Early life-history consequences of growth-hormone transgenesis in rainbow trout reared in stream ecosystem mesocosms

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Abstract

There is persistent commercial interest in the use of growth modified fishes for shortening production cycles and increasing overall food production, but there is concern over the potential impact that transgenic fishes might have if ever released into nature. To explore the ecological consequences of transgenic fish, we performed two experiments in which the early growth and survival of growth-hormone transgenic rainbow trout (Oncorhynchus mykiss) were assessed in naturalized stream mesocosms that either contained predators or were predator-free. We paid special attention to the survival bottleneck that occurs during the early life-history of salmonids, and conducted experiments at two age classes (first-feeding fry and 60 days post-first-feeding) that lie on either side of the bottleneck. In the late summer, the first-feeding transgenic trout could not match the growth potential of their wild-type siblings when reared in a hydrodynamically complex and oligotrophic environment, irrespective of predation pressure. Furthermore, overall survival of transgenic fry was lower than in wild-type (transgenic = 30% without predators, 8% with predators; wild-type = 81% without predators, 31% with predators). In the experiment with 60-day old fry, we explored the effects of the transgene in different genetic backgrounds (wild versus domesticated). We found no difference in overwinter survival but significantly higher growth by transgenic trout, irrespective of genetic background. We conclude that the high mortality of GH-transgenic trout during first-feeding reflects an inability to sustain the basic metabolic requirements necessary for life in complex, stream environments. However, when older, GH-transgenic fish display a competitive advantage over wild-type fry, and show greater growth and equal survival as wild-type. These results demonstrate how developmental age and time of year can influence the response of genotypes to environmental conditions. We therefore urge caution when extrapolating the results of GH-transgenesis risk assessment studies across multiple life-history or developmental stages.

Figures

  • Fig 1. Design of the mesocosm stream tanks. Experiment 1 was conducted in a 16 metre re-circulating stream tank (panel A), landscaped with stream gravels, woody debris, and small boulders (indicated by shapes). This landscaping resulted in a main channel current that ran the length of the mesocosm (indicated by the dashed line), creating riffles and glides, away from which pools and back-eddies formed amid the woody/cobbly structures. Experiment 2 was conducted in twelve of replicated 5 metre mesocosm tanks (panel B), landscaped in a similar manner as the mesocosm stream in experiment 1. See Material and methods section and Table 1 for additional details.
  • Table 1. Initial sizes of wild-type, domestic/wild hybrid, and transgenic rainbow trout used in experiments, and the total numbers of fish used in each.
  • Fig 2. Survival and growth of wild-type (W) and transgenic-wild-type (TW) rainbow trout in a naturalized mesocosm stream environment. Survival was assessed for recently hatched trout at the end of the first two weeks of stream life, just prior to the introduction of predators to the system (Panel A), and again at the end of the experiment, after predators were added to some treatment sections (Panel B). Specific growth in mass was measured in all surviving fish at the end of the experiment (Panel C). Mesocosm stream fish were compared via a nested ANOVAmodel, with treatment and genotype] as main effects. Due to different experimental setting and design, control fish were analyzed separately but are presented here for comparison. Bars are least square means ± SEM. Different letters indicate statistically significant contrasts when = 0.05.
  • Fig 3. Comparison of daily survival of wild-type (W) and transgenic-wild-type (TW) rainbow trout in the predator-free stream segments only, throughout the entire duration of the mesocosm experiment.
  • Fig 4. The number of rainbow trout visible in each stream segment was determined at two times: daily, during the first two weeks prior to the introduction of predators (left panel), and once, just two days after predators were added to half of the stream segments (right panel). An initial total of 200 rainbow trout fry (100W, 100 TW) were placed in each stream segment for a total 800 fry. White circles signify mean numbers of fish visible in the predator-free stream segments, while black circles signify means from the predator-treated segments. The reduced number of fish visible when predators were present (black circles) are statistically significant departures from pre-predator numbers in the left panel (repeated measures, P = 0.003).
  • Fig 5. Survival and growth of wild-type (W), transgenic-wild-type (TW), domesticated/wild nontransgenic (DW), and transgenic-domestic/wild (TD/W) rainbow trout in naturalized stream tank environments with and without predators (Panel A). Specific growth in mass was measured in all surviving fish at the end of the experiment (Panel B). Bars are least square means ± SEM. Different letters indicate statistically significant contrasts when = 0.05.

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CITATION STYLE

APA

Crossin, G. T., Sundström, L. F., Vandersteen, W. E., & Devlin, R. H. (2015). Early life-history consequences of growth-hormone transgenesis in rainbow trout reared in stream ecosystem mesocosms. PLoS ONE, 10(3). https://doi.org/10.1371/journal.pone.0120173

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