Life History of the Copepod Hemicyclops Spinulosus (Poecilostomatoida, Clausidiidae) Associated with Crab Burrows with Notes On
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Plankton Benthos Res 3(4): 189–201, 2008 Plankton & Benthos Research © The Plankton Society of Japan Life history of the copepod Hemicyclops spinulosus (Poecilostomatoida, Clausidiidae) associated with crab burrows with notes on male polymorphism and precopulatory mate guarding HIROSHI ITOH1 &SHUHEI NISHIDA2* 1 Suidosha Co. Ltd, 8–11–11 Ikuta, Tama, Kawasaki 214–0038, Japan 2 Ocean Research Institute, University of Tokyo, 1–15–1 Minamidai, Nakano, Tokyo 164–8639, Japan Received 9 January 2008; Accepted 30 May 2008 Abstract: A 25-month field survey was conducted to investigate the life cycle and seasonal population fluctuations in the poecilostomatoid copepod Hemicyclops spinulosus in the burrows of the ocypodid crab Macrophthalmus japonicus in the mud-flats of the Tama-River estuary, central Japan. On the basis of sample collections in the water column and from the crab burrows, it was confirmed that H. spinulosus is planktonic during the naupliar stages and settles on the bottom during the first copepodid stage to inhabit the burrows. Furthermore, the copepods’ reproduction took place mainly during early summer to autumn with a successive decrease from autumn to winter. A supplementary observation on the burrows of the polychaete Tylorrhynchus heterochaetus suggested that these burrows are another important habi- tat of H. spinulosus. There were additional discoveries of male polymorphism and precopulatory mate guarding behav- ior by males, suggesting an adaptation in the reproductive strategy of this copepod to their narrow habitat spaces and low population densities, in contrast to the congeneric species H. gomsoensis, which co-occurs in the estuary but attains much larger population sizes and is associated with hosts having much larger burrow spaces. Key words: Life cycle, male polymorphism, mud-flat, polychaete burrow, seasonal change of Hemicyclops, together with the ecological importance of Introduction invertebrate burrowers, suggest that the genus is an interest- Poecilostomatoid copepods of the genus Hemicyclops ing group to increase our understanding of the burrow-as- have been reported from intertidal and subtidal zones, in- sociated life style and its relationship to species diversity in cluding estuarine mud-flats, all around the world with the intertidal communities (Itoh & Nishda 2007). However, exception of polar regions (Humes 1984) and ca. 40 species until recently our knowledge of these copepods had been are currently recognized (Vervoort & Ramirez 1966, Itoh & essentially limited to taxonomic descriptions, geographic Nishida 2002, Mulyadi 2005). Many species of Hemicy- distributions, morphology of post-embryonic developmen- clops occur on the body surface or in the burrows of ben- tal stages, and fragmentary descriptive remarks on their re- thic invertebrates, such as thalassinidean decapods and lationships with the host species (see Itoh 2001 for review). polychaetes, during their copepodid stages (Humes 1984). Among the species of Hemicyclops commonly distrib- The first copepodids (CIs) of some species have also been uted in the mud-flats of the Tama-River estuary, the life collected from the water column, often predominating in cycle and seasonal fluctuation of H. gomsoensis Ho & Kim, local plankton assemblages (Itoh & Nishida 1991), and the most abundant species inhabiting the burrows of the these have sometimes been called “Saphirella-like copepo- mud shrimp Upogebia major (de Haan) and the ocypodid dids”, referring to the specialized body form that is shared crab Macrophthalmus japonicus (de Haan), have been in- by some other members of the Clausidiidae and related vestigated by Itoh and Nishida (2007). The present study families (e.g. Gooding 1963, 1988, Izawa 1986, Kim & Ho deals with H. spinulosus Itoh & Nishida, the second-most 1992, Itoh & Nishida 1995, Itoh 2006). abundant species in the area (Itoh 2001, Itoh & Nishida The ecological characteristics and the systematic position 2007), mainly on the basis of a 25-month observation on the field populations in the water column and from the bur- * Corresponding author: Shuhei Nishida; E-mail: [email protected] rows of M. japonicus, a major benthic habitat of the cope- 190 H. ITOH & S. NISHIDA pod as presumed in the initial stage of the study (Itoh 2001, sieve. The filtered river water contained dinoflagellates Itoh & Nishida 2007). In addition, at a later stage of the (mainly Prorocentrum spp.) at high concentration, hence no sampling program we found that the copepods are also as- additional foods were supplied. Specimens representing all sociated with the polychaete Tylorrhynchus heterochaetus 6 naupliar stages (NI-NVI) were obtained from this culture. (Quatrefages), the burrows of which frequently are in con- The copepodid stages collected from the burrows of M. tact with Macrophthalmus burrows. Hence a collection was japonicus on 12 June (for CI-CIV) and 9 October 1999 (for made from the polychaete burrows for a comparison of the CV-CVI) were examined. All specimens were fixed and population structure of the copepods between the hosts. We preserved in 2% formaldehyde/river-water buffered with also describe, for the first time in Hemicyclops, two types sodium tetraborate. The morphology of specimens repre- (medium- and large sized) of non-typical males and precop- senting each stage was examined and illustrated, and body ulatory mate guarding behavior, and discuss their signifi- dimensions (body length and width for the nauplii; body cance in the copepod’s reproduction. length, from the anterior margin of prosome to the posterior margin of the caudal ramus excluding the caudal setae, for Materials and Methods the copepodids) were measured under a compound micro- scope. Study site The Tama River is among the biggest of the rivers flow- Seasonal change of population structure 3 ing into Tokyo Bay, with an average discharge of 36.6 m Populations of H. spinulosus in the Tama-River estuary Ϫ1 s and a width of ca. 500 m at its mouth (Ministry of Land, were investigated monthly from May 1998 to May 2000 Infrastructure and Transport, Japan: http://www.keihin.ktr. within 2 h before and after low spring tides. mlit.go.jp/english/index.htm). The present study sites are Plankton samples were collected at Site P by towing a Ј Ј located on a mud-flat (35°32 N, 139°46 E) bordering the hand net (mouth diameter, 20 cm; mesh size, 100 mm) 3 right bank of the river (Fig. 1). Site M is located 4.2 km up- times along the shoreline for a distance of 10 m, then fixed stream from the river mouth where burrows of Macroph- and preserved in 2% buffered formaldehyde/river-water. thalmus japonicus are abundant, between the mean sea While a mesh size of 100 mm may not be fine enough to re- level and the mean high water level of neap tide (MHWN), tain younger nauplii (body width of NI: ca. 80 mm), it was and has reed bushes on its bank side. Sampling for the not feasible to use finer mesh due to the abundance of sus- planktonic stages was done at 0.5 m-depth offshore of Site pended particles in the river water, which would have M, referred to as Site P. caused serious clogging of the net. The nauplii and copepo- dids of H. spinulosus were sorted and enumerated under a Life cycle and developmental stages compound or a stereo microscope. The counts were con- As a basis for the study of population structure, the mor- verted to abundance per cubic meter applying the mouth phological changes of Hemicyclops spinulosus were fol- area and towing distance of the net and assuming 100% fil- lowed through all developmental stages. Adult females car- tration efficiency. rying egg sacs were collected with a pipette (see next sec- The benthic populations of H. spinulosus were sampled tion) from the burrows of M. japonicus at Site M on 16 from the burrows of M. japonicus, identified, and counted May 1998. Egg sacs were removed and kept at 20°C in a as described in Itoh and Nishida (2007). Briefly, we sam- 50-mL Petri dish containing 30-mL river water that was pled 10 burrows that appeared to have few connections with collected from Site P and filtered through a 20-mm nylon burrows of other benthic animals, such as conspecific crabs, Fig. 1. Map of study sites. Site P: plankton sampling. Site M: sampling from burrows of Macrophthalmus japonicus. Burrow-associated copepods 191 or another crab Ilyoplax pusilla (de Haan), by digging the dance between the crab- and polychaete burrows were ex- substrate by hand and sucking the entire aqueous content of amined by Mann-Whitney’s U-test, while differences in the the burrows with a large (50 mL) plastic pipette. The cope- stage composition, sex ratios, and the ratios of females car- pods were sorted from this sample, identified to the species rying spermatophores were examined by the Chi-square level and the numbers of each developmental stage and sex test. Wilcoxon’s signed-ranks test was applied to test for were counted. The counts from the burrows were converted differences in temperature and salinity between sites to abundances per burrow. The body length and width, and throughout the study period. prosome length (PL) of adult females and males were mea- sured to the nearest 10 mm for all specimens. The presence/ Results absence of egg sacs and spermatophores was also recorded in the females. Life cycle and developmental stages The temperature of the offshore- and burrow water was From the rearing experiment and field sampling, it was measured with a mercury thermometer on site, while salin- confirmed that the post-embryonic life of Hemicyclops ity of the water sample was determined in the laboratory spinulosus comprises 6 naupliar and 6 copepodid stages, with a salinometer (DigiAuto-3G: Tsurumi Seiki Co. Ltd). wherein the CI is the Saphirella-like copepodid and the CVI is the adult (Fig.