Proposal (693) to South American Classification Committee
Recognize Formicivora paludicola as a valid species
Effect on South American Check-List: This proposal would add a newly described species to SACC official list.
Background: Buzzetti et al. (2013) described a new species of antwren, Formicivora paludicola (São Paulo Marsh Antwren), from the São Paulo state, Brazil, which was discovered at only about 40 minutes by car from the São Paulo city, one of the largest cities in the world. The species was found in only few localities in the Paraíba do Sul river valley, and although its range should have originally at least 300 km2 of marshes, the current area of occupancy is estimated in less than 1.5 km2 and its population is smaller than a thousand individuals (Del-Rio 2014). The species, as in the case of Formicivora (Stymphalornis) acutirostris, is restricted to marsh habitats, a feature unseen in other Thamnophilidae (Zimmer & Isler 2003, Reinert et al. 2007). The two species are allopatric, being separated by about 350 km, and by about 600 m in altitudinal range: F. paludicola occurs between 600 and 760 m (Buzzetti et al. 2013), and F. acutirostris between 0 and 25 m (Reinert et al. 2007). Formicivora paludicola (n = 13 skin specimens and 37 living birds) can be diagnosed from its sister species Formicivora acutirostris (n = 13 skin specimens and 69 living birds) by plumage characteristics and a smaller bill length, with both species being also diagnosable by representing monophyletic mitochondrial lineages that diverged in the last one million years (Buzzetti et al. 2013). Vocalizations of the two species overlap in several parameters, but do not fit the guidelines proposed by Isler et al. (1998) for species recognition in the Thamnophilidae using degree of difference in vocalizations. Nonetheless, the vocalizations of F. paludicola are lower-pitched, and the two differ in their aggressive call (but sample size for such vocalizations is small).
Analysis: Currently SACC recognizes eight species of Formicivora (iheringi, erythronotos, grisea, serrana, littoralis, melanogaster, and grantsaui), and one species in the genus Stymphalornis. Gonzaga (2001), based on a dataset of vocalizations and morphology analyzed by parsimony, was the first to suggest that to keep Formicivora monophyletic, (1) F. iheringi should be excluded from the genus, and (2) Stymphalornis should be synonymized with Formicivora. More recent studies (Bravo 2012, Belmonte-Lopes 2013, Bravo et al. 2014) using DNA data (three mitochondrial genes, one nuclear intron, and two nuclear exons) recovered an arrangement similar to that proposed by Gonzaga (2001), also suggesting the need to exclude F. iheringi and to include Stymphalornis in Formicivora.
Data from morphology, vocalizations, and genetics leave no doubt that F. paludicola is sister to F. acutirostris, and Buzzetti et al. (2013) diagnosed F. paludicola only in relation to F. acutirostris. Formicivora paludicola was diagnosed based on plumage (darker than in F. acutirostris in both sexes), smaller size and weight (statistically significant differences but with overlap in measurements), and consistent genetic differences in some positions of three mitochondrial genes (cytochrome b, ND2, and ND3, uncorrected genetic distances between species ranging between 0.003-0.017). The phylogenetic analysis presented in the description showed a high support for the monophyly of F. paludicola and F. acutirostris, but did not include a large sample of both taxa (n = 3 for F. paludicola, and n = 4 for F. acutirostris). Additional analysis based on a larger sample of the ND2 for F. acutirostris (n = 78 individuals) also supports the monophyly of both taxa (R. Belmonte-Lopes, unpub. data).
The measurements of the vocalizations of the taxa not fit the criteria of Isler et al. (1998) for species recognition in antbirds due to the large overlap, but in terms of means, the loudsong of F. paludicola has a shorter phrase duration, a shorter duration of the second note, and a shorter interval between the first and second notes (Buzzetti et al. 2013). Buzzetti et al. (2013) also pointed out differences between the two taxa in the form of the contact call note and differences in what they called aggressive call; but the sample was small (n = 4 individuals and 48 calls for F. paludicola, and n = 2 individuals and 2 calls for F. acutirostris) and showed overlap in frequency and temporal parameters. Even so, Buzzetti et al. (2013) did not consider this an impediment to describing paludicola as a species, and they stated on p. 285 that “In this context it is worth mentioning the example of Terenura maculata and T. sicki, species with evident plumage differences, with the latter replacing the former in the northern Atlantic Forest, but which do not fit the diagnostic criteria proposed for vocalizations by Isler et al. (1998) (see Minns et al. 2009), as in the case of F. paludicola and F. acutirostris.”
Buzzetti et al. (2013) discussed two possible hypotheses for the isolation of the two taxa, one related to river capture and neotectonic events (that occurred in the last 1.2 Million years), and another related to population isolation due to sea level changes, but they are not mutually exclusive. More important, the authors stress in the description, p. 286, that “Independently of the biogeographical events involved in the speciation between F. paludicola and F. acutirostris, we consider that, in spite of present day climatic change and the predicted rise in sea level (Church & White 2006, IPCC 2007), there is no possibility of expansion in the ranges of F. paludicola and F. acutirostris and contact between them in the near future. Under an evolutionary and conservationist view, F. paludicola represents a distinct evolutionary lineage from F. acutirostris, and as so it should be a target for conservation action.”
Recommendation: I would argue for a “YES” vote to recognize Formicivora paludicola as a valid species in the SACC list. From an evolutionary standpoint, both taxa already show differences in plumage and in some morphometrics and vocal parameters, and although there is still extensive overlap in several measurements, the populations of F. paludicola and F. acutirostris are already deriving toward the fixation of different characteristics. This can be seen as a case of disruptive selection (see Hendry et al. 2009) in two allopatric populations, or as a case of incipient speciation (see Brelsford & Irwin 2009), what is expected if the two taxa diverged only in the last one million years. Even not being able to rule out that both species would freely interbreed if in contact (which would make them not fit Ernest Mayr’s biological species concept - BSC), such contact is not expected to occur naturally in several human lifetimes, if it ever occurs at all, because of the landscape changes made by civilization.
The two taxa (F. paludicola and F. acutirostris) lack vocal differences sufficient for species rank according to the criteria proposed by Isler et al. (1998), which can be seen as an argument for the species not fitting in the BSC due to supposed lack of differences in vocal parameters that could be associated with mating. Because F. paludicola and F. acutirostris are allopatric taxa with very similar habits and biology, there are no strong pressures toward change in its vocal parameters. If we consider an absence of strong pressures, differentiation would occur at random over time, with fewer differences expected in such recently diverged taxa. Other allopatric taxa that also do not meet the Isler et al. (1998) criteria for species recognition in antbirds (Terenura maculata/T. sicki; Minns et al. 2009; Formicivora serrana/F. littoralis; Firme & Raposo 2011) are currently treated as separate species by the SACC; therefore, not meeting the thresholds for species recognition of Isler et al. (1998) should not be considered an impediment to the recognition of allopatric thamnophilid species. Additionally, repertoires of these two taxa contain as many as 16 different vocalizations (see Willis 1967), and so it is still possible that the two taxa have distinctive characteristics in vocalizations not analyzed in the description of F. paludicola that.
Currently, BirdLife International adopts the SACC taxonomy for evaluating species for the IUCN RedList, so a species not recognized by the SACC is not even evaluated for inclusion in the list. In reality, if a species is not included in IUCN RedList, it means that there will be no international aid for conservation of such taxa. Formicivora paludicola is considered “critically endangered” in the São Paulo state RedList (Silveira, 2009), and the evaluation of Del-Rio (2014) suggested that the species should be listed as “critically endangered” in the IUCN RedList due to its area of occupancy being estimated in less than 1.5 km2. Because the area of range is so small, if F. paludicola were considered the same species as F. acutirostris, this would not change the category of F. acutirostris as an “endangered” species, but certainly could lead to the loss of the small divergent evolutionary lineage represented by F. paludicola.
Ricardo Belmonte-Lopes, Bianca L. Reinert & Luís F. Silveira, November 2015
Belmonte-Lopes, R. 2013. Investigando o isolamento esplêndido da América do Sul: filogenia e biogeografia histórica dos Thamnophilidae (Aves: Passeriformes: Tyranni). Ph.D. dissertation. Curitiba: Universidade Federal do Paraná.
Bravo, G.A. 2012. Phenotypic and niche evolution in the Antbirds (Aves, Thamnophilidae). Ph.D. Dissertation. Baton Rouge: Louisiana State University.
Bravo, G.A., Remsen, J.V. Jr., Brumfield, R.T. 2014. Adaptive processes drive ecomorphological convergent evolution in antwrens (Thamnophilidae). Evolution 68(10): 2757–2774.
Brelsford, A., Irwin, D.E. 2009. Incipient speciation despite little assortative mating: the Yellow-rumped Warbler hybrid zone. Evolution 63(12): 3050-3060.
Buzzetti, D.C., Belmonte-Lopes, R., Reinert, B.L., Silveira, L.F., Bornschein, M.R. 2013. A new species of Formicivora Swainson, 1824 (Thamnophilidae) from the state of São Paulo, Brazil. Revista Brasileira de Ornitologia 21(4): 269-291.
Church, J.A. & White, N.J. 2006. A 20th century acceleration in global sea-level rise. Geophysical Research Letters, 33: LO1602, doi:10.1029/2005GL024826
Del-Rio, G. 2014. Distribuição, habitat e área de vida do bicudinho-do-brejo-paulista (Formicivora paludicola). Msc. Dissertation in Zoology. São Paulo: Universidade de São Paulo.
Firme, D. & Raposo, M. 2011. Taxonomy and geographic variation of Formicivora serrana (Hellmayr, 1929) and Formicivora littoralis Gonzaga and Pacheco, 1990 (Aves: Passeriformes: Thamnophilidae). Zootaxa, 2742: 1-33.
Gonzaga, L.A.P. 2001. Análise filogenética do gênero Formicivora Swainson, 1825 (Aves: Passeriformes: Thamnophilidae) baseada em caracteres morfológicos e vocais. Ph.D. dissertation. Rio de Janeiro: Universidade Federal do Rio de Janeiro.
Hendry, A.P., Huber, S.K., De León, L.F., Herrel, A., Podos, J. 2009. Disruptive selection in a bimodal population of Darwin finches. Proc. R. Soc. B. 276: 753-759.
IPCC. 2007. Cambio climático 2007: informe de sínteses. Cambridge: Cambridge University Press.
Minns, J.C.; Buzzetti, D.R.C.; Albano, C.G.; Whittaker, A.; Grosset, A.E. & Parrini, R. 2009. Birds of Brazil/Aves do Brasil. DVD-ROM. Vinhedo: Avis Brasilis Editora.
Reinert, B.L.; Bornschein, M.R. & Firkowski, C. 2007. Distribuição, tamanho populacional, hábitat e conservação do bicudinho-do-brejo Stymphalornis acutirostris Bornschein, Reinert e Teixeira, 1995 (Thamnophilidae). Revista Brasileira de Ornitologia, 15(4): 493-519.
Silveira, L.F. 2009. Formicivora aff. acutirostris in Fauna Ameaçada de extinção no Estado de São Paulo: Vertebrados. (P.M. Bressan et al., eds.). Fundação Parque Zoológico de São Paulo e Secretaria do Meio Ambiente do Estado de São Paulo.
Willis, E.O. 1967. Behavior of Bicolored Antbirds. University of California Publications in Zoology, 79: 1-132.
Zimmer, K. J. & Isler, M.L. 2003. Family Thamnophilidae (Typical Antbirds), pp. 448-681. In: del Hoyo, J.; Elliott, A. & Christie, D. A. (eds.). Handbook of The Birds of The World, Vol. 8. Broadbills to Tapaculos. Barcelona: Lynx Edicions.
Comments from Stiles: “YES, hesitantly – this is definitely a borderline case of what looks like ongoing speciation, but given distribution and plumage differences, these two might best be considered members of a superspecies.”
Comments from Stotz: “NO. This is a tough case, very near the boundary of separate species versus subspecies. I am open to changing my vote if others provide arguments to support this split. The fairly minor plumage differences, limited vocal differences, and small genetic distance argue against specific recognition for me. The differing elevational ranges are an argument for splitting them, but there are species with disjunct lowland and montane pops. in SE Brazil.
“We should separately consider the generic treatment that this proposal uses. I have not looked into it, in any detail, but looks like Stymphalornis is embedded in Formicivora. However, Bravo et al , if fully implemented, has a number of additional implications for our generic treatment of antwrens.”
Comments from Zimmer: “Yuck! I’m really on the fence with this one. I think the authors of the proposal are correct in their assertion that secondary contact between paludicola and acutirostris is unlikely, and therefore, the two taxa are, at this point, on independent evolutionary trajectories. I also agree that, from a conservation perspective, recognizing paludicola as a distinct species could be important down the line in prioritizing the allocation of resources. For these reasons, I really, really want to vote “yes” on this proposal. But I don’t think that I can. I have a lot of field experience with both taxa – I’ve photographed, videotaped and tape-recorded multiple individuals of each – and if there are vocal differences between them, you couldn’t prove it by me. On many occasions, I’ve lured paludicola in with recordings of acutirostris songs and calls, and I’ve done the same with acutirostris, using recordings of paludicola. So, reciprocal playback experiments have shown birds from each population to respond readily to vocalizations of the other. Vocal analyses, as far as I can tell, failed to produce even a single diagnosable character – each character measured revealed overlapping samples, and this was with relatively small sample sizes for each taxon. This is a far cry from coming close to the suggested “three character” threshold of Isler et al. (1998). Similarly, the morphometric characters of “smaller size and weight” showed “statistically significant differences, but with overlap in measurements.” In other words, there were no diagnosable morphometric characters either. That leaves us with plumage characters. Females of the two taxa are very similar in plumage, whereas males differ primarily in the degree of saturation of pigmentation on the underparts (paludicola males being charcoal to blackish gray below; acutirostris males being more lead gray). I don’t think that using the degree of differentiation between Terenura maculata and T. sicki as a “yardstick” is the appropriate one here. While female T. sicki is quite similar to both sexes of maculata (differing primarily in the orange belly versus pale yellow), male sicki is much more different from males of maculata in plumage than paludicola and acutirostris are from one another. Also, I’m not at all sure that Minns et al. (2009) actually conducted a quantitative vocal analysis involving the two species of Terenura, as is implied by the authors of this proposal when stating that the two species did not differ vocally. Instead, I would argue that the more appropriate comparison to the present Formicivora/Stymphalornis situation is to look at the recently described Cinclodes espinhacensis and how it differs or fails to differ from the allopatric C. pabsti: minimal genetic divergence; no diagnosable vocal characters; response of each taxon to audio playback of the other in two-way trials; similar ecological requirements and behaviors; and plumage distinctions that hinge primarily on degree of color saturation (mainly in males). In the case of C. espinhacensis, we voted to treat it as a subspecies of pabsti, and that’s the path I’m inclined to take with paludicola. I would love to be proved wrong. So, NO.”
Comments from Robbins: “NO, for now. I’m primarily basing my tentative decision on the comments by Kevin Zimmer.”
Comments from Claramunt: “YES. Although the new taxon is very similar to F. acutirostris, it is diagnosable (distinct with no overlap) from it in three traits: 1) male underparts color (black versus gray) with no overlap or signs o intergradations, 2) bill length, again with no overlap, and 3) mitochondrial DNA, at the degree of complete reciprocal monophyly. Kevin mentioned overlap in morphometric characters but overlooked the fact that there is no overlap in exposed culmen even if male and females are combined (paludicola: 10.9-13.5mm, n=66; acutirostris: 13.8-14.9 mm, n=17). Of course the gap is small and a larger sample may reveal a slight overlap, but the point is that the bill differences are significant for a pair of very closely related taxa. These consistent differences in three presumably independent sets of traits are indicative of a history of independent evolution (isolation) indicating that paludicola and acutirostris are two independent lineages. Therefore, paludicola is a different species from the point of view of species as lineages. Regarding the presence of intrinsic reproductive barriers, the situation is less clear. Vocalizations are extremely similar so I’m not surprised that they respond to each other in playback trials. However, once a female approached a male, visual cues should play a role, and here is when the black versus gray breasts of males may play a role in sexual selection and isolation. I know this sounds speculative, but it seems to me that the difference between black and gray can be readily noticed by female thamnophilids; some male antbirds are gray, others are black, others are gray with black throats, and these differences are fixed within species, with no gradients or shades. It is possible that male breast color in these two antbirds may result in reproductive isolation. I don’t agree that the situation is similar to Cinclodes p. espinhacensis; paludicola differs from acutirostris with no overlap in three independent traits, one of which could play a role in species discrimination and sexual isolation. I admit that the situation is somewhat speculative under BSC criteria but I give paludicola the benefit of the doubt.”
Comments from Pacheco: “A tentative YES. The absence of overlap of two of its morphological characters, as pointed out by Santiago, allow me to recognize paludicola as a species, as long as their isolation is now a fact.”
Comments from Areta: “A painful NO. As others have noted, this is a borderline case for people requesting hard-based biological data to support a species-level split. It is clear that paludicola and acutirostris are distinct and diagnosable taxa based on morphological (subtle male color differences, different bill-length and other minor differences in measurements) and molecular (reciprocal monophyly of recently [250-640 ky bp] diverged clades) data. The question is whether this suffices to consider them different at the species level or not. Given the virtual lack of differences between paludicola and acutirostris in long-range and short-range vocal signals, playback responses described by Kevin, the extreme similarity in habitat use and the very similar females, I think that the minor differences in coloration/shape will not suffice to avoid extensive successful mating between members of these taxa.
“I do not support conservation-oriented taxonomic judgments: a taxonomic decision should be independent of the conservation "value" attributed to the populations/species/genus/family being evaluated. I wonder why we (meaning people concerned with nature conservation) need to recognize a species as such for it to merit conservation attention. Yes, policy makers are not biologists, but it is not difficult to understand that a different "unique thing" (taxon, population, culture) needs to be saved from extinction given its peculiarities. In this oversimplification in the name of conservation we are loosing precious biodiversity because we are contributing to perpetuate a simple and distorted view of the natural world by politicians, giving up the true complexities of nature. In this case, the preservation of ongoing evolutionary differentiation is for me the main reason to preserve both "cattail-antbirds". Preserving the processes and their products is more important than preserving just products. This is what I think conservation should aim at.”
Comments from Jaramillo: “YES. I will be honest and say that I am basing this on the comments of others, as the situation is borderline, and others have certainly more experience or have good arguments on how to deal with this problematic issue. I am troubled by the voice being similar between these two related taxa, but on the other hand a clear plumage difference seems important too. So I am influenced by Santiago’s comments, and give this a borderline YES, benefit of the doubt.”
Comments from Remsen: “NO. The new taxon is clearly a diagnosable unit and thus at leas a valid subspecies under BSC. The proposal suggests that we would require parapatry to test species rank under the BSC, but this is not the case (and this seems to be widely misunderstood). For allopatric taxa under the BSC, the question asked in terms of species rank takes a comparative approach: have the taxa diverged to the level of species rank as extrapolated from the “knowns,” i.e. those cases in which there is no doubt as to rank, i.e. sympatric and parapatric taxa in the same group of birds? In this case, the answer is NO. Minor differences in plumage and morphology are not associated with cessation of free gene flow in Thamnophilidae, but a certain degree of vocal divergence is (as shown by the Isler-Whitney paper).
“As for conservation, as painful as these facts are, I strongly believe that assigning rank should be completely independent of conservation concerns. Otherwise, such influences will backfire on the credibility of the scientific community and play into the hands of those who mistrust the objectivity of scientists. Hopefully, conservation efforts can still be directed at preserving the habitat of this evolutionary unit regardless of taxon rank.”