Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71(S4): e57292, diciembre 2023 (Publicado Nov. 01, 2023)

Lobomycosis Like Disease in Bottlenose Dolphins Tursiops truncatus

(Artiodactyla: Delphinidae) from Costa Rica Pacific Waters

Juan Diego Pacheco-Polanco1*; https://orcid.org/0000-0003-3592-0950

David Herra-Miranda1; https://orcid.org/0000-0003-2056-5060

Lenin Oviedo Correa1; https://orcid.org/0000-0001-8015-1367

1. Laboratorio de Ecología de Mamíferos Marinos Tropicales, Centro de Investigación de Cetáceos-Costa Rica (CEIC),

Puntarenas, Costa Rica; dpachecop@gmail.com (*Correspondence); leninovi1@gmail.com; davidceic@gmail.com

Received 02-VIII-2022. Corrected 22-IV-2023. Accepted 07-VI-2023.

ABSTRACT

Introduction: Lobomycosis, is a chronic mycotic disease of the skin and sub-dermal tissue caused by

Paracoccidioides ceti, which affects dolphins worldwide. In Costa Rica, the incidence of lobomycosis Like Disease

(LLD) has been documented in inshore common bottlenose dolphins (Tursiops truncatus) from the waters of

Golfo Dulce, South Pacific.

Objective: Examine the prevalence pattern of LLD in inshore T. truncatus from Costa Rica Pacific waters, specifi-

cally in Golfo Dulce and Golfo de Nicoya.

Methods: We examined over 20 000 photographs of T. truncatus, collected during long-term research on ceta-

ceans in 2005-2020 (n = 476 surveys), in Golfo Dulce, as well of nine sightings T. truncatus from the Golfo de

Nicoya , obtained during 17 samplings events in 2014-2022, these records for the presence of LLD allowed to

calculate the prevalence rate with a confidence interval.

Results: The prevalence rate of LLD in adult photo-identified individuals was 13.1 % (CI: 12 -14.2) in Golfo

Dulce, and 100 % in Golfo de Nicoya, considering the size of the population for the period of 2022.

Conclusion: The persistence and high prevalence levels of LLD in small, localized, communities of T. truncatus

are a cause for serious concern.

Key words: bottlenose dolphin; lobomycosis Like Disease; Golfo Dulce; Golfo de Nicoya; inshore ecotype.

RESUMEN

Enfermedad similar a la generada por Lobomicosis en delfines nariz de botella Tursiops truncatus

(Artiodactyla: Delphinidae) de las aguas del Pacífico de Costa Rica

Introducción: La enfermedad similar a Lobomicosis (LLD), asociada al hongo Paracoccidioides cetii, es una con-

dición dérmica frecuentemente reportada en pequeños cetáceos alrededor del mundo. En Costa Rica se ha docu-

mentado la presencia de LLD en Tursiops truncatus del ecotipo costero en aguas del Golfo Dulce, Pacífico Sur.

Objetivo: Examinar el patrón de prevalencia de la enfermedad en el ecotipo costero de T. truncatus en la costa

Pacífica de Costa Rica, específicamente en Golfo Dulce y Golfo de Nicoya.

Métodos: Se examinaron cerca de 20 000 registros fotográficos de T. truncatus provenientes de un monitoreo de

cetáceos a largo plazo entre el 2005-2020 (n = 476 muestreos) en Golfo Dulce, así como nueve encuentros de T.

truncatus en Golfo de Nicoya derivados de 17 muestreos realizados entre 2014-2022, estos registros fueron ana-

lizados, para identificar y estimar el índice promedio de prevalencia de LLD mediante un intervalo de confianza.

Resultados: El índice promedio de prevalencia de LLD en individuos adultos marcados es de 13.1 % (CI: 12–14.2)

en Golfo Dulce, y de 100 % en Golfo de Nicoya considerando el tamaño de la población para el periodo del 2022.

https://doi.org/10.15517/rev.biol.trop..v71iS4.57292

SUPPLEMENT • SMALL CETACEANS

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71(S4): e57292, diciembre 2023 (Publicado Nov. 01, 2023)

INTRODUCTION

Skin lesions have been described in odon-

tocetes and mysticetes worldwide (Burdett Hart

et al., 2012; Van Bressem and Van Waerebeek.,

1996; Wilson et al., 1999). They may be caused

by viruses, bacteria, fungi, and protozoa and

appear to have been increasing in frequency

during the last two decades (Daura-Jorge &

Simões-Lopes, 2011; Van Bressem et al., 2009).

Their occurrence and severity seem to be relat-

ed to natural and anthropogenic factors such as

water quality, inland water discharges, climate

change, and habitat degradation (Burdett Hart

et al., 2012; Daura-Jorge & Simões-Lopes, 2011;

Gómez-Salazar et al., 2012; Harzen & Brunnick,

1997; Kiszka et al., 2009; Moore, 2008; Van

Bressem et al., 2009; Wilson et al., 1999).

Caused by the yeast-like organism Paracoc-

cidioides ceti, (Vilela, et al., 2016), lobomycosis

(lacaziosis) is a chronic fungal disease of the skin

and subdermal tissues that affects dolphins. It is

characterized by raised, sometimes ulcerated or

plaque-like, dermal lesions of grayish, whitish,

or slightly pinkish color that can spread to dis-

figure large areas of the dorsal, dorsolateral, and

pedunculated regions of the body (Bermudez et

al, 2009; Bessensen et al. 2014; Daura-Jorge &

Simões-Lopes, 2011; Félix, Van Bressem et al.

2019; Kiszka et al. 2009; Murdoch et al. 2010;

Paniz-Mondolfi et al. 2012; Ramos et al. 2018;

Rotstein et al. 2009, Van Bressem et al. 2009,

Van Bressem et al. 2015).

Lobomycosis-like disease (LLD) is a condi-

tion whose clinical presentation is reminiscent

of lobomycosis but lacks confirmation based

on histologic and molecular diagnosis (Kiszka

et al., 2009; Ramos et al., 2018; Van Bressem et

al., 2009, 2015; Vilela et al., 2021). Nevertheless,

there is a very good correlation between at-sea

observations and corresponding photographic

documentation and laboratory diagnosis (Mur-

doch et al. 2008; Sacristan et al. 2015; Van Bres-

sem et al., 2007), even up to 100 %, as reported

by Murdoch et al. (2008). In the common bot-

tlenose dolphin, cases of lobomycosis appear to

be significantly associated with disorders of the

adaptive immune system, which may be related

to chronic exposure to chemicals and biological

pollutants (Reif et al., 2009).

In Costa Rica, the prevalence of LLD has

been documented in inshore bottlenose dol-

phins in the waters of Golfo Dulce in the period

1991-1992, 2010-2011 (Bessesen et al., 2014).

Here, we examine the prevalence of LLD in

inshore bottlenose dolphins, Tursiops truncatus

(Montagu, 1821)) from Costa Rican Pacific

waters, update previous observations of the

incidence in the Golfo Dulce bottlenose dol-

phin population ten years after the first obser-

vation, and report new cases of the disease in a

small, localized dolphin population inhabiting

Golfo de Nicoya.

Golfo Dulce is a 50 km long and 10–15

km wide tectonic embayment located in Costa

Rica between 8°33’N and 83°14’W (Acevedo

& Burkhart, 1998; Cubero, 1998; Oviedo et

al., 2015; Rincón & Ballestero, 2015; Svend-

sen et al., 2006). The main freshwater inputs

come from the Coto-Colorado, Tigre, Esquinas

and Rincón rivers. This embayment has been

divided into three sub-areas defined by topog-

raphy and oceanographic conditions: the inner

basin, the sill area, and the transitional oceanic

area at the mouth of Golfo Dulce (Dalsgaard

et al., 2003, Dalsgaard et al., 2005; Ferdelman

et al., 2006; Morales et al., 2015; Oviedo et

al., 2009, Oviedo et al., 2015; Quirós, 2003;

Thamdrup et al., 1996).

Conclusión: La alta incidencia de LLD y el tamaño poblacional notablemente reducido de T. truncatus en aguas

del Golfo Dulce y Golfo de Nicoya podría ser indicativo de una baja calidad de agua y degradación ambiental, por

la presión de las actividades humanas que se realizan en las zonas costeras.

Palabras clave: Delfín Nariz de Botella; enfermedad similar a Lobomicosis; Golfo Dulce; Golfo de Nicoya; Costa

Pacífica; ecotipo costero.

Nomenclature: SMT1: Supplementary material Table 1; SMF1: Supplementary material Figure 1.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71(S4): e57292, diciembre 2023 (Publicado Nov. 01, 2023)

Golfo de Nicoya is located on the Pacific

coast of Costa Rica (10”N, 85°W) and is one

of the largest estuaries (1 530 km²) in Central

America. It extends about 80 km from its nar-

rowest point at the mouth of the Tempisque

River to its widest point (about 55 km) where it

borders the open ocean (Maurer & Vargas 1984;

Brenes et al., 2001; Wolf et al., 1998).

We conducted 476 photo-identifica-

tion surveys in Golfo Dulce and 17 in Golfo

de Nicoya, using a 7-m-long boat powered

by a 115-horsepower four-stroke engine as

a research platform during two seasons, wet

(June - October) and dry (November - May),

from 2005 to 2022. Each survey was conducted

between 7:00 am and 4:00 pm on a given

day. There were four observers on board the

research vessel, with one observer acting as

the primary photographer, usually assisted by

another secondary surveyor, to photograph as

many dolphins in the group as possible. Photo-

graphs were taken with an SRL digital camera

(Canon 7D/70D) equipped with a 400 mm

telephoto lens. In the presence of a group of

dolphins, we photographed the dorsal fins of all

individuals within the group, as perpendicular

to the body axis as possible. Photographs were

classified according to the classes described

in Sanchez-Robledo et al. (2020). A quality

criterion was prioritized in photographic data

processing (Karczmarki et al., 2005). Therefore,

only high-quality images (80 % and above on a

quality scale from 1 to 100 %) were selected and

used in the analysis. The photo processing was

designed to eliminate any sampling bias, there-

by strengthening one of the key assumptions of

the capture-mark-recapture models, the likeli-

hood of homogeneous capture of all individu-

als in the group. Once all LLD photographic

records were organized and selected, we vali-

dated the diagnosis after consultation with an

expert (Marie-Françoise Van Bressem, personal

communication, 6 October, 2022). After analy-

sis and classification of all folders, we counted

the number of individuals with LLD.

We estimated an LLD prevalence rate,

taking into account the individual history

of encounters, which allowed us to calculate

annual prevalence indices from the rainy sea-

son of 2011 to the rainy season of 2020. This

was done by considering the annual presence

records of non-calf individuals with photo-

graphic evidence of LLD in relation to all non-

calf individuals recorded and photographed in

that year. The latter resulted in a prevalence rate

for Golfo Dulce, presented with a confidence

interval. In the case of Golfo de Nicoya, the

number of individuals with LLD in all surveys

where coastal bottlenose dolphins were record-

ed was also equal to the number of individuals

recorded and photographed per year, due to

the low number of dolphins in this population.

Data consisted of 590 T. truncatus sighting

records collected during long-term cetacean

research (2005 - 2020) in Golfo Dulce. In Golfo

de Nicoya, the data collected consists of nine

sightings of T. truncatus from 17 boat sampling

events (2014: n = 6; 2015: n = 8, 2019: n = 1,

2022: n = 2).

In the period 2005-2020, the average per-

centage of dolphins identified with LLD in

Golfo Dulce was 13.1 (CI: 12 – 14.2) in 105 dol-

phins photo-identified (Fig. 1; Supplementary

Table 1). The highest prevalence estimated in

2014 was 16.2 %, whereas the lowest prevalence

was estimated at 9.1 % in 2019 (SMT1), within

this range most of the prevalence values varied

around 12 to 14 %.

These prevalence levels are comparable

with those reported for other coastal popula-

tions of T. truncatus from South America (5.4 %

- 44.4 %), North America (12.4 %), and Tursiops

aduncus (Ehrenberg, 1832 [1833]) from Africa

(8.4 %), the percentage of individuals with skin

lesions in Golfo Dulce is consistent with those

reported in these locations (Kiszka et al., 2009;

Moreno et al., 2008; Murdoch et al., 2008; Félix,

Van Bressem et al., 2019).

The estimated prevalence of LLD in T.

truncatus from the Golfo de Nicoya was 100 %

(LLD dolphin; n = 6 from identified individu-

als, all of them adults; n = 6) (Fig. 1) in 2019

and 2022. Such a high prevalence rate in an

inshore dolphin community is unprecedented.

The highest prevalence rate reported until now

was 44.4 % in a small community (n= 9) of

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71(S4): e57292, diciembre 2023 (Publicado Nov. 01, 2023)

T. truncatus from Salinas, Ecuador (Félix, Van

Bressem et al., 2019). In Golfo Dulce the major-

ity of LLD cases were documented in males

(n=5), with only two females affected by the

disease and two unidentified sex individuals.

Similarly, in Golfo de Nicoya three males were

identified as LLD dolphins, along with two

females and one unidentified sex individual.

The lesions of the dorsal fin progressed over

years in a dolphin TtGN005 from Golfo de

Nicoya and individual TtGD003 from Golfo

Dulce (Fig. 1).

There are intrinsic demographic character-

istics that differ between these two populations,

while the coastal bottlenose dolphin population

in Golfo Dulce would be considered discrete at

just over 100 individuals, with a portion of it

showing important site fidelity (Oviedo, 2018),

the Golfo de Nicoya population is smaller than

ten individuals. In the course of our assessment,

we captured the same adult individuals on each

sampling occasion, suggesting not only site

fidelity but also an apparent lack of immigra-

tion into this population. There are other simi-

larly small populations of the coastal bottlenose

dolphin ecotype elsewhere in Latin America,

such as the Santa Elena Peninsula, Ecuador,

where these dolphins were observed intermit-

tently from 2005-2018, with a mean group size

of 5.31 dolphins/group (SD = 1. 97, range 1–10)

(Félix, Zavala et al., 2019), and in the Traman-

dai estuary in southern Brazil, where they have

been observed since the early 90s, with an aver-

age of nine dolphins (including calves) com-

monly recorded over the years (Di Giacomo &

Otts, 2016), with at least two dolphins affected

by LLD (study period 1991- 2008) (Moreno et

al., 2008). Félix, Zavala et al. (2019) suggested

that such small dolphin populations may be a

remnant of larger communities, possibly affect-

ed by external environmental stressors, likely of

anthropogenic origin. In the case of Golfo de

Nicoya, the high prevalence of LLD in such a

small community is a cause for serious concern.

Demography and social behavior influ-

ence the incidence and transmission of the

disease (Félix, Van Bressem et al., 2019). Even

though the analysis of social behavior and

characteristics of these populations is in prog-

ress. There are important similarities in terms of

sex classes occurrence, distribution, and social

behavior profiles of both populations, with that

reported by Félix, Van Bressem et al (2019).

In the case of Golfo de Nicoya, as mentioned

above, the high prevalence could be explained

primarily by the demography of such a small,

localized community, where most of the indi-

viduals affected are males, basically half of the

adults observed in the field, with at least a high

ranked individual (TtGN001; Fig.1). Whereas,

in Golfo Dulce, LLD is equally observed mostly

in males (five out of nine cases). The medium

to low prevalence rate (13.14 %) could be

affected by the incidence of the disease in one

out of two male alliances. This lower-ranked

pair (TtGD015 and TtGD016; Fig.1) had a

wider home range than the dominant alliance.

All of this supports the notion of horizontal

disease transmission and geographic spread by

non-resident individuals (Félix, Van Bressem et

al., 2019; Van Bressem et al., 2015).

Although differences in sample size may

explain some of this variation, environmental

and individual factors are also likely to play

an important role. Burdett Hart et al. (2011)

suggested that differences in freshwater input

could influence the development and persis-

tence of lobomycosis between T. truncatus

communities of west and east coast estuaries in

Florida; this could be the case for Golfo Dulce

and Nicoya.

In Golfo Dulce and Golfo de Nicoya, the

presence of polychlorinated biphenyl com-

pounds (PCBs, DDT, DDD, DDE, dieldrin, and

BHC) is associated with agriculture practices

(Spongberg & Davis, 1998; Spongberg, 2004a;

Spongberg, 2004b; Umaña., 1998. Along the

riverbanks draining into the Golfo Dulce, a

number of agricultural practices have been

developed, such as cattle ranching and mono-

cultures of African palm and banana (Umaña,

1998). The increase in these activities has intro-

duced heavy metals (Fe 5.8 ug/g, Zn 96 ug/g,

Cu 87 ug/g, Pb 6 ug/g) and organochlorine

pesticides into the water column (5000 ug/g)

and sediments (15.7 ug/g) (Acuña-González et

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71(S4): e57292, diciembre 2023 (Publicado Nov. 01, 2023)

al., 2004; Spongberg & Davis, 1998; Spongberg,

2004a; Spongberg, 2004b).

Many other anthropogenic activities,

including agriculture, forestry, tourism, aqua-

culture, salt-mining, mining and industry have

been carried out in the Golfo de Nicoya, mak-

ing the area vulnerable to contamination by

petroleum hydrocarbons, wastewater, pesti-

cides, heavy metals and organic compounds

(León Coto et al., 1998; Marín-Alpizar, 2000;

Fig. 1. A. Cases of lobomycosis-like disease in inshore bottlenose dolphins from Golfo Dulce (framed by dark blue rectangle)

and Golfo de Nicoya (framed by light blue rectangle) in the Pacific waters of Costa Rica. 1.b Lesion progression in individual

TtGD003 (Golfo Dulce) and TtGN005 (Golfo de Nicoya).

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71(S4): e57292, diciembre 2023 (Publicado Nov. 01, 2023)

Morera-Gonzalez et al., 2019;). These can be

associated with other particles and become

available to biota and bioaccumulate in the

lipid tissues of organisms (León Coto et al.,

1998; Marín-Alpizar, 2000; Morera-Gonzalez

et al., 2019).

Very low concentrations of PCBs and DDT

can bioaccumulate and suppress the immune

system of these animals, thereby facilitating the

onset of disease (Jepson et al., 2005; Reif et al.,

2009; Ross., 2002), which could be the case in

the Golfo Dulce and Golfo de Nicoya bottle-

nose dolphin population.

The anthropogenic impacts that the coastal

populations of T. truncatus have been exposed

to may become critical and even cause a decline

in the largest and smallest populations of these

coastal dolphins in the country. Although there

is no documented mortality caused by the

disease in Golfo Dulce and Golfo de Nicoya,

a high rate of disease could lead to septicemia,

considering the severity and sometimes open

lesions, these can be exposed to bacteria (Van

Bressem et al. 2015). Additionally, the spread

to key anatomical areas, such as the rostrum,

could impede prey consumption and result in

emaciated individuals. If we put more pressure

on these areas through coastal development,

such as marinas and luxury hotels, the ceta-

cean populations and the tourism industry that

depends on them would be at risk. The restrict-

ed geographic range used by these populations

of T. truncatus and the strong dependence of

these dolphins on specific environmental char-

acteristics (structure and available resources)

makes them vulnerable to habitat loss and deg-

radation. The persistence, and high prevalence

levels of LLD, in small, localized, communities

of T. truncatus in the Pacific Ocean of Costa

Rica is a cause for serious concern.

Ethical statement: the 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 acknowledgments

section. A signed document has been filed in

the journal archives.

See supplementary material

a15v71s4-MS1

ACKNOWLEDGMENTS

This study has been possible thanks to the

valuable support of citizen science, fostered by

the institutions: International Student Volun-

teers (2011-2013); in particular by the support

of Wagner Quirós, Earthwatch Institute (2013-

2023), especially the following internal funding

schemes: Arunas A and Pamela A, Chesonis

Family Foundation and Gaye Hill and Jeff Urbi-

na (2013-2014) and Gaye Hill and Jeff Urbina

(2015-2016). Special thanks to each group of

volunteers, who accompanied us on each field

trip. Thanks to our CEIC partners: the Medina

family for providing us with our base in Rincon

de Osa. Special thanks to our captain “Taboga”.

We thank Marie-Françoise Van Bressem, for

her expertise and advice and three anonymous

reviewers for their contribution to improving

the manuscript.

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