Wednesday, July 1, 2009

Review of "Sensory Evolution on the Threshold"

Last year Hans Thewissen and Sirpa Nummela published an edited volume with Springer Verlag entitled, "Sensory Evolution on the Theshold". The text covers how sensory biology in aquatic amniotes (and other secondarily aquatic tetrapods) copes with perceiving the world around them.
It is an excellent, uncommon resource, and I highly recommend it. In fact, I reviewed it for the Journal of Mammalian Evolution, and it was published online in October 2008. But, as we all know, printed journals are limited to page charges. Being the wordy sort I am, my initial draft was MUCH longer. Although not as cleanly written, I strove in that version to go through the text in detail and do what I wish more book reviews did - fill in the gaps. That is not to say that this book has many gaps at all, it is really an impressive collection full of details. But being a human endeavor, error is inevitable, and though I doubt I could do as good a job of the book myself, I'm afforded the luxury of simply reading it and noticing some references that are missing. So, herewith I present the full version of the review as a wrote it initially. Though the starting phrases are similar, the content is vastly different in its scope, mainly because large parts had to be edited out to fit within the limitations of a printed journal. This is NOT the same text as the printed review, but I hope it might be useful, mainly for the additional references, so that students of these subjects might have less searching to do.

(NOTE: I would strongly suggest that if this interests you, that you consider joining the Society for the Study of Mammalian Evolution - the membership is only $35, you get the journal and would be in some rare company because the membership of the group is unusually small, considering how many folks study mammal evolution. So join the group!)

So, here is the unabridged version of the review:

Adaptive Convergences in Perception Recognized

Sensory Evolution on the Threshold – Adaptations in Secondarily Aquatic Vertebrates. Edited by J. G. M. Thewissen and Sirpa Nummela. Berkeley: University of California Press. 2008. 351 pp., $75 (cloth). ISBN 978-0-520-252783.

by Brian Lee Beatty

Functional morphology has its limitations, partly because of the inability to divorce the influences of ancestry from function in understanding the form of a given structure. For instance, hypsodonty in a horses, camels, and oreodonts are commonly given examples of adaptation to grazing, yet once evolved, hypsodonty may have simply added to niche breadth and not restricted an animal’s diet to grass exclusively (Feranec, 2003; Mihlbachler and Solounias, 2006). Though the source of morphology can never reasonably be categorized as “inherited” versus “functional”, as these two are not likely to exist without each other, the study of how distinct clades converge on similar forms and specializations is perhaps the best way in which to understand how organisms adapt to different foods, environments, and lifestyles. Once one gets past their charismatic megafauna role in popular culture, marine mammals can be seen as ideal study animals for looking at such convergences because of the numerous times they have returned to an aquatic lifestyle. The physical and chemical environments of air versus water are very, very different (Denny, 1993), and the body forms of marine mammals have proven to be exemplars of convergence in form for functional reasons (Fish, 2000; Pabst et al., 1999). Though marine mammals are similar in physiology and anatomy to the best known vertebrates, mice and men, they are not a natural group and focusing only on them leaves out the majority of vertebrates and far more than half of the clades that have returned to an aquatic lifestyle. The editors of Sensory Evolution on the Threshold, J. G. M. Thewissen and Sirpa Nummela, are known for their work on marine mammals (Nummela et al., 2004), but it is clear from this book that they recognize the importance of having a broader view of secondarily aquatic vertebrates and how many have converged on similar forms despite very disparate ancestries.

In Sensory Evolution on the Threshold, we get the most complete review I have seen of sensory biology and physics in secondarily aquatic vertebrates, from lissamphibia to squamates, birds, and mammals with no particular bias toward one group. The book starts with a concise, but detailed account of the diversity of secondarily aquatic vertebrates, with sections for each major group of vertebrates written by separate authors, some of which are authors of separate chapters in the book. These short sections detailing groups such as lissamphibia, birds, and mammals are nice brief summaries and do the most comprehensive job of reviewing the diversity of secondarily aquatic vertebrates that I have ever seen. I could envision myself citing them frequently, if it weren’t for the complicated act of citing a section within a chapter within an edited volume, each with separate authors/editors. Though they may be complicated to cite, each of these sections is worth it as a starting point for anyone starting work on these groups.


After this brief introductory chapter, the text is broken down into six sections, one for each sense: chemical senses, vision, hearing, balance, mechanoreception, as well as magnetoreception and electroreception. Each of these sections begins with a chapter on the physics and biology of that sensory modality in water. At first I found myself frustrated by reading so many reviews of topics already familiar from other books on specific sensory systems (Land and Nilsson, 2002; Smith, 2000; Stebbins, 1983), but realized that not only do these chapters help ease readers not familiar with these other works, but it also helps the reader construct ideas about what information is important to understanding the discussions of the anatomy and physiology that follow in chapters detailing how these senses work in various aquatic groups.

Chemical senses comprise seven chapters of their own, giving them more pages than any other sensory modality covered in this book. Though not as important to marine mammals as to other aquatic vertebrates, chemical senses are so complex and important to virtually all other vertebrates that they certainly warrant the attention.

For example, in Chapters 2, 3, 4 and 5 the detailed account of the role of the primary olfactory nerves and the vomeronasal organ in the reception of different stimuli really conveys how vomeronasal function is not cut-and-dry. In Chapters 4 (by Reiss and Eisthen) and 5 (by Schwenk), we get a glimpse of how nasal cavities in lissamphibians and nonavian reptiles can link subtle features of internal morphology to chemoreceptive abilities and the interplay between breathing, eating, and olfaction. Chapters such as this make it easy to imagine this as a starting point for people working on sensory adaptations in tetrapod origins or even Sauropterygia. Schwenk even provides a page or two on mosasaurs, phytosaurs, and plesiosaurs, full of inferences and insights that cannot help but stimulate speculation.

Chapter 6 (by Hieronymous) covers aquatic birds in a brief, detailed anatomical way. Though there is no doubt that many birds are aquatic, the amount of time and manner in which they use water is so diverse that birds (Hémery, 2001; Kristoffersen, 2001), perhaps like large ungulates, make it hard to narrowly define ‘semiaquatic’. This problem itself is probably responsible for many paleoecological misunderstandings about the Neornithes, as well as pterosaurs (Mazin, 2001). Hieronymous is an example of clarity when it comes to restricting how he partitions the continuum from terrestrial to fully aquatic. Hieronymous starts out defining what he means by ‘aquatic’ and keeps the chapter limited to a review of general details of what is known for major groups and points out what research is sorely lacking. These gaps in the knowledge of bird biology must be systemic, as even though Hieronymous provides far more details, this chapter reminds me of reviews on bird feeding biology (Rubega, 2000) that also point out the large gaps in our knowledge of modern taxa. Like many of the chapters in this volume, perhaps excluding those on vision, Hieronymous places this limited data optimized on a cladogram, hinting at what may be assumed and what work there is to be done.

Pihlström’s chapter (7) on chemical sense in aquatic mammals touches on the little published information there is for fossil groups briefly, but focuses on modern mammal groups. Pihlström demonstrates his attention to detail in noting the difference between mysticete and odontocete olfactory anatomy, adding to the growing amount of evidence informing us about the big physiological differences between these two groups as they diverged in the late Eocene and early Oligocene (Beatty and Rothschild, 2008; Fitzgerald, 2006; Lindberg and Pyenson, 2007). The only modern aquatic non-cetacean artiodactyls are the Hippopotamidae, and it is unfortunate that Pihlström’s review of this family does not more thoroughly include some significant findings of the role of olfaction in behavior (Zapico, 1999) that demonstrate how terrestrial these animals really are. Still, Pihlström demonstrates his mastery over this topic in his analysis of olfactory bulb volume with respect to body size of some of the smaller semiaquatic mammals in the conclusion of this chapter. Despite how anecdotal the data may suggest a reduction in olfactory bulb volume with becoming semiaquatic, he deftly conveys a need for caution in light of the fact that many semiaquatic taxa are larger than other non-semiaquatic sister taxa, as his data suggests that the only significant differences in olfactory bulb size seem to occur with fully aquatic taxa. Though this leaves more questions than answers, it gives me hope that chemoreception may be a possible dividing line between aquatic and semiaquatic mammals.

The second sensory modality covered is vision. Starting with Kröger’s chapter (8) on the physics of light in air and water, he brings up quite a number of important and novel concerns about vision underwater as compared to terrestrial environments. And though he succeeds in addressing the importance of pressure, sediment loads and salinity in how it may affect eyes as organs when exposed to different aquatic environments, the differences among aquatic habitats with respect to the role of temperature or salinity on the refractive index was not mentioned, even though this data is available (Denny, 1993). Though this does not devalue this useful chapter significantly, this information could be important to animals that move between environments of different temperature and/or osmolarity (e.g., deep diving cetaceans, manatees, possibly many transitional forms). Perhaps more importantly, though subsequent chapters make use of diopters as important units of vision, this chapter does not describe what they are or how they are measured. Even though not important to explain methodologically here, it would have been a better use of the space given to the speed of light in air and water, which has less relevance to the comparative anatomy.

Kröger and Katzir’s chapter (9) on the anatomy and physiology of eyes in aquatic tetrapods reviews specializations of the eyes of modern aquatic tetrapods for not only being fully aquatic, but also goes into detailed discussions of how a number of groups deal with vision when in water as well as when in air. In addition, their discussion of the meaning of eye size for vision in ichthyosaurs is expertly executed, as are the lengthy discussions of how many birds correct for the refraction of underwater prey when hunting from the air, and how odontocete eyes function. For the sake of completeness I feel it useful to report some recent references to the anatomy of Harderian glands in odontocetes (Bodyak and Stepanova, 1994; Ortiz et al., 2007) that are lacking in their discussion of the so-called ‘whale tear’, though this is hardly an oversight of much importance. Likewise, the hypothesis that Platanista (the South Asian river dolphin) may be able to use its light sensitive eyes to form an image in air (Waller, 1983) is not evaluated, and discussion of the use of these eyes as means to identify the surface during side-swimming (Purves and Pilleri, 1973) is absent, despite its relevance when comparing these with other river dolphins whose environments are similarly murky but lack such visual atrophy. The review of vision in sirenians is very thorough, in particular with its reference to findings about manatee corneal vascularity, which has recently been shown to be the result of a lack of expression of sflt-1, which is the normal means of suppressing vascularity in the cornea of all other mammals (Ambati et al., 2006).

Regarding perhaps the most obvious question that comes to mind when one sees this book, the position of orbits on the skull of aquatic and semiaquatic taxa (such as the hippopotamus staring at you from the cover of the book), the authors here only devote a brief discussion. This discussion is unfortunately very superficial, with apparently little care to discern between the derived states of the position of the orbits in the examples they provide to determine the ancestral state of Cetaceans. I believe the authors would not be so likely to continue to draw comparisons to hippos if they had been more careful to note that orbit position Hippopotamus is much more dorsal and derived than in Choeropsis or the putative ancestors of hippos, anthracotheriids. Similarly, there is very little reason to believe that the ‘transitional form’ Ambulocetus represents the ancestral state of subsequent archaeocetes, as all putative sister taxa to cetaceans have laterally-oriented orbits, including anthracotheriids, cebochoerids (Theodor and Foss, 2005), and raoellids (Thewissen et al., 2007) (though it is clear that the authors could not have included this latter reference in the time frame of publishing this chapter). Still, this chapter should be recognized for being a detailed review of a very complex and important subject in the study of aquatic tetrapods, and these omissions should be seen as stimuli for research, not faults.

Hearing is perhaps the sensory modality that has received the most attention with respect to aquatic mammals, particularly because of specializations for echolocation found in cetaceans. Nummela and Thewissen’s chapter on the physics of sound in air and water is the most clear and concise explanations of this topic I have seen, particularly with respect to the importance of acoustic impedance. This chapter is deficient in data comparing how the speed of sound varies in water of different salinities and temperatures, even though its importance is acknowledged in the text and data of this sort is available (Denny, 1993). The chapters on hearing in aquatic amphibians, reptiles, and birds by Hetherington, and mammals by Nummela are not only thorough in their descriptions of data for modern taxa, but Hetherington’s chapter is particularly attentive to fossil amniote taxa as well. I was a bit disappointed that no discussion of hearing in hippopotamids was included in Nummela’s chapter, especially with regard to new information on underwater hearing in common hippos that has recently come to light (Barklow, 2004).

The sense of balance is started with a chapter (14) by Sipla and Spoor on “The Physics and Physiology of Balance”, which is kept concise and clear. Georgi and Sipla’s following chapter (15) on balance in aquatic reptiles and birds avoids repeating details of how semicircular canals work and gets straight to exploring how canal shape changes may reflect aquatic specializations. In so doing, they help convey the importance of phylogenetic context, as the aquatic specializations of many non-mammalian amniotes can only be recognized in comparison with other close relatives, and not necessarily as “rules of construction” of their own. But some patterns do emerge from their presentation of original data and discriminant function analyses, making this chapter a valuable early look at their research that can be found nowhere else.

Likewise, Spoor & Thewissen’s chapter (16) on the semicircular canals of aquatic and semiaquatic mammals presents not only a complete review of previous research, but adds considerably more new data and analysis as well. Of particular interest are the new, conservative estimates about semicircular duct lumen size and how it may affect a canal’s response speed, as well as new data and analysis of pinnipeds, otters, and other semiaquatic rodents and monotremes. One minor technical error is the omission of one citation from the literature cited that is referenced in the text (Jansen and Jansen, 1969), an error so minor it is only worth noting here for the sake of completeness.

Instead of studies of nociception, thermoreception, muscle spindles, or even general spinal nerve mechanoreceptors, Denhardt & Mauck’s (chapter 17) introduction to the physics and physiology of mechanoreception, as well as their following chapter (18) on mechanoreception in secondarily aquatic vertebrates, focus almost entirely on the trigeminal system of mechanoreception that innervates facial areas. The reason for this becomes clear, as this is where most aquatic specializations exist for actively seeking prey items. The attention to the work of Daphne Soares and the folks at the University of Maryland on dome pressure receptors in Alligator is particularly striking, as is Denhardt’s own work on pinniped vibrissae. This chapter has an enticing number of notes on what we still need to know, as well as small tastes of unpublished research by Denhardt and Mauck that make it a stimulating read.

The chapter (19) on magnetoreception by Hofmann and Wilkens is brief, but highlights the significant data on magnetoreception in sea turtles as well as the scant data for cetaceans. Though it is disappointing to read that so little research as been done outside of birds due to logistical difficulties in the study of magnetoreception, I suspect someone reading this chapter will be stimulated to invent new ways of exploring this topic and astound us in the future.

Chapter 20 on electroreception is equally brief, primarily because it is a sense largely lost in amniotes even though it is known to have evolved early on in vertebrate evolution. The data presented on monotremes, particularly the platypus, is excellent, though the suggestion that some dolphins (Sotalia) have electrosense is reported based primarily on similarities in vascularity of their vestigial hairless follicles (Mauck et al., 2000) and unpublished research by Denhardt (which is also brought up in Denhardt and Mauck’s chapter on mechanoreception). In addition to these unusual compelling cases, Wilkens and Hofmann do something rare, they report on other aquatic mammals that are known NOT to have electrosensory abilities.

The concluding chapter, by Thewissen and Nummela, presents new preliminary findings concerning the evolution of sensory systems in fossil cetaceans. They manage an exemplary job of applying the concepts for modern animals laid out in the previous chapters, particularly with vision. I was disappointed that for all of the data on fossil whales presented that their only analyses were of absolute eye size and eye size scaled to body size (with a following statement that increased eye size = increased vision), even though recent studies indicate that eye size scales with brain size quite well with little or no indication of visual specializations (Burton, 2006). Likewise, the inference of enhanced mechanoreception based on the pits and grooves on the rostrum of pakicetids is poorly supported. The statement that manatee rostra are densely pitted where their fields of vibrissae occur is inaccurate, and in general comparisons of a pakicetid rostrum’s pits to the muscular hydrostat of a manatee are poorly conceived. In contrast, their discussion of the sensory landscape of cetaceans, especially their figure illustrating their ideas, is compelling. Their overall scenario regarding this landscape is plausible, even though in this context they seem to be treating early cetaceans as a lineage instead of a number of groups that may not represent the ancestral condition of later taxa. The dichotomy did not start with the advent of the Neoceti, and I am surprised that no cladogram with sensory system data optimized on it was presented to depict the diversity of archaeocetes and early Neoceti.

In their approach to coordinating comprehensive reviews of sensory systems in all secondarily aquatic vertebrates, what Thewissen and Nummela have coordinated here can only be compared to other great integrative biology or functional morphology volumes such Feeding (Schwenk, 2000), The Skull: Volume 3 (Hanken and Hall, 1993), Mechanics and Physiology of Animal Swimming (Maddock et al., 1994), or Secondary Adaptation of Tetrapods to Life in Water (Mazin and Buffrénil, 2001). Though it seems like a plethora of details largely concerning modern vertebrates, it is apparent from these authors that there is still much to be done for modern and especially fossil vertebrates. In this volume I hope that current and incoming generations of paleontologists and organismal biologists will see golden opportunities and inspirations for future paths of study. Now, with this book in hand, I hope that path will be taken by many more.

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7 comments:

  1. Wow, thanks!! Great review!! Very thorough! I bought this book some time ago and have been reading it sporadically (I'm easily distracted by shorter reads), since I want to read it chapter by chapter it will take some time anyways. It is definitely a must for people who work with aquatic vertebrates.

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  2. yep...another great blog post, although reading them always makes me realize just how much more literature reading I need to do...

    ReplyDelete
  3. ...or how much time I waste reading instead of writing!

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  4. Impressive reviews! Need to update myself constantly.

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    book review help

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