Biol Invasions (2012) 14:2471–2478 DOI 10.1007/s10530-012-0250-9
INVASION NOTE
Massive invasion of Arctodiaptomus dorsalis (Copepoda, Calanoida, Diaptomidae) in Philippine lakes: a threat to Asian zooplankton biodiversity? Rey Donne S. Papa • Huiming Li • Dino T. Tordesillas • Boping Han • Henri J. Dumont
Received: 13 December 2011 / Accepted: 11 May 2012 / Published online: 26 May 2012 Ó Springer Science+Business Media B.V. 2012
Abstract A study originally intended to update the systematics and zoogeography of calanoid copepods in Philippine lakes has led to the discovery of an invasion by the Neotropical Arctodiaptomus dorsalis. It now occurs in 18 out of 27 lakes in the archipelago. Only four of the 12 previously recorded native and endemic calanoids have been encountered in the lakes, which may indicate that most have been displaced by A. dorsalis, although a general deterioration of water quality by fish culture may also have contributed to a suppression of the local fauna. Undescribed species may have been affected as well. A. dorsalis was first reported in the Philippines from Laguna de Bay in 1991, where it was said to have been introduced via ship drinking water reserves, but co-introduction with tilapia is more probable. Intensive aquaculture practices during the R. D. S. Papa (&) D. T. Tordesillas Graduate School and Research Center for the Natural and Applied Sciences, University of Santo Tomas, Manila, Philippines e-mail:
[email protected];
[email protected] H. Li B. Han H. J. Dumont Department of Ecology and Institute of Hydrobiology, Jinan University, 510632 Guangzhou, China D. T. Tordesillas Department of Biology, St. Paul University, Quezon City, Philippines H. J. Dumont Department of Biology, Ghent University, Ghent, Belgium
past 20 years have aided its dispersal to other areas and have provided environmental conditions that favor its survival. The rapid spread of A. dorsalis, paralleled by a loss of calanoid diversity in the Philippines, may repeat itself if this opportunistic species succeeds in spreading to mainland Asia. Keywords Aquaculture Lake biodiversity Laguna de Bay Transcontinental introductions
Introduction Studies on Philippine calanoid zooplankton were pioneered by Wright (1928), Kiefer (1928a, b, 1930), and Brehm (1933, 1942), with an early synthesis dating back to the Wallacea Expedition (Woltereck et al. 1941) but with little follow-up in subsequent decades. In the 1970s, the freshwater zooplankton in the Philippines enumerated a total of only 125 species of Copepoda, Cladocera and Rotifera. More recent estimates put the total number of freshwater zooplankton species in the Philippines at a meager 141 spp. (Mamaril Sr and Fernando 1978; Mamaril Sr 2001). This over-all lack of scientific interest in zooplankton and low number of studies in the country may now have become an irreversible handicap, as a recent attempt to update our knowledge has instead revealed the presence, often in overwhelming numbers, of an invasive calanoid copepod. Such non-indigenous zooplankton (NIZ) invasions are
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widely recognized as a global cause for concern. The review by Bollens et al. (2002) enumerated 29 case studies among cnidarians, rotifers, cladocerans, copepods, mysids, and insects. That number may have more than doubled since, but to date, almost no cases from the tropics have been documented. Arctodiaptomus dorsalis (Marsh 1907) is a Neotropical calanoid species originally described from lakes near New Orleans, Louisiana. Its core range extends between the Gulf of Mexico and the Caribbean Sea, from the southern United States to Central America and northern South America. A spread to new localities such as Virginia and Indiana has been attributed to aquaculture and, generally, the species was found to benefit from eutrophic environments (Reid 2007). Its ecological flexibility is further illustrated by the broad range of physical habitats in which it occurs, and that spans the range from large lakes to small, weedy ponds (Segers et al. 1995). In the Philippines, Tuyor and Baay (2001) noted the occurrence of A. dorsalis in Lakes Laguna de Bay, Mainit and Sebu, but it was with certainty recorded in the first lake since 1991 (M. Directo, unpublished report to International Zooplankton course, Gent University, 1993). Residents of these three lakes practice aquaculture using fish pens or cages, with African Oreochromis niloticus (hereafter called tilapia) as the main species cultured. The utilization of Philippine lakes for aquaculture has led to an increase in total fish production, provided a new and affordable food for the growing Filipino population and created a steady source of income for many lakeshore residents. However, its under-regulated proliferation and the lack of comprehensive management took its toll, leading to an eutrophication of previously shallow but pristine lakes (Tamayo-Zafaralla et al. 2002; Zafaralla 1992) and a loss of biodiversity. This paper reports the occurrence of Arctodiaptomus dorsalis (Fig. 1) in Philippine lakes during a survey originally aimed at updating their diversity of calanoid copepods, discusses its possible effects on the native zooplankton, and predicts an expansion of the invader to continental Asian regions beyond the Philippines in the near future.
Methods The Philippines is an archipelago of 7,107 islands where recent studies have listed around 70 lakes
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(Guerrero III 2001). Our study sites were selected based on location (lakes found on large, inhabited islands were prioritized), accessibility (presence of nearby roads and other means of transport), and utilization (open water fisheries, aquaculture, and tourism). Security issues were also considered in lake selection. Several transects perpendicular to the shore were established, the number of which depended on lake size. Zooplankton was collected using 100, 80 and 50 lm mesh plankton nets towed vertically in different sites along transects which covered both the littoral and limnetic zones. Samples collected from the same area were integrated and fixed in 5 % formalin. A total of 27 lakes were surveyed between 2006 and 2011 (Fig. 2). Generally, the lakes included conservation and research priority areas for inland waters (Guerrero III 2001; Ong et al. 2002) (Table 1). Our expectation was to find a substantial number of species or higher taxa, new to the Philippines or to science. Samples were split for quantitative and qualitative analysis. Calanoids were sorted and identified to species level in the laboratory using a WILD stereoscopic microscope. Identifications were done using an Olympus compound microscope and taxonomic keys such as Shen and Tai (1979), Dussart and Defaye (2001), and Ranga Reddy (1991). For Arctodiaptomus dorsalis specifically, a comparison of Philippine specimens was done with the original description by Marsh (1907). Abundance of A. dorsalis was compared with other copepod and cladoceran taxa found in the samples after making replicate counts in a Sedgewick Rafter counting chamber in an Olympus compound microscope.
Results Arctodiaptomus dorsalis, of which the salient morphological characters are illustrated in Fig. 1, was present in 18 out of the 27 lakes. These lakes were mostly located in the southern part of Luzon Island. Mindanao, the second largest island in the archipelago also had two lakes with A. dorsalis. Further analysis revealed that there were only three lakes that contained one or more other calanoid species. Two of these lakes are located in Luzon. Lake Paoay contains the endemic Filipinodiaptomus insulanus as well as Monglodiaptomus birulai. Lake Taal has Pseudodiaptomus brehmi together with A. dorsalis, and is the
Massive invasion of A. dorsalis in Philippine lakes
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Fig. 1 Arctodiaptomus dorsalis a Female cephalothorax b Male habitus c Female urosome d Female P5 with endopod nearly as long as exopodite 1 e Male P5with lateral spine inserted proximal to the middle of the right of exopodite 2 with
the spine longer than exopodite 2 f Female P4 with single medial dorsal process g Male right antennule terminal segment h Male right antennule showing geniculation. Scale bars a and b— 0.2 mm; c–h—0.05 mm
only lake in which the latter co-occurred with another calanoid. Lake Danao on Leyte Island finally, yielded ‘‘Diaptomus’’ vexillifer Brehm 1933, a poorly
described species of unsettled generic status that has not been found outside that lake. Seven lakes did not have calanoid copepods. There were variations in the
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Fig. 2 Map of the Philippine archipelago showing the locations of the different lakes included in this study
abundance and contribution of calanoid copepods to the total crustacean zooplankton population whenever they were present (Fig. 3). A. dorsalis dominated the calanoid copepod community of Lake Taal, where it co-existed with P. brehmi. Except for Lakes Danao (Leyte) and Mohikap where D. vexillifer and A. dorsalis each comprised more than 50 % of the crustacean zooplankton, cladocerans and cyclopoid copepods were the dominant taxa compared to calanoid copepods.
Discussion Although Arctodiaptomus dorsalis has been reported in Philippine lakes such as Lakes Laguna de Bay, Mainit and Sebu as early as 1991 (Tuyor and Baay 2001), and it therefore must have existed there since the mid or early 1980s, nobody noticed that it had gone
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beyond its usual geographic range and affected the native calanoid fauna of the Philippines. Our results show that this invasion now hampers the possibility of finding previously unrecorded endemic calanoid species in the Philippines. In neighboring countries such as Thailand and Vietnam, the discovery of new calanoid species has more than tripled the local species richness since the 1970s (Sanoamuang and Teeramaethee 2006; Defaye 2002). The absence of previously recorded calanoid species from most of our collections indicates that A. dorsalis may have displaced these and perhaps many others from their habitats before studies could assess their diversity. Even the common Tropodiaptomus spp. listed in Lai et al. (1979), Mamaril Sr. (1986, 2001) and Mamaril Sr. and Fernando (1978) could not be recovered from their previous lakes. The endemic Filipinodiaptomus insulanus was only observed in Lake Paoay, whereas before it was found in Laguna de Bay (Mamaril Sr.
Massive invasion of A. dorsalis in Philippine lakes
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Table 1 Physical characteristics and a comparison between the calanoid species collected from 2006 to 2011 with those found in primary literature for the different Philippine lakes included in this study Island
Lake
Coordinates (N, E)
Depth (m)
Altitude (masl)
Area (ha)
Calanoid spp. 2006–2011
Calanoid spp. in primary literature
Luzon
Paoay
18°70 16.247400 , 120°320 25.72800
3–5
19
387.5
F. insulanus
F. insulanus
M. birulai
T. australis
Laguna de Bay*
14°230 7.681200 , 121°170 4.969800
2.8
11.5
90000
A. dorsalis
F. insulanus P. nostradamus T. gigantoviger A. dorsalis
Caliraya
14°180 11.317800 , 121°310 46.311600
DD
289
719.2
A. dorsalis
Lumot-Mahipon*
14°150 20.93400 , 121°320 49.088400
DD
293
317.7
A. dorsalis
NPL
Tadlak*
14°100 57.352800 , 121°120 23.324400
58
-2
25.1
A. dorsalis
NPL
Sampalok*
18°70 16.247400 , 120°320 25.72800
25
134
96.6
A. dorsalis
NPL
Bunot*
14°40 59.998200 , 121°200 59.999400
23
153
30.5
A. dorsalis
NPL
Calibato*
14°60 15.001200 , 121°220 37.999200
156
184
43
A. dorsalis
NPL
Mohikap*
14°70 22.5300 , 121°200 2.431800
30(max)
99
22.9
A. dorsalis
NPL
Palakpakin*
14°60 40.279800 , 121°200 19.837800
8
136
47.9
A. dorsalis
NPL
Pandin*
14°70 0.000600 , 121°220 0.001200
62
225
20.9
A. dorsalis
NPL
Yambo*
14°110 66.66700 , 121°360 66.66700
40(max)
225
30.5
A. dorsalis
NPL
Taal*
13°560 54.99900 , 121°00 26.999400
90
2.5
24356.4
A. dorsalis
T. vicinus
P. brehmi
P. brehmi
Buhi*
13°270 24.998400 , 123°300 51.001200
7
88
1704
A. dorsalis
NPL
T. vicinus (malaicus var. prasinus)
Bato*
13°190 54.998400 , 123°210 32.000400
4.5
10
10500.9
A. dorsalis
NPL
Baao*
13°270 49.513800 , 123°180 57.538800
2.5
4
1633.6
A. dorsalis
NPL
Bulusan
12°450 41.68800 , 124°50 29.78100
DD
360
17.7
None
NPL
Mindoro
Naujan*
13°100 10.999200 , 121°200 54.999600
19
20
14568
A. dorsalis
P. brehmi
Negros
Balinsasayaw
9°210 59.104200 , 123°90 18.903600
134(max)
874
6973.9
None
NPL
Danao
9°210 2.00100 , 123°100 59.998800
DD
898
6973.9
None
NPL
Kabalin-an
9°210 59.104200 , 123°90 18.903600
DD
719
6973.9
None
NPL
Cebu
Danao
10°400 35.27400 , 124°200 34.29900
0.91–54.9
5
649
None
NPL
Leyte
Danao
10°520 5.00100 , 124°510 20.998800
DD
635
140
D. vexillifer
F. insulanus D. vexillifer
Mindanao
Sebu*
6°130 27.000600 , 124°420 11.998800
5
696
354
A. dorsalis
A. dorsalis
Lahit
6°150 6.997800 , 124°420 5400
DD
666
17.2
None
None
Siloton*
6°130 33.189600 , 124°430 51.65700
DD
664
64.8
A. dorsalis
None
Mainit
9°260 2.000400 , 125°310 59.998200
128
42
17060
None
A. dorsalis
NPL no primary literature, DD data deficient, * lakes with aquaculture
2001), and perhaps Lake Danao (Leyte Island) (Tuyor and Baay 2001). Pseudodiaptomus brehmi, recorded for Lake Taal (Papa and Zafaralla 2011) was not found in its type locality of Lake Naujan (Mindoro Island) where we found high densities of A. dorsalis instead. We did, however, find Mongolodiaptomus birulai in Lake Paoay. This is a new record for this lake and, in fact, the only new record we could make. The first and only recorded occurrence of M. birulai was in Baguio
City (Lai et al. 1979), less than 200 km south of Lake Paoay. Table 1 includes calanoid species found in primary literature (i.e. peer-reviewed publications) for comparison with the present findings. It convincingly shows that lakes previously occupied by native species had now been taken over by A. dorsalis. However, it also illustrates how little valid information exists on the zooplankton diversity of Philippine lakes. How many of these lakes may have contained significantly
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Fig. 3 Relative abundances of crustacean zooplankton present in the sampled lakes. Taxon name is followed by #, $, C or N to denote male, female, copepodite or nauplii, respectively
higher calanoid diversity before the invasion can only be guessed at. Reid (2007) noted the ease with which A. dorsalis established itself in new habitats in the Americas. Our results, show that A. dorsalis is also capable of a transcontinental invasion. Tuyor and Baay (2001) suggested A. dorsalis to have been introduced first to Laguna de Bay with drinking water reserves from ships and barges that have been discharged upon their arrival in the Philippines. This is a possible, but perhaps not the most plausible scenario. Maritime trade routes between Central America (e.g. Mexico) and the Philippines have existed since the 1500s. The large number of ships currently traversing this route has also increased the probability of planktonic species being introduced through this manner. The first recorded occurrence of A. dorsalis in the Philippines was in Laguna de Bay, which is connected to the port area of Manila Bay via the Pasig River. We also found that A. dorsalis is the only calanoid species in the Pasig River. However, the initial introduction of tilapia and other species like milkfish was also originally in Laguna de Bay where the aquaculture of tilapia began in 1974 and a co-introduction with these initial inocula may have occurred. Most fry and fingerlings used to stock aquaculture sites elsewhere in the Philippines also initially came from Laguna de Bay. Zooplankton may easily have been co-dispersed to other areas and islands where nearly all major lakes
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currently have cultures of tilapia. This is why lakes near Laguna de Bay (located in southern Luzon and Mindoro Is.) all have A. dorsalis. A factor which almost certainly contributed to the success of Arctodiaptomus, once it colonized lake Laguna de Bay, is its preference for eutrophic environments, and its capability for living in even the smallest ponds (Segers et al. 1995). Woltereck et al. (1941) described Philippine lakes as by nature eutrophic, but with clear water and well developed littoral vegetation zones. The increased trophic levels of these lakes after several years with aquaculture thus provided a favorable environment for the establishment of A. dorsalis. The spread of A. dorsalis to previously unoccupied areas in North, Central and South America was also related to aquaculture and eutrophication (Reid 2007). All these conditions were likewise present in the Philippine setting after the onset of large-scale tilapia culturing. The disappearance of pre-existing faunas, calanoids and others, may therefore have little to do with a competitive superiority of the Arctodiaptomus, but simply reflect a deteriorated environment, vacated by its previous, autochthonous fauna. However, competitive exclusion by an introduced planktonic species has been suggested in a study of the invasion of the copepod Eudiaptomus gracilis in Lake Candia (Italy). The discovery of E. gracilis in the lake was followed by the disappearance of the native E. padanus within only
Massive invasion of A. dorsalis in Philippine lakes
7 months, which was largely attributed to interspecific differences in reproductive rates and juvenile mortality (Riccardi and Giussani 2007). Finally, now that it has established itself so widely in the Philippines, A. dorsalis may use this archipelago as a bridgehead from which to invade mainland Asia, similar to the spread of A. dorsalis into previously uninvaded areas of the United States (Reid 2007; Cole 1961). Significant trade of aquaculture products exist between Asian countries where similar aquaculture practices also exist. Tilapia culturing is widespread in Thailand, Indochina, and south China, and so the environmental conditions there are equally conducive to a successful invasion by Arctodiaptomus, and perhaps to a disappearance or, at least, significant impoverishment of the rich local calanoid faunas. Acknowledgments We thank Jonathan Carlo Briones and Vhon Oliver Garcia for technical assistance. This research was funded by the Research Center for the Natural and Applied Sciences—University of Santo Tomas and the Institute of Hydrobiology—Jinan University. Additional funding was obtained from the Philippine Council for Aquatic and Marine Research and Development for the sample collection in the Seven Lakes of San Pablo, Laguna. Support from the grant for leading talent scientists of Guandong Province to Dr. Henri Dumont is likewise greatly appreciated.
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