Seasonal changes in species composition ofglass eels of the genus Anguilla (Teleostei:
Anguillidae) recruiting to the Cagayan River,Luzon Island, the Philippines
By Jun Aoyama*, Tatsuki Yoshinaga, Akira Shinoda, Fumiaki Shirotori,Apolinario V. Yambot and Yu-San Han
AbstractTropical species of anguillid glass eels have been recently exploited to be a substitute for the commercially important A. japonica or A. anguilla, so information about their life histories is needed to facilitate conservation. To understand ecological aspects of glass eel recruitment patterns of tropical eels, Anguilla spp., monthly monitoring of species compositions at the river mouth of the Cagayan River in northern Luzon of the Philippines was carried out at different time periods from May 2008 to September 2009 and from November 2011 to December 2012. Species identifications were made for 32,178 glass eels using morphology and / or genetics and a total of five anguillid species, A. bicolor pacifica, A. celebesensis, A. japonica, A. luzonensis and A. marmorata were found. In both time periods A. marmorata was dominant followed by A. luzonensis and A. bicolor pacifica, but the proportion of A. marmorata decreased from 55.1 % in 2008-2009 to 41.2 % in 2011-2012, with A. bicolor pacifica increasing from 3.9 % to 26.3 % and A. luzonensis staying relatively stable (41.0 %, 32.5%). Two other species, A. japonica and A. celebesensis, that were reported in previous studies from the Cagayan River were extremely rare. This study indicated that selective glass eel catch of a commercially preferred tropical species in this area is not feasible, as the harvest will include a high proportion of by-catch of economically less important species, potentially having significant impacts on their populations.
*Corresponding author. E-mail: [email protected]
Pacific Science, vol. 69, no. 2October 20, 2014 (Early view)
INTRODUCTION
A total of 19 species / subspecies of the genus anguilla are presently known in the world, with most of
them being found in tropical regions (aoyama 2009, watanabe et al. 2009). The catadromous life histories
of anguillid eels have been intensively studied during the last decade, providing significant advancements
in understanding of the ecology of these fascinating species. However, most research activities have
concentrated on temperate species and their tropical counterparts have been less-studied (see Aoyama
2009).
Anguillid eels have long been a fishery resource throughout their distribution range. In particular,
Japanese eels (A. japonica) have crucial economic importance in East Asia where they have been
intensively exploited for decades (Silfvergrip 2009). Recent critical shortages of glass eels for aquaculture
have greatly impacted the eel industries in East Asia and have stimulated increasing economic interest in
tropical anguillid species that have been less exploited so far. Commercial exploitation of tropical
anguillids for international trade has therefore likely increased in recent years.
The Philippines is a principal source of glass eel supply to East Asia because of its
geographic advantage close to the final destination and the possible occurrence of A. japonica
glass eels in the northern part of Luzon Island (Crook and Nakamura 2013, Tabeta et al. 1976).
However, the recent finding of a cryptic species, A. luzonensis, from Luzon Island (Watanabe et
al. 2009) indicates that the commercial exploitations of glass eels in this area has been carried
out without clear biological or ecological information about the species being harvested. Indeed,
Yoshinaga et al. (2014) recently found that glass eels of A. luzonensis were collected by local fishermen at
the estuary of the Cagayan River for export to East Asia in 2009. These facts strongly suggest the need for
reassessment of the anguillid eels in this area in order to understand their life histories and ecology to
facilitate their management and conservation.
The East Asia Eel Resource Consortium (EASEC) consists of scientists, traders, fishermen, non-
profit organizations and governmental officials from Taiwan, Mainland China, South Korea and Japan
and was established in 1998 to share the latest information about conservation, aquaculture and trade of
2
the Japanese eel. EASEC started monitoring glass eel recruitment in Japan (Aoyama et al. 2012) and
Taiwan (Han 2013) from 2009. The research initiative was named ‘Eel River Project’. Considering recent
commercial interest in tropical anguillids as an alternative to the Japanese eel or the European eel in East
Asia, EASEC concluded that an Eel River Project was needed to determine the present status of glass eels
recruiting to the Philippines. This paper reports species identities and changes in the species composition
of glass eels recruiting to the Cagayan River estuary, northern Luzon, the Philippines at both monthly and
interannual time scales.
MATERIALS AND METHODS
Samples
Glass eels were sampled monthly from a commercial fisherman who operated set nets in the river mouth
of the Cagayan River on northern Luzon Island of the Philippines during May 2008 to September 2009
(Period I) and November 2011 to December 2012 (Period II, Fig. 1, Table 1). Set nets consisted of a bag
cod-end with 5 m long and 2 m height wings on either side and were operated throughout the year for
glass eel catches.
Eels sampled for the present study varied from 103 to 2327 individuals per month depending on
the catch and price of glass eels in the field (Table 1). The specimens were preserved in 99.5 % v/v
ethanol immediately after collection and were transferred to the laboratory at ambient temperature for
subsequent analyses. It should be noted that the samples do not indicate the absolute abundance of glass
eels recruiting to the Cagayan River, and statistical records are not available for the overall catches and
trading from the local government or any fisheries agency.
Morphological species identification
Glass eels of five species, A. bicolor pacifica, A. celebesensis, A. japonica, A. marmorata and the recently
described A. luzonensis have been reported from the Cagayan River (Han et al. 2012, Tabeta et al. 1976,
Watanabe et al. 2009). The specimens collected in the present study were first classified morphologically
into two groups, the short-finned (A. bicolor pacifica) or the long-finned (the other four species), based on
3
the length between verticals through the anus and origin of the dorsal fin in percent of the total length
(AD/TL), following previous studies (Ege 1939, Leander et al. 2012, Tabeta et al. 1976, Watanabe 2003,
Watanabe et al. 2004). Among the long-finned specimens (AD/TL > 5), A. japonica was identified by the
absence of cutaneous caudal pigmentation that is well developed in the other long-finned species
(Leander et al. 2012, Tabeta et al. 1976, Yoshinaga et al. 2014).
Genetic species identification
All long-finned specimens collected in Period I were genetically identified using the species-specific PCR
amplification method reported by Han et al. (2012). Specimens that showed no clear specific
amplification and some individuals (8-163) from each month that showed an AD/TL value of less than 13
% (A. luzonensis or A. celebesensis) were further identified using a partial sequence of the mitochondrial
cytochrome b gene to confirm their species identification (Table 1). In Period II, 85-96 long-finned
specimens (A. celebesensis or A. luzonensis or A. marmorata) were randomly selected from each month,
resulting in 1209 specimens being identified using a partial sequence of the mitochondrial 16S rRNA
gene. The genetic methods were described in detail elsewhere (Han et al. 2012 for Period I, Yoshinaga et
al. 2014 for Period II).
The sequences were matched with the previously described data in DDBJ/EMBL/GenBank
databases by a BLAST search. The relative abundances of the long-finned species genetically identified
from the monthly sub-sampled specimens for Period II were scaled up to estimate the proportional species
composition of each month. Genetic data obtained in the present study are available upon request to the
corresponding author.
RESULTS
A total of five species, A. bicolor pacifica, A. celebesensis, A. japonica, A. luzonensis and A. marmorata,
were morphologically and / or genetically identified among the 32,178 total glass eel specimens examined
in the present study (Table 1, Fig. 2). However, only 20 A. celebesensis and one A. japonica were found
suggesting that they are extremely rare in the Cagayan River (Fig. 2). The other three species, A. bicolor
4
pacifica, A. luzonensis and A. marmorata showed consistent recruitment almost throughout the year but
with different seasonal peaks and annual fluctuation patterns.
During Period I that examined a total of 8,643 glass eels, A. marmorata was the dominant species
(55.1 % of all glass eels) followed by A. luzonensis (41.0 %) and A. bicolor pacifica (3.9 %). A.
marmorata comprised a high proportion of the glass eels sampled from October 2008 to June 2009 (52.7 -
95.2 %) while it comprised only 7.5 - 37.7 % during July to September both in 2008 and 2009 (Fig. 2A).
A. luzonensis exhibited an increase in relative abundance during July to September (60.3 - 86.6 % in 2008
and 73.3 - 88.6 % in 2009), with low abundance in the other months (2.1 - 32.7%, Fig. 2A). A. bicolor
pacifica was a low proportion of the catch (0 - 14.6 %) all year round (Fig. 2A).
In Period II that examined a total of 23,535 glass eels, A. marmorata decreased to 38.0 % and A.
bicolor pacifica increased to 29.5 %, while A. luzonensis comprised a similar proportion (32.5 %) as in
Period I. The nine month period of high A. marmorata relative abundance found in Period I was
diminished to five months from January to May in 2012 and A. bicolor pacifica significantly dominated
(more than 95 %) in November and December 2011 (Fig. 2B). A similar pattern of an increase of A.
bicolor pacifica seemed to occur in October and November 2012, although A. marmorata was found in
relatively high proportion during these months (35.0 %, 49.4%, respectively, Fig. 2B)
DISCUSSION
Glass eels in the Cagayan River
The present study was the first to make monthly observations of the species composition of glass eels
recruiting to the Cagayan River in different time periods (May 2008 -September 2009 and November
2011 - November 2012). It clearly showed that A. bicolor pacifica, A. luzonensis and A. marmorata glass
eels are consistently recruiting to the study area, but A. celebesensis and A. japonica that were reported in
the previous studies rarely occurred.
The North Pacific population of A. marmorata that is distributed from Sulawesi Island north
through the Philippines to southern Japan (Ishikawa et al. 2004, Minegishi et al. 2008) has a spawning
area in the North Equatorial Current (NEC) to the west of the Mariana Islands (Miller et al. 2002). They
5
also spawn at a variety of times throughout the year (Kuroki et al. 2009, Miller et al. 2009). Recently,
Kuroki et al. (2012) analyzed a small number of leptocephali of A. luzonensis collected in the tropical
western North Pacific region and suggested their spawning area and larval migration processes were
similar to the North Pacific population of A. marmorata . In contrast, the spawning area and subsequent
larval migration of A. bicolor pacifica in the North Pacific are almost not known, because only large
leptocephali of this species have been collected (Miller et al. 2009).
The different fluctuation patterns found for A. bicolor pacifica, A. luzonensis and A. marmorata in
the present study give new insights into their spawning ecology. Given that A. luzonensis and A.
marmorata experience the same oceanographic conditions from their similar spawning areas to northern
Luzon, these two species might be expected to show a similar fluctuation pattern in their recruitment.
However, the actual proportion of A. marmorata decreased from 55.1 % in period I to 38.0 % in period II,
whereas A. luzonensis had almost the same percentages in the two periods (41.0 % and 32.5%,
respectively). This may be due to having different spawning seasons or peaks, with the former species
spawning almost throughout the year and the latter possibly spawning in the spring season from February
to May (Kuroki et al. 2012). Considering that only five large sized leptocephali of A. luzonensis (29.2 -
51.2 mm in TL, Kuroki et al. 2012) have ever been found in the north Pacific (Shinoda et al. 2011), it is
also possible that A. luzonensis spawns somewhere different from A. marmorata, causing it to have
different larval transport patterns. Similarly the fluctuation pattern of A. bicolor pacifica found in the
present study suggested that they spawn in a different area and their larvae reach northern Luzon through
a different route that of A. marmorata and A. luzonensis.
The present study showed significant fluctuations in the species composition of glass eels
recruited to the Cagayan River. Considering the sympatric distribution of several anguillid species in the
tropics and their specific reproductive characters that vary inter-annually (See Aoyama 2009, Hagihara et
al. 2012, Miller 2009, Miller et al. 2009), it is reasonably supposed that the species composition of glass
eels in the tropics drastically changes year by year. This has also been reported for A. celebesensis in the
Poigar River, Sulawesi Island, Indonesia (Sugeha et al. 2001). Accordingly, selective catch of a
commercially preferred species, such as A. bicolor pacifica that is a plain-skinned species like the
6
Japanese eel is quite difficult. The glass eel catch in the tropics is likely to include a high proportion of
by-catch of economically less important species and could potentially result in significant impact on the
by-catch species. Further observation of the actual amount of glass eels being harvested and precautionary
conservation measures for tropical anguillid eels are urgently needed.
Revisiting the species range of A. celebesensis and A. japonica
The present study clearly revealed that the glass eels of A. celebesensis and A. japonica that were
previously reported from the Cagayan River rarely occurred during the time periods of this study. Tabeta
et al. (1976) found six A. japonica among 5,404 glass eels or elvers collected at the Cagayan River during
1970 - 1974, and Yoshinaga et al. (2014) more recently identified 52 A. japonica glass eels from a total of
767 specimens sampled in 2009 from the same area. Following these reports, the present study also found
A. japonica in this area, but only one glass eel in February 2009 among the 32,178 glass eels collected
during a total of 29 months in the different years. These facts suggest that A. japonica only rarely recruits
to the northern Luzon region, probably only as a result of a specific oceanographic condition transporting
them to this area, as apparently occurred in 2009. But even after they enter the estuary, A. japonica likely
may not survive in the Cagayan River system during their growth phase, because of environmental
constraints in the tropical habitat or interspecies competition with the tropical anguillid species. Indeed,
Jamandre et al. (2007) who surveyed the anguillids in the Cagayan River system did not find A. japonica
in the river. The species range of A. japonica has long been thought to include the northern Philippines
(e.g., Silfvergrip 2009, Watanabe et al. 2004), but no adults (yellow or silver eel) have ever been found in
this region. Therefore, the northern Philippines should probably not be considered as part of the species
range of A. japonica.
The geographic distribution of A. celebesensis also needs reconsideration. This species was
thought to inhabit the western tropical North Pacific region mainly from Indonesia (Ege 1939, Silfvergrip
2009, Watanabe 2003) to the Philippines (Arai et al., 2003, Tabeta et al., 1976) to as far as Taiwan (Tzeng
1982). However, Watanabe et al. (2009) recently described A. luzonensis, which was morphologically
indistinguishable from A. celebesensis. The present study found that the northern part of Luzon rarely had
7
A. celebesensis glass eels arriving there, but A. luzonensis occurred consistently as the second-most
dominant species. Spawning areas of A. celebesensis have been found in the Indonesian waters of the
Celebes Sea and Tomini Bay (Aoyama et al. 2003) and the large leptocephali of A. luzonensis were found
in the NEC region far offshore in the western North Pacific (Kuroki et al. 2012). This suggests that A.
celebesensis is mainly distributed around Sulawesi Island and adjacent areas with their spawning sites
located nearby and being reached after a short-distance migration (Aoyama et al. 2003, Kuroki et al.
2006). In contrast, A. luzonensis that spawns in the western North Pacific, disperses westward during their
larval migration in the NEC (Kuroki et al. 2012). Arai et al. (2003) reported a significant difference in the
larval duration of A. celebesensis from Indonesia (the Poso River (98 ± 7.2 days) and the Poigar River (90
± 13.6 days) in Sulawesi Island) and the Philippines (the Cagayan River (124 ± 12.0 days) in Luzon
Island). This difference was probably because their morphologicaly-identified samples of A. celebesensis
from the Cagayan River were actually glass eels A. luzonensis, a species that was unknown at that time.
Present knowledge on A. celebesensis as well as their species range should be carefully revisited in
consideration with the newly described A. luzonensis.
ACKNOWLEDGMENTS
This study was partly supported by grants-in-aid for Scientific Research from the Japan Society for the
Promotion of Science (Nos. 21405024, 5450281), National Science Council of the Executive Yuan,
Taiwan (NSC 99-2313-B-002-021-MY3, NSC 102-2321-B-002 -073, NSC 102-2628-B-002 -023 -MY3)
and the Philippine Council for Aquatic and Marine Research and Development (PCAMRD), Department
of Science and Technology, Commission on Higher Education, Philippines for the funding.
8
Figure 1. A. Map of the western North Pacific region showing the approximate location of the
offshore spawning area (shaded oval) of Anguilla marmorata and the North Equatorial Current
and adjacent major currents. B. Map showing the northern part of Luzon Island and C. the river
mouth of the Cagayan River with the glass eel collection area (square with dashed line) where the
set nets were located.
10
Figure 2. Monthly changes in the relative abundance of anguillid glass eels recruiting to the
Cagayan River during Period I in May 2008 to September 2009 (A) and Period II in November
2011 to December 2012 (B). * One specimens of A. japonica was found in February 2009.
11
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