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Introduction: A Surfeit of Lampreys

  • Margaret F. DockerEmail author
  • John B. Hume
  • Benjamin J. Clemens
Chapter
Part of the Fish & Fisheries Series book series (FIFI, volume 37)

Abstract

Lampreys have long been the food of kings. They have been highly appreciated by the English monarchy and upper classes since medieval times, and long before that, by the ancient Romans, the Māori, and Native Americans. ­Historically, lampreys have also received attention from at least a small group of anatomists and other scientists (including Sigmund Freud), given their “lofty” status at the base of the vertebrate family tree (and their wonderfully large reticulospinal neurons that are so amenable to experimental manipulation). Research related to lamprey biology increased in the 1950s in support of sea lamprey control in the Laurentian Great Lakes, and these efforts considerably advanced our understanding of lamprey ecology, behavior, and chemical communication. Recently, lampreys have started getting more widespread attention. Research related to lamprey endocrinology (­particularly the pivotal hypothalamic-pituitary axis and gonadotropin-releasing hormones), the ecology and conservation of native lampreys, and the use of lampreys in evolutionary developmental (evo-devo) and biomedical studies has raised the profile of this group of ancient fishes. Lampreys are providing important and promising model systems in our quest to better understand the early evolutionary history of the vertebrates—particularly given the recent publication of the complete sea lamprey genome—and their increasing use in biomedical research is providing insights into treatment for people suffering from blood coagulation disorders, biliary atresia, hemochromatosis, and spinal cord injuries. In this introduction to Vols. 1 and 2 of Lampreys: Biology, Conservation and Control, we provide a broad perspective on the cultural, ecological, and scientific importance of lampreys, outline some historical trends in lamprey research, and celebrate the ­growing ­interest—among scientists and laypeople—in this previously underappreciated group of fishes.

Keywords

Adaptive immunity Agnathan Anti-coagulants Biliary atresia Biomedical Biorobotics Conservation Cyclostome Evo-devo Gnathostomes Hemochromatosis Lamprey fisheries Sea lamprey control Sea lamprey genome Spinal cord regeneration Vertebrate evolution 

1.1 Introduction

Lampreys have long been the food of kings. They were highly appreciated by the ancient Romans 2,000 years ago and by the English monarchy and upper classes since medieval times. King Henry I of England is famously said to have died after eating a surfeit of lampreys (although the lampreys themselves were perhaps not to blame for his overindulgence). The Māori in New Zealand and Native Americans in the Columbia River basin have also long valued lampreys for human consumption and ceremonial purposes. Historically, lampreys have also received attention from at least a small group of anatomists and other scientists, often in an attempt to understand the origin of the vertebrate body plan.

Research related to lamprey biology increased in the 1950s in support of control of sea lamprey Petromyzon marinus in the Laurentian Great Lakes and continues today. These efforts have considerably advanced our understanding of lamprey ecology, behavior, and chemical communication. Recently, however, lampreys are receiving more widespread attention. For example, the use of lampreys in evolutionary developmental (evo-devo) and biomedical studies has further raised the profile of this group of ancient fishes, and the sequencing of the complete sea lamprey genome (Smith et al. 2013) was a major milestone. Research related to the ecology and conservation of native lampreys throughout many parts of the world has also increased, along with a greater appreciation for lampreys among laypeople. For example, “Neunaugen” (the German word for lampreys, deriving from the impression that they have “nine eyes” on each side of the body—the actual eye, the pineal or “third eye,” and the seven lateral gill openings; Fig. 1.1) were named “Fish of the Year” in 2012 by the German Sport Fishermen Association, the Ministry for Nature Conservation, the German Angler Association, and the German Sport Divers Association (European Fly Angler 2012).

Fig. 1.1

European river lamprey Lampetra fluviatilis captured during its upstream migration (at the end of February 2009) from the River Sorraia in the Tagus River basin, Portugal (total length c. 25 cm). All extant lamprey species possess seven pairs of gills; these plus the eyes and the single median pineal gland (the so-called third eye, located behind the nostril) have earned lampreys the German name “Neunaugen” (“nine eyes”). This species, although still abundant throughout its northern European range, is extremely rare in the Iberian Peninsula. (Photo: © Bernardo R Quintella)

In this introduction to Vols. 1 and 2 of Lampreys: Biology, Conservation and Control, we provide a broad perspective on the historical, ecological, and scientific importance of lampreys, outline some interesting trends in lamprey research (e.g., in terms of topics and species covered), and celebrate the growing interest in this previously underappreciated group of fishes. This chapter will also outline the intended scope of the book and explain the nomenclatural conventions followed within. Subsequent chapters focus on detailed aspects of lamprey biology, but this introduction—which attempts to provide breadth rather than depth—is intended to place lamprey research into a broader context and demonstrate its relevance across a range of disciplines. Given their status as one of the oldest living groups of vertebrates, lampreys are finally starting to receive the attention they deserve.

1.1.1 Are Lampreys the Oldest Living Group of Vertebrates or One of the Oldest Living Groups of Vertebrates?

Whether the so-called cyclostomes—the extant jawless fishes, the hagfishes and lampreys—form a monophyletic group (i.e., are each other’s closest relative) has been considered “one of the most vexing problems in vertebrate phylogenetics” (Near 2009) and a “taxonomic dispute that has troubled scientists for more than a century” (Nicholls 2009). Providing a detailed review of this taxonomic dispute is beyond the scope of this chapter (see Janvier 2007, 2010; Near 2009; see Chap.  2), but its resolution is important in order to understand the earliest events in vertebrate evolution (see Sect. 1.2.3.2). In brief, morphological characters typically suggest cyclostome paraphyly, that is, that lampreys are the sister group to the jawed vertebrates (superclass Gnathostomata) and that hagfishes represent an earlier offshoot from the vertebrate family tree. Lampreys were thought to share many derived traits or synapomorphies with the jawed vertebrates, such as rudimentary vertebrae, a closed circulatory system, neural control of heart rate, and the ability to osmoregulate. Lampreys were therefore generally considered the oldest extant vertebrates, whereas hagfishes were considered craniates but not vertebrates (Nelson 2006). Nelson (2006) therefore placed extant hagfishes and lampreys into separate superclasses (Myxinomorphi and Petromyzontomorphi) rather than the paraphyletic ­superclass Agnatha. Recent and compelling molecular evidence, however, ­strongly supports extant agnathans as a monophyletic group (e.g., Kuraku et al. 1999; ­Delarbre et al. 2002; Takezaki et al. 2003; Heimberg et al. 2010; Fig. 1.2a) and, in fact, suggests that hagfishes have “long overlooked vertebral ­elements” (­Janvier 2011; Ota et al. 2011, 2013). Thus, throughout this book, lampreys are considered one of the (two) oldest living groups of vertebrates and, given the evidence for ­cyclostome monophyly, lampreys and hagfishes are equally distant from—or ­equally related to—the jawed vertebrates.

Fig. 1.2

Schematic representation showing presumed phylogenetic relationship between lampreys and other vertebrates. a Current understanding of the relationship among extant vertebrates (i.e., the “cyclostome monophyly” hypothesis), which holds that the extant jawless fishes (hagfishes and lampreys) shared an ancestor more recently with each other than either group did with the jawed vertebrates (the gnathostomes). This hypothesis is supported by considerable molecular evidence (e.g., Heimberg et al. 2010; see Sect. 1.1.1); under this hypothesis, both hagfishes and lampreys would be considered vertebrates. Interrelationships among the jawed vertebrates follow Nelson (2006); names of the five classes of extant fishes are given in bold; the numbers of extant species in each lineage are from Nelson (2006) or, for lampreys, from this volume (see Chaps.  2 and  8). Note that “fishes” is not a monophyletic group, even when the jawless fishes are omitted, nor is the former taxonomic group Osteichthyes (the “bony fishes,” which traditionally included the actinopterygian and sarcopterygian fishes) monophyletic when the tetrapods are excluded. b Relationship among the agnathans and gnathostomes according to the “cyclostome paraphyly” hypothesis and when extinct agnathans are included. This hypothesis is generally supported by morphological data (see Sect. 1.1.1); under this scheme, hagfishes are often considered craniates but not vertebrates (Nelson 2006). Note that, regardless of whether the cyclostomes (the extant jawless fishes) form a monophyletic group, agnathans are paraphyletic when extinct jawless fishes are included

Cyclostome monophyly, however, means only that hagfishes and lampreys are each other’s closest living relative; it does not necessarily mean that these lineages are closely related. Near (2009) suggested that the long-standing difficulties in resolving the relationship among hagfishes, lampreys, and gnathostomes are likely the result of trying to resolve events that occurred over a very short timescale relative to the hundreds of millions of years that have passed since. Recognizable hagfish and lamprey fossils have been found that date back at least 300–360 million years (Bardack 1991, 1998; Gess et al. 2006; see Chap.  2), indicating long independent evolutionary histories for these two lineages. It is important to recognize the significant differences between these two cyclostome lineages. Furthermore, it must be remembered that the lampreys and hagfishes (with approximately 40 and 70 extant species, ­respectively) are but a small representation of the once diverse jawless fishes, which included the now-extinct conodonts and ostracoderms (Nelson 2006). Despite compelling evidence for monophyly of the extant agnathans, there is little dispute that the agnathans represent a paraphyetic group when the extinct jawless fishes are included (Fig. 1.2b). Hence, although “agnathan” is a useful term for describing jawless vertebrates, it is not used in this book as a formal taxonomic term. Given, however, that lampreys and hagfishes are the sole survivors of this once diverse assemblage, these “living fossils” (sensu Janvier 2007) are absolutely invaluable for helping to piece together the evolutionary history of the vertebrates (Sect. 1.2.3.2).

1.1.2 Are Lampreys Fishes?

Some biologists who work on jawed fishes are often adamant that lampreys are not “true” fishes. This was indeed once the case (e.g., when the senior author of this chapter was a graduate student preparing for her PhD comprehensive exam). In the second edition of his authoritative Fishes of the World, Nelson (1984) recognized ­Pisces (including only the cartilaginous and bony fishes) as a formal taxon (Fig. 1.2a). With the third edition, however, Nelson (1994) adopted a cladistics classification and Pisces or “fishes” was no longer given taxonomic rank since it ­constitutes a paraphyletic group (i.e., the tetrapods are also descended from the common ancestor of all jawed fishes; Fig. 1.2a). Even the bony fishes—commonly, but no longer formally, known as the Osteicthyes, and including the ray-finned fishes (­Actinopterygii) and the sarcopterygian fishes (i.e., lungfishes and coelacanths)—are paraphyletic. Nelson (2006) covered this nicely in the Introduction to the fourth edition of Fishes of the World. Fishes therefore no longer has formal taxonomic meaning, and we follow Nelson (2006), who simply, but artificially, defined fishes as “aquatic vertebrates that have gills throughout their life and limbs, if any, in the shape of fins” and ­include hagfishes and lampreys in this group. Lampreys are fishes; after all, they are being covered in Springer’s Fish and Fisheries series!

1.2 The Cultural, Ecological, and General Scientific Value of Lampreys

As introduced above, lampreys—as one of the two surviving lineages of ancient jawless vertebrates—are not (or should not be) of interest to only lamprey biologists. The following sections provide overviews of the broader cultural, ecological, and scientific significance of this fascinating group of animals.

1.2.1 Historical and Cultural Significance of Lampreys

In some cultures, lampreys have long been valued for food and ceremonial ­purposes. Pacific lamprey Entosphenus tridentatus have been fished by Native ­Americans in the Columbia and Klamath river basins of the western United States for thousands of years (Close et al. 2002; Petersen Lewis 2009). In addition to being an important subsistence food (in part due to their high caloric value), Pacific lamprey also have medicinal and ceremonial value (Close et al. 2002). Called “ksuyas” or “asum” in the native tongue of the mid-Columbia Plateau tribes, Pacific lamprey are regarded as one of their cultural icons (Close et al. 2002). It is this long-held appreciation for Pacific lamprey that has been the impetus for many of the conservation efforts recently initiated for this species (see Chap.  8). The Māori in New Zealand have likewise used pouched lamprey Geotria australis for human consumption and ceremonial purposes (McDowall 1990), and native people in Alaska traditionally consumed the Arctic lamprey Lethenteron camtschaticum and used its rendered oil as fuel for lamps. In Japan, the Arctic lamprey is also highly valued as a medicine against night blindness (Renaud 2011).

Lampreys have also been appreciated as food in Europe, and references to lampreys have appeared in popular texts for close to 2,000 years. Romans of the first and second centuries considered them to be “regal food” (Renaud 2011), rearing them in ponds for such (and perhaps other) purposes. Pliny the Elder, in his Naturalis Historia from 77 AD, provides accounts of one Roman who became so excessively fond of a lamprey that, when it was dead, “he could not hold but weepe for love of it” (Holland 1601). When a Roman noblewoman later inherited this lamprey pond, she took such a liking to another lamprey that she reportedly adorned its gills with golden earrings. Pliny, however, painted a less favorable picture of lampreys when he recounted that the orator Vedius Pollio “kept in ponds huge lampreys that had been trained to eat men, and he was accustomed to throw to them such of his slaves that he desired put to death.” This misunderstanding of—but apparent fascination with—the nature of lampreys persisted well into the twelfth century, as this excerpt from the Aberdeen Bestiary (1200) indicates: “Lampreys, it is said, are of the female sex only and conceive from intercourse with snakes; as a result, fishermen catch it by calling it with a snake’s hiss.”

In medieval Europe, lampreys were regularly captured and consumed by kings and commoners alike. They were especially appreciated during fasting periods ­because their taste was considered much meatier than that of most other fishes. The ruling monarchs of England were particularly fond of lampreys (both sea lamprey and European river lamprey Lampetra fluviatilis), which they would obtain from the fisheries of Gloucester on the River Severn. King Henry I (1068–1135) is said to have died following an overindulgence of lampreys while on a military campaign in northern France, although it is disingenuous to suggest that it was a direct result of the meal itself (Dickens 1852; Deshpande 2002). In 1200, King John fined the city of Gloucester 40 marks (approximately £ 362,000 or $ 578,000 today) for forgetting to send him a lamprey pie at Christmas. In 1242, King Henry III was reported to have paid 12 pounds, seven shillings, and three pence for 188 lamprey, equivalent to approximately £ 168,000 ($ 268,000) today (Skinner 2012). A baked lamprey pie continues to be presented to the ruling monarch of England on special occasions; Queen Elizabeth II received one on the occasion of her coronation in 1952 and for her Silver Jubilee in 1977 (Renaud 2011; The Telegraph 2012). For the monarch’s Diamond Jubilee in 2012, however, the city of Gloucester had to use Great Lakes sea lamprey because none were to be found in the River Severn (The Telegraph 2012). However, given the concern for the “surfeit” of mercury in Great Lakes sea lamprey (see Chap.  8), it is not known if the lamprey pie was eaten by the Queen. Fans of the television series Game of Thrones (which is based on the fantasy novels, collectively entitled A Song of Ice and Fire, by George R. R. Martin) will be familiar with lamprey pie.

In the eighteenth century, however, lampreys (particularly the European river lamprey) came to be exploited more and more efficiently in England and, given their apparent abundance, declined in value—culturally and monetarily. In the ­River Thames, for example, European river lamprey were captured by the ­hundreds of thousands (Wheeler 1979), and sold (for only £ 2–5 per 1000 lamprey; ­Hardisty 2006) to European cod fishermen for use as bait (see Chap.  8). According to ­Lanzing (1959), live lamprey would be held on board ship in large holding tanks and “every ship’s crew included a ‘lamprey biter’ who killed the animal by a bite to the head thus destroying the brain. The paralyzed lamprey was then placed on an angling hook.” The only commercial lamprey fishery currently operating in the U.K. (in the River Ouse) again supplies European river lamprey as bait for angling (although, until 2011, the lamprey were technically captured as “by-catch” in a licensed eel Anguilla anguilla fishery; Masters et al. 2006; Foulds and Lucas 2014).

Exploitation of European river lamprey for food, however, continues throughout much of northern Europe (e.g., in Finland, Sweden, Latvia, Estonia, Lithuania, Poland, and Russia; Sjöberg 2011; Lajus et al. 2013), and sea lamprey is fished commercially in France (Beaulaton et al. 2008), Spain (Gradín 2010), and Portugal (Quintella 2006; Mateus et al. 2012). Both species are still regarded as local delicacies, particularly in recent decades when—due largely to the effects of industrialization and urbanization—they have become scarcer (see Chap.  8). In the 1960s, for example, gourmets in Poland and Lithuania were reported to wait with great anticipation for the by-then infrequent appearance of lamprey in the fish markets or a sign (e.g., the sound of a rifleshot or the sight of a red flag over a beach snack bar) “­proclaiming that fresh, roasted lampreys were available” (Sterba 1962). The purchase of these river lamprey, however, depended on “a well-filled purse” (Sterba 1962). Sea lamprey fetch even higher prices; a single sea lamprey in Portugal can cost € 45–50 (over $ 60) during the peak of the season (and, unfortunately, makes them a popular target for poachers; Quintella 2006; Andrade et al. 2007). In the 1990s, the idea of marketing sea lamprey from the North ­American Great Lakes (given their surfeit there) in Portugal and Spain was explored, but Great Lakes lamprey have mercury levels that are too high to meet European Union standards (MacEachen et al. 2000; Jeffrey L. Gunderson, Minnesota Sea Grant, Duluth, MN, personal communication, 2014). Lampreys figure prominently on the coats of arms in at least two European municipalities—Arbo in northwestern Spain and Nakkila in southwestern Finland (Municipality of Arbo 2010; Radio UusJussi 2013)—and ­lamprey festivals are held annually in Arbo and in villages in Latvia (e.g., ­Carnikava) and Portugal (e.g., Montemor-o-Velho).

Commercial fisheries for other lamprey species have been more limited, but nevertheless indicate the historical local significance of these species. There were important fisheries for the Caspian lamprey Caspiomyzon wagneri in Russia and ­Azerbaijan into the twentieth century, but these fisheries are no longer viable (Holčík 1986). Pacific lamprey were fished commercially in the Columbia River basin in Oregon and Washington state in the early twentieth century, but catches of this species were largely used in fishmeal (e.g., for hatchery salmon) or as teaching material in comparative vertebrate anatomy classes (Close et al. 2002; Renaud 2011). The Arctic lamprey is harvested commercially in Japan, and a small commercial fishery commenced for this species in Alaska in 2003 (Hayes and Salomone 2004).

1.2.2 Ecological Significance of Lampreys

Regardless of their direct value to humans as food, lampreys are also known to play important ecological roles at all stages of their life cycle. Larval lampreys are key components at the base of the food chain, and they can represent a large portion of the biomass in streams where they are abundant. Beamish and Youson (1987), for example, showed that the North American river lamprey Lampetra ayresii is the dominant organism by weight in the bottom sediments of the Fraser River in ­British Columbia. Larval lampreys are important in nutrient cycling, facilitating the conversion of nutrients derived from detritus and algae into stored biomass (see Chap.  3). Experimental removal of larval Pacific lamprey from the South Fork Eel River in north-central California appeared to impact the detrital processing of the river (Timothy Wootton, University of Chicago, Chicago, IL, personal communication, 2014). In anadromous species, the carcasses of spawned out lampreys are thought to provide a significant amount of marine-derived nutrients to freshwater aquatic ecosystems, in the same way that Pacific salmon do (e.g., Naiman et al. 2002). Lampreys are also ecosystem engineers; the burrowing and feeding activities of larval lampreys significantly increase substrate oxygen levels (Shirakawa et al. 2013) and the nest-building activity of spawning lampreys increases ­streambed complexity in ways that appear to benefit other fishes and stream invertebrates (Sousa et al. 2012; Hogg et al. 2014).

Lampreys are a food source for other animals (Cochran 2009), both ­during the larval stage (e.g., during emergence from their nests or during scouring events that dislodge larvae from their burrows) and then again—and particularly—­during downstream migration, following metamorphosis. Outmigrating lampreys can ­significantly contribute to the diet of predatory fishes, birds (e.g., gulls and terms), and pinnipeds (see Close et al. 2002). Furthermore, in most anadromous species, outmigration appears to occur in pulses (correlated with abrupt ­increases in ­discharge; see Chap.  3), and this glut of young adult lampreys may buffer predation on commercially valuable juvenile salmonids, during their downstream ­migration and as they enter the ocean. Roffe and Mate (1984), for example, found that ­Pacific lamprey were the principal prey of pinnipeds in the lower reaches and estuary of the Rogue River in Oregon (constituting a higher proportion of their diet, by both weight and frequency, than salmonids). Similarly, in Scotland, sawbill ducks ­Mergus ­merganser have been reported to be “stuffed” with young lampreys rather than with commercially valuable salmon smolts (Ayrshire Rivers Trust, Ayr, U.K., personal communication, 2013). The extent to which feeding-phase lampreys are preyed upon, particularly at sea, is less well known. Predation is thought to be lower during this stage (Nursall and Buchwald 1972; Scott and Crossman 1973), since the adults are well dispersed. However, Cochran (2009) suggests that predation on lampreys will often go undetected, given their lack of bone and other hard structures (with the exception of their keratinized teeth; Roffe and Mate 1984) that would be resistant to digestion. Adult lampreys are again concentrated, and thus vulnerable to predation (human and other), during their upstream migration and spawning. For example, Steller sea lions Eumetopias jubatus at the mouth of the Klamath River feed largely on upstream migrating Pacific lamprey (Beamish 1980). During and after spawning—which occurs during daylight hours in shallow streams—they are fed on by a variety of aquatic, aerial, and terrestrial predators (Scott and Crossman 1973).

Parasitic lampreys are also important predators in aquatic ecosystems, thus ­constituting key components at both the base and top of the food chain. Parasitic lampreys are generally not viewed very favorably by commercial fishers or anglers since, as noted by Cochran (1994), prey species used by lampreys often coincide with the commercially and recreationally important fishes preferred by humans (see Renaud and Cochran in press). For example, the large (e.g., ­Pacific and sea ­lampreys) and even the smaller (e.g., North American river lamprey) anadromous lampreys, when abundant, provide competition to humans interested in Pacific ­salmon ­Oncorhynchus spp., Atlantic salmon Salmo salar, or cod Gadus spp. (Beamish and Neville 1995; Orlov et al. 2008; Renaud and Cochran in press). However, lampreys feed on a variety of fish species and even marine mammals (­Silva et al. 2014; Renaud and Cochran in press), suggesting that they may be less likely than other predators (including humans) to significantly ­deplete one or a few prey species. A notable exception is the Great Lakes sea ­lamprey; the devastating effect of this invasive species on commercial fish stocks in the ­Laurentian Great Lakes is well documented (see SLIS 1980; Marsden and Siefkes in press). However, there is no evidence that native lampreys are ­detrimental to the ecosystems in which they occur (Heard 1966; Beamish 1980; Renaud 1997; Close et al. 2002).

1.2.3 Scientific Significance of Lampreys

Lampreys are one of the oldest living groups of vertebrates, and have survived at least four of the five mass extinction events documented since the Cambrian explosion. Given their importance, therefore, as “living fossils,” lampreys provide important insight into the evolution of the vertebrates. It is no coincidence, of course, that university students everywhere have long been made to dissect lampreys during comparative vertebrate anatomy classes. Research related to general lamprey biology (particularly in support of sea lamprey control and conservation of native lampreys) is detailed in subsequent chapters of this book. The following sections, in contrast, demonstrate the relevance of lampreys and lamprey research across a wide range of disciplines.

1.2.3.1 Research Trends

Well over 20,000 scientific manuscripts have been published that directly or indirectly use lampreys as a study organism. Searching the database Web of Science (Thompson Reuters) using the term “lamprey*” generated 22,239 records from 1864 until the end of 2013, and many influential papers [e.g., Schultze (1856) and Müller (1856) on ­lamprey development; see Richardson et al. (2010)] predate this time period. For comparison, the search term “fish*” located 2,348,556 papers from 1864 to 2013. Granted, not all records for fishes will have been retrieved with this broad search term but, considering that extant lampreys comprise only 0.14 % of the almost 28,000 recognized species of living fishes (Nelson 2006), the observation that they represent as much as 0.95 % of the papers written on fishes is a testament to their scientific importance. Other numerically larger (e.g., cartilaginous fishes with almost 1,000 described species) and more commercially valuable (e.g., salmonids) taxa certainly receive more attention in the scientific literature. A total of 53,977 (2.30 % of the total for fishes) and 147,404 (6.38 %) records were retrieved using “chondrichthy*” and “­salmon,” respectively; we acknowledge that the search term “salmon” will not include all papers on salmonids, but the search term “salmon*” recovered a very large number of papers on salmonella. Compared to lampreys, other species-poor but evolutionarily important groups of fishes (Fig. 1.2a) are not as well represented: only 5,036 records (0.21 % of the total for fishes) were retrieved for hagfishes (search term “hagfish*”); 1,871 records (0.08 %) were retrieved for lungfishes (search term “lungfish*”); and 18,091 records (0.77 %) were retrieved for sturgeons (search term “sturgeon*”).

Furthermore, there has been a clear increase in the number of papers written on lampreys in recent decades (Table 1.1). From 1864 until 1943, an average of only 30 papers that directly or indirectly used lampreys as a study organism were published per decade. Since 1984, between 1,739 and 8,264 lamprey papers were published per decade (i.e., almost 70 per month in 2004–2013). Even accounting for the dramatic increase in the number of scientific papers published in all disciplines over this time period, we still see a proportionally greater increase in lamprey papers; from 1864 until 1943, papers that directly or indirectly dealt with lampreys represented 0.4 % of all papers on fishes versus 1.1 % and 0.9 % in the last two decades (Table 1.1).

Table 1.1

Number of papers published between 1864 and 2013 that employed lampreys as direct or indirect study organisms, that is, that were retrieved in the database Web of Science (Thompson Reuters) using “lamprey*” as the search term. Number of papers is given per decade for each time interval indicated; number of papers is approximate. Number of papers retrieved using “fish*” as the search term is also given, as is the number of lamprey papers as a percentage of all fish papers. Total number of lamprey papers retrieved for 1864–2013 using research areas defined by Web of Science (and including “Control” as an additional search term of interest) is listed (note that research areas are not mutually exclusive, i.e., a manuscript classified as “Cell Biology” may simultaneously be defined as “Immunology”). For each time interval, the percentage of lamprey papers retrieved for each research area is given, the maximum percentage for each research area is in bold, and the trend over time for that research area (i.e., increasing ↑ or decreasing ↓ in proportion) is noted

 

Trend

2004–2013

1994–2003

1984–1993

1974–1983

1964–1973

1954–1963

1944–1953

1934–1943

1864–1933*

Total

1864–2013

Lamprey*

 

8,264

5,620

1,739

1,174

813

316

115

74

34

18,352

Fish*

 

958,685

489,141

267,130

335,783

168,934

48,195

21,274

18,687

8,161

 

Percent Lamprey*

0.9

1.1

0.7

0.3

0.5

0.7

0.5

0.4

0.4

 

Zoology

13.6

13.2

13.1

15.7

17.6

26.6

35.8

29.8

51.9

5,455

Neuroscience/Neurology

7.1

11.3

11.5

7.2

5.4

5.4

2.6

3.2

1.1

3,380

Biochemistry/Molecular Biology

9.2

9.5

8.7

7.8

8.9

5.6

0.7

1.1

1.6

3,335

Physiology

 

4.1

6.2

7.8

6.8

5.4

1.2

1.3

4.3

2.7

2,201

Cell Biology

 

2.9

5.3

8.5

6.2

5.2

2.1

0.0

0.0

0.0

1,982

Environmental Science/Ecology

6.7

4.7

3.6

4.9

5.9

2.1

2.0

1.1

1.6

1,941

Endocrinology/Metabolism

 

2.7

4.7

6.7

7.2

6.2

4.5

3.3

6.4

0.5

1,844

Anatomy/Morphology

2.5

3 .4

6.3

8.2

6.6

6.4

4.6

10.6

7.0

1,764

Developmental Biology

3.8

3.8

4.6

5.5

5.4

7.8

11.9

8.5

9.2

1,674

Marine/Freshwater Biology

5.8

3.9

2.3

3.5

2.2

0.4

0.7

0.0

2.2

1,473

Life Sciences/Biomedicine

4.6

3.4

3.0

3.8

5.3

14.4

11.9

24.5

17.3

1,570

Genetics/Heredity

6.6

4.0

1.8

1.4

1.2

0.4

0.0

0.0

0.0

1,407

Control

4.5

5.2

2.2

2.1

2.5

3.9

4.0

3.2

0.5

1,402

Evolutionary Biology

4.7

3.4

2.1

1.7

2.2

0.6

2.0

1.1

1.1

1,201

Behavioral Science

4.5

3.6

2.4

1.2

0.8

0.8

0.0

0.0

0.5

1,157

Biodiversity/Conservation

2.4

1.9

1.4

1.3

3.5

9.5

15.2

3.2

0.0

792

Immunology

2.4

1.8

2.3

2.2

2.0

0.4

0.0

0.0

0.0

804

Reproductive Biology

 

1.8

1.6

1.8

2.2

2.2

1.4

0.7

0.0

0.5

688

Cardiovascular System/Cardiology

 

0.7

0.9

2.1

3.2

4.7

2.7

2.6

2.1

1.6

637

Pharmacology

 

1.9

2.1

2.2

2.0

1.6

0.6

0.0

0.0

0.0

754

Fisheries

2.5

1.3

0.9

1.7

1.6

1.6

0.0

0.0

0.0

625

Nutrition/Dietetics

1.2

0.9

1.0

1.2

0.6

0.4

0.0

1.1

0.5

383

Biophysics

1.2

1.4

1.0

0.8

0.5

0.6

0.0

0.0

0.0

413

Respiratory System

 

0.7

0.8

1.1

1.2

1.0

0.0

0.7

0.0

0.0

327

Toxicology

 

0.7

0.7

0.8

0.8

0.9

0.4

0.0

0.0

0.0

275

Computational Biology

1.0

0.6

0.6

0.3

0.2

0.0

0.0

0.0

0.0

236

Palaeontology

0.3

0.2

0.1

0.1

0.2

0.0

0.0

0.0

0.0

80

It is also of considerable interest to see how the focus of lamprey research has shifted since 1864. Using the research areas defined by the database Web of Science (and including “Control” as an additional search term of interest) shows a shift in research focus from more basic descriptions of lamprey biology to their use as model systems in the fields of evolutionary development, biomedical research, and bioengineering (Table 1.1). Whereas such research areas as “Zoology,” “Developmental biology,” and “Anatomy/morphology” represented as much as 51.9, 11.9, and 10.6 %, respectively, of all lamprey records retrieved in decades prior to 1953, they made up only 13.6, 3.8, and 2.5 % of retrieved papers in 2004–2013. In contrast, research areas such as “Neuroscience/neurology,” “Biochemistry/molecular biology,” and “Genetics/heredity” not surprisingly increased in prominence from < 2 % of all lamprey papers prior to 1943 to 6.6–9.2 % in 2004–2013. Exciting discoveries in some of these research areas will be discussed in Sect. 1.5 and in subsequent chapters (e.g., see Chaps.  2,  4 and  7; Lee and McCauley in press). Not all increases depended on novel technologies; publications related to “Ecology/environmental science,” “Marine/freshwater biology,” and “Behavioral science” represented 0.5–2.2 % of all publications prior to 1943 and 4.5–6.7 % in 2004–2013. Much of this research directly or indirectly (e.g., through a better understanding of the basic biology and ecological requirements of these species) relates to the control of invasive sea lamprey or the conservation and management of native species (see Chaps.  3,  5,  6 and  8; Marsden and Siefkes in press).

The majority of research conducted on lampreys has focused on relatively few species. Perhaps not surprisingly, over 60 % of all records retrieved through Web of Science for the 1864–2013 interval dealt directly or indirectly with sea lamprey (Table 1.2). Research on European river lamprey and European brook lamprey Lampetra planeri comprised 14 % and 6 % of the total, respectively, and records retrieved for Arctic lamprey represented 4.9 % of the total. Despite increased interest in native lampreys in recent decades (e.g., anadromous Pacific lamprey and the many freshwater parasitic and non-parasitic lampreys with more restricted distributions), research on these species is still relatively limited. It is our hope that this is changing. Of necessity, we must often extrapolate among lamprey species and such extrapolations appear to be justified in many respects (e.g., given similarities in the ecology of larval lampreys: see Chap.  3). However, it is also becoming clear that there are, in many cases, pronounced species-specific differences (e.g., with respect to passage abilities: see Chap.  5; mating systems: see Chap.  6; and variability of life history type: Docker and Potter in press). These differences have significant management implications (Clemens et al. 2010; see Chaps.  5 and  8). This book has therefore attempted to include broader coverage of these other species (see Sect. 1.3.1), and we look forward to a greater research emphasis on these species.

Table 1.2

Number of papers published between 1864 and 2013 that were retrieved in the database Web of Science (Thompson Reuters) on each of the following species or groups of lampreys (i.e., using the search terms indicated), and percentage of total. For some species (e.g., Pacific lamprey, Arctic lamprey, American brook lamprey) search terms were chosen to maximize the number of papers retrieved, given changes in classification over time. (see Chap.  2)

Species or group

Search term

Number

Percent of total

Sea lamprey Petromyzon marinus

Petromyzon marinus

7,165

60.7

European river lamprey Lampetra fluviatilis

Lampetra fluviatilis

1,657

14.0

European brook lamprey Lampetra planeri

Lampetra planeri

710

6.0

Arctic lamprey Lethenteron camtschaticum

Lamprey* and japonic*

559

4.9

 

Lamprey* and camtschatic*

21

 

Ichthyomyzon spp.

Ichthyomyzon

536

4.5

Pouched lamprey Geotria australis

Geotria

303

2.6

Pacific lamprey Entosphenus tridentatus

Lamprey* and tridentat*

257

2.2

Eudontomyzon spp.

Eudontomyzon

152

1.3

Mordacia spp.

Mordacia

102

0.9

Far Eastern brook lamprey Lethenteron reissneri

Lamprey* and reissneri

96

0.8

American brook lamprey Lethenteron appendix

American brook lamprey*

68

0.6

Western brook lamprey Lampetra richardsoni

Lampetra richardsoni

61

0.5

Caspian lamprey Caspiomyzon wagneri

Caspiomyzon

44

0.4

North American river lamprey Lampetra ayresii

Lampetra ayresi*

40

0.3

Tetrapleurodon spp.

Tetrapleurodon or lamprey* and spadice* or lamprey* and gemin*

25

0.2

  

11,796

 

1.2.3.2 Evolutionary Significance of Lampreys

Lampreys have received considerable attention in evolutionary studies, given their important phylogenetic position. They are the extant representatives of a lineage that diverged from the ancestor to the jawed vertebrates approximately 500 million years ago (Janvier 2007). Due to their relatively conserved morphology over the past 360 million years (Gess et al. 2006), these “living fossils” (a term first coined by Charles Darwin in his On the Origin of Species) are providing invaluable insight into the events that occurred at the dawn of vertebrate evolution and during the subsequent evolution of the gnathostomes (Janvier 1996; Kawauchi and Sower 2006; Osório and Rétaux 2008).

The origin of vertebrates represents one of the major jumps in evolution (Griffith 1994), and there is a large gulf between the non-vertebrate chordates—the lancelets (Cephalochordata) and tunicates (Urochordata), all of which are mostly-sessile marine filter feeders—and the active and morphologically complex Vertebrata. Given the relative paucity of the fossil record prior to the origin of mineralized tissue—and, of course, even well-preserved fossils provide little or no information on the physiology, development, or genomics of the organism—study of the extant ­jawless vertebrates is helping to piece together the early evolutionary history of our group (Nicholls 2009; Shimeld and Donoghue 2012).

The major vertebrate advancements include: a cranium and pronounced cephalization; a set of highly specialized paired sense organs (i.e., image-forming eyes, olfactory organs, the lateral line, and various structures derived from the lateral line that are found in the inner ear); a large brain to integrate sensory information; an axial skeleton and muscle segmentation that permits effective swimming; neural crest cells (which give rise to the craniofacial skeleton and other derivatives); more complex circulatory, respiratory, and digestive systems; a glomerular kidney; and a complex endocrine system with pituitary, pineal, thyroid, and adrenal glands (Griffith 1994; Shimeld and Donoghue 2012). These advancements permitted “the active, sentient life” that distinguishes the vertebrates from the non-vertebrate chordates (Griffith 1994). Cyclostome paraphyly (i.e., with hagfishes representing an earlier offshoot from the craniate lineage) implied a more “gradual assembly of vertebrate characters” (Shimeld and Donoghue 2012). The strong support now available for cyclostome monophyly (see Sect. 1.1.1) suggests an even more phenotypically complex ancestral vertebrate, and further widens the gulf between the vertebrate and non-vertebrate chordates (Shimeld and Donoghue 2012).

Studies in lampreys have been instrumental in furthering our understanding of the evolution of vertebrate locomotion (e.g., Bicanski et al. 2013; Hsu et al. 2013), the vertebrate eye (e.g., Collin 2010; see Collin and Potter in press), and the neuroendocrine system (e.g., Kawauchi and Sower 2006; see Chap.  7). Up until the late 1970s, for example, it was thought that the agnathan vertebrates did not have the same neuroendocrine control of reproduction that is seen in the gnathostomes, again suggesting a more gradual evolution of complexity in the vertebrates. More than 30 years of research by Stacia Sower and colleagues, however, has firmly established that lampreys do have a complex hypothalamic-pituitary-gonadal axis and thus shows this to also be a vertebrate innovation and seminal event that emerged prior to or during the differentiation of the ancestral agnathans. Much has now been learned about the evolution of the key neuroendocrine hormones, especially the pivotal gonadotropin-releasing hormones, in vertebrates through this research on lampreys (see Chap.  7). Evidence for neuroendocrine control of reproduction in hagfishes is more recent and far less extensive, but it likewise suggests that hagfishes possess a hypothalamic-pituitary system (Sower et al. 1995; Uchida et al. 2010, 2013).

Comparisons between lampreys and jawed vertebrates have also been critical for shedding light on the evolution in the gnathostome lineage of articulated jaws and paired fins and appendages. Lampreys are being increasingly used in evo-devo studies, exploring the evolution and development, for example, of the neural crest and skeletal muscle of vertebrates, and the hinged jaw and paired appendages of gnathostomes (see Kuratani 2005, 2012; Shigetani et al. 2005; Osório and Rétaux 2008; Shimeld and Donoghue 2012; Lee and McCauley in press).

Lampreys and hagfishes have also been key to elucidating the evolution of adaptive immunity in vertebrates. Adaptive immunity, also known as acquired immunity, is the ability to recall previous encounters with a “nearly unlimited variety of antigens” (Minton 2009), thus leading to a more rapid and efficient response to subsequent encounters with the same pathogen. This antigen-specific memory, which is the basis of vaccination, leads to a rapid and efficient secondary immune response but requires “extraordinarily diverse repertoires of somatically assembled antigen receptors” (Boehm et al. 2012). Adaptive immunity is considered another hallmark of the vertebrates but, unlike the jawed vertebrates that recognize antigens using immunoglobulin-based B-cell and T-cell receptors, extant agnathans use variable lymphocyte receptors (VLRs). Both jawless and jawed vertebrates create the necessary diversity of antigen receptor genes through gene rearrangement, but the mechanisms are different in the two vertebrate lineages. In lampreys and hagfishes, antigen receptor diversity is generated through the somatic assembly of variable leucine-rich repeat (LRR) modules, whose product is expressed clonally on lymphocytes (Kasahara 2013; Kishishita and Nagawa 2014). However, despite the ­independent evolution of alternative antigen receptor systems in jawless and jawed vertebrates, it also appears that their adaptive immune systems share some fundamental similarities. In particular, recent evidence suggests that both agnathan and gnathostome vertebrates have three major lymphocyte lineages (i.e., that lampreys and hagfishes have one B-cell-like lineage and two T-cell-like lineages; ­Hirano et al. 2013; Li et al. 2013), suggesting that these cell lineages were present in the common vertebrate ancestor before the advent of the different antigen receptor gene rearrangement systems (Kasahara 2013; Kishishita and Nagawa 2014). In both agnathans and gnathostomes, only one type of antigen receptor is expressed per lymphocyte, and the three different lineages of lymphocytes express three different antigen receptors (Kishishita and Nagawa 2014). Given the intriguing similarities and differences between the agnathan and gnathostome systems, further study of the lamprey (and hagfish) adaptive immune system will improve our fundamental understanding of “this elegant system” (Kishishita and Nagawa 2014), and can potentially improve treatment for people with faulty immune systems (Boehm et al. 2012).

Evidence has recently emerged suggesting that “hemoglobin” has also evolved independently in agnathan and gnathostome vertebrates. Phylogenetic analysis of the vertebrate globin gene superfamily suggests that a specialized oxygen transport function was acquired independently in paralogous globin genes (i.e., genes that diverged after a gene or genome duplication event) in jawless and jawed vertebrates (Hoffmann et al. 2010). These results indicate that lamprey and hagfish hemoglobin is most closely related to the gnathostome cytoglobin protein. The two vertebrate lineages therefore appear to make use of functionally similar (but “independently invented”) respiratory pigments to increase the oxygen carrying capabilities of the blood, a key physiological innovation that permitted larger body size and “opened up new opportunities for the evolution of aerobic metabolism” in vertebrates (Hoffmann et al. 2010).

The recent publication of the sea lamprey genome assembly (Smith et al. 2013)—and other advances in developmental biology and molecular genetics (e.g., McCauley and Bronner-Fraser 2006; Nikitina et al. 2009; Heath et al. 2014; see Lee and McCauley in press)—now promise to lead to further advances in many of the research areas described above (and countless others). Freely available as a public resource, sequencing of the sea lamprey genome is already providing valuable information on genes related, for example, to olfaction (Libants et al. 2009), neuron regeneration in the central nervous system (Smith et al. 2011), and the ­neuroendocrine control of reproduction (Decatur et al. 2013). By virtue of its phylogenetic position, the sea lamprey genome is “uniquely poised to provide insight into the ancestry of vertebrate genomes and the underlying principles of vertebrate biology” (Smith et al. 2013). One major finding that emerged from sequencing of this genome is confirmation that two rounds of genome duplication likely occurred prior to the agnathan-gnathostome divergence (Barucchi et al. 2013; Decatur et al. 2013; Smith et al. 2013; see Chap.  7). Although it has long been thought that two large-scale genome duplications occurred during the evolution of early vertebrates (Ohno 1970), there has been continuing controversy over whether the second duplication occurred in the lineage leading to all extant vertebrates or whether there was one round of duplication prior to and one round of duplication after divergence of the jawless vertebrates (see Kuraku et al. 2009; Shimeld and Donoghue 2012). Gene and especially genome duplication events are thought to provide genetic raw material for evolution; two rounds of whole genome duplication at the base of the vertebrate family tree (i.e., on either side of the large gulf that exists between the non-vertebrate chordates and even the earliest extant vertebrates) would have enabled the large number of vertebrate-specific innovations (Ohno 1970; Shimeld and Holland 2000).

Also of interest in this regard is the recent report of potential horizontal gene transfer (HGT) between lampreys and their teleost hosts (Kuraku et al. 2012). Highly similar sequences of a DNA transposon were discovered in multiple fishes that are phylogenetically disparate, but almost all of these fishes serve as hosts to parasitic lampreys, suggesting that these elements were transferred through ­parasite-host interactions (Kuraku et al. 2012). HGT has been well documented in prokaryotes (e.g., Gogarten et al. 2002)—and increasingly so in eukaryotes (through viral infection, phagocytosis, symbiosis, and parasitism)—and has been speculated to enhance the evolutionary potential of the recipient lineage (Koonin 2009; Wijayawardena et al. 2013).

Another feature of the sea lamprey genome that has generated interest is the observation of programmed genome rearrangement (PGR); during embryogenesis, approximately 20 % of the germline genome (hundreds of millions of base pairs) is lost from somatic cell lineages (Smith et al. 2009). Although a small number of programmed local rearrangements is typical during development in vertebrates (and more extensive genomic reorganizations have been noted in some invertebrate species; e.g., Goday and Esteban 2001; Bachmann-Waldmann et al. 2004; ­McKinnon and Drouin 2013), lampreys and hagfishes (Kubota et al. 1997; Kojima et al. 2010) are the only vertebrates known to undergo broad-scale PGR. Programmed ­genome rearrangement and loss may represent an ancient biological strategy to ensure that pluripotential functions are segregated to the germline, thereby preventing the potential for somatic misexpression (Smith et al. 2009, 2012). Understanding the mechanisms by which agnathan vertebrates regulate programmed changes to their genomes has the potential to help understand the dysregulated changes that give rise to cancers and other genomic disorders (Smith et al. 2009).

Lampreys (and hagfishes) are thus providing important and promising model systems in our quest to better understand the evolutionary history of the vertebrates. Neither lampreys nor hagfishes are directly representative of the common vertebrate ancestor (specializations unique to each lineage appear to have arisen early in phylogeny and then been retained), but comparisons among lampreys, hagfishes, and gnathostomes are providing great insights into the morphology, physiology, development, and genomics of the common ancestor to all vertebrates (Janvier 2007; Shimeld and Donoghue 2012). This exciting topic is reviewed very briefly here; interested readers are directed to the many excellent reviews on this topic (e.g., ­Shigetani et al. 2005; Osório and Rétaux 2008; Kuratani 2012; Shimeld and ­Donoghue 2012; Lee and McCauley in press) and are encouraged to follow what are sure to be exciting advancements in the next decade and beyond.

1.2.3.3 Use of Lampreys in Biomedical and Biomimetic Studies

Lampreys have long been used as models in biomedical research (Table 1.1). For example, Sigmund Freud, while a young medical student, studied the spinal ganglia and spinal cord in the lamprey (Freud 1877, 1878). Such biomedical research continues today and, recently, a biorobotic system inspired by lampreys has been developed as an investigative tool for studying high level motor tasks. A brief overview of some areas in which lampreys may provide insights into the treatment of human health problems and as a prototype for studies on vertebrate locomotion is provided below.

Anti-coagulants

The salivary glands of blood-feeding organisms have long been of interest to pharmacologists and biochemists, due to the bioactive substances that they contain (Odani et al. 2012). The European medicinal leech Hirudo medicinalis, for example, was used therapeutically as far back as 2,500 years ago (e.g., with Hippocrates advocating bloodletting as a means of balancing “the four humors”). Its saliva contains approximately 30 biologically active substances, including the peptide hirudin to keep the blood flowing and enzymes to anesthetize the host and reduce inflammation at the site of the bite (Nature 2012). Hirudin was isolated in the 1950s, and recombinant techniques are now used to produce hirudin for treatment of blood coagulation disorders (Rydel et al. 1991). The salivary gland secretions of many other hematophagous animals have been studied for their possible biomedical applications; these include insects such as mosquitoes, ticks, and the kissing bugs Rhodnius prolixus and Triatoma infestans, as well as vampire bats Desmodus rotundus, with their colorfully named anti-coagulant “draculin” (see Basanova et al. 2002; Odani et al. 2012). The anti-coagulating action of the buccal gland secretions in parasitic lampreys was identified by Gage and Gage-Day in 1927, but the biochemical nature of these secretions has received little attention until recently. The diverse bioactive proteins (termed “lamphredin” by Lennon in 1954) are being investigated in the Arctic ­lamprey, and have been shown to have fibrinogenolytic and vasodilatory properties (Ito et al. 2007; Xiao et al. 2007, 2012). In addition to these proteinaceous components, Odani et al. (2012) discovered L-3-hydroxykynurenine O-­sulphate in the buccal glands of this species; this molecule, remarkably, was found in Rhodnius prolixus and Triatoma infestans in the 1960s (see Odani et al. 2012). The buccal gland ­secretions of parasitic lampreys are thus another potential source for the development of novel anti-coagulants, local anesthetics, immunosuppressants, and thrombolytic agents (Xiao et al. 2012).

Biliary Atresia

Research on lampreys may also improve our understanding of a medical condition known as cholestasis, whereby bile is unable to flow from the liver to the duodenum and, in particular, biliary atresia, the most common cause of cholestasis during infancy (Youson 1993; Morii et al. 2012; Suchy 2013). In the congenital form of biliary atresia, babies are born lacking a common bile duct between the liver and small intestine, resulting in jaundice, malabsorption of nutrients and growth retardation, fat-soluble vitamin deficiencies, and eventually cirrhosis. While biliary atresia is rare, it is fatal if a liver transplant is not possible (Youson 1993; Morii et al. 2012). Lampreys are an excellent—and again unparalleled—vertebrate model system in which to study cholestasis. Larval lampreys possess an intrahepatic gallbladder and a biliary tree that is well equipped for the storage, transport, and elimination of bile into the intestine; at metamorphosis, however, lampreys undergo a programmed loss of the gall bladder and biliary tree (see Chap.  4) and yet are able to survive without these structures—for several years in some parasitic species (Youson 1993). As expected, bile pigments (­bilirubin and biliverdin) are not detected in the serum of larval lampreys, but become detectable after biliary atresia (Makos and Youson 1987). However, serum concentrations following metamorphosis are lower than expected (e.g., compared to humans suffering from jaundice), suggesting either storage of bile in the liver or another organ or an alternate mechanism for the transport and elimination of these potentially toxic pigments (Makos and Youson 1987; Youson 1993). Bilirubin concentration has been shown to increase dramatically in the liver and caudal intestine of sea lamprey following loss of the larval bile ducts (Langille and ­Youson 1983; Makos and Youson 1988), leading to suggestions that bilirubin in the liver may be mobilized and transported (via the blood) to the caudal intestine for subsequent elimination (Langille and Youson 1983; Youson 1993). Bilirubin and biliverdin may be bound for transport and detoxified by lamprey-specific serum proteins (Filosa et al. 1982). Serum bilirubin and biliverdin concentrations were higher in upstream migrants, but were only slightly above normal values observed in humans (Makos and Youson 1987). What is more remarkable are reports of one population of American brook lamprey Lethenteron appendix larvae with serum biliverdin concentrations ranging from 142 to 305 μmol/L (Eng and Youson 1991). In this population, the bile ducts are infested with larval nematodes (Pybus et al. 1978), causing bile pigment regurgitation into the blood. The highest value recorded in a human with biliverdinemia is 46 μmol/L (Greenberg et al. 1971), and yet there is no evidence of deleterious effects in these larvae (Eng and Youson 1991). Thus, juvenile and adult lampreys apparently respond to the normal programmed loss of the gall bladder and biliary tree by using alternate mechanisms for the transport and elimination of bile pigments whereas, under conditions of abnormal cholestasis, larvae appear able to cope with very high levels of these otherwise toxic bile pigments. Recent studies have identified apoptosis as an early event in bile duct loss in induced (Boomer et al. 2010) and spontaneous (Morii et al. 2010) metamorphosis, and have investigated the way in which lampreys are able to deal with cytotoxic bile salts (i.e., in addition to bile pigments) following biliary atresia (Yeh et al. 2012; Cai et al. 2013).

Iron Loading

Lampreys could provide insights into treatment for people suffering from hemochromatosis, a genetic condition in which the body absorbs an excessive amount of iron from the diet. In individuals with hemochromatosis, iron continues to be absorbed even after the body’s daily requirements are met, and this excess is stored in different organs and tissues (e.g., liver, heart, pituitary gland; Nichols and Bacon 1989). Hereditary hemochromatosis is the most common single-gene disease in western populations, affecting 1 out of every 200–300 people (American Diabetes Association 2013). Once diagnosed, it can be managed by the regular removal of blood but, if untreated, it can result in chronic fatigue, arthritis, diabetes, heart and liver disease, and may eventually lead to death (Nichols and Bacon 1989). Given their sanguivorous foraging strategy, parasitic lampreys ingest large amounts of iron, and have a unique capacity to store and tolerate high concentrations of iron in various body tissues (e.g., liver and adipose tissue; Tsioros et al. 1996; Tsioros and Youson 1997). Another sanguivorous vertebrate, the vampire bat—despite a daily iron intake 800-fold greater than that of humans—controls iron content by controlling rate of absorption (Morton and Wimsatt 1980; Morton and Janning 1982). Furthermore, exceptional iron concentrations in lampreys are not just observed in blood-feeding adults; larvae also show very high iron concentrations, apparently as the result of maternal transfer (probably during vitellogenesis) and uptake from the substrate (Tsioros et al. 1996). Larval lampreys accumulate iron in their blood and nephric fold at levels that would be toxic to other vertebrates: compared with 127 μg/100 mL in the serum of a normal average man (Underwood 1977), levels ranging from 5,119 to 26,773 μg/100 mL have been reported in larval lampreys (e.g., Macey et al. 1982a, 1985; Macey and Potter 1986; Youson et al. 1987). Plasma iron concentrations decline markedly at metamorphosis (e.g., Macey et al. 1982b), but iron concentration in the liver shows a dramatic increase (Harris et al. 1990); by the end of metamorphosis, lamprey hepatocytes resemble the iron-loaded hepatocytes seen in humans suffering from hemochromatosis (Youson et al. 1983). Since neither larvae nor adults show any deleterious effects as a result of this excess iron, lampreys are an excellent model system to elucidate the biochemical mechanisms by which they counteract the problems associated with iron loading in other vertebrates (Youson et al. 1983; Tsioros and Youson 1997; Macey et al. 1988). The activity of detoxifying enzymes responsible for minimizing the production of hydroxyl radicals (e.g., superoxide dismutase in the liver; Macey et al. 1988; Harris et al. 1990, 1995) and the nature of the iron-binding proteins in the plasma (e.g., ferritin; Macey et al. 1982b; Andersen et al. 1998) have received some attention (see Chap.  4), but beg further study.

Spinal Cord Regeneration

The lamprey central nervous system (CNS) shares its basic organization and structure with other vertebrates (Rovainen 1979; Grillner and Jessell 2009), but is characterized by two features in particular that have led to its extensive use as a model system in neurological studies. Not only might the comparatively simple brain and neural networks reflect the structure of early vertebrate ancestors, but lampreys are endowed with both unusually large (“giant”) reticulospinal (RS) neurons and the ability to recover nearly full function after complete spinal cord transection (Rovainen 1976). The large size of both the somata and axons of the giant RS neurons allows for microinjection of substances (e.g., tracers, antibodies, recombinant proteins) for experimental manipulation, and allows detailed examination of their responses to injury and regeneration (Smith et al. 2011). In most vertebrates, including humans, severe spinal cord injury results in permanent loss of voluntary motor control below the lesion site due to the low regenerative capacity of injured RS neurons (Bradbury and ­McMahon 2006). In contrast, lampreys are capable of spontaneous functional recovery due to the regeneration of RS axons, even following complete spinal cord transections (Cohen 1988; Cohen et al. 1988, 1989; Rodicio and Barreiro-Iglesias 2012). In fact, lampreys are the only vertebrates for which sufficient experimental data exist to satisfy the criteria for functional spinal cord regeneration after injury, as defined by the National Institutes of Neurological Disorders and Stroke (Cohen et al. 1988, 1989). With lampreys as a model, we may be able to better understand what factors promote or inhibit regeneration (e.g., Smith et al. 2011; Lau et al. 2011, 2013; Pale et al. 2013; Zhang et al. 2011, 2014) and develop novel therapies for people suffering from motor neuron disease and injury (Cornide-Petronio et al. 2011).

Biomimetics

Lampreys have also been the inspiration for biorobotic research, representing an exciting intersection between neuroscience and robotics (Ijspeert et al. 2013). Their relatively simple and well-studied neural networks and their highly efficient swimming abilities—requiring coordination between the nervous system, the musculoskeletal system, and the environment—have led to their selection as simple animal models in which to study the general principles of locomotion (e.g., Kozlov et al. 2009; Stefanini et al. 2012; Manfredi et al. 2013). Lamprey-like bioinspired robots are the basis of the European LAMPETRA (Life-like Artifacts for Motor-Postural Experiments and development of new control Technologies inspired by Rapid Animal locomotion) project (Ijspeert et al. 2013). Lamprey spinal central pattern generator networks have been explored through large-scale computer simulations (Kozlov et al. 2009); validation of these biological models is now possible with robots (Stefanini et al. 2012; Manfredi et al. 2013). Recently, a lamprey was used as the basis for a computer-simulated animal model that was able to move around an environment containing visually detectable objects. This model was able to respond to multiple, sometimes conflicting, stimuli and provided accurate predictions of how even an animal with neural lesions would subsequently interact with its environment (Kamali Sarvestani et al. 2013). In addition to providing new insights into functioning of the vertebrate central nervous system, these lamprey-inspired robots may also lead to new engineering solutions for high-performance artificial locomotion (Ijspeert et al. 2013).

1.3 Introduction to Lampreys: Biology, Conservation and Control

1.3.1 Focus of the Book

This book is intended to provide a comprehensive review of the phylogeny, evolution, ecology, and general biology of lampreys, including coverage of the conservation of native lampreys, control of the invasive sea lamprey in the Laurentian Great Lakes, and the use of lampreys as vertebrate model organisms. It is meant to provide an update to influential previous compilations, particularly Hardisty and ­Potter’s five-volume The Biology of Lampreys (Hardisty and Potter 1971a, 1972, 1981, 1982a, b) and the Proceedings of the 1979 Sea Lamprey International Symposium, published in the Canadian Journal of Fisheries and Aquatic Sciences (SLIS 1980). The advent of new technologies (e.g., improved electrofishing gear, miniaturized active and passive transmitters, molecular genetic markers)—and a continuing or renewed interest, respectively, in the control and conservation of lampreys (see Chap.  8; Marsden and Siefkes in press)—have led to many advances in our knowledge of lamprey ecology and behavior (see Chaps.  3,  5 and  6; Renaud and Cochran in press). Studies on the endogenous control of metamorphosis (see Chap.  4), lamprey pheromones (see Chaps.  5 and  6), reproductive endocrinology (see Chap.  7; Docker et al. in press), molecular phylogenetics (see Chap.  2; Docker and Potter in press), and genomics (Lee and McCauley in press) were in their infancy or unknown three decades ago.

A conscious effort has been made to include coverage of the less well-known lamprey species, if for no other reason than to highlight the gaps in our knowledge regarding them, and to include topics of interest to lamprey researchers worldwide and coverage of international conservation and management efforts. It is hoped that this book will be used as a reference for researchers working on any aspect of lamprey biology—the already-dedicated lamprey biologist (for whom there is no such thing as a surfeit of lampreys), those just starting to use lampreys as model organisms (but who appreciate the need to better understand the biology of their model), and fishery managers whose mandate is to control or conserve lamprey populations.

1.3.2 Nomenclatural Conventions

As is the case in any discipline, there exists some disagreement and confusion regarding how we name and discuss lampreys (e.g., regarding the names of the ­different stages in their complex life cycle and accepted common and scientific names for each species). The conventions adopted for this book (and the rationale for doing so) are outlined below.

What Are the Appropriate Names of Each Stage in the Lamprey Life Cycle?

Terms used to describe the stages of a lamprey life cycle are diverse and may include the following: ammocoetes (or larvae) → transformers (or metamorphosing lampreys) → juveniles (metamorphosed but sexually-immature lampreys, including macrophthalmia, downstream migrants, and feeding-phase “adults”) → upstream migrants → sexually-mature adults. There is not universal agreement, however, on the use of these terms and not all apply to all lamprey species. The term “ammocoetes” is a holdover from times when larval and post-metamorphic lampreys were considered separate genera of cyclostome fishes (with hagfishes comprising the third cyclostome genus; Duméril 1806). “Ammocoetes” literally (in Greek) means “burrower of sand” (Renaud 2011; cf. sand lances Ammodytes spp.). Decades later, Müller (1856) recognized that the ammocoete was in fact an immature developmental stage of a lamprey, yet the term was still used to refer to larval lampreys. In this book, either term is used (at the discretion of the contributing authors), although we prefer to use “larval lamprey” when writing for more general audiences as the term “ammocoetes,” in our opinion, conveys no more additional information than the more universally-understood term “larva.” The term “transformer” is more of a colloquial term, generally referring to lampreys that are undergoing metamorphosis (transformation). “Transformer” is often used in place of the less concise term “metamorphosing lamprey.” Although it is rarely used by those describing the process of metamorphosis (e.g., Youson and Potter 1979; see Chap.  4), where precision is preferred to concision—and Applegate (1950) used the less concise but more informative terms “transforming lampreys,” “lampreys in advanced stages of transformation,” “recently-transformed lampreys,” or “newly-transformed lampreys”—it is a useful term when knowledge of the specific stages of metamorphosis is either not available or not essential. Lampreys that have completed metamorphosis but are not yet sexually mature are generally referred to as “juveniles” (see Chap.  3), although this term is sometimes (but should not be) confused with the larval stage. The juvenile stage may include a “macrophthalmia” stage, the immediate post-metamorphic stage so named because of its conspicuous eyes when compared to the blind larvae. This term was apparently first applied to this stage by Maskell (1929), referring to juvenile pouched lamprey (Fig. 1.3), but the term originated in 1897 when the ­Chilean form of this species was described as Macrophthalmia chilensis (Plate 1897). Although the eyes are smaller in non-­parasitic species (see Fig.  4.1), the term has also—but less frequently—been applied to immediately post-metamorphic brook lampreys (e.g., Hardisty et al. 1970). In parasitic species, the macrophthalmia stage ends with the onset of feeding (Hardisty and Potter 1971b). After observing that feeding in Pacific lamprey commenced (in either fresh or salt water) almost immediately after the completion of metamorphosis, Beamish (1980) suggested that this species does not have a macrophthalmia stage or it is very short. The term “macrophthalmia” is still used (e.g., Moser et al. 2007; Streif 2009), but reference simply to “recently-transformed lampreys” (or “recently-transformed juveniles”) and “downstream migrants” (or “downstream-migrating juveniles”) is more common. The parasitic feeding phase is technically still part of the juvenile stage since the lampreys are sexually immature; sexual maturation (and hence “­adulthood”) occurs sometime during or upon completion of upstream migration (see Chap.  5; Docker et al. in press). In non-parasitic species, the juvenile stage is truncated or essentially non-existent (Hardisty 2006; Docker 2009); since the “sexual products are almost ripe on the eve of metamorphosis” (Berg 1948), the adult stage in brook lampreys is generally said to commence on completion of metamorphosis.

Fig. 1.3

Pouched lamprey Geotria australis “macrophthalmia” from the Okuti River in the South Island of New Zealand. Although the large eyes for which this stage is named are evident in all species (particularly parasitic species), the beautiful iridescent blue coloration seen here is unique to pouched lamprey. (Photo: © http://www.rodmorris.co.nz)

What Is the Correct Plural of “Lamprey”?

This book will follow the convention used by Nelson (2006) regarding the use of “fish” versus “fishes” and refer to individuals of more than one species as “lampreys” (e.g., lampreys have long been valued for food and ceremonial purposes, 12 sea and European river lampreys were captured) and one or more individuals of a single species as “lamprey” (e.g., 12 sea lamprey were captured, the Pacific lamprey were tracked for six months).

How Many Lamprey Species Are There?

Several years ago, the senior author of this chapter wrote in the introduction of a manuscript on lamprey phylogeny that there were “approximately 40 species of lampreys worldwide.” One of the peer reviewers asked that the exact number of lamprey species be given, but there is no exact, universally agreed upon, objectively definable number. Although most biologists (lamprey and otherwise) agree that species are evolutionarily independent units that are isolated by a lack of gene flow, there is a lack of consensus on how—in practice—these evolutionarily independent units are recognized (Mayden 1997; de Queiroz 2007). Do two groups of organisms, for example, need to exhibit diagnostic morphological differences to be recognized as distinct species or are diagnostic molecular differences, even in the absence of clear morphological differences, sufficient indication of evolutionary independence? At what point are differences among populations considered species-level differences rather than, say, differences among subspecies? Are obvious morphological differences (e.g., between parasitic and non-parasitic “paired” lamprey species as adults) necessarily indicative of a lack of gene flow? Debating the relative merits of the three most commonly applied species concepts (i.e., the morphological, biological, and phylogenetic species concepts) is far beyond the scope of this chapter (see Mayden 1997; Docker 2009), but readers should be aware that inferring the boundaries between species (and hence the number of distinct species) can be subjective. Whereas Renaud (2011) recognized 40 species in his Lampreys of the World, Potter et al. (see Chap.  2) recognize 41 species and Maitland et al. (see Chap.  8)—recognizing three recently-described “cryptic” brook lamprey species (Mateus et al. 2013) as distinct from European brook lamprey—list 44 species. It is also important to acknowledge that these numbers are for formally described species; a number of putative lamprey species (e.g., Yamazaki et al. 2003; Boguski et al. 2012) have not yet been described (see Chap.  2). Thus, a succinct answer to the question “How many lamprey species are there?” still remains “approximately 40.”

What Are the Conventions Used for Common and Scientific Names in this Book?

Within each chapter, both scientific and common names are given on first use, and common names are used exclusively thereafter. The only exception is in the chapter dealing with lamprey taxonomy (see Chap.  2), where the scientific names are more informative in that context (i.e., with placement in the same genus implying closer relationship). In Chap.  2, where genus names that start with the same letter are abbreviated, the first two letters are used (e.g., Le. and La. to distinguish Lethenteron from Lampetra). The scientific names follow the American Fisheries Society’s (AFS) seventh edition of Common and Scientific Names of Fishes from the United States, Canada, and Mexico (Page et al. 2013a) for North American species and, with one exception (the Po brook lamprey Lampetra zanandreai; see Chap.  2), FishBase (Froese and Pauly 2014) for other species. The describing authorities and date of authorship are given in Appendix 2.1; note that, in the case of changed genus and species combinations (i.e., where a species has been reassigned to a different genus than that in which it was originally described), the authorship and date are set in parentheses. Common names used in the book generally agree with the standard common names recommended in the AFS Names of Fishes list (Page et al. 2013a) or those used in FishBase, but authors were not restricted to using these names only. In some cases, common names selected by the AFS are not yet well known (particularly elsewhere in the world) or their stabilities have yet to be proven (see Kendall 2002); in other cases, experts working on these species prefer other common names (see Table  2.1). In no case have more than two common names been used for a single species and, of course, the species in question has been clearly identified on first mention by its scientific name. Thus, it was felt that the use of alternate (i.e., other common) common names would reduce (and not lead to) confusion among readers, particularly given the intended international audience for this book.

Why Are Common Names Not Capitalized in this Book?

In 2002, an ad hoc committee of the American Society of Ichthyologists and Herpetologists (ASIH) advocated capitalizing the common names of fish species (Nelson et al. 2002). Two compelling arguments for capitalization included elimination of ambiguity (i.e., because “treating common names as proper nouns ensures that adjectives are recognized as part of the names rather than as a descriptive adjective”) and giving ­emphasis to the name (letting it “stand out and be easier to spot in scientific publications”). In December 2003, the editorial board of Copeia, the journal of the ASIH, started capitalizing species common names in this journal. The seventh edition of ­Common and Scientific Names of Fishes from the United States, Canada, and Mexico (Page et al. 2013a) included capitalization of English (but not French or Spanish) common names and, as of January 2013, AFS publications (e.g., Transactions of the American Fisheries Society, North American Journal of Fisheries Management, Fisheries, Journal of Aquatic Animal Health) likewise required that English common names be capitalized. Some organizations [e.g., the International Union for the Conservation of Nature (IUCN) and the Committee on the Status of Endangered Wildlife in Canada (COSEWIC)] have followed suit. Despite this recent trend toward capitalization of (English) common names, however, common names are not capitalized in this book. It was the editor’s feeling that, despite being passionately embraced by many ichthyologists and fish biologists, the preference for capitalized common names is far from universal. Even among North American ichthyologists, there seems to be dissent (e.g., Kendall 2002) and the majority of “fishy” journals in which many of us publish (e.g., Journal of Fish Biology, Canadian Journal of Fisheries and Aquatic Sciences, Environmental Biology of Fishes, Journal of Applied Ichthyology, Ecology of Freshwater Fish, Fish and Fisheries) do not capitalize common names. Furthermore, given that there are subtle rules associated with the capitalization of common names (e.g., individual species names are capitalized but not the common portions of names shared by two or more species, common names of fish species are capitalized but not the names of non-fish species, common names of subspecies are capitalized but not the names of life history variants; see Page et al. 2013b), the editor was concerned that this will create a divide between ichthyologists and other biologists interested in lampreys. Having fewer rules for common names is more likely to improve communication among those interested in lampreys. The use, on first mention, of both common names and scientific names (with all the latter’s rules; International Commission on Zoological Nomenclature 1999) should prevent any ambiguity. Thus, despite the many arguments given for capitalization—and our willingness, of course, to capitalize common names when required—we felt it was both unnecessary and premature to do so in this book. Let’s see first if this preference for capitalized common names has, like lampreys, a broad global distribution and the ability to stand the test of time.

Notes

Acknowledgments

We gratefully acknowledge Judy Anderson, Elizabeth Docker, Ian Docker, and Meagan Robidoux for their interesting discussions about lampreys and their feedback on this chapter.

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Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Margaret F. Docker
    • 1
    Email author
  • John B. Hume
    • 2
  • Benjamin J. Clemens
    • 3
  1. 1.Department of Biological SciencesUniversity of ManitobaWinnipegCanada
  2. 2.Department of Fisheries and WildlifeMichigan State UniversityEast LansingUSA
  3. 3.Oregon Department of Fish and WildlifeCorvallisUSA

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