Infective prey leads to a partial role reversal in a predator-prey interaction

Abstract

An infective prey has the potential to infect, kill and consume its predator. Such a prey-predator relationship fundamentally differs from the predator-prey interaction because the prey can directly profit from the predator as a growth resource. Here we present a population dynamics model of partial role reversal in the predator-prey interaction of two species, the bottom dwelling marine deposit feeder sea cucumber Apostichopus japonicus and an important food source for the sea cucumber but potentially infective bacterium Vibrio splendidus. We analyse the effects of different parameters, e.g. infectivity and grazing rate, on the population sizes. We show that relative population sizes of the sea cucumber and V. Splendidus may switch with increasing infectivity. We also show that in the partial role reversal interaction the infective prey may benefit from the presence of the predator such that the population size may exceed the value of the carrying capacity of the prey in the absence of the predator. We also analysed the conditions for species extinction. The extinction of the prey, V. splendidus, may occur when its growth rate is low, or in the absence of infectivity. The extinction of the predator, A. japonicus, may follow if either the infectivity of the prey is high or a moderately infective prey is abundant. We conclude that partial role reversal is an undervalued subject in predator-prey studies.

Fig 1. A schematic presentation of the predator-infective prey model.

The predator (S), A. japonicus, is a bottom feeder (i). An essential part of the detritus hosts the parasite V. splendidus (C). Both A. japonicus and V. splendidus are generalists (vi, vii) such that they are able to survive in the absence of the other species. V. splendidus infects A. japonicus (I, ii). The disease mortality of A. Japonicus enhances the growth of the V. splendidus (v). A fraction of the infected A. japonicus recovers from the infection (iii). Both the healthy (S) and infected (I) hosts die naturally (iv).

Fig 2. Infectivity affects both prey and predator population sizes.

(A) and (B) The population size of the prey and predators, respectively. (C) A closer view to the switch points (o, Δ) in the predator population. Red, purple and blue lines represent fast (r_C = 50), medium (r_C = 5) and slow (r_C = 0.5) growth rates. The predator’s grazing rate g = 3.0·10⁻⁴ and the infective proportion of the prey α = 0.001.

Fig 3. Proportion of infective prey α affects the population in the same way as infectivity e_SI.

(A) Slowly growing prey with low infectivity can proliferate only if the majority of the prey are infective. (B) Even high proportions of infective prey cause only a slight decrease in predator population. High infectivity e_SI prevents the extinction of the prey. (C) Highly infective prey thrives best when it forms relatively small part of the prey population because (D) the predator becomes extinct if the majority of the prey are infective (α≳0.4). Red, purple and blue lines are fast (r_C = 50), medium (r_C = 5) and slow (r_C = 0.5) growth rates. Infectivity values are e_SI = 10⁻¹³ in subfigures A and B, and e_SI = 10⁻¹¹ in subfigures C and D.

Fig 4. An increase in the infectivity may reverse the effect of predator grazing rate on the predator population size.

(A) and (B) The prey’s infectivity e_SI is low. Increasing the predator grazing rate g decreases prey and increases predator population sizes. (C) and (D) In contrast, if e_SI is slightly greater, then increasing grazing rate decreases the population levels of the prey as well as of the predator. Red, purple and blue lines are fast (r_C = 50), medium (r_C = 5) and slow (r_C = 0.5) growth rates. The infectivity values are e_SI = 10⁻¹³ in subfigures A and B, and e_SI = 10⁻¹⁰ in subfigures C and D.

Fig 5. Predator grazing rate g affects the extinction of prey.

Extinction of prey is possible if the predator’s grazing rate g is higher than the threshold defined by the prey’s growth rate. If the prey’s infectivity e_SI is high, only a small fraction α of the prey population needs to be infective to escape the extinction. Prey growth rate is r_C = 10.

Fig 6. The eradication of the predator by the prey is possible above the lines defining the fraction α of the infective prey.

If the infective prey forms a small fraction α of the available prey population, the high prey infectivity e_SI and predator grazing rate g are needed to eradicate the predator. To the contrary, if the infective fraction α is large a low infectivity e_SI or a low grazing rate g is needed for the predator to prevail. Using the parameters for A. japonicus and V. splendidus the predator survives always if α<0.011. At very low grazing rate or infectivity the predator does not consume enough infective prey to suffer extinction. Prey growth rate is r_C = 10.