An amazing amount of new information has been discovered since I published my first book on chickadees (Smith 1991). Among the most fundamental of these advances is the work of Frank Gill and his colleagues on the genetic relationships within the Family Paridae. Working with mitochondrial DNA, in particular the mitochondrial cytochrome-B gene, Gill et al. (2005) have arrived at an overview of the degree of relatedness among the members of this avian family. Evidently there have been two independent invasions of North America by Parids. The first of these is estimated to have occurred approximately 4 million years ago (mya), and led to the present species of crested titmice in this continent. The second invasion, about 3.5 mya, led to the chickadees (Gill et al. 2005).
It is unfortunate that there has been a general lack of agreement as to whether the distinct lineages among Parids world-wide, as described by Gill and his colleagues, should be considered as distinct, separate genera (as adopted by the American Ornithologist Union in North America in the 1990s), or whether these should be merely subgenera (the prevalent view until recently on the other side of the Atlantic see Preface). This disagreement between North American and European editors led to the rather confusing situation in which the species I work with, the black-capped chickadee, remains Parus atricapillus in European journals, while having undergone the unfortunate and convoluted journey through Poecile atricapilla to Poecile atricapillus in North American journals. Be that as it may, the important thing is that this work has clarified which species belong in which lineages, and how closely each of these lineages is to the others. All North
American crested titmice are in the same lineage, which is closest to, but distinct from, that of the Eurasian crested tits. By contrast, while all of the North American chickadees are in the same basic group, they have not diverged sufficiently from certain Eurasian relatives (e.g. willow and marsh tits, among others) to be considered a separate lineage from those species. "The recent adoption of the new generic names by the British Ornithologists Union and International Ornithological Congress for all tits world-wide appears to be finally resolving this issue (see Preface)."
North American chickadees can be further divided into two phenotypically distinct groups: those with black caps and whistled songs (the black-capped, Carolina, mountain and Mexican chickadees); and those with brown or grey caps, which typically lack whistled songs (the chestnut-backed, boreal chickadees, and Siberian tits). In general, a lot more work has been done on the first four species; it is therefore particularly welcome to have a chapter in this book exploring the phylogeography of chestnut-backed chickadees (Chapter 6). Although three subspecies of chestnut-backed chickadees are recognized, microsatellite analysis indicates that there are actually four genetically distinct populations now alive: two in British Columbia (Queen Charlotte Islands, and south-eastern B.C.); one confined to Alaska (central Alaska); and a large coastal group. Burg set out to discover how this particular distribution has arisen. In particular, she was exploring the effect of Pleistocene glaciations on the evolution of these four lineages. Based on careful analysis of the genetic differences and similarities between and among these four groups, Burg has concluded that the current distribution and lineages of chestnut-backed chickadees is the result of colonization (after glaciation) from multiple refugia, rather than having either a single northern or single southern source.
Another chapter using molecular biological techniques is that of Curry et al. (Chapter 7), working with black-capped and Carolina chickadees. These two species, while evidently not each others' closest relatives (Gill et al. 1993, 2005), are nevertheless the two chickadee species that interbreed most regularly, along a quite long and broad hybrid zone. Curry and his colleagues' work on this hybrid zone reveals a dynamic situation in which the Carolina genes appear to be pushing northward into what was formerly purely black-capped chickadee populations. This is rather horrifying information to people like me who count on knowing what species they are working on! In the broad zone of interbreeding, Curry documents that an individual bird's morphological characteristics might suggest it is purely one species, while its vocalizations might be very typically the other species—and genetically it might be anywhere along a continuum from either pure species. As Curry and his colleagues point out, morphological features such as feather edgings or bib size might be genetically based, but at least some aspects of vocalizations, in particular whistled songs, must be learned; hence even a purely Carolina chickadee might sing a black-capped chickadee song, and vice versa. And now Curry and his colleagues are finding a trend for increasing numbers of bilingual birds in their study areas. This applies not only to whistled songs, but also to some true calls (especially the dee calls of the chick-a-dee call complex). And just to make it even more confusing, a given bird's call's similarity to one of the pure species has no particular correlation with the same individual's song's similarity: that is, an individual might give a black-capped chickadee whistled song, but have the shorter dee notes of a Carolina chickadee in its chick-a-dee call notes. And now Curry et al. have shown that birds giving more Carolina-like calls had more black-capped-like hybrid index scores. I pity the poor female attempting to make a suitable mate choice in a situation like this! Actually, Curry et al. conclude that vocal patterns may be less important than other aspects of the birds' mating systems. Nevertheless, it is clear that a lot of mistakes are made, as the hybrid zone is broad and pushing rapidly northward.
One of the rather startling findings of Gill and his colleagues is that, despite this broad and dynamic hybrid zone, it is the mountain chickadee, rather than the Carolina, that is the species most closely related to black-capped chickadees. Martin and Norris (Chapter 8) have explored some ecological aspects of an area in the interior of British Columbia where these two species are sympatric. One important difference between the two is that black-capped chickadees typically excavate their own nest cavities, while mountain chickadees must depend on cavities created by other birds.
Martin and Norris work in an area with fluctuating food supply for nesting chickadees. One of the really interesting findings they have is that in years with a high insect food supply, mountain chickadees were able to increase their nest density far more strongly than could the rarer, but dominant, black-capped chickadees. It would be really interesting to follow up their suggestion and attempt to measure the actual cost of nest site excavation. Another factor to investigate is whether the black-capped chickadees might respond to increasing food levels not by varying their breeding density but rather by increasing their clutch size.
Ratcliffe, Mennill, and Schubert (Chapter 9) examine factors affecting winter social rank and fitness in black-capped chickadees. Their work has documented a variety of factors that can influence a given bird's position in its winter flock (I might remind the reader that the relative rank between members of a breeding pair typically reverses in the breeding season, with females becoming dominant over their mates, Smith 1980).
The effects of age and of sex are both well known. Ratcliffe et al. have gone well beyond these (while further clarifying and quantifying the effects of both). Some of the correlates with dominance that they have found include body condition: high-ranked chickadees of each sex are leaner than lower-ranking birds (thus making them more maneuverable in predator escape situations). Ratcliffe's group has also shown that plumage characteristics, like the darkness of the cap and bib, and brighter white, is correlated with rank, at least in males. They have also shown that higher-ranked unpaired males are selected faster by females (Otter and Ratcliffe 1996).
How is initial rank achieved and maintained? Ratcliffe et al. have found, at least for males, that the suppression hypothesis, which states that dominant individuals condition their subordinates to lose through ongoing attacks, best fits the observed behavior in the field. Finally, they found, again just for males, that males that lived longer (and thus achieved higher rank) did indeed have greater fitness, as measured by lifetime reproductive success; nevertheless this seemed to be a reflection simply of whether or not the males reproduced at all, rather than showing any finer-scale difference between individuals.
Another area in which an enormous amount of work has been done since 1991 is physiology, including (especially) neurophysiology. One of the major areas of advance concerns neurophysiological aspects of food storage, or caching behavior. Black-capped chickadees, and other members of the Poecile group, are scatter-hoarders: they can store hundreds and often thousands of seeds, each in a different place. There is now abundant evidence, especially for black-capped chickadees, that the birds can remember precisely where they stored particular items, and then can go back and retrieve the stored food.
Exploration of this behavior has proceeded along several lines. One is purely behavioral. In a particularly elegant experiment (Brodbeck 1994) showed that black-capped chickadees used a hierarchy of cues to return to the location of a particular food item. Rather amazingly, overall location within the aviary was most important, relative position within an array of boxes in the aviary was second, and color of the box was third most important for the chickadees. Clearly their spatial capabilities are exceptional, and we need to explore the neural basis for these abilities.
And so we come to the hippocampus. Although the hippocampus in birds is homologous to that in mammals, the avian structure is more accessible for investigation, being not as buried within the brain tissue (Sherry and Hoshooley, Chapter 2). As in mammals, this structure is strongly associated with spatial ability. In the last few years, our knowledge about the avian hippocampus, and especially that of Parids, has increased enormously. We now know several factors that can affect the size of this structure. One of these is geographic location of the population. For example, Pravosudov (Chapter 3) has shown that black-capped chickadees in Alaska have significantly larger hippocampi than do Colorado chickadees. The rather more startling continental difference, with European birds across many avian families having significantly larger hippocampi than their North American counterparts, has yet to be fully explained, although, as Sherry and Hoshooley point out, the difference seems not explicable as merely an artifact of differing laboratory procedures, but actually a genuine phenomenon. Clearly this puzzling difference in hippocampus size is both a necessary and a promising area for future research on both sides of the Atlantic.
Another facet of hippocampal research is in adult neurogenesis. A great deal of controversy exists here, and the data are not easily interpreted. Sherry and Hoshooley suggest that neurogenesis in many Parids may, in fact, be relatively constant throughout the year, but the attrition rate of old cells may vary with the season.
Actually a number of factors affect the size of the hippocampus, and also the ability of a bird to perform spatial tasks. One of these is stress, especially as measured by levels of corticosterone. Pravosudov (Chapter 3) has shown that moderate levels enhance spatial memory tasks in mountain chickadees, although exactly how this affects the hippocampus is not yet known. Dominance rank is also important, with dominant birds performing memory tasks significantly better than subordinates. Pravosudov found no rank difference in either hippocampus size or number of neurons in the hippocampus, but the difference may be related to cell turnover: his findings suggest that cell proliferation rates in subordinate birds were significantly lower than in dominants.
One factor that seemingly may affect the hippocampus, at least directly, is photoperiod (Phillmore and MacDougall-Shackleton, Chapter 4), although, frustratingly, data on free-living birds do not seem to agree with data taken on birds in captivity. Any photoperiod effect may be mediated by a number of factors present in field conditions but not available in the artificial simplicity of the lab.
Clearly photoperiod has an enormous effect on reproductive physiology. Black-capped chickadees, like most songbirds, are absolutely photorefractory (Chapter 4). But, as Ramsay and Otter (Chapter 5) point out, photoperiod does not explain year-to-year variations in reproductive timing. For that, one needs to look at look at population and individual differences. For example, variations in sensitivity to photoperiodic changes can explain population differences in onset of breeding in blue tits (Lambrechts et al. 1997). Individual females also are remarkably consistent from year to year as to when they begin laying eggs (Chapter 5). Other factors, such as food levels, temperature, and parasite loads, may also affect female timing; now we are beginning to look at the effects of more global factors, such as the North Atlantic Oscillation, and global warming, on clutch initiation dates.
The last three chapters in this book deal with conservation and habitat management. This is a welcome addition to the subjects I attempted to cover in my first book. Parids are relatively sedentary, and not particularly good long-distance flyers. They will go long distances around an open area, rather than attempt to cross the open space (Desrochers and Bélisle, Chapter 15). Habitat fragmentation can have a big impact on their ability to move from place to place. Even for relatively large Parids, such as tufted titmice, movements from patch to patch are greatly enhanced if those patches are connected by wooded corridors (Olson and Grubb, Chapter 16). Certainly in these days of increasing human population, habitat fragmentation will only increase, and it is important for us to understand the impact of factors, such as patch size of blocks of forest, and the importance of connecting links, on the local bird populations. Otter et al. (Chapter 17) touch on a particularly important area. In forest management, matrix (intervening habitat that connects patches of relatively undisturbed habitat), has been claimed to provide alternative breeding habitat for a number of species. While this management technique does provide cover and enhances movements between patches of relatively undisturbed habitats, Otter et al. has shown that the matrix often is largely unsuitable for successful breeding among the birds it appears to retain. Careful studies of this nature and quality are absolutely essential to assess popular management techniques.
Finally, one of the areas where the greatest recent progress has been made is the field of vocal communication. The three most complex vocalizations: the whistled fee-bee song (Chapters 10 and 14), the gargle call, which some have argued might be considered to share some of the functions of a song (Chapters 11 and 12), and the chick-a-dee call complex, with its syntax and incredible complexities (Chapters 10 and 13), are all addressed in detail in this volume.
Nevertheless, while an enormous amount is now known about Parid (and in particular chickadee) communication, enormous gaps in our knowledge remain. It is unfortunate that the work on both whistled songs and gargles has been done almost exclusively on males (with females considered, when at all, primarily as recipients of male-produced signals). Yet females produce both of these vocalizations. The function of these notes, and how recipients of either sex respond to them, is as yet largely uninvestigated.
The other, truly enormous hole in our understanding of communication in Parids is in the area of visual signals. One approach to the study of visual signals is to investigate variation and function of plumage patches (e.g. Otter and Ratcliffe 1999; Mennill et al. 2003; Doucet et al. 2004; Woodcock et al. 2005). Black-capped chickadees, which appear superficially to human eyes as monochromatic, are actually sexually dichromatic (Chapter 9). Males have brighter whites and greys and blacker blacks than females; patch sizes vary consistently too. Remarkably, these subtle plumage variations reflect not only sex but also rank (Mennill et al. 2003; Doucet et al. 2004), and are correlated with female mate choice (Doucet et al. 2004; Woodcock et al. 2005). Similar functions of plumage patch variation have been found in other Parids as well (e.g. Ferns and Hinsley 2004).
But where we still know surprisingly little is in the area of postural signals. Susan T. Smith (1972) gave brief descriptions of the postural signal repertoire of Carolina chickadees. Black-capped chickadees give many similar signals; I attempted to illustrate some of these in my more recent book (Smith 1997). A few displays, such as body-ruffling (Piaskowski et al. 1991) and single wing flick (Smith 1996) have been described, but nobody has attempted a comprehensive overview of visual displays that might balance the vocal repertoire papers of Ficken et al. (1978) for black-capped chickadees, and Ficken (1990a, 1990b) for Mexican chickadees. Indeed, surprisingly little is known about visual signals in most other North American Parids. One can argue that the software technology exists for the study of vocal signals, but not for visual signals; I suspect that had the pressure been stronger to develop visual signal software, that might have been produced first. One can also argue that vocal signals are a lot easier to study, and I agree. I am not sure I agree with Smith (1972) when she suggested that visual signals merely back up vocalizations. Certainly we need to obtain data to test this hypothesis. With the state of video technology today, both descriptive and manipulative experiments are possible, even with fast-moving species such as chickadees (e.g. Baker et al. 1996). Titmice, being somewhat slower, might make even better subjects for a thorough examination of the role of visual signals. Their crests make them particularly good subjects for such a study. Grubb (1998) refers to the crest of the tufted titmouse as a "semaphore signal" (Grubb 1998:16), where raised crests signal excitement or aggression, with flattened crests signaling the opposite (passivity and subordination). Quantitative data on such a role should be relatively easily obtained. Rigorous study on Parid visual communication is sorely needed, especially here in North America. This surely is a wide open area for future research.
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