Accepted: 12 February 2017

DOI: 10.1111/maec.12432

ORIGINAL ARTICLE

Environmental factors influencing aggregation of manta rays

(Manta birostris) off the northeastern coast of the Yucatan
Peninsula

Ana Hacohen-Domené1 | Raúl O. Martínez-Rincón2 | Felipe Galván-Magaña1 |

Natalí Cárdenas-Palomo3 | Jorge Herrera-Silveira3

1
Instituto Polinécnico Nacional–Centro
Interdisciplinario de Ciencias Marinas Abstract
(CICIMAR), La Paz, Mexico Manta rays inhabit tropical, subtropical and temperate waters. Aggregation sites of
2
CONACYT–Centro de Investigaciones
manta rays have been recognized worldwide, but the reasons for this behavior are still
Biológicas del Noroeste (CIBNOR), La Paz,
Mexico poorly understood. This study describes environmental factors influencing aggrega-
3
Centro de Investigación y Estudios tion sites of the giant manta ray (Manta birostris) off the northeastern coast of the
Avanzados–IPN, Mérida, Yucatán, Mexico
Yucatan Peninsula. Observations of manta rays were obtained from scientific surveys
Correspondence conducted during 2006–2011. Environmental data were obtained from satellite im-
Raúl O. Martínez-Rincón, Centro de
agery. The maximum entropy (Maxent) method for habitat modeling was used to de-
Investigaciones Biológicas del Noroeste
(CIBNOR), La Paz, Mexico. termine the effects of environmental conditions on the species and predict suitable
Email: raul.martinez.rincon@gmail.com
habitat for manta rays in this region. Primary productivity and distance to the coast
Funding information were the most influential variables, suggesting that aggregation occurs in highly pro-
‘Programa de monitoreo del habitat del
ductive coastal waters. The distribution of manta rays predicted by the Maxent model
tiburón ballena’ (CINVESTAV/PRONATURA
Whale Shark Habitat Monitoring Program); showed that the most suitable habitat within the study area is located off the north-
Proyecto Fondo Mixto FOMIX-Yucatán;
eastern coast of the Yucatán Peninsula, more precisely, northeast of Isla Holbox and
Programa de Pequeñas Donaciones del
PNUD; Nature Conservancy northwest of Isla Contoy. Seasonal patterns of distribution suggest that the most suit-
able conditions are present from July through September.

KEYWORDS
habitat suitability, maxent, primary productivity, satellite imagery

1 | INTRODUCTION
The genus Manta has two species: (i) Manta birostris, the most widely
distributed, inhabiting tropical, subtropical and temperate waters of
the world; and (ii) Manta alfredi, a smaller species, inhabiting coastal,
tropical waters of the Pacific and Indian Oceans (Marshall, Compagno,
& Bennett, 2009). Recent morphological and meristic evidence sup-
ports the existence of a third species, currently called Manta sp. cf.
birostris (commonly called the Caribbean manta), which is found in the
Caribbean Sea, Gulf of Mexico, and along the east coast of the USA
(Marshall et al., 2009). Discussion of this potential third species has re-
cently increased as a result of a study conducted by Hinojosa-­Alvarez,
Walter, Diaz-­Jaimes, Galván-­Magaña, and Paig-­Tran (2016), in which
the authors presented genetic and morphometric evidence supporting
a third Manta ray species, resident to the coastal waters of the Gulf of
Mexico. However, until formally accepted, and for the purpose of this
study, we list this manta ray as M. birostris.
Manta birostris aggregate in certain areas and remain resident or
aggregate seasonally and make seasonal long-­
distance migrations
(Dewar et al., 2008; Graham et al., 2012; Girondot et al., 2015). This
species is common in areas with warm and highly productive waters.
Generally, they are passive filter feeders, feeding almost exclusively on
zooplankton, although they may also consume some fish and crusta-
ceans (Duffy & Abbott, 2003; Essumang, 2010; Graham et al., 2012).
Manta ray populations, as well as other mobulid rays, are currently
declining (Dewar et al., 2008; Marshall, Dudgeon, & Bennett, 2011;
Marshall, Bennett et al., 2011), largely due to the increasing demand
for the brachial filter plates used in traditional Chinese medicines in

Marine Ecology. 2017;38:e12432. wileyonlinelibrary.com/journal/maec © 2017 Blackwell Verlag GmbH | 1 of 9

https://doi.org/10.1111/maec.12432
2 of 9 | HACOHEN-­DOMENÉ et al.

Asia (White, Giles, & Potter, 2006). This demand has led to fishermen
targeting mobulid rays and also retaining them when caught inciden-
tally (White et al., 2006).
Ecological data on manta rays, including distribution, habitat pref-
erence and environmental factors affecting their distribution, are lim-
ited. Manta rays are listed as vulnerable in the International Union
for Conservation of Nature Red List of Threatened Species (Marshall,
Bennett et al., 2011; Ward-­Paige, Davi, & Worm, 2013). The distribution
of manta rays is assumed to coincide with areas of abundant prey and
high primary productivity, making it relatively easy to locate and exploit
populations (Ward-­Paige et al., 2013; Jaine et al., 2014). Preliminary
photo-­identification of M. birostris along the northeast coast of the
Yucatan Peninsula (Martínez-­Urrea, 2012), and analysis of satellite data
suggest strong site fidelity to this area (Graham et al., 2012).
Observations of manta rays have become an objective of recre-
ational divers and ecotourists (O’Malley, Lee-­Brooks, & Medd, 2013).
The northeastern part of the Yucatan Peninsula plays an important
role in the tourism industry. Services are provided to observe and
swim with whale sharks and manta rays, as both aggregate in large
numbers in the area (Graham et al., 2012). Most research in the area
focuses on whale sharks (Cárdenas-­Palomo, Herrera-­Silveira, & Reyes,
2010; De la Parra-­Venegas et al., 2011; Hueter, Tyminski, & de la
Parra, 2013; Cárdenas-­Palomo, Herrera-­Silveira, Velázquez-­Abunader,
Reyes, & Ordonez, 2015; Hacohen-­Domené et al., 2015), as this area
is one of the largest whale shark aggregation sites in the world (De la
Parra-­Venegas et al., 2011; Hueter et al., 2013).
Species distribution models are powerful tools for predicting hab-
itat suitability, using presence-­only data (sighting records) and relating
environmental variables to occurrence at aggregation sites (Phillips,
Anderson, & Schapire, 2006; Elith & Leathwick, 2009). We used max-
imum entropy (Maxent) models (Phillips et al., 2006) because this
by the effect of the upwelling system along the coast. Coastal up-
welling occurs throughout the year, but is more intense during spring
and summer (Merino, 1997). Marine megafauna are typically abundant
in the upwelling area (Antochiw-­Alonzo, 2010; Cuevas, González,
Segovia, & Sosa, 2010; De la Parra-­Venegas et al., 2011; Graham
et al., 2012). The study site is within the marine protected area called
the Tiburón Ballena (Whale Shark) Biosphere Reserve (DOF 2009),
adjacent to the Yum Balam Federal Protected Area and surrounding
areas (Figure 1).
2.2 | Manta ray data
Manta ray (M. birostris) sightings were recorded during scientific
surveys conducted by the Proyecto Manta Caribe (MEX-­US CN-­
09-­360) in the study area from February 2006 through December
2011. A second set of opportunistic manta ray sightings was
­recorded during scientific surveys for whale sharks conducted by
the CINVESTAV/PRONATURA Whale Shark Habitat Monitoring
Program from April 2006 through September 2011. The data
­include date and location of sighting, recorded on boats using a
Global Positioning System receiver, of manta rays. A total of 528
manta rays was observed in 146 sightings (Figure 1, Table 1).
Maxent models do not require data transformation (e.g. standardi-
zation); therefore, both data sets of manta ray sightings were used
without further data ­manipulation. Furthermore, although the ana-
lysed manta ­occurrence ­records come from two different data sets,
both were ­collected using a standardized method to locate mantas
and whale sharks in the study area.
3°N

* Manta birostris
approach is appropriate when systematic biological survey data are
lacking and/or limited in coverage. The model does not require ab-
sence data for the species being modeled; instead, it uses background
22.5°

environmental data for the entire study area.

20
0
Providing new evidence of M. birostris distribution and habitat
preferences, and identifying the areas of greatest ecological impor- Whale Shark Biosphere Reserve
22°N

tance within the range of the species are essential to ensure successful **
* *
management of the manta ray in this area. Thus, the primary goal of *** Afuera zone
***************** ***
************************** ** *
this study was to describe the suitability of habitats for manta ray in * * * * * ******
**************
21.5°N

this region through maximum entropy modeling. We also analysed the Holbox
Holbox *** * Isla
Isla Contoy
Contoy
***
*
spatial and seasonal distributions of manta rays and their variability Cabo
Cabo Catoche
Catoche * *

in response to different environmental characteristics during scien-

Isla
Isla Mujeres
Mujeres
Cancún
Cancún

tific boat surveys conducted from 2006 to 2011. These results may
100
21°N

be used as complementary information to improve management deci- 600

sions for the species in the study area.

100
0
100
20.5°N

100
Cozumel
Cozumel

2 | MATERIAL AND METHODS

8°W 86.5° 6°W

2.1 | Study area F I G U R E 1 Study area. Stars represent sightings of manta rays
from 2006 to 2011, dashed lines are isobaths (in meters) and the
The study area is located off the northern and northeastern coasts of polygon is the boundary of the Tiburón Ballena (Whale Shark)
the Yucatan Peninsula, an area of high primary productivity generated Biosphere Reserve
HACOHEN-­DOMENÉ et al. | 3 of 9

T A B L E 1 Number of observed manta

2006 2007 2008 2009 2010 2011 Total
rays (Manta birostris; shown on left) and
number of sightings (shown on right) off May [1, 1] [18, 10] [9, 8] [2, 1] [0, 0] [6, 2] [36, 22]
the northeastern coast of the Yucatan June [0, 0] [29, 13] [24, 9] [12, 4] [0, 0] [0, 0] [65, 26]
Peninsula
July [83, 17] [50, 17] [11, 5] [7, 3] [9, 2] [0, 0] [160, 43]
August [49, 6] [74, 15] [13, 11] [1, 1] [38, 7] [0, 0] [175, 40]
September [3, 2] [71, 8] [16, 4] [2, 1] [0, 0] [0, 0] [92, 15]
Total [136, 26] [242, 63] [73, 37] [24, 10] [47, 9] [6, 2] [528, 146]

incomplete information regarding the target distribution (Phillips

2.3 | Environmental factors
We used sea surface temperature, concentration of chlorophyll-­a, pri-
mary productivity, depth and two bathymetry-­derived variables (dis-
tance to the coast and slope). All environmental data were obtained
from the Environmental Research Division’s Data Access Program
data server of National Oceanic and Atmospheric Administration
(Table 2). Distance to the coast and slope were computed using dis-
tance and terrain functions of the “raster” package (Hijmans, 2015) of
the software R 3.2.0 (R Core Team, 2015). As the spatial resolution
varies for the different environmental factors, they were all projected
to 0.041° grid cells, using the projectRaster function in R.
2.4 | Species distribution model
Species distribution modeling has been successfully used to model
distributions of terrestrial and marine species. The specific sta-
tistical model selected to predict habitat preference of a species
depends on the type of data available (e.g. presence/absence vs.
presence-­only). For example, if data consist of presence/absence
or abundance records, logistic regression models, like generalized
linear models or generalized additive models, can be used (Wood,
2006; Zuur, Ieno, Walker, Saveliev, & Smith, 2009). However, if
data consist of presence-­only data and no standardization method
can be applied to the data to get an index to measure abundance
of the species, a Maxent model is the most suitable (Elith et al.,
2011), as this methodology uses presence records and environ-
mental background data. A Maxent model estimates a target
probability distribution and identifies the probable distribution of
maximum entropy, subject to a set of limitations that represent the
et al., 2006).
We used Maxent to describe habitat suitability for the manta ray
along the coast of the Yucatan Peninsula and determine its preferred
environmental conditions in this area. Maxent is part of the “dismo”
package in the R 3.2.0 software. For modeling, we used the six envi-
ronmental factors listed above as predictor variables, and geographic
location of manta rays as single occurrence records (i.e. ignoring the
number of animals sighted) as the response variable. Environmental
data were aggregated into 4 × 4 km grids cells, which is the most de-
tailed spatial resolution in the data sets.
Performance of the model was evaluated using the area under
curve (AUC). The AUC represent the probability that a random positive
instance and a random negative instance are correctly classified. In
presence-­only modeling, the technique is applied to distinguish pres-
ence from random occurrence, rather than presence from absence
(Phillips et al., 2006). The AUC is an indicator of whether the model
predicts species distribution better than random conditions, and can
be used to prove statistical significance. An AUC >0.5 indicates the
model performed better than random, 0.5 indicates “random” and <0.5
means that the model performed worse than random (Phillips et al.,
2006).
To determine which factors contribute most to the best-­fitted
model, we used the factor contribution percentages from Maxent
modeling. These percentages are calculated as the increase in regu-
larized gain added to the contribution of the corresponding factor for
each iteration of the training algorithm. The increase in regularized
gain is added to the contribution of the corresponding factor or sub-
tracted from it if the change to the absolute value of lambda is nega-
tive (Hijmans, Phillips, Leathwick, & Elith, 2015).

TABLE 2 Environmental variables used as background data in the maximum entropy model

Spatial and temporal

Environmental variable Data source resolution Units

Sea surface temperature Environmental Research Division’s Data Access Program (ERDDAP) .041°monthly °C
http://coastwatch.pfeg.noaa.gov/erddap/index.html
Chlorophyll-­a concentration ERDDAP http://coastwatch.pfeg.noaa.gov/erddap/index.html .041°monthly mg/m3
Primary productivity ERDDAP http://coastwatch.pfeg.noaa.gov/erddap/index.html .083°monthly mg C·m−2·day−1
Depth ERDDAP http://coastwatch.pfeg.noaa.gov/erddap/index.html .008°static m
Distance to the coast Derived from bathymetry .008°static km
Slope Derived from bathymetry .008°static Degrees
4 of 9 | HACOHEN-­DOMENÉ et al.

T A B L E 3 Variable contributions, as
May June July August September General
percentages, and area under curve (AUC)
AUC 0.94 0.96 0.98 0.96 0.94 0.97 of the maximum entropy models for the
Depth 4.15 4.09 11.90 0.33 5.61 5.73 manta ray (Manta birostris)

Distance 41.60 31.90 18.50 8.05 53.80 25.00

Primary productivity 51.60 63.60 54.40 83.10 15.90 59.60
SST 1.03 0.46 6.34 4.57 23.10 6.13
Slope 1.56 0.00 8.89 4.00 1.62 3.52

Variables contributing the most to each model are highlighted in bold. Details of the environmental
variables are described in Table 2.
SST, sea surface temperature.

We also examined seasonal variability in manta ray distribution by
constructing five Maxent models, one for each month (May through
September). Each model was constructed using the monthly average
of the environmental factors obtained from satellite images from 2003
through 2015.
We used the best-­fit model, referred to herein as the general
model (Table 3), to predict spatial distribution of the probability of oc-
currence of manta rays off the coast of the Yucatan Peninsula; these
predictions can be interpreted as an index of habitat suitability and
have values from 0 to 100. Additionally, we used environmental data
of the 5 months and the 5 monthly Maxent models to describe sea-
sonal variability in the distribution of the manta ray.
3 | RESULTS
From May 2006 through September 2011, 146 sightings of manta
rays were recorded. Most of them were observed swimming alone
or in pairs; however, some sightings consisted of groups of 10 or
more swimming together. Most manta rays were observed in July
and August (Table 2). Most were observed within the Tiburón Ballena
Biosphere Reserve, north of Cabo Catoche (at the eastern tip of Isla
Holbox) and northwest of Isla Contoy (Figure 1). Manta rays were
observed within 50 km of the shore in water <100 m and a bottom
with a low slope gradient (<0.5°). This area is in the transition zone
between the Gulf of Mexico and the Caribbean Sea.
Average sea surface temperatures in this area range from 24.8°C
during January–February to 29.1°C during August–September
(Figure 2). The concentration of chlorophyll-­a (Chla) peaks during July
(mean Chla = 1.7 mg C/m3) and is lowest in November–December
(mean Chla = 0.9 mg C/m3). These concentrations agree with maxi-
mum (July mean = 2766.7 mg C·m−2·day−1) and minimum primary pro-
ductivity (Figure 2).
The Pearson product-­moment correlation co-efficient showed that
Chla and primary productivity are highly correlated (r = .89, p < .05).
Therefore Chla was removed from the Maxent models to avoid collin-
earity (Zuur et al., 2009), as Chla has more overdispersed values than
primary production. Correlation values obtained from the comparison
of other predictor variables had values <.6; therefore, we considered
that the collinearity among these variables was not significant (Zuur
et al., 2009; Dormann et al., 2013). The general Maxent model per-
formed better than random and produced an AUC score of 0.97. In this
model, the most influential factor was primary productivity (59.6%),
followed by distance from the coast (25.0%; Table 3). Similar results
were obtained with the monthly Maxent models: the most influential
factor in the distribution of manta rays was the primary productivity
from May to August, whereas in September the most influential vari-
able was distance to the coast followed by sea surface temperature.
The effects of the environmental factors on the presence of manta
rays were tested using partial dependence plots. These plots suggest
that the probability of the presence of a manta ray in the study area is
higher when the sea surface temperature is >27°C, at higher primary
productivity (4,500 mg C·m−2·day−1), in shallow waters (<10 m), close
to shore (<50 km) and a bottom slope <0.5° (Figure 3).
The resulting prediction map of the general model (Figure 4,
bottom-­right panel) shows that the suitable habitat for manta rays
is within the Tiburón Ballena Biosphere Reserve area, north of Cabo
Catoche and northwest of Isla Contoy.
The monthly maps of predicted habitat suitability (Figure 4) show
that there is a seasonal pattern of distribution. The May and June mod-
els predicted the lowest probabilities of occurrence, whereas the July
through September models predicted higher probabilities. From these
maps, it seems that the core area of the species is located northwest of
Isla Contoy, and this core expands in size to the west from July through
September. The Maxent model constructed with data from May seems
to have poor predictive performance; therefore, this specific model’s
predictions must be taken with caution.
4 | DISCUSSION
Acoustic and satellite tracking programs have been successfully de-
ployed to describe the distribution of manta rays in several parts of
the world (Dewar et al., 2008; Deakos, 2012; Graham et al., 2012;
Jaine et al., 2014), providing valuable information about their biology
and ecology. However, these survey programs require sophisticated
and expensive equipment and are limited to a few individuals that can
be tracked during a survey.
In this work, we used statistical methods coupled with opportunis-
tic manta ray sightings to describe the species’ distribution and habitat
HACOHEN-­DOMENÉ et al.
F I G U R E 2 Monthly changes in sea
surface temperature (SST), chlorophyll-­a
(CHLa) and primary productivity (PP) off
the northeastern coast of the Yucatan
Peninsula from 2006 through 2011.
Solid line = median, box = first and third
quantiles, whiskers = 1.5 times inter-­
quartile range
preferences. Using Maxent models, we attempt to describe the envi-
ronmental factors that led to aggregation sites in the area off the coast
of the Yucatan Peninsula from 2006 through 2011.
During this study, manta rays were present from May through
September, reflecting their seasonal presence; however, tourist ser-
vice providers and fishermen in the area state that manta rays are
present during the rest of the year (tourist service providers in Isla
Holbox, personal communication). Seasonal movements of manta
rays have been documented in Venezuela (Notarbartolo-­
di-­
Sciara
& Hillyer, 1989), New Zealand (Duffy & Abbott, 2003), Komodo
National Park in Indonesia (Dewar et al., 2008), Brazil (Luiz, Balboni,
Kodja, Andrade, & Marum, 2009), the Maldives in the Indian Ocean
(Anderson, Adam, & Goes, 2011) and Eastern Australia (Couturier
et al., 2011). Other works suggest that seasonal spatial variations in
manta ray distribution are associated with changes in water tempera-
ture or primary production (Dewar et al., 2008; Luiz et al., 2009; Jaine
et al., 2014). We observed that the distribution of manta rays varies
from May through September within the study area (Figure 4). Our
data suggest that the variability in manta rays is driven by the seasonal
upwelling present in the area, which increases the plankton concen-
trations significantly, the primary prey of the species. Although we did
not analyse feeding habits of manta rays in this study, previous stud-
ies conducted in the Yucatan Peninsula have suggested that manta
| 5 of 9
rays likely feed on copepods, chaetognaths and fish eggs (Graham
et al., 2012).
Using Maxent models, we examined the effects of depth, dis-
tance to coast, and bottom slope upon the presence of manta rays
because previous investigations (Dewar et al., 2008; Jaine et al., 2012)
mentioned that the continental shelf is an important factor affecting
upwelling. Our results show that aggregation sites occur in shallow
waters close to coasts with a low bottom slope. When the Yucatan
Current is intense during the spring and summer, upwelling occurs on
the Eastern Yucatan Shelf, leading to a two-­layered water column of
Caribbean Surface Water and upwelled water that did not mix in the
summer (Merino, 1997). Cochrane (1968, 1969) proposed that up-
welling events in this area are caused by bottom friction of the Yucatan
Current against the slope on the eastern margin of the Yucatan Shelf,
forcing upward cold and nutrient rich Caribbean waters by the rapid
change in depth (Figure S1). This creates optimal conditions for the en-
hancement of primary productivity and development of zooplankton
biomass (Cárdenas-­Palomo et al., 2010), the primary food of manta
rays.
Our results show that primary production and distance to the coast
were the most influential variables in the Maxent model (Table 3). This
reveals that manta rays are mostly in shallow, coastal waters where
upwelling is present, which relates to primary productivity. Most of
6 of 9 | HACOHEN-­DOMENÉ et al.

F I G U R E 3 Effect plots of the predictor variables on the presence of the manta ray Manta birostris, explained by maximum entropy modeling.
y-­axis represents the probability of presence. SST, sea surface temperature; PP, primary productivity; D_coast, distance from coast

the sightings were to the north of the Yucatan Peninsula, where the
continental platform is very extensive and shallow. To the east, the
depth of the platform increases abruptly. Previous research involv-
ing satellite tracking in the study area demonstrated that manta rays
are rarely sighted in water deeper than 50 m (Graham et al., 2012).
Satellite data were used to examine the movement of manta rays in
the study area, revealing movement into coastal waters where upwell-
ing and thermal fronts are present (Graham et al., 2012). Jaine et al.
(2014) found that M. alfredi tend to aggregate in areas of Australia
with high primary production forced by mesoscale eddies. We did not
search for mesoscale eddies in the study area, but we observed that
satellite imagery of Chla and sea surface temperature also suggest
that manta rays aggregate where Chla plumes and cold water mass
are present (Figure S1).
We included sea surface temperature in our analysis because it has
been correlated with the distribution of planktivorous elasmobranchs
(Dewar et al., 2008; Rowat, Gore, Meekan, Lawler, & Bradshaw,
2009; McKinney, Hoffmayer, Wu, Fulford, & Hendon, 2012; Sequeira,
Mellin, Bradshaw, Rowat, & Meekan, 2012; Sequeira, Mellin, Fordham,
Meekan, & Bradshaw, 2013; Rohner et al., 2013). During the study
period, the temperature was within the optimum temperature range
recorded for manta rays (Dewar et al., 2008; Clark, 2010; Graham
et al., 2012) and similar to temperatures recorded previously for the
study area (Merino, 1997; Cárdenas-­Palomo et al., 2015). High abun-
dance ranges from late spring (May) through late summer, generally
with a peak in July through August, when mean sea surface tem-
peratures are >26°C. In other areas, manta rays are observed where
average temperatures are lower (Kashiwagi, Marshall, Bennett, &
Ovenden, 2011). Dewar et al. (2008) stated that manta rays tolerate a
wide range of temperatures, between 21 and 30°C.
The prediction maps for August and September show that manta
rays may inhabit a more extensive area than other months in the coast
of the Yucantan Peninsula. Freedman and Roy (2012) argued that this
behavior reflects the increased primary productivity found inshore and
the search for food when coastal waters are warmest, implying that
temperature is more important when primary productivity is low.
The prediction maps show that manta rays inhabit mainly the
northeast of Contoy Island; however, in recent years (from 2009 until
now), the presence of manta rays in a zone known as “the Afuera” has
been more frequent. This zone is located southeast of Contoy Island
HACOHEN-­DOMENÉ et al. | 7 of 9

22.0

22.0

22.0
21.8

21.8

21.8
21.6

21.6

21.6
21.4

21.4

21.4
21.2

21.2

21.2
May Jun Jul
21.0

21.0

21.0
−87.4 −87.2 −87.0 −86.8 −86.6 −87.4 −87.2 −87.0 −86.8 −86.6 −87.4 −87.2 −87.0 −86.8 −86.6
22.0

22.0

22.0
21.8

21.8

21.8
21.6

21.6

21.6
21.4

21.4

21.4
21.2

21.2

21.2
Aug Sep General
21.0

21.0

21.0
−87.4 −87.2 −87.0 −86.8 −86.6 −87.4 −87.2 −87.0 −86.8 −86.6 −87.4 −87.2 −87.0 −86.8 −86.6

0 10 20 30 40 50 60 70 80 90 100
Habitat suitability (%)

F I G U R E 4 Habitat suitability maps for the manta ray Manta birostris in the northeastern coastal area of Yucatan Peninsula. The polygon is the
boundary of the Tiburón Ballena (Whale Shark) Biosphere Reserve

and outside of the protected area (Figure 1). “The Afuera” zone has
been identified as one of the most important whale shark aggrega-
tion areas in the Mexican Caribbean. De la Parra-­Venegas et al. (2011)
demonstrated that this area attracts dense aggregations of whale
sharks, even when surrounding waters are considered as oligotrophic.
These authors showed that the large aggregations are due to the pres-
ence of dense homogenous patches of fish eggs of the little tunny
(Euthynnus alletteratus), which support aggregations of large marine
animals like whale sharks and manta rays.
SUM MARY
Observations made during the study period, model results (Figure 3)
and prediction maps (Figure 4) all indicate that the manta rays use dis-
crete areas from July through September; this is an important obser-
vation that must be considered in developing management strategies.
We argue that variability in their distribution is related to the effects
of upwelling that generate biological productivity. By identifying sea-
sonal variability in manta ray distribution and the suitability of their
habitat, this study serves as an initial step toward developing new
management strategies for the area.
AC KNOW L ED G EM ENTS
We thank Ira Fogel of CIBNOR for editorial services. Funding was
provided by the ‘Programa de monitoreo del habitat del tiburón bal-
lena’ (CINVESTAV/PRONATURA Whale Shark Habitat Monitoring
Program), Proyecto Fondo Mixto FOMIX-­
Yucatán (CONACYT
#108897), Programa de Pequeñas Donaciones del Programa de las
Naciones Unidas para el Desarrollo, The Nature Conservancy, and
Project MEX-­US CN-­09-­360. A.H.D. and N.C.P. were recipients of
doctoral fellowships (CONACYT 318076 and 206588, respectively).
F.G.M. is a fellow of Instituto Politécnico Nacional - Comisión de
Operación y Fomento de Actividades Académicas and Instituto
Politécnico Nacional - Estímulos al Desempeño de los Investigadores.
We thank the editors and anonymous reviewers for their valuable
comments and suggestions, which led to significant improvements in
the final manuscript.
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How to cite this article: Hacohen-Domené A, Martínez-Rincón
RO, Galván-Magaña F, Cárdenas-Palomo N, Herrera-Silveira J.
Environmental factors influencing aggregation of manta
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