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Behavioural responses to predators and predation risk in four species of larval anurans
Anim. Behav., 1989, 38, 1039-1047
Behavioural responses to predators and predation risk in four species of larval anurans SHARON
P. L A W L E R
Department of Biological Sciences, P.O. 1059, Rutgers University, Piscataway, NJ 08855-1059, U.S.A.
Abstract. Tadpoles of four anuran species show interspecific behavioural differences that could explain differential predation on these species in artifciat ponds. Replicated observations of tadpoles in aquaria revealed that the spring peeper, Hyla crucifer, is quiescent and benthic; Fowler's toad, Bufo woodhousei, is active and benthic; the grey treefrog, Hyla versicolor, is active and pelagic; and the Pine Barrens tree frog, Hyla andersonii, is intermediate in activity and microhabitat position. Species with high activity levels survived poorly in independent artificial pond predation studies, relative to less active species. Costs of low activity level may include poor competitive ability, and/or slow development with increased risk of death from pond drying. Comparisons of tadpole behaviour in aquaria with and without predators present demonstrate that all four species decrease activity with a salamander, the red-spotted newt, Notophthalrnus viridescens, and a fish, the black-banded sunfish, Enneacanthus obesus. Hyla andersonii became more benthic with these predators. Hyla versicolor and H. andersonii decreased conspicuous activities in response to a dragonfly naiad, Pantala. Bufo woodhousei responded to E. obesus even though B. woodhousei tadpoles are unpalatable to fish. Inactive H. crucifer responded less to predators than other species but survived well with predators. Baseline prey activity levels (observed in the absence of predators) may be more important than shifts in activity levels in response to predators in determining differential predation.
The impact of predation on prey species composition depends on both the physical and behavioural characteristics of the prey. Differences in prey vulnerability are often attributed solely to differences in prey size, palatability or morphology, yet behaviour may be central to the outcome of many predator-prey interactions. Prey activity level or microhabitat use could affect prey vulnerability. Active prey may be more conspicuous to predator s , and predator-prey encounter rates may differ among microhabitats. Both activity level and microhabitat use may reflect compromises between demands imposed by predator evasion, competition for resources and other factors. Because behavioural differences among prey may influence vulnerabilities to predators (e.g. Mauzey et al. 1968; Morin 1986), interactions between prey behaviour and predation demand further study. It is especially important to explore the relations between prey behaviour and vulnerability to predation in communities of physically similar prey, where morphological differences are unlikely to explain differential predation. Predators differentially attack tadpole species, even when tadpoles are similar in size and coloration (Morin 1983). Some competitively inferior tadpoles can survive in 0003-3472/89/121039+09 $03.00/0
communities with predators, while competitively superior tadpoles fail to persist (Morin 1983). A behavioural mechanism may be responsible for persistence with predators, since spring peepers, Hyla crucifer, a competitively inferior but persistent species, shifts its microhabitat use to avoid predators (Morin 1986). Such shifts indicate that different behavioural responses to predators might explain different vulnerabilities to predators. I examine the behavioural responses of four species of larval anurans that are sympatric in the New Jersey Pine Barrens (H. crucifer; Pine Barren's treefrog, H. andersonii; grey treefrog, H. versicolor; and Fowler's toad, Bufo woodhousei) to predacious fish, newts and dragonfly larvae (black-banded sunfish, Enneacanthus obesus; red-spotted newt, Notophthalmus viridescens; and Pantala), to explore possible behavioural mechanisms of coexistence with predators. Enneacanthus obesus and Pantala are common in the Pine Barrens, while N. viridescens occurs with these species in other geographical areas. Inclusion of N. viridescens permits comparisons with Morin's (1983, 1986, 1987) studies of the effects of predation on tadpoles. I address several interrelated questions about how tadpole behaviour may influence vulnerability to
9 1989 The Association for the Study of Animal Behaviour 1039
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Animal Behaviour, 38, 6
predation. Do tadpole species differ in activities or microhabitat use when predators are not immediately present? Such differences in prey behaviour could affect the frequency of predator-prey encounters. Do tadpoles alter activities or microhabitat use when predators are present? Differences among species in the ability to shift activities or microhabitat use could also change predation risk. Are interspecific differences in prey behaviour correlated with survival in the presence of predators? Such correlations would indicate that behaviour is important to differential predation.
METHODS
Study Animals
Tadpoles of B. woodhousei, H. crucifer, H. andersonii and H. versicolor overlap in size and are all cryptically coloured, so it is unlikely that different effects of predators on these species simply depend on prey morphology. Bufo woodhousei tadpoles are unpalatable to fish, which often reject them unharmed (Kruse & Stone 1984), however newts eat them readily (personal observation). If behavioural defences are costly, B. woodhousei might respond less strongly to fish. The other three prey species are palatable to all three predators. I reared tadpoles from eggs obtained by collecting amplectant pairs of frogs from Ocean County, New Jersey. I pooled hatchling tadpoles from several pairs for each species. I transferred hatchlings of 4-7 days of age to predator-free holding ponds. Holding ponds were either plastic wading pools or painted steel cattle watering tanks. These ponds were filled with stream water, 1 litre of a mixed plankton sample from Pine Barrens ponds, one packed dishpan of hay, and 30 or 50 g of Purina trout chow (wading pools and tanks, respectively, similar to Morin 1983). Screen lids were used to exclude predatory insects from the ponds. I collected newts from a temporary pond in Worthington State Forest, Warren Count3), New Jersey, and fish from Greenwood Forest Wildlife Management Area, Ocean County, New Jersey. Newts and fish were held in 40-1itre aquaria, and fed trout chow ad libitum until 24 h before an experiment. I collected dragonfly larvae from un-
covered artificial ponds near the tadpole holding ponds. Dragonfly larvae were captured on the first day of use. Trial Procedure
I observed tadpole behaviour in 20 40-1itre glass aquaria, filled to equal levels with well water, and maintained at 24~ One-way mirror film on the aquarium walls, combined with 15-W fluorescent lamps placed 10 em above the water surface, isolated tadpoles from visual stimuli originating outside the tanks. A layer of mixed sand and gravel measuring 2 cm deep, topped with a few waterlogged leaves and pine needles approximated natural benthic refugia. I changed the water in all tanks between trials to eliminate possible carry over of semiochemical predator cues (Petranka et al. 1987). I added 0.2 g of finely ground trout chow to each tank before each experiment set as food for the tadpoles. I transferred one tadpole from the holding tanks to each of the 20 aquaria the day before an experiment. Tadpoles acclimated to their new surroundings overnight (14-18 h). I observed responses between 0800 and 1800 hours. In each experiment, 10 randomly selected tanks were predator-free controls, and 10 were predator treatments. Trials began when I added a predator to predator treatments, or a small rock (approximately 2 cm 3) to control treatments to control for the disturbance of predator addition. I recorded tadpole behaviour and microhabitat position in the tank at 15-s intervals for a maximum of 10 min, or until the predator ended the trial by eating the tadpole. Categories of tadpole behaviours and microhabitat positions are listed in Table I. Replicates of the trials were run sequentially using a different individual predator in each tank. Individual tadpoles were only tested once to avoid conditioning to predators. I observed 10 tadpoles per treatment for each species. After each experiment, I measured snout-vent length and total lengths of surviving tadpoles to the nearest mm, and determined the developmental stage of the tadpoles (Gosner 1960). Predators consumed very few tadpoles during the trials, and the tadpoles that were consumed appeared to be within the size range of other uneaten prey. ! tested tadpoles singly, although ponds usually contain many tadpoles, and some species form aggregations (Wassersug 1973). Single-tadpole
Lawler: Behavioural responses in anurans
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Table I. Tadpole activities and microhabitat positions Description Activity Swim Hide Rise Bob Rasp Immobile Microhabitat Top Side Bottom Midwater Top/Side Bottom/Side
The tadpole propels itself through the water with tail and body movements Approximately 70% of the tadpole's body is beneath leaf litter Body held immobile, the tadpole rises The tadpole's mouth breaks the water surface The tadpole scrapes at a surface with its mouthparts Immobile Tadpole within 3 cm of the water surface Tadpole within 1 cm of the tank side Tadpole within 3 cm of the tank bottom Tadpole not in bottom, side or top areas Tadpole at top, and within 1 cm of the tank side Tadpole at bottom, and within 1 cm of the tank side
observations are justified because (1) only one of the four species, B. woodhousei, forms aggregations, and by using a uniform method I could compare results across species, (2) the aquaria had a density of 1 tadpole/40 litres, which is within the range of densities for tadpoles in natural ponds (see Morin 1983), and (3) I could accurately track individuals. I usually tested two or three prey species during the same experiment to compare the species' behaviour at similar developmental stages and to control for any effects of date of observation. When experiments continued for more than 1 day, I observed equal numbers of each species each day, holding the tank treatment constant between days, without changing the water. I tested the responses of the four tadpole species to newts and fish, and also tested responses of H. andersonii and H. versicolor to dragonfly larvae. I tested tadpoles at two or more developmental stages because behavioural responses to predators may change as predation risk decreases during growth and development. The youngest tadpoles tested were 7-13 days old (larval stage 25, Gosner 1960), and I refer to these as 'hatchlings' below. All hatchlings had resorbed their yolk and begun to feed.
Statistical Analysis I analysed tadpole behaviour and microhabitat data separately using two-factor multivariate analyses of variance (MANOVAs). I tested three
main null hypotheses: (1) species do not differ in activities or microhabitat use; (2) tadpoles do not respond to predators by changing activities or microhabitat use; and (3) species do not differ in their responses to predators. A significant 'species effect' in the M A N O V A s rejects hypothesis (1), a significant 'predator effect' rejects (2) and an interaction effect rejects (3). Response variables were the frequencies that I observed a tadpole perform each activity, or occupy each microhabitat position within a trial. In order to include some incomplete trials where a predator ate the tadpole, I divided the frequency that a tadpole exhibited each behaviour by the total n u m b e r of observations in its trial. This procedure converted the frequency of each behaviour into a percentage of the total n u m b e r of observations. Trials with less than five observations were not analysed. I only analysed variables (activities or microhabitat positions) exhibited by at least three tadpoles of any one of the species in each experiment set. That is, I omitted a variable from analysis if only one or two tadpoles per species exhibited that behaviour. M A N O V A s of entire experiments determined the significance of species and predator effects, and species • predator interactions. For significant M A N O V A s (P < 0-05), Bonferroni t-tests on each variable determined which variables differed among species or treatments. I used additional M A N O V A s on data for single species in some cases where the two-factor M A N O V A showed a species • treatment interac-
Animal Behaviour, 38, 6
1042 Table II. Mannova summaries
Activities Species Experiment I BW (4 mm, 25)I HA (5 mm, 25) HC (4 mm, 25) HV (4 mm, 25) Experiment II HA (5 ram, 25) HV (4 mm, 25) Experiment II1 HA (6 mm, 26) BW (7 mm, 30) HV (6 mm, 27) Experiment IV HA (13 mm, 34) HV (8 mm, 29) Experiment V HA (15 mm, 37) BW (13 mm, 37) HC (13 mm, 37) Experiment VI HA (15 mm, 40) BW (13 mm, 40) HC (14 mm, 40)
Predator Newt
Fish
Fish
Newt
Newt
Source Species Predator Spp*Pred (swim rasp
Wilk's L
df
Microhabitat P
Wilk's L
df
P
0-8041 (3,71) 0.2279 0.9641 (1,71) 0.6407 0.8965 (3,71) 0.8127 immobile hide):~
0.7264 (3,72) 0.0305* 0.9041 (1,72) 0.1331 0.8485 (3,72) 0.4740 (tside side bottom bside)
Species 0 . 7 7 7 6 (1,35) 0.0815 Predator 0-7582 (I,35) 0.0581 Spp*Pred 0.9269 (1,35) 0.6443 (swim bob rasp immobile)
0.5571 (1,35) 0.0020* 0.7739 (1,35) 0-1399 0-9332 (1,35) 0.8145 (tside mid side bottom bside)
Species Predator Spp*Pred (swim bob
0.5105 (2,53) 0.0007** 0.9350 (1,53) 0.7633 0.7196 (2,53) 0-1656 (top tside mid side bottom bside)
0 . 6 1 5 5 (2,52) 0.0019" 0.7746 (1,52) 0.0125" 0.8612 (2,52) 0.4799 rasp immobile)
Species 0 . 7 2 5 1 (1,36) 0.0567 Predator 0.5645 (1,36) 0.0018" Spp*Pred 0.9039 (1,36) 0.6418 (swim rise bob rasp immobile)
0.6219 (1,36) 0.0072* 0.8119 (1,36) 0.2231 0.7636 (1,36) 0-1083 (top tside side bside bottom)
Species Predator Spp*Pred (swim bob
0.4845 (2,54) 0.0001"** 0.8426 (1,54) 0.1167 0-6003 (2,54) 0.0031" (top tside side bottom bside)
0.4656 (2,54) 0-0001"** 0.5630 (1,54) 0.0001"** 0-6804 (2,54) 0.0096* rasp immobile)
Species 0 . 5 8 2 5 (2,54) 0-0004** Predator 0.5490 (1,54) 0-0001"** Spp*Pred 0-6802 (2,54) 0.0095* (swim bob rasp immobile)
0.5210 (2,53) 0.0003** 0.8643 (1,53) 0.1956 0.6965 (2,53) 0.0482* (top tside side bottom bside)
Species Predator Spp*Pred (swim rasp
0 . 7 7 0 8 (l,34) 0.0375* 0.6427 (1,34) 0.0025* 0.8518 (1,34) 0.1572 immobile)
0.7802 (1,34) 0.1674 0.8766 (1,34) 0.5292 0.7144 (1,34) 0-0607 (top tside side bottom bside)
Experiment VIII Species HA (14 mm, 39) Dragon- Predator HV (11 mm, 29) fly Spp*Pred (swim bob
0 . 6 3 0 3 (1,34) 0-0127" 0.5856 (1,34) 0"0049* 0.8747 (1,34) 0.5197 rasp immobile)
0.5644 (1,34) 0.0024* 0'7707 (1,34) 0.1332 0.7978 (1,34) 0.1975 (top tside side bottom bside)
Experiment VII HA (14 mm, 40) BW (13 mm, 40)
Fish
Newt
HA: Hyla andersonii; HV: H. versicolor, HC: H. crucifer; BW: B. woodhousei. * P <0"05, ** P<0.001, *** P<0.0001. t Snout-vent length, stage (Gosner 1960). :~Variables analysed: tside, top/side; mid, midwater; bside, bottom/side.
tion, and it appeared that different responses of species may have been obscured. I then performed Bonferroni t-tests to identify which variables differed a m o n g treatments. A n y differences between species or treatments for a particular variable (e.g. rasping) that I list below were significant at P < 0.05 in Bonferroni t-tests.
RESULTS
Hatehlings Hatchlings o f the four species were immobile and benthic (in the bottom or bottom/side areas) in most observations, and did not respond to predators (Table II, experiments I and II). O f the four, B.
1043
Lawler: Behavioural responses in anurans I00 90 ~:
100 90 80 > 70 60 50 g 40 50
(a)
80
~d 6O 5O 40
m g
LL
20 IO
o ioo 9o
0 I00 90
(b)
80 7o
80 70
5- 60 55 50
50
b)
60 40 30
2O I0 0
,BW C
BW Fish
HA C
HA Fish
HV C
HV Fish
20 I0 0
~BW C
BW Fish
HA C
HA Fish
HC C
HC Fish
Figure 1. Activities (a) and microhabitat use (b) of B.
Figure 2. Activities (a) and microhabitat use (b) of B.
woodhousei (BW), H. andersonii (HA) and H. versicolor (HV) with and without Enneacanthus obesus. C: control treatment; Fish: predator treatment. Species were at stages 30, 26 and 27, respectively (Gosner 1960). Tadpoles in predator treatments were predominantly immobile, rasping and swimming less than those in control treatments. Bufo woodhousei were on the bottom more frequently than H. versicolor. Key: (a) 9 immobile, [] rasp, [] swim; [] bob; (b) 9 bottom, [] midwater, [] top.
woodhousei (BW), H. andersonii (HA), and H. crucifer (HC) with and without Enneacanthus obesus. C: control treatment; Fish: predator treatment. Species were at mean stage 40 (Gosner 1960). Hyla crucifer was immobile more frequently than other species. Hyla andersonii were in the top more frequently than other species. All species increased immobility in predator treatments. Key as in
woodhousei was benthic in nearly lO0%of observations, while the other species spent some time near the water surface. Hyla andersonii and H. versicolor hatchlings were immobile in most observations, and did not respond to fish. Hyla versieolor was more benthic in experiment II than experiment I.
Interspecific Differences Among Older Tadpoles Tadpoles past the hatchling stage showed interspecific differences in activities and microhabitat use (Table II, Figs 1,2). Bufo woodhousei was active and benthic, and moved more than H. crucifer. Hyla crucifer was inactive and benthic, and both H. crucifer and B. woodhousei were in the tank bottom in more observations than either H. andersonii or H. versicolor; H. andersonii was more active than either B. woodhousei or H, crucifer, and H. versico-
Fig. 1. lor was most active, pelagic and bobbed frequently. Hyla andersonii also bobbed occasionally, but inconsistently among experiments.
Effects of Predators Tadpoles past stage 26 responded to predators (Table II). All of the species became less active with newts and fish, although the degree of change differed among species. Hyla andersonii also changed its microhabitat use with newts and fish, and both H. andersonii and H. versicolor decreased conspicuous activities in response to dragonfly larvae. I list the effects of predators on single response variables below, for each species. Bufo woodhousei responded to the newt by increasing its frequency of immobility from 36 to 70% in experiment V, and responded to the fish by increasing its frequency of immobility from 40 to 95% (experiment VI, Fig. 2). There was a corresponding reduction in conspicuous activities, such
1044
Animal Behaviour, 38, 6
as swimming and rasping, in the presence of either predator. A second experiment with newts (experiment VII) showed a decrease in rasping, but there was no increase in frequency of immobility. Hyla andersonii increased immobility with newts, but did not increase immobility with fish (experiments V and VI). However, tadpoles always tended to be less active with predators. Hyla andersonii also changed its microhabitat use with newts. A species x predator interaction (Table II, experiment V), indicated that changes in microhabitat use in response to newts depended on the responding species. A separate M A N O V A and subsequent Bonferroni t-tests showed that H. andersonii spends less time in the top of the tank in the presence of newts than in controls (Wilk's lambda = 0.4066, P < 0.002). Hyla crucifer showed a slight increase in immobility with predators in experiments V and VI. Separate MANOVAs on the H. cruciJer data showed predator treatment effects (newts: Wilk's lambda=0.5088, P < 0-0023; fish: Wilk's lambda = 0.4918, P < 0-0062). Subsequent Bonferroni t-tests of variable means showed that H. crueifer moved less and rasped less in predator tanks than in controls. Hyla crueifer changed its behaviour less than H. andersonff or B. woodhousei, probably because it is inactive even in predator-free tanks. Hyla crueifer did not change its microhabitat use with predators. Hyla versieolor was immobile more frequently with fish and newts than in controls (experiments I I I & IV). Hyla versieolor and H. andersonii also responded to dragonfly larvae by decreasing swimrning and rasping (experiment VIII). Activity Level and Survival with Predators I compared activity levels measured in the experiments above with tadpole survival in artificial ponds with N. viridescens, to determine whether active species are more vulnerable to predators than inactive species. Although there were no interspecific differences in tadpole activity in predator treatments (where all species were predominantly immobile), species' activity levels differed widely in predator-free tanks. Active species may be more vulnerable to predation even though they respond to predators at close range because (1) activity could attract the attention of predators that the tadpoles have not yet detected, and (2) active tadpoles move around, and may
therefore encounter sit-and-wait predators more often. To estimate activity levels, I averaged the percentage time active (100% - % time immobile) for tadpoles in predator-free controls for H. crucifer and B. woodhousei (stage 37-40), and H. versicolor (stage 29). Tadpole survival with the red-spotted newt was from Morin (1986) for H. crucifer, Morin (1987) for H. versicolor, and Bristow (unpublished data) for B. woodhousei. Comparable survival data for H. andersonii were unavailable. I used tadpole survival from ponds with a predator density of 2 newts/1000 litre (two per pond). To adjust for mortality from causes other than predation (e.g. competition), I divided survival in ponds with newts by survival in predator-free ponds with the same initial density of tadpoles. There is a clear positive relation between baseline levels of activity measured in predator-free aquaria, and survival with predators in artificial ponds (Spearman rank correlation=l). Species that moved less were less vulnerable to predation. Hyla versicolor had a 4% adjusted survival with newts in artificial ponds and was active in 66.5% of laboratory observations, compared with 36% survival in B. woodhousei (59-7% activity), and 88% survival in H. crueler (20'5% activity).
DISCUSSION lnterspecific Differences in Activity and Microhabitat Use Hatchlings of all four anuran species were predominantly inactive and benthic even in the absence of predators and did not respond to predators. Hatchlings may remain immobile to avoid attracting predators. Immobility is a common defence for cryptic animals (Cott 1940; Robinson 1969) and has been reported in some tadpoles (Wassersug 1971). Small tadpoles are highly vulnerable to predation (Brodie & Formanowicz 1983; Travis et al. 1985), and Stein & Magnuson (1976) found that larger prey were more active than smaller, more vulnerable prey in the presence of predators. Interspecific differences in activity and microhabitat use appeared later in development. Differences in species' activity levels were correlated with survival in artificial ponds with predators, suggesting that high activity levels increase predator-prey encounters. However, microhabitat use does not
Lawler: Behavioural responses in anurans
1045
seem to be strongly linked to survival, as two benthic species (H. crucifer and B. woodhousei) showed very different survival with predators in artificial ponds. Hyla erucifer survives well compared to B. woodhousei. This indicates that immobility in the benthic area is a more effective defence than a benthic habit alone.
sponse. Also, although B. woodhousei tadpoles are unpalatable to fish, their high activity level probably renders them conspicuous and vulnerable to attack; this could lead to injury or death even if the fish rejected the tadpole. Immobility may be a vital backup with naive predators, or if unpalatability fails to deter predators.
Responses to Predators
Activity Level, Survival and Competitive Ability
Tadpoles decreased activity in the presence of predators although they were not exposed to predators until the trials. A n innate response to predators in inexperienced prey would be advantageous when any experience with a predator is potentially lethal (Sih 1987). A response to predators in naive animals implies that predation has historically been a strong selective force (Seghers 1974; Giles 1984). Hyla andersonii became more benthic in the presence of predators. A benthic habit could be a defence against visually foraging predators for several reasons: light decreases with depth, tadpoles are more cryptic against an irregular, similarly coloured background than in the water column, and motion near the bottom can stir up silt, further hiding the prey. While the tadpoles in this study responded to predators, Woodward (1983) found that four anuran species (Rana pipiens, R. eatesbeiana and two temporary pond Scaphiopus spp.) did not respond to any of four predator species. However, Woodward's observations were fewer and less detailed than mine. He tested 20-25 tadpoles per species in a bucket that had quadrants marked on the bottom, and recorded whether the tadpole had changed quadrants at 15-s intervals over 90 s. It is possible that this method underestimated movement, because a tadpole that moved within a quadrant, or out of and back into the same quadrant within 15 s would be scored as immobile. Two lines of evidence suggest that responses to predators are general rather than finely tuned to specific predators. Tadpoles responded to an allopatric predator (the newt), and B. woodhousei responded to the fish, which find them unpalatable. Small, vulnerable animals that are endangered by many predators may respond defensively to a wide range of stimuli (Thorpe 1963; Hurley & Hartline 1974). However, red-spotted newts overlap with all four tadpole species outside of the Pine Barrens, so this is not conclusive evidence for a general re-
Active tadpole species survived poorly with redspotted newts in artificial ponds. Why are active species active despite this increased predation? Activity levels may reflect the need to garner resources as well as the need to avoid predators. Tadpoles in temporary ponds risk death from pond drying, and low activity levels could increase this risk by slowing foraging rates, which prolongs development (Wilbur & Collins 1973). Bufo woodhousei and H. versicolor have active tadpoles with short larval periods, metamorphosing from artificial ponds in about 35 days, while less active H. erucifer often require 50 days or more to complete development (see M orin 1987 for H. versicolor and H. crucifer data). Hyla erucifer often breeds in temporary ponds and has a long larval period; however, this species breeds in early spring (March-early May) and temporary ponds in this area usually do not dry up until July or August. In addition to prolonging development, low activity levels could decrease competitive ability. Inactive tadpoles may lose out in scramble competition for dwindling resources. Hyla erucifer are relatively inactive, and Morin (1983) demonstrated that H. crueifer was the least successful competitor in a guild of six larval anurans in predator-free artificial ponds. Bufo woodhousei and H. versieolor had the most active tadpoles. Bufo terrestris (related to B. woodhousei) and H. ehrysoseelis (a diploid sibling species of tetraploid H. versieolor) were the second and third most successful competitors. Scaphiopus holbrooki, an extremely active tadpole, was the competitive dominant. Other possible costs of low activity include reduced size at metamorphosis and prolonged risk of predation before attainment of an invulnerable size (Mittlebach & Chesson 1987).
Behavioural Strategies in Temporary-pond Anuran Larvae Predation and pond drying are two important causes of mortality in tadpoles in temporary ponds,
Animal Behaviour, 38, 6
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and these factors may select for different types of behaviour. Predation could select for prey inactivity to reduce conspicuousness, while pond drying could select for active foraging to speed metamorphosis. Tadpoles in temporary ponds need behavioural defences that do not slow development. Flexible defences (e.g. temporary immobility or refuging) may be more suitable than fixed defences. Fixed defences would not allow shifts in foraging strategies to increase growth rates when predation pressure is low (Sih 1987). My results support the prediction of flexible behavioural defences for animals living in temporary ponds: three of the four species I observed decreased activity dramatically with predators present. Hyla crucifer was less flexible: it showed a small decrease in activity with predators, but was generally inactive. Fixed behaviours could be favoured if the risk in sampling the environment for predators is high; the price of learning whether predators are nearby can be death ~Sih 1987). Consistent with this idea, H. crucifer was the least vulnerable to predation in artificial ponds. Interestingly, a species' baseline activity level was a better predictor of survival with predators than was the magnitude of the shift in activity levels in response to predators. This suggests that the effects of baseline activity levels o f prey on the predators' initial detection of the prey, or predator-prey encounter rates, may be more important than subsequent behaviourat responses. Such baseline differences among species, rather than responses to predators per se, may ultimately help to explain the impact of predators on behaviourally diverse prey.
ACKNOWLEDGMENTS I thank Drs Joanna Burger and Terry McGuire, whose useful suggestions greatly improved this work. Peter Morin deserves special thanks for his unsparing support and encouragement during all phases of this project, and particularly for his help in preparing the manuscript. This research was supported by grants from the Anne and James H. Leathem Scholarship Fund, and by National Science Foundation grants BSR-8414395 and BSR-8704519 to Peter J. Morin.
REFERENCES Brodie, E. D. & Formanowicz, D. R., Jr. I983. Prey size preference of predators: differential vulnerability of larval anurans. Herpetologica, 39, 67 75.
Cott, H. B. 1940. Adaptive Coloration in Anima&. London; Methuen. Giles, N. 1984. Development of the overhead fright response in wild and predator naive three-spined sticklebacks, Gasterosteus aculeatus L. Anim. Behav., 32, 276-279. Gosner, N. 1960. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 16, 183-190. Hurley, A. C. & Hartline, P. H. 1974. Escape response in the damselfish Chromis cyanea (Pisces: Pomacentridae): a quantitative study. Anita. Behav., 22, 430-437. Kruse, K. C. & Stone, B. M. 1984. Largemouth bass (Micropterus salmoides) learn to avoid feeding on toad (Bufo) tadpoles. Anita. Behav., 32, 1035-1039. Mauzey, K. P., Birkeland, C. & Dayton, P. 1968. Feeding behavior of Asteroids and escape responses of their prey in the Puget Sound region. Ecology, 49, 603 619. Mittlebach, G. G. & Chesson, P. L. 1987. Predation risk: indirect effects on fish populations. In: Predation." Direct and lndirect Impacts on Aquatic Communities (Ed. by W. C. Kerfoot & A. Sih), pp. 315-332. Hanover, New Hampshire: University Press of New England. Morin, P. J. 1983. Predation, competition, and the composition of larval anuran guilds. EcoL Monogr., 53, 119-138. Morin, P. J. 1986. Interactions between intraspecific competition and predation in an amphibian predatorprey system. Ecology, 67, 713-720. Morin, P. J. 1987. Predation, bleeding asynchrony, and the outcome of competition among treefrog tadpoles. Ecology, 68, 675-683. Petranka, J. W., Kats, L. B. & Sih, A. 1987. Predator prey interactions among fish and larval amphibians: use of chemical cues to detect predatory fish. Anim. Behav., 35, 420 425. Robinson, M. H. 1969. Defenses against visually hunting predators. Evol. Biol., 3, 225-257. Seghers, B. H. 1974. Geographic variation in the responses of guppies (Poecilia reticulata) to aerial predators. Oecologia (Berl.), 14, 93-98. Sih, A. 1987. Predators and prey lifestyles: an evolutionary and ecological overview. In: Predation: Direct and Indirect Impacts on Aquatic Communities (Ed. by W. C. Kerfoot & A. Sih), pp. 203-224. Hanover, New Hampshire: University Press of New England. Stein, R. A. & Magnuson, J. J. 1976. Behavioural response of crayfish to a fish predator. Ecology, 57, 751-761. Thorpe, W. H. 1963. Learning and Instinct in Animals. Cambridge, Massachusetts: Harvard University Press. Travis, J., Keen, W. H. & Juilianna, J. 1985. The role of relative body size in a predator-prey relationship between dragonfly naiads and larval anurans. Oikos, 45, 59-65. Wassersug, R. J. 197 I. On the comparative palatability of some dry-season tadpoles from Costa Rica. Am. Midl. Nat., 86, 101-109. Wassersug, R. J. 1973. Aspects of social behavior in anuran larvae. In: Evolutionary Biology of the Anurans (Ed. by J. L. Vial), pp. 273 297. Columbia, Missouri: University of Missouri Press.
Lawler." Behavioural responses in anurans Wilbur, H. M. & Collins, J. P. 1973. Ecological aspects of amphibian metamorphosis. Science, N.Y., 182, 13051314. Woodward, B. D. 1983. Predator-prey interactions and
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breeding-pond use of temporary-pond species in a desert anuran community. Ecology, 64, 1549-1555. (Received 16 November 1988; revised 13 February 1989; MS. number: A5357)
Behavioural responses to predators and predation risk in four species of larval anurans SHARON
P. L A W L E R
Department of Biological Sciences, P.O. 1059, Rutgers University, Piscataway, NJ 08855-1059, U.S.A.
Abstract. Tadpoles of four anuran species show interspecific behavioural differences that could explain differential predation on these species in artifciat ponds. Replicated observations of tadpoles in aquaria revealed that the spring peeper, Hyla crucifer, is quiescent and benthic; Fowler's toad, Bufo woodhousei, is active and benthic; the grey treefrog, Hyla versicolor, is active and pelagic; and the Pine Barrens tree frog, Hyla andersonii, is intermediate in activity and microhabitat position. Species with high activity levels survived poorly in independent artificial pond predation studies, relative to less active species. Costs of low activity level may include poor competitive ability, and/or slow development with increased risk of death from pond drying. Comparisons of tadpole behaviour in aquaria with and without predators present demonstrate that all four species decrease activity with a salamander, the red-spotted newt, Notophthalrnus viridescens, and a fish, the black-banded sunfish, Enneacanthus obesus. Hyla andersonii became more benthic with these predators. Hyla versicolor and H. andersonii decreased conspicuous activities in response to a dragonfly naiad, Pantala. Bufo woodhousei responded to E. obesus even though B. woodhousei tadpoles are unpalatable to fish. Inactive H. crucifer responded less to predators than other species but survived well with predators. Baseline prey activity levels (observed in the absence of predators) may be more important than shifts in activity levels in response to predators in determining differential predation.
The impact of predation on prey species composition depends on both the physical and behavioural characteristics of the prey. Differences in prey vulnerability are often attributed solely to differences in prey size, palatability or morphology, yet behaviour may be central to the outcome of many predator-prey interactions. Prey activity level or microhabitat use could affect prey vulnerability. Active prey may be more conspicuous to predator s , and predator-prey encounter rates may differ among microhabitats. Both activity level and microhabitat use may reflect compromises between demands imposed by predator evasion, competition for resources and other factors. Because behavioural differences among prey may influence vulnerabilities to predators (e.g. Mauzey et al. 1968; Morin 1986), interactions between prey behaviour and predation demand further study. It is especially important to explore the relations between prey behaviour and vulnerability to predation in communities of physically similar prey, where morphological differences are unlikely to explain differential predation. Predators differentially attack tadpole species, even when tadpoles are similar in size and coloration (Morin 1983). Some competitively inferior tadpoles can survive in 0003-3472/89/121039+09 $03.00/0
communities with predators, while competitively superior tadpoles fail to persist (Morin 1983). A behavioural mechanism may be responsible for persistence with predators, since spring peepers, Hyla crucifer, a competitively inferior but persistent species, shifts its microhabitat use to avoid predators (Morin 1986). Such shifts indicate that different behavioural responses to predators might explain different vulnerabilities to predators. I examine the behavioural responses of four species of larval anurans that are sympatric in the New Jersey Pine Barrens (H. crucifer; Pine Barren's treefrog, H. andersonii; grey treefrog, H. versicolor; and Fowler's toad, Bufo woodhousei) to predacious fish, newts and dragonfly larvae (black-banded sunfish, Enneacanthus obesus; red-spotted newt, Notophthalmus viridescens; and Pantala), to explore possible behavioural mechanisms of coexistence with predators. Enneacanthus obesus and Pantala are common in the Pine Barrens, while N. viridescens occurs with these species in other geographical areas. Inclusion of N. viridescens permits comparisons with Morin's (1983, 1986, 1987) studies of the effects of predation on tadpoles. I address several interrelated questions about how tadpole behaviour may influence vulnerability to
9 1989 The Association for the Study of Animal Behaviour 1039
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Animal Behaviour, 38, 6
predation. Do tadpole species differ in activities or microhabitat use when predators are not immediately present? Such differences in prey behaviour could affect the frequency of predator-prey encounters. Do tadpoles alter activities or microhabitat use when predators are present? Differences among species in the ability to shift activities or microhabitat use could also change predation risk. Are interspecific differences in prey behaviour correlated with survival in the presence of predators? Such correlations would indicate that behaviour is important to differential predation.
METHODS
Study Animals
Tadpoles of B. woodhousei, H. crucifer, H. andersonii and H. versicolor overlap in size and are all cryptically coloured, so it is unlikely that different effects of predators on these species simply depend on prey morphology. Bufo woodhousei tadpoles are unpalatable to fish, which often reject them unharmed (Kruse & Stone 1984), however newts eat them readily (personal observation). If behavioural defences are costly, B. woodhousei might respond less strongly to fish. The other three prey species are palatable to all three predators. I reared tadpoles from eggs obtained by collecting amplectant pairs of frogs from Ocean County, New Jersey. I pooled hatchling tadpoles from several pairs for each species. I transferred hatchlings of 4-7 days of age to predator-free holding ponds. Holding ponds were either plastic wading pools or painted steel cattle watering tanks. These ponds were filled with stream water, 1 litre of a mixed plankton sample from Pine Barrens ponds, one packed dishpan of hay, and 30 or 50 g of Purina trout chow (wading pools and tanks, respectively, similar to Morin 1983). Screen lids were used to exclude predatory insects from the ponds. I collected newts from a temporary pond in Worthington State Forest, Warren Count3), New Jersey, and fish from Greenwood Forest Wildlife Management Area, Ocean County, New Jersey. Newts and fish were held in 40-1itre aquaria, and fed trout chow ad libitum until 24 h before an experiment. I collected dragonfly larvae from un-
covered artificial ponds near the tadpole holding ponds. Dragonfly larvae were captured on the first day of use. Trial Procedure
I observed tadpole behaviour in 20 40-1itre glass aquaria, filled to equal levels with well water, and maintained at 24~ One-way mirror film on the aquarium walls, combined with 15-W fluorescent lamps placed 10 em above the water surface, isolated tadpoles from visual stimuli originating outside the tanks. A layer of mixed sand and gravel measuring 2 cm deep, topped with a few waterlogged leaves and pine needles approximated natural benthic refugia. I changed the water in all tanks between trials to eliminate possible carry over of semiochemical predator cues (Petranka et al. 1987). I added 0.2 g of finely ground trout chow to each tank before each experiment set as food for the tadpoles. I transferred one tadpole from the holding tanks to each of the 20 aquaria the day before an experiment. Tadpoles acclimated to their new surroundings overnight (14-18 h). I observed responses between 0800 and 1800 hours. In each experiment, 10 randomly selected tanks were predator-free controls, and 10 were predator treatments. Trials began when I added a predator to predator treatments, or a small rock (approximately 2 cm 3) to control treatments to control for the disturbance of predator addition. I recorded tadpole behaviour and microhabitat position in the tank at 15-s intervals for a maximum of 10 min, or until the predator ended the trial by eating the tadpole. Categories of tadpole behaviours and microhabitat positions are listed in Table I. Replicates of the trials were run sequentially using a different individual predator in each tank. Individual tadpoles were only tested once to avoid conditioning to predators. I observed 10 tadpoles per treatment for each species. After each experiment, I measured snout-vent length and total lengths of surviving tadpoles to the nearest mm, and determined the developmental stage of the tadpoles (Gosner 1960). Predators consumed very few tadpoles during the trials, and the tadpoles that were consumed appeared to be within the size range of other uneaten prey. ! tested tadpoles singly, although ponds usually contain many tadpoles, and some species form aggregations (Wassersug 1973). Single-tadpole
Lawler: Behavioural responses in anurans
1041
Table I. Tadpole activities and microhabitat positions Description Activity Swim Hide Rise Bob Rasp Immobile Microhabitat Top Side Bottom Midwater Top/Side Bottom/Side
The tadpole propels itself through the water with tail and body movements Approximately 70% of the tadpole's body is beneath leaf litter Body held immobile, the tadpole rises The tadpole's mouth breaks the water surface The tadpole scrapes at a surface with its mouthparts Immobile Tadpole within 3 cm of the water surface Tadpole within 1 cm of the tank side Tadpole within 3 cm of the tank bottom Tadpole not in bottom, side or top areas Tadpole at top, and within 1 cm of the tank side Tadpole at bottom, and within 1 cm of the tank side
observations are justified because (1) only one of the four species, B. woodhousei, forms aggregations, and by using a uniform method I could compare results across species, (2) the aquaria had a density of 1 tadpole/40 litres, which is within the range of densities for tadpoles in natural ponds (see Morin 1983), and (3) I could accurately track individuals. I usually tested two or three prey species during the same experiment to compare the species' behaviour at similar developmental stages and to control for any effects of date of observation. When experiments continued for more than 1 day, I observed equal numbers of each species each day, holding the tank treatment constant between days, without changing the water. I tested the responses of the four tadpole species to newts and fish, and also tested responses of H. andersonii and H. versicolor to dragonfly larvae. I tested tadpoles at two or more developmental stages because behavioural responses to predators may change as predation risk decreases during growth and development. The youngest tadpoles tested were 7-13 days old (larval stage 25, Gosner 1960), and I refer to these as 'hatchlings' below. All hatchlings had resorbed their yolk and begun to feed.
Statistical Analysis I analysed tadpole behaviour and microhabitat data separately using two-factor multivariate analyses of variance (MANOVAs). I tested three
main null hypotheses: (1) species do not differ in activities or microhabitat use; (2) tadpoles do not respond to predators by changing activities or microhabitat use; and (3) species do not differ in their responses to predators. A significant 'species effect' in the M A N O V A s rejects hypothesis (1), a significant 'predator effect' rejects (2) and an interaction effect rejects (3). Response variables were the frequencies that I observed a tadpole perform each activity, or occupy each microhabitat position within a trial. In order to include some incomplete trials where a predator ate the tadpole, I divided the frequency that a tadpole exhibited each behaviour by the total n u m b e r of observations in its trial. This procedure converted the frequency of each behaviour into a percentage of the total n u m b e r of observations. Trials with less than five observations were not analysed. I only analysed variables (activities or microhabitat positions) exhibited by at least three tadpoles of any one of the species in each experiment set. That is, I omitted a variable from analysis if only one or two tadpoles per species exhibited that behaviour. M A N O V A s of entire experiments determined the significance of species and predator effects, and species • predator interactions. For significant M A N O V A s (P < 0-05), Bonferroni t-tests on each variable determined which variables differed among species or treatments. I used additional M A N O V A s on data for single species in some cases where the two-factor M A N O V A showed a species • treatment interac-
Animal Behaviour, 38, 6
1042 Table II. Mannova summaries
Activities Species Experiment I BW (4 mm, 25)I HA (5 mm, 25) HC (4 mm, 25) HV (4 mm, 25) Experiment II HA (5 ram, 25) HV (4 mm, 25) Experiment II1 HA (6 mm, 26) BW (7 mm, 30) HV (6 mm, 27) Experiment IV HA (13 mm, 34) HV (8 mm, 29) Experiment V HA (15 mm, 37) BW (13 mm, 37) HC (13 mm, 37) Experiment VI HA (15 mm, 40) BW (13 mm, 40) HC (14 mm, 40)
Predator Newt
Fish
Fish
Newt
Newt
Source Species Predator Spp*Pred (swim rasp
Wilk's L
df
Microhabitat P
Wilk's L
df
P
0-8041 (3,71) 0.2279 0.9641 (1,71) 0.6407 0.8965 (3,71) 0.8127 immobile hide):~
0.7264 (3,72) 0.0305* 0.9041 (1,72) 0.1331 0.8485 (3,72) 0.4740 (tside side bottom bside)
Species 0 . 7 7 7 6 (1,35) 0.0815 Predator 0-7582 (I,35) 0.0581 Spp*Pred 0.9269 (1,35) 0.6443 (swim bob rasp immobile)
0.5571 (1,35) 0.0020* 0.7739 (1,35) 0-1399 0-9332 (1,35) 0.8145 (tside mid side bottom bside)
Species Predator Spp*Pred (swim bob
0.5105 (2,53) 0.0007** 0.9350 (1,53) 0.7633 0.7196 (2,53) 0-1656 (top tside mid side bottom bside)
0 . 6 1 5 5 (2,52) 0.0019" 0.7746 (1,52) 0.0125" 0.8612 (2,52) 0.4799 rasp immobile)
Species 0 . 7 2 5 1 (1,36) 0.0567 Predator 0.5645 (1,36) 0.0018" Spp*Pred 0.9039 (1,36) 0.6418 (swim rise bob rasp immobile)
0.6219 (1,36) 0.0072* 0.8119 (1,36) 0.2231 0.7636 (1,36) 0-1083 (top tside side bside bottom)
Species Predator Spp*Pred (swim bob
0.4845 (2,54) 0.0001"** 0.8426 (1,54) 0.1167 0-6003 (2,54) 0.0031" (top tside side bottom bside)
0.4656 (2,54) 0-0001"** 0.5630 (1,54) 0.0001"** 0-6804 (2,54) 0.0096* rasp immobile)
Species 0 . 5 8 2 5 (2,54) 0-0004** Predator 0.5490 (1,54) 0-0001"** Spp*Pred 0-6802 (2,54) 0.0095* (swim bob rasp immobile)
0.5210 (2,53) 0.0003** 0.8643 (1,53) 0.1956 0.6965 (2,53) 0.0482* (top tside side bottom bside)
Species Predator Spp*Pred (swim rasp
0 . 7 7 0 8 (l,34) 0.0375* 0.6427 (1,34) 0.0025* 0.8518 (1,34) 0.1572 immobile)
0.7802 (1,34) 0.1674 0.8766 (1,34) 0.5292 0.7144 (1,34) 0-0607 (top tside side bottom bside)
Experiment VIII Species HA (14 mm, 39) Dragon- Predator HV (11 mm, 29) fly Spp*Pred (swim bob
0 . 6 3 0 3 (1,34) 0-0127" 0.5856 (1,34) 0"0049* 0.8747 (1,34) 0.5197 rasp immobile)
0.5644 (1,34) 0.0024* 0'7707 (1,34) 0.1332 0.7978 (1,34) 0.1975 (top tside side bottom bside)
Experiment VII HA (14 mm, 40) BW (13 mm, 40)
Fish
Newt
HA: Hyla andersonii; HV: H. versicolor, HC: H. crucifer; BW: B. woodhousei. * P <0"05, ** P<0.001, *** P<0.0001. t Snout-vent length, stage (Gosner 1960). :~Variables analysed: tside, top/side; mid, midwater; bside, bottom/side.
tion, and it appeared that different responses of species may have been obscured. I then performed Bonferroni t-tests to identify which variables differed a m o n g treatments. A n y differences between species or treatments for a particular variable (e.g. rasping) that I list below were significant at P < 0.05 in Bonferroni t-tests.
RESULTS
Hatehlings Hatchlings o f the four species were immobile and benthic (in the bottom or bottom/side areas) in most observations, and did not respond to predators (Table II, experiments I and II). O f the four, B.
1043
Lawler: Behavioural responses in anurans I00 90 ~:
100 90 80 > 70 60 50 g 40 50
(a)
80
~d 6O 5O 40
m g
LL
20 IO
o ioo 9o
0 I00 90
(b)
80 7o
80 70
5- 60 55 50
50
b)
60 40 30
2O I0 0
,BW C
BW Fish
HA C
HA Fish
HV C
HV Fish
20 I0 0
~BW C
BW Fish
HA C
HA Fish
HC C
HC Fish
Figure 1. Activities (a) and microhabitat use (b) of B.
Figure 2. Activities (a) and microhabitat use (b) of B.
woodhousei (BW), H. andersonii (HA) and H. versicolor (HV) with and without Enneacanthus obesus. C: control treatment; Fish: predator treatment. Species were at stages 30, 26 and 27, respectively (Gosner 1960). Tadpoles in predator treatments were predominantly immobile, rasping and swimming less than those in control treatments. Bufo woodhousei were on the bottom more frequently than H. versicolor. Key: (a) 9 immobile, [] rasp, [] swim; [] bob; (b) 9 bottom, [] midwater, [] top.
woodhousei (BW), H. andersonii (HA), and H. crucifer (HC) with and without Enneacanthus obesus. C: control treatment; Fish: predator treatment. Species were at mean stage 40 (Gosner 1960). Hyla crucifer was immobile more frequently than other species. Hyla andersonii were in the top more frequently than other species. All species increased immobility in predator treatments. Key as in
woodhousei was benthic in nearly lO0%of observations, while the other species spent some time near the water surface. Hyla andersonii and H. versicolor hatchlings were immobile in most observations, and did not respond to fish. Hyla versieolor was more benthic in experiment II than experiment I.
Interspecific Differences Among Older Tadpoles Tadpoles past the hatchling stage showed interspecific differences in activities and microhabitat use (Table II, Figs 1,2). Bufo woodhousei was active and benthic, and moved more than H. crucifer. Hyla crucifer was inactive and benthic, and both H. crucifer and B. woodhousei were in the tank bottom in more observations than either H. andersonii or H. versicolor; H. andersonii was more active than either B. woodhousei or H, crucifer, and H. versico-
Fig. 1. lor was most active, pelagic and bobbed frequently. Hyla andersonii also bobbed occasionally, but inconsistently among experiments.
Effects of Predators Tadpoles past stage 26 responded to predators (Table II). All of the species became less active with newts and fish, although the degree of change differed among species. Hyla andersonii also changed its microhabitat use with newts and fish, and both H. andersonii and H. versicolor decreased conspicuous activities in response to dragonfly larvae. I list the effects of predators on single response variables below, for each species. Bufo woodhousei responded to the newt by increasing its frequency of immobility from 36 to 70% in experiment V, and responded to the fish by increasing its frequency of immobility from 40 to 95% (experiment VI, Fig. 2). There was a corresponding reduction in conspicuous activities, such
1044
Animal Behaviour, 38, 6
as swimming and rasping, in the presence of either predator. A second experiment with newts (experiment VII) showed a decrease in rasping, but there was no increase in frequency of immobility. Hyla andersonii increased immobility with newts, but did not increase immobility with fish (experiments V and VI). However, tadpoles always tended to be less active with predators. Hyla andersonii also changed its microhabitat use with newts. A species x predator interaction (Table II, experiment V), indicated that changes in microhabitat use in response to newts depended on the responding species. A separate M A N O V A and subsequent Bonferroni t-tests showed that H. andersonii spends less time in the top of the tank in the presence of newts than in controls (Wilk's lambda = 0.4066, P < 0.002). Hyla crucifer showed a slight increase in immobility with predators in experiments V and VI. Separate MANOVAs on the H. cruciJer data showed predator treatment effects (newts: Wilk's lambda=0.5088, P < 0-0023; fish: Wilk's lambda = 0.4918, P < 0-0062). Subsequent Bonferroni t-tests of variable means showed that H. crueifer moved less and rasped less in predator tanks than in controls. Hyla crueifer changed its behaviour less than H. andersonff or B. woodhousei, probably because it is inactive even in predator-free tanks. Hyla crueifer did not change its microhabitat use with predators. Hyla versieolor was immobile more frequently with fish and newts than in controls (experiments I I I & IV). Hyla versieolor and H. andersonii also responded to dragonfly larvae by decreasing swimrning and rasping (experiment VIII). Activity Level and Survival with Predators I compared activity levels measured in the experiments above with tadpole survival in artificial ponds with N. viridescens, to determine whether active species are more vulnerable to predators than inactive species. Although there were no interspecific differences in tadpole activity in predator treatments (where all species were predominantly immobile), species' activity levels differed widely in predator-free tanks. Active species may be more vulnerable to predation even though they respond to predators at close range because (1) activity could attract the attention of predators that the tadpoles have not yet detected, and (2) active tadpoles move around, and may
therefore encounter sit-and-wait predators more often. To estimate activity levels, I averaged the percentage time active (100% - % time immobile) for tadpoles in predator-free controls for H. crucifer and B. woodhousei (stage 37-40), and H. versicolor (stage 29). Tadpole survival with the red-spotted newt was from Morin (1986) for H. crucifer, Morin (1987) for H. versicolor, and Bristow (unpublished data) for B. woodhousei. Comparable survival data for H. andersonii were unavailable. I used tadpole survival from ponds with a predator density of 2 newts/1000 litre (two per pond). To adjust for mortality from causes other than predation (e.g. competition), I divided survival in ponds with newts by survival in predator-free ponds with the same initial density of tadpoles. There is a clear positive relation between baseline levels of activity measured in predator-free aquaria, and survival with predators in artificial ponds (Spearman rank correlation=l). Species that moved less were less vulnerable to predation. Hyla versicolor had a 4% adjusted survival with newts in artificial ponds and was active in 66.5% of laboratory observations, compared with 36% survival in B. woodhousei (59-7% activity), and 88% survival in H. crueler (20'5% activity).
DISCUSSION lnterspecific Differences in Activity and Microhabitat Use Hatchlings of all four anuran species were predominantly inactive and benthic even in the absence of predators and did not respond to predators. Hatchlings may remain immobile to avoid attracting predators. Immobility is a common defence for cryptic animals (Cott 1940; Robinson 1969) and has been reported in some tadpoles (Wassersug 1971). Small tadpoles are highly vulnerable to predation (Brodie & Formanowicz 1983; Travis et al. 1985), and Stein & Magnuson (1976) found that larger prey were more active than smaller, more vulnerable prey in the presence of predators. Interspecific differences in activity and microhabitat use appeared later in development. Differences in species' activity levels were correlated with survival in artificial ponds with predators, suggesting that high activity levels increase predator-prey encounters. However, microhabitat use does not
Lawler: Behavioural responses in anurans
1045
seem to be strongly linked to survival, as two benthic species (H. crucifer and B. woodhousei) showed very different survival with predators in artificial ponds. Hyla erucifer survives well compared to B. woodhousei. This indicates that immobility in the benthic area is a more effective defence than a benthic habit alone.
sponse. Also, although B. woodhousei tadpoles are unpalatable to fish, their high activity level probably renders them conspicuous and vulnerable to attack; this could lead to injury or death even if the fish rejected the tadpole. Immobility may be a vital backup with naive predators, or if unpalatability fails to deter predators.
Responses to Predators
Activity Level, Survival and Competitive Ability
Tadpoles decreased activity in the presence of predators although they were not exposed to predators until the trials. A n innate response to predators in inexperienced prey would be advantageous when any experience with a predator is potentially lethal (Sih 1987). A response to predators in naive animals implies that predation has historically been a strong selective force (Seghers 1974; Giles 1984). Hyla andersonii became more benthic in the presence of predators. A benthic habit could be a defence against visually foraging predators for several reasons: light decreases with depth, tadpoles are more cryptic against an irregular, similarly coloured background than in the water column, and motion near the bottom can stir up silt, further hiding the prey. While the tadpoles in this study responded to predators, Woodward (1983) found that four anuran species (Rana pipiens, R. eatesbeiana and two temporary pond Scaphiopus spp.) did not respond to any of four predator species. However, Woodward's observations were fewer and less detailed than mine. He tested 20-25 tadpoles per species in a bucket that had quadrants marked on the bottom, and recorded whether the tadpole had changed quadrants at 15-s intervals over 90 s. It is possible that this method underestimated movement, because a tadpole that moved within a quadrant, or out of and back into the same quadrant within 15 s would be scored as immobile. Two lines of evidence suggest that responses to predators are general rather than finely tuned to specific predators. Tadpoles responded to an allopatric predator (the newt), and B. woodhousei responded to the fish, which find them unpalatable. Small, vulnerable animals that are endangered by many predators may respond defensively to a wide range of stimuli (Thorpe 1963; Hurley & Hartline 1974). However, red-spotted newts overlap with all four tadpole species outside of the Pine Barrens, so this is not conclusive evidence for a general re-
Active tadpole species survived poorly with redspotted newts in artificial ponds. Why are active species active despite this increased predation? Activity levels may reflect the need to garner resources as well as the need to avoid predators. Tadpoles in temporary ponds risk death from pond drying, and low activity levels could increase this risk by slowing foraging rates, which prolongs development (Wilbur & Collins 1973). Bufo woodhousei and H. versicolor have active tadpoles with short larval periods, metamorphosing from artificial ponds in about 35 days, while less active H. erucifer often require 50 days or more to complete development (see M orin 1987 for H. versicolor and H. crucifer data). Hyla erucifer often breeds in temporary ponds and has a long larval period; however, this species breeds in early spring (March-early May) and temporary ponds in this area usually do not dry up until July or August. In addition to prolonging development, low activity levels could decrease competitive ability. Inactive tadpoles may lose out in scramble competition for dwindling resources. Hyla erucifer are relatively inactive, and Morin (1983) demonstrated that H. crueifer was the least successful competitor in a guild of six larval anurans in predator-free artificial ponds. Bufo woodhousei and H. versieolor had the most active tadpoles. Bufo terrestris (related to B. woodhousei) and H. ehrysoseelis (a diploid sibling species of tetraploid H. versieolor) were the second and third most successful competitors. Scaphiopus holbrooki, an extremely active tadpole, was the competitive dominant. Other possible costs of low activity include reduced size at metamorphosis and prolonged risk of predation before attainment of an invulnerable size (Mittlebach & Chesson 1987).
Behavioural Strategies in Temporary-pond Anuran Larvae Predation and pond drying are two important causes of mortality in tadpoles in temporary ponds,
Animal Behaviour, 38, 6
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and these factors may select for different types of behaviour. Predation could select for prey inactivity to reduce conspicuousness, while pond drying could select for active foraging to speed metamorphosis. Tadpoles in temporary ponds need behavioural defences that do not slow development. Flexible defences (e.g. temporary immobility or refuging) may be more suitable than fixed defences. Fixed defences would not allow shifts in foraging strategies to increase growth rates when predation pressure is low (Sih 1987). My results support the prediction of flexible behavioural defences for animals living in temporary ponds: three of the four species I observed decreased activity dramatically with predators present. Hyla crucifer was less flexible: it showed a small decrease in activity with predators, but was generally inactive. Fixed behaviours could be favoured if the risk in sampling the environment for predators is high; the price of learning whether predators are nearby can be death ~Sih 1987). Consistent with this idea, H. crucifer was the least vulnerable to predation in artificial ponds. Interestingly, a species' baseline activity level was a better predictor of survival with predators than was the magnitude of the shift in activity levels in response to predators. This suggests that the effects of baseline activity levels o f prey on the predators' initial detection of the prey, or predator-prey encounter rates, may be more important than subsequent behaviourat responses. Such baseline differences among species, rather than responses to predators per se, may ultimately help to explain the impact of predators on behaviourally diverse prey.
ACKNOWLEDGMENTS I thank Drs Joanna Burger and Terry McGuire, whose useful suggestions greatly improved this work. Peter Morin deserves special thanks for his unsparing support and encouragement during all phases of this project, and particularly for his help in preparing the manuscript. This research was supported by grants from the Anne and James H. Leathem Scholarship Fund, and by National Science Foundation grants BSR-8414395 and BSR-8704519 to Peter J. Morin.
REFERENCES Brodie, E. D. & Formanowicz, D. R., Jr. I983. Prey size preference of predators: differential vulnerability of larval anurans. Herpetologica, 39, 67 75.
Cott, H. B. 1940. Adaptive Coloration in Anima&. London; Methuen. Giles, N. 1984. Development of the overhead fright response in wild and predator naive three-spined sticklebacks, Gasterosteus aculeatus L. Anim. Behav., 32, 276-279. Gosner, N. 1960. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 16, 183-190. Hurley, A. C. & Hartline, P. H. 1974. Escape response in the damselfish Chromis cyanea (Pisces: Pomacentridae): a quantitative study. Anita. Behav., 22, 430-437. Kruse, K. C. & Stone, B. M. 1984. Largemouth bass (Micropterus salmoides) learn to avoid feeding on toad (Bufo) tadpoles. Anita. Behav., 32, 1035-1039. Mauzey, K. P., Birkeland, C. & Dayton, P. 1968. Feeding behavior of Asteroids and escape responses of their prey in the Puget Sound region. Ecology, 49, 603 619. Mittlebach, G. G. & Chesson, P. L. 1987. Predation risk: indirect effects on fish populations. In: Predation." Direct and lndirect Impacts on Aquatic Communities (Ed. by W. C. Kerfoot & A. Sih), pp. 315-332. Hanover, New Hampshire: University Press of New England. Morin, P. J. 1983. Predation, competition, and the composition of larval anuran guilds. EcoL Monogr., 53, 119-138. Morin, P. J. 1986. Interactions between intraspecific competition and predation in an amphibian predatorprey system. Ecology, 67, 713-720. Morin, P. J. 1987. Predation, bleeding asynchrony, and the outcome of competition among treefrog tadpoles. Ecology, 68, 675-683. Petranka, J. W., Kats, L. B. & Sih, A. 1987. Predator prey interactions among fish and larval amphibians: use of chemical cues to detect predatory fish. Anim. Behav., 35, 420 425. Robinson, M. H. 1969. Defenses against visually hunting predators. Evol. Biol., 3, 225-257. Seghers, B. H. 1974. Geographic variation in the responses of guppies (Poecilia reticulata) to aerial predators. Oecologia (Berl.), 14, 93-98. Sih, A. 1987. Predators and prey lifestyles: an evolutionary and ecological overview. In: Predation: Direct and Indirect Impacts on Aquatic Communities (Ed. by W. C. Kerfoot & A. Sih), pp. 203-224. Hanover, New Hampshire: University Press of New England. Stein, R. A. & Magnuson, J. J. 1976. Behavioural response of crayfish to a fish predator. Ecology, 57, 751-761. Thorpe, W. H. 1963. Learning and Instinct in Animals. Cambridge, Massachusetts: Harvard University Press. Travis, J., Keen, W. H. & Juilianna, J. 1985. The role of relative body size in a predator-prey relationship between dragonfly naiads and larval anurans. Oikos, 45, 59-65. Wassersug, R. J. 197 I. On the comparative palatability of some dry-season tadpoles from Costa Rica. Am. Midl. Nat., 86, 101-109. Wassersug, R. J. 1973. Aspects of social behavior in anuran larvae. In: Evolutionary Biology of the Anurans (Ed. by J. L. Vial), pp. 273 297. Columbia, Missouri: University of Missouri Press.
Lawler." Behavioural responses in anurans Wilbur, H. M. & Collins, J. P. 1973. Ecological aspects of amphibian metamorphosis. Science, N.Y., 182, 13051314. Woodward, B. D. 1983. Predator-prey interactions and
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breeding-pond use of temporary-pond species in a desert anuran community. Ecology, 64, 1549-1555. (Received 16 November 1988; revised 13 February 1989; MS. number: A5357)