Notas científicas
Injuries caused by the invasive armoured suckermouth catfish
Pterygoplichthys sp. in three captive Antillean manatees
Trichechus manatus manatus
Lesiones ocasionadas por el bagre armado del Amazonas
Pterygoplichthys sp. en tres manatíes antillanos en
cautiverio Trichechus manatus manatus
1Departamento de Sistemática y Ecología
Acuática, El Colegio de la Frontera Sur, Unidad Chetumal. Avenida Centenario km
5.5, Chetumal, Quintana Roo, 77014. México.
2Conservación, Manejo y Aprovechamiento
Sustentable de Flora y Fauna AC. Calle 4 Sur-Poniente 174, Colonia Centro,
Tuxtla Gutiérrez, Chiapas, 29000. México.
ABSTRACT
Background:
The interaction between Pterygoplichthys and Florida
manatee (Trichechus manatus latirostris) was recorded
approximately 13 years ago in Florida, United States. In Mexico, this
interaction has not been documented neither in the wild nor in captivity.
Until now it was supposed that Pterygoplichthys attach to
manatees to forage the epibiota of the skin without causing any damage.
However, some behaviour displayed suggests pain, stress, and discomfort when
these fish attach to the manatee’s skin.
Goals:
To determine if the skin wounds found in three captive manatees are
associated with the presence of Pterygoplichthys in the
facilities where they are housed.
Methods:
By trawling a large artificial lagoon (AL) for three consecutive days, every
six months for two and a half years we decimated the local population of
Pterygoplichthys; in the management pool (MP), fish
were removed manually. Additionally, we reduced the time individuals spent
in the management facilities by releasing them into the AL.
Results:
Total disappearance of the skin wounds was achieved in three years, due to
their decreased interaction with the catfish (both through the reduction of
the population of Pterygoplichthys and of the time spent by
the manatees in the MP).
Conclusions:
Injuries were caused by the fact that manatees lived in a small space,
without food available for the catfish, which caused an increase in the
frequency and aggressiveness of the encounters. Therefore, we recommend
creating and implementing strategies to reduce
Pterygoplichthys populations in places where manatees
inhabit, because in the future the wounds they cause could be a potential
threat for the long-term population viability of the endangered Antillean
manatee.
Keywords: Antillean manatee; Chiapas; Interactions; Invasive species; Pterigoplichthys
RESUMEN
Antecedentes:
La interacción entre Pterygoplichthys y el manatí de Florida
(Trichechus manatus latirostris) se registró desde hace
aproximadamente 13 años en Florida, Estados Unidos. En México, esta
interacción no ha sido documentada en vida libre ni en cautiverio. Hasta
este momento, se creía que el pez diablo se adhería al manatí solamente para
consumir la epibiota que vive en su piel sin ocasionarle ningún daño. Sin
embargo, algunos comportamientos documentados sugieren dolor, estrés e
incomodidad cuando este pez se adhiere a la piel del manatí.
Objetivos:
Determinar si existe una relación entre las heridas cutáneas presentes en
tres manatíes en cautiverio y la presencia de
Pterygoplichthys en las instalaciones donde se
encuentran albergados.
Métodos:
Se diezmó la población de Pterygoplichthys mediante la
técnica de arrastre en una laguna artificial grande (LA) durante tres días
consecutivos, cada seis meses durante dos años y medio; en el estanque de
manejo (EM), la remoción fue manual. Además, redujimos el tiempo que los
individuos pasaban en el EM al liberarlos en la LA.
Resultados:
La desaparición total de las heridas cutáneas se logró en dos años y medio,
gracias a la reducción de la interacción de los manatíes con los peces
diablo (tanto a través de la reducción de la población de
Pterygoplichthys como a que se disminuyó el tiempo que
pasaban los manatíes en el EM).
Conclusiones:
Las lesiones ocasionadas por Pterygoplichthys se debían a
que los manatíes habitaban en un espacio reducido y sin alimento disponible
para los peces; esto causó un aumento en la frecuencia y agresividad de los
encuentros. Por lo que recomendamos crear e implementar medidas para reducir
las poblaciones de peces diablo en los lugares donde habitan los manatíes,
ya que en el futuro esto podría convertirse en una amenaza para la
viabilidad a largo plazo de las poblaciones de una especie amenazada como lo
es el manatí antillano.
Palabras clave: Chiapas; Especie invasiva; Interacciones; Manatí antillano; Pez diablo
The Grijalva and Usumacinta rivers, the most important rivers in southern Mexico, begin
their course in Guatemala and flow through the states of Chiapas and Tabasco (Pease et al., 2012). In the
Mexican side of this basin, Miller (2005)
documented the presence of 115 fish species, 41 out of which are endemic. There are also
two species of aquatic mammals, the Neotropical river otter (Lontra
longicaudis, Olfers 1818) and the Antillean manatee (Trichechus
manatus manatus, Linnaeus 1758), considered near-threatened and endangered,
respectively, by the IUCN (Self-Sullivan &
Mignucci-Giannoni, 2008; Rheingantz &
Trinca, 2015).
Over the last 15 years, Mexican freshwater ecosystems have been affected by the presence
of the invasive armoured suckermouth catfish (Pterygoplichthys
pardalis, Castelnau 1855 and another species of the genus) (Mendoza et al., 2007). This
species is tolerant to extreme changes of temperature, flow, salinity and quality of
water (Capps et al., 2011; Bijukumar et al., 2015).
Additionally, its early reproduction, nest construction, parental care, high fertility
rate (800 to 1500 eggs per female) and larval survival have facilitated its invasion in
water bodies from all over the world (Tello et
al., 1992; Hoover et
al., 2004).
Armoured catfish interactions with other species include its predators (Power, 1984; Willard, 1985; Bistoni et
al., 1995; Aguilar & Di-Bernardo,
2004; Kasper et al.,
2008; Bonino et al.,
2009; Borteiro et al.,
2009; Cabral et al.,
2010; Ríos-Muñoz, 2015) and the
Florida manatee (T. m. latirostris) (Nico et al., 2009). This last interaction is controversial,
because it is not clear whether it is beneficial or harmful to manatee’s health. Nico et al. (2009) mentioned that
catfish attached to manatees to feed on the epibiota that live on their skin and
searching for protection from its predators. In Florida, no injured manatees had been
observed due to catfish attachment and in surveys analysing catfish gut contents, no
epibiont (e.g., copepods, nematodes, ostracods) was found only algae (Gibbs et al., 2010). However, when
manatees have a catfish attached, they have been observed agitated, irritated,
discomforted and attempting to dislodge catfish; these reactions have been also observed
when larger jacks and Archosargus probatocephalus, Walbaum 1792, peck
the manatees (Nico et al., 2009;
Gibbs et al., 2010). This
suggests that some structures of fish oral apparatus (teeth) are harming manatees.
Manatees in southern Mexico are considered abundant (Colmenero & Hoz, 1986; Álvarez et
al.,1988), but in the last two decades, orphaned and injured
animals have been rescued and transferred to different institutions (e.g., zoos,
aquariums, universities, wildlife rescue centres) (Ortega-Argueta & Castelblanco-Martínez, 2018) of the states of Chiapas
and Tabasco to provide them with veterinary clinical assistance. In most of the
facilities where these animals are housed, the water used to fill the pools comes from
the hydrological network of the lower basin of the Grijalva-Usumacinta, which increases
the frequency and intensity of the contact among catfish and manatees.
Three adult female manatees are kept in an artificial lagoon (AL) (6824 m2
total area) in Palenque, Chiapas, Mexico (17º 29’10’’ N, 92º 01’10’’ W). This lagoon is
connected to a management pool (MP) (8.40 m wide, 7.20 m long and 2.10 m deep), where
veterinarians inspect animals and keepers conduct training sessions. The water filling
these artificial water bodies is turbid and comes from a nearby lagoon (1 km away). Two
of the manatees arrived in August 2011 from an aquarium from Veracruz, Mexico. One of
them has a total length (TL) of 2.75 m (13 years old), weighing 650 kg and the other has
a TL of 2.87 m, and weighs 700 kg (14 years old). The third one (TL=3.28 m, unknown age
and weighs 850 kg) was rescued from the wild in May 2013 from nearby Catazajá wetlands
(Figure 1A). Upon its arrival, none of the
manatees presented wounds, just the wild one presented a buoyancy problem derived from
ingestion of plastic garbage. Since their arrival, the females that came from the
aquarium lived in the MP, due to the difficulty to handle them in the AL. On the other
hand, the wild female spent a few weeks in the MP while recovering from the buoyancy
problem; after the veterinarians discharged her, she was released to the AL.
In December 2013, as part of a routinely veterinary examination, the water of the MP was
removed and while examining the manatees’ skin we observed rounded and irregular lesions
through the dorsal region (head, thorax, pectoral flippers, abdomen, fluke) (Figure 1B, D-E); no other clinical sign was observed.
Cutaneous lesions of the three manatees were similar in appearance (width from 0.4 to
2.1 cm; length from 0.5 to 2.3 cm), irregular, sometimes well defined, with an abnormal
thickening of the skin showing a rough surface and a light grey to off-white coloration.
Occasionally the lesions showed very prominent borders and a whitish depressed centre
(crater-like). These lesions were interpreted as ulcers in healing process. No systemic
or topical medication was administered to the individuals. During each examination, we
observed that wounds were healing slowly from the periphery to the centre. This type of
healing process has been observed previously by one of the authors in other injured
manatees from the Mexican Caribbean (Pérez-Flores
et al., 2010). Finally, in January 2017, we performed
the last clinical evaluation and observed a total recovery of cutaneous wounds (Figure 1C).
After inspecting the MP carefully, we didn’t find any object that could cause these kinds
of injuries, except for the presence of 120 suckermouth catfish. Therefore, in May 2014
we decided to establish a protocol to reduce the population of catfish in AL and MP, and
to monitor the manatees’ skin healing process. First, we removed the water from the MP
every 20 days to take out catfish and track the healing process of the wounds. Second,
periodic extraction of catfish from the AL was performed by trawling three consecutive
days every six months for two and a half years. Since we performed the first trawling,
we decided to release the two manatees held in the MP into the AL to avoid contact
between the manatees and the catfish.
The eradication of catfish from the MP was achieved in five months by removing catfish
every time we emptied the MP (every 20 days) and closing the gates that connect with the
AL. Meanwhile, hundreds of catfish were removed from the AL since the first trawling;
however, complete eradication was not possible due to the characteristics of the
lagoon.
It was previously assumed that the interaction between P. pardalis and
manatees was not harmful for the latter (Nico et
al., 2009; Gibbs et
al., 2010). However, Williams
(2005) and Nico et al.
(2009) mentioned that catfish sometimes bite the skin of manatees, causing
them to squirm and roll, flip the fluke, increase vocalizations, and rub their body
against some superficies (e.g., branches, logs, stream bottom). Despite the fact that
manatee skin is thick, we believe that this kind of behaviour is displayed as a
consequence of pain or discomfort caused by the scrapping-feeding movements of
P. pardalis (Adriaens et
al., 2009). Catfish present a row of rake-like teeth, which they
use to scrape up to one and a half meters deep in different kind of substrates they have
invaded (Mendoza et al., 2007;
Adriaens et al., 2009).
The parts of the body where we observed the wounds (head, snout, dorsal and ventral
regions, and caudal fluke) are the same parts where catfish are usually found attached
(Nico et al., 2009).
Furthermore, the length of Pterygoplichthys sp. found in the MP (28.0
to 44.6 cm) coincides with the length (30-40 cm) of catfish attached to manatees in
Florida (Nico et al., 2009).
Williams (2005) and Nico et al. (2009) observed up to 40 catfish
attached to a single manatee for a period of four minutes; however, it only takes one
armoured catfish attached to a manatee to provoke a change in latter’s behaviour (Gibbs et al., 2010). Due to low
visibility, we only observed catfish attached (a maximum of 2 minutes) to the manatees
during the training sessions, but when manatees swam on the surface most of the fish
detached.
We hypothesize that two factors induced catfish to injure manatees. First, the long
period of time spent by manatees in the MP. The MP is a small concrete reduced space
where manatees cannot escape from catfish; this could increase the frequency and
intensity of the attachment to the skin causing the observed wounds. Second, walls and
floor of the MP were constantly cleaned, preventing the accumulation of organic
particles; thus, the only source of food for Pterygoplichthys were the
algae present in manatees’ body, and once the algae were removed, they probably began to
scrape manatees’ skin.
We assumed that the main factor that contributes to heal the wounds of the manatees was
the declining and eradication of catfish population from AL and MP respectively. This
process must be carried out through the periodic extraction followed by killing, due to
the rapid rate of colonisation of this species (Schmitter-Soto et al., 2015).
This interaction has probably been carried out since catfish invaded the fluvial-lagoon
systems of Chiapas and Tabasco; however, the turbidity of the water makes it difficult
to document it. The reduction of size of water bodies during the dry season could favour
the contact between manatees and catfish; this might be harmful for manatees’ health,
since it is speculated that dermal scavenging is associated with the papilloma virus
(Nico et al., 2009). For
these reasons, it is necessary to create and implement strategies to control or
eradicate armoured catfish populations, since there is evidence that this species is
increasingly abundant and could be a potential threat to the long-term population
viability of the endangered Antillean manatee in the South of Mexico.
ACKNOWLEDGEMENTS
We thank the personnel of the Zoological Institution in Chiapas. Special thanks to
Adriana de los Santos for helping in the manuscript. This manuscript benefited from
comments by Juan Jacobo Schmitter Soto and two anonymous reviewers.
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