Evidence of Závora Bay as a critical site for reef manta rays,
Mobula alfredi, in southern Mozambique
| Nakia Cullain
| Stephanie Kathleen Venables
| Charles Griffiths
| Andrea Denise Marshall
Department of Biological Sciences, University
of Cape Town, Cape Town, South Africa
Marine Megafauna Foundation, West Palm
Beach, Florida, USA
Department of Biology, Dalhousie University,
Halifax, Nova Scotia, Canada
Departamento de Biología, Facultad de
Ciencias del Mar y Ambientales, Universidad
de Cádiz, Cádiz, Spain
Michelle Carpenter, Department of Biological
Sciences, University of Cape Town, Private
Bag, Rondebosch, Cape Town 7700,
University of Cape Town, Grant/Award
Number: 2020 Faculty Fellowship
The largest known reef manta ray (Mobula alfredi) population in Africa has been moni-
tored for more than 20 years at several locations on the coast of the Inhambane
Province in southern Mozambique. Nonetheless, before this study, little had been
reported on the population dynamics of M. alfredi from Závora, a remote bay in the
region. Photographic mark-recapture was used to investigate the size and structure
of M. alfredi that aggregate at “Red Sands,”a reef cleaning station in Závora Bay. An
11 year photographic data set was used to identify 583 M. alfredi individuals
between 2010 and 2021. More than half of M. alfredi individuals were resighted at
least once, with most encounters (up to 18 for one individual) occurring during the
peak sighting period in July–November each year. An even sex ratio was observed,
44% females and 50% males, with no significant difference in resightings between
the sexes. Pollock's robust design population models were used to estimate annual
abundance, emigration, annual apparent survival and capture probability at Red Sands
from July to November over a 6 year period (2016–2021). Abundance estimates var-
ied year to year, ranging from 35 (95% C.I. [30, 45]) up to 233 (95% C.I. [224, 249])
M. alfredi individuals. Given the seasonal affinity of M. alfredi observed at Red Sands,
this study highlights the importance of understanding fine-scale site use within the
larger home range of this population to develop local management strategies.
mark recapture, Mobulidae, photo-ID, population demography, robust design, southern Africa
The purpose of this study is to better understand areas of critical habitat for reef manta rays in
southern Mozambique, specifically, the use of a cleaning station called “Red Sands”(RS) in Závora
Bay in the Inhambane Province. This is important because cleaning stations, areas on reef where
fish remove parasites or dead skin off of a “client”animal, are sites that manta rays have been
found to repeatedly return to. The authors found a large seasonal abundance of manta rays at RS,
displaying the importance of this site for the greater southern Mozambique population. As RS is
currently unprotected, the study demonstrates the need for immediate site-specific protection.
Received: 15 March 2022 Accepted: 7 June 2022
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.
© 2022 The Authors. Journal of Fish Biology published by John Wiley & Sons Ltd on behalf of Fisheries Society of the British Isles.
J Fish Biol. 2022;1–12. wileyonlinelibrary.com/journal/jfb 1
Understanding population trends of large, migratory, marine species can
be challenging because of the difficulty in assessing habitat use within
their estimated home range. Knowledge of fine-scale visitation patterns
at specific locations through focused site-specific studies can be benefi-
cial to understanding population dynamics, identifying priority areas for
protection and developing local management regimes. The use of pho-
tographic mark-recapture is rapidly co-evolving in parallel with both
technological advancements in camera equipment, open-source web-
sites, algorithm development and growth in citizen science initiatives (e.
g., public data submissions and increased internet access), making it an
increasingly powerful tool for long-term population monitoring of wide-
ranging species across many taxa and habitat types (Karanth, 1995;
Dala-Corte et al., 2016;Marshall&Pierce,2012;McConkey,1999;
Schofield et al., 2008; Towner et al., 2013; Wiirsig & Jefferson, 1990).
Predictable aggregations at certain sites allow snapshots of population
sizes, trends and movement patterns of these elusive species.
Manta rays (order Myliobatiformes) are wide-ranging, pelagic filter
feeders that aggregate at inshore reefs, islands or seamounts (Couturier
et al., 2012;Murieet al., 2020;Harriset al., 2020). Their aggregations
can be directly related to foraging, or at cleaning stations in close prox-
imity to feeding grounds, to solicit cleaning services by symbiotic fish
and sometimes engage in social or reproductive interactions (Couturier
et al., 2011; Limbaugh, 1961; Stevens, 2016). The unique and stable
ventral markings of individual rays have facilitated photo-identification
(photo-ID) studies at these aggregation sites, providing the foundation
for manta ray research in many locations across the globe (e.g., Coutu-
rier et al., 2014; Deakos et al., 2011;Germanovet al., 2019;Harris
et al., 2020; Homma et al., 1999; Kumli & Rubin, 2008;Marshallet al.,
2011; Stevens, 2016). This technique has been used to assess home
range (Deakos et al., 2011;Kashiwagiet al., 2011), longevity (Clark,
2010; Couturier et al., 2014; Kashiwagi, 2014; Rubin, 2002), migration
patterns (Armstrong et al., 2019; Germanov & Marshall, 2014), site
affinity (Couturier et al., 2011; Germanov et al., 2019;Marshallet al.,
2011), reproductive ecology (Deakos et al., 2011;Marshall&Bennett,
2010a;Stevens,2016) and estimating abundance (Beale et al., 2019;
Couturier et al., 2014;Venables,2020). Regional reef manta ray
[Mobula alfredi (Kreft, 1868)] photo-ID databases vary substantially in
the total number of individuals identified over time, ranging from popu-
lations in the low hundreds (Axworthy et al., 2019;Carpentieret al.,
2019; Deakos et al., 2011; Kashiwagi, 2014;Peel,2019) to those in the
thousands (Armstrong et al., 2019;Stevens,2016; Venables, 2020).
Mark-recapture population modelling provides a tool through
which photo-ID data can be analysed to provide abundance estimates.
Predictable patterns in the use of critical habitats, such as cleaning
stations and feeding locations, make M. alfredi a suitable candidate for
this technique (Couturier et al., 2011; Venables, 2020). With an initial
photo of the ventral spot patterning signifying an individual's “mark”
and subsequent photos representing their “recaptures,”these data
are further analysed through models to estimate population parame-
ters (Couturier et al., 2014; Grusd et al., 2019). Previous mark-
recapture studies of M. alfredi have used various model types [i.e.,
Cormack–Jolly–Seber (CJS); Petersen's method; Pollock's robust
design (PRD)] (Couturier et al., 2014; Deakos et al., 2011; Kitchen-
Wheeler et al., 2012; Marshall et al., 2011). More recently, the robust
design has proven useful, with the ability to account for temporary
emigration and capture heterogeneity, which are inherent in mobile
marine species (Couturier et al., 2014; Venables, 2020). PRD models
are characterised by marginal dependence between abundance and
survival estimators, as well as estimation of temporary emigration, all
of which improve the precision of population estimates and interpre-
tations of the relationship between abundance and survival (Grusd
et al., 2019; Kendall et al., 1995; Pollock, 1981; Pollock et al., 1990).
A 16 year study in Mozambique documented the largest photo-
identified population of M. alfredi in Africa, with the number of identi-
fied individuals currently reported to be 1209 (Marshall et al., 2011;
Venables, 2020). With increased annual sampling effort, M. alfredi
continues to exhibit long-term affinity to monitored cleaning stations
in Mozambique; some individuals returning to the same sites for more
than 15 years (Venables, 2020). Estimations of annual abundances in
the Praia do Tofo region peaked at 836 individuals in 2004–2005
(Venables, 2020). However, sightings declined of up to 88% between
2003 and 2011 (Rohner et al., 2013), and estimates of only 100 indi-
viduals sighted in Tofo after 2013 (Venables, 2020) have raised imme-
diate concern about the health of this population. M. alfredi is listed
on the IUCN Red List as Vulnerable (Marshall et al., 2018) and is glob-
ally threatened from direct harvesting of the gill plates for the Asian
market, by-catch, destructive fisheries methods and coastal develop-
ment, which in turn leads to increased boat strikes, habitat loss and
pollution (Couturier et al., 2012; Croll et al., 2016; Fernando & Stewart
2021; Lawson et al., 2017; O'Malley et al., 2016). Monitoring of popu-
lations of this threatened species is thus crucial for future IUCN Red
List assessments and further development of local management
actions, such as the designation of new marine-protected areas and
regulations surrounding fisheries and tourism operations.
Although the Tofo region has been consistently monitored since
2003, an aggregation site for M. alfredi 90 km south in Závora has not
yet been assessed. The authors of this study aim to better understand
this specific aggregation and assess its importance for the larger
southern Mozambican population of M. alfredi. They use an 11 year
photo-ID database of individuals to describe population demo-
graphics, site affinity and resightings data. Using PRD mark-recapture
modelling, they estimate annual abundance and population parame-
ters including apparent survival, emigration and recapture probability
at RS between 2016 and 2021. The findings can be used to inform
the development of local conservation strategies and guide the design
and implementation of spatial management approaches, such as
marine-protected areas, in the Závora Bay region of the Inhambane
2|MATERIALS AND METHODS
2.1 |Study site
In Mozambique, M. alfredi is most commonly encountered in the
coastal waters of the Inhambane Province, particularly from the
2CARPENTER ET AL.
Bazaruto Archipelago in the north to Závora in the south (Figure 1).
This 350 km stretch of coastline joins a narrow continental shelf that
experiences regular upwelling events, resulting in productive waters
that attract several planktivorous species, including whale sharks,
Rhincodon typus, giant manta rays, Mobula birostris, and shortfin devil
rays, Mobula kuhlii (Rohner et al., 2013; Quartly & Srokosz, 2004).
M. alfredi has been monitored in Závora since 2010; nonetheless,
because of limited resources, the remoteness of this location and min-
imal tourism/recreational diving, a comprehensive sampling design
was not initiated until 2016. Red Sands (RS) is a rocky reef with scat-
tered corals and sponges, at 12–18 m depth, c. 3 km offshore. The site
is characterised by variability in environmental conditions: with hori-
zontal visibility ranging 1–20 m, various levels of current and surge,
and sea temperatures ranging from 16 to 23C in the winter and up to
27C in the summer (Cullain, unpubl. data).
2.2 |Sampling effort and design
Photographic sampling by trained researchers was conducted at RS
on SCUBA diving between 2010 and 2021. Weather, logistical limita-
tions and COVID-19 restrictions prohibited consistent, daily sampling
effort throughout and between years. During each survey, teams of
two to eight divers swam a transect that covered all monitored clean-
ing stations that make up RS. Upon encountering an individual
M. alfredi, a photo of the unique markings on the ventral surface was
taken. Sex was determined by the presence of external claspers for
males and absence for females (Marshall & Bennett, 2010a). The
authors assessed male maturity by the size of reproductive organs,
individuals being considered adult once the claspers extended past
the posterior edge of the pectoral fins (Marshall & Bennett, 2010a).
Female maturity was determined by the observation of pregnancy
(when the abdomen was clearly expanded), or the presence of repro-
ductive scars usually on the left pectoral fin (99% lateralisation:
Marshall & Bennett, 2010a). A female that was not noticeably preg-
nant, nor had mating scars, was recorded as unknown maturity. The
total number of identified and unidentified individuals were pooled
for each day of sampling. Resightings of an individual were recorded
when identified more than 24 h after the last sighting.
The authors used photo-ID data collected from 2010 to 2021
to assess population demographics. Mean counts of individuals or
time periods between sightings were calculated to assess the num-
ber and resightings of males and females (± standard deviation).
Mark-recapture models require consistent survey effort and because
of the nature of the current data set, only the most recent 6 years
fit these criteria (82% of the total identifications). Therefore, data
collected at RS during the 5 month peak season (July–November) of
2016–2021 were included in the PRD modelling, resulting in six pri-
mary periods (years) and 29 secondary periods (months; Table 1).
Of the total 583 M. alfredi individuals catalogued for Závora,
401 were photo-identified at RS between 2016 and 2021 and
were included in the PRD. Of these, individuals of undetermined
FIGURE 1 Study map of Závora Bay showing the location of the Red Sands cleaning station and the bathymetry of the bay
CARPENTER ET AL.3
sex (n=18) were removed for the final PRD analysis that included
sex as a covariate.
2.3 |Mark-recapture analysis
The authors used a PRD with Huggins’estimator to analyse 6 year
photographic mark-recapture data of M. alfredi at RS, Závora
(Huggins, 1989; Pollock et al., 1990). Models were assembled using
package “RMark”(Laake, 2013) in R Version 4.1.2 (R Core Team,
2021), the R interface to programme MARK (Cooch & White, 2006;
White & Burnham, 1999). The six peak seasons were selected as pri-
mary periods because of higher M. alfredi sightings; each winter sea-
son had five monthly secondary periods (July–November), except
2016 which had four (July–October), because of no survey effort in
November 2016. Mobula alfredi sightings were lower in December–
June; therefore, these months were excluded to allow adequate time
between primary periods to detect fluctuations in the population
(Kendall, 1999; Silva et al., 2009). Few M. alfredi individuals (n=21)
were sighted at other reefs in Závora, but never encountered at RS;
therefore, these individuals were excluded from the present study
(Supporting Information Table S1).
PRD models have the following assumptions: all ventral markings
on M. alfredi individuals were unique and remained stable over time,
the population was open to immigration, emigration, natality and mor-
tality between years, full closure within the aggregation months and
equal survival probability on all individuals (Cooch & White, 2006;
Kendall et al., 1995; Smith et al., 2013; Williams et al., 2002). Closure
was not assumed at RS specifically; rather the authors of this study
assumed that the individuals encountered at RS remained in the
Závora Bay region during these time periods and were thus recap-
tured at RS.
The authors evaluated apparent survival between primary periods
as time-constant φ(), time varying φ(t) and with a group effect for sex
φ(sex). Models including time-varying survival consistently yielded
inestimable parameters. The authors deemed it appropriate to exclude
time-varying survival from the final model set due to the longevity of
M. alfredi once mature; previous studies on M. alfredi populations
found survival estimates close to 1.0 between years (Couturier et al.,
2014; Kitchen-Wheeler et al., 2012). The temporary emigration
parameter represents the probability of present individuals in the pop-
ulation being absent for capture in a specific period (Kendall et al.,
1997). This was assessed as Markovian (γ0and γ00), random γ(γ0=γ00 )
or none (γ0,γ00 =0). Capture pand recapture cprobabilities were
modelled as time-constant p(), time-varying per year p(y) and with
effects of sampling effort p(s). Equal capture and recapture probability
(p=c) was excluded from the final candidate model set due to inesti-
mable parameters resulting from the variability of encounters per sec-
ondary period. Parameter estimates were model averaged based on
the model weight. The authors evaluated the confidence interval (C.I.)
and standard error (S.E.) of each estimated parameter. The PRD analy-
sis was subsequently conducted on the same data with pooled sexes
to yield numbers for total population abundance across the primary
periods. AICc was used to evaluate the best model that fitted the
data, determined by the smallest AICc value (Burnham & Anderson,
2004). A Mann–Whitney U-test was conducted using the “exac-
tRankTests”R package to analyse the effect of sex on the total num-
ber of recaptures during the study period, with individuals of
undetermined sex excluded from the analysis (Hothorn & Hornik
2021). Significance was accepted at P< 0.05.
2.4 |Lagged identification rates
The authors used lagged identification rates (LIR), the probability of
resighting an individual after a given time lag, to estimate site use of
M. alfredi at RS (Whitehead, 2001). The SOCPROG 2.9 programme
(Whitehead, 2009), specifically the “movement analysis”module, was
used. The authors compared observed individual sighting data from
2016 to 2021, when there was consistent survey effort, to several
exponential mathematical models that represented various habitat
use scenarios, including permanent residency, emigration and mortal-
ity, emigration and reimmigration, emigration and reimmigration with
mortality and a cyclical pattern of appearance. The quasi-AIC values
were used to select the best supported model due to the overdisper-
sion of the data (Whitehead, 2007). Data were bootstrapped
100 times, with 1000 maximum evaluations, to estimate the standard
error and parameter precision (Buckland & Garthwaite, 1991;
3.1 |Population demographics
Sampling effort at RS ranged from 0 to 37 dives per month, with one
or two dives of 44–72 min duration conducted per day, resulting in a
monthly sampling effort of between 44 and 1252 min (Table 1). The
TABLE 1 Sampling effort (minutes)
during primary periods (years) and
secondary periods (months) used for
Pollock's robust design of Mobula alfredi
at Red Sands, Závora, Mozambique
Secondary period 2016 2017 2018 2019 2020 2021
July 68 459 584 833 182 420
August 318 445 570 1252 569 790
September 194 771 725 615 609 828
October 95 481 632 469 44 471
November 0; omitted for PRD 696 456 369 72 333
4CARPENTER ET AL.
number of M. alfredi individuals in the photo-ID database increased
throughout the study period with large numbers of new identifica-
tions between 2010–2011 and 2017–2018 (Figure 2). Until 2016, the
number of newly identified M. alfredi surpassed resights, and after
2017, the number of resighted individuals exceeded new IDs
(Figure 3). An average of three individuals (±4.29) and up to 61 individ-
uals (10% of the photographed population) in a single day were identi-
fied visiting RS during peak season (2016–2021; n=274 total
identifications in one July–November season).
Between 2010 and 2021, the authors recorded 1509 encounters
of 583 individual M. alfredi in Závora Bay. More than half, 54% (n=
312), of these were resighted at least once; 57% (n=331) of individ-
uals were seen only within a single year and 43% (n=252) across
multiple years. The mean time interval between initial and subsequent
sightings was 455 days (±694), with 10 individuals recorded with a
resighting interval of 1000 days or more, and a maximum of
10.9 years (3996 days) between resightings. The population exhibited
an even sex ratio, whereby 44% (n=255) were females, 50% were
males (n=295) and sex could not be determined for 6% (n=33).
There was no significant difference in the mean number of sightings
between females and males 2.82 (±2.34) and 2.53 (±2.34), respec-
tively (Mann–Whitney U-test; P=0.7981). Although more males than
females were resighted (males, n=171; females, n=139) in Závora,
individuals in the database that were sighted six or fewer times con-
sisted of mostly males, whereas individuals sighted seven times or
more during the study period were almost all females (Figure 4). Only
mature females had more than 10 sightings during the study period,
with the most resighted individual identified 18 times.
The authors recorded 44 pregnancies across 36 females during
the 11 year study period. Five individuals were observed to be preg-
nant on more than one occasion, with a mean postpartum interval of
33.4 (±8.8 months; Supporting Information Figure S1). About 56%
Number of idenﬁed individualsNumber of idenﬁed individuals
FIGURE 2 Discovery curve of
identified Mobula alfredi individuals
from 2010 to 2021 in Závora,
1 2 3 4 5 6
Rao of resights/new idenﬁcaons
Year of study
2016 2020 2021
FIGURE 3 Total number of newly
identified Mobula alfredi () and the
total number of resights ( ) in each
primary period of the study, and the
ratio of resights/new at Red Sands
(), in Závora, Mozambique
CARPENTER ET AL.5
(n=326) of M. alfredi were defined as mature, 49% (n=288) being
males and 7% females (n=38), although for most females maturity
could not be determined (n=250).
3.2 |Robust design
Eighteen candidate models were evaluated in the PRD analysis.
Models that integrated Markovian emigration, with capture probabil-
ity varying by sampling effort, were best supported (Table 2). The best
supported PRD model consisted of sex-dependent survival,
Markovian temporary emigration and an effect of sampling effort on
capture probability (Table 2). Annual apparent survival was estimated
higher for males than females, at 0.848 (0.09; 95% C.I. [0.597, 0.954])
and 0.823 (0.08; 95% C.I. [0.602, 0.935]), respectively (Supporting
Information Table S2). Capture probability dependent on sampling
effort fluctuated between primary periods, with the highest in 2020
(0.69; 95% C.I. [0.60, 0.76]) and lowest in 2016 (0.16; 95% C.I. [0.14,
0.18]) (Supporting Information Table S2). Overall annual abundances
ranged from 35 (95% C.I. [30, 45]) in 2016 to 233 (95% C.I. [224, 249])
FIGURE 4 Total number of Mobula alfredi identified at Red Sands in Závora, Mozambique: female (black ), male (grey ) and undetermined
TABLE 2 Selection of Pollock's
robust design (n=18) candidate models
for estimations of population size (N),
survival (φ; constant or sex varying),
temporary emigration (γ00 and γ0;
Markovian, random or none), capture (p)
and recapture (c) probabilities (constant,
with response to capture, varying by year
or varying by sampling effort) of Mobula
alfredi individuals that use Red Sands in
Model Rank npar AICc ΔAICc Model weight Deviance
=c() 1 15 4137.92 0.00 0.846 5047.43
=c() 2 13 4141.32 3.40 0.154 5039.88
=c() 3 7 4195.45 57.53 0.000 5113.87
=c() 4 5 4198.89 60.97 0.000 5121.37
=c() 5 9 4236.52 98.60 0.000 5150.85
=c() 6 10 4238.52 100.65 0.000 5150.85
=c() 7 7 4240.40 102.49 0.000 5158.82
=c() 8 8 4242.44 104.53 0.000 5158.82
=c() 9 16 4242.52 104.60 0.000 5142.40
=c() 10 14 4245.91 107.99 0.000 5149.95
=c() 11 6 4295.44 157.52 0.000 5215.90
=c() 12 4 4299.05 161.13 0.000 5223.56
ρ=c() 13 5 4352.64 214.73 0.000 5275.13
ρ=c() 14 3 4356.10 218.18 0.000 5282.63
ρ=c() 15 11 4359.07 221.16 0.000 5269.31
ρ=c() 16 9 4362.09 224.17 0.000 5276.43
ρ=c() 17 4 4364.08 226.16 0.000 5288.59
=c() 18 2 4367.73 229.81 0.000 5296.27
6CARPENTER ET AL.
in 2017 (Table 3). Differences in annual abundance estimates were
marginal for males and females, at 20–115 and 13–110, respectively
3.3 |Lagged identification rates
The best fit LIR models were F and H, which were practically equiva-
lent at <2 based on the ΔQAIC values (Supporting Information Table
S3). Nonetheless, model H made biological sense for the data, which
incorporated immigration, reimmigration and permanent emigration
and/or mortality (Table 4). Approximately 58 individuals (S.E.=16.19,
95% C.I. [35.37, 95.71]) were estimated to be present in the study area
on a given day. Mobula alfredi individuals had a mean residence time
of 4 days (S.E.=27.82, 95% C.I. [1.53, 80.02] days), with 10 days
(S.E.=415.81, 95% C.I. [5.22, 155.49] days) away from the study area.
Permanent emigration and/or mortality was estimated at 0.00029
(S.E.=0.00029, 95% C.I.[0.00024, 0.00070]). The plotted LIR curve
decreased rapidly from the date after identification indicating that
most individuals were transient to RS, with temporal annual use of RS
TABLE 3 Population size (N) for
males, females and overall Mobula alfredi
at Red Sands in Závora, Mozambique,
from the weighted average of the best-fit
models, and the number of uniquely
photo-identified individuals between July
2016 and November 2021
Sex Method Year Weighted average S.E. 95% C.I.
Male PRD 2016 20 2.71 17–28
2017 115 3.79 110–126
2018 61 2.55 58–69
2019 59 2.50 56–66
2020 106 3.60 102–117
2021 27 1.61 26–33
Photo-ID 2016–2021 215
Female PRD 2016 13 2.19 11–21
2017 110 3.67 105–120
2018 36 1.88 34–42
2019 54 2.38 52–62
2020 74 2.87 70–83
2021 18 1.31 17–24
Photo-ID 2016–2021 168
Overall PRD 2016 35 3.63 30–45
2017 233 6.16 224–249
2018 102 3.51 98–112
2019 114 3.77 109–125
2020 185 5.22 178–199
2021 49 2.24 46–56
Photo-ID 2016–2021 401
2016 2017 2018 2019 2020 2021
FIGURE 5 Estimates of yearly
abundance of Mobula alfredi (N) ± 95%
C.I. at Red Sands in Závora,
Mozambique from 2016 to 2021,
estimated from the best-fit model
(φSexγ00Mγ0Mρs=c()) with sex as a
covariate (a; grey =male,
CARPENTER ET AL.7
(Figure 6). The plotted LIR curve then levels and decreases until the
end of the study period suggesting emigration and subsequent return
and/or return to the area each season. The declining rate of the LIR
displays individual dispersal and the shape of the curve indicates a
short residency period at the aggregation site, with reimmigration at a
later stage by a proportion of the individuals (Whitehead, 2009).
In this study, the authors describe a seasonal, site-specific aggregation
of M. alfredi at RS, an aggregation site in Závora Bay, showing this site
to be an important regional habitat for the species. Half of the
583 identified individuals displayed affinity to this location (54%
resighting rate) despite belonging to a larger, wide-ranging population
(Venables et al., 2021). A total of 312 individuals returned to RS on
multiple occasions, up to a maximum of 18 times during the 11 year
study period, with no difference in site use between the sexes.
Estimated annual abundance at RS ranged from 35 to 233 individuals
during the July–November season. This seasonal peak in abundance
combined with the resighting rate of individuals reflects the seasonal
importance of the Závora region for a proportion of the larger
M. alfredi population in southern Mozambique. Compared with other
monitored M. alfredi populations that found constant survival to be
≥0.9 (Deakos et al., 2011; Couturier et al., 2014), there was a lower
apparent survival (males, 0.848; females, 0.823) at RS, suggesting
transience during periods when conditions are not favourable for visi-
tation to Závora Bay. This was further supported by an average resi-
dence time of 4 days estimated using LIR.
Mobula alfredi habitat use varies spatially and temporally at other
well-studied locations (Armstrong et al., 2020; Dewar et al., 2008),
which is also evident in the findings. Site affinity has been globally
reported for M. alfredi, with individuals consistently returning to clean-
ing station reefs over long periods of time, up to 30 years (Couturier
et al., 2014; Couturier et al., 2018; Dewar et al., 2008; Venables et al.,
2020). The results show that M. alfredi presently aggregate at one
shallow reef in Závora, rather than a collection of deeper reefs (25–
30 m) as documented in Tofo (Marshall et al., 2011; Venables, 2020).
Higher resighting rates were found at RS (54%) compared with clean-
ing stations in eastern Australia (Couturier et al., 2011) and Tofo
(Venables, 2020), but less than Indonesia, Hawaii and the Maldives
(Couturier et al., 2011; Deakos et al., 2011; Germanov et al., 2019;
Harris & Stevens, 2021). The authors found seasonal peaks in sight-
ings at Závora, as opposed to year-round sightings at other identified
M. alfredi aggregations in the Inhambane Province (Venables, 2020).
Island populations of M. alfredi in the western Indian Ocean also
exhibit year-round site use, with seasonally driven peaks related to
monsoon winds (Peel et al., 2019; Stevens, 2016). Although oceanic
processes such as monsoonal shifts, seasonal-driven currents and
tides affect M. alfredi site use in the Komodo National Park, Indonesia
and eastern Australia, ontogenetic patterns were found to influence
habitat use in Nusa Penida, Indonesia, the Gulf of Mexico and Hawaii,
and the authors suggest these could be potential drivers of M. alfredi
use of RS (Armstrong et al., 2020; Axworthy et al., 2019; Dewar et al.,
2008; Germanov et al., 2019; Harris et al., 2021; Stewart et al., 2018).
Further telemetry studies and direct assessments of zooplankton
abundance and composition may be needed to identify the drivers of
M. alfredi visitation to Závora and improve our understanding of them.
Mozambique and Australia are among few places in the world
where M. alfredi live along an extended continental coastline, which
may explain the observed transience of individuals at these locations
(Armstrong et al., 2020; Venables, 2020). Long-term monitoring of
both of these M. alfredi populations show habitat use of an entire
coastline where movement patterns may result from temporal shifts
in productivity, as opposed to island habitats, which may have more
TABLE 4 Model selection for lagged identification rate of reef
manta rays in Závora Bay, Mozambique (2016–2021)
Model Model description ΔQAIC
A Closed (1/a1=N) 89.60
B Closed (a1=N) 89.60
C Emigration/mortality (a1=emigration rate;
D Emigration/mortality (a1=N;a2=mean
E Emigration +reimmigration (a1=emigration
rate; a2/(a2+a3) =proportion of population
in study area at any time)
F Emigration +reimmigration (a1=N;a2=res
time in; a3=res time out
G Emigration +reimmigration +mortality 9.93
H Emigration +reimmigration +mortality a1=N;
a2=res time in; a3=res time out;
I Cyclical a1cos (a2td)+a3 93.56
FIGURE 6 Empirical data (mean ± S.E.) for the lagged
identification rate, the probability of re-identifying Mobula alfredi in
Závora Bay, Mozambique, over increasing time periods, with fitted
emigration plus reimmigration plus mortality model
8CARPENTER ET AL.
reliable food sources in the area (Armstrong et al., 2020; Peel et al.,
2019, Peel et al., 2020; Rohner et al., 2013; Venables, 2020). The lon-
gest point-to-point migration reported for an individual M. alfredi was
1150 km in Australia (Armstrong et al., 2019), whereas telemetry stud-
ies in Mozambique found rapid movements of up to 90 km in a single
day (Venables et al., 2020). The Inhambane coastline consists of a nar-
row continental shelf with mesoscale, eddy-driven upwelling in the
Mozambican channel, which contributes to productivity, thus its fluc-
tuation may drive M. alfredi movements up and down the coast
(Quartly & Srokosz, 2004; Rohner et al., 2013). The support of
Markovian emigration in the PRD models further implies that some
M. alfredi individuals leave for multiple seasons and eventually return.
Variations in movement and visitation patterns between the years
could be attributed to oceanic processes that affect zooplankton
patchiness and distribution including El Niño Southern Oscillation
(ENSO) and/or dipole effects (Beale et al., 2019; Folt & Burns, 1999;
Whitney & Crow, 2007).
The annual abundance of M. alfredi identified at this single reef in
Závora is high when compared to aggregations in Hawaii (Axworthy
et al., 2019; Deakos et al., 2011), the Seychelles (Peel, 2019) and
Japan (Kashiwagi, 2014), and lower when compared to the seasonal,
site-specific, aggregation at Lady Elliot Island, Australia (Couturier
et al., 2014). Previously published abundance estimates (2003–2012)
from the Tofo region of the Inhambane Province (Marshall et al.,
2011; Venables, 2020) were larger than our estimates for Závora, but
with fewer overall resightings. Nonetheless, after 2013, Venables
(2020) found <100 M. alfredi individuals to be using the reefs around
Tofo, whereas in the present study abundances at RS were consis-
tently >100 from 2017 to 2020. Abundance estimates between 2016
and 2021 varied noticeably, with 2017 and 2020 having greater cap-
ture rates compared to other primary periods. Such variation each
year may be attributed to productivity shifts or ontogenetic factors,
although further study is required to confirm this.
Both sexes displayed similar use of RS in contrast to many moni-
tored locations where females are more frequently resighted
(Marshall et al., 2011; Setyawan et al., 2018). The observed even sex
ratio in this study supported preliminary findings by Venables (2020),
but in contrast to the 61% female-bias found in Tofo (Venables,
2020). Often when a greater geographic area is monitored with
increased information on the metapopulation, even sex ratios have
been reported, including in the Maldives and French Polynesia, or
more uncommonly at a single site (Carpentier et al., 2019; Perryman
et al., 2019; Stevens, 2016; Venables, 2020). Male M. alfredi were pri-
marily mature at RS, with several juveniles that later returned as
mature over the course of the study. The main difference in site use
by the sexes was that specific mature females (n=13) were resighted
on 10 or more occasions, with some of these individuals encountered
at RS over a duration of almost 11 years. Our findings of an aggrega-
tion of M. alfredi returning to this exact reef may reflect the impor-
tance of this site for sociality and/or courtship ritual (Perryman et al.,
2021; Stevens et al., 2018; Thorburn et al., 2019).
An estimated average residence time of 4 days from the LIR anal-
ysis suggests M. alfredi individuals to visit the study site for a short
period of time in peak season and then leave. The large ranges in stan-
dard error and 95% C.I. in the LIR analysis are likely due to the individ-
ual variability in sightings from the empirical data, and the variation in
sightings year to year, which was also apparent in the PRD analysis.
The residence time to RS was lower than M. alfredi populations
around islands in French Polynesia (range 66–130 days) and Coral
Bay, Australia (56 days); nonetheless, residence time out was lower
than French Polynesia (range 59–117) and Coral Bay, Australia
(92 days), suggesting that in Závora, individuals are more likely to
move in and out of the study area even during peak season
(Armstrong et al., 2020; Carpentier et al., 2019).
Challenging weather conditions, the logistics of operating in a
remote location and resource availability contributed to uneven sam-
pling effort throughout the study period. The authors accounted for
this in the PRD analysis by modelling capture probability with an
effect of sampling effort. Further limitation in sampling for the PRD
included times when an individual was present at the aggregation but
not photographed. Such limitations are characteristic of M. alfredi
photo-ID studies, including potential violations of model assumptions
(i.e., survival probability being the same for all individuals) (Deakos
et al., 2011; Couturier et al., 2014; Venables, 2020). Given the level of
anthropogenic impact (Venables, 2020) and predation pressure
(Marshall & Bennett, 2010b) affecting southern Mozambique may
result in similar survivorship of this specific aggregation. Considering
their longevity, this 6 year analysis is brief relative to the life span of
M. alfredi. Nevertheless, the PRD in this context provided baseline
estimations of the number of M. alfredi that use RS in Závora,
Mozambique, an area which is currently unprotected.
More than 20 years of research along the Inhambane Province
has identified the largest known M. alfredi population in Africa, yet
with drastic declines in sightings, of up to 88% (Marshall et al., 2011;
Rohner et al., 2013; Venables, 2020). This population is now stated to
be of immediate conservation concern by local and international sci-
entists (Peel, 2019; Rohner et al., 2013; Tibiriçá et al., 2011; Venables,
2020). Mobula alfredi is listed in Appendix II (2013) of the Convention
for International Trade in Endangered Species (CITES) and in Appendi-
ces I and II (2014) of the Conservation of Migratory Species of Wild
Animals (CMS). Nationally, manta species were protected under
Mozambican law in 2017 (Law 5/2017) which banned fishing of
CITES-listed species; nonetheless, little was enforced (Boletim da
Republica May 2017; Venables, 2020). As a vulnerable (Marshall et al.,
2018) and economically important species (Venables et al., 2016),
M. alfredi officially received national protection in 2021 (Boletim da
República, 2020); nonetheless, along the Inhambane coastline, they
remain under threat from indiscriminate netting and longlining, partic-
ularly in the south of the province (Marshall et al., 2011; Temple et al.,
2018). To increase protection of this mobile species in Mozambique, it
is essential to focus on priority habitats where they might be at risk,
such as RS, where a seasonal inshore aggregation occurs every year.
At present, the majority of protected critical habitat is concentrated in
the north of the province in the Bazaruto Archipelago (Pelegrín et al.,
2015). Although part of a single breeding population, photo-ID and
acoustic telemetry have indicated preferential habitat use to different
CARPENTER ET AL.9
sites, meaning that M. alfredi individuals using the northern regions do
not show equal visitation to the southern regions of Tofo and Závora
(Venables et al., 2020). Anthropogenic pressures from fishing continue
to impact the southern M. alfredi in most of their home range, includ-
ing Závora, which is at the southern extent of the area where they are
most commonly encountered in Mozambique. Therefore, the authors
recommend immediate, site-specific protection of key habitats in the
south, such as RS, as an essential step for conservation management.
They also advocate for the design and implementation of a standalone
marine-protected area in Závora Bay to protect the larger critical habi-
tat for elasmobranchs in this southern region of the Inhambane
Province (O'Connor & Cullain, 2021). The Inhambane coast was
declared a Mission Blue Hope Spot in 2022 in recognition of its diver-
sity of threatened species, and the government of Mozambique has
proposed to implement a large seascape-type environmental protec-
tion area (EPA) from the Bazaruto Archipelago southwards towards
Závora (Administraç˜ao Nacional das
Areas de Conservaç˜ao and
Conservation International, 2020). Given the trajectory of the decline
of the M. alfredi population along this coastline and the seasonal
importance of this habitat, the authors advise the protection of
Závora Bay be prioritised during this process.
M.C. conceived the central idea of the article. Data collected by
N.R.C. and Y.T. with some contributions by all authors. Analysis by
M.C. with input by S.K.V. Written by M.C. with input from all other
We thank Závora Lab and MAR Expeditions for starting the research and
management of the data. We thank Ms. Linda Cooke from Závora Lodge,
Mr. Paul Vukovich, the University of Cape Town Department of Biological
Sciences and the Marine Megafauna Foundation for supporting this work.
We thank Dr. Simon Pierce for his advice on the LIR analysis.
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ing Information section at the end of this article.
How to cite this article: Carpenter, M., Cullain, N., Venables,
S. K., Tibiriçá, Y., Griffiths, C., & Marshall, A. D. (2022).
Evidence of Závora Bay as a critical site for reef manta rays,
Mobula alfredi, in southern Mozambique. Journal of Fish
12 CARPENTER ET AL.