The biology of hypogean fishes Developments in environmental biology of fishes 21 Series Editor EUGENE K. BALON The biology of hypogean fishes Guest Editor: Aldemaro Romero Reprinted from Environmental biology offishes, Volume 62 (1-3), 2001 with addition of species and subject index .... " Springer-Science+Business Media, B.Y. A C.I.P. Catalogue record for this book is available from the library of Congress Cover design by Eugene K. Balon using posterior portion of Amhlyopsis rosae and Typhlichthys suhterraneus by Loubna Bennis in the respective Threatened fishes of the world one pagers of Aldemaro Romero (Env. BioI. Fish. 52: 434 and 53: 74). The logo designed by Christine Flegler-Balon, based on an idea of Emma Spertus Printed on acid-free paper ISBN 978-90-481-5848-5 ISBN 978-94-015-9795-1 (eBook) DOI 10.1007/978-94-015-9795-1 All Rights Reserved ©2001 Springer Science+Business Media Dordrecht Originally published by Kluwer Academic Publishers in 200 I. Softcover reprint of the hardcover I st edition 2001 No part of the material protected by this copyright notice may be reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording or by any information storage and retrieval system, without written permission from the copyright owner. CONTENTS An introduction to the special volume on the biology of hypogean fishes, by A. Romero 7-12 It's a wonderful hypogean life: a guide to the troglomorphic fishes of the world, by A. Romero & K.M. Paulson 13-41 Scientists prefer them blind: the history of hypogean fish research, by A. Romero 43-71 Nontroglobitic fishes in Bruffey-Hills Creek Cave, West Virginia, and other caves worldwide, by W.J. Poly 73-83 Part 1. Anatomy, physiology and behavior The mechanosensory lateral line system of the hypogean form of Astyanax fasciatus, by J.C. Montgomery, S. Coombs & C.F. Baker 87-96 Metabolie rate and natural history of Ozark cavefish, Amb/yopsis rosae, in Logan Cave, Arkansas, by G.L. Adams & J.E. Johnson 97-105 Locomotory responses of the cave cyprinid Phreatichthys andruzzii to chemical signals from conspecifics and related species: new findings, by R. Berti & L. Zorn 107-114 Responses to light in epigean and hypogean populations of Gambusia affinis (Cyprinodonti formes: Poeciliidae), by M.M. Camassa 115-118 Temporal organization in locomotor activity of the hypogean loach, Nemacheilus evezardi, and its epigean ancestor, by A. K. Pati 119-129 Part 2. Ecology and conservation Ecology of subterranean fishes: an overview, by E. Trajano 133-160 Population biology and growth of Ozark cavefish in Logan Cave National Wildlife Refuge, Arkansas, by J.Z. Brown & J.E. Johnson 161-169 Threatened fishes of the wor/d: Ophisternon infernale (Hubbs, 1938) (Synbranchidae), by R. Medina-Gonza/ez, G. Proud/ove, L. Chumba-Segura & T. /lifte 170 How hydrogeology has shaped the ecology of Missouri's Ozark cavefish, Amb/yopsis rosae, and southern cavefish, Typhlichthys subterraneus: insights on the sightless from under 171-194 standing the underground, by D.B. Noltie & C.M. Wicks Habitat and population data of troglobitic armored cave catfish, Ancistrus cryptophtha/mus Reis, 1987, from central Brazil (Siluriformes: Loricariidae), by E. Trajano 195-200 The conservation status of hypogean fishes, by G.S. Proudlove 201-213 Threatened fishes of the wor/d: Ogilbia pearsei (Hubbs, 1938) (Bythitidae), by G. Proud/ove, R. Medina-Gonza/ez, L. Chumba-Segura & T. /lifte 214 Status of the federally endangered Alabama cavefish, Speop/atyrhinus pou/soni (Amblyop sidae), in Key Cave and surrounding caves, Alabama, by B.R. Kuhajda & R.L. Mayden 215-222 Part 3. Genetics and evolution Genetic differentiation among populations of the cave fish Schistura oedipus (Cypriniformes: Balitoridae) by R.B. Borowsky & L. Mertz 225-231 Origins and relationship of cave populations of the blind Mexican tetra, Astyanax fasciatus, in the Sierra de EI Abra, by L. Espinasa & R.B. Borowsky 233-237 Threatened fishes of the wor/d: Caecobarbus geertsii Bou/enger, 1921 (Cyprinidae), by G.S. Proud/ove & A. Romero 238 Morphological and physiological correlates of evolutionary reduction of metabolie rate among amblyopsid cave fishes, by T.L. Poulson 239-249 Convergent adaptations to cave life in the Rhamdia laticauda catfish group (Pimelodidae, Teleostei), by H. Wilkens 251-261 A review of morphological and behavioural changes in the cave molly, Poecilia mexicana, from Tabasco, Mexico, by J. Parzefall 263-275 Part 4. Special cases Troglomorphic sculpins of the Cottus carolinae species group in Perry County, Missouri: distribution, external morphology, and conservation status, by S.M. Surr, G.L. Adams, 279-296 J.K. Krejca, R.J. Paul & M.L. Warren, Jr. Milyeringa veritas (Eleotridae), a remarkably versatile cave fish from the arid tropics of northwestern Australia, by W.F. Humphreys 297-313 Mexican blindeats genus Prietella (Siluriformes: Ictaluridae): an overview of recent explorations, by DA Hendrickson, J.K. Krejca & J.M. Rodrfguez Martinez 315-337 A new blind cave fish population of genus Astyanax: geography, morphology and behavior, by L. Espinasa, P. Rivas-Manzano & H. Espinosa Perez 339-344 Adaptations of cave fishes with some comparisons to deep-sea fishes, by T.L. Poulson 345-364 Species and subject index 365-376 How newly evolving species of cave fish learn to navigate. Environmental Biology of Fishes 62: 7-12, 200l. © 2001 Kluwer Academic Publishers. An introduction to the special volume on the biology of hypogean fishes Aldemaro Romero Environmental Studies Program and Department of Biology, Macalester College, 1600 Grand Ave., St. Paul, MN 55105-1899, U.S.A. (e-mai!: [email protected]) Patterns, diversification, and something else of a particular species or a particular problem among hypogean fishes; others have only visited this subject Hypogean fishes have always been a source of in order to test their ideas in a particular field. Studies amazement and amusement throughout the history have ranged from taxonomy to behavior, from mor of ichthyology (Romero 2001). Controversies have phology to ecology; methodologies have encompassed ranged from evolutionary issues to behavioral field studies as weH as the application of the latest adaptations, from taxonomy to ecology. The funda behavioral and molecular laboratory techniques. No mental reason behind those controversies is that a wonder there is a lot of information out there but not number of adaptations usuaHy referred to as 'troglo too much of a synthesis. morphisms', especiaHy blindness and depigmentation, So far the only attempt to provide such a synthesis have already been found in nearly 90 species that are was Thines's (1969) book, which was largely a compi largely taxonomicaHy unrelated (Romero & Paulson lation of known facts. Since then, many changes have 2001). Although reduction and/or loss of eyes and pig occurred; not only have a great deal of new species been mentation seem to be common, the degree to which discovered, but new approaches have been taken that they occur varies and, to make matters more compli have profoundly influenced how the scientific commu cated, not aH hypogean fishes have those adaptations. nity looks at this subject. Hence, the idea of this special In some cases these species/populations freely come in volume on the biology hypogean fishes. and out of caves; in others, our access to them has been Here we present 27 articles written by 38 authors limited to occasional coHections from weHs. In some from nine countries. Some ofthem tackle very specific cases these species are known from a single specimen; issues; others provide a syntheses on specific issues. in others they are represented by several populations. What foHows is a general overview of these articles. Some hypogean habitats in which these fishes are found seem to be very poor in nutrients, while others are sup plied with constant and abundant amounts of organic As a matter of introduction material. In most cases, the fish in question is the only vertebrate found in its habitat, in others, they share their Romero & Paulson (2001) provide a general list habitat with other hypogean fishes. Many species of of hypogean fishes that present well-established non-hypogean fishes show some of the features of cave troglomorphism. There they summarize information fishes. That is the case of fishes living in murky waters not previously synthesized elsewhere, with special or the deep-sea; however, no hypogean fish has been emphasis on those features that could be used for com found displaying some of the remarkable adaptations of parative purposes to better understand the biology of abyssal fishes such as bioluminescence and darkening these fishes. Thus, in addition to the scientific names coloration. and the (not always known) common names for these Thus, besides being subject to (in most cases) per fishes, the article includes information about the ety manent darkness, there seems to be no common rule to molo gy of their scientific name, major synonyms, be applied here, or is there? his tory, distribution, habitat and ecology, and remarks One of the pursuits of science is finding common of troglomorphisms found among these species as patterns in nature; however, that goal has remained weH as any other unusual feature described for them. elusive for hypogean fish researchers. Some of those Included in this article are references to two poorly researchers have devoted their entire life to the study studied features that may be more common than 8 previously thought: structural simplification or loss 'picture' of their environment, a process that has been of both their scales and swim(gas)bladder. Remarks called active hydrodynamic imaging. are also made regarding the possible phylogenetic Adams & Johnson (2001) studied the metabolic relationships of each species. rate and natural history of Ozark cavefish, Amblyopsis Romero's (2001) article on the history of hypogean rosae, in Logan Cave, Arkansas, and found that fish research represents an attempt to give a histori seasonal relationships between mass and oxygen con cal context to past and present efforts to understand sumption may reflect alterations in environmental the biology of these animals. It contains both qual conditions (i.e. food availability, ambient dissolved itative and quantitative information on how research oxygen) and changes in susceptibility to handling has progressed through times, defining the rather clear stress. They also report that cannibalism may not cut historical periods which were largely influenced by always be the rule for this amblyopsid species, as philosophical concepts and geography. This article tries previously suggested. to explain why if hypogean fishes represent such an Berti & Zorn (2001) report their most recent research interesting model for evolutionary studies, they have on the locomotory responses of the cave cyprinid yet to become a popular model for research among Phreatichthys andruzzii to chemical signals from con non-speleological investigators. specifics and related species. Contrary to what was Poly (2001) provides not only a study on non previously believed, they found that there was not a troglobitic fishes for a particular cave in West Virginia, positive chemotaxis to the odor of known or unknown but also synthesizes information about other non conspecifics, but rather a strong negative chemotaxis troglobitic species from the rest of the world. This towards the odor of unfamiliar conspecifics and of indi represents a new and healthy trend: students of cave viduals belonging to the closely related species Barbus fishes had until recently concentrated almost exclu conchonius. sively on hypogean fishes with troglomorphic features Camassa (2001) studied the responses to light in considering non-troglobitic ones as mere 'accidentals' epigean and hypogean populations of the poeciliid worthy of little more than a footnote. Yet, with the Gambusia affinis from the brackish water basins of the gradual abandonment of typological views and the 'Spunnulate' dolinas system of Torre Castiglione, in understanding that these fishes can actually provide southeastern Italy. She found that the hypogean indi clues to understanding hypogean fish evolution (they viduals showed, on average, scotophilia (photophobia) are sort of 'missing links'), now there is an increasing with little variability in their responses. On the other interest in them (see some other articles below). hand, epigean and spring-dwelling individuals of In general, these chapters demonstrate that although G. affinis from the same region showed the opposite a great deal of progress has been made in the last behavior and with a great variability in their responses few decades, a number of issues need to be resolved, when compared with cave-dwelling conspecifics. from conceptual to methodological ones, and that most Pati (2001) presents the results of his latest exper hypogean species, whether they are troglomorphic or iments on the temporal organization in locomotor not, remain poorly known, which has hampered some activity of the hypogean loach, Nemacheilus evezardi, of the attempts to synthesize information. and its epigean ancestor. His studies suggest that hypogean fish still possess a functional oscillator underlying their overt circadian rhythm in locomotor Anatomy, physiology and behavior activity, although the ecophysiological significance of this proposition is yet to be fully understood. The relationships between morphology, physiology and behavior has always been an important component of hypogean fish research, and five articles in this Ecology and conservation volume represent current research in that tradition. Montgomery et al. (2001), for example, provide an In the last decade, there has been an increased interest excellent synthesis of theirs and others' research on the on the ecology and conservation status of these fishes. mechanosensory lateral line system of the hypo ge an Thanks to the use of capture-recapture methods, which form of the characid Astyanax Jasciatus. They show allows the gathering of data instead of the mostly how their enhanced lateralline capabilities with respect casual observations of the past, new testable hypotheses to their sighted relatives allow them to build up a have been presented and more precise information 9 has beeome available. Trajano (2001a), for example, Three papers of the series 'Threatened fish of presents an overview on the eeology ofhypogean fishes the world' round up this seetion with narratives on by synthesizing the available eeologieal data and eom Caecobarbus geertsii (Proudlove & Romero 2001), paratively analyzing that in an evolutionary eontext. Ophisternon inJernale (Medina-Gonzalez et al. 2001), Brown & Johnson (2001) give us the results oftheir and Ogilbia pearsei (Proudlove et al. 2001). population studies and growth of the Ozark eavefish, Amblyopsis rosae, in Logan Cave National Wildlife Refuge, Arkansas. Aeeording to their results, this Genetics and evolution threatened speeies, endemie to the Springfield Plateau of the Ozark Highlands in Arkansas, Missouri, and This seetion contains five articles that exarnine genetie Oklahoma, has a maximum life span of 4-5 years. They and evolutionary issues from different perspeetives. found that this fish has an average rate of growth of Moleeular teehniques are helping tremendously to 0.6 mm per month, though smaller fish grew faster than understand the true evolutionary nature of many larger fish hypogean populations while underlying the fact that Noltie & Wieks (2001), on the other hand, took drastie phenotypie differenees between epigean and a look at how hydrogeology has shaped the eeology hypogean populations may result from very little of Missouri's Ozark eavefish, Amblyopsis rosae, and genetie modifieations. Borowsky & Mertz (2001) for the southem eavefish, Typhlichthys subterraneus. They example, report on the genetie differentiation among explored how the differenees in geography, geology, populations of the balitorid eave fish, Schistura oedi and hydrology in the habitats of both fish interaet in pus, from Thailand by using DNA analysis. They found shaping the habitat in whieh these two speeies dweIl, that the five populations they studied were little differ the resulting eeologieal eonstraints that the fishes face, entiated and that S. oedipus appears to be more c10sely how their eeologies and populations refteet these eon related to S. poculi than to S. reidi, a proposed sister straints, and how eonservation and management efforts taxon. may need to be tailored to best eompliment the unique Espinasa & Borowsky (2001) used RAPD markers challenges that eaeh speeies presents. to explore the origins and relationships of eave popu Trajano (2001 b) studied the habitat and popula lations of the blind Mexiean tetra, Astyanax Jasciatus, tion biology of the armored eave eatfish, Ancistrus in the Sierra de EI Abra. Their results indicate that cryptophthalmus, from Central Brazil and found this all eave populations are more c10sely related to one speeies to be a typical bottom-dweller with a strong another than they are to the surfaee populations. This preference for roeky substrates in fast-ftowing stream suggests that present day eave populations derived from sectors, while having relatively high population densi a eommon aneestral stock, most like1y due to a single ties when eompared to other eavefishes, eonservatively eolonization event, or altematively, that strong gene estimated at 20000 individuals. ftow among eave populations has oeeurred, raising pre Proudlove (2001) synthesized the eonservation eaution against eonsidering eaeh eave population as status of hypogean fishes and found that these fishes independent. are suseeptible to five main threats: habitat degrada Poulson (200la) studied the morphologieal and tion, hydrological manipulations, environmental pollu physiologieal eorrelates of evolutionary reduetion of tion, overexploitation, and introdueed exotie speeies. metabolie rate among amblyopsid eave fishes. He Beeause they are endemie to small areas and have reports multiple eorrelates of reduetion in metabolie small populations, any threat eould have serious eon rate during evolutionary adaptation to eaves in the fish sequenees. Some species are reeeiving eonservation family Amblyopsidae. He found that no trait that eould attention; however, most reeeive none. eontribute to a lowered metabolie rate is in the same Kuhajda & Mayden (2001) diseuss the status of the rank order as metabolie rate, though eolleetively the federally endangered Alabama eavefish, Speoplatyrhi reduetions were in the same order as metabolie rates. nus poulsoni, in eaves of Alabama. They found that its He explains that this was as expeeted with eonvergent population is relatively stable, but reeommend eontin evolution of eomplex traits. uous monitoring. They also observed a single speei Wilkens (200 I) deseribes the eonvergent adaptations men of Typhlichthys subterraneus in Key Cave, whieh to eave life in the pimelodid Rhamdia laticauda eatfish falsifies the previous assumption that these two speeies group from Central Ameriea. This speeies gave rise to were allopatrie. a number of eave speeies. Comparison between two