Behavior is a crucial component of ecology that mediates how animals interact with one another and with the environment. Behaviors can allow animals to avoid the harmful effects of things like competition, predation, and extreme abiotic conditions. However, animals often have constraints that limit the potential benefits of their behaviors, so we addressed what factors contribute to these constraints in plant-aphid-wasp systems. Parasitoids of aphids are tiny wasps that lay their eggs in aphids, where the larva feeds and develops. Each aphid can only sustain a single parasitoid, so parasitoids mark aphids when they lay an egg to discourage others from laying additional eggs. Not all parasitoids mark aphids the same way, and whether species with different marks can recognize one another’s mark was unclear. We found that parasitoids with different marks fail to respond to one another’s marks. Because these parasitoids laid eggs in aphids that were already parasitized, competition between them will occur through mortal combat between the larvae rather than egg-laying restraint in the adults. Parasitoid attack induces aphid behaviors such as fighting, running away, or dropping off the host plant. These behaviors can deter or evade the attacker, but they cost the aphid an opportunity to feed. This feeding interruption decreases the number of offspring the aphids produce. When aphids run from a threat, they usually resettle on the newest leaves of a plant, where their reproduction is enhanced. However, when they drop from a plant to escape, they resettle randomly and do not benefit from the better location, indicating that more vigorous responses can lose benefits. We also showed that aphids exhibit similar movement and resettling behaviors when disturbed by heat shocks. However, this behavior did not affect aphid reproduction or survival when induced by a heat shock. While movement to new leaves appears to be a general response to several disturbances, its benefits to aphids only occur in specific situations. We have shown that behaviors can be constrained by unfamiliar stimuli and the general context in which they are invoked. These constraints can dictate how insects interact with each other and the environment.