the ability to control the sex of individual eggs; therefore, a mother may be able to choose whether she prefers each egg laid to be a male or female. This means that offspring sex ratios are not usually left to chance. From an evolutionary standpoint, this can be very beneficial, as different circumstances may favor the success of sons versus daughters.

But how does one know if it would be better to have more sons or daughters? Evolutionary theory suggests that if the potential benefits of raising one sex over the other vary in relation to environmental or maternal conditions, then females should favor the production of that sex. Typically, high quality sons are more beneficial to mothers, because they have the potential to produce far more grandchildren than daughters can (males can mate many times, but females are limited by how many eggs they can produce, incubate, and raise to fledging). More grandchildren = greater lifelong success.  Still, there is a risk to biasing offspring production toward sons; if the son is low quality (competitively inferior), he may not reproduce at all.  On the other hand, daughters tend to be “cheaper” to raise than sons. They need less resources to reach maturity, and if they survive, they almost always reproduce. With this in mind, one could logically say that producing daughters represents the “safe bet”—you might get a smaller payout (in terms of numbers of grandchildren), but you know you’ll get something.

Armed with this information, we chose to investigate whether Saltmarsh Sparrows manipulate the sex of their offspring based on environmental or maternal conditions as we would expect based on evolutionary theory. These tidal marsh specialist birds live a stressful life—they build nests in the marsh grasses just inches above the marsh surface that is regularly subjected to tidal flooding. Nests are more likely to escape these flooding events and successfully fledge offspring if they are timed to fledge within the 28 day lunar tidal cycle. Saltmarsh Sparrows are also one of the world’s most promiscuous birds, with almost every egg in a nest having a different father thanks to the scramble of competition among males for access to females. These characteristics provide interesting hypotheses in the context of evolutionary theory, so we asked, would Saltmarsh Sparrow mothers produce more sons, who would be larger and a) more likely to survive a nest flooding event and b) have the ability to produce more offspring through multiple matings? Or would they take the “safe bet” and produce more females?

To test our hypotheses, we collected nesting data from Saltmarsh Sparrow breeding locations in New England marshes over five years. We used DNA analysis to determine the sex of Saltmarsh Sparrow chicks and calculated the offspring sex ratio for our four study sites and across the whole study population. We then used a modeling approach to determine if there was an influence of environmental conditions (year, tidal flooding, precipitation), temporal effects (nest initiation in relation to flood tides, timing within the breeding season), or maternal condition on offspring sex ratios.

Surprisingly, we found an even offspring sex ratio of 1.03:1 (males to females) across all years and sites, and offspring sex ratios did not vary as a function of the environment, tidal flooding risk, or female condition. What we did find was an interesting pattern of annual variation between male and female bias that mirrored the adult sex ratio in the preceding year.

While numerous studies have provided evidence that female birds may have the ability to adjust offspring sex ratios in an adaptive way, we found no evidence for adaptive sex ratio manipulation in Saltmarsh Sparrows in relation to our hypotheses. Instead, the observed time-lagged relationship between offspring and adult sex ratio meets expectations of frequency-dependent selection, whereby females respond to higher frequencies of one sex by increasing production of the rarer sex, which would have a temporary fitness advantage. Our findings overall show support for balanced offspring sex ratios at a population level over time.

AUTHOR BLOG: Recognizing the Importance of Female Birdsong

Karan Odom & Lauryn Benedict

Linked paper: A call to document female bird songs: Applications for diverse fields by K.J. Odom and L. Benedict, The Auk: Ornithological Advances 135:2, April 2018.

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House Wrens are among the familiar birds in which females sing. Photo credit: J. Hudgins/USFWS

Can you name ten North American or European bird species in which females sing? Can you name twenty? Fifty? That may seem like a lot, but in fact it’s only a small percentage of temperate-zone bird species with female song. There are at least 144 North American passerine species with female song, and many more non-passerines with elaborate vocalizations that could be classified as song (defining “song” is a topic we won’t even go into here!). Across all avian species, approximately 64% have female song, but these estimates are rough. The true numbers could be much higher. Why are the estimates so rough? Because documentation and reports of female song are lacking. We highlight this problem in our paper “A call to document female bird songs: Applications for diverse fields.” We ask all of you to help us address the deficit.

We know that the data are out there; we regularly have conversations with ornithologists and citizen scientists who tell us that they have observed singing females in myriad species. Our response: Publish it! Archive it! We’ve chatted with many senior researchers who have years of data including observations and recordings of female song in their study populations, but who haven’t published these data because female song is rare or is not their main research focus. We’ve also heard from students working as field assistants whose cohorts regularly observe singing females, but those observations are seldom documented. On field projects with many technicians, word-of-mouth data can be extensive and highly informative, but staff turnover means that known population traits never get put down on paper (or audio).

Citizen scientists frequently tell us about singing females, and many of them have taken the next step to document their observations through The Female Bird Song Project. Contributors have recorded female song in species as diverse as the Mexican Sheartail (Doricha eliza), Black-goggled Tanager (Trichothraupis melanops), Saffron Finch (Sicalis flaveola), and Cerulean Warbler (Setophaga cerulea), all of which seem to be the first documentation of female song in their species!

Each of these contributions plays a role in understanding the distribution of species with female song – data that researchers can use to address a wide range of biological questions. A complete picture of when and how female birds sing will offer insights into the biological mechanisms, evolution, and applications of avian vocal signals. Neurobiologists can ask how bird brains perceive and produce these variable signals, and whether that differs by sex. Evolutionary ecologists can ask why songs differ among species with different ecology and life-history traits. Conservation biologists can use songs to census and monitor the presence of males and females across populations.

What can you do? Don’t assume that a singing bird is a male. Look, listen, and document without bias. Teach your students to do the same. In 73% of all bird species we lack enough published information to even determine whether females sing. We are confident, however, that in some of those species females do sing because we have talked to colleagues about them. Common knowledge suggests that female song is rare, but our experiences make us question that: if all ornithologists talked to each other about female song the way that they talk to us, then that assumption would change. Your random observations of a female warbler singing can probably be backed up by the observations of many others. Females of temperate-breeding species may not sing as often as males, but when we pool all our knowledge and observations it’s likely that we’ll find more parity than we expect.

AUTHOR BLOG: Latitudinal Gradient in Bird Survival

Gonçalo Ferraz

Linked paper: Age effects on survival of Amazon forest birds and the latitudinal gradient in bird survival by A.P. Muñoz, M. Kéry, P.V. Martins, and G. Ferraz, The Auk: Ornithological Advances 135:2, April 2018.

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A Guianan Warbling Antbird, Hypocnemis cantator, banded and ready for release. Photo credit: E. Johnson

Bold, recurring patterns are fascinating, and more so if they are unexplained. For biologists living in the tropics, perhaps the most striking examples are the various latitudinal gradients in community and life history metrics. Science excites our curiosity in the search for universal rules, but large-scale latitudinal patterns hint that some things may be fundamentally different in different parts of the world. Could there be really such a thing as “tropical biology”?

One of the best-documented of these latitudinal gradients is the tendency for avian clutch size to increase with increasing latitude. Since there is no evidence that high-latitude populations grow faster than equatorial ones, it’s been widely assumed that some other life history trait must also change with latitude to compensate for the variation in clutch size. Thus, throughout the second half of the 20th century, the idea that adult tropical birds live longer than their temperate counterparts became widely accepted among ornithologists.

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A Rufous-throated Antbird, Gymnopithys rufigula. Photo credit: E. Johnson

The acceptance of a latitudinal gradient in survival, however, was more based on common sense than hard data—so much so that when Karr et al. (1990, The American Naturalist 136: 277-291) challenged the idea in a paper subtitled “Will the dogma survive?” there were not many voices sounding in defense of the “dogma.” Indeed, two decades later, Corey Tarwater and colleagues suggested that, if there is no latitudinal trend in the survival of adult birds, there could be a trend in the survival of juveniles (2011, Ecology 92: 1271-1281). Their work drew on detailed analysis of age-dependent survival in one Central American passerine species and proposed that tropical juveniles survive more than temperate juveniles. If adult survival shows no relationship with latitude this implies relatively little difference between adult and juvenile survival in the tropics.

For a paper just published in The Auk, Alejandra P. Muñoz, myself, and our colleagues used bird banding data to tackle the problem of the latitudinal gradient in bird survival on two fronts. First, we quantified the effect of age on survival for forty species of Amazon forest passerines, showing that adults at our tropical site had substantially higher survival probabilities than juveniles. Second, we compared our adult survival estimates with estimates from 175 species from Peru to Alaska and found that survival does decrease with increasing latitude. This latitudinal effect persists even after accounting for effects of migration mode, phylogeny, and time of data collection, and we conclude that the latitudinal gradient in survival is a fact after all, at least as seen among New World forest passerines.

Our work benefited a great deal from two recent advances. First, there is an ongoing transformation in how tropical ornithologists assess bird age. The Wolfe-Ryder-Pyle molt-cycle system, which we employed, is extremely useful for aging birds in populations that have poorly delimited breeding periods, which is typical of tropical regions. This was central for quantifying the effect of age on survival. Second, we tapped into the phenomenal database of Vital Rates of North American Birds made available by the Institute of Bird Populations (IBP), enabling us to include data from as far north as Alaska. The IBP estimates, combined with a wealth of tropical passerine survival estimates published since 1990, made it possible to take up Karr et al.’s (1990) challenge anew.

From the analytical perspective, we used a multi-species Cormack-Jolly-Seber (CJS) approach, a standard method for estimating apparent survival from capture-recapture data on open populations, to model our Amazon data. We treated each of the forty species in our dataset as a random draw from a wider distribution of species, and the inference about age effects was made at the level of this wider distribution, strengthening the generality of the conclusions. The CJS accounts for the possibility of capture failure, and a “mixture” component of the model, developed by co-author Marc Kéry, makes it possible to incorporate birds of unknown age in the analysis. Our work thus addresses a variety of sources of uncertainty before reaching its final conclusions.

The observation of a latitudinal trend in survival probability helps explain the maintenance of a latitudinal trend in clutch size, but it need not be the only explanation. It’s also possible, for example, that the number of clutches laid each year also varies with latitude in association with the length of the breeding season. With or without latitudinal change in number of clutches, one cannot tell whether the variation in survival we documented is a sufficient explanation for the current variation in clutch size. What’s more, even if one explains the maintenance of current variation, there is still the question of how that variation evolved. There is certainly still much to explore in the latitudinal variation of bird life history traits.

AUTHOR BLOG: Finding the Perfect Spot: Nest-Site Choice and Predator Avoidance in Asian Houbara

João L. Guilherme

Linked paper: Consistent nest-site selection across habitats increases fitness in Asian Houbara by J.L. Guilherme, R.J. Burnside, N.J. Collar, and P.M. Dolman, The Auk: Ornithological Advances 135:2, April 2018.

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A female Asian Houbara runs away from the nest area.

For birds that nest on the ground, discretion is everything. As they are especially at risk from predators, choosing where to nest may carry life or death consequences for themselves, their eggs, and their progeny.

We study the ecology of the Asian Houbara (Chlamydotis macqueenii) in the semi-deserts of southern Uzbekistan, as part of a long-term effort to gain insight into the dynamics of this wild population. The landscape has extensive low-density shrub coverage and tends to all look the same on first glance, but a closer look reveals subtly distinct habitats with shrub communities that differ in not just species composition, but also in the size and number of shrubs. The Asian Houbara is a highly cryptic ground-nesting bird inextricably associated with these habitats, breeding throughout. For 23 long days, females have the sole responsibility of laying, incubating, and protecting the eggs, and themselves, from the freezing cold and the strong sun, and from the desert predators such as foxes and monitor lizards.

This behavior of nesting in structurally different habitats made us question if females were choosing similar vegetation structure for nest sites and whether these choices had an impact on their nest success.

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A rare glimpse at a female Asian Houbara on her nest.

By following houbara tracks, we succeeded at finding 210 nests. Then we took it upon ourselves to identify and measure the height of the shrubs around all nests and at 194 random locations. Obviously, this was done after the nest was finished and the female and chicks had left the area. In the end, we identified 30 species and measured a total 35,853 shrubs! After running some statistical analysis we found that females were indeed choosing the same nest site features consistently across three structurally different habitats. Their selection was so fine-tuned that the optimal shrub height of about 30 centimeters had the greatest probability of being selected in all habitats. Furthermore, the scrape was consistently in the middle of shrubs that offered some degree of concealment, but enough visibility for the female to anticipate approaching predators.

So, females were choosing similar nest site across habitats, but we wondered if these features were helping them avoid nest predation.

To investigate this, we monitored the nests, placing temperature loggers inside the nest scrape and setting video cameras to collect information through the entire incubation so that we could classify if a nest was successful or if it had failed and, in that case, why (see video here). We found that nests in higher vegetation had a lower probability of being predated, with the likelihood being that the higher vegetation offered more concealment from predators. However, females would not nest in even higher vegetation, as this would eliminate their ability to see around and anticipate approaching predators. In fact, from more than 200 monitored nests, there was not a single time when a female was predated, which normally occurs in other ground nesting birds—females seem to value the old adage “run and hide, live to fight another day.” Nest camera footage showed us that females were eternally vigilant, with their heads extended so they could see just above the vegetation and surreptitiously leave the nest before a predator arrived. In this way, we found the connection between the choice of nest site and the chance of losing the nest to predation.

In a landscape where everything looks the same, there were in reality different habitats where nesting Asian Houbara had to find the “perfect spot” that maximized the chances of hatching while reducing the danger of being depredated. For a species of conservation concern, it is very important to maintain good productivity and minimize changes in vegetation structure away from the optimal choices, as these may lead to abandonment of previously suitable nesting areas, lower nest survival, or increased predation risk for the incubating female.

AUTHOR BLOG: Tracking the Japanese Bush-Warbler Invasion of Hawaii

Jeff Foster

Linked paper: Population genetics of an island invasion by Japanese Bush-Warblers in Hawaii, USA by J.T. Foster, F.M. Walker, B.D. Rannals, and D.E. Sanchez, The Auk: Ornithological Advances 135:2, April 2018.

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A Japanese Bush-Warbler in Hawaii. Photo credit: J. Denny

Over the past several centuries, Hawaii’s native bird populations have been decimated due to an array of factors, including introduced diseases (avian malaria and pox), introduced rats, habitat change, and hunting. As a result, most live near the tops of the mountains and have small populations. Few birds and remote locations make studying many of these native populations incredibly challenging.

In contrast, Hawaii is also home to many introduced birds that can be seen everywhere, from Brazilian Cardinals and Common Mynas on the beaches to Japanese White-eyes and various game birds at the mountaintops. Various organizations in Hawaii introduced these birds from elsewhere in the world to have birdsong fill the air again and occasionally to serve as pest control for crops. Over 170 species have been brought to Hawaii and released into the wild. Of these releases, at least 54 species now have breeding populations, and most seem destined to stay for the long haul. Many species, such as the Japanese White-eye, Northern Cardinal, Zebra Dove, and Common Myna, have robust populations and can be found in a variety of habitats.

One introduced species, the Japanese Bush-Warbler, is perhaps the coolest of them all. However, despite its prominent place as the iconic harbinger of spring in Japan, few people in Hawaii think much of this species—perhaps because it is often heard but rarely seen, or perhaps because when one does finally spy a bush-warbler, it is a drab olive-brown with few prominent markings. Whatever the reason for overlooking it, bush-warblers have successfully colonized most brushy habitats on all of the main Hawaiian Islands. They were released on the island of Oahu in the 1920s, and after decades of population growth on Oahu, they naturally spread to the remaining main Hawaiian Islands by 1997.

Birds on islands have provided some of the best historical examples of the evolutionary process—think Charles Darwin in the Galapagos and Alfred Russel Wallace in the Malay Archipelago. Capturing cases of evolution “in action” is difficult. However, introductions of non-native birds into the Hawaiian Islands provide numerous opportunities for research, particularly in assessing potential evolutionary changes over a relatively short time frame. In this study, we were afforded a unique opportunity to look at the evolution of the Japanese Bush-Warbler within the past several decades by combining population genetic analyses of this species with a detailed invasion timeline on each island. As a result, we were able to see how rapidly genetic changes can occur during an invasion. We found both expected patterns, such as a decline in genetic diversity on the most recently invaded island, and an unexpected pattern, potential assortative mating on each island. These findings suggesting substantial room for future work in a system and setting that is pretty hard to match.

AUTHOR BLOG: Call Variation Suggests Roles for Natural History & Ecology in Marsh Bird Vocal Evolution

Sarah Luttrell

Linked paper: Geographic variation in call structure, likelihood, and call-song associations across subspecies boundaries, migratory patterns, and habitat types in the Marsh Wren (Cistothorus palustris) by S.A.M. Luttrell and B. Lohr, The Auk: Ornithological Advances 135:1, January 2018.

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Marsh Wrens’ calls vary across their geographic range. Photo credit: S. Luttrell

Many bird species have unique geographic signatures in their vocalizations similar to human “accents.” Most of what we know about geographic variation in bird sounds comes from studies of bird song. Song has been a rich subject for studying geographic variation because it is typically learned, allowing song to change more quickly across space and time than a purely genetic trait. Song, however, is only one type of signal in a bird’s vocal repertoire. We wanted to build a broader picture of how vocal behavior evolves and changes among populations by looking at a large repertoire of sounds at once. Most birds have multiple call types in addition to their songs. Each call or song type is an individual trait used under unique circumstances, and that means that each one may be under different selective pressures. As a result, looking at multiple vocalizations may reveal multiple patterns of geographic variation, or, if their geographic patterns are similar, it may suggest a general process of vocal evolution. There are many ways in which vocalizations might change over time or distance. For example, changes could be random—as long as the signal still sends the correct message, some aspects of its acoustic structure could drift among populations. Additionally, vocal signals may be under selection to reduce distortion caused by the habitat in which they are produced and heard. Think about how sounds are distorted differently in an open, bare hallway versus a musician’s sound booth and how the local acoustics might alter a listener’s ability to understand you. Furthermore, if some aspect of the sound is learned, then copy errors or innovations during learning can result in passing down cultural changes over time. These are just a few ways in which sounds might be altered, and no two vocalizations are necessarily influenced in the same way by the same set of selective pressures.

In order to compare vocal repertoires among populations, we looked at several subspecies of the Marsh Wren. Marsh Wrens provide a natural experiment in vocal variation due to ecological and natural history differences among the subspecies. The five eastern North America subspecies we focused on are found in two distinct habitats (freshwater marshes and saltmarshes), and they exhibit three migratory patterns (resident, partially migratory, and fully migratory). Our first challenge was to describe and classify the call repertoire for Marsh Wrens. We identified seven discrete call types. Three of the seven calls varied in acoustic properties that were consistent with differences in either migratory pattern or habitat type. Surprisingly, we also found that four calls were more common in some subspecies than others and that the differences were greatest between habitat types. This variation in call production may indicate differences in behavior or timing of breeding among the subspecies with different ecologies. Our results suggest that while not all vocal signals are changing at the same rate or in the same way, differences in habitat type and migratory behavior may be related to the biggest differences in vocal behavior. Interestingly, the calls that showed the greatest differences were calls used in mate attraction and territory defense, while calls related to alarm or distress were similar across subspecies, natural history, and habitat type. This result suggests that sexual selection could be driving or reinforcing changes between populations with different ecologies.

In the future, we are excited to explore another unusual phenomenon that we report in this paper: the use of calls as embedded elements in song. Like most songbirds, Marsh Wren males sing during the breeding season to attract mates and defend territories. Unlike those of most songbirds, we found that, depending on the subspecies, 73-93% of male Marsh Wren songs contained embedded calls. Do embedded calls confer some additional message to the song? Does this behavior vary across the breeding season? Are there specific structural rules regarding the embedded call pattern within song? Stay tuned as we untangle the structural complexity and geographic variation in songs with embedded call elements in Marsh Wrens across the rest of their range. Does your study species use calls in a song-related context? If so, contact us at luttrell.sa@gmail.com—we would be excited hear about it!

AUTHOR BLOG: Understanding How Management Affects a Flagship Reed Bed Bird Species

Thomas Oliver Mérő

Linked paper: Reed management influences philopatry to reed habitats in the Great Reed-Warbler (Acrocephalus arundinaceus) by T.O. Mérő, A. Žuljević, K. Varga, and S. Lengyel, The Condor: Ornithological Applications 120:1, February 2018.

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A color-banded singing Great Reed Warbler male, April 2015.

Wetlands are inhabited by disproportionately large number of plants and animals and yet are among the most endangered habitats worldwide due to human-caused habitat loss and fragmentation. Ecologists and conservation biologists work hard on saving wetlands by using various techniques such as vegetation management (e.g. breaking up homogeneous reed beds), water regulation (e.g. maintaining a flood/drought cycle), or reintroduction of extinct species (e.g. cranes in the U.K.). Several recent studies have shown that the management of wetlands such as reed beds by controlling the water level and removing the vegetation by mowing, burning, or grazing can increase species richness and diversity; however, we know less about whether such management provides better conditions for survival and reproduction of single species whose presence is important to other species.

The Great Reed Warbler (Acrocephalus arundinaceus) is an Old World, long-distance migrant bird that breeds in reed habitats of the Western Palearctic and winters in sub-Saharan Africa. In central Europe, the Great Reed Warbler is a widespread breeder inhabiting almost all types of reed habitats (ponds, marshes, canals etc.). Great Reed Warblers arrive in mid-April from their wintering grounds and stay until the end of breeding season in late July.

We have studied the breeding ecology of Great Reed Warblers in northern Serbia for eight years. The region hosts a nice array of wetland habitat types, ranging from oxbows of the Danube to small and large canals, and from sand and clay mining ponds to marshes in natural depressions. For our work, we distinguished six types of reed habitats based on our own observations and information from local water management companies. The six types, which differ in their shape, size, vegetation cover, and water regime, are mining ponds, marshes, large canals, and three classes of small canals.

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Although large canals are preferred by large-winged, probably high-quality, males for nesting, this habitat type provides suboptimal conditions for breeding due to high brood parasitism by Cuckoos; therefore, this habitat type likely functions as an ecological trap.

These wetlands are managed by reed mowing and burning, which led us to wonder how reed management influences the birds and other wetland animals. Specifically, we were interested in whether and how management influences the survival and reproduction of Great Reed Warblers, a flagship species of lowland wetlands in central Europe. Reed management by burning and mowing offered a good opportunity to study the responses of Great Reed Warblers in each of the reed habitat types. For example, we recognized early on that larger-winged, presumably higher-quality, males tend to occupy reed habitats with little management and deep, stable water, which are typically found along large canals.

We color-banded all individuals (both adults and hatch-year birds) from the beginning of our study and regularly checked all reed beds every year during the nesting season to explore potential differences in survival and reproduction of birds in the six reed habitats. We were also curious to find out how reed management and water availability influence survival and reproduction. We first analyzed data on survival and encounter probability that were collected over seven breeding seasons (2009-2015).

We found that the encounter probability of birds banded as hatch-year birds was higher in reed habitats with shallower water, while that of those banded as adults was higher in reed habitats with deeper water. These opposite relationships between hatch-year birds and adults may indicate that experienced adults occupy qualitatively better habitats, similarly to large-winged males (mentioned above). When data were analyzed separately for the sexes, we found that the encounter probability of males depended on variation in reed management and in water depth. In contrast, for females, encounter probability depended only on water depth, i.e. encounter probability increased with water depth. Furthermore, most of the adults and hatch-year birds returned to the reed habitat that they had been occupying initially, indicating that Great Reed Warblers display unexpectedly high fidelity to the reed habitat type they hatched in or bred in before.

How do these results translate to management recommendations? We all want the best possible management for the birds we admire and study. Evidence found in our study showed that reed management by mowing and/or burning influences return rates of juveniles and adult males and females in different ways. These results suggest that in practice, spatially variable reed management should be applied and water with varying depths should be maintained to maximize the return rates of Great Reed Warblers. This is often easier said than done. However, the multitude of reed habitats in our study and the good working relationships we developed with water management authorities and other stakeholders will allow more detailed, experimental studies of the influence of management and the allocation of optimal combinations of management for the benefit of wetland birds.