Invertebrate drift in the Tambun stream in Danum Valley
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1 Invertebrate drift in the Tambun stream in Danum Valley Anita Bousa, Wildlife Conservation Society, Lao PDR Chiara De Cesare, University of Innsbruck, Austria Abstract The invertebrate drift is the main food source of stream fish, but do the fish eat just the aquatic animals or do they also eat the terrestrial animals that drop down into the water? The drift composition was measured and fish gut contents were examined in the Tambun stream (Danum Valley, Sabah, Borneo). The results show that invertebrate drift in the Tambun Stream accounted for 41 million potential food particles drifting down the Tambun Stream each 24 hours. The numbers of aquatic animals drifting were greatest at night. The reason may be that the animals are minimising risks of being eaten by fish, which are visual predators. Also, the fish guts content showed that the fish prefer terrestrial and aquatic animal to exuviae. The terrestrial animals drop accidentally into the water and flounder. They are not adapted to the water environment and are therefore more vulnerable to predation in water. The aquatic animals are adapted to living and surviving under these conditions through structural and behavioural adaptation. One of those adaptations could be the voluntary drift during the night, when they are not visible to fish. Such controlled drift allows redistribution with minimum risk. INTRODUCTION Water flow and the swimming fish are visible and easily recordable features of streams. But there are also less obvious movements of smaller cryptic animals in freshwater habitats. Animals are resuspended from the bottom and carried downstream. Are these movements accidental and driven just by the water flow or are they deliberate and adaptive and controlled by natural selection? Forest and freshwater ecosystems are deeply connected. A continuous exchange of energy and nutrients takes place between them. Forests may contribute organic detritus, leaves and twigs and even whole trees that decompose in the water and provide energy for the stream community. In turn, insects may emerge as adults from the stream and provide food for birds, bats, spiders and reptiles in the adjacent forest. There are longer connections also, for example among migratory fish, bears that eat them and then excrete nutrients to the forest floor that the fish have acquired in the ocean. Forest trees take up these nutrients, returning organic detritus to the rivers that ultimately contributes food for invertebrates and then the young salmon. Pristine tropical ecosystems are characterised by low free nutrients and high diversity because on the one hand high rainfall leaches nutrients readily from the system if there are no mechanisms within the forest to retain scarce nutrients and on the other a long history has led to differentiation of many Bousa&deCesare2011.doc 1 Tropical Biology Association
2 species that maintain such mechanisms. Tropical streams are often very low in nutrients and the aquatic invertebrate communities are sparser compared with temperate systems. There is thus more competition for nutrients and also high predation rates because long growth seasons allow reproduction of fish several times per year. All these factors may contribute to the generally low numbers of invertebrates found in many tropical streams (Vannoto (1980); in Fenoglio et al., 2002).. Like all predators fish play a very important role in freshwaters. Their feeding behaviour can control the prey-populations (e.g. aquatic stages of invertebrates like mayfly larvae). And they can transfer energy and nutrients to the forest if they are preyed on by terrestrial amphibians (e.g. lizards) or mammals (e.g. bears, humans). The food sources for the fish in a stream may come from both terrestrial and aquatic origins. They include invertebrates, plant material and other fish. There are also detritovore species fish like Lobocheilos bo (Popta, 1904). Food sources may differ in a stream and in a main stem river in both composition and amount; in a big river, for example, there will be more sediment than in a small one but less oxygen and less overhanging vegetation. Fish are visual feeders; hence they can only catch prey if they see it. Aquatic invertebrates have developed various adaptations to cope with the risks of displacement by the water currents that also make them incidentally less visible to the fish. They have a brownish camouflage colour and often flat body shape to cling closely on or under rocks. Their body shape and legs are streamlined and well adapted to the motion of the water. If they move they move quickly. However, sometimes they do become detached and suspended in the currents and are then said to be part of the drift. The drift is the downstream transport of aquatic organism in the river (Fenoglio et al., 2002). It may have a very important colonisation value for example in recovery after disturbance (Fenoglio et al., 2002). Also the gene flow in riverine species is linked to the drift (Chaput-Bardy et al., 2008). The drift of larvae is described as accidental in the literature; but less is known about the possibility of non-accidental drift for deliberate redistribution. In the drift, invertebrates are much more vulnerable to being eaten by fish. Drift at night, when the fish cannot see them, might seem thus to be less risky than drift during daylight. Bousa&deCesare2011.doc 2 Tropical Biology Association
3 Aims This study investigates the food sources for fish in an environment that has only a small invertebrate community, yet a visibly obvious fish population and to determine whether drift of aquatic animals is random or shows patterns that might be adaptive. It was to investigate the feeding preferences of the fish in the Tambun stream in the Danum Valley and the role of terrestrial animals that accidentally fall into the stream compared with truly aquatic food and to seek patterns in the timing of the aquatic animal drift that might avoid the risks of fish predation. METHODS The site of the study is the ca. 300 m long last stretch of the Tambun headstream before the confluence into the Sigama River next to the Danum Valley Field Centre (DVFC) in the Malaysian region of Sabah (Borneo). The Tambun stream is surrounded by primary forest on one side and confines with the DVFC trails and habitations on the other side. About 10 km 2 of forest were logged in the 1980s. The Tambun headstream has a conductivity of about 50 µscm -1 and no detectable nitrogen. There is a big overhang of vegetation all along the stream so that there is a great uptake from plant material and animals dropping from the forest into the water The drift experiment This experiment was conducted twice. The first run was conducted in the Tambun stream on 17 th October 2010 from 10:00 a.m. until 1:00 p.m. of the 18 th October. Four benthos nets with 20 cm x 24 cm openings and 42 cm bag depth of 0.25 mm mesh were set across the Tambun stream to catch aquatic animals drifting in the water and the terrestrial animals that drop into the stream (Figure 1). The four nets were sampled every three hours, over 28 hours. The number of invertebrates (size generally < 2 mm) in each sample were counted), classified into four groups (aquatic animals, aquatic animal exuviae, terrestrial animal and terrestrial animal exuviae) and preserved in ethanol. Exuviae were only counted for the first sample in the first Figure 1. One of the drift nets on run, but for all samples in the second. The second run was conducted the study site. on 21 October 2010 starting at 9:00 am. The same procedure was used but the number of replicates was reduced to three nets, left for 34 hours with samples taken every four hours. On 21 st October there was a storm rainfall at 3 p.m. which increased the stream flow greatly for several hours overnight. Therefore a correction of 1.3 (proportion between number of animals found before the storm and after) was attempt for dilution during flood. Bousa&deCesare2011.doc 3 Tropical Biology Association
4 The collected data were tested for significance with One way ANOVA test (Minitab 14) and by regression (Excel X for Mac, 2001). Food particles number To estimate the number of food particles drifting in the stream the discharge was first measured with the formula (equation 1). D = l *x*v (1) D discharge (m 3 sec -1 ) l width of the stream bed (m) x average of the depth measured every m along l (m) v velocity of the current (m sec -1 ) The numbers of animals and exuviae drifting in the stream per 24 hrs were calculated by multiplying D by the total number of animals and exuviae counted per unit volume Fish sampling in stream and river On the 17 th October 2010 twenty fish (Nematabramis everetti, Cyprinidae) (Figure 2) were caught by seine netting in the Tambun headstream. Five were dissected and the contents of their guts were counted using the categories used for stream drift. The remaining 13 were kept alive in a running water aquarium for observation of their feeding behaviour. The proportions of the animal and exuviae classes found in the guts and in the nets (drift experiment 2.1) were compared with the Ivlev Selectivity Index (Ivlev, 1961). Figure 2. Nematabramis everetti caught on the 17 th October 2010 in the Tambun stream. D=(r-p)/r+p-2rp (3) r, proportion in guts p, proportion in food available A value of -1 means complete discrimination, 0 no selection, and +1 maximum positive selection). Thirteen fishes (one Clarias teysmani (Clariidae); six Paracrosschilus sp; two Lobocheilus bo; one Lobocheilus sp; and two Epalzeorhynchus kalliurus (all Cyprinidae)) were caught in a gill net set overnight on the 18 th October 2010 at the confluence of the Tambun headstream with the Segama River. All had entered the net from the Segama River; none had entered from the Tambun stream. Bousa&deCesare2011.doc 4 Tropical Biology Association
5 Feeding experiment 13 Nematabramis everetti were kept in an aquarium for 3 days. During 48 hrs after they were caught, a variety of terrestrial invertebrates was dropped into the water and the reaction of the fish observed. RESULTS Drift composition About 41 million potential food particles drifted down the Tambun stream per day. About 25 million of this was animals (both terrestrial and aquatic), the remainder were exuviae of both aquatic and terrestrial invertebrate. The compositions of the drift for run 2 are shown in Figure 3. In the first run, aquatic animals dominated (64%) on the terrestrial animals (16%). Figure 3. Percentage of terrestrial animals, aquatic animals, terrestrial animals exuviae and aquatic animal exuviae in second run. Based on all samples from the run 2. The composition of the food particles changed with time. Figures 4 and 5 show two examples of composition of food particles found in the nets at different times. Stone- and mayflies were always present, but in the evening juvenile fish were also found. In the first run sixteen different categories were counted, and seventeen in the second run. Bousa&deCesare2011.doc 5 Tropical Biology Association
6 Psephenid beetles 0% trichoptera 6% water bettles 8% mite 1% water skater 1% snails 0% others 2% Uknown 0% mayfly 26% water penny larvae 1% caseless 0% fish 1% damselfly 0% fly 7% dragonfly 1% stonefly 46% Figure 4. Percentage of aquatic animals in run 1 on 18 October 2010 at 7:00 a.m. mite 1% Psephenid beetles 1% water bettles 7% trichoptera 3% fish 1% fly 2% water penny larvae 0% dragonfly 0% damselfly 0% caseless 0% water skater 0% stonefly 50% snails 0% others 1% Uknown 3% mayfly 31% Figure 5. Percentage of aquatic animals in run 1 on 17 October 2010 at 22:00. Drift experiment Animals Aquatic animals were more abundant than terrestrial animals in the drift, with one exception in each run (Figures 6 and 7), but terrestrial animals were not scarce. Bousa&deCesare2011.doc 6 Tropical Biology Association
7 The number of terrestrial animals in the drift was almost constant through the period, while the number of aquatic animals changed with the time, with greater numbers towards the end of the day and at night. In the first run most aquatic animals were collected at 4 and 7 p.m. (Figure 6), based on mean values for the four nets at each time. Figure 7 shows that during the second run of the experiment the number of animals was greater at 7 p.m. decreasing but still high at 9 p.m. The number of animals was low during the next day and increased again after sunset. Figure 6. Average number of terrestrial, aquatic and total animals counted per net per 3 hours since 10:00 a.m. in the first run. Figure 7. Average number of terrestrial, aquatic and total animals counted per net per 4 hours since 9:00 a.m. in the second run. Bousa&deCesare2011.doc 7 Tropical Biology Association
8 However, mean numbers may be misleading because variance between replicates was high. Regressions using separate replicate data were thus calculated. Polynomial regressions gave the best fit to the data. The regressions for aquatic and terrestrial animals in both runs are shown in Figures 8 to 14. The peak number of animals per net occurs in all regressions around 1 a.m. Figure 8. Regression for the aquatic animals in the first run. R is significant for at a < α < Figure 9. Regression for the terrestrial animals in the first run. R is not significant. Bousa&deCesare2011.doc 8 Tropical Biology Association
9 Figure 10. Regression for the aquatic animals in the second run. R is significant for α < Figure 11. Regression for the terrestrial animals in the second run. R is significant for α < Exuviae The number of exuviae was almost constant during the second run. Higher values were recorded in the beginning and in the end of the experiment (Figure 12). Bousa&deCesare2011.doc 9 Tropical Biology Association
10 Figure 12. Exuviae per net per 4 hrs during the second run. Figure 13. Regression for the aquatic exuviae in the second run. R is significant for α = 0.05 Bousa&deCesare2011.doc 10 Tropical Biology Association
11 Figure 14. Regression for the exuviae of terrestrial invertebrate in the second run. R is significant for α < Time graphs for classes with more than 25% Changes with time for the two most abundant (more than 25% in at least one replicate) classes of recorded animals (Figures 15 and 16) show that stonefly larvae were dominating in run 1 while mayfly larvae were dominating in run 2. The two classes followed the same pattern of distribution with time, with peak numbers in the latter part of the day and at night. Figure 15. Average of mayfly and stonefly larvae individuals counted per net every 3 hours since 10:00 a.m. in the first run. Bousa&deCesare2011.doc 11 Tropical Biology Association
12 Figure 16. Average of mayfly and stonefly larvae individuals counted per net every 4 hours since 09:00 a.m. in the second run. Fish gut contents Nematabramis everetti fed on both terrestrial and aquatic animals and also on their exuviae. Gutcontents of seven fish from the Tambun headstream are shown in Figure 17. The gut contents were compared with the composition of the potential food particles in run 2 of the drift experiment. The positive numbers in Table 1 show that the fish prefers terrestrial and aquatic animals to exuviae (both terrestrial and aquatic). Figure 17. Percentages of animals and exuviae both terrestrial and aquatic founded in the guts contents of Nematabramis everetti. Bousa&deCesare2011.doc 12 Tropical Biology Association
13 Table 1. Ivlev-Selectivity-Index for the categories of food particles present in the Tambun headstream and in the guts of the fish Food particles terrestrial animals 0.25 aquatic animals 0.38 exuvie of aquatic invertebrates exuvie of terrestrial invertebr. Ivlev-Selectivity Index Feeding experiments The thirteen Nematabramis everetti were successfully fed butterflies, spiders, ants, crickets, flies, cicadas and bugs. Only a millipede (poisonous) and a large beetle were refused. The first was not even touched, the second was chewed by three different fish and each time was rejected. Also the visual feeding behaviour of the fish could be observed. DISCUSSION The fish of the headstream Tambun are feeding on both aquatic and terrestrial animals and their exuviae. One possible reason is the low nutrient conditions in the stream. The conductivity is very low (about 50 µs cm -1 ) and nitrate is undetectable. The surrounding forest is near pristine and might be expected to be very efficient in retaining nutrients Supplies of aquatic organisms are thus low and subsidy from the forest necessary. The fish seem not to like exuviae but since there is not enough other food available they are eating them. The exuvie are made of chitin, which could be a not easily digestable nitrogen source. The terrestrial animals drop accidentally into the water and flounder. They are not adapted to the water environment and are therefore more vulnerable to predation in water. The aquatic animals are adapted to living and surviving under these conditions through structural and behavioural adaptation. One of those adaptations could be the voluntary drift during the night, when they are not visible to fish. Our results show this. The first run of the drift experiment was under ordinary conditions, the stream had a base flow. During the second run a storm rainfall occurred and caused a flash flow. This has on one site diluted the drift particles in more water. On the other site the violence of the flow can have caused the accidental movement of drift particles during the time of the flash flood. Bousa&deCesare2011.doc 13 Tropical Biology Association
14 Fish from the main Segama river were feeding on detritus, probably from the sediments and were likely to move into the Tambun for drift food supplies. The main river has a large rise and fall and this prevents development of biological communities on the sand and gravel banks at its edge. This river is also very turbid and fish may have difficulty in finding food. It is possible that at least at high water they might move into the Tambun, where food supplies, although sparse, may be richer than in the main stem. The fish are of larger species than Nematabramis, however, and may be excluded at low water levels in the Tambun. Low nutrient availability is also suggested by the low numbers of shredders in adjacent streams as shown by previous studies on leaf litter (Figure 18). Bags with litter were left for 2 weeks in the water another headstream in Danum Valley and showed no damage. The algae cover on stones wasn t exhaustively studied but there was inconsiderable macrophytic algae cover, which is also directly linked to the low nutrient conditions. Figure 18. Ecosystem-diagram by Prof Brian Moss Bousa&deCesare2011.doc 14 Tropical Biology Association
15 The explanation for the low free nutrients conditions for the study site is a combination of three processes: the fast nutrient uptake by the roots of the plants (and by the mycorrhizae on them), the interception of salt and nutrients by the worm (Johnson & Bosi, 2010) and the canopy litter trapping and recycling. Figure 18 shows how these processes which occur in the forest have a direct impact on the community composition of the freshwater and also the behaviour of fish and aquatic invertebrates. There are several factors which can affect the results of this kind of study. First are the unexpected. A large monitor lizard attracted by the fish in the gill net certainly removed some of them, but is unlikely to have biased the results. Heavy rainfall and a high flood increased the dilution of organism in the samples. Second are systematic but expected problems. Gut contents are at a stage in digestion, which makes them hard to recognise and ethical considerations demand that only limited numbers be sacrificed. Thirdly, there are human factors: for example in the first run of the drift experiment the role of the exuviae was underestimated and it was decided not to count them. They were counted in the second run, but the high flood made the results of this run more difficult to interpret. Nonetheless the work has provided strong indications of both the role of forest animals and of exuviae in the functioning of the ecosystem and of deliberate and probably adaptive drift among some of the stream animals. REFERENCES Chaput-Bardy, A. Lemaire, C., Picard, D. & Secondi, J. (2008) In-stream and overland dispersal across a river network influences gene flow in a freshwater insect, Calopteryx. Molecular Ecology 17: Vannoto (1980) in Fenoglio, S., Agosta, P..B.O., T. & Cucco, M. (2002) Field experiments on colonization and movements of stream invertebrates in an Apennine river (Visone, NW Italy). Hydrobiologia 474: Bousa&deCesare2011.doc 15 Tropical Biology Association
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