Proportional fitness loss and the timing of defensive investment: a cohesive framework across animals and plants

Abstract

The risk of consumption is a pervasive aspect of ecology and recent work has focused on synthesis of consumer–resource interactions (e.g., enemy–victim ecology). Despite this, theories pertaining to the timing and magnitude of defenses in animals and plants have largely developed independently. However, both animals and plants share the common dilemma of uncertainty of attack, can gather information from the environment to predict future attacks and alter their defensive investment accordingly. Here, we present a novel, unifying framework based on the way an organism’s ability to defend itself during an attack can shape their pre-attack investment in defense. This framework provides a useful perspective on the nature of information use and variation in defensive investment across the sequence of attack-related events, both within and among species. It predicts that organisms with greater proportional fitness loss if attacked will gather and respond to risk information earlier in the attack sequence, while those that have lower proportional fitness loss may wait until attack is underway. This framework offers a common platform to compare and discuss consumer effects and provides novel insights into the way risk information can propagate through populations, communities, and ecosystems.

Box. 1: Proportional fitness loss of an individual and its timing of defense

We suggest the proportional fitness loss (PFL) if an individual does not initiate defense until attacked is a critical component of understanding its defensive investment. PFL relies on an individual’s fitness potential if it initiates defense prior to an attack compared to its fitness potential if it initiates defense during an attack. For example, individual A is 50% likely to survive if it defends during the detection stage and only 20% likely to survive if it defends during an attack, its PFL is 60% ((50−20)/50). Individual B has a 95% chance of surviving if it defends during the detection stage and a 30% chance of survival, if it defends during an attack, its PFL is 68%. From this scenario, it becomes clear that the PFL of an individual depends on both its ability to survive an attack and, also, the effectiveness of its early defense. In such a scenario, individual B has a higher PFL and should initiate defense earlier than individual A, even though it has a higher probability of surviving an attack. Our concept helps to clarify why individuals with low expected fitness, regardless of whether they initiate defense early or late (thus a low PFL), would be expected to wait and initiate defense late (if at all) given the ineffectiveness of their (early) defense.

The fact that consumer-resource encounters progress through time along a common interaction sequence of events (Lima and Dill 1990; Karban and Baldwin 1997, Caro 2005; Fig. 1) allows us to build relative PFL curves across the interaction sequence to better understand the timing of defensive investment. As individuals delay their defensive investment, their fitness potential will approach that which they would have if they did not invest in defense until attacked. This also allows us to visualize inflection points where fitness potential will greatly decrease if defense is not initiated. In the first two examples above, the fitness potential difference between early and late defensive investment is relatively large and, if their PFL curve was relatively linear, both individuals may greatly increase their survival for incremental advances in the timing of their defense. Alternatively, if, for example, we extend the above scenario such that individual A had a 95% chance of survival if it defended during the encounter stage (thus a PFL of 79% between encounter and attack, but a 47% PFL between encounter and detection), while individual B had a 99.9% chance of survival if it defended during the encounter stage (thus a PFL of 70%, but only 4% PFL between encounter and detection), our curve would predict that individual A would most benefit from defending during the encounter stage, while individual B may benefit from delaying defensive investment until the detection stage.

Additionally, if individuals invest too early or respond to unreliable information they will pay a cost of unnecessary defense (e.g., cost of defense itself, missed opportunity costs, reductions in growth and reproduction). The willingness of individuals to pay a cost of unnecessary defense will also depend on their PFL. Individuals with a high PFL can pay a relatively high cost of unnecessary defense and still benefit significantly from early defensive investment. Alternatively, individuals with a low PFL if attacked may not be willing to pay as high a cost of unnecessary defense and should defend relatively later.

While we discuss the fitness aspect of PFL as a loss of survival, individual fitness could also be measured as a loss of reproduction (number of babies born or weaned, loss of litters, loss of seed set or flowers, etc.) or a loss of growth or tissue (in many species growth is directly related to reproductive potential and in the case of plants or other organisms that can be partially consumed a loss of tissue may be a better metric) if attacked. It is important to appreciate that in these latter two fitness measures, with respect to PFL, the loss of fitness is due to attack not the initiation of defense (as is often the case). Because of this, however, these latter two fitness measures may be particularly insightful given (i) they can be used to estimate PFL if attacked, but also the cost of unnecessary defense (defending too early) and (ii) that they can be used to estimate the loss of relative fitness at any point along the interaction sequence when defense is initiated. Understanding an individual’s PFL across the interaction sequence will provide valuable insights into when it should initiate defense and has significant implications for understanding how prey and plants will respond to the risk of consumption.