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Diversity of white spot patterns in the eagle ray Aetobatus laticeps

(Myliobatiformes: Aetobatidae) in the north Pacific coast of Costa Rica

Diego Fallas-Madrigal1,2; https://orcid.org/0000-0001-9327-0752

Alejandra Castelo-Corona3; https://orcid.org/0000-0003-3378-4297

Diego Mejías4; https://orcid.org/0000-0002-0177-8274

Steve Stephens-Cárdenas2; https://orcid.org/0000-0002-6090-9158

Jennyfer Astorga-Arias5; https://orcid.org/0000-0002-8384-4342

José L. Molina-Quirós1; https://orcid.org/0000-0001-7163-6004

Sebastián Hernández1,6; https://orcid.org/0000-0002-2908-6050

1. Biomolecular Laboratory, Center for International Programs and Sustainability Studies, Universidad Veritas, San José,

Costa Rica; niuvinor@gmail.com, jmolina@veritas.cr, shernandez@veritas.cr

2. Escuela de Ciencias Biológicas, Universidad Latina de Costa Rica, San José, Costa Rica; steve.stephens@ulatina.net

3. Tecnológico Nacional de México, Campus Bahía Banderas, Jalisco, México; alejandracasteloc@gmail.com

4. Locomotion Producciones, Guanacaste, Costa Rica; diegomejias@mac.com

5. School of Management and Spanish Department, California Lutheran University, Thousand Oaks, California, United

States of America; astorgajennyfera@gmail.com

6. Sala de Colecciones, Facultad de Ciencias del Mar, Universidad Católica del Norte, Coquimbo, Chile.

Received 30-I-2021. Corrected 13-IV-2021. Accepted 12-VII-2021.

ABSTRACT

Introduction: The Pacific white-spotted eagle ray Aetobatus laticeps, has recently separated from the Atlantic

A. narinari based on both morphological and genetic evidence. This species is characterized by a dark body

with numerous white spots all over its dorsal side. Considering the type, shape, number, and distribution of these

natural markings as potential identifiers at the individual level, we studied the variation in the spot patterns.

Objective: Describe and compare the white spot pattern (type and distribution) of individuals and evaluate their

potential use as identifiers at the individual level.

Methods: We analyzed 54 videos (105 subsequent extracted photos) and 19 photographic records that were

taken at different sites along the Pacific coast of northern Costa Rica.

Results: Seventeen distinctive types of white spots were identified across the entire dorsal side of the rays.

Significant differences between each major body section (pectoral fins, back, head, and pelvic fins) were found

in the type and frequency of white spots. The type ‘single spot’ was commonly distributed across the entire

dorsal side, and the spot pattern on the pelvic fins was informative to identify 72 individuals.

Conclusions: The analysis of the type, shape, and distribution of white spots in A. laticeps determined several

combinations of white spot patterns that be used for further taxonomic description and provide potential identi-

fication of the individual for future population studies along with its distribution.

Key words: photo-ID; marks; morphology; Eastern Tropical Pacific; description; characterization; batoid.

Fallas-Madrigal, D., Castelo-Corona, A., Mejías, D., Stephens-

Cárdenas, S., Astorga-Arias, J., Molina-Quirós, J. L., &

Hernández, S. (2021). Diversity of white spot patterns

in the eagle ray Aetobatus laticeps (Myliobatiformes:

Aetobatidae) in the north Pacific coast of Costa Rica.

Revista de Biología Tropical, 69(Suppl. 2), S267-S276.

https://doi.org/10.15517/rbt.v69iS2.48323

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Assessment of the dynamics of the wild

population for their management and conserva-

tion efforts requires information from the popu-

lation trends, population sizes, and biological

parameters, i.e., longevity, sexual maturity, and

fecundity (Musick & Bonfil, 2005; Porsiel,

2018). In this regard, the discrete characteriza-

tion of the coloration pattern of a particular spe-

cies and the identification of the population’s

members is imperative to appraise population

constraints (Porsiel, 2018). For instance, mark

and recapture methods have allowed individual

identification and provided insights into the

migration and behavior patterns in areas where

species can be observed year-round, among

other biological parameters (Cerutti-Pereyra

et al., 2017; Flowers, Henderson, Lupton, &

Chapman, 2017; Sellas et al., 2015).

Invasive and non-invasive methods are

used to tag individuals in the wild (Speed,

Meekan, & Bradshaw, 2007). Non-invasive

methods such as pigmentation patterns and

spotted mark analysis, serve to identify indi-

viduals, e.g., the jaguar Panthera onca (Lin-

naeus 1758) (Carrera-Treviño, Lira-Torres,

Martínez-García, & López-Hernández, 2016),

the tiger Panthera tigris (Linnaeus 1758)

(Ullas-Karanth & Nichols, 1998), butterflies

such as Heliconius charitonia ramsdeni Com-

stock & Brown 1950 (Denis-Ávila & Cruz-

Flores, 2017), the whale shark Rhyncodon

typus Smith 1828 (Andrzejaczek et al., 2016)

and the spotted eagle ray Aetobatus narinari

(Euphrasen 1790) (Bassos-Hull et al., 2014;

González-Ramos, Santos-Moreno, Rosas-

Alquicira, & Fuentes-Mascorro, 2016). In the

case of elasmobranch species, this method is

less invasive and prevents large individuals

from experiencing episodes of stress, altering

their natural behavior and survival during the

handling process (Porsiel, 2018).

The pigmentation pattern and other ana-

tomical differences i.e., disc size, can vary

through the distribution range of eagle rays

(McEachran, De Carvalho, & Carpenter, 2002)

(Myliobatiformes: Aetobatidae). In Aetobatus

(Aetobatidae), genus comprises five species

distributed worldwide, where genetic studies

reveal three allopatric species: A. narinari in

the Atlantic, A. ocellatus (Kuhl 1823) in the

Indo-West Pacific, and A. laticeps (Gill 1865)

in the Eastern Pacific (Naylor et al., 2012;

Richards, Henning, Witzell, & Shivji, 2009;

White, Last, Naylor, Jensen, & Caira, 2010).

The Pacific white-spotted eagle ray (A. lati-

ceps), display a bluish-black dorsal coloration

with very noticeable and abundant white spots

(Last et al., 2016). It is suggested that chromatic

and other morphological traits denote distinct

geographic units for the eagle ray A. narinari

(McEachran et al., 2002; Sales et al., 2019). In

addition, Sales et al. (2019) showed that males

of A. narinari tend to have well-defined spots,

whereas females present indistinct spots.

The North Pacific coast of Costa Rica

is highly productive and dynamic due to its

unique oceanographic characteristics, i.e.,

strong seasonal upwelling events, local and

regional ocean currents, gyres, weather condi-

tions, and ocean surface temperatures (Fiedler,

2002; Robertson & Allen, 2015). This area has

several year-round habitats for batoid species,

e.g., Urotrygon spp. (Porsiel, 2018; Robertson

& Allen, 2015), revealing large aggregations

within small shallow bays. However, other

more mobile batoid species such as A. laticeps

and Aetomylaeus asperrimus (Gilbert 1898)

may occur seasonally (Chávez et al., in press).

Here, we describe the diversity and distribu-

tion of white spots, and recaptured photo IDs

based on the entire dorsal side, in specimens

of A. laticeps from the North Pacific coast of

Costa Rica.

MATERIALS AND METHODS

Data collection: A total of 54 independent

videos (105 subsequent extracted photos) and

19 photographic records of A. laticeps were

collected from 10 sampling sites distributed

along the Pacific coast of northern Costa Rica

from January 2015 to December 2019 (Table 1,

Fig. 1). These recordings were taken on freediv-

ing surveys that ranged between 1 and 10 m

depth, using a GoPro Hero 4 camera (GoPro

Inc). On each dive, the entire dorsal side of

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each observed eagle ray was recorded. To

capture the entire, white-spotted pattern, the

videos were reviewed by targeting the frontal

plane to the dorsal side of the individuals. Each

captured video was standardized with the same

recording quality properties (1080p / 60fps vid-

eos). Because water turbidity can interfere with

video quality, efforts were made to approach

the eagle rays within 1 m to obtain the best

possible image quality.

TABLE 1

Sampling sites where Aetobatus laticeps (Myliobatiformes: Aetobatidae) individuals were recorded along

the Pacific coast of northern Costa Rica (2015-2019)

Sites Abbreviation Coordinates

Latitude Longitude

Salinas Bay SB 11°2’11” - 11°1’57” N 85°42’46” - 85°42’5” W

Rajada Beach RB 11°1’39” - 11°1’28” N 85°45’13” - 85°45’3” W

Pilas Beach PB 11°0’46” - 11° 0’37” N 85°44’37” - 85°44’29” W

Lora Island LI 11°0’39” - 11°0’34” N 85°45’5” - 85°44’58” W

Manzanillo Beach MB 11°0’28” - 11°0’23” N 85°44’0” - 85°43’54” W

Muñeco Island MI 10°59’7” - 10°58’37”N 85°43’16” - 85°42’43” W

Cornuda Island CI 11°0’17” - 10°59’60” N 85°44’56 - 85°44’39” W

Matapalitos Beach MPB 10°56’6” - 10°55’53” N 85°47’45” - 85°47’18” W

Cocineras Island CI 10°51’17’’ - 10°51’15’’ N 85°54’17” - 85°54’13’’ W

Flamingo Sting Ray City FSC 10°26’46’’ 1°26’35’’ N 85°46’42’’ - 85°46’33’’ W

Fig. 1. Map of 10 sampling sites surveyed to obtain visual material from Aetobatus laticeps. These are: Salinas Bay (SB, N

= 1), Rajada Beach (RB, N = 2), Pilas Beach (PB, N = 1), Lora Island (LI, N = 2), Manzanillo Beach (MB N = 17), Muñeco

Island (MI, N = 27), Cornuda Island (CI, N = 9), Matapalitos Beach (MPB, N = 12), Cocinera Island (CoI, N = 1), and

Flamingo Sting Ray City (FSC, N = 1). The “N” means visual samples per site.

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Data management and processing: The

database included sampling sites, dates, and

the number of videos or photos. Images were

extracted and saved from each video. To iden-

tify the white spot diversity, an initial review of

different white spot types was assessed, catego-

rizing them into single component units, and

groups (Fig. 2). These spot units were defined

as conspicuous, distinctive, and uniform shapes

that occur in A. laticeps dorsal patterns. Fre-

quent white spot types were recognized e.g.,

‘single spot’, ‘two close single spots’, ‘two

merged single spots’ and ‘semi-empty circle’,

and infrequent ones i.e., resting white spot

types. Then, these white spots were counted

for the entire dorsal side divided in four zones:

pectoral fins, back, head, and pelvic fins (Fig.

3). All white spots were visually counted using

the Adobe Photoshop CC 2017 32 bits software

and, the frequency of occurrence of each spot

type was calculated by zone.

Statistical analysis: The mean percentage

of dominant spot type ‘single spot’, was used to

test for statistical differences in left/right pecto-

ral fins, as well as left/right sides of the back,

using a univariate paired t-test implemented

in Past 3 software (Hammer, Harper, & Ryan,

2001). When no statistical differences were

found between the right/left sections of pecto-

ral fins and back, they were treated, in further

analysis, as a single analytical unit, using

mean values. For major pattern composition

analyses, only ‘single spot’, ‘two close single

spots’, ‘two merged single spots’ and ‘semi-

empty circle’ were included, as they were the

most frequent patterns (cumulative frequency

≥ 80 %). Infrequent white spot patterns were

Fig. 2. White spot type diversity identified on the entire back side of Aetobatus laticeps. (A) shows the overall diversity

of white spot types grouped according to their similarity. 1 and 2 are considered simpler white spot types while 3 to 17 are

considered complex types. (B) individual examples showing each type of white spot pattern.

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excluded from the analyses (≤ 1 % frequency).

The pelvic fins and the head were excluded

from this analysis given their relatively smaller

size, proportion, and diversity of white spots,

in contrast with the pectoral fins and back. In

addition, an ANOVA test was used to deter-

mine the differences in the occurrence of white

spots among body zones. For each test, when

significant differences were detected, a Tukey

post hoc HSD test was performed in order to

identify specific differences between mean

frequency values among body zones (α = 0.05).

Differences in body zone based on the

frequency of spot type and count were assessed

with an Analysis of Similitude (ANOSIM)

(Ornés, Herbst, Spillner, Mewes, & Rauch,

2014). ANOSIM uses permutations to identify

the similarity of samples within an assigned

group, compared to samples from other groups

(Tillett et al., 2011). A SIMPER test was then

implemented to identify the spot-type frequen-

cies generating observed differences (Fig. 3).

RESULTS

A total of 124 photos of A. laticeps

comprehended the database, i.e., 105 photos

extracted from videos plus 19 photographic

records. From this, 75 photos were assigned

to different individuals, comprising 72 indi-

viduals and 3 recaptures. Due to high-quality

resolution and accuracy to identify white spots,

only 62 photos-different individuals were used

for further analysis. Seventeen distinctive types

of white spots were identified and grouped in

four categories (Fig. 2). Not all eagle rays had

the same 17 white spot types (Table S1). Some

white spot types i.e., ‘single spot’, ‘two close

single spots’, ‘two merged single spots’, and

‘semi-empty circle’ (Fig. 2) were more frequent

than others. The most frequent white spot type

for each zone was ‘single spot’, with a value

close to 97 % for the head, followed by 63 %

for the back, 55 % for the pectoral fins, and 28

% for the pelvic fins.

When comparing right and left ‘single

spot’ frequency, no significant differences were

found in both pectorals (T = 0.250, d.f. = 1.212,

P = 0.803) and back-sides (T = 0.065, d.f. =

0.487, P = 0.949), therefore pectoral and back

zones were considered as two single units.

ANOVA and Tukey tests identified significant

differences in the frequencies of three out of the

four most common white spot patterns (Table

S2). For both ‘single spot’ (F = 86.040, d.f. =

3, P < 0.001) and ‘two close single spots’ (F =

26.890, d.f. = 3, P < 0.001), frequencies dif-

fered in all body zone pair comparisons except,

for pectoral fins and back. The ‘single spot’

was the dominant spot type on the head of each

individual sampled. For ‘two merged singles

spots’ (F = 29.630, d.f. = 3, P < 0.001), the head

presented significant differences with every

other body zone, as this spot type had signifi-

cantly low frequencies when compared to other

body zones. For ‘semi-empty circle’ spots, the

ANOVA test was performed excluding the

head section category, as it showed extremely

Fig. 3. Photo from the entire back side categorized by body

zones, showing the pectoral fins (A), back (B), head (C),

and pelvic fins (D).

Individual identification: Differentiation

of individuals from total samples was per-

formed by comparing the white spot pattern

present on each pelvic fin by eye inspection.

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low frequencies of the pattern (< 0.1 %). The

results showed no statistical differences in the

frequencies among body zones (F = 1.47, d.f. =

3, P = 0.23) (Fig. 4).

The ANOSIM test identified overall dif-

ferences in body zones associated with the

occurrence of the four most frequent white spot

types (Global R = 0.349, P = 0.001). SIMPER

analysis showed differences in the cumulative

contribution of each white spot type between

each body zone, i.e., ‘single spot’ (43.690

%), ‘two close single spots’ (20.290 %), ‘two

merged single spots’ (18.680 %), and ‘semi-

empty circle’ (17.340 %) (Fig. 4, Table S3).

The ‘single spot’ type was the most frequent

spot type in every area tested (mean range 28

% – 98 %), followed by ‘two close single spots’

(mean range 2.080 % – 24.800 %), and ‘two

merged single spots’ (mean range 0.580 % –

17.900 %). ‘Semi-empty circle’ was the least

common spot type of the major spot pattern

components (mean range 0.07 % – 11.4 %).

Overall, most individuals were recognized

based on their pelvic fins and successfully con-

firmed using the white spot pattern. From the

75 photos used for identification, two samples

were absent of visually identifiable spot pat-

terns on pelvic fins, requiring the identification

of the individual to come from the white spot

pattern of the entire dorsal side. Individual dif-

ferentiation analysis based on the white spot

pattern recognized 72 different eagle rays and

3 recaptured individuals detected from the

videos/photos.

DISCUSSION

Our results provide novel information on

the diversity of white spots of A. laticeps,

determining several combinations that should

be considered for a better taxonomic descrip-

tion (Gill, 1867; Last et al., 2016). To date,

these descriptions considered only single white

spots on the dorsal surface without mentioning

Fig. 4. Bar plots presenting the mean occurrence of the four most representative white spot types among body zones. Being

pectoral fins (—), back (—), head (—), and pelvic fins (—).

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the different types and shapes that can be

found. This diversity found is characterized by

many ‘single spots’ on their pectoral fins, back,

and head zones, while the pelvic fins have a

greater distribution of complex types of spots.

Pelvic fins are a natural marker to rec-

ognize individuals by providing a type of

fingerprint for their identification. These fin-

gerprinting marks make it easier to determine

whether an individual has already been identi-

fied or not (recaptured). In this context, we

successfully recognized more than 70 unique

individuals based on the white spot pattern in

the pelvic fins from the individual’s videos/

photos. Furthermore, identifying samples with

white spot patterns of the entire dorsal side was

also successful due to the different patterns

shown between individuals.

The study of these morphological features

can provide important data such as popula-

tion dynamics that could help to solve some

taxonomic problems (Palmeira & Rosa, 2014).

Furthermore, a study of the differences in

white spot pattern between sexes would be

useful. However, this was not studied due to

the unreliable observation of the absence or

presence of claspers in most individuals. It is

important to note that, although not part of this

study, we found some individuals (N = 4) with

black underlying edges from the pectoral tip on

the ventral body side to the dorsal side. This

is considered to be unusual (Last et al., 2016)

and is likely common in neonates and juvenile

individuals. Therefore, a better morphological

description is needed, considering more distant

sites from the continental distribution from

Mexico to Ecuador, as well as its oceanic island

distribution e.g., Cocos Island (Costa Rica).

Also, several pictures of Aetobatus indi-

viduals have revealed an additional putative

eagle ray species from Cocos Island based

on the white spot pattern. Video and pictures

recorded from several eagle rays evidence a

greyish dorsal coloration with numerous small

white spots (a minimized version of ‘single

spot’ in A. laticeps). The anterior edges from

the pectoral fins show the absence of white

spots, the posterior edge has distinct rows

of little white spots, and a moderately long

fleshy rostral lobe (Fig. 5). This white spot pat-

tern resembles its sister species, A. ocellatus.

Considering that A. ocellatus has been previ-

ously documented in Cocos Island (Bussing

& López, 2005; Garrison, 2005); it is impera-

tive to clarify the validity of the species of the

Aetobatus complex along the Eastern Tropical

Pacific. A comprehensive taxonomic study of

this genera, contrasting morphological criteria

Fig. 5. Continental and oceanic island pattern. In A, an individual of A. laticeps sighted at the sampling site (North Pacific

coast of Costa Rica), while in B a different pattern is observed found in Cocos Island.

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with molecular studies may unravel a putative

second species in the region (Concha, Caira,

Marques, & Pompert, 2014; Naylor et al.,

2012; Sales et al., 2019).

Several genetic studies have been carried

out for Aetobatus (Concha et al., 2014; Naylor

et al., 2012; Richards et al., 2009; Sales et al.,

2019; White et al., 2010), but morphological

information is scarce since material from this

genus is usually not available in biological

collections due their large size. In this context,

a general description of the white-spotted pig-

mentation on the entire dorsal side described

by Last et al. (2016) established “white spots or

ocelli” for A. laticeps and “white spot to bluish

spots” for A. narinari and A. ocellatus. This

represents a taxonomic issue with the descrip-

tion from these three allopatric Aetobatus spe-

cies with similar coloration patterns (Naylor et

al., 2012; White, 2014; White et al., 2010). The

present study provides an important finding

based on the white spot pattern which allows

the differentiation of individuals as well as

populations. Given the importance of expand-

ing the current information on the white spot

pattern in this species and possible A. laticeps

complex, further studies are needed in other

areas along its distribution, considering the

pigmentation pattern among other morphologi-

cal diagnostic features. Based on pigmentation

patterns and molecular markers tools, it would

be possible to reassess the taxonomic status of

Aetobatus species in the Eastern Tropical Pacif-

ic. Besides, the individual marks combined

with tagging programs may help to provide

unknown demographic information such as

population size, movements, and connectivity

between different regions.

Ethical statement: authors declare that

they all agree with this publication and made

significant contributions; that there is no con-

flict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are fully

and clearly stated in the acknowledgements

section. A signed document has been filed in

the journal archives.

See Digital Appendix at: /

Ver Apéndice digital en: revistas.ucr.ac.cr

ACKNOWLEDGMENTS

To the NGO Equipo Tora Carey, for

their fellow support on the collection of data,

especially to their seasonal volunteer Ariadna

Ayén-Vouillamoz.

RESUMEN

Diversidad de patrones de manchas blancas de

Aetobatus laticeps (Myliobatiformes: Aetobatidae)

en la costa del Pacífico Norte de Costa Rica

Introducción: La raya águila de manchas blancas del Pací-

fico, Aetobatus laticeps, se ha separado recientemente de A.

narinari del Atlántico basándose en pruebas tanto morfo-

lógicas como genéticas. Esta especie se caracteriza por un

cuerpo oscuro con numerosas manchas blancas en toda su

parte dorsal. Considerando el tipo, la forma, el número y la

distribución de estas marcas naturales como identificadores

potenciales a nivel individual, estudiamos la variación en

los patrones de manchas.

Objetivo: Describir y comparar el patrón de manchas

blancas (tipo y distribución) de individuos y evaluar su

uso potencial como identificadores a nivel individual en

especímenes recapturados.

Métodos: Analizamos 54 videos (con 105 fotografías

extraídas posteriormente) y 19 registros fotográficos que

fueron tomados en diferentes sitios a lo largo de la costa

pacífica del norte de Costa Rica.

Resultados: Se identificaron diecisiete tipos distintivos de

manchas blancas en todo el lado dorsal de los radios. Se

encontraron diferencias significativas entre cada sección

principal del cuerpo (aletas pectorales, espalda, cabeza y

aletas pélvicas) en el tipo y frecuencia de manchas blancas.

El tipo ‘punto único’ se distribuyó comúnmente en todo el

lado dorsal, y el patrón de puntos en las aletas pélvicas fue

informativo para identificar 72 individuos.

Conclusiones: El análisis del tipo, la forma y la distri-

bución de las manchas blancas en A. laticeps determinó

varias combinaciones de patrones de manchas blancas que

se utilizarán para una descripción taxonómica adicional

y brindan una identificación potencial del individuo para

futuros estudios de población a lo largo de su distribución.

Palabras clave: foto-ID; marcas; morfología; Pacífico

Tropical Oriental; descripción; caracterización; batoideos.

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