2. INTRODUCTION
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If one follows the food web from man through fishes one may eventually reach the plankton of fresh- and brackish waters. Of the plankton organisms the zooplanktons are important for many fishes, including some of the species that are cultivated in ponds, pens and cages all over the Philippines (Aquino, 1982, Aquino et Nielsen, 1983, Fernando, 2002a, Hartmut, 2003, Nielsen, 1983, SOGREAH-Report, 1974, Papa, 2008a) - just take a view over Laguna de Bay and bee convinced

Zooplankton in the food chain.

Zooplankton constitutes the main food of most fish species when these are at their young, post-larval stage. Insects and other organisms from the littoral zone supplement the zooplankton. Some fishes like the herbivorous cichlids switch from being zooplanktivory to plant diet at a very early age (Fernando, 2002a). . The invasive Mosquito fish, Gambusia affinis, is widespread and common in canals, creeks, swamps, ponds and shallow areas of lakes. It feeds on zooplanktons, small insects and detritus (Joshi, 2006).  One of the major reasons why larger fish abandon this food source is that it becomes too small relative to their body size and is too dispersed in the water to be profitable. Practically the only way for larger fish to obtain sufficient quantities is by filter feeding (e.g. bighead carp). Nevertheless, the larger plankters are normally scarce in or absent from the diets of phytoplanktivorous fish such as milkfish and tilapia. These fish move to slowly through the water when filtering than zooplanktivorous fish do, allowing the larger plankton to escape (Richter, 2001).

Sustainable fisheries development thus partly depends on the availability of adequate zooplankton as principal food items of early life history stages of economically important fish species as well as of the adults of some species (Mamaril, 2001a). The cultured bighead carp, Hypophthalmichthys nobilis (Richardson, 1845) feed on zooplankton mechanical filtering of the water through the gillrakers with an interrraker distance of 60-100 µm, it is able to select especially copepodits from the water in Laguna de Bay, shown by Petersen (1981e) and Santiago (2004). The catadromous milkfish Chanos chanos (Forsskål, 1775), that breed in the sea, feed on the abundant zooplankton there and then enter freshwater to take advantage directly or indirectly of the year round food supply and the high primary production (Gross et al. in Fernando, 2002a). 

 

In Lake Taal in Batangas the clupeid freshwater sardine Sardinella tawilis (HERRE 1927) exhibit surface filter feeding with particulate filtering capacity. Periodically it has a planktivorous diet of zooplankton such as ostracods, cladocerans (Bosmina sp., Moina sp., Diaphanosoma sp., Ceriodaphnia sp. and Simocephalus sp.) copepods (Cyclopoids and Calanoids), and rotifers (Brachionus spp.). In a more recent study Bosmina sp. had the highest occurrence items in the stomachs of tawilis purchased from the market.

“Tawilis” sold at the Binangonan Market. Photo Flemming Petersen, 2013

Planktivorous fishes may have a direct effect on these large zooplankton groups (Papa, 2008a,  Papa et al. 2011b) and the cladocerans even almost eliminated by fish (Fernando, 2002a). The freshwater sardine is thus an important example of the importance of zooplankton as a trophic link between phytoplankton and fishes. Visually guided planktivorous fish can thus exert strong predation pressure, which zooplankton avoid by migrating downwards to a depth where low irradiance prevents detection (Papa, 2008a, Carlos 1982.).

 

An example of a food web in a lake. After Petersen 1981e
 

In at study of vertical distribution during daylight, copepods with eggs where thus primarily found near the bottom of the shallow, but turbid lake Laguna de Bay, invisible for the zooplanktivorous fishes (Petersen, 1981e).  The high predation from zooplanktivorous fishes and fish-larvae, the competition from phytoplanktivorous fishes are reducing the diversity of zooplankton of tropical freshwater (compared with temperate waters), the size of zooplankton animals and the total biomass. As a consequence the zooplankton of the tropical lakes does not control phytoplankton biomass (Fernando, 2002a) as seen in many temperate lakes. In the Danish Lake Esrom, Daphnia sp., which is rare in the tropical freshwaters, controlled the phytoplankton-biomass in the warm summer period (Petersen, 1983).

Other factors can influence the composition of zooplankton in a lake. Other factors can influence the composition of zooplankton in a lake. In general the zooplankton community structure, population dynamics, and production are strongly influenced by lake productivity, and zooplankton is of this reason a useful indicator of eutrophication of lakes. (Papa et al. 2011b). Difference in diversity and distribution of the zooplankton within a lake may be influenced by anthropogenic eutrophication, like the 10.000 fish cages in the Northern basin of Taal lake (Gulati 2009). Further weather conditions can have an impact on the zooplankton distribution, this is especially the case for tropical zooplanktons, since their relatively smaller size (Papa et al. 2011b).  Studies have shown that physico-chemical parameters can be correlated to zooplankton abundance, species number and diversity. The study by the Papa and his group  (Lazo, 2009) has revealed a moderate to high correlation to rotifers population in Pasig River to the dissolved oxygen in the river.

 

 

 

The most dominate zooplankton in Laguna de Bay before 1980 was cladocerans followed by copepods and then rotifers. This was about the time when the total fish pen area was at its maximum (ca. 30,000 ha). Declining zooplankton biomass has been marked between 1982 and 1983. The expanding fish pen industry, the operation of the Hydraulic Control Structure (HCS) across the Napindan channel had become operational in regulating the flow of water in and out of the lake via the Pasig River, and lake pollution had separate adverse effects on the zooplankton. Shifts in the structural features of zooplankton communities became apparent seven year after the operation of the HCS, or 4 to 5 yr after the demolition of fish pens. Copepods became dominant over the cladocerans and rotifers in that order (Nielsen, 1983, Tamayo-Zafaralla et al., 2002).

There is no doubt that zooplankton enters into the diet of different species and stages of fish, but the role of Cladocera, Copepoda and Rotifera in the food of these fishes is only recently being investigated. (Fernando, 2002a, Papa 2008a, Petersen, 1981e, Richter, H. 2001, Santiago et al., 2004). It is the hope of the author that this key will help in intensifying the research about this problem, finding the per capita ration of zooplankton (and other animals) necessary for raising a fish to recruitment stage in fishery or to fingerling stage for fish culture, as on of the most important ways of getting more animal protein at less cost.
 

Zooplankton studies of  secondary production has been done in Laguna de Bay (Petersen 1981e, Nielsen 1983). These studies were a part of ecological investigations including measurement of primary production and important physical and chemical parameters and gave a further insight in the factors determining the fish production, modifying the conclusions from the SOGREAH-report (1974).  As pointed out in Nielsen et al. (1981) and Nielsen (1981), the limiting factors for fish production varied between inorganic turbidity (November-May), self shading (May-August) and phosphorous (not nitrogen as stated in the SOGREA-report (1974)) in September to October. The period of self shading of phytoplankton, was the period of high primary production, followed by a period of high biomass and secondary production of zooplankton. And a documented maximum in growth rate of Tilapia in fish pens from May  to August. The total annual primary production was found to be 5 g*L^-1*yr^-1 (wet weight) giving raise to a secondary production of zooplankton of 0.38 g*L^-1*yr^-1 (Divided by Rotifers: 17 %, Cladocera: 19 % and Copepods: 64 %). In order to make decisions about sustainable aquaculture management in the Philippine Freshwaters, research projects like these, has to be considered in the future.

 

Example of productivity of plankton in a lake. Here Laguna de Bay 1980. (after Petersen 1981)

 

Systematic studies.

Since the earliest report of a Philippine rotifer zooplankton species (Semper, 1872, 1875), the first publications about systematics of about Philippine freshwater zooplankton species are mainly written in the German language (Brehm 1933a, 1937, 1938, Kiefer 1928b, 1930a, 1939a, 1939b, Woltereck 1941a) and a few in English (Marsh 1932, Wright 1928a, 1928c, 1937). Woltereck's paper (1941a) is very extensive, including zooplankton as well as records of phytoplankton, molluscs, some macro crustaceans, and fishes from major lakes in the Philippines, together with Hydrobiological notes. Ueno (1966) included further 6 species to the list from his collections in Luzon.

The first comprehensive papers are the studies by Mamaril and Fernando (1978a,b, 1986a) who noted that there are around 125 species of freshwater zooplankton belonging to Rotifera, Cladocera and Copepoda. Of the total, 61 species belong to Rotifera, 49 to Cladocera and 15 to Copepoda. Mamaril 's papers mainly describe species collected from the shorelines of the sampling localities. In this way of sampling, primarily species found in ponds and the littoral zone of lakes have been recorded and some pelagical zooplankton species was not included.

Laguna de Bay, Fish pens and Manila Skyline, 2013

 

Lai, Mamaril and Fernando (1979a) had revised the freshwater calanoid copepods of the Philippines and created a new genus (Filipinodiaptomus) for an endemic species of the Philippines. My own studies revealed a few more records for the Philippines through a one-year ecological study of Laguna de Bay, mainly (Petersen 1981e, Petersen and Carlos 1984a).
Korovchinsky (1913) review the research on Cladocera exploration of taxon richness in the Philippines in the following matter: “A more extensive, though rather routine, investigation was made on the Cladocera of the Philippines, with 49 species recorded by Mamaril and Fernando (1978).This survey was the last for these islands (for cladocerans). The species list published later (Mamaril, 2001), fully repeated the list from the previous publication. Other studies concerned only individual water bodies (Papa et al., 2011, 2012).” The paper by Pascual et al. (1914) implies that research on Cladocera is still going strong.
The planktonic cyclopoid copepods of the Philippines has recently been studied and revised by Papa and Hołyńska (2013). A new species was found in Lake Siliton (Mindanao) and named Mesocyclops augusti, after the Philippine nestor of zooplankton studies: Augustus Mamaril.

Recently the Rotifers have been further studied (Tuyor and Segers, 1999). In a study by Berbano et al (2001c) 6 species of Rotifera, 8 species of cladocerans and 6 species of copepods were found in Lake Taal where the Keratella procurva, Diaphanosoma sarsi and Eucyclops "serrulatus" were the most abundant rotifer, cladoceran and copepod, respectively. The literature about Taal Lake has just been reviewed by Papa and Mamaril (2011a) and species composition updated by Papa et al. (2012b). Further the composition, abundance and distribution in space and in time of the rotifers of Pasig River has been investigated by Papa and his team (Lazo et al, 2009a). Factors as dissolved oxygen, temperature and salinity affected the abundance of the species, among which pollution tolerant and indicator species from Brachionus (e.g. B. caudatus), Keratella (e.g. K. tropica) and Filinia were among the most common rotifers. The Philippine species of Diaphanosoma are investigated and revised by Korovchinsky (1986, 1991, 1998a, 2000a+b)). The mainly marine Calanoid copepods of the genus Pseudodiaptomus was studied by Walter (1986b) and Walter et al (2006).
Very recently samples of cladocerans collected from 86 freshwater ecosystems in 2006 to 2013 were investigated with modern anatomical techniques revealed of 16 species. Bosminids were mainly collected from the islands of Luzon and Mindanao, rarely in the Visayans, while Sididae and Chydoridae were distributed throughout the archipelago (Pascual et al. 2014).

 

 

Fernando, (1979) writes about the characteristics of tropical zooplankton: “A contrast between temperate and tropical Cladocera, Copepoda and Rotifera zooplankton fauna shows a markedly different size composition and species diversity. There are fewer species, and these are generally smaller in the tropics than in either the North or South Temperate Zones. Larger species of the genera Daphnia and Simocephalus are relatively rare [or absent] in the tropics, while members of Eurycercus and Saycia are absent. The genera Diaphanosoma and Moina substitute these species in the limnetic niche in the tropic waters of the Philippine like Taal Lake (Papa et al., 2012b). Members of the families Holopedidae, Leptodoridae and Polyphemidae increase in abundance toward the temperate regions. Two small cyclopoid copepods are common in tropical zooplankton, while many of the common larger species of other regions are absent or very rare. The chief  rotifer components are Keratella tropica and species of Brachionus. Species of non-indigenous zooplankton like Brachionus havanaensis and Arctodiaptomus dorsalis have recently been introduced to the Philippine lakes. One factor favoring this introduction of invasive species is the introduction of aquacultures as seen in Laguna de Bay and Lake Taal (Papa et al., 2012b) who states: “As the under-regulated aquaculture practices and the introduction of alien [fish-] species continue in many lakes in the archipelago, more alterations to the native limnetic fauna may occur”.
Papa et al. discovered an invasion by the Neotropical Arctodiaptomus dorsalis in 18 out of 27 lakes in the archipelago. Further they only found four of the 12 previously recorded native and endemic calanoids in the lakes. This may indicate a displacement by A. dorsalis eventually boosted by a general deterioration of water quality of the lakes.

 

The key

The aim of this work is to give the researcher of the Philippines a key is to overcome one of the main constraints in doing ecological-aquaculture studies of zooplankton in the Philippine freshwaters - the key literature for determination of species. [Use of the key outside the Philippines shouldn’t be done isolated from keys for the local areas  (e.g. Jose & Sanalkumar (2012). A good supplement would be Fernando (2002b)]

The key will hopefully be useful in zooplankton studies, which might be planned in ecological and limnological studies in connection with aquaculture. Although primarily a systematic paper, rather it is intended as a handbook of the freshwater zooplankton ecologist, and is though included some ecological notes. For further reading se Fernando (2002a).
 

The key include information from the published literature to which I have access to (see list of literature) and personal observations about the zooplankton done during own ecological studies in the Philippines, primarily at SEAFDEC BRS in 1979-81 sponsored by the Danish Foreign Ministry, DANIDA-department.

The list of species of zooplankton in the Philippines is still expanded with new records for the Philippines. Further research will, without doubt, recover more species to be added to the list. This is said to warn against not being open-minded for the possibility of finding still unknown species of zooplankton for the Philippines. In other words do not try to fit not described species into the key. Some benthos species may also occasionally be sampled. See Fernando, 2002a for worldwide keys of tropical zooplankton.

Rey Donne S. Papa studying zooplankton in microscope.

 

Sampling of zooplankton.

Included in the key are more than 80 species of euzooplankton, holoplankton or true zooplankton adapted to live in the limnetic or pelagic zone (Pelagic zone refers to the free water mass in the sea and in lakes, while limnetic zone refers to lakes only) of the lakes and those littoral forms, which are often found among the euzooplankton as visitors or tychozooplankton.

The recent paper by Papa and Mamaril (2008c): Methods in Zooplankton Sampling, Ecology and Identification for General Biology Teachers included this paper; gives a review of the basic methods of sampling zooplankton quantitatively.

In ecological studies of zooplankton a Sedgwick-­Rafter counting chamber is a must, or better (and more expensive) settling chambers used with an inverted microscope. Only if very large species (e.g. Diaphanosoma) are studied, stereo lupe will be sufficient in counting and measurements (Petersen 1983).

In order to determine the species, the animals have to be studied under microscope. Rotifers should be studied alive. They can be kept alive in a refrigerator for considerable periods of time. Some species, however, can be determined when preserved in 5% formalin (those with stiff shell). The diagnosis of some species is based on the detailed structure of the trophi (jaws). To study the trophi the specimen is irrigated with a dilute sodium hypochlorite under a cover slip on a glass microscope slide. The other tissues are dissolved away and the trophi can be conveniently studied.

The cladocerans, which are transparent, can be studied without dissection, while the copepods have to be dissected to determine the species. The 5th leg from the adult copepod (male or female) is an important morphological character. The use of the biological reagent “Polyvinyl Lacto­phenol” coloured red with the biological stain Lignin Pink is often used for preparation of short time objects for determination.
Se Brandl (2002a) for more information about methodology.

 

Type collection.

At the University of Santo Thomas, Manila, Rey D. S. Papa at the Research Center for the Natural and Applied Sciences, has established a Zooplankton reference Collection from the Philippines. He and his students are in a process of collecting from lakes, rivers and other freshwater ecosystems and making systematic, and ecological, studies of the Philippine zooplankton, see UST (2013). The materials from these studies are assembled in a special laboratory for this purpose.

How to analyse the data.

After collection, counting etc. of the zooplankton, the data should be analysed statistically. Papa et al (2011a) gives example of both simple at more complicated methods of analysing the data. Here only two simple methods will be mentioned.

Q_B/T :
Sládeček (1983) found that the ratio between  the number of species presents of the genera Brachionus and Trichocerca (i.e. Brachionus: Trichocerca quotient, Q_B/T) should be considered as an index of trophic levels – since Brachionus species mainly are found in eutrophic waters, while Trichocerca species prefer oligotrophic waters.  The lake can thus be regarded as
 

                      oligotrophic when Q_B/T < 1,
                      mesotrophic when Q_B/T is between 1—2, and
                      eutrophic when Q_B/T > 2. [1]

Papa et al (2011a) found a Q_B/T of 7 in Taal Lake in 2008, clearly indicating the lake as eutrophic.

Q_{Cal/(Cla+Cyc)}:

Gannon & Stemberger (1978) found that cladocerans and cyclopoid copepods are more abundant (in numbers) in eutrophic lakes, while calanoid copepods dominate oligotrophic lakes.
They found, from studies in the Great Lakes (North America), that a density of calanoid copepods comprises over 50% of the crustacean zooplankton or a ratio calanoids/ (cyclopoids + cladocerans) greater than 1 (Q_{Cal/(Cla+Cyc)} > 1) could be correlated with oligotrophy.  “But caution must be exercised in establishing one-to-one causal relationships between zooplankton composition and trophic conditions since other factors, especially toxic pollutants and size-selective predation, may exert considerable influence on changes in the community composition” (Gannon & Stemberger(1978). 

Papa et al (2011a) found a Q_{Cal/(Cla+Cyc)} <  0.5 in Taal lake, thus computed to quantify a zooplankton community characteristic for the eutrophic status found of the lake.

 

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[1] If no species of Trichocerca is found then set the denominator to 1

How to use the key.

The presented key is ordinary "two-choose" (dichotomous) - rarely three-choose - key and is arranged, as much as possible, systematically according to the literature. The main morphological and some ecological information are included in the key. It has to be said that most investigations of the ecology of zooplankton has taken place outside the tropical region, and can only be applied tentatively to the Philippine region. Exception is first of all the Lewis’ (1979) opus on Lake Lanao zooplankton, a comprehensive analysis of the zooplankton community of a tropical lake. It is advised as inspiration in the planning of any ecological zooplankton study. Petersen (1981e) estimated secondary productions of all major zooplanktons through one year in Laguna de Bay. Papa et al. (2007a, 2008c) studied in a five-month monitoring of Paoay Lake the Impact of blooms of the colonial green algae Botryococcus braunii on the Zooplankton of Paoay Lake founding that both the composition and the abundance of zooplankton in Paoay Lake were negatively affected by the occurrence of B. braunii.  

 

The localities of occurrence are primarily only mentioned for major lakes of the 59-70 Philippine lakes (Papa and Mamaril, 2011a). A figure of the location of some major Philippine freshwater lakes is modified from (1984a):

More information can be found in the literature (Woltereck 1941a, Mamaril and Fernando 1978b). The illustrations, following the key, are from two sources: Firstly by copying from the lite­rature by simple tracing technique (Flössner 1972, Kiefer 1978, Mamaril 1978a, Pontin 1978c, Ruttner-Kolisko 1972 (R-K)) and secondly from the original drawings by the author (1980, marked FP₈₀). The black bars in the illustrations equal 100 microns or 100 μm or 0.1 mm if no other measure is noted. Most of the original drawings are copied in the same scale in order to give the "beginner" in zooplankton studies a good chance to recognize the species and compare the dimensions relatively to the other species found in the samples. In some figures preserved specimens are included to show how they appear in fixed condition (e.g. 76a) and some are shown at different angles as might be observed in the counting chambers. Finally some photos are added to the key to give a more visual impression of the animal as seen in the microscope. These photos are all original photos. The numbers in the key (la, lb, 2a, 2b, etc.) correspond to the numbers in the illustrations. The key and the illustrations, therefore, can be crosschecked together. The literature quoted in the key (after the species name) is given only as year of publication. To find the the reference it is necessary to find the author name in the chronological list of literature, and there upon enter the alphabetical list of literature. The index gives key and illustration numbers for all species and groups. It has to be noted that information about a species also can be found in the key for the genera. The Internet can often give further information about the species – use the scientific name as key words for the search.
                       

Acknowledgements

The Binangonan Freshwater Research Station (SEAFDEC) at Tapao Point, Binangonan, Rizal, has given me a good opportunity to study the zooplankton populations in Laguna de Bay and other lakes (se 1984a) and made me realize the importance of zooplankton studies in aquaculture research. Thanks to Dr. Santiago, Jr. (Former chief of SEAFDEC Aquaculture Department) for full-hearted support and to Mr. Andy Santiago (M.S.) for organization of the ecological/limnological team­work. A special thank to Mr. Manuel Carlos for being a patient and inspiring counterpart. Mr. H. Segers (Belgium) for personal correspondence about the Philippine rotifers. Further thanks to following persons being involved in different ways of the publishing of the key: late Dr. J. B. Pantastico (SEAFDEC), Director Roger S. V. Pullin (ICLARM), Rey Donne S. Papa (University of Santo Tomas), Hanne Kamstrup, Mr. B . H. Nielsen (Denmark), Ole P. Udvang (Norway). This edition has not been, if not for the interest, discussions and comments from Rey Donne S. Papa (MS), a leading researcher in Philippine zooplankton, with a wide international network being mentor for a new generation af zooplankton researchers. Finally a very special thanks to Professor A. Mamaril   (University of the Philippines) for reviewing the manuscript of the 1^st edition of the key and for giving many good and professional advices and suggestions. This work would not be without his great expertise on what he calls "the little beasts" of the Philippine Lakes. They are lovely.

 

 

Augustus Mamaril, Sr.	Rey Donne S. Papa –2008	May 1979 - Philippines

 

Flemming Petersen

Denmark, 2014

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[1] Coordinates of BRS laboratories at SEAFDEC: 14^o 24' 44'' N, 121 ^o 12' 57'' E

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