The effect of respiratory mode and oxygen concentration on the risk of aerial predation in fishes

DONALD L. KRAMER,' DAVID MANLEY, AND RAY BOURGEOIS Department of Biology, McGill University, 1205 Avenue Docteur Penjield, Montreal, P.Q., Canada H3A IBI

Received July 28, 1982

KRAMER, D. L., D. MANLEY, and R. BOURGEOIS. 1983. The effect of respiratory mode and oxygen concentration on the risk of aerial predation in fishes. Can. J. Zool. 61: 653-665.

Six bimodal and six water-breathing species of fish were exposed to predation by a green heron (Butorides striatus) in a laboratory experiment to examine the hypothesis that aerial predation selects against the evolution and use of air breathing. Tests were performed at 1.6 and 0.5 mg 02.L-' (po2 = 30 and 9 Torr, respectively; 1 Torr = 133.322 Pa). Most water breathers avoided the surface at 1.6 mg.L-' but not at 0.5 mg.L-', where they performed aquatic surface respiration. Most bimodal species breathed air at both oxygen concentrations. The risk of capture increased with proximity to the surface. The prey species responded to the predator by increasing mean depth, decreasing the rate of air breathing or aquatic surface respiration, and avoiding the vicinity of the predator when surfacing. Despite these and other antipredator characteristics, all species were vulnerable to capture in the test situation. Overall, the survivorship of water-breathing fishes was significantly higher than that of bimodal species at 1.6 mg.LP1 and similar to that of bimodal species at 0.5 mg.L-'. Aerial predation pressure should favor water breathing over air breathing except at oxygen concentrations lower than 0.5 mg.L-'.

KRAMER, D. L., D. MANLEY et R. BOURGEOIS. 1983. The effect of respiratory mode and oxygen concentration on the risk of aerial predation in fishes. Can. J. Zool. 61: 653-665.

Six esphces de poissons a respiration aquatique et six especes a respiration bimodale ont kt6 soumises a la prkdation par un hkron vert (Butorides striatus) au cours d'une expkrience de laboratoire destinke a kprouver I'hypothhse selon laquelle la predation akrienne dkfavorise l'kvolution et l'utilisation de la respiration akrienne. Des concentrations de 1,6 mg 02.L-' (PO;! = 30Ton, 1 Torr = 133,322 Pa) et de 0,5 mg 02.L-' (po2 = 9 Ton) ont kt6 utiliskes au cours des expkriences. La plupart des poissons a respiration aquatique Cvitaient la surface a 1,6 mg-L-' , mais, a 0,5 mg.L-' , ils respiraient prhs de la surface. La plupart des especes a respiration bimodale respiraient I'air aux deux concentrations d'oxyghne. Les risques d'Ctre capturC augmentent en surface. Les especes proies rkagissent a la prksence du prCdateur en nageant a une profondeur moyenne plus grande, en diminuant leur taux de respiration aCrienne ou de respiration aquatique en surface et en s'kloignant du voisinage du prkdateur pour faire surface. En dCpit de ces stratdgies anti-prkdatrices, toutes les esphces sont restkes vulnCrables au cours des tests. En gCnCral, la survie des poissons a respiration purement aquatique s'est avCrCe significativement plus Clevke que celle des espces a respiration bimodale a 1,6 mg 02.L-' , et semblable a celle des especes a respiration bimodale a 0,5 mg 02.L-'. La pression de la prtdation adrienne semble donc favoriser la respiration aquatique plut6t qu'akrienne, sauf aux concentrations d'oxyghne infkrieures a 0,5 mg.L-'.

[Traduit par le journal]

Introduction In habitats subject to dissolved oxygen deficiency

(hypoxia), the fishes may show one of three responses to oxygen reduction. Some species breathe air (Johansen 1970), a few survive on anaerobiosis (Blaika 1958; Hochachka and Somero 197 1 ) , but most perform aqua- tic surface respiration, using the higher levels of dissolved oxygen at the air-water interface (Lewis 1970; Gee et al. 1978; Kramer and McClure 1982). Comparative physiology suggests that aerial respiration should be energetically much less costly than aquatic respiration (e.g . , Hughes 1963; Dejours 1976; Schmidt- Nielsen 1979), and that this advantage becomes more pronounced as dissolved oxygen declines (Hughes and Shelton 1962). Thus, it is surprising that even in habitats with significant periods of hypoxia, the majority of species are water breathers, incapable of aerial respira-

' ~u tho r to whom reprint requests should be addressed.

tion (Carter and Beadle 193 1; Kramer et al. 1978; Kramer 1982). Furthermore, many air breathers are actually bimodal and use aquatic respiration predomi- nantly or exclusively until dissolved oxygen levels become extremely low (Johansen 1970; Gee 1976). One would expect large energetic savings to favor both the evolution of air breathing in water-breathing species and the maximal use of air breathing in bimodal species.

This apparent paradox has several possible explana- tions (Gans 1970a, 1970 b; Kramer and McClure 198 1 ; Kramer 1983). One hypothesis suggests that aerial respiration is selected against because it subjects fishes to higher levels of aerial predation, especially from wading and plunge-diving birds (Gans 1970a, 1970 b; Kramer and Graham 1976; Stevens and Holeton 1978; Randall et al. 198 1). Fish surfacing to breathe air would be more vulnerable than water-breathing fish, at least in well-oxygenated water. Under hypoxic conditions, it is less obvious how water breathing could be favored,

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654 CAN. J. ZOOL. VOL. 61, 1983

because fish performing aquatic surface respiration often spend 50-95% of their time at the surface (Gee et al. 1978; Kramer and Mehegan 198 1; Kramer and McClure 1982). This would seem to make aquatic surface respiration much riskier than air breathing. However, aquatic surface respiration is often initiated at lower levels of dissolved oxygen than those at which air breathing begins to increase (Kramer and McClure 1982), perhaps because specialization on aquatic respi- ration permits more effective oxygen extraction under hypoxic conditions (e.g., Graham et al. 1978). Thus, predation could favor aquatic resiration even in hypoxic habitats if this respiratory mode reduces the oxygen concentration at which any surface exposure is neces- sary. The increased risk during extreme hypoxia would be balanced by reduced risk, as compared with air breathing, during periods of milder hypoxia.

Support for the hypothesis that predation has influ- enced the evolution of aerial respiration comes from behavioral features of air breathing that are most easily explained as adaptations to reduce risk. These features include the irregularity, speed, and social synchroniza- tion of air breathing, and its responsiveness to disturb- ance (Kramer and Graham 1976), as well as the pattern of expiration after inspiration (Graham et al. 1977). However, there is no direct evidence that air breathing actually does increase risk. The hypothesis depends upon the assumptions that aerial predation is an impor- tant selective factor on fish populations, that risk of aerial predation is affected by exposure to the surface, and that air breathing significantly increases surface exposure. While a general negative correlation between risk and distance from the surface seems reasonable a priori, the actual pattern of change in risk has not been studied. Similarly, while air breathing and aquatic surface respiration must to some extent increase surface exposure, the potential of fish to reduce the duration and frequency of these trips, or the possession of other antipredator adaptations, might make the increase neg- ligible. Flexibility in surface use has been studied in a few species subjected to disturbances such as shadows and splashes (Kramer and Graham 1976; Gee 1980, 198 1 ; Kramer and Mehegan 198 1 ) , but responses to real predators have not been examined. There has been no previous comparison of surface use in bimodal and water-breathing fish under the same conditions. The present report examines the predation hypothesis by investigating (i) the relation between distance from the surface and risk of capture by an aerial predator, (ii) the extent to which bimodal and water-breathing fish alter their respiratory use of the surface in the presence of a real predator, and (iii) the relative vulnerability of bimodal and water-breathing fish at two levels of hypoxia in the laboratory.

Methods The predator, a hand-reared, 1-year-old male green heron

(Butorides striatus virescens) weighing 240 g, was maintained in an indoor flight cage (1 13 x 183 x 190 cm) and fed about 50g frozen or live fish daily. Butorides striatus has a worldwide distribution, being found especially in habitats with an abundance of dense, woody vegetation (Hancock and Elliot 1978). It is a rather short-legged species and typically hunts in extreme shallows or from a perch adjacent to deeper water (Meyerriecks 1962) where it captures a wide range of fishes and invertebrates (Palmer 1962).

The experimental prey consisted of 18 individuals of each of six species of water-breathing and six species of air-breathing freshwater fishes. Diversity of prey species within each mode was used to improve the generality of the comparison between modes. Species choice was governed by availability and by an attempt to balance the range of sizes, shapes, and antipredator defenses between the two respiratory modes. Names, body forms, and specimen sizes are given in Fig. 1. Umbra and Lepomis were captured near Montreal, Canada. The other species were tropical or subtropical forms purchased from aquarium dealers.

Experiments were carried out in a room (240 x 244 x 244 cm) connected by a passageway to the heron's flight cage. The test arena was an aquarium 1 1 2 x 38 x 43 cm deep, placed 97 cm above the floor of the room. Lighting was provided by two cool white fluorescent bulbs 53 cm above the water surface. A 7.-cm diameter branch placed lengthwise just above the water surface provided a perch from which the heron generally hunted, although it also used the aquarium sides. Fine gravel filled the aquarium to a depth of 10 cm, and the water level was maintained 30 cm above the gravel. The glass side of the aquarium was divided by black lines into four vertical sectors and three depth zones to facilitate recording predator and prey positions. A submersible heater maintained the water at 26.5"C (maximum range 26-27.5"C). The water was rapidly and continuously pumped between the aquarium and a 190-L narrow-necked bottle in which it was deoxyge- nated using compressed nitrogen. Oxygen concentration was adjusted by varying the nitrogen flow rate. Water circulation prevented local subsurface variation in oxygen concentration and temperature. Both were monitored by a Yellow Springs Instruments model 57 oxygen meter with a probe and continuously operating stirrer attachment placed in one comer of the aquarium. The instrument was checked by the Winkler method and was air-calibrated several times during each trial. The experiment consisted of nine sets of trials. In each set one trial was carried out at an oxygen concentration of 1.6 mg-L-' (po2 = 30 Torr; 1 Torr = 133.322Pa) and the other at 0.5 mg-L-' (9 Torr). These levels are both hypoxic, 19.5 and 6.1% saturation, respectively. They were chosen on the basis of previous studies (e.g. Gee et al. 1978; Kramer and McClure 1982) with the intention that air breathing would be performed by bimodal species at both concentrations while only the lower concentration would induce aquatic surface respiration in water-breathing species. The order of treatments within each set was randomized. Individual trials at the higher oxygen averaged 1.52.- 1.60 mg-L-' , with an overall mean of 1.57 mg. L-' and a maximum range of 1 .30- 1.80 mg.L-' in individual

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KRAMER ET AL.

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FIG. 1. Prey species used in a study of responses to an aerial predator, showing names, general body form, and the distribution of weights and lengths. Short vertical lines give the means, rectangles represent two standard errors of the mean, and horizontal lines give ranges. For each species the data for nine individuals tested at 1.6 mg 02-L-' are presented above the data for another nine tested at 0.5 mg 02.L-'.

readings. The lower oxygen trial means were 0.43-0.63 mg.L-' with a mean of 0.51 mg-L-' and a maximum range of 0.40-0.65 rng.LP'.

On the day preceding a trial one fish of each species was weighed, measured, and placed in an acclimation tank in which oxygen was lowered to the required level over several hours. The fish were then transferred to the experimental tank and allowed further acclimation overnight. On the next day we made final corrections in oxygen concentration and tempera- ture, then took a 50-min control record of fish depth and respiratory use of the surface. For this, two observers sat quietly 135 cm in front of the aquarium. Once each minute one observer recorded the depth zone of each fish (0-lOcm, 10-20 cm, 20-30 cm) and whether it was performing aquatic surface respiration, defined as contact with the surface. The second observer used a Datamyte 900 Event Recorder to record the time and sector of all air breaths. After 50 min oxygen and temperature were checked and adjusted if neces- sary, and the heron was allowed to enter the test room. A second 50-min record was made, starting when the heron alighted on the perch. In addition to the information recorded in the control period, the second observer noted the position of

the heron, defined by the sector below its eye, and the species, time, and depth zone of all captures. After the observation period the heron continued hunting, while oxygen, tempera- ture, and surviving species were monitored at regular inter- vals. The trial was terminated when one or no fish remained or the heron had hunted for 12.5 h without reaching this criterion. This sometimes necessitated completion of the experiment on a 2nd day. The total weight of fish per trial averaged 28.3 g. This was insufficient to satiate the heron which could consume as much as 100 g of fish per day.

As an indication of the relative risk of prey in each depth zone we used Chesson's alpha

where ri is the proportion of captures from depth zone i, pi is the proportion of fish in depth zone i (Chesson 1978). Chesson's alpha is a preferred index of risk because it can be derived from a stochastic model of predator-prey interactions and because it is unaffected by changes in the relative numbers in each prey category (Lechowicz 1982). The index varies from 0 to 1 with the sum for all categories equal to 1.

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656 CAN. J. ZOOL. VOL. 61, 1983

Results Success of the predator

1 BMB,0.5 ~ = 3 4 [ BMB, 1.6 N=39 0 I

The heron usually hunted while crouched motionless or walking slowly along the perch or edges of the - aquarium. Less frequently, rapid walking or running

20 ,122 ,308

with sudden, jerky movements were seen. These pat- 0 .O 1 1 .008 terns are thought to flush prey from hiding (Kushlan - 3 0 1976a) and were observed-more often after the heron had hunted for long periods without fish approaching the surface. Usually, the heron captured prey with a rapid strike in which fish were grasped or speared with the bill while the bird remained on the perch. But it also showed probing and groping near the bottom with its beak and on occasion dived into the tank from the perch. Strikes at fish near the bottom were often preceded by several incomplete attempts and appeared slower than strikes near the surface. All patterns except probing and groping have been described in field observations of this species (Palmer 1962; Kushlan 1977). Probing and groping, defined according to whether the beak is opened or closed, have been reported in other heron species.

Captures were approximately evenly distributed among the three depth zones at 1.6 mg-L-' and favored the top third at 0.5 mg-L-', despite the fact that fish of both respiratory modes at both oxygen concentrations strongly favored the lower third of the aquarium (Fig. 2). G-tests in all cases showed highly significant differences between the distribution of fish and the distribution of captures (G > 58, df = 2, p < 0.005). Risk was consistently highest in the top lOcm, much lower in the 10- to 20-cm zone, and very low in the 20- to 30-cm zone (Fig. 2). Within each respiratory mode risk in the top 10cm was also higher at 0.5 mg-L-' than it was at 1.6 mg-L-'.

Although considered an index of "feeding prefer- ence," Chesson's alpha does not separate preference by the predator from differential escape by ,the prey. Our observations suggested preferential hunting in the top lOcm, but we also obtained evidence of lower success per strike at greater dep,ths, mostly because of prey avoidance tactics. During the final four sets of trials we recorded strikes that missed as well as successful captures. Table 1 shows that the success rate declined from 75.7% in the top 10 cm to 19.8% in the bottom 10 cm. Since air-breathing is a characteristic movement, we were able to recognize when fish were rising to breathe. Out of 49 observed captures of air-breathing fish, fish were rising to breathe in 25 cases (51%). In several additional cases the heron was alerted to the presence of a fish by a breath, then pursued and captured it as it dove.

Responses by the jish The fish in general reacted very strongly to the

l l l l l ! . l l , '

0 25 5 0 75 100 0 25 5 0 75 100

P E R C E N T FIG. 2 . Percent capture success by a green heron in relation

to fish depth, respiratory mode, and dissolved oxygen concen- tration. Data are presented for six species of bimodal breathing (BMB) and six species of water-breathing (WB) fishes tested at 1.6 and 0.5 mg 0 2 - ~ - ' . Bars show the distribution of fishes and dots the distribution of captures. N is the total number of captures observed. The distribution of fishes is based on one record per minute 0.f the position of each of 54 fishes (9 of each species) for up to 50 min or until it was captured (1267-2443 point observations). The relative risk in each depth zone is indicated by Chesson's alpha index shown to the right of each bar.

TABLE 1 . Capture success of a green heron in relation to depth of prey

Depth (cm)

0-10 10-20 20-30 Total

Total strikes 37 14 86 137 Total captures 28 8 17 5 3 % success 75.7 57.1 19.8 38.7

predator, showing much more vigorous orientation and avoidance responses to the heron than they had to disturbances from the experimenters in the pretrial manipulations. We quantified changes in depth, rates of air breathing or aquatic surface respiration, and location of air breaths. Mean depth, calculated from the propor- tion of time in each depth zone and at the surface, increased greatly for all species in the presence of the heron (Table 2). This change was statistically significant in all except the two cases in which there were insufficient data to perform the test. Figure 3 shows the percent time in each zone during control observations and in the presence of the heron. At 1.6 mg-L-' in the absence of the heron, bimodal and water-breathing fish were fairly well distributed over the three zones. At

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CAN. J . ZOOL. VOL. 61, 1983

FIG. 3. The effect of dissolved oxygen concentration and the presence of a heron on the percent time spent in three depth zones by bimodal and water-breathing fish. Observations at 1.6 mg 02.L-' are above and at 0.5 mg 02.L-' below. For each depth the mean percent time spent by each species is shown for control observations before the heron was introduced (0) and for observations in the presence of the heron (@). Sample sizes are given in Table 2. The small numbers identify individual species as in Fig. 1 .

0.5 rng-L-' the bimodal fish were also distributed fairly evenly among the three zones, but water-breathing fish occurred more frequently in the top 10 cm because of increased use of aquatic surface respiration. These patterns changed dramatically in the presence of the heron. At 1.6 mg-L-' water-breathing fish essentially eliminated their use of the top 20 cm, and most bimodal fish did the same. At 0.5 mg.L-' not all water-breathing fish reduced their use of the top two zones to the same extent as they had at 1.6 mg.L-', and there was a similar tendency for some bimodal species to be found in the top 20 cm.

Respiration also changed significantly in the presence of the predator. Air-breathing rates dropped in all bimodal species at both oxygen concentrations. These differences were statistically significant in all cases where a sufficient number of individuals survived long enough to permit a test (Table 3A). Two patterns can be seen. Trichogaster , Helostoma, and Macro- podus reduced air-breathing rates by 28-83% but still continued to breathe at least once in l0min. Most

Hypostomus did not surface at all during the observa- tion period with the heron; their mean reduction was over 95%. From the limited data obtained, Pangasius appeared to fit the former pattern and Umbra the latter. The use of aquatic surface respiration by water- breathing fish also changed markedly in the presence of the heron (Table 3B). Before the heron was introduced, tropical water breathers spent only 0.2-5.1% of their time at the surface at 1.6 mg-L-', while Lepomis spent 33.8%. The tropical species ceased aquatic surface respiration in the heron's presence, and Lepomis re- duced its surface use to 1.0%. At 0.5 mg. L-' under control conditions, all species showed high rates of aquatic surface respiration ranging from 24.4 to 93.8% of time at the surface. With the heron present aquatic surface respiration was eliminated in Cichlasoma and Jordanella and reduced to less than 1.5% of the time in Xiphophorus, Hemigrammus, and Brachydanio. Le- pomis appeared to reduce its use of aquatic surface respiration to a lesser extent, but was captured so quickly that an adequate measure was not obtained.

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660 CAN. J. ZOOL. VOL. 61, 1983

T R I C H O G A S T E R H E L O S T O M A M A C R O P O D U S n = 2 8 8 n = 8 5 9

FIG. 4. Location of breathing sites by Trichogaster, Helostoma, and Macropodus, in relation to position of a heron. The top row indicates percentage of breaths in each sector of the aquarium during control observations before the heron was introduced. The next four lines are the distribution of breaths with the heron successively in sectors one through four. Heron position is indicated by the letter H. The number of breaths with the heron in each sector is indicated.

In addition to air-breathing rates, the surfacing behavior of the bimodal species changed in response to the heron. Instead of a continuous movement the fish often approached the surface very slowly, diving at any sudden movement. After getting close to the surface, the breath was accomplished in a very rapid dart and dive. For Trichogaster , Helostoma, and Macropodus, which breathed frequently in the presence of the heron, we were able to quantify the effect of the predator on breathing site (Fig. 4). In the absence of the predator the distribution of breathing sites of all three species were significantly different from random (G-test, G > 45, p < 0.005 in all cases). Trichogaster and Helostoma used the center sectors more than the ends; Macropodus used the ends. In the presence of the predator all species showed a strong avoidance of the sector in which the heron was located, usually maximal breathing fre- quency in the most distant sector, and an increased occurrence at the ends as opposed to the middle sectors of the tank. The distribution of breaths was significantly different from the control series for all four heron locations and all three species (G-test, G > 12, p < 0.01), except for Macropodus with the heron in sector 1

in which only nine breaths were recorded (0.05 < p < 0.10). These results were not caused by a simple flight response with the fish always occupying the sector most distant from the heron. Often, they would remain near the bottom in the same sector as the heron and suddenly dash to the most distant sector to breathe before the heron could change its position. Avoidance was not complete in part because the heron stalked the fish, attempting to remain above them. When they breathed in a sector occupied by the heron, the fish often surfaced on the side of the perch opposite the heron.

Respiratory modes and survival In order to examine the effect of respiratory mode on

survival, all species in each mode were pooled, and the number of surviving fish of each mode was compared for successive time intervals. At 1.6 m g - ~ - ' water- breathing fishes had much better survival than bimodal species (Fig. 5A). After 10 min of hunting significantly more water-breathing than bimodal fishes remained, and this pattern persisted until the end of the test ( p < 0.005, Wilcoxon matched-pairs test, one-tailed). At 0.5 mg.

FIG. 5. The effect of respiratory mode and dissolved oxygen concentration on susceptibility of fish to predation by a heron. (A) Total number of fish surviving in relation to heron hunting time. A, 0 , water-breathing (WB) fish; A, 0 , bimodal (BMB) species; 0 , 0 , 1.6 mg 02.L-'; A, A, 0.5 mg 02.L-'. (B) Risk, measured by Chesson's alpha index, of bimodal fishes relative to water-breathing fishes in relation to heron hunting time. 0 , 1.6 mg 02.L-'; A, 0.5 mg o2.LP'. The broken line at 0.5 indicates equal risk for both modes. Values larger than this indicate increased risk of capture for bimodal fishes. Lower values indicate increased risk for water-breath- ing fishes.

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TABLE 4. The effect of species on survival time of fishes subjected to predation by a heron. The table shows results of a Friedman analysis of variance for experiments with six bimodal and six water-

breathing species at two oxygen concentrations

1.6 mg O,.L-' 0.5 mg o~.L- '

Bimodal Water-breathing Combined Bimodal Water-breathing Combined

L-' the survivorship of water-breathing fish was signifi- cantly reduced as compared with 1.6 mg-L-' ( p < 0.005). Survival of water-breathing forms was still slightly higher than that of bimodal forms at 0.5 mg. L-'. Using a two-tailed test because this effect had not been predicted, the difference was significant ( p < 0.02) from the 30th through the 60th min of hunting.

Chesson's alpha provided an index of the relative risk of bimodal and water-breathing fishes throughout the experiment (Fig. 5B). For this calculation pi was the proportion of surviving fish of respiratory mode i. and ri was the proportion of captures of respiratory mode i during a given time interval. Of 14 intervals at 1.6 mg. L-' the risk of bimodal species was greater than that of water-breathers in all except one. Of twelve intervals at 0.5 mg.L-' the risk of bimodal forms was greater than that of water breathers in 8.

Other species characteristics besides respiratory mode affected susceptibility to the heron. Friedman analysis of variance showed significant effects of species for the entire set of 12 species and for the 6 species within each respiratory mode considered sepa- rately (Table 4). Figure 6 shows mean survival time for each species, and Table 5 presents the two-way inter- specific comparisons. Large interspecific differences are apparent, and the ranking of bimodal and water- breathing species reflects both the overall greater aver- age risk of bimodal forms and the increased strength of this effect at 1.6 mg-L-' .The number of significant interspecific differences is less at 0.5 mg-L-' than at 1.6 mg.L-' . Of the water-breathing species, Lepomis had poor survival, similar to the bimodal forms at both oxygen concentrations, as did Brachydanio at 0.5 mg-L-'. On the other hand, Helostoma tended to have relatively high survival for a bimodal species, especially at 0.5 mgaL-'. Helostoma was the only species for which there was any indication of avoidance by the heron. Sometimes Helostoma surfaced close to the heron without being attacked. Nevertheless, only 6 of 18 individuals survived to the end of the trial, all at 0.5 mg-L-'. None of the supposed antipredator adapta- tions of the other species, including the spines and armor

of Hypostomus protected them from the heron. The tendency of Hypostomus to hide motionless rendered it vulnerable to the heron even at the bottom, and reduced its survival time despite its low rate of surfacing. The most active species, Xiphophorus, Brachydanio, and Hemigrammus, were the least vulnerable at 1.6 mg-L-' because they remained near the bottom and dodged the strikes by the heron. However, low oxygen had a much stronger effect on the vulnerability of these species than on the relatively less active Jordanella and Cichlasoma. Perhaps the more active species had a higher oxygen demand, requiring greater use of aquatic surface respira- tion (see Table 3). Pangasius, the most active bimodal species, was the most vulnerable because it swam continuously in midwater making it very conspicuous. It surfaced often and did not respond strongly to the predator.

Discussion This study supports the hypothesis that the act of air

breathing increases the risk of aerial predation. In the trials at 1.6 mg O2-L-l when most bimodal species were air breathing while most water-breathing species were not using aquatic surface respiration, the bimodal fishes were at much higher risk of capture. Although there were interspecific differences within each mode, the bimodal and water-breathing forms covered a similar range of size, shape, and escape tactics. Thus, it is likely that air breathing itself was the major contributor to the difference in risk between the two groups. This conclu- sion is strengthened by the observation that more than half the captures of bimodal fish occurred during breaths despite the very small proportion of total time occupied by this activity.

Air breathing increased risk because it required an approach to the surface. Our study showed that overall risk of capture was much higher in the top IOcm, although the heron could effectively capture prey to a depth of at least 30 cm. Capture success in the top 10 cm was about 1.3 times as high as in the 10- to 20-cm zone and 3.8 times as high as in the 20- to 30-cm zone. Thus, it is not surprising that the heron attacked fish more

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662 CAN. J . ZOOL. VOL. 61, 1983

P A N G A S I U S

M A C R O P O D U S 1.6

UMBRA

L E P O M I S

T R I C H O G A S T E R

H Y P O S T O M U S

J O R D A N E L L A

H E L O S T O M A

C I C H L A S O M A

P A N G A S I U S

L E P O M I S

UMBRA

M A C R O P O D U S

B R A C H Y D A N I O

HY P O S T O M U S

T R I C H O G A S T E R

X I P H O P H O R U S

H E M I G R A M M U S

JORDANELLA

H E L O S T O M A

C I C H L A S O M A

I I

0 20 0 400 ' 600 800

S U R V I V A L ( M I N ) FIG. 6. Survival time of 12 species of fish subjected to heron

predation. Bars show means and lines one standard error. Shaded bars represent bimodal species and open bars water- breathing species. The data in the upper panel were obtained at 1.6 mg 02.L-' and in the lower panel at 0 .5 mg o2-L-' .

frequently near the surface. Fish in this position are probably more vulnerable because they can be more precisely localized, because there is less resistance from the water to the speed of the strike, and because they have less time from the initiation of a strike in which to escape.

It is important to consider the extent to which these results are applicable to more natural circumstances. In the field, variation in light levels, surface glare and rippling, water clarity, and cover might affect both the absolute level and the gradient of risk with depth. Observations of the success of terns foraging under a variety of weather conditions (Dunn 1973) show that it is not always easy to predict whether these features will increase the advantage of predator or of prey. Neverthe- less, it seems likely that the surface will always be

riskier than greater depths, provided that aerial predators are not completely excluded. This conclusion is suppor- ted by field studies showing preferential feeding by wading and diving birds on fishes frequenting the littoral zone or surface waters farther from shore (Whitfield and Blaber 1978, 1979; Ashmole and Ashmole 1967) and suggesting increased vulnerability of fishes as they are forced nearer to the surface by drying of isolated ponds (Kushlan 1976b), low tide (Kushlan 1977; Mace and Fisher 198 1 2), oxygen gradients (Kushlan 1977), and pursuit by predatory fishes (Ashmole and Ashmole 1967).

Our study prevented the fish from using intraspecific social defence strategies such as schooling and the synchronization of breaths and confined them in the vicinity of the predator. Such strategies would change our conclusions only if they were totally effective in thwarting aerial predation. This seems unlikely but requires further experimentation. The only relevant field evidence is the suggestion by Whitfield and Blaber (1978) that Clarias, a benthic bimodal fish, is attacked by its aerial predators while surfacing to breathe.

The risk associated with the act of breathing is a selective force potentially favoring the retention of water-breathing capacity in fish which have evolved air breathing. Many species of air-breathing fish possess well-developed gills and use aquatic respiration pre- dominantly or exclusively except under hypoxic condi- tions (Johansen 1970; Gee 1976; Singh 1976). This study showed that air-breathing fish have the potential to greatly reduce their frequency of surfacing, even under extremely hypoxic conditions. Hypostomus reduced air breathing so much that it might have been completely protected, given deeper or more turbid water or addi- tional shelter. It is not known whether the reductions in air breathing were achieved through a lowering of oxygen demand, an increase in aquatic ventilation, or a change in the amount of oxygen extracted from each breath. Several previous studies have documented re- ductions in air breathing by fishes and amphibians in response to surface disturbances (Kramer and Graham 1976; Baird 1982), and Gee (1981) showed that such reductions were associated with an increase in aquatic ventilation in mudminnows.

Predation pressure should also favor the minimization of aquatic surface respiration. The increased risk of water breathers at 0.5 mg o2-L-' compared with 1.6 mg-L-' was most likely due to their increased use of

2 ~ a c e , P. M. , and J . M. Fisher. 1981. Bird predation on juvenile salmonids in the Big Qualicum Estuary, Vancouver Island. Unpublished report to Department of Fisheries and Oceans Canada (Vancouver). Available from P. Mace, Insti- tute of Animal Resource Ecology, University of British Columbia, 2204 Main Mall, Vancouver, B.C. Canada V6T 1W5.

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TABLE 5 . Interspecific differences in survival o f heron predation

( A ) 1.6 mg 02.L-'

Species 5 3 6 1 1 2 4 2 8 7 9 1 1 1 0

(5)Pangasius - * * * * ** ** ** ** ** ** ** (3)Macropodus * - - * ** ** ** ** ** ** (6 ) Umbra * - - - - - * ** ** ** ** ** ( 1 ) Trichogaster * - - - - - ** ** ** **

(12) Lepomis * - - - - . - . ** * ** (4)Hypostomus ** * - - - - - - . * ** ** (2)Helostoma ** ** * - - - - ** ** ** (8)Jordanella ** ** ** - - - - - - * ** ** (7)Cichlasoma ** ** ** ** - - - * * ** (9)Xiphophorus ** ** ** ** ** * ** * * - - -

(l l)Brachydanio ** ** ** ** * ** ** ** * - - -

(lO)Hemigrammus** ** ** ** ** ** ** ** ** - - -

( B ) 0 .5 mg o2-L-'

Species 5 1 2 6 3 1 1 4 1 1 0 8 9 2 7

(5)Pangasius - - - * ** ** ** ** ** ** ** ( 12) Lepomis - - . . * * * * * * * * * * *

( 6 ) Umbra - - - - - * * * * * * * * * * * (3 ) Macropodus - - - * * * ** **

( l l ) B r a c h y d a n i o * - - - - - - - * * ** (4)Hypostomus ** * * - - - - - * * ** (")Trichogaster ** ** * * - - - - - - ** **

(lO)Hemigrammus** * * - - - - - - - * (8 ) Jordanella ** ** ** * - - - - - - - * (9)Xiphophorus ** * ** * * * - - - - - * (2)Helostoma ** ** ** ** * * ** - - - - - (7)Cichlasoma ** ** ** ** ** ** ** * * * - -

NOTE: Species are listed in order of increasing mean rank of survival time. Numbers refer to species as in Fig. 1. Symbols indicate probability that each pair of species does not differ in survival time (Wilcoxon matched-pairs test, two-tailed): **, p S 0.01; *, p S 0.05; *, p S 1.0; -, p > 1.0).

aquatic surface respiration. In previous comparative studies 0.8 mg.L-' was the modal oxygen concentration at which both temperate and tropical fish species spent 50% of their time at the surface (Gee et al. 1978; Kramer and McClure 1982). Gee et al. (1978) suggested that most species used aquatic surface respiration only when normal subsurface respiration was no longer possible. In a detailed investigation of aquatic surface respiration in guppies, an artificial aerial predator stimulus had only minor, short-term effects on use of the surface (Kramer and Mehegan 1981). Therefore, the large extent to which water-breathing species reduced their use of aquatic surface respiration even at 0.5 mg.L-' was unexpected.

In addition to reducing surface use among both water breathers and air breathers, aerial predation might favor one respiratory mode over the other if their patterns of minimal surface exposure in relation to oxygen concen- tration are not the same. It seems likely that water

breathers would often have a lower threshold for the initiation of surface use than bimodal breathers, as observed in this study, because of the advantages of specialization on aquatic respiration. On the other hand, once aquatic surface respiration begins, water breathers might have much higher exposure than air breathers. Whether water breathing or bimodal breathing would be favored would depend on the amount of time that the oxygen concentration was above or below the level at which aquatic surface respiration requires more expo- sure than air breathing. The present study suggests that this critical level could be below 0.5 mg.L-', thus favoring water breathing in most oxygen regimes, but additional work will be needed to determine the general- ity of this result.

A final point concerns whether aerial predators are sufficiently widespread and numerous to exert a signifi- cant selective pressure on fish respiratory patterns. Direct evidence supporting this assumption comes from

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664 CAN. J. ZOOL. VOL. 61, 1983

estimates of food consumption by predators attacking known fish populations (Alexander 1979; Welcomme 1979; Mace and Fisher 1981 (see footnote 2)), from measured rates of mortality which could be attributed principally to birds (Blaber 1973; Kushlan 1976 b) , and from the effects of reductions in predator populations (Elson 1962). Indirect support comes from the wide- spread occurrence of well-developed responses to aerial predators. In addition to changes in air breathing and aquatic surface respiration, these include movement away from the surface (Seghers 1974; Gee 1980, 198 1 ; present study), social synchronization of breaths (Gee 1980; Baird 1982), changes in foraging rate and site (Milinski and Heller 1978), and avoidance of the vicinity of the predator (Mock 1980; present study). One would not expect the evolution of these responses in such a diversity of species if aerial predators were not an important source of mortality on fish populations.

Support for the predation hypothesis does not neces- sarily exclude other explanations for the relative lack of air breathing. Kramer and McClure ( 198 1) provided evidence for significant travel costs associated with air breathing; other costs, including disruption of ongoing activities, hydrostatic difficulties, increased drag as a consequence of increased volume, problems with C02 excretion, and circulatory inefficiencies have also been suggested (Gans 1970a, 1970b; Gee 1981; Kramer 1983). Finally, some studies on the cost of ventilation in reptiles and amphibia suggest that the advantages to air breathing may not be as great as generally assumed (West and Jones 1975; Kinney and White 1977). Such factors, in addition to predation, must be taken into account in attempts to develop a general explanation for the evolution of respiratory patterns.

Acknowledgements We thank Doug Mock and Peter Boag for encourage-

ment and advice on heron-rearing, Ken Nakatsuru and Roberto Cavalcanti for advice on computing, and M. Power, G. Caldwell, and J. Gee for comments on the manuscript. The research was supported by the Natural Sciences and Engineering Research Council of Canada. Preliminary studies were aided by a McGill Biology Department Independent Studies Grant to D. M.

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al u

se o

nly.