Anneke M van den Brink Reproduction in crabs: strategies, invasiveness and environmental influences thereon i Thesis committee Promotor Prof. Dr. H.J. Lindeboom Professor of Marine Ecology Wageningen University Co-promotors Prof. Dr. A.C. Smaal Professor of Sustainable Shellfish Culture Wageningen University Prof. Dr. C. McLay Retired Marine Biologist University of Canterbury, Christchurch, New Zealand Other members Prof. Dr. J. van der Meer, NIOZ, Den Burg, The Netherlands Prof. Dr. A.J. Murk, Wageningen University Prof. Dr. J-C. Dauvin, Université de Caen Basse Normandie, France Dr. P. Clark, Natural History Museum, London, UK This thesis was conducted under the auspices of the Research School for Socio-Economic and Natural Sciences of the Environment (SENSE). ii Reproduction in crabs: strategies, invasiveness and environmental influences thereon Anneke M van den Brink Thesis submitted in fulfilment of the requirements for the degree of doctor at Wageningen University by the authority of the Rector Magnificus Prof. dr. M.J. Kropff, in the presence of the Thesis Committee appointed by the Academic Board to be defended in public on Tuesday 16 April 2013 at 4 p.m. in the Aula. iii Anneke Maria van den Brink Reproduction in crabs: strategies, invasiveness and environmental influences thereon 164 pages PhD thesis, Wageningen University, Wageningen. The Netherlands (2013) With references, with summary in English and Dutch ISBN: 978-94-6173-523-2 iv For my three true loves: Jonathon, Sebastian and Mathias Hutchens v Preface Preface It has been many years since I first started studying crabs. Now that my current study draws to a close I can’t help but think how those feisty little creatures have somehow become part of me, from the same silly jokes I hear a thousand times to the insessent urge to look under rocks on the shore to see what creatures I can find. From the beginning I found those little, sideways walking, weapon wielding crustaceans intriguing, particularly the big attitude they have despite their small size. More than once blood was drawn from my finger by a tightly clenched cheliped as my study subject made it clear that it would not go down without a fight, even against something many times bigger and stronger than itself, and sometimes it would win its freedom. I suppose you could say that they taught me that one should not give up the fight in the face of seemingly insurmountable odds. Thus closes a chapter in my life. I look forward to new challenges and continuing research in the furture. Anneke van den Brink Cover art thanks to Mare and Nanne van den Heuvel vi Contents Contents Preface .............................................................................................................................................. vi Contents ........................................................................................................................................... vii Chapter 1: General Introduction ....................................................................................................... 9 Chapter 2: Relative growth and size at sexual maturity in Halicarcinus cookii (Brachyura: Hymenosomatidae): why are some crabs precocious moulters? .......................................... 25 Chapter 3: Competing for last place: Mating behaviour in a pill-box crab, Halicarcinus cookii (Brachyura: Hymenosomatidae) ............................................................................................... 43 Chapter 4: Use of the sterile male technique to investigate sperm competition, storage, and use in a pill-box crab Halicarcinus cookii (Brachyura: Hymenosomatidae) ............................ 65 Chapter 5: The effect of temperature on brood duration in three Halicarcinus species (Crustacea: Brachyura: Hymenosomatidae) ............................................................................ 83 Chapter 6: Some like it hot: The effect of temperature on brood development in the invasive crab Hemigrapsus takanoi, (Decapoda: Brachyura: Varunidae). ........................................... 97 Chapter 7: Competition and niche segregation following the arrival of Hemigrapsus takanoi in the formerly Carcinus maenas dominated Dutch delta. ................................................... 115 Chapter 8: General Discussion ..................................................................................................... 139 Summary: English - Dutch ............................................................................................................. 153 Acknowledgments.......................................................................................................................... 162 Curriculum Vitae ............................................................................................................................. 163 vii viii General Introduction Chapter 1: General Introduction Chapter 1 BACKGROUND Crab reproductive biology is a complicated and multi-faceted concept. Strategies, behaviour and physiology are inextricably interconnected and vary widely between species. The variation in strategies lies predominantly with the allocation of energy between growth and reproduction. Some species separate growth and reproductive phases, while others intersperse the phases throughout their life. This thesis delves into the world of crab reproduction and investigates the various features of the reproductive biology of crabs with the aim of identifying the consequences of these variations to the individual crab and the population in which it exists. The two primary study species, Halicarcinus cookii and Hemigrapsus takanoi are similar in size and habitat preferences, but represent different reproductive strategies. These species are used as examples to broaden the current knowledge of influences on, and consequences of their reproductive strategies. Both physiological and external influences on reproduction, and their effects are considered along with population dynamics and ecology. Growth and reproduction in crabs Reproduction and growth are competing factors for energy, both of which are dependent on the moult cycle in crustaceans. The moult cycle in crustaceans is highly energy-demanding and correlated with the seasons. Although the relative importance of environmental changes may vary among different species and environments, breeding cycles are generally linked with seasonal changes in such a way that offspring are produced at a time most favourable to their survival (Raviv et al., 2008). Moulting and reproduction are coordinated in a wide variety of ways in decapod crustaceans. The physiological nature of a species regulates the reproductive cycle, both by internal cues (e.g. moult cycle interval, integumental reproductive-related machinery, energy allocation, maternal care and embryonic development of offspring) and by external cues (e.g. habitat and season) (Raviv et al., 2008). McLay and Lopez Greco (2011) suggested that the reproductive strategy in crabs depends on three factors: whether the species shows indeterminate or determinate growth; hard or soft shell mating, and whether the seminal receptacle is dorsal or ventral. Crabs with indeterminate growth continue to moult and grow throughout their lives. As an individual female grows, she can produce more eggs per brood and cross a size threshold to avoid some predators as well as increase competitiveness for food and space. However, with continual moulting the crabs are regularly vulnerable to predators and damage while soft shelled. Determinate growth occurs in species that experience a terminal, pubertal moult after which they are reproductively active but no longer grow. While these species avoid the regular vulnerable soft shelled stage as adults, they are limited in growth to the size at the terminal moult. In some crab species, the female is only physically able to mate while soft shelled after mating. For internal fertilisation in crabs the male must physically insert his gonopods into the female’s gonopore to deliver sperm. For crustaceans this means that the exoskeleton of the female must be flexible enough to receive the gonopod. In species with soft shell mating, mating occurs only while the females exoskeleton has not yet hardened directly after moulting. In species with hard shell mating, mating is possible while the female’s General Introduction integument is hard, this may be due to continuously open gonopores or temporary decalcification of an operculum covering the gonopore. Seminal receptacles are structures within the female’s body that collect and store sperm so that the female has a ready supply to fertilise her eggs. The unfertilised eggs travel through the oviduct into the seminal receptacle where they are fertilised and are then extruded through the vagina to the vaginal opening (through which sperm is delivered during mating) and into the external brood chamber. In species with dorsal seminal receptacles the oviduct attaches to the seminal receptacle at the opposite end to the vagina, thus the eggs are fertilised by the oldest stored sperm. In species with ventral seminal receptacles the oviduct connects with the seminal receptacle at the same end as the vagina so that the eggs are fertilised by the newest of the stored sperm. Some species have an intermediate type of seminal receptacles where the oviduct is attached near the middle of the seminal receptacle (McLay & López Greco, 2011). The different reproductive strategies of crustaceans defined by the combination of growth strategy,