Gastrointestinal investigation of parasites and Enterobacteriaceae in loggerhead sea turtles from Italian coasts

Abstract

BackgroundCaretta caretta is the most abundant sea turtle species in the Mediterranean, and studies on this species have vastly expanded during recent years, including those investigating gut bacterial and parasitic communities. Members of these communities have been reported with variable prevalence and pathogenicity, mainly depending on their host and environment (e.g. lifespan, distribution, habitat, diet, health status and stressors). Indeed, many species commonly inhabiting the sea turtle gastrointestinal tract exhibit an opportunistic behaviour.This study aimed to provide baseline data on enterobacterial and parasitic composition, through bacteriological culture-based methods and the FLOTAC parasitological technique, in cloacal and faecal samples of 30 live Caretta caretta, examined upon their arrival at the Marine Turtle Research Centre (Portici, Italy).ResultsEnterobacteriaceae were isolated in 18/23 cloacal samples (78.3%), with Citrobacter and Morganella as the most common genera, followed by Proteus, Enterobacter, Providencia, and Hafnia. Parasitic elements were detected in 11/30 faecal samples (36.7%), with Enodiotrema, Rhytidodes, and Eimeria as most common genera, followed by Pachypsolus and Cymatocarpus. Additionally, Angiodyctium is reported for the first time in this host. The majority (47.8%) of sea turtles hosted exclusively Enterobacteriaceae, whereas 30.4% hosted both parasites and Enterobacteriaceae; the remaining 21.8% hosted neither of the agents.ConclusionsBacteria and parasites evaluated in the present study are common in Mediterranean loggerhead sea turtles, with slight differences between the western and eastern basin. Although naturally present in the gastrointestinal system of free-living sea turtles, their relationship with these hosts might range from mutualism to parasitism. Indeed, members of the gut community might express their pathogenic potential in immune-compromised animals, such as those in rehabilitation facilities. Therefore, it is advisable to include in the standard work-up of rescued sea turtles a screening procedure for such opportunistic agents, in order to better evaluate the animal’s health status and achieve timely intervention with appropriate treatment, thus improving rehabilitation. Furthermore, data collected from free-living sea turtles represent a starting point for investigating wild populations. However, further studies are needed to clarify the differences between sea turtle’s normal gut microbiome and pathobiome.

Antibiotic Resistance of Gram-Negative Bacteria from Wild Captured Loggerhead Sea Turtles

“…was found; however, some differences in terms of prevalence of some taxa were registered. In fact, Enterobacter, Citrobacter, Providentia and Shewanella were more frequently found in weak turtles; this result is in accordance with previous reports on the microbial composition of sea turtles injured by anthropogenic threats, or feeding on longlines bait and on marine debris [9,10,13,27,28]. The vulnerability of loggerhead turtles to be colonized in their gut by aerobic heterotrophic bacteria may be related to different stress conditions due to their illness or a debilitated health status that may result in an altered metabolic state [49].…”

“…have been isolated from both marine [46], freshwater fish [47] and molluscs [48]. S. putrefaciens, described as a pathogen of marine organisms, is a species commonly isolated from the cloaca of loggerhead sea turtles also in the Mediterranean Sea [9,10,28] as well as reported in this study.…”

“…Except for resistance to trimethoprim-sulfamethoxazole, that was higher in the cloacal isolates of this study (31% and 37% in healthy and weak animals, respectively) than in the latter report (22.7%), a less frequency of resistant phenotype was found. Precisely, in this survey, the percentage of isolates resistant to chloramphenicol (11% and 4% of isolates from healthy and weak animals), to ciprofloxacin (13% and 7%), to nalidixic acid (3% in both healthy and weak animals), to streptomycin (7% and 4%) and to tetracycline (18% and 7%) was lower than the resistance percentage (39%, 30%, 30%, 37% and 71%) found in other reports on stranded, recovered or dead sea turtles [9,10,28]. In a more recent report [13] on stranded and dead sea turtles, only resistance to tetracycline (19%) was similar.…”

“…The latter were the sea turtles with a problem (hook, plastic presence, gastrointestinal occlusion, collision with a boat) that needed a recovery period. A significant correlation was found among the different body measurements recorded To date, a few studies investigated the microbial community associated with Caretta caretta by using culture-dependent methods [9,10,[27][28][29] or metagenomic analysis [30][31][32], and even fewer studies were carried out on the antibiotic resistance of isolates [9,10,13,28]. All the latter studies collected samples from animals that needed to be recovered for several reasons (traumas, ingestion of fishing hooks, parasitosis, respiratory disorders) [9,10,13,28], or found dead along the seacoast [13].…”

Is Caretta Caretta a Carrier of Antibiotic Resistance in the Mediterranean Sea?

“…Sea turtles are considered an excellent bio-indicator of marine pollution [13][14][15][16][17][18]. Due to their feeding, reproductive habits, longevity and frequency in the coastal areas affected by anthropogenic activities, they could encounter and acquire autochthonous antibiotic-resistant microorganisms of polluted areas.…”