Article

Decreased selectivity during mate choice in a small-sized
population of a long-lived seabird

Joël Bried, Malvina Andris, Marie-Pierre Dubois and Philippe Jarne

J. Bried (https://orcid.org/0000-0001-7377-4304) ✉ (joelbried@yahoo.com) and M. Andris, Centro Okeanos, MARE (Marine and Environmental Sciences Centre), Depto de Oceanografia e Pescas, Univ. dos Açores, Horta, Açores, Portugal. JB also at: 8 Avenue de la Reine Nathalie, Biarritz, France.
– M.-P. Dubois and P. Jarne, CEFE UMR 5175, CNRS – Univ. de Montpellier – Univ. Paul-Valéry Montpellier – IRD – EPHE, Montpellier Cedex 5, France.

Journal of Avian Biology
2021: e02837
doi: 10.1111/jav.02837

Subject Editor: Paulo Catry
Editor-in-Chief: Jan-Åke Nilsson
Accepted 5 September 2021

As biparental care is crucial for breeding success in Procellariiformes seabirds (i.e. albatrosses and petrels), these species are expected to be choosy during pair formation. However, the choice of partners is limited in small-sized populations, which might lead to random pairing. In Procellariiformes, the consequences of such limitations for mating strategies have been examined in a single species. Here, we studied mate choice in another Procellariiforme, Bulwer's petrel *Bulweria bulwerii*, in the Azores (ca 70 breeding pairs), where the species has suffered a dramatic population decline. We based our approach on both a 11-year demographic survey (capture-mark-recapture) and a genetic approach (microsatellites, n=127 individuals). The genetic data suggest that this small population is not inbred and did not experience a genetic bottleneck. Moreover, pairing occurred randomly with respect to genetic relatedness, we detected no extrapair parentage (n=35 offspring), and pair fecundity was unrelated to relatedness between partners. From our demographic survey, we detected no assortative mating with respect to body measurements and breeding experience and observed very few divorces, most of which were probably forced. This contrasts with the pattern previously observed in the much larger population from the Selvagens archipelago (assortative mating with respect to bill size and high divorce rate). We suggest that the Bulwer's petrels from the Azores pair with any available partner and retain it as long as possible despite the fact that reproductive performance did not improve with pair common experience, possibly to avoid skipping breeding years in case of divorce. We recommend determining whether decreased choosiness during mate choice also occurs in reduced populations of other Procellariiform species. This might have implications for the conservation of small threatened seabird populations.

Keywords: body size, *Bulweria bulwerii*, inbreeding, mate choice, microsatellite markers, small populations

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Introduction

Due to constraints resulting from oviparity and the necessity to forage at sea while
breeding on land, obligate biparental care and social monogamy have evolved in

© 2021 The Authors. Journal of Avian Biology published by John Wiley & Sons Ltd on behalf of Nordic Society Oikos

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seabirds (Lack 1968), and mate choice is supposed to have a crucial importance for successful breeding in these species (Bried and Jouventin 2002). The order Procellariiformes (i.e. albatrosses and petrels) is a group of seabirds characterized by very low fecundity (a single egg per breeding attempt without replacement in case of failure), deferred sexual maturity and high life expectancy (Warham 1990). During incubation and chick-rearing, adult Procellariiformes can perform long (i.e. several days) foraging trips and biparental investment is high (several months from egg laying until the chick fledges; Warham 1990). Although 1) choosiness during mate choice should be expected under these conditions, and 2) pair formation can take several years in these species (reviewed by Bried and Jouventin 2002), random mating seems to occur in several Procellariiform populations or species (at least, with respect to the criteria that were considered; Supporting information).

This might be explained by strong competition for nests and/or mates, resulting from insufficient nest supply or a biased sex ratio, which may constrain social mate choice (Barbraud and Jouventin 1998, Jouventin and Bried 2001) and might also affect genetic monogamy (Jouventin et al. 2007, Bried et al. 2010). Indeed, constraints on social mate choice may result in the existence of extra-pair paternities (EPPs) (Sullivan 1994), enabling females to adjust the choice of their social male through extra-pair copulations (EPCs) and/or males that failed to obtain a nest/mate to avoid missing a breeding year by copulating with paired females (Jouventin et al. 2007, Bried et al. 2010). Although low EPP rates are expected in long-lived species with obligate biparental care (Griffith et al. 2002), EPPs have been observed in Procellariiform populations under such circumstances (Jouventin et al. 2007, Young et al. 2008, Bried et al. 2010).

However, these issues were mostly addressed in reasonably large populations (at least several hundred pairs) of species that are unlikely to have experienced demographic or genetic bottlenecks. In some Procellariiform populations with low genetic variability, EPP rates can be surprisingly high (Huyvaert et al. 2006), because females may seek EPCs in order to avoid inbreeding (Tregenza and Wedell 2000), or because males might be tolerant to EPCs performed by males to which they are genetically related (Huyvaert and Parker 2010). Alternatively, if genetic similarity between males is high, exerting choosiness during mate choice and seeking EPCs should not yield significant benefits to females (Øigarden et al. 2010), and EPP rates should be low (Petrie and Kempenaers 1998). Procellariiformes show low divorce rates (Bried and Jouventin 2002), even when constraints on social mate choice are important (Jouventin and Bried 2001, Jouventin et al. 2007, Bried et al. 2010). As in many other long-lived bird species, divorce is generally associated with poor reproductive performance due to e.g. incompatibility between the partners (the 'incompatibility' hypothesis predicts that pairs with little common breeding experience and poor reproductive performance should be most likely to divorce), or with a higher probability to breed successfully with a new mate ('better option' hypothesis; for a review of

the hypotheses concerning divorce see Choudhury 1995; for a review of the factors of divorce in seabirds see Bried and Jouventin 2002).

To the best of our knowledge, the consequences of a low number of potential sexual partners for social mate choice and genetic mating system in Procellariiform species that have experienced a demographic bottleneck were examined only in Monteiro's storm-petrel *Hydrobates monteiroi*, a species which suffered a dramatic decline in the 16th century (Nava et al. 2017). Given, however, that Monteiro's storm-petrel is endemic to the Azores, Nava et al. (2017) could not compare their results with data from larger populations of this species.

Bulwer's petrel *Bulweria bulwerii* offers an excellent opportunity to fill this gap. This species has a pantropical/subtropical distribution. In the Atlantic, it reaches the northern limit of its breeding distribution in the Azores (Megyesi and O'Daniel 2020). Bulwer's petrels were abundant when the Portuguese settled in this archipelago at the end of the 15th century. However, they were extirpated from the main islands following the introduction of predatory mammals by man (Monteiro et al. 1996b). Currently, their only known breeding locations in the Azores are the mammal-free Vila, Baixo and Praia islets, with ca 50 breeding pairs on Vila islet (Monteiro et al. 1999, J. Bried unpubl.) and about 20 on Baixo and Praia islets (Monteiro et al. 1999). The mating strategy of Bulwer's petrel was studied in the large population (between 5000 and 11 000 pairs, Mougin 1989a, Ramírez et al. 2008) from Selvagem Grande (also situated in the northern subtropical Atlantic, about 1200 km south-east from the Azores, Fig. 1) by Mougin (1989b, 1990, 1996), who found that birds paired assortatively based on bill size, and that divorce was mostly caused by the absence of at least one of the former partners, which had taken a 'sabbatical' year, and by habitat instability. However, Mougin did not conduct any genetic study.

In the northern subtropical Atlantic, including in the Azores, Bulwer's petrels return from the sea to their colonies from mid- to late April onwards, and must form their pair bonds before undertaking a pre-laying exodus at sea (ca four weeks, Nunes and Vicente 1995, Megyesi and O'Daniel 2020) during which egg formation occurs in females while males replenish their body reserves prior to incubation (Warham 1990). Thereafter, laying occurs, in late May-early June (Jouanin et al. 1979, Mougin et al. 1992, Monteiro et al. 1996a, V. C. Neves and J. Bried unpubl.). In small populations such as that from Vila islet, the number of potential mates is limited, so that assessing their quality should not be too time-consuming and/or more time might be devoted to the evaluation of each individual, a priori allowing greater choosiness than in a large population (Oh and Badyaev 2010). However, phenotypic and genotypic variability may be lower in small populations than in large ones, making it difficult to assess individual quality. In addition, since all individuals do not return simultaneously ashore during the pre-laying period and given the duration of the pre-laying exodus, birds may not have much time to obtain a partner. In addition, not only
<figure><img src="image_3.png" /><figcaption>Figure 1. Situation of Vila islet in the Azores archipelago. Situation of the Azores (with Vila islet off Santa Maria island), Madeira and Selvagem Grande in the north-eastern subtropical Atlantic.</figcaption></figure>

potential social partners may be available at the colony only
during a short period of time but also only a small fraction of
them (that is, very few individuals in absolute numbers) may
be available per unit of time. Under these conditions, birds
might actually face non-negligible constraints when search-
ing for a suitable partner, and decreased choosiness associated
with a low EPP rate might be expected (above).

Therefore, the aims of this study were to 1) determine if a
loss of genetic variability was associated with the demographic
bottleneck experienced by Bulwer's petrels in the Azores, 2)
investigate whether the Bulwer's petrels from Vila islet chose
their social mates on the basis of phenotypic (bill dimensions,
body size, previous breeding experience) or genetic (related-
ness) characteristics, 3) determine if EPPs occurred at this
location, 4) determine whether mate retention allows an
improvement of reproductive performance in the Bulwer's
petrels from Vila islet, as it does in other long-lived bird spe-
cies (reviewed by Bried and Jouventin 2002), and 5) identify
the correlates of divorce and the consequences of the loss of
the previous mate. These issues were addressed based on both
a genetic (microsatellite) study and a demographic survey
conducted over 11 years.

Methods

Fieldwork was conducted on Vila islet (36°55′N, 25°10′W, 0.08 km²), off Santa Maria island, Azores archipelago (Fig. 1). Bulwer's petrel is a small (mean body mass 98 g, Monteiro et al. 1996a) seabird. Like all petrels (Warham 1990), it is socially monogamous and has a long breeding cycle (on average 106 days from laying until chick departure to sea) during which both parents incubate their single egg and feed the chick (Megyesi and O'Daniel 2020). On Vila islet, breeders return to the colony in late April–early May, laying occurs in early June, and chicks hatch in late July and fledge in late September (Monteiro et al. 1996a, V. C. Neves and J. Bried unpubl.).

Demographic and morphometric data: collection
and processing

Our demographic survey was conducted from 2002 to 2012
included. Birds were monitored each year using capture-
mark-recapture. Since Bulwer's petrels return to and leave
the colonies only at night (Megyesi and O'Daniel 2020,
authors' pers. obs.), adults were captured by hand in their nests during both incubation and daytime to avoid mistaking prospecting individuals that visit the colony and can enter burrows (J. Bried unpubl.) for the actual breeders, and therefore for the chicks' social parents. Such mistakes would have led us to overestimate EPP rates. The two partners of each pair were captured, ringed for identification or identified from their ring number, and measured (wing length using a stopped ruler to the nearest mm; tarsus length, culmen length and bill depth at the gonys using a vernier caliper to the nearest 0.1 mm). Since Mougin (1989b) found that the Bulwer's petrels from Selvagem Grande paired assortatively based on a bill size index defined as the product of culmen length by bill depth at the gonys, we also calculated a bill size index using the same definition. All measurements were taken by JB during incubation or early chick-rearing, allowing controlling for remige abrasion stage. However, a single parameter may be insufficient to reflect body size (Rising and Somers 1989) when checking for assortative mating by size. Therefore, we performed a principal component analysis on wing length, tarsus length and culmen length, using the first component (PC1 scores; Axis 1 explained 50.8% of the variance) as an indicator of overall body size (Chastel et al. 1995). All the adults measured in our study colony (n=266 individuals) were included in the analysis.

Nesting cavities were marked with individual numbers, enabling us to identify which pair was breeding in a given nest. Chicks were ringed before fledging, allowing to estimate the reproductive performance of each pair. Given the small size of our study population, all accessible nests (that is, 85-90% of the total estimated number of nests on the islet) were included in our monitoring.

## Genetic data: collection and processing

Blood samples were collected from adults upon their first capture in 2002, 2003 and 2004. For the reasons mentioned above, capturing adults during the daytime also prevented us from overestimating EPP rates after wrongly assigning social paternity to non-breeding prospectors. Chicks were sampled a few days after hatching. In order to increase sample size, we also took tissues from dead embryos in those eggs that had failed to hatch.

50-100 µl of blood were taken from the tarsal vein of each live individual (adult or chick), using disposable needles and capillary tubes. Muscle, liver or down samples were collected from seven dead embryos. Blood and tissue samples were stored under the conditions described in Bried et al. (2010).

We obtained samples from 91 adults, 30 chicks and seven dead embryos. After taking into account the adults that reunited with their former partner, divorced, died or became widowers between 2002 and 2004, this represented 30 full families (18 with one chick, five with a dead embryo, five with two chicks sampled over two different years, two with one chick plus one dead embryo), one family involving a chick and its social father, plus 32 adults (12 pairs and eight

individuals whose partner was not identified) whose egg was infertile or had disappeared when we sampled the chicks.

We extracted bird DNA using the QIAmp Tissue Kit (QIAGEN). Eleven microsatellite loci (autosomal loci Bb2, Bb3, Bb7, Bb10, Bb12, Bb20, Bb21, Bb22, Bb23, Bb25, plus the sex-linked Bb11, Molecular Ecology Resources Primer Development Consortium 2010) were amplified by polymerase chain reaction (PCR). PCRs were multiplexed for three subsets of loci (Bb2, Bb7, Bb20 and Bb22; Bb10, Bb11, Bb12, Bb21 and Bb23; Bb3 and Bb25) in 10 µl final volume including 0.2 µM of each primer and 1 µl of genomic DNA and using the QIAGEN multiplex PCR kit. PCRs were conducted using the protocol described in Molecular Ecology Resources Primer Development Consortium (2010).

PCR products were run in the same groups as for PCRs. For each group, three µl of diluted PCR products (1/80) were pooled in 15 µl of deionized formamide and 0.2 µl GeneScan-500 LIZ size standard and analysed on an ABI 3130 Genetic Analyser.

Genotypes were analysed using GeneMapper 4.0 (Applied Biosystems). Each profile was analysed by an observer who was unaware of family relationships. The same observer repeated the analyses after 4-5 days under the same conditions, except that individuals were processed in a different order. The matching rate concerning each genotype for each allele between the two sessions was 100%. To ensure the reliability of our results, we re-extracted DNA from 25 individuals, redid PCRs and ran the PCR products again. Genotype analyses yielded the same results as after the first DNA extraction. Since Bulwer's petrels show very weak sexual size dimorphism (Mougin 1989b, see also Results), 118 adults (57 males, 61 females), including those that were genotyped, plus the offspring from 2002 to 2004 included, were sexed using molecular methods (Fridolfsson and Ellegren 1999). The sex of 48 other adults (18 males, 30 females), including some chicks that later recruited into the breeding population, was inferred from that of their partner for which molecular sexing had been conducted.

## Checking for the existence of a genetic bottleneck

To check if the demographic bottleneck experienced by Bulwer's petrels in the Azores was associated with a genetic bottleneck, we used the BOTTLENECK software, which relies on the method of Cornuet and Luikart (1996) and allows detecting recent genetic bottlenecks using allelic frequencies. The observed heterozygosity is compared with the heterozygosity expected under mutation-drift equilibrium given the number of alleles present in the population. An excess of heterozygosity is generally expected after a bottleneck, whereas a deficit is expected in growing populations. For microsatellites, however, it remains unclear which model of mutation is the most appropriate (Jarne and Lagoda 1996, Goldstein and Schlötterer 1999). For this reason, we conducted the tests (after excluding Locus Bb11) assuming the stepwise mutation model (SMM), the infinite allele model (IAM) and the two-phase mutation model (TPM).
## Mate choice criteria: assortative mating and genetic relatedness between pair mates

When testing if there was an assortative mating based on body measurements or structural body size (PC1 scores), we used two methods. First, we considered the pairs that were observed each year and we analysed our study years separately, after conducting generalized linear models (GLMs) or Spearman rank correlations, according to whether or not the conditions for GLMs were met (that is, whether or not model residuals were normally distributed, Kéry and Hatfield 2003). Second, we considered all the sexed pairs that were observed in our study together. In this situation, however, a given individual could be involved in several pair bonds (after e.g. the death of its former partner and/or a divorce). To overcome this problem, we used the MIXED procedure of SAS (with the Kenward-Roger degrees of freedom method, SAS Inst. 2020), an equivalent of generalized linear mixed models which allows accounting for the correlations between observations concerning the same individual, can use data from individuals for which there are missing observations, allows within-individual effects to consist of continuous variables and to vary for the same individual, and analyses the data in their original form. To do this, we considered female (male) identity as a random effect.

To determine whether pairing occurred with respect to previous breeding experience, we checked if male experience (defined as the number of previous breeding attempts) was correlated with female experience. We also determined whether or not inexperienced individuals (i.e. first-time breeders) were more likely to form pair bonds with inexperienced partners than were experienced individuals (i.e. individuals known to have bred in the past) upon re-mating.

Relatedness between social partners was estimated using Moment Estimates of Relatedness (MER) (Wang 2002; ver. 3 downloadable from <www.zoo.cam.ac.uk/ioz>), after excluding the sex-linked locus Bb11. To test whether pairing occurred at random with respect to genetic relatedness, we compared the relatedness of pair mates with that of male-female pairs drawn at random using a resampling procedure implemented in RESAMPLING PROCEDURES ver. 1.3 (Howell 2001), to account for non-independence of individual pairs. The procedure was repeated 5000 times.

## Extra-pair parentage, mate retention, correlates and consequences of divorce

To conduct parentage analyses, we compared chick genotypes with those of their social parents, and we excluded paternity (maternity) when the genotype of a chick mismatched that of its social father (mother) at two loci at least. A single mismatch between offspring and parental genotypes was interpreted as a mutation.

Only birds known to have made at least one breeding attempt in the past were used when calculating mate fidelity rates and determining the causes of divorce. Mate fidelity was defined as 1 minus the probability of divorce, the latter parameter being the total number of divorces divided by the

total number of pair × years when both previous partners survive from one year to the next during the study period (Black 1996).

Because the probabilities of divorcing and fledging a chick can be considered as binary (yes/no) variables, we performed logistic regressions to determine which factors (if any) influenced divorce and reproductive performance, respectively. Since we had several years of data concerning mate retention and reproductive performance for many pairs, we performed logistic regressions for repeated measures (GENMOD procedure, binomial distribution, logit link; SAS Inst. 2020) to determine whether 1) the probability of divorce depended on pair common breeding experience (i.e. the number of breeding attempts made by a pair before divorcing or reuniting), previous reproductive performance and/or genetic relatedness between mates, and 2) reproductive performance depended on pair common breeding experience and genetic relatedness between mates. We used the ‘repeated’ statement of GENMOD, which allows an unequal number of measures. Given that in long-lived species with obligate biparental care like petrels (Warham 1990), both sexes should exert choosiness during mate choice (reviewed by Bried and Jouventin 2002) and initiate divorce (Birkhead and Møller 1996), it seemed reasonable to consider pairs as ‘functional’ units independent from each other, and we controlled for non-independence between social pair mates using pairs as the ‘repeated’ subject. When determining if the probability of divorce depended on previous reproductive performance and pair common breeding experience, our small sample size prevented us from controlling for relatedness between pair mates. When determining if the reproductive performance of newly formed pairs depended on the previous breeding experience of each of the new partners, and given that some individuals were involved in several pair bonds, we also used the GENMOD procedure. Results from logistic regressions with repeated measures conducted using GENMOD were obtained from the models using generalized estimating equations (GEE). When using GEEs, the mean response depends on the independent variables and the parameter estimates describe the effects of the explanatory variables on the population (unlike generalized linear mixed models, which produce conditional estimates). For the sake of clarity, the methodologies used to address the main objectives of this study concerning social mate choice and divorce are also presented in Table 1.

## Specifications concerning the statistical analyses

When determining the costs of widowhood in terms of missed breeding years, it must be noted that some individuals could skip several years. To avoid a bias in the distribution of missed breeding years due to individuals forming new pair bonds quickly after losing their previous mate, the individuals whose partner was not recaptured after 2007 (i.e. five years before the end of our survey) were not considered.

All tests were two-tailed unless otherwise stated, and probability levels < 0.05 were considered significant.
<table><caption>Table 1. Methodology used to address our main questions concerning social mate choice, reproductive performance and the correlates of divorce, and qualitative outline of the results obtained.</caption><thead><tr><th>Data considered</th><th>Analytical methodology</th><th>Qualitative results</th></tr></thead><tbody><tr><td>Assortative pairing</td><td>GLM or Spearman rank correlation</td><td>No assortative pairing</td></tr><tr><td>Measurements of pair mates, each year considered separately</td><td>MIXED procedure</td><td>No assortative pairing</td></tr><tr><td>Measurements of pair mates, all sexed pairs observed during our study</td><td>Spearman rank correlation</td><td>No assortative pairing</td></tr><tr><td>Previous breeding experience of pair mates</td><td>Resampling procedure</td><td>Random pairing</td></tr><tr><td>Pairing with respect to genetic relatedness</td><td>Logistic regression for repeated measures (GENMOD procedure, GEE estimates)</td><td>No effect of pair common experience and no effect of pair fate</td></tr><tr><td>Coefficients of genetic relatedness between pair mates versus all other theoretically possible male × female pairs</td><td>Spearman rank correlation</td><td>No significant correlation</td></tr><tr><td>Correlates of reproductive performance: did reproductive performance depend on pair common experience, pair fate (i.e. partners ended up divorcing or did not divorce) and genetic relatedness between pair partners?</td><td>Logistic regression for repeated measures (GENMOD procedure, GEE estimates)</td><td>No effect of previous reproductive performance and no effect of pair common experience</td></tr><tr><td>Probability of fledging a chick ~ pair common experience + pair fate</td><td>Mann-Whitney U</td><td>No significant difference</td></tr><tr><td>Did pair fecundity depend on the genetic relatedness between partners?</td><td>Wilcoxon matched pairs signed rank test</td><td>No improvement in reproductive performance</td></tr><tr><td>Correlates of divorce: did the probability of divorce depend on previous reproductive performance, genetic relatedness between pair partners and pair common experience?</td><td>Wilcoxon matched pairs signed rank test</td><td>No improvement in reproductive performance</td></tr><tr><td>Probability of divorce ~ previous reproductive performance + pair common experience</td><td>Logistic regression for repeated measures (GENMOD procedure, GEE estimates)</td><td>No effect of previous reproductive performance and no effect of pair common experience</td></tr><tr><td>Relatedness coefficients between pair mates in pairs that divorced versus pairs that did not divorce</td><td>Mann-Whitney U</td><td>No significant difference</td></tr><tr><td>Consequences of divorce in terms of reproduction</td><td>Wilcoxon matched pairs signed rank test</td><td>No improvement in reproductive performance</td></tr><tr><td>Reproductive performance during the first breeding attempt with the new mate versus last year before divorcing</td><td>Wilcoxon matched pairs signed rank test</td><td>No improvement in reproductive performance</td></tr><tr><td>Reproductive performance during the second breeding attempt with the new mate versus during the first breeding attempt</td><td>Wilcoxon matched pairs signed rank test</td><td>No improvement in reproductive performance</td></tr></tbody></table>

We presented the results from logistic regressions and GLMs using full models, that is, incorporating all the independent variables to be tested and removing non-significant interactions (Whittingham et al. 2006). To determine the power of some tests (i.e. the probability to avoid a type II error given our data), power analyses were conducted using GPOWER (Faul and Erdfelder 1992). Means are given ± SD, unless otherwise stated.

# Results

## Population genetic structure: did a genetic bottleneck occur?

The results concerning the 91 adult Bulwer's petrels that were successfully genotyped at the 11 loci (except one individual at locus Bb7) are given in Molecular Ecology Resources Primer Development Consortium (2010) and, for allele frequency distribution, in Supporting information. In brief, we detected two to eight alleles per locus, no significant linkage disequilibrium and no significant inbreeding.

In adults, a possible excess of heterozygosity was found using the IAM (one-tailed Wilcoxon sign rank test: $p=0.012$, but sign test: $p=0.197$), but not under the SMM and the TPM (same tests, all $p > 0.18$). Overall, there was

no evidence of a genetic bottleneck when considering allele frequencies.

## Do Bulwer's petrels choose their social partners based on body measurements, genetic relatedness or previous breeding experience?

### All pairs

We found no significant sex differences concerning wing length and tarsus length (Wilcoxon rank sum test, both $p > 0.11$; power to detect a small effect size [$ES=0.2$] $> 0.23$; power to detect a medium ES [$ES=0.5$] $> 0.87$; power to detect a large ES [$ES=0.8$] $> 0.99$). However, males had significantly longer culmens than females (21.8 ± 0.6 mm, $n=72$, versus 21.2 ± 0.7 mm, $n=86$; Wilcoxon rank sum test, $z=4.93$, $p < 0.0001$) and their bills were also deeper at the gonys (7.9 ± 0.3 mm, $n=67$, versus 7.5 ± 0.2 mm, $n=73$; Wilcoxon rank sum test, $z=7.52$, $p < 0.0001$; note that sample sizes do not correspond to those mentioned in the Methods because we included the sexed chicks that later returned as adults).

When considering each of our study years separately, we found no assortative mating based on univariate measurements (GLM and Spearman rank correlations, all $p > 0.06$) or on the bill size index (GLM, all $p > 0.36$). No assortative mating on the basis of overall body size was detected either (GLM, all $p > 0.1$), except in 2004 when we found a positive correlation
between the PC1 scores of males and those of their female partners ($F_{1,23}=4.79, p=0.039$; Supporting information for power analyses). When we considered all the sexed pairs we observed during our study, we also failed to observe significant correlations between male and female measurements, regardless of whether female identity or male identity was chosen as a random effect (MIXED procedure, n=80-97 pairs, depending on the considered measurement, all $p > 0.097$).

Pairing in Bulwer's petrels did not occur on the basis of genetic relatedness either (resampling test, means: 2002: $t=-0.88, p=0.55$, ES=0.334, power to detect such an effect size if true=0.224; 2003: $t=-0.75, p=0.60$, ES=0.276, power=0.255; 2004: $t=-0.53, p=0.66$, ES=0.194, power=0.168; variances: 2002: $t=-0.84, p=0.52$, ES=0.316, power=0.205; 2003: $t=0.30, p=0.81$, ES=0.110, power=0.081; 2004: $t=0.46, p=0.71$, ES=0.169, power=0.139).

## Newly formed pairs

We found no assortative mating based on body parts measurements and on structural body size in the pairs formed by two inexperienced (i.e. first-time breeding) partners (Spearman rank correlation, all $p > 0.3$; for power analyses see Supporting information).

Among the 70 newly formed pairs comprising at least one inexperienced partner, the second partner was inexperienced in 33 cases, experienced (i.e. known to have bred in the past) in 26 cases, and its experience was unknown in 11 cases. When considering the 60 pairs newly formed after the loss (divorce or death) of the previous partner, the new mate was inexperienced in 32 cases, experienced in 20 cases and its experience was unknown in eight cases.

After assuming that the partners of unknown status were inexperienced when forming pair bonds with first-time breeders, and experienced when pairing with divorcees and widowers, we tested if inexperienced individuals were more likely to choose inexperienced partners than were experienced individuals upon re-mating. Under these conditions, first-time breeders would have paired with inexperienced partners in 44 cases out of 70, and experienced individuals would have re-mated with first-time breeders in 32 cases out of 60. The difference was not significant (G-test with Williams' adjustment, $G_{1W}=1.19, p=0.27$; power to detect a medium effect size [ES=0.3] with our data=0.928, power to detect a large effect size [ES=0.5]=0.999). When making opposite assumptions about the partners of unknown status, however, we could not rule out the hypothesis that inexperienced individuals might form pair bonds with experienced partners more often than experienced individuals ($G_{1W}=4.99, p=0.025$). When considering the 45 pairs for which we knew exactly the breeding experience of the two partners before their first breeding attempt together, the experience of the male was not correlated with that of the female (Spearman rank correlation, $r=0.151, p > 0.2$; ES=0.151, power to detect it if true=0.170, sample size required to detect it with a power of 0.8=339 pairs).

## Parentage analyses and genetic mating system

We successfully genotyped 28 full families at the 11 loci (22 with a single chick or dead embryo, six with two offspring over two different years), plus the family involving a chick and its social father. In another family, we could genotype two chicks but we failed to amplify the parental DNA. In four families, we observed a mismatch between offspring and parental genotypes at only one allele at one locus. Such mismatches were considered to result from mutations occurring in within-pair offspring. In the remaining cases, including the incomplete family made up by a chick and its social father, the genotype of the chick matched that of its social parents at each allele for each locus. Therefore, we detected no extra-pair parentage in the Bulwer's petrels from Vila islet.

## Relationships between pair common experience and reproductive performance

When considering the pair bonds that terminated in the course of our study, reproductive performance was not related to pair common breeding experience, regardless of whether divorce or widowhood caused pair bond disruption (Table 2). Therefore, we found no benefit from mate retention. In newly formed pairs, however, the probability of fledging a chick was significantly higher in pairs made up by an experienced male and an inexperienced female than in pairs formed by two experienced partners, two inexperienced partners or by an inexperienced male and an experienced female (Table 3).

## Correlates of divorce and consequences of the loss of the previous partner

### Factors of divorce

The divorce rate was 6.7% ($n=208$ pair × years). The longest observed pair bonds lasted at least ten years, and we recorded two temporary divorces, that is, two individuals bred with a new partner while their former partner was absent and resumed breeding with their former mate the next year.

Neither pair breeding experience nor previous reproductive performance influenced permanent divorce (GENMOD, $n=92$, analysis of GEE estimates: pair experience: $z=0.89, p=0.373$; reproductive performance: $z=0.43, p=0.670$; intercept: $z=-3.97, p < 0.0001$). As written in the Methods section, our small sample size did not allow controlling for relatedness between pair mates, pair breeding experience and

<table><caption>Table 2. Effect of pair fate (that is, ended up divorcing or did not divorce) and common experience on reproductive performance (GENMOD, analysis of GEE parameter estimates, $n=115$). The first level of pair fate, 'did not divorce', was used as a baseline.</caption><thead><tr><th rowspan="2">Parameter</th><th rowspan="2">Estimate</th><th colspan="2">95% confidence interval</th><th rowspan="2">z</th><th rowspan="2">p</th></tr><tr></tr></thead><tbody><tr><td>Intercept</td><td>-0.378</td><td>-1.169 to 0.412</td><td>-0.94</td><td>0.348</td></tr><tr><td>Pair experience</td><td>0.208</td><td>-0.274 to 0.691</td><td>0.85</td><td>0.398</td></tr><tr><td>Pair fate (divorce)</td><td>0.184</td><td>-0.741 to 1.108</td><td>0.39</td><td>0.697</td></tr></tbody></table>
<table><caption>Table 3. Factors influencing reproductive performance in newly formed Bulwer's petrel pairs (GENMOD, analysis of GEE parameter estimates, n=70). EM=experienced male; IM=inexperienced male; EF=experienced female; IF=inexperienced female.</caption><thead><tr><th>Parameter</th><th>Estimate</th><th>95% confidence interval</th><th>z</th><th>p</th></tr></thead><tbody><tr><td>Intercept</td><td>-0.236</td><td>-0.913 to 0.441</td><td>-0.68</td><td>0.494</td></tr><tr><td>Pair composition</td><td></td><td></td><td></td><td></td></tr><tr><td>EM × EF</td><td>1.084</td><td>-0.383 to 2.551</td><td>1.45</td><td>0.148</td></tr><tr><td>IM × EF</td><td>-0.274</td><td>-1.952 to 1.403</td><td>-0.32</td><td>0.748</td></tr><tr><td>EM × IF</td><td>1.489</td><td>0.188-2.790</td><td>2.24</td><td>0.025</td></tr></tbody></table>

The first level of the variable 'pair composition' (here, IM × IF) was used as a baseline. The results presented here are those when considering females as the 'repeated' subject. We obtained similar results when considering males as the 'repeated' subject.

reproductive performance simultaneously. When considering the pair bonds that terminated in the course of our study, however, relatedness coefficients between pair mates did not differ between the pairs that ended up divorcing permanently and the pairs that did not divorce (Mann-Whitney U = 98, n₁=37, n₂=5, p > 0.8), and pair fecundity (expressed as the number of chicks fledged per year) was not correlated with relatedness between partners (Spearman rank correlation, n=12, r=-0.025, p=0.94, only the pairs monitored for at least four years were considered here; ES=0.0255; power of our study to detect such an effect size=0.051; sample size required to detect it with a power of 0.8=12065 pairs).

The 12 permanent divorces that occurred in the course of our study were all associated with a sabbatical year taken by at least one of the former mates. Note, however, that one of the former mates in eight cases, and both former mates in two cases, were recaptured at the colony during their non-breeding years. In five cases, the former pair left their nest, which remained vacant until the end of our study in two cases (note that in one of these, the nest had been excavated by Cory's shearwaters *Calonectris borealis*) and was taken over by a new pair in three cases. In the remaining seven cases, one of the former partners formed a new pair bond at its usual nest. However, divorce was not an obligate consequence of nest changes. Indeed, 13 pairs changed nest together and 24 of the 62 nest changes followed by a breeding attempt in the new nest were made by individuals that retained their partner, the distance between the old and the new nest ranging from 0.3 to 30 m.

### Consequences of divorce and widowhood for reproduction and re-mating

Divorcees could miss several breeding years before re-mating, and we found a female which divorced in 2005 and was still unpaired in 2012 (that is, the last year of our demographic survey). The divorcees that managed to resume breeding with a new partner could skip up to four years before re-mating (mean number of missed breeding years: 1.6 ± 0.4 SE, n=15; because of our small sample size, we considered all the permanent divorces here, so that a bias due to recently divorced individuals forming new pair bonds quickly may be possible). Their reproductive performance during their first breeding attempt with the new partner was not better than the year preceding divorce (Wilcoxon matched pairs signed rank test, T₄=18, n=10, p > 0.2), and for the eight individuals whose reproductive performance during the second breeding attempt with the new partner was known, we found no significant difference compared to the first one (Wilcoxon matched pairs signed rank test, T₄=7.5, n=4, p > 0.5).

Similarly, widowers skipped 2.61 years ± 0.44 SE on average (range: 0-6 years, n=19; we considered only the widow-hoods until 2007 included) before resuming breeding. Not only widowers and divorcees could skip breeding years even if they retained their nest, but we recaptured eight widowers and one divorcee at their nest as non-breeders, apparently without any potential future partner, before they formed new pair bonds the next year. Like divorcees, widowers did not have a higher or lower breeding success during the first breeding attempt with their new partner than during the last year with their former partner (Wilcoxon matched pairs signed rank test, T₄=51.5, n=17, p > 0.2).

When a divorcee or a widower formed a pair bond with a new partner but retained its nest, the new mate was inexperienced in 19 cases, experienced in seven cases and of unknown status in three cases. When re-mating was associated with a nest change, the new partner was inexperienced in 13 cases, experienced in 13 cases and of unknown status in five cases (Table 4).

When assuming that the proportions of experienced and inexperienced individuals among the new partners of unknown status were the same as for new partners of known experience, the widowers and divorcees that retained their nest tended to form new pair bonds with first-time breeders more often than those that changed nest, although not significantly so (21 out of 29 cases versus 15 out of 31; G-test with

<table><caption>Table 4. Experience of the new partners of the individuals that lost their former mate (after its death or after a divorce) according to whether the latter retained their nest or changed nest upon re-mating.</caption><thead><tr><th>Experience of the new partner</th><th>Retained their nest</th><th>Changed nest</th></tr></thead><tbody><tr><td>In absolute terms</td><td></td><td></td></tr><tr><td>Inexperienced</td><td>19</td><td>13</td></tr><tr><td>Experienced</td><td>7</td><td>13</td></tr><tr><td>Undetermined</td><td>3</td><td>5</td></tr><tr><td>Compared with the divorcee's/widower's experience</td><td></td><td></td></tr><tr><td>Less experienced</td><td>21</td><td>15</td></tr><tr><td>As experienced or more experienced</td><td>2</td><td>3</td></tr><tr><td>Undetermined</td><td>6</td><td>13</td></tr></tbody></table>
Williams' adjustment, G<sub>1W</sub>=3.56, p=0.06). We obtained a similar result after removing the new partners of undetermined experience from our data set (G<sub>1W</sub>=2.87, p=0.09; power to detect a small effect size ES=0.3] with our data: both > 0.58; power to detect a medium effect size [ES=0.5]: both ≥ 0.95).

The proportions of widowers and divorcees that re-mated with new partners that were less experienced, as experienced and more experienced than themselves did not significantly differ according to whether they had retained their nest or changed nest, except if we assumed that the new partners of undetermined status were 'less experienced' in at least 22 cases when paired to the divorcees and widowers that retained their nest, and in 15 cases when paired to those that changed nest (G-test with Williams' adjustment, G<sub>1W</sub>, all p < 0.046, Table 4). After accounting for the existence of new partners of unknown experience (three cases), widowed Bulwer's petrels formed new pair bonds with experienced individuals (i.e. other widowers or divorcees) in 30-37.5% of cases (n=40).

When the new partners of divorcees and widowers were experienced, their origin was known in 18 cases (in the remaining cases we had a doubt about the nest where their previous breeding attempt had occurred). Re-mating with the nearest neighbour occurred in three cases only; the 15 other new partners came from, or were occupying, more distant nests. There was no difference between sexes (Fisher's exact test, p=1).

Discussion

No genetic bottleneck in the Bulwer's petrels from
the Azores

We detected no signs of a genetic bottleneck and inbreeding
in the Bulwer's petrels from the Azores despite very small cur-
rent population size. However, small petrel populations can
retain a reasonably high genetic diversity, even in endemic
species (Lawrence et al. 2008, Nava et al. 2017). In the pres-
ent case, the discovery during our study of two individuals
breeding on Vila islet that had previously been captured on
the Desertas islands (Madeira archipelago), ca 900 km south-
east of Vila, suggests that gene flow might occur between
these islands and the Azores, especially when considering that
Madeira is the nearest breeding locality of Bulwer's petrel
(Fig. 1). Under these conditions, and given that the Desertas
hold the largest Bulwer's petrel population from the northern
Atlantic (45 000 pairs, Catry et al. 2015), emigration from
this locality to the Azores might help maintaining a reason-
able genetic diversity on Vila islet. However, further research
is necessary to confirm this hypothesis.

Decreased selectivity during mate choice

In contrast to Selvagem Grande (Mougin 1989b), pair forma-
tion in the Bulwer's petrels from Vila islet occurred randomly
with respect to bill size. We also observed random pairing

with respect to the size of other body parts, overall structural
body size (except in 2004, but the observed correlation prob-
ably occurred by chance), genetic relatedness and, contrary to
some other Procellariiform species (Brooke 1990, Sagar et al.
2002), breeding experience. Also, inexperienced individuals
did not choose inexperienced partners more often than did
the experienced individuals that formed new pair bonds after
a divorce or the disappearance of their previous mate, and
contrary to widowed wandering albatrosses *Diomedea exulans*
(Jouventin et al. 1999), widowed Bulwer's petrels did not
prefer widowed individuals when forming new pair bonds.

When considering the formation of a new pair bond after
a divorce or the death of the previous partner, the Bulwer's
petrels that retained their nest tended to re-mate with inex-
perienced partners more often that those that changed nest,
similarly to divorced Monteiro's storm-petrels (Nava et al.
2017). We explain this phenomenon in the same manner as
Nava et al. (2017), that is, experienced individuals might out-
compete first-time breeders for nests/mates. Consequently
the latter would obtain poor quality nests/partners
and/or would content themselves with filling vacancies. On
Selvagem Grande, Mougin (1990, 1996) found that widowed
and divorced Bulwer's petrels that retained their nest formed
new pair bonds with individuals that were more experienced,
less experienced than, or equally experienced as themselves
in proportions similar to those that changed nest. Amongst
those that changed nest, the new partner was inexperienced
in 56% of cases, a proportion similar to that observed on Vila
islet where re-mating occurred with an inexperienced partner
in 42-58% of cases. Nonetheless, and in contrast to other
petrel species (e.g. snow petrel *Pagodroma nivea*, Jouventin
and Bried 2001; Cory's shearwater, Mougin et al. 1988,
2001, Bried et al. 2010), the Bulwer's petrels from Vila islet
that had lost their previous partner did not re-mate preferen-
tially with neighbours.

Genetic monogamy associated with social
monogamy

Although Bulwer's petrels seemed to choose their partners at random on Vila islet, we found no case of EPP, contrary to what occurs in the Cory's shearwaters from the same location (Bried et al. 2010). Our failure to detect EPPs is not surprising given that 1) EPCs have never yet been observed in Bulwer's petrel (Megyesi and O'Daniel 2020), and 2) low EPP rates are expected in long-lived species with obligate biparental care (Griffith et al. 2002). In some cases, EPP might result from a strategy aimed at avoiding inbreeding in strongly philopatric populations where the opportunities to exert choosiness during social mate choice are limited (Tarvin et al. 2005 and references therein, also suggested by Huyvaert and Parker 2010 in the waved albatross *Phoebastria irrorata*). On Vila islet, Bulwer's petrels exhibit a certain level of philopatry (J. Bried unpubl.) like many Procellariiform species (Warham 1990), and they also breed in very low numbers. However, the population from Vila islet is not inbred, and as far as we know, EPPs are not related to inbreeding avoidance in
Procellariiformes (Austin and Parkin 1996, Quillfeldt et al. 2001, Bried et al. 2010, Huyvaert and Parker 2010) except perhaps in the wandering albatross (Jouventin et al. 2007).

## No effect of pair common experience on reproductive performance

In contrast again to the Bulwer's petrels from Selvagem Grande (Mougin 1997) and also to several other seabird species, including Procellariiformes (reviews in Hunt 1980, Bried and Jouventin 2002; see also Jouventin and Bried 2001, Nava et al. 2017), we did not find that reproductive performance improved with pair breeding experience. In newly formed pairs, however, the probability of fledging a chick was highest in pairs formed by an experienced male and an inexperienced female. This finding suggests that experience in male Bulwer's petrels is important for breeding success, possibly because like all Procellariiform males (Warham 1990), they take the first incubation shift, which is also the longest (Nunes and Vicente 1998, Nunes 2000). However, we have no explanation for why the new pairs formed by two experienced individuals are not as successful, contrary to what occurs in the same species on Selvagem Grande (Mougin 1997; however this author did not find statistically significant differences amongst the different categories of pairs) or in other seabird species, including Procellariiformes (reviewed by Bried and Jouventin 2002, but see Sagar et al. 2002). We can just speculate that in Bulwer's petrel, the partners of such pairs might take longer to achieve a sufficient degree of coordination, as observed in Laysan albatrosses *Phoebastria immutabilis* (Van Ryzin and Fisher 1976).

## Correlates of divorce

Not only we did not detect extra-pair parentage on Vila islet but also the divorce rate at this locality was lower than on Selvagem Grande (11.5–11.8%; Mougin 1990, 1996). Actually, it was similar to that observed in the part of Mougin's study area on Selvagem Grande where the stability of the breeding habitat was highest (5%, Mougin 1990), and might indeed be explained by the overall high stability of the breeding habitat on Vila islet. Indeed, very few nests on Vila disappeared or became unsuitable from one year to the next, essentially due to excavation and/or take over by the much larger Cory's shearwaters (Bried and Bourgeois 2005, J. Bried unpubl.). Divorces occurred during a sabbatical year of at least one of the former partners, like on Selvagem Grande (Mougin 1996). However, permanent divorces were unrelated to reproductive performance and pair common experience, and in many cases, one or both previous partners were recaptured as non-breeders (but not in the same nest) the year following their last breeding attempt together while the old nest became occupied by one or two newcomers. This strongly suggests that the most common cause of divorce was nest usurpation. Among the divorcees that changed nest upon re-mating, two individuals may have taken over their new nest (that is, the former occupants were observed the same

year, but in other nests), but they had lower reproductive performances than before divorcing. Therefore, our results do not support the 'incompatibility' and 'better option' hypotheses, but are compatible with the 'forced divorce' or the 'musical chairs' hypotheses which state that the occupancy of the nest by newcomers prevents the former pair from reuniting (Choudhury 1995). To which extent, however, divorce is associated with nest availability remains unclear. Indeed, divorce occurred irrespective of nest occupancy rate, only 12 of the 63 nests that were occupied at least once during our study were occupied each year, and the vacancies left after the nest change by one of the former partners upon divorce (or after its death as well) were not always immediately filled.

Nonetheless, divorce did not always follow nest change in Bulwer's petrel. Indeed, 38.7% of nests changes associated with a breeding attempt in the new nest on Vila islet were performed by individuals that retained their previous mate. Mougin (1996) found a similar value (35.7%) on Selvagem Grande. While the old and the new burrow were there generally a few metres apart (Mougin 1996), mate retention on Vila islet was possible even if they were several tens of metres apart. Although Mougin (1990) showed that mate fidelity was positively correlated with nest fidelity in the Bulwer's petrels from Selvagem Grande, our findings, and his as well, are compatible with the existence of genuine pair bonds in Procellariiformes and not with the hypothesis that mate retention arises merely from nest fidelity (see also Bried et al. 2003).

## Conclusions

Like in the Azores-endemic Monteiro's storm-petrel, the demographic bottleneck experienced by Bulwer's petrels in the Azores did not result in a genetic bottleneck, pair formation occurred randomly with respect to genetic relatedness, and pair fecundity was unrelated to genetic relatedness between pair mates. However, and contrary to Mougin (1989b) in the large population from Selvagem Grande, we found no assortative pairing based on morphological criteria. The apparently decreased choosiness and the low divorce rate (the latter being also favoured by habitat stability) on Vila islet might be related to the limited opportunity of finding suitable partners during the pre-laying period, so that individuals would form pair bonds with any available partner and retain it for as many years as possible despite the fact that reproductive performance did not improve with pair common experience, possibly to avoid skipping breeding years in case of divorce (Jouventin and Bried 2001). Supporting the hypothesis of fewer encounters on Vila islet than on Selvagem Grande, the breeding density of Bulwer's petrels is much lower on the 8-ha Vila islet (6.25 pairs ha⁻¹) than on the 280-ha (Granadeiro et al. 2009) Selvagens islands (17.86 pairs ha⁻¹, calculated from Costa et al. 2003).

To what extent this strategy can explain the low breeding success on Vila islet compared to other localities from the northern subtropical Atlantic (46% of breeding attempts were on average across years successful on Vila islet, versus 56% on
Selvagem Grande (Mougin 1997) and 65% on the Desertas islands (calculated from Nunes 2000 and Boieiro et al. 2018)) is beyond the scope of our study and remains to be investigated, especially given that seabird breeding success is primarily influenced by food availability at sea (Schreiber 2002, Inchausti et al. 2003).

Whatsoever, we encourage future studies aimed at evaluating whether individuals from very small populations in other seabird species, resulting from either a demographic bottleneck or a founder event (Young et al. 2008), become less choosy during mate choice. This might have implications when establishing conservation programmes in threatened species. Our findings, combined with those from studies on other petrel species (Barbraud and Jouventin 1998, Jouventin and Bried 2001, Carey 2011 contra Bradley et al. 1995 and Einoder et al. 2008, Bried et al. 2010 contra Nava et al. 2014), also confirm that apparently decreased choosiness during social mate choice is not incompatible with high year-to-year mate fidelity in Procellariiformes, and that these species, despite being considered as examples of long-term monogamy, exhibit a certain degree of flexibility in their mating strategies.

*Acknowledgements* – V. C. Neves, K. Bourgeois, E. Álamo-Carrasco and R. Fontaine provided field assistance. J. M. Soares and the Clube Naval from Santa Maria provided transportation to Vila islet. We are also grateful to the staff from Gemex (ex SMGE) at CEFE (Montpellier) and from the ‘plateforme génotypage-séquençage’ of Labex Cemeb (Montpellier). Finally, we thank P. Catry and two anonymous reviewers for their constructive comments.

*Funding* – This study was part of the project PTDC/BIABDE/67286/2006 funded by FCT and by FEDER through the Programme COMPETE (Ref: FCOMP-01-0124-FEDER-007061), and coordinated by JB. It also received fundings from two Luso-French Integrated Actions Programmes (PESSOA 4.1.1/França and PAUILF F-30/07). The Programmes ‘MARE’ (Integrated Management of Coastal and Marine Sites of the Azores, Life contract B4-3200/98-509), ‘OGAMP’ (Planning and Management of Marine Protected Areas, Interreg IIIB-MAC/4.2/A2), ‘MARMAC’ (Knowledge, Promotion and Valorization for a Sustainable Utilization of Marine Protected Areas in Macaronesia, Interreg IIIB/FEDER/MARMAC/003-4/2005-6 and Interreg IIIB-05/MAC/4.2/A4), and MoniAves, all coordinated by R. S. Santos, also provided support for fieldwork. IMAR-DOP/UAç is funded by FCT and DRCT-Azores as Research Unit 531 and Associate Laboratory 9 (ISR-Lisbon).

*Permits* – Permits for fieldwork and blood sampling were issued to JB by the Direção Regional do Ambiente dos Açores.

## Author contributions

**J. Bried**: Conceptualization (lead); Data curation (lead); Formal analysis (lead); Funding acquisition (lead); Investigation (lead); Methodology (equal); Project administration (lead); Resources (equal); Supervision (equal); Validation (equal); Visualization (equal); Writing – original draft (lead); Writing – review and editing (lead). **Malvina Andris**: Conceptualization (supporting); Data curation

(supporting); Formal analysis (equal); Investigation (equal); Methodology (equal); Resources (supporting); Software (equal); Validation (supporting); Visualization (supporting); Writing – original draft (supporting); Writing – review and editing (supporting). **Marie-Pierre Dubois**: Data curation (supporting); Formal analysis (supporting); Investigation (supporting); Methodology (equal); Resources (equal); Software (equal); Supervision (supporting); Validation (supporting); Visualization (supporting); Writing – original draft (supporting); Writing – review and editing (supporting). **Philippe Jarne**: Conceptualization (supporting); Data curation (supporting); Formal analysis (supporting); Investigation (supporting); Methodology (supporting); Resources (supporting); Software (supporting); Supervision (equal); Validation (supporting); Visualization (supporting); Writing – original draft (supporting); Writing – review and editing (supporting).

## Transparent Peer Review

The peer review history for this article is available at <https://publons.com/publon/10.1111/jav.02837>.

## Data availability statement

Data are available from the Dryad Digital Repository: <http://dx.doi.org/10.5061/dryad.k0p2ngf8w> (Bried et al. 2021).

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