Impacts of multiple stressors on growth and metabolic rate of Malaclemys terrapin

Abstract

Coastal species encounter numerous physiological stressors ranging from daily fluctuations in salinity and temperature to anthropogenic contaminants, yet the effects of such stressor combinations on aquatic organisms remain largely unknown. Exposure to environmental contaminants, such as polychlorinated biphenyls (PCBs), can disrupt physiological processes, and while physiological responses to salinity change are well understood, the combined effects of salinity change and contaminants on these processes are unknown. Marine and brackish water turtles are often simultaneously exposed to both stressors. We exposed male, eight-month-old diamondback terrapins to one of four salinity treatments (0, 10, 20, and 30 parts per thousand) in the presence and absence of the anthropogenic stressor 3,3',4,4',5-pentachlorobiphenyl (PCB 126, 20 microg/g via intraperitoneal injection) and monitored growth (carapace length and mass) and metabolic rate for six months. Exposure to PCB 126 significantly reduced growth (p < 0.0001), lowered standard metabolic rates (SMRs; p < 0.0001), and altered respiratory pattern (p < 0.0001). Salinity stress reduced growth (p < 0.0001) and altered the respiratory pattern (p < 0.0001) but had no overall effect on metabolic rate (p = 0.33). No interactive effects of PCBs and salinity were seen on either growth or metabolic rate. Our data indicate terrapins may be able to cope with some effects of salinity change through physiological adjustments but are less able to cope with PCBs. We show that PCB 126 disrupts the ecophysiological mechanisms that affect life history traits and thus ultimately could alter population structure and dynamics. The present study enriches our understanding of the environmental toxicology of reptiles and aids in the interpretation of health conditions documented in field-collected turtles contaminated with PCBs.

Integrative demographic modeling reveals population level impacts of PCB toxicity to juvenile snapping turtles

“…In other turtle species, a variety of clinical health parameters were affected by PCBs (Keller et al, 2004), which could translate to whole organism responses leading to decreased growth. More corroborative of our approach to modeling PCB effects on growth are two recent studies on diamondback terrapins in which significant effects of a single intraperitoneal injection of 20 mg/g PCB-126 on growth of juvenile turtles were observed (Holliday et al, 2009;Holliday and Holliday, 2012). Following the 180 day post-exposure period, turtles exposed to PCB-126 were approximately 11% smaller than control turtles.…”

“…We also separately evaluated projected impacts of PCBs on growth beyond year 2 juveniles by assuming a 5, 10 or 15% reduction in yearly growth rate in PCB-exposed snapping turtles. This evaluation of a PCBinduced effect on growth rate is justified based on observed impacts of PCBs on snapping turtles (Eisenreich et al, 2009) as well as effects of PCBs on growth rates in diamondback terrapins (Holliday et al, 2009;Holliday and Holliday, 2012). Specifically, Holliday et al, 2009 observed significant effects on growth and metabolism following intraperitoneal injection of PCBs to diamondback terrapins.…”

“…Although effects of PCBs have been observed in other species (Aulerich and Ringer, 1977;Örn et al, 1998;Harris and Elliott, 2011), the study by Eisenreich et al (2009) is among the few studies on PCB exposure and effects in wild turtles. Another laboratory study has also shown that PCBs can decrease growth rates in juvenile turtles (Malaclemys terrapin; Holliday et al, 2009) and the observed effect may, in part, be mediated by affects on bone density (Holliday and Holliday, 2012). Despite the strong and obvious indicators of PCB toxicity to turtles, uncertainties remain regarding how these effects observed in juvenile turtles may manifest at the population level.…”

“…Based upon previous long-term studies of snapping turtle life histories, we constructed and parameterized a combined age-and stage-structured demographic model. As well, we explored the impacts that PCBs might have on time to reproduction by developing a growth model that we then altered to reflect potential effects of PCBs based on studies of growth of PCB exposed diamondback terrapins (Holliday et al, 2009;Holliday and Holliday, 2012). Population growth rate and population size through time were specifically included as outputs.…”

Population status of freshwater turtles across a PCB contamination gradient

“…Dose-response studies provide an avenue of inquiry and indicate that PCBs can cause adverse impacts to individual turtles (e.g. Eisenreich et al 2009, Holliday et al 2009, Holliday & Holliday 2012, Yu et al 2012. Such studies can be advantageous for isolating the effect of exposure level to a particular contaminant on the performance of specific traits of individuals; however, implications of such studies of population-level endpoints remain unclear.…”