Predator Avoidance in Extremophile Fish

Extreme habitats are often characterized by reduced predation pressures, thus representing refuges for the inhabiting species. The present study was designed to investigate predator avoidance of extremophile populations of Poecilia mexicana and P. sulphuraria that either live in hydrogen sulfide-rich (sulfidic) springs or cave habitats, both of which are known to have impoverished piscine predator regimes. Focal fishes that inhabited sulfidic springs showed slightly weaker avoidance reactions when presented with several naturally occurring predatory cichlids, but strongest differences to populations from non-sulfidic habitats were found in a decreased shoaling tendency with non-predatory swordtail (Xiphophorus hellerii) females. When comparing avoidance reactions between P. mexicana from a sulfidic cave (Cueva del Azufre) and the adjacent sulfidic surface creek (El Azufre), we found only slight differences in predator avoidance, but surface fish reacted much more strongly to the non-predatory cichlid Vieja bifasciata. Our third experiment was designed to disentangle learned from innate effects of predator recognition. We compared laboratory-reared (i.e., predator-naïve) and wild-caught (i.e., predator-experienced) individuals of P. mexicana from a non-sulfidic river and found no differences in their reaction towards the presented predators. Overall, our results indicate (1) that predator avoidance is still functional in extremophile Poecilia spp. and (2) that predator recognition and avoidance reactions have a strong genetic basis.

[1]  S. Brereton.  Life , 1876, The Indian medical gazette.

[2]  D. Rosen,et al.  A Cavernicolous Form of the Poeciliid Fish Poecilia sphenops from Tabasco, Mexico , 1962 .

[3]  J. Parzefall.  Zur Vergleichenden Ethologie Verschiedener Mollienesia-Arten Einschliesslich Einer Höhlenform Von M. Sphenops , 1969 .

[4]  J. Parzefall,et al.  Über degenerative und konstruktive Merkmale bei einer phylogenetisch jungen Höhlenform von Poecilia sphenops (Pisces, Poeciliidae) , 1973 .

[5]  J. Endler.  NATURAL SELECTION ON COLOR PATTERNS IN POECILIA RETICULATA , 1980, Evolution; international journal of organic evolution.

[6]  B. Peckarsky,et al.  Why do Ephemerella nymphs scorpion posture : a ghost of predation past? , 1988 .

[7]  C. Magnhagen.  Predation risk as a cost of reproduction. , 1991, Trends in ecology & evolution.

[8]  T. Bagarinao.  Sulfide as an environmental factor and toxicant: tolerance and adaptations in aquatic organisms , 1992 .

[9]  D. Conkel.  Cichlids of North and Central America , 1993 .

[10]  A. Covich,et al.  Responses of a Freshwater Shrimp to Chemical and Tactile Stimuli from a Large Decapod Predator , 1994, Journal of the North American Benthological Society.

[11]  J. Endler,et al.  GEOGRAPHIC VARIATION IN FEMALE PREFERENCES FOR MALE TRAITS IN POECILIA RETICULATA , 1995, Evolution; international journal of organic evolution.

[12]  K. Warburton,et al.  Species discrimination in guppies: learned responses to visual cues , 1996, Animal Behaviour.

[13]  D. Chivers,et al.  Chemical alarm signalling in aquatic predator-prey systems: A review and prospectus , 1998 .

[14]  M. Grieshaber,et al.  Animal adaptations for tolerance and exploitation of poisonous sulfide. , 1998, Annual review of physiology.

[15]  J. Byers.  American Pronghorn: Social Adaptations and the Ghosts of Predators Past , 1998 .

[16]  J. Endler,et al.  Geographic variation in behavior : perspectives on evolutionary mechanisms , 1999 .

[17]  Daniel T. Blumstein,et al.  Training Captive‐Bred or Translocated Animals to Avoid Predators , 2000 .

[18]  Response of naïve two-spotted gobies Gobiusculus flavescens to visual and chemical stimuli of their natural predator, cod Gadus morhua , 2001 .

[19]  Janice C. Daniel,et al.  Isolation from mammalian predators differentially affects two congeners , 2002 .

[20]  R. R. Krausz.  Living in Groups , 2013 .

[21]  C. Amsler,et al.  Chemo-tactile predator avoidance responses of the common Antarctic limpet Nacella concinna , 2002, Polar Biology.

[22]  Grant E. Brown.  Learning about danger: chemical alarm cues and local risk assessment in prey fishes , 2003 .

[23]  A. Magurran,et al.  Effects of relaxed predation pressure on visual predator recognition in the guppy , 2003, Behavioral Ecology and Sociobiology.

[24]  A. Magurran,et al.  Learned predator recognition and antipredator responses in fishes , 2003 .

[25]  D. Chivers,et al.  Differential learning rates of chemical versus visual cues of a northern pike by fathead minnows in a natural habitat , 1997, Environmental Biology of Fishes.

[26]  J. Parzefall,et al.  A review of Morphological and Behavioural Changes in the Cave Molly, Poecilia Mexicana, from Tabasco, Mexico , 2004, Environmental Biology of Fishes.

[27]  Ingo Schlupp,et al.  Cave molly females (Poecilia mexicana, Poeciliidae, Teleostei) like well-fed males , 2005, Behavioral Ecology and Sociobiology.

[28]  Ingo Schlupp,et al.  Spectral sensitivity of mollies: comparing surface‐ and cave‐dwelling Atlantic mollies, Poecilia mexicana , 2006 .

[29]  Robert R. Miller,et al.  Freshwater Fishes of Mexico , 2006 .

[30]  H. Fisher,et al.  Alteration of the chemical environment disrupts communication in a freshwater fish , 2006, Proceedings of the Royal Society B: Biological Sciences.

[31]  O. Giere,et al.  Life on the edge: hydrogen sulfide and the fish communities of a Mexican cave and surrounding waters , 2006, Extremophiles.

[32]  I. Schlupp,et al.  Reduction of the association preference for conspecifics in cave-dwelling Atlantic mollies, Poecilia mexicana , 2006, Behavioral Ecology and Sociobiology.

[33]  B. D. Wisenden,et al.  Sound the alarm: learned association of predation risk with novel auditory stimuli by fathead minnows (Pimephales promelas) and glowlight tetras (Hemigrammus erythrozonus) after single simultaneous pairings with conspecific chemical alarm cues , 2007, Environmental Biology of Fishes.

[34]  D. Blumstein.  The Multipredator Hypothesis and the Evolutionary Persistence of Antipredator Behavior , 2006 .

[35]  Ingo Schlupp,et al.  Predation of a cave fish (Poecilia mexicana, Poeciliidae) by a giant water‐bug (Belostoma, Belostomatidae) in a Mexican sulphur cave , 2007 .

[36]  I. Schlupp,et al.  Local adaptation and pronounced genetic differentiation in an extremophile fish, Poecilia mexicana, inhabiting a Mexican cave with toxic hydrogen sulphide , 2006, Molecular ecology.

[37]  O. Giere,et al.  Survival in an extreme habitat: the roles of behaviour and energy limitation , 2007, Naturwissenschaften.

[38]  I. Schlupp,et al.  Sexual harassment in live-bearing fishes (Poeciliidae): comparing courting and noncourting species , 2007 .

[39]  M. C. Ferrari,et al.  Generalization of learned predator recognition: an experimental test and framework for future studies , 2007, Proceedings of the Royal Society B: Biological Sciences.

[40]  Ingo Schlupp,et al.  Parallel evolution leads to reduced shoaling behavior in two cave dwelling populations of Atlantic mollies (Poecilia mexicana, Poeciliidae, Teleostei) , 2008, Environmental Biology of Fishes.

[41]  L. Morrell,et al.  RISK-SENSITIVE ANTIPREDATOR BEHAVIOR IN THE TRINIDADIAN GUPPY, POECILIA RETICULATA. , 2008, Ecology.

[42]  M. Plath,et al.  Male-biased predation of a cave fish by a giant water bug , 2008, Naturwissenschaften.

[43]  I. Schlupp,et al.  Two endemic and endangered fishes, Poecilia sulphuraria (Alvarez, 1948) and Gambusia eurystoma Miller, 1975 (Poeciliidae, Teleostei) as only survivors in a small sulphidic habitat , 2008 .

[44]  M. Tobler,et al.  A morphological gradient revisited: cave mollies vary not only in eye size , 2009, Environmental Biology of Fishes.

[45]  M. Plath,et al.  Compensatory behaviour in response to sulphide-induced hypoxia affects time budgets, feeding efficiency, and predation risk , 2009 .

[46]  K. Scharnweber,et al.  Variation along the shy–bold continuum in extremophile fishes (Poecilia mexicana, Poecilia sulphuraria) , 2009, Behavioral Ecology and Sociobiology.

[47]  Henrik G. Smith,et al.  Picking personalities apart: estimating the influence of predation, sex and body size on boldness in the guppy Poecilia reticulata , 2010 .

[48]  I. Schlupp,et al.  Toxic hydrogen sulfide and dark caves: life-history adaptations in a livebearing fish (Poecilia mexicana, Poeciliidae). , 2010, Ecology.

[49]  D. Algom,et al.  Visual Cues for Predator Face Recognition by Reef Fishes , 2010 .

[50]  Martin Plath,et al.  Predation by Three Species of Spiders on a cave Fish in a Mexican Sulphur Cave , 2010 .

[51]  Ingo Schlupp,et al.  Extreme habitats are not refuges: poeciliids suffer from increased aerial predation risk in sulphidic southern Mexican habitats , 2010 .

[52]  J. Parzefall.  Rückbildung aggressiver Verhaltensweisen bei einer Höhlenform von Poecilia sphenops (Pisces, Poeciliidae) , 2010 .

[53]  J. Evans,et al.  Ecology and Evolution of Poeciliid Fishes , 2011 .

[54]  K. Winemiller,et al.  Hydrogen sulfide, bacteria, and fish: a unique, subterranean food chain. , 2011, Ecology.

[55]  A. Pilastro,et al.  Postcopulatory Sexual Selection , 2020, Encyclopedia of Personality and Individual Differences.

[56]  I. Schlupp,et al.  Toxic hydrogen sulphide and dark caves: pronounced male life‐history divergence among locally adapted Poecilia mexicana (Poeciliidae) , 2011, Journal of evolutionary biology.

[57]  Martin Plath,et al.  Predation on a Cave Fish by the Freshwater Crab Avotrichodactylus Bidens (Bott, 1969) (Brachyura, Trichodactylidae) in a Mexican Sulfur Cave , 2011 .

[58]  David Bierbach,et al.  EVOLUTION IN EXTREME ENVIRONMENTS: REPLICATED PHENOTYPIC DIFFERENTIATION IN LIVEBEARING FISH INHABITING SULFIDIC SPRINGS , 2011, Evolution; international journal of organic evolution.

[59]  Culum Brown,et al.  Predation risk and decision making in poeciliid prey , 2011 .

[60]  D. Bierbach,et al.  Predator-induced changes of female mating preferences: innate and experiential effects , 2011, BMC Evolutionary Biology.

[61]  D. Bierbach,et al.  Divergent Evolution of Male Aggressive Behaviour: Another Reproductive Isolation Barrier in Extremophile Poeciliid Fishes? , 2011, International journal of evolutionary biology.