Research Article

Land Use, Macroalgae, and a Tumor-Forming Disease in Marine Turtles

  • Kyle S. Van Houtan mail,

    Affiliations: Pacific Islands Fisheries Science Center, National Oceanic and Atmospheric Administration (NOAA) Fisheries Service, Honolulu, Hawaii, United States of America, Nicholas School of the Environment and Earth Sciences, Duke University, Durham, North Carolina, United States of America

  • Stacy K. Hargrove,

    Affiliation: Pacific Islands Fisheries Science Center, National Oceanic and Atmospheric Administration (NOAA) Fisheries Service, Honolulu, Hawaii, United States of America

  • George H. Balazs

    Affiliation: Pacific Islands Fisheries Science Center, National Oceanic and Atmospheric Administration (NOAA) Fisheries Service, Honolulu, Hawaii, United States of America

  • Published: September 29, 2010
  • DOI: 10.1371/journal.pone.0012900

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Potential link between fibropapillomatosis in Hawai'ian marine turtles and non-native algae

Posted by Mathias_Ackermann on 14 Jan 2011 at 01:24 GMT

The suggested link between fibropapillomatosis (FP) in Hawai'ian marine turtles and non-native macroalgae is indeed very interesting. As mentioned in the Introduction to the present article, FP became a problem for Hawai'ian green turtles only in the 1980s, incidentally when the same problem emerged among marine turtles in Florida. I always wondered how an epidemic could start-off simultaneously at two geographic locations as far apart as Hawai'i and Florida. But then, I stumbled over some statements of Celia M. Smith, Professor of Botany at the University of Hawai’i, who testified on April 15, 2005, regarding the impact of marine invasive algae before the US House of Representatives. Among others, she mentioned that in the 1970s various species of exotic algae were introduced from the Philippines and the Caribbean to Hawai'ian waters. There were both legal and illegal introductions. Most often, the algae were placed in pens on the reef adjacent to the Hawai'ian Institute of Marine Biology in Kaneohe Bay. Citation: "… Water motion in that region was sufficient for parts of the plants to break and be carried off the reef, eventually allowing for the escape of these algae to other regions of Kaneohe Bay. …". Moreover, she mentioned that the red alga Hypnea musciformis, which is specifically mentioned in the present article, readily spread from there to other Hawai'ian islands and posed a particular problem for Maui. (Kaneohe Bay and Maui mentioned in the present article as most highly infested with FP-cases.)
The authors of the article speculate that elevated arginine (Arg) levels, passed to turtles as they forage on the red algae, may be a factor promoting the FP-tumors. They argue that high Arg may help the FP-associated herpesvirus (Chelonid herpesvirus 5, ChHV5) to replicate and somehow overcome the turtle's immune defenses. I do not have arguments against the views of the authors. However, I like to suggest that maybe a vector for transmission of ChHV5 may accidentally have been co-introduced with the exotic algae. My preferred possibility would be the marine leech Ozobranchus, which has been suggested as a potential vector (Greenblatt et al., 2004). Unfortunately, the Ozobranchus species that might be involved was not specified in the publication. However, Ozobranchus branchiatus is known to have a preference for green turtles (Chelonia mydas), which are the main victim of ChHV5, and to inhabit both the Atlantic and the Pacific Ocean (McGowin et al., 2010). Virus-infected O. branchiatus could have been brought from the Caribbean to Hawai'i together with the newly introduced algae. Since the turtles like to forage on those, the leeches would also have met immediately their preferred host. Interestingly, the authors of the present article dated the introduction of the non-native algae back to the 1950s. However, my timing (the 1970s, based on Prof. Smith's testimony), introducing the foreign algae only a few years prior to the onset of the FP-epidemic, makes even more sense and strongly supports the present authors' reasons to think about a correlation between the two events. It would be quite interesting to know, whether or not the Hawai'ian O. branchiatus have direct relatives in the Caribbean.

Greenblatt et al., 2004. The Ozobranchus leech is a candidate mechanical vector for the fibropapilloma-associated turtle herpesvirus found latently infecting skin tumors on Hawaiian green turtles (Chelonia mydas). Virology, 321:101-110.
McGowin et al., 2010. Genetic barcoding of marine leeches (Ozobranchus spp.) from Florida sea turtles and their divergence in host specificity. Molecular Ecology Resources, doi: 10.111/j.1755-0998.2010.02946.x.

No competing interests declared.

RE: Potential link between fibropapillomatosis in Hawai'ian marine turtles and non-native algae

vanhoutan replied to Mathias_Ackermann on 24 May 2011 at 16:51 GMT

Thanks for your comments Mathias and your interest in our research.

George Balazs collected O. branchiatus leeches in 1976 at Necker in the Northwestern Hawaiian Islands. More importantly, marine leeches are only seen in a very small portion of turtles of green turtles here in Hawaii. The Greenblatt study only found herpesvirus DNA in some of the leeches they collected. Abbott's book on Hawaiian rhodophytes (cited in our paper) states that the 1950s was when nonnative macroalgae were introduced to Hawaii. She is the authority on the subject. Celia was one of her students and one of my collaborators and a friend. In her testimony she was referring to several mari/aquaculture projects which notoriously began in Kaneohe Bay in the 70s. Her main work has been to undo the devastating impacts of those now abandoned commercial (and illegal) projects. And that was the subject of her testimony. Incidentally, it is not simply the reds, but chlorophytes as well.

Herbst shows that the viruses themselves have been around for tens of 1000s of years, even in Hawaii. But only in the last few decades has the disease emerged. Your idea of a contemporary virus transfer is inconsistent with Herbst's viral genome analysis. He concluded that ecological/environmental factors must have emerged that promote the virus. Our paper begins with that result and applies almost 30 years of data examining spatial and temporal variation, clustering, and incidence. Our restuls show strong links to a local cause stemming from land-based Nitrogen and macroalgae. These links are not simply supported by the data, they are the data. The explanation of these patterns involving foraging and arginine sequestration and herpes promotion is extremely well supported. Dozens of studies from virology, immunology, histopathology, oncology, plant physiology, geospatial analysis, foraing ecology, natural history, and our own field studies support this link. Since we've published this paper, I have been contacted by cancer researchers all over the world revealing their own research programmes in arginine and tumor-formation, but in human cancers.

We currently are testing the ideas put forth in the Discussion and have some fascinating results already. Nonnative algae have an amazing capacity to convert solar energy and N into tissue. We hope to be able to share the results of this work soon.

No competing interests declared.