Growth rate and retention of learned predator cues by juvenile rainbow trout: faster-growing fish forget sooner

Abstract

Under conditions of spatial and/or temporal variability in predation risk, prey 19 organisms often rely on acquired predator recognition to balance the trade-offs between 20 energy intake and risk avoidance. The question of 'for how long' should prey retain this 21 learned information is poorly understood. Here, we test the hypothesis that the growth 22 rate experienced by prey should influence the length of the 'memory window'. In a 23 series of laboratory experiments, we manipulated growth rate of juvenile rainbow trout 24 and conditioned them to recognize a novel predator cue. We subsequently tested for 25 learned recognition either 24 hours or 8 days post-conditioning. Our results suggest that 26 trout with high versus low growth rates did not differ in their response to learned predator 27 cues when tested 24 hours post-conditioning. However, trout on a high growth rate 28 exhibited no response to the predator cues after 8 days (i.e., did not retain the recognition 29 of the predator odour), whereas trout on a lower growth rate retained a strong recognition 30 of the predator. Trout that differed in their growth rate only after conditioning did not 31 differ in their patterns of retention, demonstrating growth rate after learning does not 32 influence retention. Trout of different initial sizes fed a similar diet (% body mass.day -1 ) 33 showed no difference in retention of the predator cue. Together, these data suggest that 34 growth rate at the time of conditioning determines the 'memory window' of trout. The 35 implications for threat-sensitive predator avoidance models are described. 36 37 38 However, simply responding to any local threat may not represent an optimal strategy 42 (Lima and Dill 1990), as predation pressure is known to be spatially and temporally 43 variable (Griffin 2004; Lima and Steury 2005; Ferrari et al. 2009). A wide variety of 44 taxonomically diverse prey species rely, therefore, on associative learning (acquired 45 predator recognition) to assess the risk associated with potential predators (Brown 2003; 46 Griffin 2004). Learned, versus 'innate', predator recognition allows prey to make 47 dynamic adjustments to predation threats, and to balance the conflicting pressures of 48 predator avoidance and energy intake (i.e., threat-sensitive learning; Ferrari et al. 2005; 49 Ferrari and Chivers 2006; Gonzalo et al. 2010). Within aquatic ecosystems, such predator 50 recognition learning is often facilitated through the pairing of damage released chemical 51 alarm cues (Chivers and Smith 1998) with the sight or smell of a novel predator (Brown 52 2003). Acquired predator recognition has been shown to increase probability of survival 53 during staged encounters with live predators (Mirza and Chivers 2000; Darwish et al. 54 2005; Eiben and Persons 2007; Shier and Owings 2007). 55Given that predation is indeed variable, a relevant, yet poorly understood question 56 is how long should prey exhibit (i.e., retain) an overt response to acquired information? 57 Following a single pairing of a...

Learning about Danger: Chemical Alarm Cues and Threat‐Sensitive Assessment of Predation Risk by Fishes

“…Slower growth rates, simple life histories or a lack of morphological defences should increase the value of learned information, and hence extend the length of the memory window. Brown et al (2011b) directly tested this model by manipulating the growth rate of juvenile rainbow trout and testing for the retention of the learned recognition of pumpkinseed odour. Trout were fed either high or low food rations for a period of 7 days (sufficient to induce different growth rates) and then conditioned to recognise the odour of pumpkinseed as a threat.…”

“…Small (∼0.6 g) and large (∼1.8 g) trout exhibited similar responses when tested for recognition on both testing days, suggesting that retention of learned recognition is not influenced by absolute size. Modified from Brown et al (2011b). suggest that growth rate does indeed influence the length of the memory window. A likely proximate mechanism in this case might be that increased growth rates result in increased energy demands, resulting in a shift in threat-sensitive trade-offs in favour of risk-prone behavioural tactics in the case of high growth rate trout.…”

Learn and live: predator experience and feeding history determines prey behaviour and survival

“…Classic examples of this behaviour are shown by ants and sticklebacks that prefer a profitable but more risky food patch when hungry and a less profitable but safe patch when satiated [11,12]. Feeding history also influences memory of a predator encounter [13] and a prey's ability to evade a predatory attack [14].…”

Retention of learned predator recognition in an endangered sucker Chasmistes liorus liorus

“…As discussed above, there may have been a low perceived risk conveyed by the stimuli used to condition the sucker. Additionally, the hatchery environment is typically designed to maximize growth rate (Johnsson et al 1996), which is negatively associated with the length of memory retention (Brown et al 2011b(Brown et al , 2013. Consequently, the rearing environment of captively propagated fishes may result in a predisposition to forget predator cues more quickly.…”

“…There would be a variety of odors present at any given time in addition to the predator odor and alarm cue (Ferrari et al 2010c). Additionally, many fish predators are gape limited, and prey can outgrow their vulnerability to these predators (Brown et al 2011b(Brown et al , 2013). In their model of 'adaptive forgetting ', Ferrari et al (2010a) proposed that it would not be advantageous to form a permanent association between every odor present and danger after a single exposure to a conspecific alarm cue.…”