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Environmental variability directly affects the prevalence of divorce in monogamous albatrosses

DOI:10.1098/rspb.2021.2112
Authors:
Francesco Ventura at Woods Hole Oceanographic Institution
Francesco Ventura
José P. Granadeiro at University of Lisbon
José P. Granadeiro
Paul Lukacs at University of Montana
Paul Lukacs
Amanda Kuepfer at Falklands Conservation
Amanda Kuepfer
  • Falklands Conservation
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Abstract

In many socially monogamous species, divorce is a strategy used to correct for sub-optimal partnerships and is informed by measures of previous breeding performance. The environment affects the productivity and survival of populations, thus indirectly affecting divorce via changes in demographic rates. However, whether environmental fluctuations directly modulate the prevalence of divorce in a population remains poorly understood. Here, using a longitudinal dataset on the long-lived black-browed albatross (Thalassarche melanophris) as a model organism, we test the hypothesis that environmental variability directly affects divorce. We found that divorce rate varied across years (1% to 8%). Individuals were more likely to divorce after breeding failures. However, regardless of previous breeding performance, the probability of divorce was directly affected by the environment, increasing in years with warm sea surface temperature anomalies (SSTA). Furthermore, our state-space models show that warm SSTA increased the probability of switching mates in females in successful relationships. For the first time, to our knowledge, we document the disruptive effects of challenging environmental conditions on the breeding processes of a monogamous population, potentially mediated by higher reproductive costs, changes in phenology and physiological stress. Environmentally driven divorce may therefore represent an overlooked consequence of global change.
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Research
Cite this article: Ventura F, Granadeiro JP,
Lukacs PM, Kuepfer A, Catry P. 2021
Environmental variability directly affects the
prevalence of divorce in monogamous
albatrosses. Proc. R. Soc. B 288: 20212112.
https://doi.org/10.1098/rspb.2021.2112
Received: 23 September 2021
Accepted: 3 November 2021
Subject Category:
Ecology
Subject Areas:
ecology
Keywords:
divorce, social monogamy, environment,
state-space model, seabird, albatross
Author for correspondence:
Francesco Ventura
e-mail: fraventura.92@gmail.com
Electronic supplementary material is available
online at https://doi.org/10.6084/m9.figshare.
c.5713071.
Environmental variability directly affects
the prevalence of divorce in monogamous
albatrosses
Francesco Ventura
1
, José Pedro Granadeiro
1
, Paul M. Lukacs
2
,
Amanda Kuepfer
3,4
and Paulo Catry
5
1
CESAM, Departamento de Biologia Animal, Faculdade de Ciências, Universidade de Lisboa, Campo Grande,
Lisboa 1749-016, Portugal
2
Wildlife Biology Program, Department of Ecosystem and Conservation Sciences, W. A. Franke College of Forestry
and Conservation, University of Montana, Missoula, MT 59812, USA
3
SAERI—South Atlantic Environmental Research Institute, Stanley, Falkland Islands FIQQ 1ZZ, UK
4
Environment and Sustainability Institute, University of Exeter, Penryn Campus, Penryn TR10 9FE, UK
5
MARE –Marine and Environmental Sciences Centre, ISPA –Instituto Universitário, Rua Jardim do Tabaco 34,
Lisboa 1149-041, Portugal
FV, 0000-0002-1584-2433; JPG, 0000-0002-7207-3474; AK, 0000-0002-3559-8802
In many socially monogamous species, divorce is a strategy used to correct for
sub-optimal partnerships and is informed by measures of previous breeding
performance. The environment affects the productivity and survival of popu-
lations, thus indirectly affecting divorce via changes in demographic rates.
However, whether environmental fluctuations directly modulate the preva-
lence of divorce in a population remains poorly understood. Here, using a
longitudinal dataset on the long-lived black-browed albatross (Thalassarche mel-
anophris) as a model organism, we test the hypothesis that environmental
variability directly affects divorce. We found that divorce rate varied across
years (1% to 8%). Individuals were more likely to divorce after breeding fail-
ures. However, regardless of previous breeding performance, the probability
of divorce was directly affected by the environment, increasing in years with
warm sea surface temperature anomalies (SSTA). Furthermore, our state-
space models show that warm SSTA increased the probability of switching
mates in females in successful relationships. For the first time, to our knowl-
edge, we document the disruptive effects of challenging environmental
conditions on the breeding processes of a monogamous population, potentially
mediated by higher reproductive costs, changes in phenology and physiologi-
cal stress. Environmentally driven divorce may therefore represent an
overlooked consequence of global change.
1. Background
Social monogamy is a widespread mating system, almost ubiquitous in birds,
shared by over 90% of avian species [1] and also present in some mammal
species in the orders Primates, Macroscelidea and Carnivora [2]. Different
species exhibit various degrees of fidelity to their mate, resulting in different
rates of maintenance of pair bonds, which is a function of the rates of widowing
but also of divorce [3,4]. Owing to intra-sexual competition, the choice of mate
is seldom unconstrained and many individuals in the population have to settle
with a sub-optimal partnership. Across a wide range of species, divorce was
found to be a strategy aimed at correcting for these sub-optimal partnerships,
resulting in an improvement of the reproductive success of one or both
members of the pair [4–6].
Divorce is often an adaptive behavioural mechanism driven by the
‘win–stay, lose–switch’information gathering process, in which measures of
previous breeding performance inform the decision of an individual to re-
mate with their old partner (stay) or find a new one (switch) [3,7,8]. Several
© 2021 The Author(s) Published by the Royal Society. All rights reserved.
... Many studies have shown that divorce may be adaptive (Culina, Lachish, & Sheldon, 2015), including in albatross species (Ventura et al., 2021). However, as Jeschke et al. (2007) pointed out, "adaptive divorce may in general be less common than usually assumed," and a diversity of divorce mechanisms may exist within a population. ...
... Despite the fact that females are the choosy sex in many species (Ventura et al., 2021), they have never been observed seeking extrapair copulations in this population (Jouventin et al., 2007). Hence, without information on the precise behavioral sequences that lead to divorce, it is difficult to conclude whether or not females choose to divorce because they are not limited by the availability of mates. ...
Causes and consequences of pair‐bond disruption in a sex‐skewed population of a long‐lived monogamous seabird
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Many animals form long‐term monogamous pair‐bonds, and the disruption of a pair‐bond (through either divorce or widowhood) can have significant consequences for individual vital rates (survival, breeding, and breeding success probabilities) and life‐history outcomes (lifetime reproductive success, life expectancy). Here, we investigated the causes and consequences of pair‐bond disruption in wandering albatross (Diomedea exulans). State‐of‐the‐art statistical and mathematical approaches were developed to estimate divorce and widowhood rates and their impacts on vital rates and life‐history outcomes. In this population, females incur a higher mortality rate due to incidental fishery bycatch, hence the population is male‐skewed. Therefore, we first posited that males show higher widowhood rates negatively correlated with fishing effort, and females have higher divorce rates because they have more mating opportunities. Furthermore, we expected that divorce can be an adaptive strategy, whereby individuals improve breeding success by breeding with a new partner of better quality. Finally, we posited that pair‐bond disruptions can reduce survival and breeding probabilities due to the cost of remating processes, with important consequences for life‐history outcomes. As expected, we show that males have higher widowhood rates than females and females have higher divorce rates in this male‐skewed population. However, no correlation was found between fishing effort and male widowhood. Secondly, contrary to our expectation, we found that divorce is likely non‐adaptive in this population. We propose that divorce in this population is caused by an intruder who outcompetes the original partner in line with the “forced divorce” hypothesis. Furthermore, we found a 16.7% and 18.0% reduction in lifetime reproductive success (LRS) only for divorced and widowed males, respectively, due to missing breeding seasons after a pair‐bond disruption. Finally, we found that divorced individuals are more likely to divorce again, but whether this is related to specific individual characteristics remains an important area of investigation.
View
... Sometimes, experienced breeders are forced to find a new partner (for example, after being widowed); however, theory predicts that choosing to divorce (when both partners survive but one or both choose a different partner for subsequent breeding attempts) may incur considerable cost (Choudhury, 1995;Ismar et al., 2010). Re-pairing (defined as a bird breeding with a new mate following divorce or partner death) is uncommon in longlived, monogamous birds, including many seabird species (Mercier et al., 2021;Ventura et al., 2021). High adult survival means seabirds are less likely to be widowed between seasons, and the fitness benefits of fidelity are widely reported in these taxa (Mills, 1973;Moody et al., 2005). ...
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In long‐lived monogamous species, the trigger of costly re‐pairing is not always clear. Limited research suggests that within‐pair behavioural compatibility may be an important driver of partnership success, as cooperation should be enhanced when pair members' decisions complement one another. Animals' decision‐making processes are influenced by personality traits – defined as individual differences in behaviour that are stable in time. Despite the potential for the personality trait ‘boldness’ to (a) directly impact individual willingness to re‐pair and (b) indirectly impact re‐pairing choices via reproductive success, there is currently little work exploring how re‐pairing decisions might be impacted by the pair members' personalities. Using a 13‐year dataset, we investigated whether within‐pair boldness and its relationship with breeding success explained re‐pairing patterns of black‐legged kittiwakes ( Rissa tridactyla ), breeding in two Arctic colonies. We found that pairs with dissimilar boldness levels were more likely to experience breeding failure and that failed pairs were more likely to re‐pair the following year. Despite this, only one colony displayed evidence of assortative mating by boldness, and there was no indication that re‐pairing impacted reproductive success the following season. Neither individual nor pair boldness directly influenced re‐pairing probability; however, in both colonies, re‐pairing birds chose partners that were slightly more similar to themselves in boldness than their previous mates. These results imply an indirect pathway by which poorer behavioural compatibility within pairs may lead to breeding failure and ultimately re‐pairing. Our findings highlight the importance of behavioural compatibility, and possibly personality, in mitigating sexual conflict and its population‐specific drivers.
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... This can reduce selection for migration (Winger et al. 2018), causing migratory bird populations to become sedentary (Pulido & Berthold 2010), while also increasing the duration of breeding seasons for resident species (Halupka & Halupka 2017). Our results suggest that these behavioural changes will dampen sexual selection, in line with previous studies showing that higher temperatures (García-Roa et al. 2020) and aseasonal climates (Botero & Rubenstein 2012;Ventura et al. 2021) can modify competition for mates and mating opportunities. Nonetheless, the precise impacts of climate change on mechanisms of sexual selection and their adaptive implications (Slatyer et al. 2012;Lumley et al. 2015;Parrett & Knell 2018;Wanders et al. 2023) are hard to predict because lengthening warm seasons have variable and species-speci c effects on reproductive phenology in both plants (Linderholm 2006) and animals (Halupka & Halupka 2017;Harvey et al. 2023). ...
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... The role of environmental heterogeneity in divorce has largely been neglected in empirical studies, but assessing this would test our prediction that populations with high levels of environmental heterogeneity have high divorce rates. Indeed, a recent study has documented the importance of temporal environmental heterogeneity for divorce in albatross (Thalassarche melanophris; Ventura et al. 2021). Our prediction that populations that divorce more are expected to have lower mean fitness ( fig. ...
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Despite widespread interest in the evolution and implications of monogamy across taxa, less attention—especially theoret-ical—has been paid toward understanding the evolution of divorce (ending a socially monogamous pairing to find a new partner). Here, we develop a model of the evolution of divorce by females in a heterogeneous environment, where females assess territory quality as a result of their breeding success. Divorce results in females leaving poor territories disproportionally more often than good territories, while death of a partner occurs independent of territory quality, giving an advantage to divorce. Increasing environmental heterogeneity, a decreasing benefit of pair experience, and moderate survival rates favor the evolution of higher divorce rates, even in the absence of variance in individual quality and knowledge of available territories. Imperfect information about territory quality constrains the evolution of divorce, typically favoring divorce strategies that remain faithful to one’s partner whenever successful reproduction occurs. Our model shows how feedbacks between divorce, widowhood, and the availability of territories are intricately linked in determining the evolutionary advantage of divorce. We detail testable predictions about populations that should be expected to divorce at high rates.
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... Temperature has increased at more than double the global average warming rate over the past 50 years, and annual precipitation has declined on several islands (le Roux 2008, le Roux & McGeoch 2008a. This change in temperature, specifically, might negatively affect Wandering Albatrosses, where high sea surface temperatures are detrimental to foraging success, and therefore adult survival in the breeding season (Pardo et al. 2017, see also Ventura et al. 2021 where increased sea surface temperatures led to higher divorce rates in Blackbrowed Albatrosses Thalassarche melanophris), which could alter where they nest in future. Altitudinal shifts in nesting sites could be a possibility, both as a result of increasing temperatures and the shift in vegetation as a result of temperature changes. ...
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Several factors may drive bird nest‐site selection, including predation risk, resource availability, weather conditions, and interaction with other individuals. Understanding the drivers affecting where birds nest is important for conservation planning, especially where environmental change may alter the distribution of suitable nest sites. This study investigates which environmental variables affect nest‐site selection by the Wandering Albatross Diomedea exulans, the world’s largest pelagic bird. Here, wind characteristics are quantitatively investigated as a driver of nest‐site selection in surface nesting birds, in addition to several topographical variables, vegetation, and geological characteristics. Nest locations from three different breeding seasons on sub‐Antarctic Marion Island were modelled to assess which environmental factors affect nest‐site selection. Elevation was the most important determinant of nest‐site selection, with Wandering Albatrosses only nesting at low elevations. Distance from the coast and terrain roughness were also important predictors, with nests more generally found close to the coast and in flatter terrain, followed by wind velocity, which showed a hump‐shaped relationship with the probability of nest occurrence. Nests occurred more frequently on coastal vegetation types, and were absent from polar desert vegetation (generally above ~ 500 m elevation). Of the variables that influence Wandering Albatross nest location, both vegetation type and wind characteristics are likely to be influenced by climate change, and have already changed over the last 50 years. As a result, the availability of suitable nest sites needs to be considered in light of future climatic change, in addition to the impacts that these changes will have on foraging patterns and prey distribution. More broadly, these results provide insights into how a wide range of environmental variables, including wind, can affect nest‐site selection of surface nesting seabirds.
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... SSTA, in particular, has previously been found to affect demographic aspects of black-browed albatross and other seabirds in the Falkland Islands (e.g. breeding success, breeding probability (Ventura et al., 2021a), breeding pair divorce rates (Ventura et al., 2021b); chick provisioning rates, and chick growth (Quillfeldt et al., 2007(Quillfeldt et al., , 2010). Monthly NPP and SSTA were calculated for January and February in the core foraging area (50% UD) of breeding birds tracked between 2008 and 2019 during early breeding (October-December; Ventura et al., 2021a; Figure 1). ...
Prey-switching to fishery discards does not compensate for poor natural foraging conditions in breeding albatross
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Fishery discards supplement food for many seabirds, but the impacts of declining discards are poorly understood. Discards may be beneficial for some populations but have negative impacts by increasing bycatch risk or because they are junk-food. The Falkland Islands support > 70% of global black-browed albatross Thalassarche melanophris populations, which feed on discards. However, the effect of discards on population demographics, and implications of fishery management changes, are unknown. We analysed stomach contents of black-browed albatross chicks across eight breeding seasons (2004–2020) from New Island, Falkland Islands, to assess variation in discard consumption and how this relates to foraging conditions and breeding success. Across years, 68%–98% of samples contained natural prey, whilst 23%–88% of samples contained fishery discards. Discard consumption was positively related to fishery catches of hoki Macruronus magellanicus and sea surface temperature anomalies SSTA (°C), and negatively related to breeding success. These results suggest a diet-switching behaviour for Falkland Islands albatrosses, whereby birds switch from preferred natural prey to suboptimal discards when environmental conditions, and hence natural feeding opportunities, are unfavourable. Crucially, this study highlights that fishery discards do not compensate for poor natural foraging conditions for breeding albatrosses in the long term.
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... As an example, European blackbirds (Turdus merula) increase their divorce rate when they are in low quality nesting sites (Desrochers & Magrath, 1993). Recently, a study on a long-lived seabird species (black-browed albatross, Thalassarche melanophris) has demonstrated for the first time empirical evidence that the prevalence of divorce can be directly modulated by environmental temporal variability via sea surface temperature variations (Ventura et al., 2021). In lower quality years, with warmer sea surface temperature anomalies, the probability of switching mate increased in albatross populations. ...
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Mate fidelity and divorce in monogamous birds
Chapter
  • May 1996
Some birds mate for life, while others have many partners. In this book, fourteen studies are brought together to compare different partnership patterns from ecological and evolutionary perspectives. The subjects have been chosen to include the same species living in different habitats (Sparrowhawks) and at different population densities (Great Tits). There are comparisons between closely related species (Mute Swans and Bewick's Swans). The studies span the globe and the behavioural gradient, from Iceland's strictly monogamous Whooper Swans to Australia's sexually promiscuous Splendid Fairy-wrens. In all cases, sexual and social relationships strongly influence a bird's survival and breeding success.
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Monogamy in the Sparrowhawk
Chapter
  • May 1996
Some birds mate for life, while others have many partners. In this book, fourteen studies are brought together to compare different partnership patterns from ecological and evolutionary perspectives. The subjects have been chosen to include the same species living in different habitats (Sparrowhawks) and at different population densities (Great Tits). There are comparisons between closely related species (Mute Swans and Bewick's Swans). The studies span the globe and the behavioural gradient, from Iceland's strictly monogamous Whooper Swans to Australia's sexually promiscuous Splendid Fairy-wrens. In all cases, sexual and social relationships strongly influence a bird's survival and breeding success.
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Article
  • Jun 2021
In long-lived marine top-predators with delayed sexual maturity such as seabirds, adult survival is predicted to drive population dynamics. Major knowledge gaps exist for the cryptic sub-adult stages of the population. Yet as the oceans undergo dramatic change, investigating the trends of top-predator populations and their responses to environmental variability is key for a process-based understanding of climate change. Using integrated population models based on a longitudinal data set spanning nearly 2 decades, we investigated the demographic rates and environmental drivers shaping the dynamics of a longevous marine top-predator population, the black-browed albatross Thalassarche melanophris in the Falklands. We quantified the dynamics of the whole population, including its cryptic sub-adult stages, and examined the effects of candidate environmental covariates on adult survival and productivity parameters. We found that high survival rates of both adults and juveniles are the main contributors to the growth of this albatross population, the only one that is increasing in the South Atlantic. The breeding parameters were affected by environmental fluctuations through bottom-up processes, with a negative effect of higher sea surface temperatures and a positive effect of wind intensity. The relatively constant adult survival was influenced by deeper ecosystem changes, captured by large-scale indices (Southern Annular Mode). Approximately half of the total population is composed of sub-adults, and the population dynamics are highly sensitive to changes in juvenile survival; addressing current knowledge gaps in these cryptic life-history stages is therefore a conservation goal of primary importance.
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adehabitatHR: Home Range Estimation
Article
  • Jul 2015
A collection of tools for the estimation of animals home range.
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