Climate change implications on reproductive success: temperature effect on penis development and fertilization of the barnacle Semibalanus balanoides
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1
Universidade de Vigo, Departamento de Ecoloxía e Bioloxía Animal, Spain
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2
Estación de Ciencias Mariñas Illa de Toralla (ECIMAT). Universidade de Vigo, Spain
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3
University of South Carolina, Department of Biological Sciences, United States
INTRODUCTION
The effects of climate change on marine ecosystems worldwide are already visible in the form of changes in species distribution and phenology (Parmesan and Yohe, 2003). Geographic distributions of species are expected to change as a result of global warming creating a considerable interest in predicting these changes. The acorn barnacle Semibalanus balanoides is the most widespread intertidal barnacle in the Northern Hemisphere and warm temperatures can inhibit its reproductive performance (Barnes and Stone, 1972; Barnes, 1992). At its southernmost European distribution limit in Northwest Iberian Peninsula, temperatures are above the thermal limit for penis development (15 °C) and fertilization (10 °C) under the winter cold limitation of reproduction hypothesis based on studies in United Kingdom at its mid-range latitudinal distribution (Barnes, 1963; Barnes & Stone, 1972; Crisp & Patel, 1969).
MATERIALS AND METHODS
We studied the effect of temperature on the reproductive success of S. balanoides in the laboratory by carrying out two consecutive experiments: penis development and fertilization. For both experiments adult S. balanoides were collected in the Ría de Arousa, NW Iberian Peninsula. Individuals were held in containers with ~100 barnacles and kept in an isothermal chamber where air temperature and light cycle were adjusted to match the field. In addition, a 6 h morning low tide was simulated daily. Barnacles were fed throughout the experiment during 3 hours every two days with a mixture of Chaetoceros sp., Phaeodactylum sp., Tetraselmis sp. and T-Isochrysis, at a final concentration of 108 cells L-1. For both experiments four different temperature treatments were used, below and above the ranges observed in the field, with two replicates per treatment. Throughout both experiments, samples were collected at 3 time-points and 15 barnacles were randomly taken from each replicate. Sizes of all individuals were measured and dry weight of somatic and gonad tissue was recorded.
For the penis development experiment individuals were collected in early September. Experimental temperatures were 14 °C, 17 °C, 20 °C and 23 °C. Samples were collected on days 27, 41 and 53. In order to determine the penis developmental stage, the number of annulations and length of the penis were measured under an optical microscope with an image analysis software (Nis-Elements BR version 4.0).
For the fertilization experiment barnacles were collected in later October. Temperature treatments were set at 12 °C, 15 °C, 18 °C and 21 °C. Samples were collected on days 26, 40 and 62. Determination of fertilization success was made through the percentage of fertilized individuals and number and size of the fertilized eggs.
Histological analyses (haematoxylin-eosin stain) of the penis and the feminine gonad were done in both experiments (10 individuals were collected in each sampling).
RESULTS AND DISCUSSION
Exposure to low temperatures (14 °C and 17 °C) allowed full penis development in all individuals while high temperature treatments (20 °C and 23 °C) inhibited it. The penis length and number of annulations were higher in barnacles exposed to low temperatures than those held at high temperatures (Figure 2). Individuals maintained below 17 °C showed a number of annulations corresponding to field observations of fully developed penes immediately before copulation (Barnes and Stone, 1972; Barnes, 1992). Although other authors found the penis length is not an accurate measurement for assessing the development stage because the penis is a very extensible organ (Barnes and Stone 1972), we obtained reliable measurements with our methodology. The mean length of the fully developed penes is far greater at low temperatures than the length of the penes of animals held at high temperatures (Fig. 1). In the developed penes setae were abundant and long and generally had sperm inside. Annulations in undeveloped penes were often poorly defined, more towards its distal part and gradually less visible towards the base (Fig. 1). The penes of animals exposed to high temperatures were noticeably shorter, thinner and harder to manipulate than the penes of animals that had remained at low temperatures. In addition, when setae were present they were noticeably few and shorter. Histological analyses showed that no spermatozoa were present in animals held at high temperatures.
Fertilization was completely inhibited (0%) in the 21 °C treatment, while at 18 °C, percent fertilization was very low (~30%). In colder treatments (12° and 15 °C) 100% fertilization was observed and it occurred ~1 month earlier than in warm treatments (i.e. at 12 °C, fertilization was already observed in the first time-point sampling). At 18 °C some of the unfertilized individuals showed sperm both inside the penis and seminal vesicles. At 21 °C, no compact ovary was present; the egg mass tissue was degraded, easily broken and difficult to manipulate, as well as the animal bodies. Moreover, at 21 °C no seminal vesicle or spermatozoa were present either by direct observation or by histological analysis.
In summary, we observed penis development success at 17 °C and fertilization in all individuals at 15 °C temperatures, demonstrating that the reproductive thresholds observed in the middle of the geographic range are exceeded by up to 5 °C in this populations at the southernmost distribution limit. This shows the adaptability of the species to local conditions and points out that Galicia may serve as a cold refuge for boreal species in European waters. In addition, the fertilization failures observed at high temperatures indicate that reproductive success of S. balanoides would be compromised in NW Iberia under the business as usual (RCP 8.5) climate change scenario.
Acknowledgements
We would like to thank ECIMAT (Universidade de Vigo) for providing the facilities, NASA and NSF agencies for funding, and Esther Pérez (Universidade de Vigo) and Luis Garabán for assistance in collecting the experimental animals.
References
Barnes, H. 1963. Light, temperature and the breeding of Balanus balanoides. Journal of Marine Biological Association of the United Kingdom 43: 717-727.
Barnes, M. 1992. The reproductive periods and condition of the penis in several species of common cirripedes. Oceanography and Marine Biology: an Annual Review 30: 483-525.
Barnes, H. and Stone, R.L. 1972. Suppression of penis development in Balanus balanoides. Journal of Experimental Marine Biology and Ecology 9: 303-309.
Crisp, D.J. and Patel, B. 1969. Environmental control of the breeding of three boreo-arctic cirripedes. Marine Biology 2: 283-295.
Parmesan, C. and Yohe, G. 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421: 37-42.
Keywords:
Climate Change,
Reproductive success,
Semibalanus balanoides,
Penis development,
Fertilization,
Barnacles,
biogeography
Conference:
XIX Iberian Symposium on Marine Biology Studies, Porto, Portugal, 5 Sep - 9 Sep, 2016.
Presentation Type:
Poster Presentation
Topic:
2. GLOBAL CHANGES, INVASIVE SPECIES AND CONSERVATION
Citation:
Herrera
M,
Macho
G,
Wethey
D and
Vázquez
E
(2016). Climate change implications on reproductive success: temperature effect on penis development and fertilization of the barnacle Semibalanus balanoides.
Front. Mar. Sci.
Conference Abstract:
XIX Iberian Symposium on Marine Biology Studies.
doi: 10.3389/conf.FMARS.2016.05.00179
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Received:
30 Apr 2016;
Published Online:
03 Sep 2016.
*
Correspondence:
Ms. Mariana Herrera, Universidade de Vigo, Departamento de Ecoloxía e Bioloxía Animal, Vigo, 36200, Spain, mherrera.biolog@gmail.com