MISUSE AND PURPORTED INCONSISTENCY OF THE HUMPHREY-PARKES SYSTEM

Howell et al. (2003) are correct that the H-P system has been applied incorrectly to many species of birds, and that this has resulted in names of molts and plumages that reflect incorrect homologies. However, such widespread misunderstanding and misuse of the H-P system does not reflect shortcomings of the system, but rather reflects the inherent complexity of molt and plumage cycles in birds, and a poor understanding of molt by many biologists who study birds: The latter results largely from a view that molt is unimportant in the life-history of birds and boring to study (reviewed by Leu and Thompson 2002).

Howell et al. (2003) acknowledge that molt and plumage homologies among closely related species may be determined by comparing the timing of, extent of, and change in plumage color resulting from each molt in the entire molt and plumage sequence of one species with that of other closely related species. However, they argue that if homologies determined in this fashion are “founded on an arbitrary point of reference…, then broader patterns of homology could be obscured” (p. 637). Thus, they maintain that “to recognize potential molt homologies it seems more helpful to identify and compare patterns of plumage succession across a broad range of taxa” (p. 637).

The “arbitrary point of reference” to which Howell et al. (2003) refer is the first prebasic molt (and first basic plumage) which they believe (1) is not homologous across birds, and, (2) is the necessary starting point for determining molt and plumage homologies according to the H-P system. To the contrary, the H-P system does not use first prebasic molt as the necessary starting point for determining molt and plumage homologies. In addition, as noted by Howell et al. (2003), non-prebasic molts probably have evolved independently multiple times. Therefore, correct homologies are more likely to result from comparison of molts and plumages among closely related species than among distantly related species, which are more likely to have molts and plumages that are similar due to evolutionary convergence rather than homology. In turn, accurate broad patterns of molt and plumage homologies can be achieved best by comparing molts and plumages among many different groups of closely related taxa (e.g., Cardinalidae, Thraupidae, and Emberizidae), as Thompson and Leu (1994) demonstrated. Howell et al. (2003) acknowledge this when they state (p. 636) that “determining [homology] can be problematic, if not impossible,” and “one should therefore be aware of a potential distinction between homologies of nonbasic plumages within a species compared to homologies between species” (p. 648; italics in original).

Similarly, many other molt scholars, some of whom Howell et al. (2003) noted, have expressed disbelief that molt and plumage homologies can be determined across all birds given their huge diversity of molt strategies (Amadon 1966, Palmer 1972, Jenni and Winkler 1994). Thus, the gauntlet has been thrown down. It is our challenge to see if broad molt and plumage homologies can be discerned, and it is my belief that the strategy for doing so is by working from the bottom up (studying closely related taxa) rather than the top down (studying distantly related taxa) as advocated by Howell et al. (2003).

PURPORTED CAUSES OF MISUSE OF THE HUMPHREY-PARKES SYSTEM

Howell et al. (2003) contend that misuse of the H-P system results from (1) using traditional first prebasic molt as the starting point for plumage succession; (2) using plumage color as a criterion for evaluating molt and plumage homologies, and (3) a widespread misconception that the H-P plumage terms basic and alternate are simply synonyms for traditional nonbreeding (or winter) and breeding (or summer) plumages. I agree wholeheartedly with the last point, but disagree with the first two points.

Regarding the first point, Howell et al. (2003) state that “the inherent inconsistency stems from the H-P system taking its starting point of cyclic plumage succession as the highly variable molt that replaces juvenal plumage with so-called first basic plumage” (p. 637). While it is true, as Howell et al. (2003) note, that Humphrey and Parkes (1959) did not discuss the possibility of the first postjuvenal molt being any molt other than first prebasic molt, Humphrey and Parkes did not preclude this possibility, and did not take first prebasic molt as the “starting point.” Indeed, Howell et al. (2003) acknowledge that Humphrey and Parkes (1959) advocated interpreting molt and plumage homologies of “immature” (predefinitive) molts and plumages by using definitive prebasic molt and definitive basic plumage as “landmarks,” and working backward toward natal plumage. However, Howell et al. (2003) mistakenly argue that by doing so “the first cycle has to be fixed from the start of the ‘first prebasic molt’ and [if] a conventional first basic plumage is absent, then in its stead some other plumage will be named first basic” (p. 638).

This argument has two major flaws. First, it overlooks the likelihood that molts, including traditional first prebasic molt, have been evolutionarily lost in different species or populations, or developmentally suppressed at the individual and population level in response to environmental conditions (e.g., hatching date, food supply, day length) or experimental (hormonal) manipulation (Beebe 1914a, Jenni and Winkler 1994, Ros 1999). If, for example, a species (or population) does not exhibit a first prebasic molt at the same approximate age at which closely related species do, and if all other molts and plumages appear homologous, then it is reasonable to conclude that first prebasic molt has been evolutionarily lost or is being developmentally suppressed in this species.

Second, Howell et al. (2003) interpret the H-P system as requiring that the first molt cycle must begin with the first prebasic molt. I believe this interpretation is unreasonably strict and incorrect. For example, it precludes the possibility of a presupplemental molt preceding the traditional first prebasic molt as has been documented in many passerines (Thompson and Leu 1994). In 1959, presupplemental molts were only known to occur in definitive cycles, not in the first cycle; thus, Humphrey and Parkes (1959) confined their discussion of presupplemental molts to definitive cycles stating that they may precede or follow prealternate molts depending on the functions that such additional molts serve. By extension, I see no reason why presupplemental molts could not evolve to precede the traditional first prebasic molt. In fact, it is likely that such presupplemental molts are widespread among passerine, and possibly nonpasserine, birds but have gone unnoticed (reviewed by Thompson and Leu 1994).

Howell et al.'s (2003) second point is that plumage coloration should not be used to help identify homologies because “the physiological processes that govern pigmentation and molt timing are independent…(Voitkevich 1966)” (p. 638). This claim is an incorrect generalization. To date, remarkably little is actually understood about the physiological processes that govern various aspects of molt, feather growth, and pigmentation. Although some physiological processes (e.g., appropriate levels of sex steroid hormones) that influence timing of molt also influence feather pigmentation in some species, other physiological processes that influence timing of molt (e.g., appropriate levels of prolactin, A. Dawson, unpubl. data) and feather growth have no influence on feather pigmentation (Thompson 1998).

As ostensible support for their claim, Howell et al. (2003) cite a number of ecologically and phylogenetically disparate species in which individuals of the same sex undergoing the same molt grow feathers that differ subtly to markedly in color. This view shows a lack of appreciation for the physiological processes responsible for individual variation in phenotypic expression. Although many species exhibit significant variation within and among individuals in the color of feathers grown over the course of a single molt, the magnitude of this variation typically is considerably less than that between successive plumages and, therefore, does not pose a serious obstacle either to identifying molts and plumages or correctly determining their homologies. Thus, plumage color is a useful character in two ways. First, in species that change color between successive plumages, old and new feathers can be distinguished from one another based on differences in plumage color. When molts overlap at the individual or population level, as occurs in many species including gulls (Laridae, Dwight 1925, Cramp 1983, Higgins and Davies 1996, Olsen and Larsson 2003), differences in plumage color between different feather generations (plumages) allows one to identify which growing feathers belong to which plumage. Thus, by using plumage color to identify the plumages to which feathers likely belong, the timing and extent of molts can de documented more accurately than if plumage color was not used. Second, these data may then be used to help determine molt and plumage homologies among closely related species. Therefore, to ignore plumage color when determining molt and plumage homologies among closely related species is to throw the baby out with the bathwater.

Howell et al. (2003) correctly note that traditional first prebasic molt in many species differs from definitive prebasic molt in that it often (1) is more limited in extent and, they claim, absent in some species, and (2) occurs at a somewhat different time of year. Thus, they assert that these differences lend support to the idea that traditional first prebasic molts are not homologous with definitive prebasic molts. I disagree. Although definitive prebasic molts usually are complete, completeness of molt per se is not a defining criterion of definitive prebasic molts. Indeed, definitive prebasic molt is partial in some species (e.g., some Old World Phylloscopus warblers; Humphrey and Parkes 1959, Williamson 1976, Jenni and Winkler 1994, Pyle 1997). Similarly, a difference in the timing of traditional first prebasic molt relative to that of definitive prebasic molt does not, by itself, indicate lack of homology between these molts; Humphrey and Parkes (1959:7) stated that “the temporal position of a homologous molt in the cycles of plumage succession may vary among different groups of birds or among individuals of a species.”

The conceptual point here is that, for determining molt homologies, timing, extent, and resulting plumage color of molt are useful criteria to be evaluated within the context of the life histories of closely related species; these criteria are not rigid rules to be followed in a biological vacuum (Rohwer et al. 1992).

DEFINING THE FIRST PLUMAGE CYCLE

Believing that traditional first prebasic molt (or any other molt in the first cycle) is never homologous with definitive prebasic molt, Howell et al. (2003:638) propose that this supposed problem can be resolved by “two logical steps: (1) assuming the ancestral molt strategy is the simplest possible,” as Humphrey and Parkes also assumed, “and (2) defining juvenal plumage as the first basic plumage,” (p. 638) thus proposing that all juvenal plumages are homologous, a proposal that was made by Humphrey and Parkes as well. They term this ancestral molt strategy the Simple Basic Strategy (SBS). Further, they propose that “molts corresponding to those present in the Simple Basic Strategy occur in all birds and…are the only molts that should be considered homologous across all species” (p. 638; italics in original). Other molt strategies are viewed as building upon the SBS by the evolutionary addition of extra molts into molt cycles. They also define the first plumage cycle “as the period between the attainment of juvenal plumage and the acquisition of the next basic plumage via a complete, or nearly complete, molt that corresponds to a molt in the Simple Basic Strategy” (p. 639, italics mine).

Juvenal plumage results from a complete prejuvenal molt of all down feathers (in species that have down), and thus satisfies the criterion that basic plumage usually results from a molt that is complete or nearly so; however, Howell et al. (2003) present no additional data which suggest that juvenal and definitive basic plumages are homologous and, therefore, might justify renaming juvenal plumage to first basic plumage. Otherwise, I agree, in principle, with the arguments above regarding the SBS, and homology of juvenal and basic plumages throughout all species of birds.

CONSISTENCY OF THE HUMPHREY-PARKES SYSTEM

Howell et al. (2003) state, and I concur, that it is preferable that the names of all prebasic molts and basic plumages be consistent across all species and numbered according to the cycle in which they occur. They present examples of many species in which all individuals undergo their first complete molt at approximately one year of age, but some individuals or populations precede this with an additional partial molt, traditionally called first prebasic molt, which Howell et al. (2003) view as a novel molt that is not homologous with definitive prebasic molt. They refer to this molt strategy as the Complex Basic Strategy (CBS); of the four molt strategies proposed by Howell et al. (2003, table 1) this is the most common one exhibited by North American and Australian birds.

Howell et al. (2003) correctly note that partial molts in the first molt cycle pose potential difficulties to determining molt and plumage homologies. However, their examples do not prove that these molts are evolutionarily new molts added to the SBS rather than prebasic molts whose extent has been reduced and temporally (developmentally) advanced in some individuals or populations relative to others. Indeed, such variability within and among populations in the timing and extent of molts, including traditional first prebasic molt, is well known (Jenni and Winkler 1994). For example, in Northern Cardinals (Cardinalis cardinalis) and Phainopeplas (Phainopepla nitens), first prebasic molt is confined solely to replacement of body plumage in many birds, whereas other birds undergo a complete first prebasic molt that is indistinguishable in its timing, extent, and resulting plumage color from that of definitive prebasic molt (Miller 1933, Sutton 1935, Thompson and Walsberg 1993, Thompson and Leu 1994, Halkin and Linville 1999, Chu and Walsberg 1999). Consistent with their definition, above, of the first plumage cycle, Howell et al. (2003:646) state that “complete postjuvenal molts are not prebasic if they do not correspond to prebasic molts in the SBS.” However, this is not the case with the first prebasic molt in Northern Cardinals or Phainopeplas (Thompson and Leu 1994). Therefore, in these species, I can think of no reason, even following Howell et al.'s system, not to conclude that the complete first prebasic molt of some individuals or populations is homologous both to partial first prebasic molt as well as to definitive prebasic molt of other individuals and populations.

Similarly, in some to all species of many nonpasserine and passerine families, such as doves (Columbidae), cuckoos (Cuculidae), many New World flycatchers (Tyrannidae), starlings (Sturnidae) and weaver finches (Ploceidae), young birds undergo a complete postjuvenal molt at the same approximate time that birds in older age cohorts undergo their complete definitive prebasic molt (Stresemann and Stresemann 1966, Poole et al. 1992–2003, Jenni and Winkler 1994, Pyle 1997). Therefore, in these species as well, the traditional first prebasic molt must be homologous with definitive prebasic molt. The competing hypothesis proposed by Howell et al. (2003) that this molt is evolutionarily new is less parsimonious.

HOWELL ET AL.'S FOUR MOLT STRATEGIES

Howell et al. (2003) describe four molt strategies beginning with, and building upon, the Simple Basic Strategy (SBS) that they allege “encompass all known patterns of plumage succession” (p. 643). Howell et al.'s table 1, which categorizes the molt strategies exhibited by species belonging to all families of North American and Australian birds into one or more of four molt strategies, is a valuable summary and a potentially useful guide for directing researchers to groups of birds to study that may be especially helpful for clarifying issues regarding molt and plumage homologies in birds. However, Howell et al. (2003) present no credible case for the existence in any species of either of two molt strategies, the Complex Basic Strategy (discussed above) and the Simple Alternate Strategy; indeed, considerable empirical data refute the existence of these strategies.

The Simple Alternate Strategy applies to species that purportedly have only a single molt in their first molt cycle, which Howell et al. (2003) argue is homologous to definitive prealternate molt. This molt strategy was first described for Western Gulls (Larus occidentalis), in which Howell and Corben (2000a, 2000b) claim that (1) young birds have a single protracted molt that occurs at the same time (late August to mid-April) as definitive prealternate molt in adults and, therefore, is homologous to it, and (2) definitive prealternate molt overlaps the last 3 months of definitive prebasic molt.

However, Howell et al. (2003) do not explain how they identified birds growing basic versus alternate plumage during the months that these two molts supposedly overlap. This illustrates a more general and serious problem throughout Howell et al. (2003): the only criteria that they offer for identifying molt and plumage homologies are calendar timing of molt and completeness of molt being indicative of a prebasic molt.

Howell et al.'s (2003) results regarding Western Gulls conflict with our knowledge of the sequence and timing of molts in Western Gulls and all other species of gulls (Dwight 1925, Cramp 1983, Poole et al. 1992–2003, Higgins and Davies 1996, Olsen and Larsson 2003). The only significant study to date of molt in Western Gulls other than Howell and Corben (2000a, 2000b), was Dwight's (1925) in which he stated that (1) the first postjuvenal molt in Western Gulls occurs in September, October and November, and that a subsequent “prenuptial” (definitive prealternate) body molt occurs in March and April; and (2) all older cohorts undergo a complete postbreeding (definitive prebasic) molt in August and September and partial prenuptial (definitive prealternate) molt in March and April. Thus, the protracted molt, if it exists, begins many months earlier than definitive prealternate molt and, therefore, is not homologous to it.

In addition, Howell and Corben's (2000a) study on Western Gulls was based mainly on visual observations of birds. Relative to examination of specimens in the hand, observations through binoculars or spotting scopes preclude the ability to collect data on molt intensity or distinguish between old and new or growing feathers that are similar in feather color, and reduces the ability to estimate the extent of new (or growing) versus old feathers, especially in species that undergo little, if any, change in plumage color between successive plumages, as is the case in the “white-headed” gulls, including Western Gulls. Thus, I believe that these factors contributed to Howell and Corben (2000a) failing to discern the protracted molting period in young Western Gulls as two separate molts rather than a single molt.

Howell and his colleagues (Howell and Corben 2000a, Howell 2001, Howell et al. 2003) claim that the Simple Alternate Strategy also occurs in species in at least eight families of nonpasserines. Data regarding many of these species either indicate that they do not follow a Simple Alternate Strategy, or are inadequate to document which molt strategy they exhibit. For example, based on Beebe (1914b), Howell et al. (2003) claim that White Ibises lack a “postjuvenal” molt, and have only a single protracted first prealternate molt. Beebe (1914b:244) states only that White Ibis do not change plumage color “during the first summer and autumn, but late in winter, usually about February, a moult begins….This moult is not a short, well defined one but proceeds slowly throughout the year.” Such a brief and anecdotal account is not adequate basis for definitively stating that this species pursues a Simple Alternate Strategy.

Similarly, based on Snyder and Russell (2002), Howell et al. (2003) claim that Carolina Parakeets (Conuropsis carolinensis), an extinct species, exhibited a Simple Alternate Strategy. Carolina Parakeets laid eggs in March and April and fledged young at least as early as 4 June. Yet, Snyder and Russell (2002) state only that they found 9 young (hatch-year or second-year) birds without molt between 7 October and 17 January, and 43 birds with molt between 17 December and 12 June; they present no data regarding the existence of any postjuvenal molts in Carolina Parakeets between early June and early October because no such data exist. Again, such an incomplete understanding of molt is not adequate basis for concluding that this species exhibited a Simple Alternate Strategy. Thus, Howell et al. (2003) have not made a convincing case that a Simple Alternate Strategy occurs in any species.

FIRST-CYCLE MOLTS AND PLUMAGES

Howell et al. (2003:647) suggest that “it is most parsimonious to consider molts and plumages present in definitive cycles to have homologous counterparts in the first cycle, unless good evidence exists to the contrary,” a notion that I agree with. They further state that in species following Simple Alternate and Complex Alternate Strategies, “first-cycle plumages can be identified that appear homologous with definitive alternate plumages” (p. 647). Yet, again, they do not present criteria other than timing and completeness of molt for homologizing molts or plumages. Thus, it is a mystery to me how Howell et al. (2003) concluded that some first-cycle molts can be “identified” as homologous with definitive prealternate molt while they simultaneously conclude that other supposedly “inserted” molts that are identical to definitive prebasic molt are not homologous with definitive prebasic molt.

Having ostensibly identified molts and plumages in the first cycle that are not homologous to any definitive molt or plumage, Howell et al. (2003) correctly recognize the need to find appropriate names for these molts and plumages if, in fact, they exist. They argue, correctly in my opinion, that using the terms presupplemental and supplemental wrongly implies homology of these nonrepeated first-cycle molts and plumages with presupplemental molts and plumages in the definitive cycles of other species. Their proposal to call all such first-cycle plumages formative plumages attained by preformative molts, where formative plumage is defined as “any nonbasic plumage present in the first cycle but not in subsequent cycles,” (p. 648) seems reasonable in that the terms are clearly defined and do not contradict or interfere with other aspects of the H-P system.

CASE STUDIES

Howell et al. (2003:637) state that one of the objectives of their paper is to “provide case studies to illustrate how [their] modified H-P system reflects presumed homology in all basic plumages.” Unfortunately, their case studies fail to do so; they are little more than a list of various taxa (Ardeidae, Anatidae, Galliformes, Charadriiformes, “near-passerines,” and passerines), and the molt strategies (SBS, CBS, SAS, or CAS) that they believe each taxon exhibits. They provide little or no explanation regarding how they reached these conclusions. Thus, readers hoping to learn criteria and guidelines for identifying molt homologies that could, in turn, be used to interpret molt data (e.g., previously published descriptions) in terms of Howell et al.'s (2003) proposed revision find little guidance in this section.

In their subsection regarding passerines, Howell et al. (2003:650) correctly state that “Thompson and Leu (1994) considered the first postjuvenal plumage of Passerina buntings as a first supplemental plumage, followed by conventional first basic.” They claim that this “involves a novel concept in molt terminology since, by H-P convention, Thompson and Leu's (1994) supplemental plumage occurs before the start of the first plumage cycle.” To the contrary, Howell et al. (2003:639) defined the first plumage cycle “as the period between the attainment of juvenal plumage and the acquisition of the next basic plumage.” Thus, the first postjuvenal molt that Thompson and Leu (1994) called a presupplemental molt occurs during the first molt cycle, not before it.

In addition, Howell et al. (2003) reject the premise, adopted in previous work by Rohwer et al. (1992) and Thompson and Leu (1994), that one of the two body molts undergone by young Passerina buntings in their first summer and fall had to be a prebasic molt. Instead, Howell et al. (2003) propose that these two body molts are preformative molts. However, once again Howell et al. (2003) do not provide any criteria by which to distinguish between first-cycle molts that are preformative versus those that are homologous with molts in the definitive cycle. The second body molt of Passerina buntings is similar in timing, extent, and to various degrees in the resulting change in plumage color, to that of older birds undergoing definitive prebasic molt (Thompson and Leu's 1994) and, therefore, is homologous with definitive prebasic molt.

HOWELL ET AL.'S PROPOSED REVISION TO THE HUMPHREY-PARKES SYSTEM

Howell et al. (2003) were motivated to propose a revised nomenclature for molt and plumage homologies because of two perceived failings of the H-P system. First, they argued that that using traditional first prebasic molt as the starting point for plumage succession leads to noncorrespondence between nomenclature and presumed homology in first basic plumages (e.g., in supposed SAS species which ostensibly lack a first prebasic molt). However, I have shown that the H-P system does not require using traditional first prebasic molt as the starting point for plumage succession; nor do first prebasic molts that have been evolutionarily lost or developmentally suppressed pose a problem for identifying molt and plumage homologies. Second, they argue that plumage color should not be used for evaluating molt and plumage homologies. However, I have shown that by using plumage color to identify the plumages to which feathers likely belong, the timing and extent of molts, and thus their homologies, can be documented more accurately than if plumage color is not used. Thus, because Howell et al.'s (2003) criticisms of the H-P system are incorrect, there is no need to revise the H-P system: it still works.

Despite the lack of need or justification for a revised H-P system, does Howell et al.'s (2003) system offer advantages over the H-P system? Unfortunately not. To follow their revised H-P system, one must accept their notion that no first-cycle molts are homologous with prebasic molts in subsequent cycles. However, this is not so as many species have a molt in their first cycle that is homologous to definitive prebasic molt (Thompson and Leu 1994). In addition, Howell et al. (2003) offer only two guidelines for identifying molt homologies: (1) molts that have similar timing are homologous, and (2) molts that are complete or nearly so are prebasic. However, Humphrey and Parkes (1959) and subsequent authors (Rohwer et al. 1992, Thompson and Leu 1994) also advocated use of these same guidelines as well as additional criteria (plumage color, extent of molt). Thus, Howell et al.'s system does not offer any new or better criteria for identifying homologies than those suggested by Humphrey and Parkes (1959) and others.

Last, Howell et al. (2003) maintain that our knowledge of molts and plumages of North American and Australian birds is relatively good. To the contrary, our knowledge of the sequence of molts and plumages, especially during early postjuvenal development, is remarkably incomplete and inaccurate (Leu and Thompson 2002). For example, previously unrecognized early postjuvenal molts and plumages have been “discovered” and documented in recent years in many species, including such geographically widespread and well-studied species as Indigo Buntings (Passerina cyanea; Rohwer 1986) and Northern Cardinals (Thompson and Leu 1994) clearly demonstrating that early postjuvenal molts and plumages of birds in North America are poorly known. Therefore, although it is possible that some first-cycle molts may be evolutionarily new molts as suggested by Howell et al. (2003), or evolutionarily lost or developmentally suppressed molts as I suggested previously, we will not have sufficient data to determine this until molts and plumages in the first cycle are studied quantitatively, in detail, in many more species of many more groups of birds. Further, to do so, it is essential that these studies be done on groups of closely related species of birds (i.e., from the bottom up), rather than across phylogenetically diverse taxa as proposed by Howell et al. (2003). Such additional knowledge may justify revising the H-P system in the future; until then, there is no reason to revise the H-P system.