Stress responses of the endemic freshwater cururu stingray (Potamotrygon cf. histrix) during transportation in the Amazon region of the Rio Negro

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Abstract

Potamotrygon cf. histrix (cururu stingray) are endemic freshwater stingrays from the middle region of the Rio Negro in the Brazilian Amazon basin and are exported worldwide as ornamentals caught by artisanal fishermen. The transport process from capture to final destination is long and stressful. This study quantified stress related changes in corticosterone, blood and water samples (baseline, pre-transport, 3 h, 12 h and 24 h) analyzed during a transport experiment which tested two water additives (tetracycline and the probiotic Efinol®). There was a significant stepwise increase in corticosterone levels in stingrays over transport time in combination with osmoregulatory disturbances suggesting a stress related role of this corticosteroid. There were significant increases in water conductivity, Na+ and K+ losses and ammonia excretion. Blood parameters such as glucose, hematocrit, red blood count and urea did not change significantly during the experiment. Glucose levels did not increase significantly during transport and this may be due to the fact that other elasmobranchs have been shown to rely more on ketone bodies for energy rather than glucose and produce ammonia as their main nitrogenous waste. The mineralocorticoid action of this hormone has been shown in elasmobranchs and most likely plays a role in osmotic homeostasis. The use of probiotic and especially antibiotic should be avoided since no beneficial effects were observed.

Introduction

There are over 800 extant elasmobranch species most of which inhabit marine environments (Heinicke et al., 2009). Of the 400 batoid (skates and rays) species at least 20 Potamotrygonid rays are exclusively freshwater and distributed among four genera: Heliotrygon (two species), Paratrygon (one species), Plesiotrygon (two species) and Potamotrygon (18 valid species) (Carvalho et al., 2003, Martin, 2005, Carvalho and Lovejoy, 2011, Carvalho and Ragno, 2011). In contrast to marine species, freshwater stingrays possess unique morphological and physiological specializations including low plasma urea levels, a reduction in rectal gland size (Thorson et al., 1983) and a reduction in the tubule length of the Ampullae of Lorenzini (Raschi and Mackanos, 1989, McGowan and Kajiura, 2009).

The Brazilian Amazon region is home to a pigmy freshwater stingray that is endemic to a small portion of the Rio Negro, a large affluent of the Amazon River. Five stingray species are legally exported from the Brazilian Amazon basin under government managed annual quotas, including Potamotrygon cf histrix, regionally called “Cururu Ray”, which has yet to be fully described. Freshwater stingrays are targeted by the ornamental industry primarily due to high economic value making them vulnerable to fishing pressure. The city of Barcelos, within the Brazilian Amazon region, is an artisanal fishing community which collects and exports thousands of ornamental fishes from the Amazon including P.cf histrix (Chao et al., 2001). The Rio Negro is a warm, ion poor, oxygen depleted, acidic river reaching 3.5 pH in some areas (Matsuo and Val, 2003, Mortatti and Probst, 2003). Small streams (igarapés) feed the main Rio Negro system with tannin rich waters supporting high ichthyological diversity. The Rio Negro Basin has a high seasonal variation in water level and the stingrays have a predetermined reproductive cycle strongly linked to the river pulse (Charvet-Almeida et al., 2005). Local fishermen catch, collect and transport stingrays with rudimentary techniques and in many cases add unmeasured and untested compounds including tetracycline to the water in an effort to minimize stress and mortality. Once taken from the wild and transported to Barcelos, the rays are carried by freight boat to Manaus in transport that can last over 24 h dependent upon river conditions. The transport occurs in overcrowded plastic totes with little water to optimize space and cost, creating unfavorable conditions to fish. Techniques developed to minimize stress during transport in teleosts have been successful in other species and include the addition of probiotic products (Gomes et al., 2008, Gomes et al., 2009). Once arriving in Manaus, fish are held in quarantine at local exporters prior to international exportation. Many stingrays are subsequently flown to Miami (FL, USA) where they are held for weeks or months prior to final shipment worldwide. The transport process is lengthy and therefore acute and chronic stress strongly impacts survivorship.

Measuring stress in elasmobranchs has been a challenge because they produce a unique stress hormone identified as 1 α hydroxicorticosterone (Idler and Truscott, 1966) which has no commercially available measuring technique. Some species of elasmobranch have also been shown to produce corticosterone however with no well-defined stress related role (Truscott and Idler, 1972, Rasmussen and Gruber, 1990, Manire et al., 2007).

The primary objective of this experiment was to investigate stress related osmoregulatory, blood parameter alterations and costicosterone responses of P. cf. histrix (cururu stingray) to two different water additives during the transport process. The secondary objective was to contribute to the general understanding of the stress response in freshwater elasmobranchs.

Section snippets

Study area and animal capture

Specimens of cururu stingray, P. cf. histrix (n = 69, weight = 240.29 ± 137.29 g; disc width = 17.14 ± 2.80 cm; mean ± SD; 26 females and 43 males) were captured by professional fishermen in areas of flooded forest covering the margins of Igarapé Puxurituba near Barcelos, (Amazonas, Brazil) with hand nets typically at night as stingrays were detected using flashlight eye shine. Once captured they were immediately placed in holding boxes and then later transferred to 1 m3 net pens, where fish were maintained

Results

Plasma corticosterone levels did not show any significant differences due to treatment but did show significant changes over time. Corticosterone basal and pre-transport levels were significantly lower from the NO-ADD, AB and PB treatment levels in all three times. Stingrays exposed to antibiotic for 12 h presented significantly lower corticosterone levels than those exposed to antibiotic 24 h (Fig. 1).

Stingrays transported with antibiotic for 3 and 12 h and probiotic for 12 h presented

Discussion

This study examined stress related changes in the hormonal and osmoregulatory characteristics of P. cf. histrix subjected to a transport experiment using water additives. For the first time corticosterone levels have been determined for this species and with additional blood and water parameters define the physiological stress response. Baseline data will be instrumental in developing best management practices for the ornamental industry and for future conservation studies of this endemic

Conclusions

We can conclude that corticosterone can be used as an indicator of stress for this species of Amazonian stingray which do not have a typical teleost hyperglycemic reaction to stress. Their osmoregulatory response is similar to most freshwater teleosts. The use of probiotic and antibiotic as water additives during transport did not reduce stress related responses and should be avoided.

Acknowledgements

The results obtained in this manuscript were possible due to funding by the National Geographic Society conservation fund (no. C47-04). The Scientific expedition as well as the collection of wild stingrays for analysis was previously authorized by the Brazilian Ministry of Science and Technology (MCT/CNPq, process no. EXC 023/05 to J. L. Marcon), and by the Federal Environmental Agency (process no. 098/2005 DIFAP/IBAMA-DF). BB, JLM and LCG are research fellowship recipients of CNPq/Brazil. The

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