A morphometric analysis of the lungs of high-altitude ducks and geese

Abstract

We examined the morphology of the lungs of five species of high-altitude resident ducks from Lake Titicaca in the Peruvian Andes (yellow-billed pintail [Anas georgica], cinnamon teal [Anas cyanoptera orinomus], puna teal [Anas puna], speckled teal [Anas flavirostris oxyptera], and ruddy duck [Oxyura jamaicensis ferruginea]) and compared them with those of the high-altitude migratory bar-headed goose (Anser indicus) and the low-altitude migratory barnacle goose (Branta leucopsis). We then determined the relationship between mass-specific lung volume, the volume densities of the component parts of the lung, and previously reported hypoxia-induced increases in pulmonary O₂ extraction. We found that the mass-specific lung volumes and the mass-specific volume of the exchange tissue were larger in the lungs of high-altitude resident birds. The bar-headed goose had a mass-specific lung volume that fell between those of the low-altitude species and the high-altitude residents, but a mass-specific volume of exchange tissue that was not significantly different than that of the high-altitude residents. The data suggest that the mass-specific volume of the lung may increase with evolutionary time spent at altitude. We found an inverse relationship between the percentage increase in pulmonary O₂ extraction and the percentage increase in ventilation across species that was independent of the volume density of the exchange tissue, at least for the resident Andean birds.

Keywords: altitude; birds; hypoxia; lungs; morphometry; pulmonary O2 extraction; pulmonary exchange tissue.

Figure 1

Sample haematoxylin and eosin‐stained section of a bird lung with a 192‐point grid lattice superimposed. Secondary bronchi and parabraonchi, blood vessels larger than capillaries, and exchange tissue are indicated. Scale bar: 100 µm

Figure 2

Mass‐specific lung volumes (cm³ kg^–1) of the species in this study. Barnacle goose, bar‐headed goose, yellow‐billed pintail, cinnamon teal, ruddy duck, puna teal, speckled teal, and Andean goose. Values for the Andean goose taken from Maina et al. (2017) are presented for comparison. Error bars represent standard error. * Indicates a significant difference between the groups indicated by the bar, † indicates a significant difference with all but the species indicated by the bar and ns, ‡ indicates a significant difference with all other species

Figure 3

Sample haematoxylin and eosin‐stained section from each species in this study. (a) yellow‐billed pintail, (b) cinnamon teal, (c) ruddy duck, (d) puna teal, (e) speckled teal, (f) barnacle goose, (g) bar‐headed goose. Scale bars: 100 µm except for the bar‐headed goose, which is 50 µm

Figure 4

Mass‐specific volumes (cm³ kg^–1) of the different components of the lung for each species. Barnacle goose, bar‐headed goose, yellow‐billed pintail, cinnamon teal, ruddy duck, puna teal, speckled teal, and Andean goose. Values for the Andean goose taken from Maina et al. (2017) are presented for comparison. Error bars represent standard error. † indicates a significant difference with all but the species indicated by the bar and ns, ‡ indicates a significant difference with all other species

Figure 5

Volume densities (% of total volume) occupied by the different components of the lung for each species. Barnacle goose, bar‐headed goose, yellow‐billed pintail, cinnamon teal, ruddy duck, puna teal, speckled teal, and Andean goose. Values for the Andean goose taken from Maina et al. (2017) are presented for comparison. Error bars represent standard error. * indicates a significant difference between the groups indicated by the bar, and ‡ indicates a significant difference with all other species

Figure 6

Mean volume densities of the secondary bronchi, primary bronchi, blood vessels larger than capillaries and exchange tissue for sections 1–5 of each lung of each of the five Andean duck species averaged together. The insert is a schematic of the lung showing the sulci where the lung interdigitates with the ribs and where the cuts were made to obtain the five sections. Error bars represent standard error

Figure 7

Comparison of the bird lung volumes in the present study (circles in red) with those of the population of birds for which similar data are available (circles in cyan, taken from Maina et al., 2017: table S8)

Figure 8

Comparisons of volume densities of primary bronchi, secondary bronchi and parabronchi (parabronchi), blood vessels, and exchange tissues for birds with different lifestyles. Lifestyles are flightless (FL), low‐altitude birds (LA), migratory glider (MG), high‐altitude resident (HAR), and high‐altitude migratory (HAM). FL: Ostrich (Struthio camelus), Emu (Dromaius novaehollandiae); LA: Barnacle goose (Branta leucopsis), Canada goose (Branta canadensis), Mute swan (Cygnus olor), Mallard duck (Anas platyrhynchos), Grosbeak weaver (Ambryispiza albifrons), White‐winged robin (Cercotrichas leukophrys), Yellow flycatcher (Chloropeta natalensis), Singing cisticola (Cisticola cantans), Robin chat (Cossypha cafra), Waxbill (Estrilda astrid), Yellow‐bellied waxbill (Estrilda melanotis), African rock martin (Hirundo fuligula), Red‐billed firefinch (Laganosticta senegala), Tropical boubou (Lanius aethiopicus), Fiscal shrike (Lanius collaris), Bronze mankin (Lonchura cucullate), Bronze sunbird (Nectarina kilimensis), Golden‐winged sunbird (Nectarina reichenowi), House sparrow (Passer domesticus), Baglafecht weaver (Ploceus baglafecht), Black‐headed weaver (Ploceus cucullatus), Spectacled weaver (Ploceus ocularis), Holub’s golden weaver (Ploceus xanthops), Tawny prinia (Prinia subflava), Canary (Serinus canaria), Yellow‐fronted canary (Serinus mozambicus), Common starling (Sturnus vulgaris), Redwing (Turdus iliacus), Olive thrush (Turdus olivaceus). MG: Razorbill (Alca torda), Spectacled guillemot (Cephus carbo), Herring gull (Larus argentatus), Common gull (Larus canus), Black‐headed gull (Larus ridibundus). HAR: Yellow‐billed pintail (Anas georgica), Cinnamon teal (Anas c. orinomus), Ruddy duck (Oxyura j. ferruginea), Speckled teal (Anas oxyptera), Puna teal (Anas puna), Andean goose (Chloephaga melanoptera). HAM: Bar‐headed goose (Anser indicus). Data are taken from Maina (2002) and Maina et al. (2017). Data from birds in the present study are shown in red. The ‘e’ and ‘o’ beside the data for the flightless birds indicate data from the emu and the ostrich

Figure 9

Comparison of percentage of exchange tissue, percentage of pulmonary O₂ extraction, and percentage of ventilation increase. (a) Percentage of the lung composed of exchange tissue. (b) Percentage of O₂ extracted from inspired air while breathing a hypoxic gas mixture (5% O₂). (c) Percentage of increase in ventilation in birds breathing the same hypoxic gas mixture (100% is normal level). Data sources for (b) and (c) are Scott et al. (2015), Lague et al. (2017) and Ivy et al. (2019)