Abstract. 1. Walnut‐infesting flies in the Rhagoletis suavis species group actively re‐use hosts for oviposition despite engaging in a genus‐typical host‐marking behaviour which, in other Rhagoletis groups, deters oviposition. In a study of the walnut fly, R. juglandis (Cresson), alternative hypotheses for the putative marking behaviour were evaluated.
2. The oviposition site attraction hypothesis proposes that the host mark guides females to oviposition sites on occupied fruit. The competition intensity signal hypothesis proposes that the host mark is an indicator of the level of competition to be incurred if fruit are re‐used.
3. In a field cage, females were presented simultaneously with fruit previously exposed to 25 females that were also allowed to oviposit and engage in the putative marking behaviour, and control fruit on which females were allowed only to oviposit. The occurrence of host marking reduced a female's propensity to oviposit from 46% to just over 10%, consistent with the competition intensity signal hypothesis only.
4. In a laboratory assay, the duration of host marking was correlated positively with the size of a female's clutch. This result, also consistent with the competition intensity signal hypothesis, suggests that the amount of marking pheromone on a fruit is a reliable indicator of the number of eggs already deposited within.
5. In a second field‐cage experiment, females were allowed to mark on fruit for 0, 10, 20, or 30 min and fruit were presented to test females. Whether or not females alighted on a particular host was not affected by the duration of marking; however, the frequency of both ovipositor probing and egg deposition decreased with increasing duration of marking. Consistent with the competition intensity signal hypothesis, this result suggests that the host mark permits females to assess the level of competition that a clutch will incur within re‐used fruit.