We demonstrate the effect of fish predation on genotype frequencies in a laboratory population composed of two Daphnia magna clones, with historically contrasting exposures to fish predation. The two clones differed in their responsiveness to predation via differential avoidance/escape behavior. The clone which coexists with fish in nature is more responsive to the presence of a fish predator, while the clone not exposed to fish predation does not exhibit the defensive reaction. Fish caused a rapid (within 18 h) and significant shift in Daphnia clonal composition, from 1:1 to 8:1, in favor of the responsive clone. Genotype-specific defensive abilities (modus defendi) can contribute greatly to the phenomenon of genotype replacement under selective predation

Lampert, W.

Pijanowska, J.

Weider, L.

English

MPG.PuRe

Oecologia (1993) 96:40-42 Oecologia 9 Springer-Verlag 1993 Predator-mediated genotypic shifts in a prey population: experimental evidence Joanna Pijanowska*, Lawrence J. Weider, Winfried Lampert Max-Planck-Institut ffir Limnologie, Postfach 165, D-24306 P16n, Germany Received: 5 April 1993 / Accepted: 12 July 1993 Abstract. We demonstrate the effect of fish predation on genotype frequencies in a laboratory population com- posed of two Daphnia magna clones, with historically contrasting exposures to fish predation. The two clones differed in their responsiveness to predation via differen- tial avoidance/escape behavior. The clone which coexists with fish in nature is more responsive to the presence of a fish predator, while the clone not exposed to fish preda- tion does not exhibit the defensive reaction. Fish caused a rapid (within 18 h) and significant shift in Daphnia clonal composition, from 1:1 to 8:1, in favor of the responsive clone. Genotype-specific defensive abilities (modus defendi) can contribute greatly to the phenomenon of genotype replacement under selective predation. Key words: D a p h n i a  - Vertical migration - Predator- induced behavior - Clonal replacement As a major source of mortality in many natural popula- tions (Elton 1927), predation can be a potent selective factor shaping avoidance and escape behavioral responses in prey populations (e.g., Sih 1987; Lima and Dill 1990). Differences among genotypes with respect to their re- sponsiveness to predation can enhance differences in their short-term survival probabilities within a prey pop- ulation. The effects of natural selection in the wild have been demonstrated for numerous traits among a wide variety of plants and animals (Endler 1986). Though predation has been invoked as a selective agent in causing evolutionary changes in many cases, direct selection for behavioral traits has only occasionally been reported in natural populations (but see Fawcett 1984; Dickman 1992). * Permanent address: Department of Hydrobiology, University of Warsaw, Nowy Swiat 67, 00 046 Warsaw, Poland Correspondence to: J. Pijanowska In this study, we investigated the effect of predation on microevolutionary changes within a prey population, based on behavioral traits. We demonstrate the effect of fish predation on genotype frequencies in a laboratory population of the freshwater parthenogenetic cladoceran Daphnia magna Straus. We non-randomly selected two genetically distinct, but morphologically indistinguish- able clones that differed in their past exposure to fish predation. One of them originates from a fishless shallow pond near Warsaw (Poland) and for the past 12 years has not been exposed to any predation in the laboratory (clone W). The second (clone B) originates from the Grol3er Binnensee (Schleswig-Holstein, Germany), a shallow brackish lake inhabited by fish. It has been re- cently reported that clones of another cladoceran, Daph- nia pulex, isolated from ponds inhabited by invertebrate predators showed significantly greater morphological response to the presence of predators than clones from predator-free ponds (Parejko and Dodson 1991). It therefore seemed plausible that clone B, which shared its recent evolutionary history with predators, would be more efficient in terms of anti-predator behavioral de- fence and, as a consequence, would be exterminated at a slower rate. Various defensive behavioral responses to fish predation (e.g. vertical and horizontal distribution patterns, direct escape abilities) have recently been exam- ined in these two clones (Pijanowska et al., unpubl, data), and the predicted differences in their behavior were in- deed found. Among a broad variety of defensive responses by planktonic animals, avoiding surface waters in daytime is recognized as an efficient mechanism that can reduce the risk of predation by visual predators, by using a spatial refuge in deep water during the day (for recent reviews see Lampert 1989, 1993). There is growing em- pirical evidence that this behavior can be induced by chemical compounds released into the environment by a potential predator, without accompanying selection/ mortality (for review see Pijanowska 1993). The com- parison of vertical distribution patterns between the two clones in a system of single, 1-m-long plexiglas tubes i l l umina ted  f rom a b o v e  ( D a w i d o w i c z  1993), u n d e r  s tan-  da rd i zed  cond i t ions  in fish-free wa te r  and  wa te r  con ta in -  ing fish exuda tes  (Loose  et al. 1992) revea led  tha t  these two clones differed r e m a r k a b l y  in thei r  behav io r a l  reac-  t ions to the  chemica l  presence  o f  a p r e d a t o r  (P i j anowska  and  D a w i d o w i c z ,  unpub l ,  da ta) .  In  fish water ,  Daphnia f rom c lone  B showed  a c lear  t endency  to s tay deeper  du r ing  the day ,  whi le  Daphnia f rom c lone  W r e m a i n e d  p e r m a n e n t l y  a t  the surface:  m e a n  day  dep th  o f  c lone B an ima l s  (42.5 _+ 8.9 cm;  mean_+ 1 SD),  differed f rom the m e a n  day  dep th  o f  c lone W (3.7___ 1.2 cm) at  P < 0 . 0 0 0 1  ( M a n n - W h i t n e y  U-test). I t  was shown elsewhere  (Dawi -  dowicz  and  L o o s e  1993; Loose  et al. 1992) tha t  in the  same expe r imen ta l  sys tem Daphnia magna f rom the Bin- nensee can  mig ra t e  even deeper ,  reach ing  the b o t t o m  o f  the tubes.  M e a n  d a y  dep ths  in fish-free wa te r  were 3.8 _+ 0.8 cm and  2.2 + 0.5 cm for  c lones B and  W,  respec-  t ively, and  d id  n o t  differ s ignif icant ly (P i j anowska  and  Dawidowicz ,  unpubl ,  da ta) .  T h o u g h  these clones do  no t  coexis t  in the  wild,  they  offer a sui table  ta rge t  for  shor t -  t e rm select ion by  a fish p r e d a t o r  since they  express  two d is t inc t  c lone-specif ic  behaviors .  41 that for the previous 24 h had contained two fish per 10 1, fed with 100 Daphnia each. Daphnia were fed with a Scenedesmus acutus suspension, at a concentration of 1 mg C 1-1. One hundred in- dividuals of each clone were offered to a single fish (sunbleak, 6.0-7.0 cm total length) in a 4.5-1 glass jar (three replicates per clone). To minimize the inter-individual variation in feeding be- havior, all six fish were starved for 24 h and then, before the ex- periment, fed with 100 Daphnia each. The number of successful attacks was noted during the first 10 min of feeding trials, starting with the first successful attack. The number of survivors was counted after 30 min. Results and discussion Fi sh -med ia t ed  mor ta l i t y  ranged  f rom 56.2 to 83.7% (72.4 + 14.3 % on average,  m e a n  • 1 SD). Regard less  o f  the s t rength o f  p r e d a t o r y  impact ,  the relat ive survival  rate  o f  clone B was up  to 8 t imes more  than  tha t  o f  clone W (Fig.  1). F i sh  caused a r ap id  (within 18 h) and  significant shift  in Daphnia clonal  compos i t ion .  Thus,  the final c lonal  p r o p o r t i o n  ( 8 B : I W )  differed significantly f rom init ial  p r o p o r t i o n  ( 1 B : I W )  at  P < 0 . 0 0 1 ,  (Z 2 goodness  o f  fit). Methods Six cylindrical plastic containers (75 cm high, 50 cm upper diameter, 150 1 capacity) were filled with lake water filtered through a 10-gin filter. Water temperature was 18.1 :t: 0.2 ~ C (mean + 1 SD), and light at the surface ranged from 0.16 to 0.18 g E m  -2 s -1. A plastic mesh-screen (4 mm mesh size) was installed at mid-depth in each container; Daphnia could easily swim through the screen. By re- stricting the movement of fish to the upper layer, we created a bottom refuge for those Daphnia that could avoid predation at the surface by downward migration. In three of the six containers, three fish (sunbleaks, Leucaspius delineatus L., of 6.5 :I: 0.9 cm mean total length) per container were allowed to swim freely for 48 h. They were transferred daily for about 1 h to glass aquaria, and fed with approximately 100 Daphnia per fish. After 48 h, fish were removed and 600 Daphnia (I:1 mixture of clones B and W, mean individual size at the beginning of the experiment 1.324-0.22 mm and 1.31 • 0.21 mm, mean :1:1 SD, respectively) were introduced to each of the six containers, and for the next 48 h, they were allowed to distribute in the water column. Daphnia were fed with a suspension of the green alga Seenedesmus aeutus at a concentration of 1 mg C 1-1, adjusted daily in each of the six containers. After 48 h, a single fish was introduced to each of those three containers which had previously held fish; they were allowed to feed for 18 h (6L:6D :6L). The three control populations were exposed neither to the fish cue nor to predatory pressure, to compare Daphnia distributions with and without fish and to provide an estimate of background mortal- ity not caused by predation. All survivors (at the end of the experiment, mean Daphnia size was 1.56+0.02 mm in clone B, and 1.47:t:0.07 mm in clone W, means :t: 1 SD) in each of the six containers were harvested from above the screen and then counted. After removing the screen, the remaining animals were harwested from below. Final clonal fre- quencies were obtained using cellulose acetate gel electrophoresis (Hebert and Beaton 1989). The glutamate-oxaloacetate transferase (GOT, EC.2.6.1.1) locus served as a diagnostic marker. All sur- vivors in the fish containers and 96 animals per control container from above and from below the screen were assayed separately. In addition to the spatial distribution patterns, we examined the direct escape capability of Daphnia from both clones assuming that a predator would less frequently attack the more evasive prey. Daphnia of each clone (mean size of animals was 1.33 _+0.02 mm in clone B, and 1.42___0.16 for clone W) were exposed for 24 h to water 0.9 0.8 0.7 0.6 i 0 . 4 1 ~  @.5 & 0.3- 0.2- 0.1. ~ O" ~ control fish Fig. 1. The effect of 18 h fish predation on the proportions of two Daphnia clones offered in the same initial numbers at the start of the experiment (means + 95 % CI). Open bars: Daphnia clone B from a lake with fish (Binnensee); shaded bars: Daphnia clone W, which had not been exposed to predation for at least I2 years frequency 0.1 0.2 0.3 0.4 0.6 0,5 0.4 0.3 0 4 0.3 03. 0.1 0 _ 0.2 0,1 O 01 0.2 surface + control Fig. 2. Final vertical distributions of two Daphnia clones after 18 h of fish feeding, shown as surface (above the screen) and bottom (below the screen) fractions of total Daphnia densities in the control and fish treatments (means+ 95% CI). Open bars: clone B; shaded bars: clone W 42 Clone-specific behavior must have affected predator choice [average value of  Manly's a preference index (Man- ly 1974) for clone B, a8 = 0.284 4- 0.116, differed from aw = 0.718 + 0.114 at P <  0.0098, two-sample t-test]. The greater survivorship of  Daphnia from clone B can be ascribed to their strong tendency to remain deeper (below the screen) in the water column (Fig. 2), which was enhanced in the presence of  fish. Experimentally tested short-term survivorship also dif- fered significantly between the two clones (144-5% survivors after 30 min of  fish feeding in clone B compared to 54- 1% in clone W, means+ 1 SD, P <  0.05, two-sample t-test, after correction for unequal variances). Daphnia from clone B showed significantly greater evasiveness when exposed to fish than animals from the same size range from clone W (mean 4- 1 SD number of  successful attacks within the first 10 min of  fish feeding trials was 22 4- 4 for clone B, which differed from 47 4- 7 for clone W at P <  0.01, two-sample t-test). When a predator is forag- ing on clone B animals, it takes it more than twice as long to successfully complete an attack sequence. Thus both, vertical distribution patterns and direct escape capability can confer resistance to fish predators and promote greater survivorship of  clone B animals. The inter-clonal differences in responsiveness to predation via differential avoidance/escape behavior are most probably related to the clones' contrasting ex- perience of  predation in the wild; i.e., Daphnia from clone B which coexist with fish in nature are more re- sponsive to the presence of  fish than animals from clone W. Gliwicz (1986) suggested that there should be a high probability of  extinction of  non-responsive genotypes when they are exposed to a predator.  In the absence of  simultaneous disruptive selection on other characters, natural selection will then result in the reduction of  genetic variance within populations (Endler 1986; Spitze 1991). However,  the outcome of  selection can be reversed within a few generations when high metabolic costs are associated with predator  avoidance. In our study, we measured one important  fitness component ,  i.e., "viabil- ity fitness". The energetic costs of  defense can strongly influence the second constituent of  individual fitness, "reproductive fitness" (Janzen 1981). In the wild, where the coexistence of  responsive and non-responsive ethoty- pes/genotypes has been shown to occur in Daphnia pop- ulations (Weider 1984, 1985; de Meester 1990), ge- notype-specific defensive abilities (modus defendi) and genotype-specific costs of  defence can contribute greatly to the phenomenon of  genotype replacement under selec- tive predation. The maintenance of  genetic variation in prey populations may be to a large extent attributed to differential viability and reproductive fitness of  different ethotypes under changing predation regimes. An obvious next step to further understanding of  the phenomenon of  genotypic replacement under selective predation would be to study the effect of  predatory pressure on a mixture of  behaviorally distinct genotypes isolated from the same population, and estimate inter-genotype differences in fitness components. Acknowledgements. We kindly ackowledge the helpful advises of Carsten Loose at various stages of this study. We thank Eva Geiss- ler and Andreas Heinken for their excellent technical assistance, and anonymous reviewers for their comments on an earlier version of this paper. References Dawidowicz P (1993) Diel vertical migration in Chaoborus flavi- cans: population patterns vs individual tracks. Arch Hydrobiol Beih Erg 39:19-28 Dawidowicz P, Pijanowska J, Ciechomski K (1990) Vertical migra- tion of Chaoborus larvae is induced by the presence of fish. Limnol Oceanogr 35:1631-1637 Dickman CR (1992) Predation and habitat shift in the house mouse, Mus domesticus. Ecology 73:313-322 Elton CS (1927) Animal ecology. Sedgewick & Jackson, London Endler JA (1986) Natural selection in the wild. Princeton University Press, Princeton Gliwicz ZM (1986) Predation and the evolution of vertical migra- tion behaviour in zooplankton. Nature 320:746-748 Fawcett MH (1984) Local and latitudinal variation in predation on an herbivorous marine snail. Ecology 65:1214-1230 Janzen DH (1981) Evolutionary ecology of personal defence. In: Townsend CR, Calow P (eds) Physiological ecology: an evolu- tionary approach to resource use. Sinauer, pp 145-164 Hebert PDN, Beaton MJ (1989) Methodologies for allozyme elec- trophoresis using cellulose acetate electrophoresis: a practical handbook. Helena Laboratories, Beaumont Lampert W (1989) The adaptive significance of diel vertical migra- tion of zooplankton. Funct Ecol 3: 21-27 Lampert W (1992) Ultimate causes of diel vertical migration of zooplankton: new evidence for the predator avoidance hypoth- esis. Arch Hydrobiol Beih Erg 39:79-88 Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68: 619-640 Loose C J, Elert E von, Dawidowicz P (1992) Chemically-induced diel vertical migration in Daphnia: a new bioassay for kairo- mones exuded by fish. Arch Hydrobiol 126:329-337 Manly BFJ (1974) A model for certain types of selection experi- ments. Biometrics 30:281-294 Meester L de (1990) Evidence for intra-population genetic variabil- ity for phototactic behavior in Daphnia magna Straus., 1820. Biol Jaarb Dodonaea 58:84-93 Parejko K, Dodson SI (1991) The evolutionary ecology of an antipredator reaction norm: Daphnia pulex and Chaoborus americanus. Evolution 45: 1665-1674 Pijanowska J (1993) Diel vertical migration in zooplankton: fixed or inducible behavior? Arch Hydrobiol Beih Erg 39:89-97 Sih A (1987) Predators and prey lifestyles: an evolutionary and ecological overview. In: Kerfoot WC, Sih A (eds) Predation: direct and indirect impacts on aquatic communities, University Press of New England, pp 203-224 Spitze K (1991) Chaoborus predation and life-history evolution in Daphnia pulex: temporal pattern of population diversity, fitness and mean life history. Evolution 45:82-92 Welder LW (1984) Spatial heterogeneity of Daphnia genotypes: Vertical migration and habitat partitioning. Limnol Oceanogr 29: 225-235 Weider LW (1985) Spatial and temporal genetic heterogeneity in a natural Daphnia population. J Plankt Res 7:101-123 

Predator-mediated genotypic shifts in a prey population: experimental evidence

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Predator-mediated genotypic shifts in a prey population: experimental evidence

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