What limits predation rates by the specialist seed‐feeder Penthobruchus germaini on an invasive shrub?

Abstract

Summary1. Specialist seed-feeders are widely used in weed biological control, but seed predation rates are frequently insufficient to cause the required impacts. Understanding the underlying reasons is prerequisite to predicting efficacy. 2. We conducted continental-scale surveys of an introduced, multi-voltine seed-feeder [Bruchidae: Penthobruchus germaini (Pic.)] on an invasive legume (Caesalpinaceae: Parkinsonia aculeata L.). We tested three hypotheses as to what limits seed predation; namely, seed escape through egg aggregation, mortality of immature beetle stages, and failure to track temporal fluctuations in resource availability. We also tested how these factors interacted with the environment and each other. 3. Mean seed predation was relatively low (2-30%), despite mean egg densities of between 0·55 and 3·2 eggs per seed. Eggs were slightly aggregated (negative binomial, k = 1·87). Unexplained egg mortality (6-44%), egg parasitism (10-70%) and larval/pupal mortality (62%) were high, but egg parasitism was the only mortality factor that was density-dependent and that varied across climatic regions. Egg densities responded poorly to rapid within-season increases in seed availability. 4. All examined factors dampened seed predation rates. However, we developed a deterministic mathematical model which showed that seed predation would still have been relatively low (5-56%) at the observed egg densities, even without direct effects of immature beetle mortality. Also, to achieve a benchmark seed predation rate of 80%, egg densities would need to be over 8·5 eggs per seed with no parasitism, and an unrealistically high 27·8 at 70% parasitism. Available data suggest that seed predation by specialist seed-feeders will often be constrained by one or more of the factors we identified. 5. Synthesis and applications . Selecting effective biological control agents is an important challenge for weed biocontrol. Our results suggest that many seed-feeders will not regulate plant populations, but that predictions of their efficacy can be greatly improved by quantifying the way eggs are distributed across seeds and the various mortality factors that affect immature beetle stages. The ability of seed-feeders to track resource fluctuations may also be predictable. For example, multivoltine insects appear better at tracking between-season and between-site variation in resource availability than sharp changes in within-season availability.

Oviposition pattern and within-season spatial and temporal variation of pre-dispersal seed predation in a population of Mimosa bimucronata trees

“…The ability to track within-season fruiting phenology is vital for these seed predators (van Klinken 2005;Raghu et al 2005;van Klinken and Flack 2008), especially in cases where resources are available for oviposition and larval growth over only a short period. Bruchines such as Bruchidius villosus feed on pollen, reaching reproductive maturity in time to oviposit on immature fruits; this life history strategy synchronises the seed beetle with its host plant (Harman 1999).…”

“…Variation in seed predation rates can also be caused by the degree of synchronisation between the life stages of the seed predator and host plant phenology. For weed biological control practice, for example, this synchronisation is extremely important for successful establishment of the seed predator in new environments, and also for maximising its impact on the target plants (Harman 1999;van Klinken and Flack 2008).…”

The role of pre- and post-dispersal seed predation in determining total seed loss

“…Total seed predation rates, even when considering the contribution of predation in all seed stages, was in the commonly-recorded range for seed predators (Kolb et al 2007;Ramírez & Traveset 2010) and is therefore less than is generally considered necessary to significantly reduce population growth rates (Kolb et al 2007;van Klinken et al 2008). Furthermore, most seed predation estimates, including ours, are likely to be maximal estimates as they are generally made at seed sinks, such as under or immediately adjacent to parent trees.…”

“…Furthermore, we demonstrate the importance of both seed dynamics and oviposition behaviour in determining total seed predation levels. Different systems will have contrasting seed dynamics (Baes et al 2001;Raghu et al 2005) and oviposition preferences (Johnson 1981;van Klinken & Flack 2008). Total seed predation rates will therefore ultimately be determined by the interaction between host species, seed predator and environment (Kauffman & Maron 2006), but can be estimated through time by individually tracking seed density and predation rates for the major seed stages.…”

“…Univoltine insects, that pass through a single generation a year, can be well synchronised with typically observed seasonal peaks in seed production (Crawley 1992). In contrast, multivoltine insects, that pass through multiple generations a year, are less able to track sharp seasonal fluctuations in pre-dispersal host resources (Raghu, Wiltshire, & Dhileepan 2005;van Klinken et al 2008). However, this can potentially be overcome if they continue exploiting more persistent post-dispersal seed stages (Johnson 1981;Lewis & Gripenberg 2008;van Klinken & Flack 2008;van Klinken & White 2011).…”