Young P. notatus. (20-79 mm SL) feed ... related Amazonian species, P. nattereri (Bellamy. 1968, Zbinden .... the observed activity patterns of young piranhas.
Environmental Biology of Fishes 29: 51-57, 1990. 0 1990 Kluwer Academic Publishers. Printed in the Netherlands
Feeding chronology of juvenile piranhas, Pygocentrus notutus, in the Venezuelan llanos Leo G. Nice Department of Zoology, Received 7.2.1989
University of Florida, Gainesville, FL 32611, U.S.A.
Accepted 1.8.1989
Key words; Fish diets, Fish feeding, Die1 feeding, Characidae, Serrasalminae, Serrasalmus,
South American fish, Tropical fish Synopsis During the 1988rainy season, I studied the 24 h feeding chronology of juvenile (40-68 mm standard length) piranhas, Pygocentrus notutus (Characidae: Serrasalminae) from a natural population inhabiting a small savanna stream in Apure State, Venezuela. Stomach contents analyses,supported by laboratory determinations of digestion rate, showed that these fish are primarily diurnal carnivores. Predatory activity on 4-5 August 1988 increased markedly after sunrise, peaked around 1100h, and essentially stopped after sunset. Means of stomach content weight-to-fish weight ratios among the periods sampled were significantly different. !3mall fish were the major prey at all hours (81% of total prey volume). Underlying factors responsible for the observed 24 h feeding patterns were not investigated, but avoidance of predation by adult piranhas, which were very active near sunset, may have been important.
Introductiam Diversity of piranha diets has received considerable study in recent years (Goulding 1980, Sazima 1984, Sazima & Andrade-Guimaraes 1987, Sazima & Zamprogno 1985, Machado-Allison & Garcia 1986, Northcote et al. 1987, Nice & Taphorn 1988, Winemiller 1989). Yet there is much to be learned about the feeding strategies of piranhas, and how these strategies relate to a particular environment. A number Iof field researchershave concluded that piranhas a.re predominately daytime predators (Lowe-McConnell 1964, Goulding 1980, Sazima & Zamprogno 198.5,Barthem 1987, Nice & Taphorn 1988, Winemiller 1989), but die1changesin feeding rate of these fish in the natural environment over a 24 h period has not been well documented. This study describes a 24 h feeding chronology
for juvenile Pygocentrus notutus (Characidae: Serrasalminae) in a natural population inhabiting a small savanna stream in Apure State, Venezuela. Pygocentrus notutus, the most abundant of the seven or more piranha speciesinhabiting the Orinoco River basin llanos of Venezuela, is a generalized predator at all sizes. Adults feed most heavily on fish (Nice & Taphorn 1988). Young P. notatus (20-79 mm SL) feed mostly on small fish and aquatic insects (Machado-Allison & Garcia 1986,Nice & Taphorn 1988). From aquarium studies of a closely related Amazonian species, P. nattereri (Bellamy 1968, Zbinden 1973), as well as previous field observations, I hypothesized that P. notutus would have a discontinuous feeding chronology, with two peaks of activity periods, one soon after sunrise and another just before sunset.
52 Study area The study site was Cafio Chiguichigui, a seasonal low-gradient, blackwater stream, in the ApureOrinoco River basin, Apure State, Venezuela (07”25’50”N, 69”35’30”W). Details of the general locality are presented in Nice & Taphorn (1985, 1988). The surrounding area is open flat savanna. Shoreline vegetation consisted primarily of grasses and forbs. The stream channel width varies from 10 to 23 m, and during the sampling period low areas adjacent to the stream were flooded. Maximum water depth was about 1.5 m. Water velocity ranged from zero in nearshore habitats to about lm set-’ immediately downstream of a dike culvert. A Secchi disc measurement of 1.1 m was taken at 1100h on 4 August 1988 under a partly cloudy sky. On 5 August 1988,0800-0830 h, water temperature was 29”C, pH 6.0, total dissolved solids Omg l-l, ammonia nitrogen less than 0.02 mg l-l, and nitrate less than l.Omg 1-l. Large floating mats of vegetation (Eichhornia crassipes and E. azurea) covered most of the nearshore areas. The major submergent plants, Ludwigia helminthorrhiza, Benjamania reflexa, and Pontederia subovata, covered about half of the stream bottom in places where strong current excluded floating plants. The major substrates were claypan and plant litter, with some mud. The region has a wet season, about May through November, and a December through April dry season. During the late dry season the stream slowly shrinks and usually dries completely.
Methods Digestion rate experiments
Digestion rate experiments, as per Darnell & Meierotto (1962), were conducted to characterize freshly ingested food items. A series of young Pygocentrus notatus (53-64mm SL) taken from the study area on 6 August 1988 were lightly anesthetized with Tricaine methanesulfonate (TMS) and transported to the laboratory, where individuals were placed in 4-8 1 tanks with fresh water (24”C, pH8.0, total dissolved solids 145 mg 1-l). After
starvation for 24 hours, each piranha was fed a single live characoid fish (25-32 mm SL). Pairs of piranhas were then killed in 10% formalin at hourly intervals (hours l-6) and the state of disintegration of the ‘standard food item’ was determined. After performing these digestion rate experiments, I was able to categorize food items as fresh (period I sensu Darnell & Meierotto 1962) or well digested but still in stomach (period II). Period I lasted about 3 hours. After 3 hours, most body scales (exposed to the stomach wall) were loose or digested away, and the hard lenses of the eyes were usually out of their orbits and floating freely. Period II prey were difficult or impossible to identify. Although insects were not used in digestion rate experiments, I defined period I insect prey as those having body plates and appendages still attached.
Feeding chronology
All fish were collected using cast nets (2m diameter, 20mm mesh size) and a small seine (5 x 2 m, 6 mm mesh). To determine feeding chronology, I made seven collections over a 25 h period from 0645 h on 4 August to 0730 h on 5 August during the rainy season. Each sampling period lasted approximately 1 h: 0645-0740; 1030-1130; 14301530; 1830-1930; 2230-2330; 0230-0330; 063& 0730. In the field, fish were preserved immediately in 10% formalin. Although six piranha species and a wide range of sizes were collected, analysis was restricted to juvenile P. notatus, because these provided the largest samples. Following transfer to 70% ethanol, each fish was measured, blotted dry on a paper towel, and weighed to the nearest 0.01 gram. Because piranhas have a well defined stomach, total stomach content weight was determined by first weighing the entire stomach, removing the stomach contents, and then subtracting the weight of the stomach wall. Stomach contents were examined using a dissecting microscope and the wet weight of any period I item was recorded. I examined the stomach contents of 123 piranhas and recorded frequency of occurrence, number, volume, and dominance
for each food item. Food categories used follow Nice & Taphorn (1988). The volume of a food item was determined by water displacement using graduated cylinders. Specimens dissected varied between 40-68 (x = 49) mm SL and 2.21-13.29 g; all are deposited in the Museo de Ciencias Naturales, UNELLEZ, Guanare, Venezuela. To adjust for fish size, stomach content weights were expressed as a percentage of total fish weight, and a mean was calculated for each sampling period. To statistically test observed differences in temporal feeding intensity, I followed the recommendation of Jenkins & Green (1977) and used a oneway analysis of variance (F test). The F ratio was derived using the 1987 statistical computer program STATGRAPHIX produced by Statistical Graphics Corporation. I used Sokal & Rohlf (1969) for all other statistical analyses.
food in the majority of stomachs throughout the 24 h period (Table 1)) recently ingested food made up only a small part of the total food volume of fishes collected between noon and the following sunrise. As expected, there was a lag between the time when period I stomach contents (i.e., recently ingested food only) peaked (1030-1130 h), and the peak for total food in the stomach (1430-1530 h) (Fig. 1, Table 1). The diet of these juveniles consisted mainly of small fish, mostly slender-bodied characins, at all periods sampled (Table 2). There were fish remains in 94 (76%) of the 123 stomachs examined and these accounted for 81% of the total volume of prey consumed. Insects, primarily dragonfly (Anisoptera) nymphs, were of secondary importance throughout the 24h period. Overall, insects were found in 77 (63%) of the stomachs examined and they made up 13% of the total food volume.
Results Discussion Juvenile Pygocentrus notutus changed feeding activity over the die1 period (Fig. l), as indicated by significant differences in stomach content weights among the seven sampling periods (p < 0.01, F(6,116 df) = 4.898). Piranha feeding activity therefore can be considered discontinuous with time. Feeding activity was most intense in the morning, tapered off in the afternoon and essentially stopped after sunset. A Student-NewmanKeuls procedure, an a posteriori test, showed that the 1030-1130h sample, with the highest mean, was significantly different from all other sample periods except 0645-0740 h of August 4 and 0630-0730 h of August 5. The maximum average (over 4.5%) stomach contents-per-fish weight in late morning fell to a minimum average of 0 around midnight. Differences between stomach content weights between the two sunrise samples of August 4 (06450740 h) and August 5 (0630-0730 h), were not significant (t == 0.18, df = 26, p> 0.05). The observed progression of period I and period II food items, expressed as a percentage of total stomach fullness, is given in Table I. Both Figure 1 and Table 1 show the large peak of period I food items in the morning (11OOh).Although there was
These young P. notutus were primarily diurnal feeders, with peak activity in the morning. In addition, similarity between two sequential morning samples suggeststhere was a regular cycle or daily feeding rhythm. Although total stomach fullness was high throughout the night (e.g., 62.5% period II food at 0300 h, Table l), this is probably accounted for by long stomach retention time of items that had been ingested the evening or day before. There are a number of possible explanations for the observed activity patterns of young piranhas. One possible reason is that the piranhas are responding to periods of higher activity of their main prey, small characins. Predator avoidance may also be important (see Werner et al. 1983). While engaged in collecting work for the present study, I observed that nearby adult P. notatus were most frequently caught with hook and line just before and during sunset. Since adult piranhas are known to attack young of the same species (Nice & Taphorn 1988)) juvenile piranhas may be restricting their foraging to periods when adults and perhaps other daytime predators (e.g., Cichla ocellark) are less active. Winemiller (1989) has suggested that large Pygo-
54 0 -total stomach contents 0 -fecently krgested items
.o a Q Pygocentrus
0700
1100
1500
1900
2300
0300
notatur
0700
Time of day Fig. 1. Twenty-four hour stomach content data for juvenile P. notatus. Mean ratio of period I (i.e., recently ingested food items) stomach weight contents expressed as a percent of weights of fish. Mean values (drawn at the midpoints of 1 hour sampling periods) are indicated by hollow circles, and vertical bars represent the 95% confidence intervals of the means, with sample sixes given above bars. Solid circles represent mean ratio of total stomach contents weight (period I and II combined) as a percent of weights of fish (confidence intervals not given). Sunrise and sunset were 0631 and 1856 h, respectively. Period ol”darkness is indicated by shading.
centrus strongly influence the daytime fish composition of open-water areas by forcing many fish to remain near cover. This may explain, in part, why juvenile piranhas are most often found in vegetated habitats (Sazima & Zamprogno 1985, Nice & Taphorn 1988). Food abundance is so great in many aquatic habitats in the llanos during the rainy season that there may be no need for young piranhas
to risk predation by moving far from cover or by expanding the time spent foraging for food. Aquarium studies of Pygocentrus nattereri, an Amazonian species closely related to P. not&us, indicate that large juveniles and small adults have two peak feeding periods during daylight, one around 0800 h and the second between 1630 and 1900h (Bellamy 1968, Zbinden 1973). Brief obser-
Table 1. Relative percentages of period I and period II stomach contents and total food volumes of juvenile piranhas, Pygocentrus notatus, by hour of collection taken on August 4-5, 1988, expressed as percentages of stomach capacity (0.4ml was used as average maximum stomach capacity). Food condition
Food items in period I condition Food items in period II condition Total food in stomachs (expressed as percent of a full stomach)
Time of capture 0645-0740
1030-1130
1430-1530
1830-1930
2230-2330
0230-0330
0630-0730
42.5 27.5
55.0 22.5
20.0 62.5
10.0 37.5
0.0 40.0
0.0 62.5
40.0 50.0
70.0
77.5
82.5
47.5
40.0
62.5
90.0
55 tomical studies of piranhas indicate they have an exceptionally well-developed visual system, and, some species, perhaps all, possessa tapetum lucidum (Ali & Raymond 1972, Ebbesson & Ito 1980, Menezes et al. 1981). I have also noted that the eyes of Venezuelan piranhas (e.g., P. notams, S. rhombeus, and S. manueli) taken at night are highly reflective. Nevertheless, piranhas do not have to rely solely on vision under low light conditions, or in turbid waters, because they also possessa welldeveloped sense of smell (see Ebbesson et al. 1981), a lateral line system, and being ostariophysaris, relatively good hearing. As presently known, the diversity of piranha diets and feeding strategies characterizes them as flexible opportunistic predators and scavengers. Piranhas live in a wide variety of habitats which differ in water clarity, and numbers and kinds of prey and predator species.Wide variations in activity patterns are reported for closely related fish, including characins such as Roeboides (Sazima 1984). Dramatic differences in activity patterns are also known within single species. Such intraspecific variation is often related to season, habitat, and age or size of individuals (Keast & Welsh 1968, Kogan 1970, Eriksson 1978, Schwassmann 1980, Provorova et al. 1986, Helfman 1986, Stewart &
vations on the behavior of other juvenile piranhas (Serrasabmn and Pristobrycon spp.) in aquaria have been less conclusive. Both diurnal (Sazima & Zamprogno 1985, Nice & Taphorn 1988) and nocturnal or crepuscular (Nice & Taphorn 1988) feeding have been reported. Catch data on fishes taken in the field with gillnets and handlines suggest piranhas are primarily active during the day (e.g., Lowe-McConnell 1964, p. 114, Goulding 1980, p. 159, Barthem 1987). Barthem (1987) reported on activity patterns of several varzea lake fishes from near Manaus, Brazil. His results, based on analysis of gillnet ca.tches,suggest an early morning peak of activity in P. nattereri, S. elongatus and S. rhombeus, and a late afternoon peak for the latter two species. Field observations in the Pantanal region of Brazil by Sazima (1988) suggest that Catoprion mento, a scale-eating specialist distantly related to other piranhas, has three peak periods of activity between 0730 and 1900 h. On the other hand, field studies also document nocturnal activities. Goulding (1980) mentioned that S. rhombeus sometimes attack fish entangled and splashing in gillnets as early as one or two hours before sunrise. Similarly, my colleagues and I have taken adult P. notatus and S. rhombeus at night using baited hooks (Nice & Taphorn 1988). Ana-
Table 2. Stom.ach contents of juvenile Pygocentrur notarus (40-68 mm SL) taken on August 4-5,1988, by hour of collection including percent total volume (%V) of food items and frequency of occurrence (F). Diet categories follow Nice & Taphom (1988), small fish include whole fish and fish flesh from small fish (unident. = unidentified).
Hour
0645-0740
1030-1130
1430-1530
1830-1930
2230-2330
0230-0330
0630-0730
Food items
%V
%V
F
%V
F
%V
%V
F
%V
F
%V
1 1
0.3 0.5
1 2
2 2
6 11
5 2 6
4 1 1 6 1 7
5
11.5 1.5 75.5
9.7 0.3 0.3 35.6 0.9 53.2
12.4
1 7 8
7 1 2 5 19 40
8.0 3.5
6.4 8.5 84.4
1.1 1.4
