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Focused and Inclusive Actions Could Ensure The Per
Focused and Inclusive Actions Could Ensure The Per
DOI: 10.1111/csp2.12702
CONTRIBUTED PAPER
1
Bazaruto Archipelago National Park,
African Parks Mozambique, Vilankulo, Abstract
Mozambique Although the dugongs of Mozambique's Bazaruto Archipelago are the last
2
Oceans Economy, Cape Peninsula known viable subpopulation along the East African coast, they remain threat-
University of Technology, Cape Town,
ened by a variety of anthropogenic and natural pressures that must be addressed
South Africa
3
World Wide Fund for Nature -
to ensure their persistence. We aimed to establish recent trends in dugong abun-
Mozambique Country Office, Maputo, dance through a series of aerial surveys carried out between 2017 and 2021 over
Mozambique the Bazaruto seascape. We also assessed hotspots of dugong distribution in this
4
Institute for Coastal and Marine
region where targeted conservation measures may prove most effective. Finally,
Research, Nelson Mandela University,
Gqeberha, South Africa we modeled dugong population growth and mortality rates under varying sce-
5
Museu de Historia Natural, Universidade narios to better understand the level of risk to anthropogenic mortality. We
Eduardo Mondlane, Maputo, derived a total abundance of 325 SD 145 dugongs. While the estimates from this
Mozambique
6
study and those from surveys in 2006–2007 (359 SD 137) suggest that dugong
Administração Nacional das Áreas de
Conservação, Maputo, Mozambique abundance has not changed significantly over the past 15 years, the confidence
7
African Parks Network, Johannesburg, intervals of these estimates are too wide to detect potentially small changes rela-
South Africa tive to the subpopulation's size. The distribution of dugong sightings within the
Bazaruto seascape over the 5-year period indicates two core zones, one of which
Correspondence
Evan Trotzuk, Bazaruto Archipelago occurs outside the limits of established conservation areas. Population viability
National Park, African Parks analyses demonstrated variability around rates of unnatural mortality that
Mozambique, Vilankulo, Inhambane
9F28+7VM, Mozambique.
would cause long-term decline in abundance. Together, these results provide
Email: evant@africanparks.org strong motivations for higher level conservation actions such as the expansion
and management of formal marine protected areas in the region and the listing
Funding information
Koltes Family; Mohammed bin Zayed of the East African dugong subpopulation within the IUCN Red List of Threat-
Species Conservation Fund; Western ened Species. Our study also highlights the importance of developing alternative
Indian Ocean Science Association livelihoods and sustainably managing small-scale fisheries in collaboration with
local communities and other stakeholders in order to reduce the prevalence of
fishing equipment and anthropogenic activities that directly or indirectly
threaten dugongs in the Bazaruto seascape.
KEYWORDS
abundance, critically endangered, dugongs, East Africa, seagrass
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. Conservation Science and Practice published by Wiley Periodicals LLC on behalf of Society for Conservation Biology.
F I G U R E 1 The area surveyed in the Bazaruto seascape designated in dark gray approximately corresponds with the 20-m isobaths in
the north (black contour lines overlaid) and the 30-m isobaths in the south, which mostly covers the geographic distribution of dugongs
throughout the area (Findlay et al., 2011).
4 of 11 TROTZUK ET AL.
after the largest island in the archipelago, the Bazaruto 2.2 | Dugong abundance estimates
seascape hosts a wide diversity of marine species, includ-
ing a variety of marine mammals, five species of sea tur- We obtained dugong abundance estimates using aerial
tle, and coral reefs (Everett & Van der Elst, 2008). Two surveys flown between January 20, 2017 and May 6, 2021
conservation areas, Bazaruto Archipelago National Park (Table 1). All team members had experience with aerial
(BANP) and the Vilanculos Coastal Wildlife Sanctuary surveys, and observers had previously flown dugong sur-
(VCWS), were established to preserve this region's eco- veys. Team members communicated with each other
logical diversity. However, these MPAs protect only a through an on-board communication system. Transects
small portion of the Bazaruto seascape. The waters of this were spaced two nautical miles apart, the minimum dis-
region are highly productive, and tens of thousands of tance that allowed for the entire survey area to be studied
local residents depend on marine resources for food secu- in a single day, or approximately 5.5 h of active observing.
rity and livelihoods. Tourism also provides a vital source For each observation, rear seat observers (RSOs)
of income for communities throughout the region. Addi- reported the distance to the observation (or angle, using
tionally, the Bazaruto seascape is an integral component an inclinometer), the number of adults, and if possible
of an Important Marine Mammal Area (IMMA) that was the number of calves. A calf was defined as an individual
recently declared in 2020 (IUCN-MMPATF, 2020). less than two-thirds the size of a closely associated adult,
The survey area (approximately 3700 km2) aligned assumed to be a cow (Sobtzick et al., 2020). The front seat
with the boundaries of recent historical surveys (Findlay observer (FSO) assessed sea state and bottom visibility of
et al., 2011). It was defined by the coastline outwards each observation for evaluation consistency (only in
toward the 30-m isobath from Cabo de São Sebastião to 2021) and recorded the location of each observation using
the northern tip of Bazaruto Island (Figure 1). To the a handheld GPS.
north of the Bazaruto Archipelago, the survey area's Surveys were only flown when the weather conditions
limits were adjusted to the coastline outwards toward the were below or equal to Beaufort state 3 and when there
20-m isobath to just beyond the Save River's mouth was no precipitation (Fitzroy, 1839; Sobtzick et al., 2020).
(Figure 1). Coverage between years in this study was While dugong abundance in Australia is typically esti-
approximately similar, particularly in areas that histori- mated using strip sampling, the earlier surveys in this
cally had higher densities of dugongs. We treated the study (2017–2018) collected data intended for distance
entire study area as a single block. While dugongs may sampling estimates, given that this particular methodology
occur in deeper waters (up to around 40 m), their pres- was previously employed for dugong abundance estimates
ence and availability for detection in such habitats is rela- in the Bazaruto seascape in 2006–2007 (Buckland
tively low, and the required transect lengths offshore et al., 2005; Findlay et al., 2011). During 2021, we collected
would significantly increase safety risks (Hagihara sufficient data to derive estimates from both strip sampling
et al., 2018; Marsh et al., 2011). Historically, few dugongs and Distance sampling in order to assess the merits of
were detected in waters deeper than 20 m (Findlay each technique under the conditions particular to the
et al., 2011). We therefore did not extend our surveys into Bazaruto seascape. Given our ability to incorporate percep-
areas further out in deeper waters. tion and availability bias into the strip sampling estimate,
May 6, 21
TROTZUK ET AL. 5 of 11
we chose to report these results as our final total abun- available for detection is seen by an observer (perception
dance. However, to compare current abundance with esti- bias) (Horvitz & Thompson, 1952; Pollock et al., 2006).
mates from previous surveys, we used results derived Following each initial estimate of abundance, we used
using Distance sampling to ensure comparable methodolo- Python (version 3.8.5) to simulate 1000 surveys. We then
gies between 2006, 2007, 2017, 2018, and 2021. estimated the standard error from all simulated abundance
Following all surveys, observations were analyzed estimates (Hagihara et al., 2018; Pollock et al., 2006).
using the Distance library in R (version 4.0.5). We tested a Finally, we calculated the standard deviation and reported
variety of models, including half-normal, hazard-rate and this value alongside a final abundance estimate, derived
uniform, with various modifications such as left/right by averaging the values of N ^ from all strip-sampling
truncation and binning (Thomas et al., 2010). The models surveys.
with the lowest Akaike Information Criteria (AICs) were
evaluated using chi-squared tests (Akaike, 1987;
Pearson, 1900). The models provided dugong abundance 2.3 | Dugong distribution and occupancy
and density estimates for each survey, which were aver-
aged for a final abundance estimate. To generate comparable estimates of distribution
For strip sampling, all observations outside of the 100– between years, we mapped error-unadjusted observations
300 m strips were removed from the dataset. We applied using ArcGIS Pro (version 2.8.2). We then used the Ker-
correction factors for availability and perception bias, which nel Density function to identify areas with higher densi-
are two errors inherent to any aerial survey (Pollock ties of dugongs, which we interpreted as approximate
et al., 2006). Availability bias quantification for this survey occupancy patterns (Low et al., 2009; Silverman, 2018).
was based on availability probability estimates (pa) defined We chose this analysis due to its ease of interpretability
by two key parameters: environmental condition index and its potential to practically inform marine spatial
(ECI) and habitat depth (Appendix S1). Different values of planning efforts in the future.
pa were derived for each combination of ECI (from 0–4) in
three distinct depth ranges (0–5 m, 5–20 m, and ≥20 m)
by researchers using artificial dugong models and dive pro- 2.4 | Viability of the Bazaruto dugong
files of tagged, wild dugongs in Northern Australia's Torres subpopulation
Strait (Hagihara et al., 2016, 2018). The estimates from the
Torres Strait were assumed to be appropriate for the In order to assess the viability of the Bazaruto subpopula-
Bazaruto subpopulation (H. Marsh, personal communica- tion, we used the population viability analysis (PVA) soft-
tion). For each observation, the FSO determined the ECI ware VORTEX (version 10.5.5) to model this dugong
by pairing in-flight evaluations of sea state and bottom vis- subpopulation (Lacy & Pollak, 2021). Some life history
ibility and evaluated depth after the survey using an open- parameters, such as number of calves or reproductive inter-
source bathymetry model (GEBCO, 2020). Perception bias, vals, were extrapolated from survey results, while others,
pd, was estimated using a modified “mark-recapture” such as lifespan or natural mortality rates, were obtained
approach designed for double observers (Ferreira from other sirenian subpopulations (Appendix S2). In cases
et al., 2011; Seber, 1982). where no data were available for dugongs (e.g., natural
To incorporate availability and perception bias (and mortality), these parameters were drawn from studied sub-
their associated errors) into the final strip sampling abun- populations of West Indian manatees (Trichechus manatus;
dance estimate, an initial error-adjusted estimate (N^) Marsh et al., 2011). We ran PVA iterations 1000 times using
was calculated from each survey using a modified Hor- our strip sampling-derived abundance estimate. In order to
vitz Thompson estimator: account for uncertainties around key life history character-
istics of the Bazaruto subpopulation, we ran six different
X
n
1 models assuming two different calving intervals (2.5 or
^¼
N , ð1Þ
j¼1
^aj p
pb p ^dj 3.0 years) and three different ages of first offspring (8, 10, or
12 years; Hagihara et al., 2016; Marsh et al., 2011). By doing
so, we aimed to estimate different potential growth rates to
where n is the total number of dugongs observed during a understand how the subpopulation may grow in the future
single survey, pb is the probability that a strip was sampled under optimal conditions (no anthropogenic mortality).
in the study area (equivalent to the proportion of the study We also modeled two different mortality scenarios to
area sampled), p^aj is the probability that the animal was estimate the unnatural death rate threshold after which the
available for detection within the sampled area (availabil- subpopulation's abundance begins to decline. Our first mor-
ity bias), and p^dj is the probability that an animal tality model, which assumed a more cautious scenario in
6 of 11 TROTZUK ET AL.
which reproductive rates were as unfavorable as biologically where z is the standard normal variate equal to 0.842 and
possible, assumed an age of first offspring of 12 years and a CV(N) is the coefficient of variation for the population esti-
calving interval of 3 years. Our second mortality scenario mate (Wade, 1998). For dugongs, Rmax can be assumed as
assumed an age of first offspring of 8 years and a calving either 0.03 or 0.05 depending on whether calving ratios
interval of 2.5 years. All simulated mortality assumed that are every 3.0 or 2.5 years, respectively, and FR is assumed
only adults were killed, and that males and females had an to be 0.1 or 0.5, which is a standard value for endangered
equal likelihood of unnatural death. or vulnerable species, respectively (Hagihara et al., 2016;
The PBR, a frequently used, conservative metric to cal- Marsh & Sobtzick, 2019). We subsequently compared PBR
culate sustainable human harvest of marine mammals, estimates with VORTEX-derived threshold mortality rates
was also calculated to provide a more cautious estimate of to provide a range of targets for management authorities
sustainable mortality rates (Hagihara et al., 2016). PBR has and other support groups involved in conserving dugongs
demonstrably captured trends in other marine mammal throughout the Bazaruto seascape.
stocks even with uncertainties around biological parame-
ters and relies only on an abundance estimate (Punt
et al., 2020). The many assumptions that are required for 3 | RESULTS
VORTEX are, thus, not necessary for this calculation. We
calculated PBR as During the 10 surveys, we observed dugongs on 163 occa-
sions, totaling 345 individuals (Figure 3a). Of these indi-
1 viduals, 42 were calves (12%). Average group size across
PBR ¼ N min Rmax F R ð2Þ
2 was 2.12 SD 2.08 individuals (Appendix S3). Group size
ranged from one to eight individuals (Figure 3a). Over
where Nmin is the minimum population estimate, Rmax is 50% of observations were of a single dugong (n = 88),
the estimated net population productivity, and FR is a while 38% were of two to four individuals (n = 63).
safety factor to account for additional uncertainties
(Wade, 1998). Nmin is equal to
3.1 | Dugong abundance estimates
N^
N min ¼ qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi , ð3Þ
Distance estimates yielded an error-unadjusted average of
exp z ln 1 þ cvðN Þ2 422 SD 146 dugongs within the study area (Table 2).
TABLE 2 Summary of dugong population and density estimates for recent surveys using both strip and distance sampling
F I G U R E 2 Abundance estimates of
dugongs for all surveys in the Bazaruto
seascape generated by distance
sampling. The two surveys in early 2018
are significantly different from all others.
Removing these two surveys, abundance
estimates suggest that the population
has remained relatively stable over the
past 4 years.
F I G U R E 3 (a) Observations of dugongs throughout the study area in dark gray from all surveys from 2017 to 2021. Circles with black
dots indicate observations when at least one calf was observed. (b) Kernel density map of all dugong observations throughout the study area.
(c) Kernel density map of all calf observations throughout the study area. (d) Kernel density map of all dugong observations in 2017.
(e) Kernel density map of all dugong observations in 2018. (f) Kernel density map of all dugong observations in 2021. *All kernel density
analyses used uncorrected observations.
Estimates derived from two surveys on March 12, 2018 estimates while excluding these two outliers returned an
and April 19, 2018 were significantly larger than all other error-unadjusted estimate of 295 SD 102 dugongs. Strip
estimates (Figure 2; Table 2). Averaging abundance sampling yielded an average estimate of 325 SD
8 of 11 TROTZUK ET AL.
dugong subpopulation in the Torres Strait, a stronghold survey team. Dugongs may rely on these sheltered habi-
where dugong abundance is considered to be stable tats for a variety of reasons, as they may provide an area
(Fuentes et al., 2016; Hagihara et al., 2018; Marsh with seagrass where both the risk of natural predation
et al., 2015). We also found comparable mean group sizes and human fishing pressure is low. Indeed, elsewhere in
between our results and historical. These qualities are Mozambique around the Primeiras and Segundas Archi-
positive indicators of the status of the Bazaruto pelago (PSA), these types of estuaries have been noted as
subpopulation. crucial for dugongs and reportedly used for calving
The wide uncertainty around our abundance esti- (Hughes & Oxley-Oxland, 1971). In these habitats
mates demonstrates that aerial surveys should not be the throughout the PSA, intense tidal fluxes made netting
only approach used to monitor trends in the Bazaruto challenging, which may partially explain the observed
subpopulation's abundance. Strip or distance sampling absence of particularly dangerous net-based fishing
alone may be sufficient to manage and protect dugongs if methods in this part of our survey area. Understanding
the population in question fulfills basic assumptions of and preserving the conditions that make these refuges
sampling, namely an even geographic distribution and such an attractive habitat for dugongs should be a prior-
relatively high abundance (Norton-Griffiths, 1978). Other ity in order to protect and preserve such characteristics
aerial survey methods, namely total counts, are not viable and properly manage the Bazaruto subpopulation.
alternatives given this seascape's vast area and dugongs' If an environmental protected area is declared in or
prevalence of moving based on tidal fluxes, which may around the Bazaruto Seascape, the sheltered bays in the
result in the double counting of dugongs. Additional north of the study area should be afforded the highest
methods to study the BANP subpopulation are thus nec- degree of protection as soon as possible. This high-level
essary to detect fluctuations or changes more rapidly. intervention should be complemented by on-the-ground
Abundance estimates generated by strip sampling, conservation actions that protect seagrass habitats and
which conforms to methods used to evaluate dugong sub- help minimize the use of dangerous fishing gear, such as
populations elsewhere in the world, suggest that there gill nets, which can cause unnatural dugong mortality.
are only 325 SD 145 individuals left in the Bazaruto sea- We consider initiatives that shift pressure from marine
scape (Hagihara et al., 2018; Marsh et al., 2002; Pollock resources, such as alternative livelihood development, to
et al., 2006). Surveys elsewhere in East Africa suggest be critical in achieving these objectives provided that
severe declines in dugong abundance along the coast over these programs are equitable and sustainable. Effective,
the past few decades (Marsh et al., 2011). This inferred impartial law enforcement may also help reduce the use
decline, the lack of other viable groups within the region of gill nets, which are legally banned throughout Mozam-
and the small number of individuals in the isolated bican waters. Finally, sensitization campaigns and long-
Bazaruto subpopulation should be used to inform a list- term engagement with small-scale fishing communities
ing assessment of the East Africa coastal dugong subpop- throughout the region could help prompt positive
ulation as critically endangered on the IUCN Red List of changes in natural resource management and encourage
Threatened Species (IUCN Standards and Petitions more sustainable fishing techniques.
Committee, 2019).
We acknowledge the challenge of such a low unnatural Dugong Lodge, Inhassoro, for their ongoing logistical
mortality rate. The difficulty of remaining below this support.
threshold is further complicated by the fact that dugong
mortality may go undetected in such a vast seascape. C O N F L I C T S O F IN T E R E S T
The authors declare no conflicts of interest.
5 | C ON C L U S I ON S DA TA AVAI LA BI LI TY S T ATE ME NT
The data used to support the conclusions of this article
The dugongs of Bazaruto remain the last known viable are presented in the article or supporting information
subpopulation along the East African coast and are esti- material.
mated at only 325 SD 145 individuals. These realities sug-
gest that the East African subpopulation may warrant ORCID
significant special conservation status, including classifi- Evan Trotzuk https://orcid.org/0000-0002-5356-9749
cation as critically endangered (IUCN Standards and Ken Findlay https://orcid.org/0000-0001-7154-8805
Petitions Committee, 2019). Additional conservation Almeida Guissamulo https://orcid.org/0000-0003-0415-
areas would need to be expanded to the north of BANP 2231
to ensure that this subpopulation receives targeted man- Angela Gaylard https://orcid.org/0000-0003-4899-4289
agement initiatives. Finally, irrespective of these high-
level measures, culturally-appropriate strategies, such as RE FER EN CES
alternative livelihood development, that either directly or Akaike, H. (1987). Factor analysis and AIC. In Selected papers of
indirectly reduce unnatural dugong mortality should also Hirotugu Akaike (pp. 371–386). Springer.
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Administração Nacional das Áreas de Conservação for
the population performance of the black rhinoceros in Kruger
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tion and the Mohamed bin Zayed Conservation fund for Findlay, K. P., Cockcroft, V. G., & Guissamulo, A. T. (2011).
their financial support of the surveys carried out between Dugong abundance and distribution in the Bazaruto Archipel-
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also like to thank the team at the Vilankulo Coastal Wild- of climatic variables on dugong calf production. PLoS One,
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