Mutualisms are often subject to perturbations by parasitism arising from third‐party interactions. How third‐party perturbations are dampened is a fundamental question pertaining to mutualism stability. Phoretic organisms that turn parasitic within a mutualism may destabilize it. If the fitness cost of such phoresy is high, then density‐dependent effects could be one mechanism to stabilize these interactions. We experimentally examined the fitness effects of a phoretic nematode community on a brood‐site pollination mutualism involving a pollinating fig wasp (the vehicle) and its associated fig species (the host for wasp and nematode development). We comprehensively investigated fitness impacts of phoresy on wasp lifespan, lifetime reproductive success, dispersal ability and predation risk as well as on host brood‐site volume and seed number. We employed a range of hitchhiker densities that encompassed natural and overloading levels for two nematode taxa (one plant‐ and one animal‐parasitic type). None of the plant host and vehicle fitness parameters were affected by wasps with low nematode transportation loads for either type of nematode. Furthermore, wasps arriving at their destinations carried lower densities of both animal‐ and plant‐parasitic nematodes compared to dispersing wasps, suggesting that there is selection on hitchhiker numbers during the dispersal process and that wasps loaded with a greater density of nematodes do not successfully disperse. Overloaded wasps had shorter flight durations, suggesting limited dispersal ability; on arrival at their destination, they suffered greater predation risk. Such overloaded wasps delivered impaired pollination services and produced fewer offspring resulting in lower lifetime fitness. Therefore, the direct and indirect effects of nematodes on their vehicles are strong. These effects also translated into impacts on host plant fitness, with the overloaded pollinators promoting the development of smaller brood sites with fewer seeds, thus reducing fig tree reproductive success. The effects of the animal parasites were greater than that of the plant parasite in this study. The third‐party interaction is therefore self‐limited and exhibits density dependence. The strong negative effects of overloading likely explain the low number of nematodes found in nature on dispersing and arriving fig wasps. Consequently, parasitic hitchhikers are unlikely to destabilize the mutualism. A free Plain Language Summary can be found within the Supporting Information of this article.

Hitchhikers (phoretic organisms) identify their vehicles using species‐specific visual, chemical and vibrational cues. However, what factors influence their choice between vehicles of the same species has rarely been investigated. Hitchhikers must not only avoid overcrowded vehicles but may also need to travel with conspecifics to ensure mates at their destination. Hence, a trade‐off between overcrowding and presence of conspecifics likely determines the choice of a vehicle especially when destination sites are distant, ephemeral and unique. Here, we investigate whether a trade‐off between the presence of conspecifics versus overcrowding by conspecifics or heterospecifics on a vehicle affects hitchhiker choice. We also investigate the sensory modality responsible for this choice. We experimentally examine these questions using a phoretic nematode community (containing plant‐ and animal‐parasitic taxa) obligately associated with a brood‐site pollination mutualism. In this model system, nematodes co‐travel with conspecifics and heterospecifics on pollinators as vehicles, between ephemeral plant brood sites to complete their developmental life cycle. In this system, hitchhiker overcrowding has proven negative impacts on vehicle and plant fitness. We expected nematodes to respond to conspecifics and heterospecific density on offered vehicles when making their choice. We found that animal‐parasitic nematodes preferred vehicles containing some conspecifics within a certain density range. However, plant‐parasitic nematodes preferentially boarded vehicles that were devoid of conspecifics or had few conspecifics. Plant parasites that preferred empty vehicles likely hitchhiked in pairs. Both nematode types employed volatile cues to discriminate between vehicles with different conspecific nematode densities. Our results suggest that vehicle overcrowding by conspecifics, most likely, guaranteed access to mates at the destination determined hitchhiker choice. Surprisingly, and contrary to our expectations, plant‐ and animal‐parasitic nematodes did not respond to heterospecific crowding on vehicles and did not discriminate between vehicles with different heterospecific nematode densities. The reason for this lack of response to heterospecific presence is unknown. This study not only shows that phoretic organisms use different strategies while choosing a vehicle but also confirms that density‐dependent effects can ensure the stability and persistence of phoretic interactions in a mutualism by balancing overcrowding against reproductive assurance.

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Ficus racemosa with an Indo Australasian distribution has so far been recorded to harbour in its fruits, nematode species of the aphelenchoid genera Schistonchus, Ficophagus and Martininema, and species of diplogastrid genera Teratodiplogaster and Pristionchus. The Indian species reported so far from Ficus racemosa lack comprehensive details on morphology and molecular characterization. In this paper, we describe, three new species of nematodes obtained from syconia (enclosed globular infructescence or fruit) of Ficus racemosa found in southern India. Ficophagus glomerata n. sp. is characterised by a small body having b=5.2-9.6, c= 18-23; slightly set-off lip region having well developed cephalic framework; secretory-excretory pore opens near the head; slender stylet with small, rounded/ sloping knobs; ovoid median bulb with relatively posteriorly-placed valve plates; males with sickle-shaped spicules having spatulate or hammer-shaped capitulum, represented by an elongate-ovoid condylus and long digitate rostrum and tail conoid with fine, hair-like terminal spike. Teratodiplogaster glomerata n. sp. is characterised by long tubular and narrow stoma with fractal pieces in prostegostom; long rectangular metacorpus; female reproductive system with conspicuous spermatheca and amoeboid sperms; males having short, arcuate spicules and keeled gubernaculum; genital papillae in the configuration of P1, P2, C, P3, P4, P5d, (P6d, P7), P8d, Ph and tail conoid with a terminal or subterminal mucro. Pristionchus glomerata n. sp. is characterised by four morphotypes mainly with variations in lip region, stoma, spicules, gubernaculum, and the position of genital papillae. Phylogenetic analyses based upon near-full-length small subunit (SSU) and D2-D3 expansion segments of large subunit (LSU) rRNA genes confirmed affinities with sister species of corresponding genera.