Fibropapillomatosis in immature Green Turtles (Chelonia mydas) from the Gulf of Venezuela

Fibropapilomatosis en juveniles de Tortuga Verde (Chelonia mydas) del Golfo de Venezuela

INTRODUCTION

Fibropapillomatosis (FP) is a disease characterized by multiple cutaneous masses. This disease was first reported affecting marine turtles (MT) in the late 1930's years (yr), primarily affecting Green Turtles (GT) (Chelonia mydas). However, it has also been reported in loggerhead (Caretta caretta), olive ridley (Lepidochelys olivacea), hawksbill (Eretmochelys imbricata), leatherback (Dermochelys coriacea), and flatback (Natator depressus) turtles [20, 21, 22]. Depending on turtle size, the location and number of tumors can contribute to the animal weakening and eventually death [18].

It is known that tumors arise from a proliferation of epidermal cells (papillomas), dermal fibroblasts (fibromas), or both (fibropapillomas) [1, 20, 30]. Several studies of FP repeatedly point to an infectious etiology involving a virus or several viruses [22]. These viruses might be spread by biological vectors or may become more tumorigenic because of biotoxins [23]. FP is a widespread disease and its incidence and prevalence are mainly in shallow waters and coastal habitats where turtles apparently become infected with the infectious agent following movement to near-shore environments [1, 22].

In Venezuela, the incidence of FP has been poorly studied, mainly due to the difficulties to access to the number of localities where MT often nest and/or reproduce [12]. Balladares et al. [3] confirmed out of 391 stranding events throughout the Caribbean coast in Venezuela, only 20 MT with noticeable presence of FP tumors. Most records were from Zulia State, where only two cases were documented between 2000 and 2006 [24]. It is important to indicate that during those yr the monitoring program was not yet standardized and records were made in an opportunistic manner [4].

The Gulf of Venezuela (GV) is an important foraging ground for MT, mainly GT; this region is characterized by extensive seagrass beds, which allows turtles to feed, reproduce and develop [27]. In the GV, an extensive consumptive use (traditional and commercial) of MT, especially GT, had been documented [7, 8, 28]. This consumptive use could lead to a public health issue at local scale due to the common practice of consumption of turtle meat, blood, and oil (in some cases consumption of turtles visible infected with FP) by local fishers [4].

Here, it was compiled and summarized all information regarding immature GT with FP affectations found stranded and/or captured in the GV, in order to assess the occurrence and frequency of this disease in this important foraging ground Southern Caribbean.

MATERIALS AND METHODS

Study area

The GV is located on the north-western Caribbean coast of Venezuela. GV is positioned at the upper and exterior depression of the Maracaibo System (Latitudes 9° and 12° N, and Longitudes 70°15’ and 72°15’ W) between Zulia and Falcon States; next to Colombia and at the Southwest of Aruba, Bonaire and Curacao Islands (FIG. 1) [27]. It has a fluctuating water dynamic, and is considered a shallow water system, with depths between 20 to 30 meters (m), temperatures from 28 to 30ºC, and salinity up to 35 practical units of salinity (UPS, by its Spanish acronym) [16, 17], and with an important upwelling area [29]. Also, GV includes a variety of habitats, from sandy beaches, mangroves forests, coral reef patches to extensive, highly productive seagrass beds [25, 27].

Data collection and analysis

All data was compiled from 2008 to 2011, following the Opportunistic Notification Network (RAO, by its Spanish acronym) methodology, which is activated primarily by members of indigenous/local communities that inhabit these coasts notifying the capture, stranding and/or direct observation of any MT its location, condition (dead or alive), and any other important remark to describe the case [4, 19]. When a MT with noticeable tumors was encountered, “in situ” measures of carapace size (curved carapace length [CCL] and width [CCW]), weight (when possible), and the presence and location of tumors were documented [13, 15, 19].

The CCL was converted to Straight Carapace Length (SCL) using the equation described by Bjornal and Bolten [10] to calculate the Body Condition Index (BCI = body mass·SCL3^-1) of each turtle with FP [9]. It was also assigned to each turtle a Severity Score (SS) determined by the size and number of tumors: 0 = non-diseased, 1 = mildly afflicted, 2 = moderately afflicted and 3 = severely afflicted [2, 11]. It was determined the number of GT in each category (SS) at each capture and/or encounter site. A linear correlation between CCL and BCI in turtles with FP was also performed to evaluate this relationship [5].

RESULTS AND DISCUSSION

From 239 reported cases of stranded and/or captured MT throughout the Western coast of the GV from 2008 to 2011, only a total of 7 individuals (2.93 %) of immature GT were reported showing large masses or skin tumors in several parts of the body (FIG. 2); noticing an increase in the previous number of records to 9 specimens with evident FP tumors (merging records from 2000 to 2011).

Before 2007, MT with noticeable diseases such as FP were not easily encountered or found in the GV. There were only two cases registered between 2000 and 2006 (1.71 % of total records; BCI = 0.63; category 1) [24]. From 2008 to 2011 monitoring and evaluation of diseases in the area increased significantly, recording a total of 7 new confirmed cases of FP in sea turtles from the GV [15, 19].

FP is considered a threat to GT populations worldwide, mainly due to its prevalence and severity [11, 22]. Overall, most MT with FP evaluated were immature (85.7 %), with CCL larger than 35 centimeters (cm), which correspond to findings in Florida, Hawaii, Brazil and Australia [2, 11, 14]. Previous research has proposed two potential explanations for the presence of FP in smaller (i.e. younger) turtles, as these individuals are exposed to the virus and several stressors associated with migration upon recruitment to neritic zones, which indicates a horizontal transmission. These stressors also might enhance the emergence of tumors and FP lesions in latently infected turtles [22]. Direct transmission may also be occurring between co-habiting turtles via interactions such as mating and aggression [20, 22]. The GV is known to be a recruiting and development area for MT, specifically, the GT population in the GV includes individuals from many rookeries throughout the Caribbean (such as Florida, México, Colombia, Costa Rica, Nicaragua, Isla de Aves [Venezuela], among others) [6] with a large number of immature individuals, hence resulting the most affected size category.

All assessed individuals were by catch from diverse artisanal fishing gears (mostly artisanal trawling nets). Body distribution of tumors (FIG. 3) was analyzed for all 7 turtles. The anterior region of the body was the most affected (37.50 % neck and venous sinus, 18.75 % anterior flippers), followed by plastron (18.75 %), posterior region (cloaca 18.75 %) and eyes (6.25 %). All individuals presented two or more body areas with FP.

As mentioned before, a larger percentage of tumors were observed in the anterior region of the MT’s body (37.50 % neck and venous sinus, 18.75 % anterior flippers). All individuals presented two or more body regions with FP, an observation also noted in studies from Florida and Hawaii [18]. According to the body distribution of these tumors, several studies indicate that external FP sometimes regress if the turtle can maintain its body condition, and also, can be treated if there are enough personnel and equipment to do so (treatments include surgical tumor removal and secondary care for debilitation) [26]. When the tumors affect the eyes and/or mouth, preventing the turtle from foraging effectively, they can lead to death from starvation. Additionally, internal tumors are particularly devastating and often overlooked when working on-site [32].

Six captured turtles with FP were registered in one locality (Kazuzain port). The average CCL was 34.7 cm (SD = 6.74 cm; Range 25.5 to 48.5) and the mean weight was 5.28 Kg (SD = 2.23 Kg; Range 1.8 to 5.9). All turtles were considered immature or juvenile (85.7 %). Only one turtle was found at another location (Porshoure port), which measured 61.9 cm CCL and had a tumor severity of the highest ranking (category 3). The individuals from Kazuzain presented a moderately afflicted condition (category 2) with 71.4 % of the total cases (FIG. 2).

MT body condition index ranged between 0.07 and 0.19. Due to the few records of turtles with FP evaluated, it was not possible to determine a significant relationship between curved carapace length, body condition index and the presence of FP in MT in the GV.

Several researchers [1, 11, 18] in the Eastern United States, Dos Santos et al. [14] in Brazil, and Van Houten et al. [31] in Hawaii have supported the argument that the occurrence and prevalence of FP are associated with coastal areas highly or moderately polluted, with high human population density, agricultural and urban runoff, sewage and/or high production of algal biotoxins. For this reason, MT are often used as a sentinel species due to their high public profile and vulnerability to degradation of the environmental health of the ecosystem [1, 22]. Although a correlation between the presence of FP and environmental factors observed in the study area was not assessed, the turtles evaluated came from coastal waters with high levels of eutrophication, habitat degradation, and pollution, which could have increased due to high precipitations during the sampling period [15, 16]. However, it is necessary to monitor environmental factors variations and/or fluctuations that can negatively affect the survival of MT populations in the GV.

CONCLUSIONS

Tumors or large skin masses related to FP were significantly noticeable from 2008 to 2011 in the immature GT from GV. Indeed, turtles with evident tumors increased from 1.71 % (between the years 2000 – 2006) to 2.93 %. Soft tissues presented in the anterior area, such as neck, venous sinus, and anterior flippers showed to be the most affected (from 37.50 % to 18.75 % of the cases recorded).

The study of MT diseases from populations in the coast of Venezuela is relatively scarce. It is necessary the assessment of the different diseases, their occurrences, dynamics, and frequency, and keep monitoring their trends over the Yr. These strategies will help on the better understanding of their implications over the MT populations that inhabit these coasts. In the GV, there is now a first in-depth approach on comprehending the occurrence and frequency of FP in immature individuals of GT.