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研究生:林德
研究生(外文):Nico Jose Leander
論文名稱:從耳石日成長輪及微化學探討西北太平洋區鱸鰻之生活史特性
論文名稱(外文):Life history traits of the giant mottled eel Anguilla marmorata in the northwestern Pacific as revealed from otolith daily growth increment and microchemistry
指導教授:曾萬年曾萬年引用關係
指導教授(外文):Wann-Nian Tzeng
口試委員:邵廣昭李國添曾晴賢王佳惠王慧瑜
口試委員(外文):Kwang-Tsao ShaoKuo-Tien LeeChyng-Shyan TzengChia-Hui WangHui-Yu wang
口試日期:2014-06-27
學位類別:博士
校院名稱:國立臺灣大學
系所名稱:漁業科學研究所
學門:農業科學學門
學類:漁業學類
論文種類:學術論文
論文出版年:2014
畢業學年度:102
語文別:英文
論文頁數:142
中文關鍵詞:耳石日成長輪鱸鰻玻璃鰻加入動態洄游環境史
外文關鍵詞:Otolithdaily growth incrementgiant mottled eelglass eelsrecruitment dynamicsmigratory environmental history
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為了瞭解西北太平洋熱帶性鱸鰻之加入動態和初期生活史以及菲律賓水域同種鰻的洄游環境史。本研究調查2005-2009年台灣東部秀姑巒溪河口玻璃鰻的種類組成,結果發現鱸鰻的玻璃鰻數量最多,占總捕獲量的98.4%;另外有少量的太平洋雙色鰻 (1.6%) 及日本鰻(<1%)。熱帶性鱸鰻的玻璃鰻的主要出現季節為春夏天,但幾乎終年都可發現;而太平洋雙色鰻的玻璃鰻的主要出現季節為秋天;溫帶性日本鰻的玻璃鰻的出現季節則是在冬天。
透過東北亞地區不同河口所捕獲的鱸鰻和日本鰻玻璃鰻的耳石日周輪分析顯示,柳葉鰻變態的日齡及早期成長率對於此兩種同域分布鰻魚的分離洄游及緯度分布扮演重要的角色。成長快、變態早的鱸鰻柳葉鰻較早加入到菲律賓;而成長慢、延遲變態的日本鰻柳葉鰻繼續向南(經由明答那峨海流)及向北(經由黑潮)飄送。另一方面,日本鰻柳葉鰻抵達菲律賓水域時尚未到變態階段,所以也不會洄游到河口,而是繼續向北散佈。這可能就是日本鰻很少在菲律賓發現而鱸鰻在菲律賓數量很多的原因。
電子微探儀(EPMA)分析顯示,採集於菲律賓呂宋島東部河川的鱸鰻耳石鍶鈣比數據和之前所報導的日本及越南的鱸鰻以及日本鰻的洄游環境史非常不同。在耳石鰻線標記之後到耳石邊緣的鍶鈣比都低於4 x 103,顯示菲律賓呂宋島東側的鱸鰻在鰻線階段進入淡水溪流後一直到被捕獲的黃鰻階段為止都悽息在淡水環境中。此結果和台灣的鱸鰻一樣,在黃鰻階段都只棲息在淡水中。而日本鰻在黃鰻階段的棲地利用則較為彈性,可在海水、鹹淡水和淡水之間洄游。種間競爭、環境喜好性以及生產力可能是造成鱸鰻和日本鰻的棲地喜好性不同的原因。本研究之發現可提供鰻魚資源保育之參考。


The present study investigated the recruitment dynamics and early life history of the tropical eel Anguilla marmorata in the northwestern Pacific as well as the migratory environmental history of the eel in the Philippine waters.
Analysis of the species composition of the recruiting glass eels in the estuary of the Hsiukuluan River, Eastern Taiwan from 2005-2009 revealed that A. marmorata was the most dominant eel species making up to 98.4% of the total catch while there were very few A. bicolor pacifica (1.6%) and A. japonica (<1%). Tropical eel species A. marmorata recruited mainly to the estuary during spring to summer but can be found year-round while A. bicolor pacifica recruited mainly during autumn. The temperate species, A. japonica, recruited mainly during winter.
Examinations of the otolith daily growth increments of A. marmorata and A. japonica glass eels collected from various rivers and estuaries in East Asia from 1992-2008 indicated that age at metamorphosis and early growth rate seem to play an important role in the segregative migration and latitudinal distribution of these two sympatric eel species in the northwestern Pacific. Faster-growing and earlier-metamorphosing leptocephali of A. marmorata recruited earlier in the Philippines while its slower-growing, delayed metamorphosing leptocephali dispersed southward (via the Mindanao Current) and northward (via the Kuroshio Current). On the other hand, the A. japonica leptocephali which arrive in the Philippine waters are apparently too young to metamorphose and migrate towards the estuaries so it will continue to drift northwards. This must be the reason why Japanese eels are seldom found in the Philippines while A. marmorata occurs in abundance.
The Sr:Ca profile in the otoliths of yellow-stage A. marmorata collected in the river of eastern Luzon, the Philippines in August 2008 revealed that it’s migratory environmental history is quite different from that previously reported from Japan and Vietnam and from A. japonica. Electron probe microanalyzer showed that after the elver check, the Sr:Ca ratio until the otolith edge were less than 4 x 10-3, indicating that after recruitment, A. marmorata just stayed in freshwater until capture, which is similar to that of A. marmorata in Taiwan. On the contrary, A. japonica has a more flexible migratory behavior in the yellow stage. It can migrate among seawater, brackish water and freshwater in the yellow eel stage. Interspecific competition, environmental factors and the productivity of the environment may play an important role in the habitat preference of A. marmorata throughout its species range. The findings of this study can provide the information for the eel conservation and management.


TABLE OF CONTENTS
Title page………………………………………………………………………………………….i
Approval sheet…………………………………………………………………………………...ii
Acknowledgement……………………………………………………………………………….iii
Abstract…………………………………………………………………………………………...v
Table of Contents………………………………………………………………………………..ix
List of Tables…………………………………………………………………………………...xiii
List of Figures…………………………………………………………………………………...xv
List of Appendices……………………………………………………………………………xxiii
CHAPTER 1: INTRODUCTION
1.1 Life history pattern of freshwater eel (Anguilla spp.)…………………………………1
1.2 Freshwater eel fishery and its problem………………………………………………..4
1.3 Population decline of freshwater eel…………………………………………………..4
1.4 Biology and population structure of Anguilla marmorata…………………………...10
1.5 Application of otolith daily growth increment and microchemistry to life history study………………………………………………………………………………….14
1.6 Current research status of Anguilla marmorata……………………………………...17
1.7 Objectives of this study………………………………………………………………19
CHAPTER 2: MATERIAL AND METHODS
2.1 Glass eel collection
2.1.1 Temporal sampling………………………………………………………...20
2.1.2 Spatial sampling……………………………………………………………24
2.2 Juvenile eel collection………………………………………………………………..27
2.3 Glass eel species identification and morphometric measurements…………………..29
2.4 DNA extraction, polymerase chain reaction (PCR) amplification and phylogenetic
analysis………………………………………………………………………………..30
2.5 Determination of glass eel developmental stages……………………………………33
2.6 Morphometric measurements of adult eels…………………………………………..37
2.7 Otolith extraction and preparation for daily growth increment and microchemistry
analyses……………………………………………………………………………...39
2.8 Life history parameters obtained from otolith daily growth increment analyses……40
CHAPTER 3: RESULTS
3.1 Species identification for the glass eel recruiting to Hsiukuluan River, Eastern
Taiwan ………………………………………………………………………………...44
3.2 Species composition of the glass eel recruited to Hsiukuluan River………………...49
3.3 Stage composition of the glass eel recruited to Hsiukuluan River ……………….....52
3.4 Comparison of morphometric characters of glass eels among species……………....55
3.5 Daily growth increments and growth checks in the otoliths of glass eel of Anguilla
marmorata …………………………………………………………………………...62
3.6 Comparison of the developmental stage composition between Anguilla marmorata
and A. japonica glass eels…………………………………………………………....72
3.7 Differences in size and age at estuarine arrival between Anguilla marmorata and
A. japonica glass eels…………………………………………………………………76
3.8 The timing of metamorphosis from leptocephalus to glass eel as indicated by otolith
daily growth rates and Sr:Ca ratios………………………...........................................79
3.9 Back-calculated hatching dates of Anguilla marmorata and A. japonica…………...85
3.10 Age at metamorphosis in relation to the growth rate and distance from the spawning
grounds………………………………………………………………………………..87
3.11 Migratory environmental history and habitat use of Anguilla marmorata juveniles in
the Philippines as indicated by otolith Sr:Ca ratios………………………………...95
CHAPTER 4: DISCUSSION
4.1 The differences in spatial recruitment patterns among species of glass eel in
Taiwan ………….........................................................................................................102
4.2 Differences in seasonal occurrence between Anguilla marmorata and A. japonica in
Taiwan………………………………………………………………………………106
4.3 The metamorphosis timing differs between Anguilla marmorata and A. japonica and
its ecological evolution significance………………………………………………...107
4.4 Delayed metamorphosis as a means of long-distance dispersal of the eel…………110
4.5 The early growth rate affects dispersal range of leptocephali ……………………..112
4.6 Spatial and temporal population genetic structure of the giant mottled eel Anguilla
marmorata in the northwestern Pacific……………………………………………..113
4.7 Migration behavior and habitat use of Anguilla marmorata in eastern Luzon,
Philippines………………………………………………………………………......115
CHAPTER 5: CONCLUSION AND PERSPECTIVE
5.1 Species-specific geographic distribution…………………………………………...118
5.2 Role of larval growth rate and metamorphosis timing in determining the geographical
distribution of the anguillid eel ……………………………………………………..118
5.3 Migratory environmental history of Anguilla marmorata is different from that of A.
japonica ……………………………………………………………………………..119
REFERENCES………………………………………………………………………………...121
APPENDICES…………………………………………………………………………………140
















LIST OF TABLES
TABLE 1. Sampling information and sample sizes of the anguillid glass eel collected in the lower reach of Hsiukuluan River, eastern Taiwan……………………………………………….23

TABLE 2. Sampling information and sample sizes of A. japonica and A. marmorata glass eel collection in various rivers and estuaries in East Asia. Values inside the parentheses indicate the number of individuals used for otolith analyses…………………………………………………26

TABLE 3. Development of pigmentation in anguillid eels (Tesch2003)……………………….36

TABLE 4. Species composition of Anguilla glass eels collected in the lower reach of Hsiukuluan
River in Eastern Taiwan from 2005-2009……………………………………………………….50

TABLE 5. Pigmentation stages of the different Anguilla eel species collected from 2 stations in the lower reach of Hsiukuluan River…………………………………………………………….53

TABLE 6. Comparison of morphometric characters among the 4 Anguilla species……………59

TABLE 7. Sampling sites, sample sizes, sampling dates, total lengths, daily age of glass eels at the estuary (Tt), daily age at metamorphosis from leptocephalus to glass eel (Tm), and the time between the metamorphosis check and estuarine arrival (Tt-m) of Anguilla japonica and A. marmorata……………………………………………………………………………………….73

TABLE 8. Pigmentation stages of glass eels of Anguilla japonica and A. marmorata collected from various rivers and estuaries in East Asia…………………………………………………...75

TABLE 9. Mean (± SD) increment widths of otoliths radii Rm, Rt, and Rt-m in of Anguilla japonica and A. marmorata glass eels.…………………………………………………………..80

TABLE 10. Age and estimated hatch date of glass eels of Anguilla japonica and A. marmorata recruiting in East Asia……………………………………………………………………………86

TABLE 11. Sampling information of the adult eels collected from a river system in Aurora province, eastern Luzon, Philippines on August 6, 2012. ………………………………………95

TABLE 12. Sampling information of the adult eels collected from an aquaculture farm in Sanya, southern Hainan province, China………………………………………………………………...96










LIST OF FIGURES
FIGURE 1. Life cycle and catadromous migration of anguillid eels…………………………….3

FIGURE 2. Recruitment (3 year running averages of geomeans of indices as % of 1979-1994 means) for the European (Moses-Saunders Index – 7 years), American (adjusted to year of arrival) and Japanese glass eels from Taiwan……………………………………………………..5

FIGURE 3. Population decline in Anguilla japonica (a; Tsukamoto et al. 2009) and A. marmorata (b; Prof. C.S. Tzeng, unpublished)…………………………………………………..8

FIGURE 4. Migration cycle of the northwestern Pacific population of Anguilla marmorata….12

FIGURE 5. Map showing the species range (thick black lines along the coasts) of Anguilla marmorata (a) and A. japonica (b) in East Asia and the geographic distribution of their larvae (data from Kuroki et al. 2006 and Tsukamoto 2009)……………………………………………13

FIGURE 6. The orientation of the semicircular canals and otoliths within the inner ear of teleost fish (a) and the transverse section of the inner ear showing the positions of each otoliths (b) (image modified from Panfili et al. 2002)……………………………………………………….16

FIGURE 7. Map showing glass eel sampling stations (1 and 2) in the lower reach of the Hsiukuluan River in eastern Taiwan……………………………………………………………..21

FIGURE 8. Fish way trap used to collect the migrating fish larvae in the lower reach of Hsiukuluan River (a) and the dimension of the tin trap (b)……………………………………...22

FIGURE 9. Map showing the geographic distributions of Anguilla japonica (thick gray lines on the coastlines) and A. marmorata (thick black lines on the coastlines) in East Asia and collection sites of samples analyzed in this study (&;#8710;, A. marmorata; Ο, A. japonica ; Cheng and Tzeng 1996)……………………………………………………………………………………………..25

FIGURE 10. Sampling location of the juvenile eels in a river system in Aurora province in eastern Luzon, Philippines……………………………………………………………………….27

FIGURE 11. Electro-fishing gear (a) used to collect juvenile eels in a river system (b) in Aurora province, eastern Luzon, Philippines…………………………………………………………….28

FIGURE 12. Schematic diagram of the methods used for anguillid glass eel species identification……………………………………………………………………………………..32

FIGURE 13. Diagram showing morphometric measurements of the glass eel…………………33

FIGURE 14a. Progressive sub-epidermal pigmentation in the anal region of the glass eel used to determine the different ontogenetic stages (after Strubberg, 1913; Bertin 1956; Tesch 2003)….34

FIGURE 14b. Developmental stages (VIA1 to VIB) in Japanese eels showing pigmentation process from glass eel to the fully pigmented elver stage at VIB. Arrows indicates the location of the unique pigmentation characteristic of each stage (adapted from Fukuda et al. 2013)……………………………………………………………………………………………..35

FIGURE 15. Diagram showing morphometric measurements of the adult eel…………………38

FIGURE 16. Schematic diagram of the measurements of radii and counts of the daily growth increments in the otoliths of the elvers (modified from Cheng and Tzeng 1996; Wang and Tzeng 2000)……………………………………………………………………………………………..43

FIGURE 17. Origins of the dorsal fin (black triangle) and anal fin (gray triangle) in longfin (a, A. japonica and b, A. marmorata, A. celebesensis and A. luzonensis) and shortfin (c, A. bicolor pacifica) glass eels………………………………………………………………………………46

FIGURE 18. Caudal in and tail bud pigmentation patterns of anguillid glass eels……………..47

FIGURE 19. Phylogenetic tree of the genus Anguilla inferred from cytochrome b sequences...48

FIGURE 20. Species composition of the recruiting glass eels collected in 2 stations at the lower reach of Hsiukuluan River, Eastern Taiwan from 2005-2009…………………………………...51

FIGURE 21. Developmental stage composition of recruiting glass eels according to sampling station…………………………………………………………………………………………….54
FIGURE 22. Length frequency distribution of glass eels of Anguilla japonica (a), A. bicolor pacifica (b), and A. marmorata (c) caught in the lower reach of Hsiukuluan River of Eastern Taiwan and A. celebesensis (d) (Tzeng 1982)…………………………………………………56

FIGURE 23. Relationship between pre-dorsal fin length and total length in the glass eels of Anguilla japonica, A. bicolor pacifica, A. marmorata and A. celebesensis (from Tzeng 1982)……………………………………………………………………………………………..60

FIGURE 24. Relationship between ano-dorsal fin length and total length in the glass eels of Anguilla japonica, A. bicolor pacifica, A. marmorata and A. celebesensis (from Tzeng 1982)...61

FIGURE 25. SEM photographs showing daily growth increments (DGIs) and growth checks in an otolith of an Anguilla marmorata elver………………………………………………………64

FIGURE 25a. Peripheral region of the Anguilla marmorata glass eel otolith showing the estuarine check (white arrow) and the otolith edge (black arrow)……………………………….65

FIGURE 25b. SEM photograph showing the metamorphosis check (black arrow) in the Anguilla marmorata glass eel otolith……………………………………………………………………...66

FIGURE 25c. SEM photograph showing the discontinuous (dark band, black arrow) and increment (light band, white arrow) zones in the Anguilla marmorata glass eel otolith………...67

FIGURE 25d. Core region of the of the Anguilla marmorata glass eel otolith showing the primordium (gray arrow), yolk-sac stage (red line), hatching check (white arrow) and the 1st feeding check (black arrow)……………………………………………………………………...68

FIGURE 26a. Core region of the A. marmorata glass eel otolith showing a distinct and well-defined primordium……………………………………………………………………………...69

FIGURE 26b. Core region of the A. marmorata glass eel otolith showing an undefined primordium………………………………………………………………………………………70

FIGURE 26c. Core region of the A. marmorata glass eel otolith showing twin primordia…………………………………………………………………………………………71

FIGURE 27. Developmental stage composition of recruiting Anguilla marmorata (a) and A. japonica glass eels……………………………………………………………………………….74

FIGURE 28. Length-frequency distribution of recruiting Anguilla marmorata glass eels from the Philippines, Taiwan, China and Japan……………………………………………………….77

FIGURE 29. Length-frequency distribution of recruiting Anguilla japonica glass eels from the Taiwan, China and Japan………………………………………………………………………...78

FIGURE 30. Profiles of otolith growth increment width (blank circle) and Sr:Ca concentration ratios measured using electron probe microanalyzer (solid diamond) from the primordium to the edge in A. marmorata glass eels…………………………………………………………………81

FIGURE 31. Otolith Sr:Ca profiles of the A. marmorata glass eels collected from the Philippines……………………………………………………………………………………….82

FIGURE 32. Otolith Sr:Ca profiles of the A. marmorata glass eels collected from Taiwan…...83

FIGURE 33. Otolith Sr:Ca profiles of the A. marmorata glass eels collected from Japan ….....84

FIGURE 34. Spatial changes in age at metamorphosis in A. marmorata (a) and A. japonica (b).............................................................................................................................................88

FIGURE 35. Spatial changes in age at recruitment in A. marmorata (a) and A. japonica (b)………………………………………………………………………………………………...89

FIGURE 36. Spatial changes in length at recruitment in A. marmorata (a) and A. japonica (b)………………………………………………………………………………………………...90

FIGURE 37. Spatial changes in time between metamorphosis and age at recruitment in A. marmorata (a) and A. japonica (b)………………………………………………………………91

FIGURE 38. Relationship between the age at metamorphosis (Tm) and growth rate (Gm) before metamorphosis in Anguilla marmorata………………………………………………………….92

FIGURE 39. Relationship between the age at metamorphosis (Tm) and growth rate (Gm) before metamorphosis in Anguilla japonica…………………………………………………………….93

FIGURE 40. Relationship between the larval dispersal distance and age at metamorphosis (Tm) in Anguilla marmorata (open symbols) and A. japonica (solid symbols)……………………….94

FIGURE 41. An otolith sample of a wild Anguilla marmorata (553.86 mm TL) from Aurora province, Philippines……………………………………………………………………………..97

FIGURE 42. An otolith sample of a cultured Anguilla marmorata (785 mm TL) from Hainan province, China…………………………………………………………………………………..98

FIGURE 43. Temporal changes in the otolith Sr:Ca ratios (measured from the core to the edge) of A. marmorata collected from the Philippines………………………………………………..100

FIGURE 44. Temporal changes in the otolith Sr:Ca ratios (measured from the core to the edge) of A. marmorata collected from an aquaculture farm in Sanya, southern Hainan Province,
China……………………………………………………………………………………………101

FIGURE 45. Distribution patterns and abundances of A. marmorata and other anguillid eels in Taiwan…………………………………………………………………………………………..105

FIGURE 46. Anguillid eel metamorphosis from leptocephalus to glass eel and some of the accompanying physiological changes…………………………………………………………..109
















LIST OF APPENDICES
APPENDIX 1. Fisheries Administrative Order 242 of the Philippines………………………..140

APPENDIX 2. Papers, abstracts and presentations related to this dissertation………………..142





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