Host manipulation by Ligula intestinalis: a cause or consequence of parasite aggregation?
Previous investigations suggest that the infection of the cyprinid roach, Rutilus rutilus, with the larval plerocercoid forms of the cestode, Ligula intestinalis, creates behavioural and morphological changes in the fish host, potentially of adaptive significance to the parasite in promoting transmission to definitive avian hosts. Here we consider whether these behavioural changes are important in shaping the distribution of parasite individuals across the fish population. An examination of field data illustrates that fish infected with a single parasite were more scarce than expected under the negative binomial distribution, and in many months were more scarce than burdens of two, three or more, leading to a bimodal distribution of worm counts (peaks at 0 and >1). This scarcity of single-larval worm infections could be accounted for a priori by a predominance of multiple infection. However, experimental infections of roach gave no evidence for the establishment of multiple worms, even when the host was challenged with multiple intermediate crustacean hosts, each multiply infected. A second hypothesis assumes that host manipulation following an initial single infection leads to an increased probability of subsequent infection (thus creating a contagious distribution). If manipulated fish are more likely to encounter infected first-intermediate hosts (through microhabitat change, increased ingestion, or both), then host manipulation could act as a powerful cause of aggregation. A number of scenarios based on contagious distribution models of aggregation are explored, contrasted with alternative compound Poisson models, and compared with the empirical data on L. intestinalis aggregation in their roach intermediate hosts. Our results indicate that parasite-induced host manipulation in this system can function simultaneously as both a consequence and a cause of parasite aggregation. This mutual interaction between host manipulation and parasite aggregation points to a set of ecological interactions that are easily missed in most experimental studies of either phenomenon.
Brown
S P
SP
Department of Zoology, University of Cambridge, Downing Street, UK. brown@isem.univ-montp2.fr
Loot
G
G
Teriokhin
A
A
Brunel
A
A
Brunel
C
C
Guégan
J-F
JF
D000818:Animals; D016010:Binomial Distribution; D002589:Cestoda / Q000254:growth & development*; D002590:Cestode Infections / Q000453:epidemiology / Q000469:parasitology / Q000662:veterinary*; D003198:Computer Simulation; D003445:Crustacea / Q000469:parasitology; D003530:Cyprinidae; D005393:Fish Diseases / Q000453:epidemiology / Q000469:parasitology*; D005602:France / Q000453:epidemiology; D006790:Host-Parasite Interactions; D008954:Models, Biological; D016012:Poisson Distribution; D012621:Seasons