Extension of the breeding season and its effects on fertilization
and development in two species of lugworm
(Arenicola marina and A. defodiens)
G.J. Watson
a,
⁎
, L.C. Hannah
b
, S.M. Gaudron
c
, K.A. Betteley
b
, M.G. Bentley
b
a
Institute of Marine Sciences, University of Portsmouth, Ferry Road, Portsmouth, PO4 9LY, UK
b
School of Marine Science and Technology, Newcastle University, Newcastle upon Tyne, NE1 7RU, UK
c
Université Pierre et Marie Curie, Laboratoire Adaptation et évolution en milieux extremes, UMR 7138 UPMC CNRS IRD MNHN,
7 quai St Bernard, 75252 Paris cedex 05, France
Received 3 August 2007; received in revised form 14 September 2007; accepted 1 October 2007
Abstract
In the autumn/winter breeding polychaetes, Arenicola marina and A. defodiens, spawning can be advanced or delayed by a
number of months through temperature manipulation of the adults. However, this manipulation may have significant consequences
for fertilization rates and embryo developmental success and so in vitro fertilizations were performed to assess the impact of
manipulation. Firstly, we used oocytes and sperm obtained from advanced or delayed individuals. For both species, using gametes
from 4 weeks advanced individuals did not result in a significant reduction in development, however, gametes from individuals
advanced (A. marina only) or delayed by 8 weeks resulted in significantly fewer embryos developing normally. Reciprocal crosses
of temperature-manipulated A. marina gametes (from 4 weeks advanced and 4 weeks delayed individuals) with those at the natural
spawning time confirmed that the reduction in developmental success in both was attributable to the oocytes. After 5 h post-
fertilization, the majority of oocytes from advanced individuals had fertilized, but by 24 h most were abnormal. For fertilizations
with gametes from delayed individuals, nearly 100% of the embryos were developing normally after 24 h, but after 144 h
significantly more were abnormal in crosses involving oocytes from delayed females. Although both species have reproductive
plasticity to extend their breeding season, the significant reduction in the numbers of competent larvae produced as the spawning is
delayed or advanced further may be a significant bottleneck in aquaculture and it may also have considerable implications for the
long-term reproductive success of a population in response to environmental change.
Sympatric populations of the species exist in many locations and the inherent variability in the breeding seasons could allow
spawning times to overlap. Artificially delaying A. marina individuals enabled fertilizations to be performed with A. defodiens at
the natural spawning time in the laboratory. Both conspecific fertilizations produced 100% trochophore larvae after 120 h, but A.
defodiens oocytes failed to fertilize after incubation with A. marina sperm, in comparison to the A. marina oocytes incubated with
A. defodiens sperm where 40% developed to the trochophore stage. This asymmetric gamete incompatibility may be one of a suite
of mechanisms to minimise hybridisation.
© 2007 Elsevier B.V. All rights reserved.
Keywords: A. defodiens; Arenicola marina; Fertilization; Heterospecific; Lugworm; Oocyte maturation
Journal of Experimental Marine Biology and Ecology 354 (2008) 17 – 27
www.elsevier.com/locate/jembe
⁎
Corresponding author. Tel.: +44 0 23 92845798; fax: +44 0 23 92845800.
E-mail address: gordon.watson@port.ac.uk (G.J. Watson).
0022-0981/$ - see front matter © 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.jembe.2007.10.002