Early life migration and population discrimination of the small yellow croaker <i>Larimichthys polyactis</i> from the Yellow Sea: inferences from otolith Sr/Ca ratios -- Journal of Oceanology and Limnology,2022,40(2):818-829

	Cite this paper:
	Dade SONG, Ying XIONG, Tao JIANG, Jian YANG, Xiaming ZHONG, Jianhua TANG. Early life migration and population discrimination of the small yellow croaker Larimichthys polyactis from the Yellow Sea: inferences from otolith Sr/Ca ratios[J]. Journal of Oceanology and Limnology, 2022, 40(2): 818-829

Early life migration and population discrimination of the small yellow croaker Larimichthys polyactis from the Yellow Sea: inferences from otolith Sr/Ca ratios

Dade SONG^1,2, Ying XIONG², Tao JIANG³, Jian YANG³, Xiaming ZHONG², Jianhua TANG²

1 College of Marine Sciences, Shanghai Ocean University, Shanghai 201306, China;
2 Jiangsu Marine Fisheries Research Institute, Nantong 226007, China;
3 Key Laboratory of Fishery Ecological Environment Assessment and Resource Conservation in Middle and Lower Reaches of Yangtze River, Freshwater Fisheries Research Center, Chinese Academy of Fishery Sciences, Wuxi 214081, China

Abstract:

The small yellow croaker Larimichthys polyactis is a benthic marine fish species of high ecological and commercial importance and is widely distributed in the northwestern Pacific Ocean, especially in the Chinese coastal waters of the Bohai, Yellow, and East China Seas. As a highly migratory species, the whole life migration of L. polyactis has been intensively studied. However, knowledge about its early life migration is scarce, and population divisions are inconsistent, limiting the ability of fishery scientists and administrators to evaluate the design and potential benefits of thorough conservation and resource-management strategies. In the present study, otolith Sr/Ca was analyzed to investigate the early migratory patterns and discriminate the populations of L. polyactis in the Yellow Sea, including two spawning groups and one overwintering group. The variation in Sr/Ca ratios of ontogenetic growth zones, including the nucleus (N), larval (L), metamorphosis (M), juvenile (J), and edge (E) zones, was measured by electron probe microanalysis. The variation in Sr/Ca ratios in early developmental growth zones was generally characterized by an evident downward trend from the N to J zone, which suggests that the early migratory pattern of L. polyactis might be from inshore to nearshore water. Canonical discriminant analysis, based on the otolith Sr/Ca ratios of the N, L, M, and J zones, allowed the successful discrimination of the two populations, namely, the northern and southern Yellow Sea groups, whose differences were mainly reflected in the L and J zones. Compared with previous studies, the traditional geographic boundaries (34°N) separating these two populations might be moving northward. The application of otolith Sr/Ca ratios based on ontogenetic stage could improve our understanding of the migration and population discrimination of L. polyactis from the Yellow Sea.

Key words: otolith microchemistry|Larimichthys polyactis|early life migration|population discrimination|the Yellow Sea

Received: 2021-02-10 Revised:

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Articles by Ying XIONG

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Articles by Jianhua TANG

References:
Arai T, Taha H, Amalina R, Iizuka Y, Chang C W.2019.Anadromy and heterogenous population of a tropical shad Tenualosa ilisha in Malaysia, as revealed by otolith microchemistry and molecular evidence.Journal of Fish Biology, 95(6):1506-1511, https://doi.org/10.1111/jfb.14154.
Arkhipkin A I, Campana S E, FitzGerald J, Thorrold S R.2004.Spatial and temporal variation in elemental signatures of statoliths from the Patagonian longfin squid (Loligo gahi).Canadian Journal of Fisheries and Aquatic Sciences, 61(7):1212-1224, https://doi.org/10.1139/f04-075.
Avigliano E, de Carvalho B M, Leisen M, Romero R, Velasco G, Vianna M, Barra F, Volpedo A V.2017.Otolith edge fingerprints as approach for stock identification of Genidens barbus.Estuarine, Coastal and Shelf Science, 194:92-96, https://doi.org/10.1016/j.ecss.2017.06.008.
Botsford L W, Hastings A, Gaines S D.2001.Dependence of sustainability on the configuration of marine reserves and larval dispersal distance.Ecology Letters, 4(2):144-150, https://doi.org/10.1046/j.1461-0248.2001.00208.x.
Campana S E.1999.Chemistry and composition of fish otoliths:pathways, mechanisms and applications.Marine Ecology Progress Series, 188:263-297, https://doi.org/10.3354/meps188263.
Carlson A K, Phelps Q E, Graeb B D S.2017.Chemistry to conservation:using otoliths to advance recreational and commercial fisheries management.Journal of Fish Biology, 90(2):505-527, https://doi.org/10.1111/jfb.13155.
Chatterjee M, Ghosh P, Ramdas L, Chakrabarti R.2015.Isotopic and geochemical characterization of invader tilapia fishes from water bodies of West Bengal and Karnataka, India.Environmental Monitoring and Assessment, 187(11):712, https://doi.org/10.1007/s10661-015-4929-0.
Chino N, McCarthy T K, Arai T.2018.Analysis of fluvial migration of the Irish pollan Coregonus autumnalis, using Sr:Ca ratios of otolith.Journal of Applied Animal Research, 46(1):609-612, https://doi.org/10.1080/097121 19.2017.1369089.
Cooke S J, Midwood J D, Thiem J D, Klimley P, Lucas M C, Thorstad E B, Eiler J, Holbrook C, Ebner B C.2013.Tracking animals in freshwater with electronic tags:past, present and future.Animal Biotelemetry, 1(1):5, https://doi.org/10.1186/2050-3385-1-5.
Cowen R K, Gawarkiewicz G, Pineda J, Thorrold S R, Werner F E.2007.Population connectivity in marine systems:an overview.Oceanography, 20(3):14-21, https://doi.org/10.5670/oceanog.2007.26.
Dai L B, Tian S Q, Peng X, Gao C X, Ye S, Du X X, Liu P.2018.Distribution of Larimichthys polyactis and its relationship with environmental factors in offshore water of southern Zhejiang.Chinese Journal of Applied Ecology, 29(4):1352-1358, https://doi.org/10.13287/j.1001-9332.201804.033. (in Chinese with English abstract)
Delerue-Ricard S, Darnaude A M, Raeymaekers J A M, Dundas S H, Skadal J, Volckaert F A M, Geffen A J.2019.Extensive larval dispersal and restricted movement of juveniles on the nursery grounds of sole in the Southern North Sea.Journal of Sea Research, 155:101822, https://doi.org/10.1016/j.seares.2019.101822.
Dou S Z, Yokouchi K, Yu X, Cao L, Kuroki M, Otake T, Tsukamoto K.2012.The migratory history of anadromous and non-anadromous tapertail anchovy Coilia nasus in the Yangtze River Estuary revealed by the otolith Sr/Ca ratio.Environmental Biology of Fishes, 95(4):481-490, https://doi.org/10.1007/s10641-012-0042-1.
Dove S G, Gillanders B M, Kingsford M J.1996.An investigation of chronological differences in the deposition of trace metals in the otoliths of two temperate reef fishes.Journal of Experimental Marine Biology and Ecology, 205(1-2):15-33, https://doi.org/10.1016/S0022-0981(96) 02610-X.
Elsdon T S, Gillanders B M.2003.Reconstructing migratory patterns of fish based on environmental influences on otolith chemistry.Reviews in Fish Biology and Fisheries, 13(3):217-235, https://doi.org/10.1023/b:rfbf.0000033071.73952.40.
Elsdon T S, Wells B K, Campana S E, Gillanders B M, Jones C M, Limburg K E, Secor D H, Thorrold S R, Walther B D.2008.Otolith chemistry to describe movements and lifehistory parameters of fishes:hypotheses, assumptions, limitations and inferences.Oceanography and Marine Biology, 46:297-330, https://doi.org/10.1201/9781420065756.ch7.Fishbase.2019.https://fishbase.in/summary/Larimichthyspolyactis.html.Accessed on 2020-10-10.
Gahagan B I, Vokoun J C, Whitledge G W, Schultz E T.2012.Evaluation of otolith microchemistry for identifying natal origin of anadromous river herring in Connecticut.Marine and Coastal Fisheries, 4(1):358-372, https://doi.org/10.1 080/19425120.2012.675967.
Gillanders B M.2005.Otolith chemistry to determine movements of diadromous and freshwater fish.Aquatic Living Resources, 18(3):291-300, https://doi.org/10.1051/alr:2005033.
Guo B, Zhang B, Jin X S.2010.Diet composition and ontogenetic variation in feeding habits of juvenile small yellow croaker Pseudosciaena polyactis Bleeker in the Yellow Sea.Journal of Fishery Sciences of China, 17(2):289-297. (in Chinese with English abstract)
Huang M H, Liang X S, Wu H, Wang Y H.2018.Different generating mechanisms for the summer surface cold patches in the Yellow Sea.Atmosphere-Ocean, 56(4):1-13, https://doi.org/10.1080/07055900.2017.1371580.
Jiang T, Liu H B, Lu M J, Chen T T, Yang J.2016.A possible connectivity among estuarine tapertail anchovy (Coilia nasus) populations in the Yangtze River, Yellow Sea, and Poyang Lake.Estuaries and Coasts, 39(6):1762-1768, https://doi.org/10.1007/s12237-016-0107-z.
Jiang T, Yang J, Lu M J, Liu H B, Chen T T, Gao Y W.2017.Discovery of a spawning area for anadromous Coilia nasus Temminck et Schlegel, 1846 in Poyang Lake, China.Journal of Applied Ichthyology, 33(2):189-192, https://doi.org/10.1111/jai.13293.
Jiang Y Q, Zhang C, Ye Z J, Tian Y J.2019.Analyses of egg size, otolith shape, and growth revealed two components of small yellow croaker in Haizhou Bay spawning stock.Journal of Oceanology and Limnology, 37(4):1423-1429, https://doi.org/10.1007/s00343-019-8105-1.
King J R, McFarlane G A.2003.Marine fish life history strategies:applications to fishery management.Fisheries Management and Ecology, 10(4):249-264, https://doi.org/10.1046/j.1365-2400.2003.00359.x.
Lee Q, Lee A, Liu Z L, Szuwalski C S.2020.Life history changes and fisheries assessment performance:a case study for small yellow croaker.Journal of Marine Science, 77(2):645-654, https://doi.org/10.1093/icesjms/fsz232.
Li Y X, Tang J H, Xu X M, Xu J, Liu Z Y, Xu H, Cheng J H.2013.Comparison of otolith microstructures in small yellow croaker larvae and juveniles from Sanmen Bay and Lvsi.Marine Fisheries, 35(4):423-431, https://doi.org/10.13233/j.cnki.mar.fish.2013.04.008. (in Chinese with English abstract)
Li Y Z, Sun M, Zhang C L, Zhang Y L, Xu B D, Ren Y P, Chen Y.2020.Evaluating fisheries conservation strategies in the socio-ecological system:a grid-based dynamic model to link spatial conservation prioritization tools with tactical fisheries management.PLoS One, 15(4):e0230946, https://doi.org/10.1371/journal.pone.0230946.
Lim H K, Le M H, An C M, Kim S Y, Park M S, Chang Y J.2010.Reproductive cycle of yellow croaker Larimichthys polyactis in southern waters off Korea.Fisheries Science, 76(6):971-980, https://doi.org/10.1007/s12562-010-0288-5.
Lin L S, Cheng J H, Jiang Y Z, Yuan X W, Li J S, Gao T X.2008.Spatial distribution and environmental characteristics of the spawning grounds of small yellow croaker in the southern Yellow Sea and the East China Sea.Acta Ecologica Sinica, 28(8):3485-3492. (in Chinese with English abstract)
Lin N, Chen Y G, Jin Y, Yuan X W, Ling J Z, Jiang Y Z.2018.Distribution of the early life stages of small yellow croaker in the Yangtze River estuary and adjacent waters.Fisheries Science, 84(2):357-363, https://doi.org/10.1007/s12562-018-1177-6.
Lin X P, Yang J Y, Guo J S, Zhang Z X, Yin Y Q, Song X Z, Zhang X H.2011.An asymmetric upwind flow, Yellow Sea Warm Current:1.new observations in the western Yellow Sea.Journal of Geophysical Research:Oceans, 116(C4):C04026, https://doi.org/10.1029/2010jc006513.
Lin X Z.1987.Biological characteristics and resources status of three main commercial fishes in offshore waters of China.Journal of Fisheries of China, 11(3):187-194. (in Chinese with English abstract)
Liu B L, Chen X J, Chen, Y, Lu H J, Qian W G.2011.Trace elements in the statoliths of jumbo flying squid off the Exclusive Economic Zones of Chile and Peru.Marine Ecology Progress Series, 429:93-101, https://doi.org/10.3354/meps09106.
Liu H B, Jiang T, Huang H H, Shen X Q, Zhu J B, Yang J.2015.Estuarine dependency in Collichthys lucidus of the Yangtze River Estuary as revealed by the environmental signature of otolith strontium and calcium.Environmental Biology of Fishes, 98(1):165-172, https://doi.org/10.1007/s10641-014-0246-7.
Liu J Y.2013.Status of marine biodiversity of the China seas.PLoS One, 8(1):e50719, https://doi.org/10.1371/journal.pone.0050719.
Liu X S.1990.Fisheries Resources Survey and Zoning in the Yellow Sea and Bohai Sea Area.Ocean Press, Beijing, China.p.191-200. (in Chinese)
Lowe W H, Allendorf F W.2010.What can genetics tell us about population connectivity? Molecular Ecology, 19(15):3038-3051, https://doi.org/10.1111/j.1365-294x.2010.04688.x.
Ma Q Y, Jiao Y, Ren Y P, Xue Y.2020.Population dynamics modelling with spatial heterogeneity for yellow croaker(Larimichthys polyactis) along the coast of China.Acta Oceanologica Sinica, 39(10):107-119, https://doi.org/10.1007/s13131-020-1602-4.
Miller B S, Kendall A W Jr.2009.Early Life History of Marine Fishes.University of California Press, Berkeley.376p.
Milton D A, Chenery S R.2001.Sources and uptake of trace metals in otoliths of juvenile barramundi (Lates calcarifer).Journal of Experimental Marine Biology and Ecology, 264(1):47-65, https://doi.org/10.1016/s0022-0981(01) 00301-x.
Murayama E, Takagi Y, Nagasawa H.2004.Immunohistochemical localization of two otolith matrix proteins in the otolith and inner ear of the rainbow trout, Oncorhynchus mykiss:comparative aspects between the adult inner ear and embryonic otocysts.Histochemistry and Cell Biology, 121(2):155-166, https://doi.org/10.1007/s00418-003-0605-5.
Ovenden J R.2013.Crinkles in connectivity:combining genetics and other types of biological data to estimate movement and interbreeding between populations.Marine and Freshwater Research, 64(3):201-207, https://doi.org/10.1071/mf12314.
Reis-Santos P, Tanner S E, França S, Vasconcelos R P, Gillanders B M, Cabral H N.2015.Connectivity within estuaries:An otolith chemistry and muscle stable isotope approach.Ocean & Coastal Management, 118:51-59, https://doi.org/10.1016/j.ocecoaman.2015.04.012.
Rodionov S, Overland J E.2005.Application of a sequential regime shift detection method to the Bering Sea ecosystem.Journal of Marine Science, 62(3):328-332, https://doi.org/10.1016/j.icesjms.2005.01.013.
Rogers T A, Fowler A J, Steer M A, Gillanders B M.2019.Discriminating natal source populations of a temperate marine fish using larval otolith chemistry.Frontiers in Marine Science, 6:711, https://doi.org/10.3389/fmars.2019.00711.
Schulz-Mirbach T, Ladich F, Plath M, Heß M.2019.Enigmatic ear stones:what we know about the functional role and evolution of fish otoliths.Biological Reviews, 94(2):457-482, https://doi.org/10.1111/brv.12463.
Sedberry G R, Loefer J K.2001.Satellite telemetry tracking of swordfish, Xiphias gladius, off the eastern United States.Marine Biology, 139(2):355-360, https://doi.org/10.1007/s002270100593.
Song J J, Zhao B, Liu J H, Cao L, Dou S Z.2018.Comparison of otolith shape descriptors and morphometrics for stock discrimination of yellow croaker along the Chinese coast.Journal of Oceanology and Limnology, 36(5):1870-1879, https://doi.org/10.1007/s00343-018-7228-0.
Sun S, Huo Y Z, Yang B.2010.Zooplankton functional groups on the continental shelf of the Yellow Sea.Deep Sea Research Part II:Topical Studies in Oceanography, 57(11-12):1006-1016, https://doi.org/10.1016/j.dsr2.2010.02.002.
Taddese F, Reid M R, Closs G P.2019.Direct relationship between water and otolith chemistry in juvenile estuarine triplefin Forsterygion nigripenne.Fisheries Research, 211:32-39, https://doi.org/10.1016/j.fishres.2018.11.002.
Tran N T, Labonne M, Hoang H D, Panfili J.2019.Changes in environmental salinity during the life of Pangasius krempfi in the Mekong Delta (Vietnam) estimated from otolith Sr:Ca ratios.Marine and Freshwater Research, 70(12):1734-1746, https://doi.org/10.1071/mf18269.
Tsukamoto K, Arai T.2001.Facultative catadromy of the eel Anguilla japonica between freshwater and seawater habitats.Marine Ecology Progress Series, 220:265-276, https://doi.org/10.3354/meps220265.
Tzeng W N.1996.Effects of salinity and ontogenetic movements on strontium:calcium ratios in the otoliths of the Japanese eel, Anguilla japonica Temminck and Schlegel.Journal of Experimental Marine Biology and Ecology, 199(1):111-122, https://doi.org/10.1016/0022-0981(95) 00185-9.
Walker K A, Trites A W, Haulena M, Weary D M.2011.A review of the effects of different marking and tagging techniques on marine mammals.Wildlife Research, 39(1):15-30, https://doi.org/10.1071/wr10177.
Walther B D.2019.The art of otolith chemistry:interpreting patterns by integrating perspectives.Marine and Freshwater Research, 70(12):1643-1658, https://doi.org/10.1071/mf18270.
Wang C H, Lin Y T, Shiao J C, You C F, Tzeng W N.2009.Spatio-temporal variation in the elemental compositions of otoliths of southern bluefin tuna Thunnus maccoyii in the Indian Ocean and its ecological implication.Journal of Fish Biology, 75(6):1173-1193, https://doi.org/10.1111/j.1095-8649.2009.02336.x.
Wang L, Liu S F, Zhuang Z M, Guo L, Meng Z N, Lin H R.2013.Population genetic studies revealed local adaptation in a high gene-flow marine fish, the small yellow croaker(Larimichthys polyactis).PLoS One, 8(12):e83493, https://doi.org/10.1371/journal.pone.0083493.
Wang X Y, Lu G Q, Zhao L L, Yang Q, Gao T X.2020.Assessment of fishery resources using environmental DNA:small yellow croaker (Larimichthys polyactis) in East China Sea.PLoS One, 15(12):e0044495, https://doi.org/10.1371/journal.pone.0244495.
Wang Y K, Huang J S, Dai Q F, Tang Y X, Sun Y, Jin X S.2016a.Insights into population structure of juvenile small yellow croaker (Larimichthys polyactis) in the Yellow Sea and the Bohai Sea from otolith elemental fingerprints.Haiyang Xuebao, 38(6):32-40, https://doi.org/10.3969/j.issn.0253-4193.2016.06.004. (in Chinese with English abstract)
Wang Y K, Huang J S, Tang X X, Jin X S, Sun Y.2016b.Stable isotopic composition of otoliths in identification of stock structure of small yellow croaker (Larimichthys polyactis) in China.Acta Oceanologica Sinica, 35(6):29-33, https://doi.org/10.1007/s13131-016-0868-z.
Xiao Y S, Song N, Li J, Xiao Z Z, Gao T X.2015.Significant population genetic structure detected in the small yellow croaker Larimichthys polyactis inferred from mitochondrial control region.Mitochondria DNA, 26(3):409-419, https://doi.org/10.3109/19401736.2013.843076.
Xiong Y, Liu H B, Jiang T, Liu P T, Tang J H, Zhong X M, Yang J, Wu L, Gao Y S.2015.Investigation on otolith microchemistry of wild Pampus argenteus and Miichthys miiuy in the Southern Yellow Sea, China.Haiyang Xuebao, 37(2):36-43, https://doi.org/10.3969/j.issn.0253-4193.2015.02.004. (in Chinese with English abstract)
Xiong Y, Yang J, Jiang T, Liu H B, Zhong X M, Tang J H.2017a.Early life history of the small yellow croaker(Larimichthys polyactis) in sandy ridges of the South Yellow Sea.Marine Biology Research, 13(9):993-1002, https://doi.org/10.1080/17451000.2017.1319067.
Xiong Y, Yang J, Jiang T, Liu H B, Zhong X M.2021.Temporal stability in the otolith Sr:Ca ratio of the yellow croaker, Larimichthys polyactis (Actinopterygii, Perciformes, Sciaenidae), from the southern Yellow Sea.Acta Ichthyologica et Piscatoria, 51(1):59-65, https://doi.org/10.3897/aiep.51.63245.
Xiong Y, Zhong X M, Tang J H, Yang J, Li L Z.2017b.Gillnet selectivity on the small yellow croaker Larimichthys polyactis in the Southern Yellow Sea.Turkish Journal of Fisheries and Aquatic Sciences, 17(6):1287-1296, https://doi.org/10.4194/1303-2712-v17_6_22.
Xiong Y, Zhong X M, Tang J H, Yang J.2016.Migration and population structure characteristics of the small yellow croaker Larimichthys polyactis in the southern Yellow Sea.Acta Oceanologica Sinica, 35(6):34-41, https://doi.org/10.1007/s13131-016-0844-7.
Xue Y, Jin X, Zhang B, Liang Z.2005.Seasonal, diel and ontogenetic variation in feeding patterns of small yellow croaker in the central Yellow Sea.Journal of Fish Biology, 67(1):33-50, https://doi.org/10.1111/j.0022-1112.2005.00677.x.
Yatsu A, Mochioka N, Morishita K, Toh H.1998.Strontium/Calcium ratios in statoliths of the neon flying squid, Ommastrephes bartrami (Cephalopoda), in the North Pacific Ocean.Marine Biology, 131(2):275-282, https://doi.org/10.1007/s002270050320.
Zhan W, Lou B, Chen R Y, Mao G M, Liu F, Xu D D, Wang L G, Ma T, Xu Q X.2016.Observation of embryonic, larva and juvenile development of small yellow croaker, Larimichthys polyactis.Oceanologia et Limnologia Sinica, 47(5):1033-1039, https://doi.org/10.11693/hyhz20160500114. (in Chinese with English abstract)
Zhang B D, Li Y L, Xue D X, Liu J X.2020.Population genomic evidence for high genetic connectivity among populations of small yellow croaker (Larimichthys polyactis) in inshore waters of China.Fisheries Research, 225:105505, https://doi.org/10.1016/j.fishres.2020.105505.
Zhang B D, Xue D X, Li Y L, Liu J X.2019a.RAD genotyping reveals fine-scale population structure and provides evidence for adaptive divergence in a commercially important fish from the northwestern Pacific Ocean.PeerJ, 7:e7242, https://doi.org/10.7717/peerj.7242.
Zhang C, Ye Z J, Wan R, Ma Q Y, Li Z G.2014.Investigating the population structure of small yellow croaker(Larimichthys polyactis) using internal and external features of otoliths.Fisheries Research, 153:41-47, https://doi.org/10.1016/j.fishres.2013.12.012.
Zhang S M, Jin S F, Zhang H, Fan W, Tang F H, Yang S L.2016.Distribution of bottom trawling effort in the Yellow Sea and East China Sea.PLoS One, 11(11):e0166640, https://doi.org/10.1371/journal.pone.0166640.
Zhang T T, Wang Y K, Yuan W, Jin X S, Chen C, Sun Y.2019b.Research on sagitta microstructure characteristics of Young of the Year (YOY) Larimichthys polyactis in the Bohai Sea.Progress in Fishery Sciences, 41(2):35-40, https://doi.org/10.19663/j.issn2095-9869.20190221001. (in Chinese with English abstract)
Zhu L X, Liang Z L, Ge C Z, Li C L.2020.An application of the Bayesian Hierarchical Approach to refining the information on main life history parameters for small yellow croaker, Larimichthys polyactis, off the coast of China.Ocean Science Journal, 55(1):143-155, https://doi.org/10.1007/s12601-020-0010-1.
Zlokovitz E R, Secor D H, Piccoli P M.2003.Patterns of migration in Hudson River striped bass as determined by otolith microchemistry.Fisheries Research, 63(2):245-259, https://doi.org/10.1016/s0165-7836(03) 00069-9.