Journal of Marine Science and Engineering Article Population Structure and Reproductive Biology of the Endangered Crab Deiratonotus japonicus (Brachyura, Camptandriidae) Surveyed for Nine Years in the Kita River, Japan Il-Kweun Oh * and Seung-Woo Lee Graduate School of Environmental Engineering, University of Kitakyushu, 1-1 Hibikino, Wakamatsu, Kitakyushu, Fukuoka 808-0135, Japan; [email protected] * Correspondence: [email protected]; Tel.: +81-93-695-3293 Received: 1 October 2020; Accepted: 12 November 2020; Published: 15 November 2020 Abstract: Deiratonotus japonicus (D. japonicus) is known as a near-threatened species, because of the changing conditions of its habitat. This species resides in isolated locations and in upstream, brackish waters from Kanagawa Prefecture to Okinawa Prefecture in Japan. In this study, we investigated the population structure and reproductive biology of D. japonicus in the Kita River, Japan. The distribution, sex ratio, breeding season, and fecundity were assessed at bimonthly intervals during spring low-tide periods from May 2001 to November 2008 and from November 2014 to January 2016 for approximately nine years. A total of 3525 crabs were collected during the sampling period: 1806 (51.2%) males, 1240 (35.2%) non-ovigerous females, and 479 (13.6%) ovigerous females. The overall sex ratio (1:0.95) did not differ significantly from the expected 1:1 ratio. The mean maximum density was 26.1 and 36.5 indiv./m2 for the first and second sampling periods, respectively, in the sampling station 5.2 km from the Kita River mouth, and all individuals were typically found approximately 4.4–6.8 km (13.2 7.8 indiv./m2) from the Kita River mouth. Carapace width (CW) ranged from 2.6 to 13.5 mm ± in males and from 2.8 to 13.4 mm in females and was significantly different between the two sexes (p < 0.05). Ovigerous females were found almost throughout the entire sampling period, with breeding peaks between July and September. The smallest ovigerous female had a CW of 3.9 mm. The seasonal frequency distribution suggested the continuous recruitment of young juveniles (CW < 3.9 mm) throughout the year, with peaks from September to November. The mean fecundity was 1008.3 183.1 (8.3 1.6 mm) eggs. Egg number in relation to CW was calculated by the formula ± ± egg number (EN) = 110.36 CW + 90.96 (R2 = 0.948, n = 41, p < 0.0001). Regression analysis showed × that fecundity was closely associated with female CW. Our results indicate that the performance of reproductive biology depends not only on continuous breeding but also on recruitment throughout the year in our study area. Keywords: Deiratonotus japonicus; camptandriidae; population structure; reproductive biology; sex ratio; fecundity 1. Introduction The family Camptandriidae currently includes 40 species and 22 genera from South Africa, West Africa, New Caledonia, and Northeast Asia. Most species of Camptandriidae live in marine, intertidal estuarine, and mangrove habitats [1–3]. Camptandriidae were previously classified as a subfamily of Ocypodidae, but now they are classified as a distinct family [4–6]. The Camptandriidae genus Deiratonotus Manning & Holthuis, 1981, contains three species: Deiratonotus cristatus (De Man, 1895), Deiratonotus japonicus (Sakai, 1934), and Deiratonotus kaoriae (Miura, Kawane & Wada, 2007) [6,7]. J. Mar. Sci. Eng. 2020, 8, 921; doi:10.3390/jmse8110921 www.mdpi.com/journal/jmse J. Mar. Sci. Eng. 2020, 8, x FOR PEER REVIEW 2 of 14 DeiratonotusJ. Mar. Sci. Eng. japonicus2020, 8, 921 (Sakai, 1934), and Deiratonotus kaoriae (Miura, Kawane & Wada, 2007) [6,7].2 of 14 D. japonicus (Sakai, 1934) and Deiratonotus tondensis (Sakai, 1983) are classified as the same species, accordingD. japonicus to Kawane(Sakai, 1934)et al. [5]. and Deiratonotus tondensis (Sakai, 1983) are classified as the same species, accordingD. japonicus to Kawane (Sakai, et 1934) al. [5 (Decapoda:]. Camptandriidae) is an endemic crab species and has been classifiedD. as japonicus a near-threatened(Sakai, 1934) species (Decapoda: in the Camptandriidae) Red Data Book isList an by endemic the Ministry crab species of the and Environment has been in Japan.classified It is as usually a near-threatened found in speciesisolated in locations the Red Data and Bookin upstream, List by the brackish Ministry waters. of the EnvironmentRecords of D. japonicusin Japan. are limited It is usually to several found localities in isolated from locations Kanagawa and Prefecture in upstream, to Okinawa brackish Prefecture waters. Records in western of JapanD. japonicus[5,8–10]. areSeveral limited aspects to several of the localities biology fromand behavior Kanagawa of Prefecture D. japonicus to Okinawa(Sakai, 1934) Prefecture have been in studied:western Yamanishi Japan [5,8 –et10 ].al. Several [8,11] aspectsand Hiu of et the al. biology [12–14] and investigated behavior of D.its japonicushabitat (Sakai,characteristics 1934) have and behaviorbeen studied: associated Yamanishi with water et al. levels, [8,11] and salinity, Hiu et an al.d [sediment;12–14] investigated Terada described its habitat its characteristics early zoeal stages and [4];behavior Oh et al. associated observed with its larval water development levels, salinity, under and sediment; laboratory Terada conditions described [10]; its earlyand Kawane zoeal stages et al. [4 ];[5] andOh Miura et al. et observed al. [7] investigated its larval development its morphological under laboratory and genetic conditions characteristics. [10]; and Kawane et al. [5] and MiuraDespite et al. the [7] relative investigated abundance its morphological of studies on and the genetic general characteristics. biology of Ocypodidae crabs, biological informationDespite on thethese relative species abundance is limited. of studiesOur study on the represents general biology the first of attempt Ocypodidae to clearly crabs, identify biological the populationinformation and on reprod theseuctive species biology is limited. of D. Ourjaponicus study in represents the Kita River; the first no attemptprevious to studies clearly have identify been publishedthe population on this and species. reproductive We investigated biology of theD. japonicusdistributionin the of Kita size River; frequency, no previous sex ratio, studies breeding have period,been publishedjuvenile recruitment, on this species. and We fecundity investigated of theD. distributionjaponicus in of the size Kita frequency, River, sexJapan. ratio, This breeding study providesperiod, information juvenile recruitment, on the biological and fecundity characteristics, of D. japonicus distribution,in the Kita River, and Japan.reproductive This study biology provides of D. information on the biological characteristics, distribution, and reproductive biology of D. japonicus, japonicus, which will also be useful in developing future conservation strategies for its specific habitat which will also be useful in developing future conservation strategies for its specific habitat and for and for environmental evaluations in the Kita River, Japan. environmental evaluations in the Kita River, Japan. 2. Materials2. Materials and and Methods Methods TheThe study study area area is islocated located in in the the Kita Kita River River estuary, estuary, Miyazaki Prefecture,Prefecture, Japan Japan (32 (32°35’26”◦3502600 N, N, 131°42’50”131◦42050 E,00 E,Figure Figure 1).1 ).Field Field sampling sampling for for D.D. japonicus japonicus was performed atatbimonthly bimonthly intervals intervals from from MayMay 2001 2001 to toNovember November 2008 2008 and and from from November November 2014 2014 to to January January 2016. 2016. Specimens Specimens were were collected collected at 38 atstations 38 stations (including (including both both left leftand and right right points points at intervals at intervals of of400 400 m m from from the the Kita Kita river river mouth to 7 km7 upstream) km upstream) during during the thespring spring low low tide, tide, using using a aquadrat quadrat trap trap with with a net (0.5(0.5 mm ×0.5 0.5 m m ×0.3 0.3 m). m). × × Generally,Generally, passive passive sampling sampling methods methods using using a atrap trap feeding feeding bait bait have have been been broadly broadly used. used. However, However, in thisin study this study no bait no was bait used was for used sampling for sampling to help to reduce help reduce the sampling the sampling time and time understand and understand the natural the habitatsnatural of habitatsD. japonicus of D. [8,10–14]. japonicus [ The8,10 –mean14]. The density mean of density the crabs of the captured crabs captured at each station at each was station obtained was by obtainedaveraging by averagingthe number the of number individuals of individuals per unit per area unit areawhere where 2 to 2 to5 5collections collections were performed.performed. NormalizedNormalized traps traps of ofthe the same same dimensions dimensions were were used used throughout throughout allall samplingssamplings to to ensure ensure the the accuracy accuracy of sampling.of sampling. Figure 1. Map showing the sampling stations of Deiratonotus japonicus from the Kita River estuary. Figure 1. Map showing the sampling stations of Deiratonotus japonicus from the Kita River estuary. The habitat characteristics, body size defined as carapace width (CW, in mm), and sex, including maturity and ovigerous condition (mainly related to the temperature or salinity of the habitat J. Mar. Sci. Eng. 2020, 8, 921 3 of 14 The habitat characteristics, body size defined as carapace width (CW, in mm), and sex, including maturity and ovigerous condition (mainly related to the temperature or salinity of the habitat environment), were recorded for female specimens. CW was measured by using Vernier calipers to approximately 0.05 mm. Sex was verified by the gonopore position and abdomen characteristics. Ovigerous females were identified by the presence of eggs on their abdomen. The population size structure was analyzed as a function of the size-frequency distribution of all individuals collected during the study period. All crabs captured for this study were released after checking their carapace width, sex, and the presence of eggs, except for some ovigerous females used for fecundity analysis.