Ecology and Evolution. 2019;9:10734–10745.
Received: 5 March 2019
Revised: 11 June 2019
Accepted: 17 June 2019
DOI: 10.1002/ece 3.5591
Mate fidelity in a polygamous shorebird, the snowy plover
Naerhulan Halimubieke1 | José O. Valdebenito1 | Philippa Harding1 |
Medardo Cruz‐López2 | Martín Alejandro Serrano‐Meneses3 | Richard James4 |
Krisztina Kupán5 | Tamás Székely1,6
1Department of Biology and Biochemistry, Milner Centre for Evolution, University of Bath, Bath, UK
2Posgrado en Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Ciudad Universitaria, Cd. México, Mexico
3Departamento de Ciencias Químico‐Biológicas, Universidad de las Américas Puebla, San Andrés Cholula, Puebla, Mexico
4Department of Physics and Centre for Net works and Collective Behaviour, University of Bath, Bath, UK
5Max Planck Institute for Ornithology, Behaviour Genetics and Evolutionary Ecology Research Group, Seewiesen, Germany
6Department of Evolutionary Zoology and Human Biolog y, University of Debrecen, Debrecen, Hungary
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,
provided the original work is properly cited.
© 2019 The Authors. Ecology an d Evolution published by John Wiley & Sons Ltd.
Krisz tina Kupán and Tamás Sz ékely are co‐auth ors shared sen ior authorsh ip to this work.
Naerhulan Halimubieke, Depar tment of
Biology and Biochemistry, Milner Centre for
Evolution, University of Bath, Bath, UK.
Krisztina Kupán, Max Planck Institute
for Ornithology, Behaviour Genetics and
Evolutionary Ecology Research Group,
This project was funded by China
Scholarship Council, CONICYT BECAS
CHILE 72170569, ÉLVONAL KKP‐126949
(the National Research, Development and
Innovation Office of Hungary), CONACY T
(Mexico), through the Convocatoria de
Investigación Científica Básica 2010‐01
(project number 157570).
Social monogamy has evolved multiple times and is particularly common in birds.
However, it is not well understood why some species live in long‐lasting monoga‐
mous partnerships while others change mates between breeding attempts. Here,
we investigate mate fidelity in a sequential polygamous shorebird, the snowy plover
(Charadrius nivosus), a species in which both males and females may have several
breeding attempts within a breeding season with the same or different mates. Using
6 years of data from a well‐monitored population in Bahía de Ceuta, Mexico, we
investigated predictors and fitness implications of mate fidelity both within and be‐
tween years. We show that in order to maximize reproductive success within a sea‐
son, individuals divorce after successful nesting and re‐mate with the same partner
after nest failure. Therefore, divorced plovers, counterintuitively, achieve higher re‐
productive success than individuals that retain their mate. We also show that differ‐
ent mating decisions between sexes predict different breeding dispersal patterns.
Taken together, our findings imply that divorce is an adaptive strategy to improve
reproductive success in a stochastic environment. Understanding mate fidelity is im‐
portant for the evolution of monogamy and polygamy, and these mating behaviors
have implications for reproductive success and population productivity.
breeding dispersal, Charadrius nivosus, divorce, mate fidelity, nesting success, polygamous
HALIMU BIEKE Et A L.
1 | INTRODUCTION
The decision of retaining a mate for several breeding events or di‐
vorcing is a key element of reproductive decisions in several species,
as it can affect reproductive success and subsequent survival of the
parents (Culina, Radersma, & Sheldon, 2014; Neff & Pitcher, 2005;
Székely, Thomas, & Cuthill, 2006; Székely, Weissing, & Komdeur,
2014). Social monogamy, defined as a system where an adult has only
one social partner of the opposite sex at a given time or throughout a
time period, is commonly observed in birds, but also occurs in inver‐
tebrates, fish, amphibians, reptiles, and mammals (Lukas & Clutton‐
Brock, 2013; Møller, 2003). Social monogamy partnerships are
highly variable in terms of duration. Some species show long‐term
mate fidelity or even life‐time mate fidelity until one partner dies
(Black, 2001; Reichard & Boesch, 20 03). Oth er species , however, ex‐
hibit short‐term mate fidelity, in which an individual terminates the
relationship at the end of one breeding attempt and initiate another
breeding with a new mate while the old partner is still alive (termed,
sequential polygamy). Why do males and females adopt short‐term
mate fidelity, while others pair for life?
Several hypotheses have been put forward emphasizing the im‐
pact of either breeding time‐constraints (or breeding success) on
mate fidelity or divorce in socially monogamous species. On the
one hand, retaining a mate reduces the time and energy costs of
searching for a new mate therefore facilitate a fast re‐mating (“fast‐
track hypothesis,” Adkins‐Regan & Tomaszycki, 2007; Perfito, Zann,
Bentley, & Hau, 2007). Retaining a mate also enhance breeding per‐
formance thereby improving reproductive success (“mate familarity
hypothesis,” Ens, Choudhury, & Black, 1996; Gabriel, Black, & Foster,
2013; Sánchez‐Macouzet, Rodríguez, & Drummond, 2014). In addi‐
tion, successful breeding may also facilitate retaining the mate for
future breeding (Black, 2001; Flodin & Blomqvist, 2012). On the
other hand, changing a mate may be beneficial in long‐lived species,
individuals divorce their partner to mate with good quality partners
in order to improve breeding success (“incompatibility hypothesis,”
Coulson, 1966; see also Kempenaers, Adriaensen, & Dhondt, 1998).
In species with short life span (or short breeding season), individu‐
als improve reproductive success by mating with multiple mates to
make the most out of limited time (“extra‐pair mating hypothesis,”
Arnqvist & Nilsson, 2000; Birkhead & Møller, 1992).
Mating decisions may be related to breeding dispersal—the lat‐
ter defined here as the movement of an adult from one breeding
location to another within or between years (Clobert, Danchin,
Dhondt, & Nichols, 2001; Greenwood, 1980). On the one hand,
breeding dispersal may differ between the sexes in response to sex
differences in mating strategies since the more polygamous sex is
expected to disperse farther to find new mating partners (D'Urban
Jackson et al., 2017; Greenwood, 1980; Székely, 2019; Trochet et
al., 2016). On the other hand, mate fidelity can be viewed as a by‐
product of site fidelity in some species (Bried, Pontier, & Jouventin,
2003; Morse & Kress, 1984), whereas changing the nest site would
lead to mate change in some other species (Pietz & Parmelee, 1994;
A further factor that may influence mate fidelity is re‐mating
opportunity. In species or populations with a biased adult sex ratio,
divorce is commonly initiated by the rare sex since the rare sex has
higher mate availability than the common sex (Liker, Freckleton, &
Székely, 2014; Parra, Beltrán, Zefania, Dos Remedios, & Székely,
2014). For example, experimental studies of species with biased
adult sex ratio showed that by experimentally creating unmated
males and females, re‐mating times were shorter for rare sex than
for common sex (Parra et al., 2014; Székely, Cuthill, & Kis, 1999).
Neverth ele ss, studies of mate fide lit y ten ded to fo cus on monog‐
amous species across breeding years, yielding different adaptive im‐
plications of mate fidelity (Bried et al., 2003; Dubois & Cézilly, 2002).
Monogamous systems are generally characterized by high level of
breeding philopatry (Moore & Ali, 1984; Saalfeld & Lanctot, 2015)
and/or bi‐parental care of the young (Eberhart‐Phillips et al., 2018),
features that tend to promote mate fidelity. However, the causes
and fitness implications of mate fidelity in sequential polygamous
species that exhibit variable duration of pair bonds (e.g., within a
breeding year), different levels of philopatry, or breeding dispersal
are still poorly understood.
Here, we investigate potential predictors and fitness implications
of mate fidelity in a sequential polygamous shorebird, the snowy
plover (Charadrius nivosus), a ground‐nest ing, near threatened shore‐
bird distributed on sparsely vegetated coasts and alkaline lakeshores
across the tempera te and tr opical regio ns of the Amer icas. They typ‐
ically lay a 3‐egg clutch with both parents providing care during the
incubation stage, chicks are precocial and nidifugous, which only
require uniparental care (usually males) during brood rearing (del
Hoyo, Elliott, Sargatal, Christie, & Juana, 2018). This species is an
ideal model for investigating mate fidelity: they have a flexible mat‐
ing system, and both males and females may have several mates se‐
quentially in a single breeding season up to four breeding attempts
(Page, Stenzel, Warriner, Warriner, & Paton, 2009). It is typically fe‐
males that mate with more partners than males do, since females
tend to desert their broods soon after hatching, and leave the males
to look after the young until independence (Carmona‐Isunza et al.,
2017; Warriner, Warriner, Page, & Stenzel, 1986). Female desertion
has been linked to male‐biased adult sex ratio (ASR): 0.53 (propor‐
tion of males in the adult population) was estimated by Stenzel et al.
(2011) based on adult survival, whereas more recent estimate that
took into account hatchling sex ratios, chick survival and adult sur‐
vival estimated a strongly male‐biased ASR (0.638, Eberhart‐Phillips
et al., 2018). Snowy plovers may still retain their mate between
clutches within or between years. Furthermore, a recent paternity
analyses showed low rates (<5%) of extra‐pair paternity in the snowy
plover so that social pairs are a good proxy for genetic relationships
and thus reflect Darwinian fitness (Maher et al., 2017).
Using snowy plovers as a model organism, here we investigate
whether mate fidelity (or divorce) is an adaptive strategy that maxi‐
mizes reproductive success in a species with limited breeding period
(Choudhury, 1995; Plaschke, Bulla, Cruz‐López, Gómez del Ángel,
& Küpper, 2019). We focus on three main aspects of mate fidel‐
ity. First, we investigate patterns of mate fidelity both within and
HALIMUBIEKE E t AL.
between years in both males and females. Second, we exp lore if pre‐
vious nesting success predict mate retention (or divorce) by males
and females both within and between years. Finally, we investigate
mate fidelity in relation to breeding dispersal and re‐mating time: (a)
whether breeding dispersal is related to mate fidelity both within
and between years; (b) whether the re‐mating time may differ be‐
tween divorced and retained mates within years.
2 | METHODS
2.1 | Study site and field methods
The present study was conducted at Bahía de Ceuta, Sinaloa, Mexico
(23°54′N, 106°57′W). In this population, snowy plovers nest on
extensive saline ponds and saltpans (approximately 150 hectares;
Carmona‐Isunza, Küpper, Serrano‐Meneses, & Székely, 2015). The
breeding season generally occurs from mid‐April to mid‐July, with
30–100 breeding pairs every year. Breeding data were collected
from 2006 to 2011 (n = 625 nests). Data collection in the field fol‐
lowed the methods of Székely, Kosztolányi, and Küpper (2008).
Briefly, we searched for nests using a mobile hide intensively within
the study site, we recorded the nest location with handheld GPS,
and the egg‐laying date was estimated based on the floatation stage
of each egg in a transparent jar with clean water. Breeding pairs were
captured with a walk‐in funnel trap placed over the nest, and they
were banded with a unique combination of three color rings and an
alpha‐numeric metal ring. Nests were monitored every 2–5 days
until 20 days of incubation and then were checked every day until
hatching to obtain nesting success data. Broods were searched in‐
tensively daily to determine the date of brood desertion. Re‐sight‐
ings of previously color banded plovers were also recorded.
2.2 | Data collection
2.2.1 | Quantification of mate fidelity
Snowy plovers that were monitored in this study were actively
choosing to retain or to divorce their mates. The mating decision
of each individual was recorded as either mate retention or divorce
in regard to their previous breeding attempt. We evaluated mating
decisions separately for banded males and females in the popula‐
tion, since the decisions may influence one another and as such
may not be independent. Individuals were included in the analyses
if they satisfied the following conditions: (a) we knew the identity
of their mate(s), (b) they were observed in at least two reproduc‐
tive attempts that were either within or between years, and (c) if
there is a mate change, only those who change their mates while the
previous mate is known to be alive are included. In total, 149 breed‐
ing events (Table 1A, 75 divorces in females, 26 divorces in males,
and 24 retentions in each sex) fitted the criterion for the within‐year
mate fidelity analysis from 2006 to 2011. For plovers with more than
two nests within a year, only the data from the first two nests were
included in the within‐year mate fidelity analysis due to the small
number of individuals with three or more nests: during the study
TABLE 1 Mate fidelity in snowy plover. (A) Number of males and females divorced or retained a mate within years, n = 149 breeding
events. (B) Number of males and females divorced or retained a mate between breeding years (late–early mate fidelity, n = 102 breeding
events; early–early mate fidelity, n = 116 breeding events; 2006–2011)
(A) Within years
Year 2006 2007 2008 2009 2 010 2011 Tota l
Number of divorces in females 11 21 10 14 12 775
Number of retentions in females 683 2 3 2 24
Number of divorces in males 583 3 4 3 26
Number of retentions in males 683 2 3 2 24
(B) Between years
Year 2006–2007 2007–2008 2008–2009 2009–2010 2010–2011 Total
late–early mate fidelity
Number of divorces in females 12 6 7 12 542
Number of retentions in females 4 1 1 3 2 11
Number of divorces in males 8 8 11 7 4 38
Number of retentions in males 4 1 1 3 2 11
early–early mate fidelity
Number of divorces in females 13 4 4 7 7 35
Number of retentions in females 1 4 2 6 3 16
Number of divorces in males 17 78710 49
Number of retentions in males 1 4 2 6 3 16
Note: See Section 2 for details.
HALIMU BIEKE Et A L.
period, there were only seven females and two males in total that
had three breeding attempts.
For individuals with one or multiple nests in each of the two
consecutive years, we evaluate between‐year mate fidelity in
two different ways (see Figure 1). First, when an individual's mate
during late season (see “relative egg‐laying date” below, late sea‐
son is when the relative egg‐laying date is >0) in year 1, had the
sa m e as the mat e in early se ason (w hen the re lati ve egg‐lay ing dat e
is <0) in year 2, it was classified as mate retention, or otherwise
divorce (hereinafter late–early mate fidelity). In total, 102 breed‐
ing events (Table 1B, 42 divorces in females, 38 divorces in males
and 11 retentions in each sex) fitted the criteria for the late–early
mate fidelity. Second, if a plover mated to the same individual in
the early seasons of both year 1 and year 2, this was classified
as retention, or divorce otherwise (hereinafter early–early mate
fidelity). In total, 116 breeding events (Table 1B, 35 divorces in
females, 49 divorces in males and 16 retentions in each sex) fitted
the criteria for the early–early mate fidelity. All individuals were
classified into three groups as divorced males, divorced females,
and retained pairs (see Sandercock, Lank, Lanctot, Kempenaers,
& Cooke, 2000).
2.2.2 | Nesting success and reproductive success
Nesting success was quantified based on the fate of the first nest of
each individual that were included in our study. The fate of nest was
recorded as either successful (at least one chick hatched) or failed
(no chicks hatched due to predation, destruction, abandonment,
eggs disappeared <15 days after estimated laying date, eggs did not
hatch, or the nest was flooded). We quantified reproductive success
as the cumulative number of hatchlings each individual produced in
all breeding attempts either within or between years.
2.2.3 | Relative egg‐laying date
The egg‐laying date was used to quantify breeding phenology. We
controlled for breeding phenological differences between years by
converting egg‐laying dates into Julian dates (“lubridate” package in
R, Grolemund & Wickham, 2011), and calculating the relative egg‐
laying date using the z‐transformation (mean = 0, SD = 1).
2.2.4 | Breeding dispersal
Within‐year breeding dispersal was defined as the straight‐line
distance (in meters) between an individual's successive nests
within a year. For between‐year breeding dispersal, we measured
the straight‐line distance between (a) the last nest in year 1 and
the first nest in year 2, and (b) the first nests of two consecutive
2.2.5 | Re‐mating time
Re‐mating time is defined as the number of days that an individual
spent on establishing a new clutch after terminating care of the pre‐
vious brood. Broods were searched in the breeding area daily. If a
parent was missing during two consecutive sightings or seen paired
to another plover, it was considered to have deserted the brood. We
estimated the date of brood desertion for a parent as the mid‐point
between the time when the individual was last seen with his/her
brood and first seen without the brood. We estimated second nest
FIGURE 1 Schematic illustration of
two estimates of between‐year mate
fidelity in snowy plovers: Early‐late and
early–early mate fidelities
HALIMUBIEKE E t AL.
egg‐laying date based on the floating stage of the eggs (see above).
We only estimated the re‐mating times within years.
2.3 | Statistical analyses
2.3.1 | Comparison of male and female mate fidelity
We analyzed mating decision as either mate retention or divorce of
a plover from an individual its previous breeding attempt. We calcu‐
lated the number of mate retentions and number of divorces in males
and females within the population for both within and between
years. We used the two‐proportion z test (Yau, 2013) to compare
the proportion of divorced females relative to the female population
to the proportion of divorced males relative to the male population
both within and between years.
2.3.2 | The relationship between mate fidelity and
We constructed separate models for males and females to investi‐
gate whether mate fidelity is related to nesting success within and
between years. Here, separation of the sexes was necessary since
nesting success is nonindependent variable within a pair; there‐
fore, individuals of a pair provide the same data points. In the latter
analyses, mate fidelity of an individual was the dependent variable,
and nesting success was used as explanatory variable. To analyse
the females, we used generalized linear mixed models (GLMM) with
binomial error and included Individual ID and Year as random effect
variables to account for the repeated identities of females among
years. For males, we used generalized linear model (GLM) with bi‐
2.3.3 | Reproductive success and mate fidelity
To investigate whether mate fidelity relates to reproductive suc‐
cess (estimated as the total number of hatchlings from both
clutches), we compared divorced males, divorced females, retained
pairs using Kruskal–Wallis tests followed by post hoc pairwise
comparisons (Dunn test) to test group differences within and be‐
2.3.4 | Breeding dispersal and mate fidelity
Models were built to investigate the relationship between breeding
dispersal and mate fidelity groups within and between years. Log‐
transformed (ln) breeding dispersal was the dependent variable, and
mate fidelity groups (divorced males, divorced females, and retained
pairs) were the explanatory variable. Linear mixed‐effects model
(LMM) via REML was fitted and maintained Individual ID and Year
as random effect variables. Then, the estimated marginal means
(emmeans from package “emmeans” in R) were calculated for each
group, post hoc pairwise comparisons adjusted by Tukey were ap‐
plied to test group differences.
2.3.5 | Re‐mating time and mate fidelity
To investigate whether re‐mating time differs between mate fidel‐
ity groups (divorced males, divorced females, and retained pairs), we
used Kruskal–Wallis tests followed by post hoc pairwise compari‐
sons (Dunn test) to test group differences within and between years.
All statistical analyses were performed using R version 3.5.1 (R Core
3 | RESULTS
3.1 | Mate fidelity between sexes
Within breeding years, males showed higher mate fidelity than fe‐
males using 149 breeding events (Table 1A, 75 divorces in females,
26 divorces in males, and 24 retentions in each sex) from 2006
to 2011, two‐proportion z test, p = .002, n = 6 years). The differ‐
ent numbers of female and male breeding attempts are due to the
fact that more females than males had multiple breeding attempts.
Between breeding years, however, we did not find a difference in
mate fidelity of males versus females (Table 1B, two‐proportion z
test; late–early mate fidelity: p = 1.00, n = 5 years; early–early mate
fidelity: p = .55, n = 5 years).
3.2 | Mate fidelity in relation to nesting success and
Within breeding years, mate fidelity was related to nesting success
since divorce was more likely when the nest hatched successfully,
whereas mate retention was more likely if the nest failed (Table 2,
females: GLMM, p < .001, male: GLM, p < .001; Figure 2). Between
breeding years, however, mate fidelity was not related to nesting
success. The latter result was consistent between the late–early
mate fidelity and early–early mate fidelity (Table 2).
Divorced plovers (both males and females) produced significantly
more hatchlings within breeding years than those retained their
mate. Reproductive success was not different between divorced
males and divorced females (Table 3, Kruskal–Wallis tests, p < .001,
followed by post hoc pairwise Dunn test; divorced females—re‐
tained pairs: p adjusted < .001, divorced males—retained pairs: p
adjusted = .05, divorced females—divorced males: p adjusted = .07;
Figure 3). Between breeding years, however, reproductive success
was not different between divorced and retained individuals neither
in the late–early nor in the early–early comparisons (Kruskal–Wallis
tests; late–early mate fidelity: χ2 = 0.20, df = 2, p = .90; early–early
mate fidelity: χ2 = 4.21, df = 2, p = .12).
3.3 | Mate fidelity in relation to breeding
dispersal and re‐mating time
Divorced females bred further away than divorced males both within
and between years (Figure 4, Table 4). Divorced males, however, did
not breed further away than retained pairs (Table 4).
HALIMU BIEKE Et A L.
TABLE 2 Mate fidelity in relation to nesting success within and between breeding years in snowy plover
Response variable Model used Explanatory variable Estimate SE z value p value
Mate fidelity Binomial (GLMM) Intercept −0.92 0.42 −2.19 .03
Nesting success 4.38 0.83 5.27 <.001
Mate fidelity Binomial (GLMM) Intercept −1 5.9 2 5.16 −3.09 .002
Nesting success 29.17 7. 59 3.84 <.0 01
Between years: late–early
Mate fidelity Binomial (GLMM) Intercept 1.39 0.79 1.75 .08
Nesting success −0.06 0.87 −0.07 .95
Mate fidelity Binomial (GLM) Intercept 1.50 0.78 1.92 .05
Nesting success −0.33 0.87 −0.38 .70
Between years: early–early
Mate fidelity Binomial (GLMM) Intercept 1.47 1.19 1.23 .22
Nesting success −0.75 1.25 −0.60 .55
Mate fidelity Binomial (GLM) Intercept 2.30 1.05 2.20 .03
Nesting success −1.3 7 1.10 −1 . 26 .21
Note: Generalized linear mixed models (GLMM) with binomial error family and including “Individual ID” and “Year” as random effect variables to ac‐
count for the repeated identities of female individuals among years. For males, generalized linear model (GLM) with binomial error family was used.
Abbreviation: SE, standard error.
Statistically significant results are presented in bold.
FIGURE 2 Mate fidelity in relation to
nesting success in (a) female and (b) male
snowy plovers within a year (see Table 2
for statistics). Logistic linear regression
lines (blue) with standard error (gray)
HALIMUBIEKE E t AL.
Finally, re‐mating times were not different between divorced
males, divorced females and retained pairs (Kruskal–Wallis test,
χ2 = 2.00, df = 2, p = .37).
4 | DISCUSSION
Previous analyses of mate fidelity were typically concerned with
either within‐year or between‐year mate fidelity and focus largely
on monogamous systems (sometimes termed mate desertion, mate
abandonment or mate change; Black, 2001; Bried et al., 2003; Flodin
& Blomqvist, 2012). Here, we take an integrative approach and in‐
vestigate mate fidelity both within and between breeding years.
Using a sequential polygamous shorebird, the snowy plover, we
identified factors that predict mate fidelity and its spatial‐temporal
manifestation in a system, in which males and females differ in their
breeding strategies and reproductive efforts.
Our analyses revealed three major results. First, males exhibit
higher within‐year mate fidelity than females. This is consistent with
the previous studies of snowy plover since females tend to desert
the brood whereas males are usually the ones that rear the young
(Carmona‐Isunza et al., 2015; Warriner et al., 1986). We suggest that
male‐biased adult sex ratio entices female parents more than male
parents to desert their brood and breed again (Eberhart‐Phillips et al.,
2017; Stenzel et al., 2011); thereby resulting in different re‐mating
opportunities and mate fidelities between males and females. The
latter results are consistent with experimental and empirical stud‐
ies that show altered adult sex ratios influences mating decisions
(Karlsson, Eroukhmanoff, & Svensson, 2010; Liker, Freckleton, &
Székely, 2013; Liker et al., 2014; Silva, Vieira, Almada, & Monteiro,
However, between years both male and female snowy plovers
demonstrated low mate fidelity. We note however that our mate
fidelity (and consequently, our divorce decision as well) was based
on local returning rates: if paired birds may breed outside the study
area and/or some of the survived adults may not return to breed
to Ceuta, these survival estimates can be biased. The annual return
rate to Ceuta are 41.5% for males (n = 378 individuals) and 35.4% for
females (n = 339 individuals, 2006–2011). Therefore, further inves‐
tigation is required to estimate more precisely the return rates using
more comprehensive spatial coverage by visiting additional breeding
sites near Ceuta and/or using GPS tags to monitor the movements of
adults within and between years.
Second, divorce was more likely after a nest hatched than after
it failed since failed breeders typically re‐nested with the same part‐
ner. Therefore, divorced plovers, counterintuitively, reared more
offspring than faithful individuals. This finding is not consistent with
studies of long‐lived bird species where low breeding success may
trigger divorce (“incompatibility hypothesis,” Black, 2001; Coulson,
1966; Jouventin & Bried, 2001). We propose that by abandoning the
Groups Z p unadjusted p adjusted
Divorced females—divorced males 1.97 <.0 01 .07
Divorced females—retained pairs 4.08 <.001 <.001
Divorced males—retained pairs 1.92 <.0 01 .05
Statistically significant results are presented in bold.
TABLE 3 Comparison of reproductive
success between mate fidelity groups
(divorced males, divorced females, and
retained pairs) within breeding years
(Kruskal–Wallis tests, p < .001, followed
by post hoc pairwise Dunn test)
FIGURE 3 Reproductive success in
relation to divorce or mate fidelity in
snowy plovers (see Table 3 for statistics).
Medians, upper, and lower quartiles, as
well as extreme values are shown
Divorced females Divorced males Retained pairs
Total number of hatchlings
HALIMU BIEKE Et A L.
brood and divorcing, individuals try to maximize their reproductive
success by producing as many clutches over the season as possible.
Divorce may be facilitated by two aspects of natural history: first,
nest and chick mortality in this population tend to be high and sto‐
chastic, and thus, parents may need several trials to produce at least
some fledglings (Cruz‐López, Eberhard‐Phillips, et al., 2017). Second,
the chicks are precocial, and thus, they only require modest care:
brooding and protection, but not feeding (Székely & Cuthill & Kis,
1999). The well‐developed hatchling then gives the opportunity for
one parent to terminate care and start breeding with a new partner
(Houston, Székely, & McNamara, 2013; McNamara, Forslund, & Lang,
1999; Székely, Webb, Houston, & McNamara, 1996). Mate retention
was, however, more likely after nest failure, in which case the paren‐
tal duties of both parents terminated at the same time; therefore,
the fastest way to breed again was to retain the previous partner
(“fast‐track hypothesis”; Perfito et al., 2007; Zann, 1994; reviewed
by Fowler, 1995; also see Adkins‐Regan & Tomaszycki, 2007).
However, breeding success in previous years may have little
impact on the re‐mating decision of snowy plovers. We presume
that the breeding time constraint facilitates early breeding with
TABLE 4 (A) Breeding dispersal in relation to mate fidelity groups (divorced males, divorced females, and retained pairs) within and
between breeding years. (B) Comparison of breeding dispersal between mate fidelity groups (divorced males, divorced females, and retained
pairs) within and between breeding years
Response variable Model used Explanatory variable Estimate SE t value
Breeding dispersal LMM Intercept 6.46 0.16 38.85
Divorced males −0.95 0. 26 −3.63
Retained pairs −0.67 0.26 −2 .58
Between years: late–early
Breeding dispersal LMM Intercept 6. 41 0.21 30.25
Divorced males −1 . 01 0.30 −3.37
Retained pairs −0.70 0.39 −1 .77
Between years: early–early
Breeding dispersal LMM Intercept 5.87 0. 29 20.48
Divorced males −0.95 0.38 −2 . 53
Retained pairs −0.73 0.33 −2.23
Groups Estimate SE df t ratio p value
0.95 0.26 111 3.60 .001
0.67 0.26 112 2.57 .03
Divorced males—retained pairs −0.28 0.26 68 −1.05 . 55
Between years: late–early
1.01 0.31 72 3.28 .005
0.70 0. 41 72 1.70 .21
Divorced males—retained pairs −0.32 0.44 85 −0.71 .76
Between years: early–early
0.95 0.38 70 2 .51 .04
0.73 0.35 56 2.09 .10
Divorced males—retained pairs −0.22 0.44 88 −0.50 .87
Note: The linear mixed‐effects model (LMM) via REML was fitted and maintained “Individual ID” and “Year” as random effect variables.
Abbreviation: SE, standard error.
Statistically significant results are presented in bold.
HALIMUBIEKE E t AL.
available mates instead of waiting for the former partner, especially
since early breeding is associated with higher nest survival (Plaschke
et al., 2019; van de Pol, Heg, Bruinzeel, Kuijper, & Verhulst, 2006;
Székely et al., 1999). Since snowy plovers only have about 2 years of
breeding life (average breeding life of males: 2.3 ± 1.6 years; females:
1.9 ± 1.2 years; Colwell, Pearson, Eberhart‐Phillips, & Dinsmore,
2013), they may not discriminate against previous mates even if they
were failed breeders Furthermore, returning to the breeding ground
may be stochastic and this can also produce decoupling between
nesting success and mate fidelity (Bried, Frédéric, & Jouventin,
1999; Gilsenan, Valcu, & Kempenaers, 2017; Handel & Gill, 2000).
Third, we found that females tend to disperse farther than males
after divorce both within and between breeding years. This follows
the general pattern of female‐biased breeding dispersal observed in
most bird species including shorebirds (Clarke, Saether, & Roskaft,
1997; Greenwood & Harvey, 1982; Liu & Zhang, 2008; Sandercock
et al., 2000). However, in polyandrous birds like snowy plovers there
is an additional reason: finding new mate while their previous mate
is taking care of the chicks (D'Urban Jackson et al., 2017). For males,
returning to previous breeding site—that is often thought as a high‐
quality site providing good brood‐rearing opportunities (Sandercock
et al., 200 0)—is a factor that reduces their aptitude moving large dis‐
tance between nests. Mate fidelity is often related to the degree of
site fidelity (Cézilly, Dubois, & Pagel, 2000; Cézilly & Johnson, 1995),
and while it would be tempting to argue that higher mate fidelity
lead to higher site fidelity in males, or vice versa high divorce rate by
females lead to more extensive breeding dispersal, to conclude the
directionality of causation—and to separate whether the males or
the females drive these relationships—would require experimental
manipulation of mate fidelity, site fidelity, or both.
Together, our results support theoretical arguments that divorce
is an adaptive strategy by which individuals improve their repro‐
ductive success (Black, 1996; Dubois & Cézilly, 2002; McNamara &
Forslund, 1996). Divorced birds reached higher number of breeding
attempts and higher breeding success than individuals that retained
their mates, at least within years. We suggest that in snowy plovers,
divorce is result from their effort to maximize reproductive out‐
put during a given time period. The birds' urge to re‐mate as many
times as possible within a breeding season and produce the highest
possible number of chicks could be traded off by lowered survival
of their abandoned broods although, given the precociality of the
young, this cost may not be prohibitive (Székely & Williams, 1995).
We suggest that the urge for a fast reproduction in snowy plovers is
an adaptive response to life histories (i.e., short life span) and breed‐
ing parameters (i.e., short breeding period and breeding success).
Additionally, time constraint in breeding confounded with the bias
FIGURE 4 Breeding dispersal (a) within year, and between year (b, late–early) and (c, early–early) in snowy plover (see Section 2 for
explanations and Table 4 for statistics). Breeding dispersal was estimated in meters and log‐transformed (ln). Medians, upper, and lower
quartiles, as well as extreme values are shown
Breeding dispersal (meters, log−transformed)
Divorced femalesDivorced malesRetained pairsDivorced females Divorced males Retained pairs
Divorced femalesDivorced males Retained pairs
HALIMU BIEKE Et A L.
in population demography (i.e., male‐biased adult sex ratio) propels
both sexes adopt different mating strategies, resulting in different
spatial dispersal patterns. Therefore, mate choice and breeding dis‐
persal are important components of their breeding strategy. We en‐
courage further investigations of breeding strategy including mate
fidelity between different polygamous shorebird populations and to
understand the generality of our findings across the various natural
populations with the intention of informing conservation decisions.
We thank all fieldwork volunteers and people who have worked and
supported the conservation project of Snowy plovers at Bahía de
Ceuta, especially to Clemens Küpper and Cristina Carmona‐Isunza
for data collection. Thanks to Jennifer McDowall, Luke Eberhart‐
Phillips, Kathryn Maher, Judit Mokos, and Brett Sandercock for their
advice on previous versions of the manuscript.
CONFLICT OF INTEREST
We have no conflict of interest to declare.
N. H., P. H., and T. S. conceived the project; K. K., M. A. S.‐M., and
M. C.‐L. provided the data; N. H. and K. K. carried out the statisti‐
cal analyses. All authors contributed critically to the drafts and gave
final approval for publication.
DATA AVA ILAB ILITY STATE MEN T
Data are available from the Dryad Digital Repository, https ://doi.
All aspects of the fieldwork were authorized by the national authori‐
ties of Mexico (Secretaría de Medio Ambiente y Recursos Naturales,
SEMARNAT; SGPA/DGVS/01717/10, SGPA/DGVS/01367/11).
Birds were ringed and handled by trained people aiming to cause as
little disturbance to birds as possible.
Naerhulan Halimubieke https://orcid.org/0000‐0002‐6928‐5986
José O. Valdebenito https://orcid.org/0000‐0002‐6709‐6305
Philippa Harding https://orcid.org/0000‐0003‐0763‐3516
Medardo Cruz‐López https://orcid.org/0000‐0003‐1737‐9398
Martín Alejandro Serrano‐Meneses https://orcid.
Richard James https://orcid.org/0000‐0002‐8647‐7218
Adkins‐Regan, E., & Tomaszycki, M. (2007). Monogamy on the fast track.
Biology Letters, 3, 617–619.
Arnqvist, G., & Nilsson, T. (2000). The evolution of polyandry: Multiple
mating and female fitness in insects. Animal Behaviour, 60, 145–164.
Birkhead, T. R., & Møller, A. P. (1992). Sperm competition in birds. London,
UK: Academic Press.
Black, J. M. (1996). Partnerships in birds. Oxford, UK: Oxford University
Black, J. M. (2001). Fitness consequences of long‐term pair bonds in
barnacle geese: Monogamy in the extreme. Behavioral Ecology, 12,
Bried, J., Frédéric, J., & Jouventin, P. (1999). Why do Aptenodytes pen‐
guins have high divorce rates? The Auk, 116, 504–512. https ://doi.
Brie d, J., Pontie r, D. , & Jo uventi n, P. (20 03). Mate fi delit y in mon ogamo us
birds: A re‐examination of the Procellariiformes. Animal Behaviour,
Carmona‐Isunza, M. C., Ancona, S. I., Székely, T., Ramallo‐González, A. P.,
Cruz‐López, M., Serrano‐Meneses, M. A., & Küpper, C. (2017). Adult
sex ratio and operational sex ratio exhibit different temporal dynam‐
ics in the wild. Behavioral Ecology, 28, 523–532.
Carmona‐Isunza, M. C., Küpper, C., Serrano‐Meneses, M. A., & Székely, T.
(2015). Court ship behavior dif fers between monogamous and polyg‐
amous plovers. Behavioral Ecology and Sociobiology, 69, 2035–2042.
Cézilly, F., Dubois, F., & Pagel, M. (200 0). Is mate fidelity related to site
fidelity? A comparative analysis in Ciconiiforms. Animal Behaviour, 59,
Cézilly, F., & Johnson, A. R. (1995). Re‐mating within and between breed‐
ing seasons in the greater flamingo, Phoenicopterus ruber roseus. Ibis,
Choudhury, S. (1995). Divorce in birds: A review of the hypotheses.
Animal Behaviour, 50, 413–429.
Clarke, A. L., Saether, B. E., & Roskaft, E. (1997). Sex biases in avian dis‐
persal: A reappraisal. Oikos, 79, 429–438.
Clober t, J., Danchin, E., Dhondt, A., & Nichols, J. D. (2001). Dispersal.
New York, NY: Oxford University Press.
Colwell, M. A., Pearson, W. J., Eberhart‐Phillips, L. J., & Dinsmore, S.
J. (2013). Apparent survival of Snowy Plovers (Charadrius nivosus)
varies with reproductive effort and between sexes. The Auk, 13 0,
Coulson, J. C. (1966). The influence of the pair‐bond and age on the
breeding biology of the Kittiwake Gull Rissa tridactyla. Journal of
Animal Ecology, 35, 269–27 9.
Cruz‐López, M., Eberhart‐Phillips, L. J., Fernández, G., Beamonte‐
Barrientos, R., Székely, T., Serrano‐Meneses, M. A., & Küpper, C.
(2017). The plight of a plover: viability of an important snowy plover
population with flexible brood care in Mexico. Biological Conservation,
Culina, A., Radersma, R., & Sheldon, B. C. (2014). Trading up: The fitness
consequences of divorce in monogamous birds. Biological Reviews of
the Cambridge Philosophical Society, 90, 1015–1034.
del Hoyo, J., Elliott, A., Sargatal, J., Christie, D. A. & de Juana, E. (Eds.).
(2018). Handbook of th e birds of the world alive. Barcelona, Spain: Lynx
Dubois, F., & Cézilly, F. (2002). Breeding success and mate retention
in birds: A meta‐analysis. Behavioral Ecology and Sociobiology, 52,
D'Urban Jackson, J., Dos Remedios, N., Maher, K. H., Zefania, S., Haig,
S., Oyler‐McCance, S., … Küpper, C. (2017). Polygamy slows down
population divergence in shorebirds. Evolution, 71, 1313–1326.
Eberhart‐Phillips, L. J., Küpper, C., Carmona‐Isunza, M. C., Vincze, O.,
Zefania, S., Cruz‐López, M., … Krüger, O. (2018). Demographic causes
HALIMUBIEKE E t AL.
of adult sex ratio variation and their consequences for parental coop‐
eration. Nature Communications, 9, 1651.
Eberhart‐Phillips, L. J., Küpper, C., Miller, T. E. X., Cruz‐López, M.,
Maher, K. H., Dos Remedios, N., … Székely, T. (2017). Sex‐specific
early survival drives adult sex ratio bias in snowy plovers and im‐
pacts mating system and population growth. Proceedings of the
National Academy of Sciences of the United States of America, 114,
Ens, B. J., Choudhury, S., & Black, J. M. (1996). Mate fidelity and divorce
in monogamous birds. In J. M. Black (Ed.), Partnerships in birds: The
study of monogamy (pp. 344–401). Oxford, UK: Oxford University
Flodin, L. A., & Blomqvist, D. (2012). Divorce and breeding dispersal in
the Dunlin Calidris alpina: Support for the better option hypothesis?
Behaviour, 149, 67 – 8 0 . h t t p s : / / d o i . o r g / 1 0 . 1 1 6 3 / 1 5 6 8 5 3 9 1 2 X 6 2 6 2 9 5
Fowler, G. S. (1995). Stages of age‐related reproductive success in birds:
Simultaneous effects of age, pair‐bond duration and reproductive
experience. American Zoologist, 35, 318–328.
Gabriel, P. O., Black, J. M., & Foster, S. (2013). Correlates and conse‐
quences of the pair bond in Steller's Jays. Ethology, 119, 178–187.
Gilsenan, C., Valcu, M., & Kempenaers, B. (2017). Difference in arrival
date at the breeding site between former pair members predicts di‐
vorce in blue tits. Animal Behaviour, 133, 57–72.
Greenwood, P. J. (1980). Mating systems, philopatry and dispersal in
birds and mammals. Animal Behaviour, 28, 1140–1162.
Greenwood, P. J., & Harvey, P. H. (1982). The natal and breeding dispersal
of birds. Annual Review of Ecolog y and Systematics, 13, 1–21.
Grolemund, G., & Wickham, H. (2011). Dates and times made easy with
lubridate. Journal of Statistical Software, 40, 25.
Handel, C. M., & Gill, R. E. (2000). Mate fidelity and breeding site tenacity
in a monogamous sandpiper, the black turnstone. Animal Behaviour,
Houston, A. I., Székely, T., & McNamara, J. M. (2013). The parental in‐
vestment models of Maynard Smith: A retrospective and prospective
view. Animal Behaviour, 86, 667–674.
Jouventin, P., & Bried, J. (2001). The effect of mate choice on speciation
in snow petrels. Animal Behaviour, 62, 123–132.
Karlsson, K., Eroukhmanoff, F., & Svensson, E. I. (2010). Phenotypic plas‐
ticity in response to the social environment: Effects of densit y and
sex ratio on mating behaviour following ecotype divergence. PLoS
ONE, 5, e12755.
Kempenaers, B., Adriaensen, F., & Dhondt, A. A. (1998). Inbreeding and
divorce in blue and great tits. Animal Behaviour, 56, 737–740. https ://
Liker, A., Freckleton, R. P., & Székely, T. (2013). The evolution of sex roles
in birds is related to adult sex ratio. Nature Communications, 4, 1587.
Liker, A., Freckleton, R. P., & Székely, T. (2014). Divorce and infidelity are
associated with skewed adult sex ratios in birds. Current Biology, 24,
Liu, Y., & Zhang, Z. W. (2008). Research progress in avian dispersal be‐
havi or. Frontiers of Biolog y in China, 3, 375.
Lukas, D., & Clutton‐Brock, T. H. (2013). The evolution of social monog‐
amy in mammals. Science, 314, 526–530.
Maher, K. H., Eberhart‐Phillips, L. J., Kosztolányi, A., Dos Remedios, N.,
Carmona‐Isunza, M. C., Cruz‐López, M., … Küpper, C . (2017). High
fidelity: Extra‐pair fertilisations in eight Charadrius plover species
are not associated with parental relatedness or social mating system.
Journal of Avian Biology, 48, 910–920.
McNamara, J. M., & Forslund, P. (1996). Divorce rates in birds: Predictions
from an optimization model. American Naturalist, 147, 609–640.
McNamara, J. M., Forslund, P., & Lang, A. (1999). An ESS model for di‐
vorce strategies in birds. Philosophical Transactions of the Royal
Society of London. Series B: Biological Sciences, 354, 223–236. https ://
Møller, A. P. (2003). The evolution of monogamy: Mating relationships,
parental care and sexual selection. In U. H. Reichard & C. Boesch
(Eds.), Monogamy mating strategies and partnerships in birds, hu‐
mans and other mammals. (pp.29‐41). Cambridge, UK: University of
Moore, J., & Ali, R. (1984). Are dispersal and inbreeding avoidance re‐
lated? Animal Behaviour, 32, 94–112. https ://doi.org/10.1016/
Morse, D. H., & Kress, S. W. (1984). The effect of burrow losses on mate
choice in Leach's storm‐petrel. The Auk, 101, 158–160.
Neff, B. D., & Pitcher, T. E. (2005). Genetic quality and sexual selection:
An integrated framework for good genes and compatible genes.
Molecular Ecology, 14, 19–38.
Page, G. W., Stenzel, L. E., Warriner, J. S., Warriner, J. C., & Paton, P.
W. (2009). Snowy plover Charadrius nivosus. In A. Poole (Ed.), The
birds of North America online. Ithaca, NY: Cornell Lab of Ornithology.
Retrieved from http://bna.birds.corne ll.edu/bna/speci es/154
Parra, J. E., Beltrán, M., Zefania, S., Dos Remedios, N., & Székely, T.
(2014). Experimental assessment of mating opportunities in three
shorebird species. Animal Behaviour, 90, 83–90.
Perfito, N., Zann, R. A ., Bentley, G. E., & Hau, M. (2007). Opportunism at
work: Habitat predictability affects reproductive readiness in free‐
living zebra finches. Functional Ecology, 21, 291–301.
Pietz, P. J., & Parmelee, D. F. (1994). Survival, site and mate fidel‐
ity in south polar skuas Catharacta maccormicki at Anvers Island,
Antarctica. Ibis, 136, 12–18.
Plaschke, S., Bulla, M., Cruz‐López, M., Gómez del Ángel, S., & Küpper, C.
(2019). Nest initiation and flooding in response to season and semi‐
lunar spring tides in a ground‐nesting shorebird. Frontiers in Zoology,
R Core Team (2018). R: A language and environment for statis tical comput‐
ing. Vienna, Austria: R Foundation for Statistical Computing.
Reichard, U. H., & Boesch, C. (2003). Monogamy: Mating strategies and
partnerships in birds, humans and other mammals. Cambridge, UK:
Cambridge University Press.
Saalfeld, S. T., & Lanctot, R. B. (2015). Conservative and opportunistic
settlement strategies in Arctic‐breeding shorebirds. The Auk, 132,
21 2–23 4 .
Sánchez‐Macouzet, O., Rodríguez, C., & Drummond, H. (2014). Better
stay together: Pair bond duration increases individual fitness inde‐
pendent of age‐related variation. Proceedings of the Royal Society B:
Biological Sciences, 281, 20132843.
Sandercock, B. K., Lank, D. B., Lanctot, R. B., Kempenaers, B., & Cooke, F.
(2000). Ecological correlates of mate fidelity in two Arctic‐breeding
sandpipers. Canadian Journal of Zoology, 78, 1948–1958.
Silva, K., Vieira, M. N., Almada, V. C., & Monteiro, N. M. (2010). Reversing
sex role reversal: Compete only when you must. Animal Behaviour,
Stenzel, L., Page, G. W., Warriner, J. C., Warriner, J. S., Neuman, K. K.,
George, D. E., … Bidstrup, F. C. (2011). Male‐skewed adult sex ratio,
survival, mating opportunity and annual productivity in the Snowy
Plover Charadrius alexandrinus. Ibis, 153, 312–322.
Székely, T. (2019). Why study plovers? The significance of non‐model
organisms in avian ecology, behaviour and evolution. Journal of
Ornithology, 160 (3), 923–933. (in press) https ://doi.org/10.1007/
Székely, T., Cuthill, I. C., & Kis, J. (1999). Brood desertion in Kentish plo‐
ver sex differences in remating opportunities. Behavioral Ecology, 10 ,
Székely, T., Kosztolányi, A., & Küpper, C. (2008). Practical guide for in‐
vestigating breeding ecology of Kentish plover Charadrius alexandri‐
nus. Unpublished Report, University of Bath, Bath, UK. Retrieved
from http://www.pennu ti.net/wp‐conte nt/uploa ds/2010/08/
HALIMU BIEKE Et A L.
Székely, T., Thomas, G. H., & Cuthill, I. C. (2006). Sexual conflict, ecology,
and breeding systems in shorebirds. BioScience, 56, 801–808.
Székely, T., Webb, J. N., Houston, A. I., & McNamara, J. M. (1996). An
evolutionary approach to offspring desertion in birds. Current
Ornithology, 13, 271–330.
Székely, T., Weissing, F. J., & Komdeur, J. (2014). Adult sex ratio variation:
Implications for breeding system evolution. Journal of Evolutionar y
Biology, 27, 1500–1512.
Székely, T., & Williams, T. D. (1995). Costs and benefits of brood deser‐
tion in female Kentish plovers, Charadrius alexandrinus. Behavioral
Ecology and Sociobiology, 37, 155–161.
Thibault, J. C. (1994). Nest‐site tenacity and mate fidelity in relation to
breeding success in Cory's shearwater Calonectris diomedea. Bird
Study, 41, 25–28.
Trochet, A., Courtois, E., Stevens, V. M., Baguette, M., Chaine, A.,
Schmeller, D. S., & Clobert, J. (2016). Evolution of sex‐biased disper‐
sal. Quarterly Review of Biology, 91, 297–320.
van de Pol, M., Heg, D., Bruinzeel, L. W., Kuijper, B., & Verhulst, S. (2006).
Experimental evidence for a causal effect of pair‐bond duration on
reproductive performance in oystercatchers (Haematopus ostrale‐
gus). Behavioral Ecology, 17, 982–991.
Warriner, J. S., Warriner, J. C., Page, G. W., & Stenzel, L. E. (1986). Mating
system and reproductive success of a small population of polyga‐
mous Snow y Plover. The Wilson Bulletin, 98, 15–37.
Yau, C. (2013). R tutorial: An R introduction to statistics (eBook). Retrieved
from http://www.r‐tutor.com/eleme ntary‐stati stics/ infer ence‐
about‐two‐popul ation s/compa rison‐two‐popul ation‐propo rtions
Zann, R. A. (1994). Reproduction in a zebra finch colony in south‐east‐
ern Australia: The significance of monogamy, precocial breeding and
multiple broods in a highly mobile species. Emu, 94, 285–299.
How to cite this article: Halimubieke N, Valdebenito JO,
Harding P, et al. Mate fidelity in a polygamous shorebird, the
snowy plover (Charadrius nivosus). Ecol Evol. 2019;9:10734–
10745. https ://doi.org/10.1002/ece3.5591