Epidermal 'alarm substance' cells of fishes maintained by non-alarm functions: possible defence against pathogens, parasites and UVB radiation.
Many fishes possess specialized epidermal cells that are ruptured by the teeth of predators, thus reliably indicating the presence of an actively foraging predator. Understanding the evolution of these cells has intrigued evolutionary ecologists because the release of these alarm chemicals is not voluntary. Here, we show that predation pressure does not influence alarm cell production in fishes. Alarm cell production is stimulated by exposure to skin-penetrating pathogens (water moulds: Saprolegnia ferax and Saprolegnia parasitica), skin-penetrating parasites (larval trematodes: Teleorchis sp. and Uvulifer sp.) and correlated with exposure to UV radiation. Suppression of the immune system with environmentally relevant levels of Cd inhibits alarm cell production of fishes challenged with Saprolegnia. These data are the first evidence that alarm substance cells have an immune function against ubiquitous environmental challenges to epidermal integrity. Our results indicate that these specialized cells arose and are maintained by natural selection owing to selfish benefits unrelated to predator-prey interactions. Cell contents released when these cells are damaged in predator attacks have secondarily acquired an ecological role as alarm cues because selection favours receivers to detect and respond adaptively to public information about predation.
Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, Saskatchewan, Canada. doug.chivers@usask.ca
Douglas P
DP
Chivers
Brian D
BD
Wisenden
Carrie J
CJ
Hindman
Tracy A
TA
Michalak
Robin C
RC
Kusch
Susan G W
SG
Kaminskyj
Kristin L
KL
Jack
Maud C O
MC
Ferrari
Robyn J
RJ
Pollock
Colin F
CF
Halbgewachs
Michael S
MS
Pollock
Shireen
S
Alemadi
Clayton T
CT
James
Rachel K
RK
Savaloja
Cameron P
CP
Goater
Amber
A
Corwin
Reehan S
RS
Mirza
Joseph M
JM
Kiesecker
Grant E
GE
Brown
James C
JC
Adrian
Patrick H
PH
Krone
Andrew R
AR
Blaustein
Alicia
A
Mathis
D000819:Animal Communication; D000818:Animals; D005075:Biological Evolution; D049109:Cell Proliferation; D003530:Cyprinidae / Q000382:microbiology / Q000469:parasitology / Q000502:physiology*; D000078404:Epidermal Cells; D004817:Epidermis / Q000382:microbiology / Q000469:parasitology / Q000528:radiation effects; D005658:Fungi; D010473:Perciformes / Q000382:microbiology / Q000469:parasitology / Q000502:physiology*; D010675:Pheromones / Q000378:metabolism*; D011235:Predatory Behavior; D014200:Trematoda; D014466:Ultraviolet Rays
D010675:Pheromones