Postembryonic development of the Tri-spine Horseshoe Crab Tachypleus tridentatus (Merostomata: Xiphosura) in a nursery habitat in the Philippines

Main Article Content

Dorkas Kaiser
https://orcid.org/0000-0002-9897-4860
Sabine Schoppe
https://orcid.org/0000-0002-8403-6806

Abstract

Populations of the Tri-spine Horseshoe Crab Tachypleus tridentatus have dramatically decreased over their distribution range and conservation efforts are now crucial.  The implementation of appropriate management strategies and stock assessment rely on accurate growth-rate estimates.  The postembryonic development of the species in the tropics, however, is not elucidated.  To provide the information needed to assess the demographics of juvenile populations and to judge the status of T. tridentatus in the Philippines, we conducted a mark-recapture experiment in a nursery habitat on Palawan Island.  The results obtained during the 10-month period provide the first consecutive data on the stepwise growth of the species in the Philippines and the first near comprehensive dataset collected within a single population of juveniles in the tropics.  By analyzing size-frequency (prosomal width) distributions of 853 individuals and by using 94 juveniles that molted during the study, 13 molt stages were differentiated.  Based on the intermolt periods of six instars, we estimated the growth curve of T. tridentatus following two models (non-linear and power function).  The data support the assumption that growth continues year-round in the tropics and also indicate that the average age of mature male and female T. tridentatus in the Philippines ranges from three to four years.  The agreement with a field study in Japan suggests that 14 postembryonic stages may be characteristic for the development of natural populations throughout the range of the species.  Though more data are needed to validate these results, the study provides a sound baseline for future studies in the tropics.

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Author Biographies

Dorkas Kaiser, Institute of Biosciences, University of Rostock, Rostock 18051, Germany; Katala Foundation Inc., Puerto Princesa City, Santa Monica, 5300 Palawan, Philippines .

In 2001: MSc, Institute of Biosciences, University of Rostock, Rostock, Germany

In 2017: None. Former PhD and for publication still working with Prof. Dr. K. Eduard Linsenmair, University of Würzburg, Department of Animal Ecology and Tropical Biology, 97074 Würzburg, Germany

Permanent address: Stauffenbergstr. 70/1, 72074 Tübingen, Germany

 

 

Sabine Schoppe, Western Philippines University, Puerto Princesa City, Aborlan, Palawan 5302, Philippines; Katala Foundation Inc., Puerto Princesa City, Santa Monica, 5300 Palawan, Philippines

In 2001: Guest Professor, Western Philippines University, Puerto Princesa City, 5300 Palawan

In 2017: Associate Professor, Western Philippines University, Puerto Princesa City, 5300 Palawan

Project Director, PFTCP/Katala Foundation, Puerto Princesa City, 5300 Palawan

References

Asano, U. (1942). On the life history of Tachypleus tridentatus. Botany and Zoology 10: 120–124 (in Japanese).

Berkson, J., C.-P. Chen, J. Mishra, P. Shin, B. Spear & J. Zaldívar-Rae (2009). A discussion of horseshoe crab management in five countries: Taiwan, India, China, United States, and Mexico, pp465–475. In: Tanacredi, J.T., M.L. Botton & D. Smith (eds.). Biology and Conservation of Horseshoe Crabs. Springer, Boston, MA, USA, 662pp.

Bonaventura, J., C. Bonaventura & S. Tesh (eds.) (1982). Physiology and Biology of Horseshoe Crabs: Studies on Normal and Environmental Stressed Animals. Alan R. Liss, Inc., New York, 316pp.

Bonilla-Gómez, J.L., X. Chiappa-Carrara, C. Galindo, G. Cuzón & G. Gaxiola (2013). Effects of adaptation to laboratory conditions on growth, molting, and food consumption of juvenile Farfantepenaeus duorarum (Decapoda: Penaeidae). Journal of Crustacean Biology 33(2): 191–197.

Botton, M.L., P.J. Loveland & T.R. Jacobsen (1992). Overwintering by trilobite larvae of the horseshoe crab Limulus polyphemus on a sandy beach of Delaware Bay (New Jersey, USA). Marine Ecology Progress Series 88: 289–292.

Caddy, J. (1987). Size-frequency analysis for Crustacea: moult increment and frequency models for stock assessment. Kuwait Bulletin of Marine Science 9: 43–61.

Cao, J., W. Guan, S. Truesdell, Y. Chen & S. Tian (2016). An individual-based probabilistic model for simulating fisheries population dynamics. Aquaculture and Fisheries 1(Supplement C): 34–40; https://doi.org/10.1016/j.aaf.2016.10.001

Carmichael, R.H., D. Rutecki & I. Valiela (2003). Abundance and population structure of the Atlantic Horseshoe Crab Limulus polyphemus in Pleasant Bay, Cape Cod. Marine Ecology Progress Series 246: 225–239.

Carmichael, R.H., D. Rutecki, B. Annett, E. Gaines & I. Valiela (2004). Position of horseshoe crabs in estuarine food webs: N and C stable isotopic study of foraging ranges and diet composition. Journal of Experimental Marine Biology and Ecology 299(2): 231–253; https://doi.org/10.1016/j.jembe.2003.09.006

Carmichael, R.H., E. Gaiues, Z. Sheller, A. Tong, A. Clapp & I. Valiela (2009). Diet composition of juvenile horseshoe crabs: implications for growth and survival of natural and cultured stocks, pp521–534. In: Tanacredi, J.T., M.L. Botton & D. Smith (eds.). Biology and Conservation of Horseshoe Crabs. Springer, Boston, MA, USA, 662pp.

Carmichael, R.H. & E. Brush (2012). Three decades of horseshoe crab rearing: a review of conditions for captive growth and survival. Reviews in Aquaculture 4(1): 32–43; https://doi.org/10.1111/j.1753-5131.2012.01059.x

Carmichael, R.H., E.E. Hieb, G. Gauvry & C.N. Shuster (2015). Examination of large exuviae with mating scars: do female American Horseshoe Crabs, Limulus polyphemus, molt after sexual maturity? pp353–366. In: Carmichael, R.H., M.L. Botton, P.K.S. Shin & S.G. Cheung (eds.). Changing Global Perspectives on Horseshoe Crab Biology, Conservation and Management. Springer International Publishing, Cham, 599pp.

Castro, M. (1992). A methodology for obtaining information on the age structure and growth rates of the Norway lobster, Nephrops norvegicus (L.) (Decapoda, Nephropoidea). Crustaceana 63(1): 29–43.

Chang, Y.-J., C.-L. Sun, Y. Chen & S.-Z. Yeh (2012). Modelling the growth of crustacean species. Reviews in Fish Biology and Fisheries 22(1): 157–187; https://doi.org/10.1007/s11160-011-9228-4

Chen, C.-P., H.-Y. Yeh & P.-F. Lin (2004). Conservation of the horseshoe crab at Kinmen, Taiwan: strategies and practices. Biodiversity & Conservation 13(10): 1889–1904; https://doi.org/10.1023/b:bioc.0000035868.11083.84

Chen, C.-P., M.C. Yang, L.F. Fan, G. Qiu, Y.Y. Liao & H.L. Hsieh (2015). Co-occurrence of juvenile horseshoe crabs Tachypleus tridentatus and Carcinoscorpius rotundicauda in an estuarine bay, southwestern China. Aquatic Biology 24(2): 117–126.

Chen, C.-P., R.F. Chen, P.H. Chen, H.C. Liu & H.L. Hsieh (2016). Intermediate culture of juvenile horseshoe crab (Tachypleus tridentatus) mixed with juvenile spotted babylon (Babylonia areolata) for restocking horseshoe crab populations. AACL Bioflux 9(3): 623–633.

Chen, Y., C.W. Lau, S.G. Cheung, C.H. Ke & P.K.S. Shin (2010). Enhanced growth of juvenile Tachypleus tridentatus (Chelicerata: Xiphosura) in the laboratory: a step towards population restocking for conservation of the species. Aquatic Biology 11(1): 37–46.

Chiu, H.M.C. & B. Morton (2003). The morphological differentiation of two horseshoe crab species, Tachypleus tridentatus and Carcinoscorpius rotundicauda (Xiphosura), in Hong Kong with a regional Asian comparison. Journal of Natural History 37(19): 2369–2382; https://doi.org/10.1080/00222930210149753

Chiu, H.M.C. & B. Morton (2004). The behaviour of juvenile horseshoe crabs, Tachypleus tridentatus (Xiphosura), on a nursery beach at Shui Hau Wan, Hong Kong. Hydrobiologia 523(1–3): 29–35; https://doi.org/10.1023/b:hydr.0000033085.71861.63

Cunningham, S.R. & M.Z. Darnell (2015). Temperature-dependent growth and molting in early juvenile blue crabs Callinectes sapidus. Journal of Shellfish Research 34(2): 505–510; https://doi.org/10.2983/035.034.0246

FAO (2006–2017). Fisheries and aquaculture software. FISAT II – FAO-ICLARM Stock Assessment Tool. In: FAO Fisheries and Aquaculture Department. FAO, Rome. Downloaded on 02 November 2017; http://www.fao.org/fishery/topic/16072/en

Field, A.P. (ed.) (2009). Discovering Statistics using SPSS (and sex and drugs and rock ’n’ roll), 3rd Edition. SAGE Publications, London, UK, 822pp.

Froese, R., A. Stern-Pirlot, H. Winker & D. Gascuel (2008). Size matters: How single-species management can contribute to ecosystem-based fisheries management. Fisheries Research 92(2–3): 231–241; http://doi.org/10.1016/j.fishres.2008.01.005

Fuiman, L.A. (1983). Growth gradients in fish larvae. Journal of Fish Biology 23(1): 117–123; https://doi.org/10.1111/j.1095-8649.1983.tb02886.x

González-Gurriarán, E., J. Freire, A.C. Fariña & A. Fernández (1998). Growth at moult and intermoult period in the Norway Lobster Nephrops norvegicus from Galician waters. ICES Journal of Marine Science 55(5): 924–940; https://doi.org/10.1006/jmsc.1998.0365

Goto, S. & O. Hattori (1929). Notes on the spawning habits and growth stages of the Japanese king-crab. X Congrès International de Zoologie 2: 1147–1155.

Gould, S.J. (1966). Allometry and size in ontogeny and phylogeny. Biological Reviews 41(4): 587–640; https://doi.org/10.1111/j.1469-185X.1966.tb01624.x

Harms, J., B. Meyer-Harms, R.R. Dawirs & K. Anger (1994). Growth and physiology of Carcinus maenas (Decapoda, Portunidae) larvae in the field and in laboratory experiments. Marine Ecology Progress Series 108: 107–118.

Hartnoll, R.G. (2001). Growth in Crustacea - twenty years on. Hydrobiologia 449(1–3): 111–122; https://doi.org/10.1023/a:1017597104367

Hiatt, R.W. (1948). The biology of the Lined Shore Crab, Pachygrapsus crassipes Randall. Pacific Science 2(3): 135–213.

Hieb, E.E., J.D. Baggett, A.M. Aven & R.H. Carmichael (2015). Effects of sediment type and tank shape on horseshoe crab (Limulus polyphemus) growth and survival in culture, pp289–302. In: Carmichael, R.H., M.L. Botton, P.K.S. Shin & S.G. Cheung (eds.). Changing Global Perspectives on Horseshoe Crab Biology, Conservation and Management. Springer International Publishing, Cham, 599pp.

Hong, S., X. Zhang, Y. Zhao, Y. Xie, Y. Zhang & H. Xu (2009). Effect of sediment type on growth and survival of juvenile horseshoe crabs (Tachypleus tridentatus), pp535–540. In: Tanacredi, J.T., M.L. Botton & D. Smith (eds.). Biology and Conservation of Horseshoe Crabs. Springer, Boston, MA, USA, 662pp.

Hsieh, H.-L. & C.-P. Chen (2009). Conservation program for the Asian horseshoe crab Tachypleus tridentatus in Taiwan: characterizing the microhabitat of nursery grounds and restoring spawning grounds, pp417–438. In: Tanacredi, J.T., M.L. Botton & D. Smith (eds.). Biology and Conservation of Horseshoe Crabs. Springer, Boston, MA, USA, 662pp.

Hsieh, H.-L. & C.-P. Chen (2015). Current status of Tachypleus tridentatus in Taiwan for Red List assessment, pp383–396. In: Carmichael, R.H., M.L. Botton, P.K.S. Shin & S.G. Cheung (eds.). Changing Global Perspectives on Horseshoe Crab Biology, Conservation and Management. Springer International Publishing, Cham, 599pp.

Hu, M., Y. Wang, Y. Chen, S.G. Cheung, P.K.S. Shin & Q. Li (2009). Summer distribution and abundance of juvenile Chinese horseshoe crabs Tachypleus tridentatus along an intertidal zone in southern China. Aquatic Biology 7(1–2): 107–112.

Hu, M., Y. Wang, S.G. Cheung & P.K.S. Shin (2013). Comparison of different frozen natural foods on survival and growth of juvenile Chinese horseshoe crab Tachypleus tridentatus (Leach, 1819): implications on laboratory culture. Aquaculture Research 44(4): 567–573; https://doi.org/10.1111/j.1365-2109.2011.03059.x

Hu, M., B.K.Y. Kwan, Y. Wang, S.G. Cheung & P.K.S. Shin (2015). Population structure and growth of juvenile horseshoe crabs Tachypleus tridentatus and Carcinoscorpius rotundicauda (Xiphosura) in southern China, pp167–180. In: Carmichael, H.R., L.M. Botton, K.S.P. Shin & G.S. Cheung (eds.). Changing Global Perspectives on Horseshoe Crab Biology, Conservation and Management. Springer International Publishing, Cham, 599pp.

Itow, T. (1993). Crisis in the Seto Inland Sea: the decimation of the horseshoe crab. EMECS Newsletter 3: 10–11.

IUCN (2017). The IUCN Red List of Threatened Species, Version 2017-3. http://www.iucnredlist.org. Downloaded on 07 December 2017.

Jegla, T.C. & J.D. Costlow (1982). Temperature and salinity effects on developmental and early posthatch stages of Limulus, pp103–113. In: Bonaventura, J., C. Bonaventura & S. Tesh (eds.). Physiology and Biology of Horseshoe Crabs: Studies on Normal and Environmentally Stressed Animals. Alan R. Liss, Inc., New York, 316pp.

Kaiser, D. (2002). Zur Ökologie und Morphologie von Tachypleus tridentatus (Leach, 1819) (Chelicerata: Merostomata) im Gezeitenwatt der Ostküste von Palawan (Philippinen). Diploma Thesis. Faculty of Biology, University of Rostock, vii+131pp.

Kawahara, D. (1982). Investigation on ecology of horseshoe crab larvae. Aquabiology 4: 380–382.

Kawahara, H. (1984). Growth and diurnal rhythm of horseshoe crabs. Nature and Animals 14: 22–26.

Kurata, H. (1962). Studies on the age and growth of crustacea. Bulletin of the Hokkaido Regional Fisheries Research Laboratory 24: 1–115.

Kwan, B.K.Y. (2015). Ecological and health perspectives of juvenile Asian horseshoe crabs. PhD Thesis. Department of Biology and Chemistry, City University of Hong Kong, xxx+226pp.

Kwan, B.K.Y., S.G. Cheung & P.K.S. Shin (2015). A dual stable isotope study for diet composition of juvenile Chinese horseshoe crab Tachypleus tridentatus (Xiphosura) on a seagrass-covered intertidal mudflat. Marine Biology 162(5): 1137–1143; https://doi.org/10.1007/s00227-015-2647-3

Kwan, B.K.Y., H.-L. Hsieh, S.G. Cheung & P.K.S. Shin (2016). Present population and habitat status of potentially threatened Asian horseshoe crabs Tachypleus tridentatus and Carcinoscorpius rotundicauda in Hong Kong: a proposal for marine protected areas. Biodiversity and Conservation 25(4): 673–692; https://doi.org/10.1007/s10531-016-1084-z

Lee, C.N. & B. Morton (2005). Experimentally derived estimates of growth by juvenile Tachypleus tridentatus and Carcinoscorpius rotundicauda (Xiphosura) from nursery beaches in Hong Kong. Journal of Experimental Marine Biology and Ecology 318(1): 39–49; https://doi.org/10.1016/j.jembe.2004.12.010

Lee, C.N.-W. & B. Morton (2016). Changes in the distributions of juvenile horseshoe crabs (Arthropoda: Chelicerata) (2002–2014) related to environmental perturbations at Pak Nai and Ha Pak Nai, Deep Bay, Hong Kong SAR, China. Marine Pollution Bulletin 108(1–2): 134-146; https://doi.org/10.1016/j.marpolbul.2016.04.037

Manca, A., F. Mohamad, A. Ahmad, M.F.A.M. Sofa & N. Ismail (2017). Tri-spine Horseshoe Crab, Tachypleus tridentatus (L.) in Sabah, Malaysia: the adult body sizes and population estimate. Journal of Asia-Pacific Biodiversity 10(3): 355–361; http://doi.org/10.1016/j.japb.2017.04.011

Mashar, A., N.A. Butet, B. Juliandi, Y. Qonita, A.A. Hakim & Y. Wardiatno (2017). Biodiversity and distribution of horseshoe crabs in northern coast of Java and southern coast of Madura. IOP Conference Series: Earth and Environmental Science 54(1): e012076; https://doi.org/10.1088/1755-1315/54/1/012076

Mohamad, F., A. Manca, A. Ahmad, M. Fawwaz, A.M. Sofa, A. Asyraf & I. Noraznawati (2016). Width-weight and length-weight relationships of the Tri-spine Horseshoe Crab, Tachypleus tridentatus (Leach 1819) from two populations in Sabah, Malaysia: implications for population management. Journal of Sustainability Science and Management 11(1): 1–13.

Morton, B. & C.N. Lee (2011). Spatial and temporal distributions of juvenile horseshoe crabs (Arthropoda: Chelicerata) approaching extirpation along the northwestern shoreline of the New Territories of Hong Kong SAR, China. Journal of Natural History 45(3-4): 227–251; https://doi.org/10.1080/00222933.2010.522263

National Ocean Service (2008). NOAA Ocean Service Education. http://oceanservice.noaa.gov/education/kits/tides/media/supp_tide07a.html. Electronic version accessed 10 February 2017.

PAGASA (2017). The Philippine Atmospheric, Geophysical and Astronomical Services Administration. http://www.pagasa.dost.gov.ph. Electronic version accessed 10 March 2017.

Robert, R., S.H.M. Ali & P.F. Amelia-Ng (2014). Demographics of horseshoe crab populations in Kota Kinabalu, Sabah, Malaysia, with emphasis on Carcinoscorpius rotundicauda and some aspects of its mating behaviour. Pertanika Journal of Tropical Agricultural Science 37(3): 375–388.

Rudkin, D.M., G.A. Young & G.S. Nowlan (2008). The oldest horseshoe crab: a new Xiphosurid from late Ordovician Konservat-Lagerstätten deposits, Manitoba, Canada. Palaeontology 51(1): 1-9; https://doi.org/10.1111/j.1475-4983.2007.00746.x

Rudloe, A. (1981). Aspects of the biology of juvenile horseshoe crabs, Limulus polyphemus. Bulletin of Marine Science 31(1): 125–133.

Rudloe, A. (1983). The effect of heavy bleeding on mortality of the horseshoe crab, Limulus polyphemus, in the natural environment. Journal of Invertebrate Pathology 42(2): 167–176; https://doi.org/10.1016/0022-2011(83)90059-9

Schoppe, S. (2002). First data on the distribution of horseshoe crabs (Chelicerata: Merostomata) in Palawan, with notes on their status in the Philippines. UPV Journal of Natural Sciences - UP Visayas 7(1–2): 198–206.

Schreibman, M.P. & C.B. Zarnoch (2009). Aquaculture methods and early growth of juvenile horseshoe crabs (Limulus polyphemus), pp501–511. In: Tanacredi, J.T., M.L. Botton & D. Smith (eds.). Biology and Conservation of Horseshoe Crabs. Springer, Boston, MA, USA, 662pp.

Sekiguchi, K., H. Seshimo & H. Sugita (1988). Post-embryonic development of the horseshoe crab. The Biological Bulletin 174(3): 337–345; https://doi.org/10.2307/1541959

Sekiguchi, K. (ed.) (1988). Biology of Horseshoe Crabs. Science House, Tokyo, Japan, 428pp.

Shuster, C.N., R.B. Barlow & H.J. Brockmann (eds.) (2003). The American Horseshoe Crab. Harvard University Press, Cambridge, 427pp.

Shuster, C.N. & K. Sekiguchi (2009). Basic habitat requirements of the extant species of horseshoe crabs (Limulacea), pp115–129. In: Tanacredi, J.T., M.L. Botton & D. Smith (eds.). Biology and Conservation of Horseshoe Crabs. Springer US, Boston, MA, 662pp.

Sokoloff, A. (1978). Observations on populations of the horseshoe crab Limulus (=Xiphosura) polyphemus. Researches on Population Ecology 19(2): 222–236; https://doi.org/10.1007/bf02518829

Tanacredi, J.T. & S. Portilla (2015). Preliminary investigation of effects of seawater pH on early development of Limulus polyphemus, pp281–287. In: Carmichael, R.H., M.L. Botton, P.K.S. Shin & S.G. Cheung (eds.). Changing Global Perspectives on Horseshoe Crab Biology, Conservation and Management. Springer International Publishing, Cham, 599pp.

Wada, T., T. Mitsushio, S. Inoue, H. Koike & R. Kawabe (2016). Movement patterns and residency of the Critically Endangered horseshoe crab Tachypleus tridentatus in a semi-enclosed bay determined using acoustic telemetry. PLoS ONE 11(2): 1–15; https://doi.org/10.1371/journal.pone.0147429

Waterman, T.H. (1954). Relative growth and the compound eye in Xiphosura. Journal of Morphology 95(1): 125–158; https://doi.org/10.1002/jmor.1050950107

Waterman, T.H. (1958). On the doubtful validity of Tachypleus hoeveni Pocock, an Indonesian horseshoe crab (Xiphosura). Postilla Yale Peabody Museum 36: 1–17.

Yamasaki, T., T. Makioka & J. Saito (1988). Morphology, pp69–132. In: Sekiguchi, K. (ed.). Biology of Horseshoe Crabs. Science House Co. Ltd., Tokyo, Japan, 428pp.

Yeh, H.Y. (1999). Life cycle, juvenile habitat and conservation strategies of the horseshoe crab (Tachypleus tridentatus) in Kinmen. PhD Thesis. National Taiwan University (in Chinese with an English abstract).

Zaleha, K., I. Hazwani, H.S. Hamidah, B.Y. Kamaruzzaman & K.C.A. Jalal (2011). Effect of salinity on the egg hatching and early larvae of horseshoe crab Tachypleus gigas (Muller, 1785) in laboratory culture. Journal of Applied Sciences 11(14): 2620–2626; https://doi.org/10.3923/jas.2011.2620.2626

Zhou, H. & B. Morton (2004). The diets of juvenile horseshoe crabs, Tachypleus tridentatus and Carcinoscorpius rotundicauda (Xiphosura), from nursery beaches proposed for conservation in Hong Kong. Journal of Natural History 38(15): 1915–1925; https://doi.org/10.1080/0022293031000155377