skip to main content


Title: Bluehead chub Nocomis leptocephalus hosts exploit selfish‐herd benefits from their heterospecific nest associates
Abstract

Prey species often congregate in groups to detect and evade predators, yet not all group members benefit equally. We observed the nesting aggregations of bluehead chub (Nocomis leptocephalus), where one nest “hosts” as many as several hundred “nest associates.” We predicted that the male chub exploits the aggregation in a manner consistent with selfish‐herd theory – specifically, by locating itself in the safest location within the aggregation (the centre) and using the aggregation to reduce its own vigilance requirements.

Vigilance was measured as the time it took the host (male) chub, first chub female and first individual of each associate species to return to the nest under differing associate abundances (hypothesised to be inversely related to risk) following a simulated predator scare. Spatial position was investigated by digitising host movement and overlaying it with the aggregation and nest's spawning pit area.

We used information theoretic statistics to analyse the effect of aggregation characteristics on the return time of chub and their nest associates. The best‐supported model included both species composition and abundance (inverse of risk) as predictors of return time. Hosts returned last under nearly all scenarios and the aggregation as a whole took longest to return in high‐risk environments. The 95% and 99% confidence ellipses of host spatial position contained the centroids of the aggregation and spawning pits, respectively, for all nests analysed (n = 11).

We conclude that the host locates itself at the centre of both the aggregation and the spawning pit area of the nest, and that the host uses the aggregation to reduce its own vigilance requirements. These results support our hypothesis that hosts use their nest associates to disproportionately decrease their risk of predation during spawning.

This is the first study to show any mixed‐species fish spawning aggregation as a selfish shoal, and to identify bluehead chub as a selfish participant in the mutualistic reproductive interactions that they host.

 
more » « less
NSF-PAR ID:
10491024
Author(s) / Creator(s):
 ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Freshwater Biology
Volume:
69
Issue:
3
ISSN:
0046-5070
Format(s):
Medium: X Size: p. 450-459
Size(s):
["p. 450-459"]
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    The development of encompassing general models of ecology is precluded by underrepresentation of certain taxa and systems. Models predicting context‐dependent outcomes of biotic interactions have been tested using plants and bacteria, but their applicability to higher taxa is largely unknown.

    We examined context dependency in a reproductive mutualism between two stream fish species: mound nest‐building bluehead chubNocomis leptocephalusand mountain redbelly daceChrosomus oreas, which often usesN. leptocephalusnests for spawning. We hypothesized that increased predator density and decreased substrate availability would increase the propensity ofC. oreasto associate withN. leptocephalusand decrease reproductive success of both species.

    In a large‐scale in situ experiment, we manipulated egg predator density and presence of both symbionts (biotic context), and replicated the experiment in habitats containing high‐ and low‐quality spawning substrate (abiotic context).

    Contradictory to our first hypothesis, we observed thatC. oreasdid not spawn without its host. The interaction outcome switched from commensalistic to mutualistic with changing abiotic and biotic contexts, although the net outcome was mutualistic.

    The results of this study yielded novel insight into how context dependency operates in vertebrate mutualisms. Although the dilution effect provided byC. oreaspositively influenced reproductive success ofN. leptocephalus, it was not enough to overcome both egg predation and poor spawning habitat quality. Outcomes of the interaction may be ultimately determined by associate density. Studies of context dependency in vertebrate systems require detailed knowledge of species life‐history traits.

     
    more » « less
  2. Parental investment by solitary nest‐building wasps and bees is predicted to be plastic, responding to variation in the sex of the offspring, the availability of food used as provisions (‘resource limitation’), the female's inventory of mature oocytes (‘egg limitation’), and risk imposed by nest parasites.

    I observed nest provisioning byAmmophila dysmica, a solitary, ground‐nesting wasp that provisions its nest with one or two caterpillar prey to evaluate the hypotheses that provisioning is shaped by caterpillar size, offspring sex, the hunting time required to capture prey, a female's egg load, and penetration of nests by the parasitesArgochrysis armillaandHilarella hilarella.

    Ammophila dysmicawere more likely to add a second provision to the nest when the first prey item was relatively small and when provisioning daughters.

    Neither the hunting time required to capture the first caterpillar prey nor the female's inventory of oocytes predicted a female's likelihood of adding a second caterpillar to a nest. Variation in oocyte inventory across females was minimal; all females examined had a mature or nearly mature oocyte remaining in the ovaries immediately after laying an egg.

    Ammophila dysmicawere much less likely to add a second caterpillar to nests that were penetrated by parasites during the first provisioning.

    Although many nest parasites have evolved adaptations to avoid detection by their hosts, oviposition byA. armillaoften appears to reveal its presence, eliciting an abrupt truncation of investment by the host in that nest.

     
    more » « less
  3. Abstract

    Acacia‐ant mutualists in the genusPseudomyrmexnest obligately in acacia plants and, as we show through stable isotope analysis, feed at a remarkably low trophic level. Insects with diets such as these sometimes depend on bacterial symbionts for nutritional enrichment. We, therefore, examine the bacterial communities associated with acacia‐ants in order to determine whether they host bacterial partners likely to contribute to their nutrition. Despite large differences in trophic position, acacia‐ants and related species with generalized diets do not host distinct bacterial taxa. However, we find that a small number of previously undescribed bacterial taxa do differ in relative abundance between acacia‐ants and generalists, including several Acetobacteraceae and Nocardiaceae lineages related to common insect associates. Comparisons with an herbivorous generalist, a parasite that feeds on acacias and a mutualistic species with a generalized diet show that trophic level is likely responsible for these small differences in bacterial community structure. While we did not experimentally test for a nutritional benefit to hosts of these bacterial lineages, metagenomic analysis reveals aBartonellarelative with an intact nitrogen‐recycling pathway widespread acrossPseudomyrmexmutualists and generalists. This taxon may be contributing to nitrogen enrichment of its ant hosts through urease activity and, concordant with an obligately host‐associated lifestyle, appears to be experiencing genomewide relaxed selection. The lack of distinctiveness in bacterial communities across trophic level in this group of ants shows a remarkable ability to adjust to varied diets, possibly with assistance from these diverse ant‐specific bacterial lineages.

     
    more » « less
  4. Abstract

    Introduced hosts are capable of introducing parasite species and altering the abundance of parasites that are already present in native hosts, but few studies have compared the tolerances of native and invasive hosts to introduced parasites or identified the traits of introduced hosts that make them supershedders of non‐native parasites.

    Here, we compare the effects of a nematodeAplectana hamatospiculathat is native to Cuba but appears to be introduced to Florida on the native Floridian treefrog,Hyla femoralis, and on the Cuban treefrog (CTF),Osteopilus septentrionalis. We were particularly interested in CTFs because their introduction to Florida has led to reported declines of native treefrogs.

    In the laboratory, infection withA. hamatospiculacaused a greater loss in body mass ofH. femoralisthan CTFs despiteH. femoralisshedding fewer total worms in their faeces than CTFs. Field collections of CTFs,H. femoralis, and another native Floridian treefrog,H.squirella(Squirrel treefrog) from Tampa, FL also showed that CTFs shed more larval worms in their faeces than both native frogs when controlling for body size. Hence, the non‐native CTF is a supershedder of this non‐native parasite that is spilling over to less tolerant native treefrogs.

    Any conservation intervention to reduce the effects of CTFs on native treefrogs would benefit from knowing the traits that contribute to the invasive host being a supershedder of this parasite. Hence, we conducted necropsies on 330 CTFs to determine how host sex and body size affect the abundance ofA. hamatospicula, and two other common parasites in this species (acuariid nematodes and trematode metacercariae).

    There was a significant linear increase inA. hamatospiculaand encysted acuariids with CTF body size, but there was no detectable relationship between host body size and the intensity of metacercariae. Female CTFs were bigger, lived longer and, on average, had moreA. hamatospiculathan male CTFs.

    Synthesis and applications. These results of the study suggest that there is parasite spillover from the invasive Cuban treefrog (CTF) to native treefrogs in Florida. Additionally, at least some of the adverse effects of CTFs on native treefrogs could be caused by the introduction and amplification of this introduced parasite, and female and larger CTFs seem to be amplifying these infections more than males and smaller CTFs, respectively, suggesting that management could benefit from targeting these individuals.

     
    more » « less
  5. Abstract

    The seeds of many plant species produce mucilage on their surfaces that when wetted and dried, firmly adheres seeds to surfaces and substrates. Previous studies have demonstrated that seed anchorage to the ground can reduce seed predation, although only a few species have thus far been tested.

    Here we investigated whether binding to the ground reduces seed removal by harvester antsPogonomyrmex subdentatus, an important granivore, for 53 species with mucilaginous seeds. We also explored functional traits that associate with seed removal risk to understand the ecological and evolutionary context of this granivory resistance trait.

    Using a field cafeteria choice experiment, we compared harvester ant seed removal of wetted ground‐bound seeds to dry unbound control seeds for these 53 species. We developed a simple assay to score dislodgement force. We examined whether this force, seed mass and seed mucilage production explained the interspecific variation in protection that we observed in field seed removal. We integrated these experiments with a broad scale test of correlates of seed attachment using a previously published dataset of attachment potential of mucilaginous seeds for 432 species, examining correlations of attachment potential with 13 plant traits and the climate characteristics of the species' range.

    Binding to the ground reduced seed removal in 42 of 53 species tested. The benefit increased with seed dislodgement force, which itself increased with mucilage production, but not with seed mass. In the larger dataset, shorter plant life span, higher temperature, more solar radiation, higher humidity, fewer wet days per year and higher seed density correlated positively with the odds of seed attachment. We also found that attachment potential showed a concave down quadratic relationship with latitude, peaking at roughly 30°. No strong evidence that any of the other six predictors correlated with attachment potential was found.

    We demonstrate that protection from granivores is a widespread convergent function of seed mucilage and is associated with mucilage production. We highlight the need for increased mechanistic investigations into this common but poorly studied trait, particularly in relation to functional drivers of the broad patterns we found.

    A freePlain Language Summarycan be found within the Supporting Information of this article.

     
    more » « less