Volume 16 Issue 1 - 2022 | 58
© Assocation of Systematic Biologists in the Philippines Abstract
The monotypic Scale-feathered Malkoha Lepidogrammus cumingi (Fraser 1839) and polytypic Red-crested Malkoha Dasylophus superciliosus (Dumont 1823) are two of the endemic cuckoos in the Philippines. The taxonomy and distribution of these endemic cuckoos are poorly known. Recent distribution data of these cuckoos showed broader distribution patterns in the islands of Luzon, Catanduanes and Marinduque; however, morphometric variations among these island populations are still unknown. While both species are sexually monomorphic, the differences between sexes were mainly based on plumage coloration. Dasylophus superciliosus is composed of two subspecies: ssp. superciliosus (Southern Luzon) and ssp.
cagayanensis (Northern Luzon). The separation of the two subspecies of D. superciliosus were determined by the differences in superciliary feather, coloration of breast plumage, and tail band. In this study, we investigated the morphometric variations (1) between subspecies of D. superciliosus, (2) among island populations and (3) between sexes (sexual dimorphism) of the two malkoha species. Four linear measurements (bill length, wing length, tarsus length, tail length) were measured from 184 museum specimens. Results showed that the Catanduanes group (n=10) of L. cumingi exhibited smaller body size than the Marinduque group (n=9). Red-crested Malkoha D. superciliosus showed significant differences between its two subspecies where the ssp. cagayanensis (n=28) exhibited smaller body size (bill length, wing length and tail length) compared to ssp. superciliosus (n=81). Lastly, this study confirms that the two malkoha species are sexually monomorphic based on the analyzed morphometric data.
Keywords: endemics, island population, linear measurements, ornithology, Philippine malkohas
Estephen B. Fortela
*, Juan Carlos T. Gonzalez
Morphometric Variation in Lepidogrammus cumingi and Dasylophus superciliosus from Greater Luzon, Philippines based on Museum Specimens
Introduction
The Philippines is a megadiverse archipelagic country home to more than 700 bird species in which almost 250 species are considered endemics (Allen 2020). One group of birds endemic to the country is the Philippine Malkohas that belong to family Cuculidae (Payne 2005). The Scale- feathered Malkoha Lepidogrammus cumingi (Fraser 1839) and Red-crested Malkoha Dasylophus superciliosus (Dumont 1823) are endemic in Luzon, Catanduanes and Marinduque islands. Lepidogrammus cumingi is a monotypic species while D. superciliosus consists of two subspecies namely: ssp.
cagayanensis (Rand and Rabor, 1967) that occurs in Cagayan and Nueva Vizcaya provinces, and ssp. superciliosus that occurs in the west and southern regions of Greater Luzon (Rand and Rabor 1967; Kennedy et al. 2000; Payne 2005;
Erritzoe et al. 2012; Fortela and Gonzalez 2021).
Several issues are still unresolved in the taxonomy and distribution of Philippine malkohas. In species D.
superciliosus, Goodman and Gonzales (1990) recognized that its two subspecies have a broad habitat range of distribution in mainland Luzon but factors that caused the delineation between subspecies are still uncertain. A recent study by Fortela University of the Philippines Los Baños, College, Laguna, Philippines, 4031
*Corresponding author: [email protected] Date Submitted: 25 September 2022
Date Accepted: 15 April 2023
and Gonzalez (2021) showed that both species have indeed broader distributions, and the subspecies ssp. cagayanensis is not restricted in the north-east region of Cagayan province but also occurs in Tuguegarao City, Benguet Province and in Nueva Vizcaya province based on the re-examined museum specimens. The distinction between the two subspecies of D. superciliosus was based on the smaller body size, short red crest feathers, less white coloration at the base of the red crest feathers, and paler breast coloration in ssp. cagayanensis compared to ssp. superciliosus (Rand and Rabor 1967).
Both malkoha species are commonly distributed in Luzon, Catanduanes and Marinduque islands (Payne 2005); however, little is known about the morphological variations among their island populations. The three island populations of L. cumingi are assumed to be the same with each other mainly due to similarities on plumage colorations. On the other hand, the Catanduanes and Marinduque populations of D. superciliosus are hypothesized to be similar with the ssp. superciliosus (Southern Luzon) in mainland Luzon than to ssp. cagayanensis (Northern Luzon) (Payne 2005). Lastly, both L. cumingi and D. superciliosus do not exhibit sexual dimorphism mainly based on plumage coloration (Payne 2005) but no conclusive information is available on the differences between sexes using morphometric data.
Given these uncertainties, this study aimed to determine the morphometric variations in L. cumingi and D. superciliosus based on museum collections, specifically, (1) to determine the morphometric variations between the subspecies of D.
superciliosus, (2) to determine the morphometric variations among island populations of the two malkoha species, and (3) to determine the morphometric differences between sexes.
Volume 16 Issue 1 - 2022 | 59 Philippine Journal of Systematic Biology Online ISSN: 2508-0342
Investigating morphometric variations in both taxa is needed following the recent updates on the distribution patterns of both species in the Greater Luzon islands.
Materials and Methods
Measurement of Morphometric Characters
Morphometric data of L. cumingi, and D. superciliosus were collected from existing museum skins of bird collections in the Zoology Division of the National Museum of Natural History Philippines (NMNHP), UPLB Museum of Natural History (UPLB MNH), American Museum of Natural History (AMNH), Delaware Museum of Natural History (DMNH), Museum of Natural History of Kansas University (KUMNH), Field Museum of Natural History (FMNH), and Yale Peabody Museum of Natural History (YPMNH).
A digital caliper was used to measure four morphometric characters in birds to the nearest millimeter. Four morphometric characters were measured following Tobias et al. (2010): 1) bill length, which is measured from bill to skull where the bill reaches the cranium to the tip; 2) tarsus length; 3) wing length
Table 1. Morphometric measurements (in mm, mean ± SD) (range) of Lepidogrammus cumingi and Dasylophus superciliosus.
(unflattened wing chord); and 4) tail length from the tip of the upper tail (centralis feather) to the point of insertion.
Identification of subpopulations
Determination of morphometric variations in two endemic malkohas was done by comparing their subpopulations. The samples of the monotypic L. cumingi were grouped into three populations representing the islands of Luzon, Catanduanes, and Marinduque. On the other hand, morphometric analysis in D. superciliosus was done first by comparing the subspecies ssp. superciliosus (Southern Luzon, Catanduanes, Marinduque) with ssp. cagayanensis (Northern Luzon). The Southern Luzon group is composed of specimens located from Bataan, Laguna, Pampanga, Quezon Province, Rizal, and provinces from Bicol region while the Northern Luzon group is composed of specimens located from Cagayan, Isabela and Nueva Vizcaya provinces (Fortela & Gonzalez 2021). Then the island populations of ssp. superciliosus in Catanduanes and Marinduque were also compared with the Southern Luzon and ssp. cagayanensis populations. Lastly, sexual dimorphism of the two species was determined by
Species N Bill Length (mm) Tail Length (mm) Tarsus Length (mm) Wing Chord (mm) Lepidogrammus cumingi
Overall 75 37.42 ± 2.32 231.55 ± 10.71 40.91 ± 7.05 159.78 ± 6.16
(32.6 - 42.8) (209.0 - 251.3) (35.6 - 47.3) (145.9 - 172.4)
Luzon 56 37.32 ± 2.53 231.19 ± 11.80 40.97 ± 2.89 159.80 ± 6.74
(32.6 - 42.8) (209.0 - 251.3) (35.6 - 47.3) (145.9 - 172.4)
Catanduanes 10 36.43 ± 0.94 225.76 ± 3.18 39.10 ± 0.58 156.02 ± 1.07
(35.4 - 38.1) (220.0 - 241.7) (37.8 - 39.8) (154.3 - 158.0)
Marinduque 9 39.20 ± 0.35 239.17 ± 1.56 42.59 ± 0.54 163.83 ± 0.81
(38.7 - 39.6) (238.0 - 241.7) (41.7 - 43.2) (162.2 - 165.1)
Male 58 37.42 ± 2.39 231.44 ± 11.07 40.94 ± 2.69 159.8 ± 6.45
(32.6 - 42.8) (209.0 - 249.9) (35.6 - 47.3) (145.9 - 171.0)
Female 17 37.42 ± 2.11 231.95 ± 9.72 40.78 ± 2.57 159.72 ± 5.19
(34.3 - 41.6) (219.0 - 251.3) (37 - 46.7) (152.0 - 172.4)
Dasylophus superciliosus
Overall 109 35.32 ± 2.54 219.57 ± 12.01 35.77 ± 2.56 149.87 ± 5.84
(30.1- 42.3) (190.0 - 245.4) (30 - 41.0) (136.7 - 161.0)
D.s. cagayanensis 28 33.63 ± 1.39 216.03 ± 10.22 35.79 ± 2.57 147.07 ± 5.29
(30.7 - 35.8) (198.0 - 234.0) (30.5 - 40.7) (136.7 - 157.0)
D.s. superciliosus 81 35.90 ± 2.57 220.80 ± 12.44 35.81 ± 2.64 150.99 ± 5.59
(30.1 - 42.3) (190.0 - 245.4) (30.0 - 41.0) (137.8 - 161.0)
South Luzon 51 36.13 ± 2.48 222.73 ± 13.14 35.92 ± 2.57 151.49 ± 5.72
(30.8 - 40.6) (197.0 - 245.4) (197.0 - 245.4) (140.6 - 161.0)
Catanduanes 11 35.90 ± 1.71 215.18 ± 71.16 35.38 ± 3.29 151.60 ± 5.44
(33.1 -39.0) (204.0 - 230.0) (30.5 - 40.4) (141.8 - 157.3)
Marinduque 19 35.27 ± 3.23 218.94 ± 11.74 35.56 ± 2.21 149.16 ± 5.48
(30.1 - 42.3) (190.0 - 239.0) (31.9 - 41.0) (137.8 - 157.1)
Male 70 35.50 ± 2.12 219.54 ± 11.11 35.44 ± 2.61 150.19 ± 6.25
(30.7 - 40.5) (190.0 - 245.0) (30.0 - 40.0) (136.7 - 161.0)
Female 39 35.21 ± 2.75 219.63 ± 13.56 35.95 ± 2.54 149.55 ± 4.82
(30.1 - 42.3) (198.0 - 245.4) (30.0 - 41.0) (140.1 - 160.7)
Figure 1. Size distribution of the four morphometric characters between the two subspecies of Dasylophus superciliosus.
comparing between two sexes.
Statistical Analysis
The measured characters were first subjected to Shapiro- Wilk’s test (alpha=0.05) to determine the normal distribution pattern for each character. We then constructed normal probability plots to identify the possible outliers from the data.
All four characters were approximately normally distributed and all the analyses were based on the untransformed data.
Univariate summary statistics of the characters was performed to determine the mean length (mm), standard deviation (SD), and size range (minimum and maximum) of the four characters for each species. Comparison among populations (between subspecies of D. superciliosus, between island populations, and between sexes) of the two species was done using One- way ANOVA (alpha = 0.05) and Welch two sample t-test (alpha = 0.05) for each character. To determine the correlation of island size with the body size of the two species, Principal Component Analysis (PCA) using correlation matrix was used to summarize the patterns of variations on the morphometric data producing independent composite variables (PC axes).
Only the characters with the highest loading scores in PC1 were considered and plotted against log-transformed island size (independent variable) using linear regression analysis.
Boxplots were generated to show differences between compared groups. All statistical analyses were performed through R v. 4.0.3 (R Core Team 2021) with RStudio (RStudio Team 2020).
Results
A total of 184 museums specimens of Lepidogrammus cumingi (n=75) and Daslyophus superciliosus (n=109) were examined and measured from various museum collections.
Table 1 summarizes the estimated mean, standard deviation, and size range of the four characters for both species.
Differences between ssp. cagayanensis and ssp. superciliosus Significant differences were observed between ssp. cagayanensis and ssp. superciliosus. Results of the Welch’s t-test between the two subspecies showed that ssp.
cagayanensis exhibits smaller mean bill length (t87= 5.82, p<0.001), shorter mean wing length (t50 = 3.58, p<0.001), and shorter mean tail length (t57 = 2.02, p<0.05) (Figure 1).
Among Island Populations
Results showed significant differences between Catanduanes and Marinduque populations in all four morphometric characters of L. cumingi which indicates that the Catanduanes population has smaller mean bill length (F2,72 = 3.88, p<0.05), shorter mean wing length (F2,72 = 4.14, p<0.054), shorter mean tarsus length (F2,72 = 4.53, p<0.05), and shorter mean tail length (F2,72 = 4.00, p<0.05) (Figure 2). There were no morphometric differences found between the Luzon population and the adjacent island populations.
Similar results were observed in D. superciliosus where there were no size differences among the three populations of ssp.
superciliosus indicating that the three geographic groups are morphometrically similar (bill length: F2,78 = 0.76, p>0.05; wing length: F2,78 = 1.26, p>0.05; tarsus length: F2,78 = 0.25, p>0.05;
tail length: F2,78 = 1.98, p>0.05) (Figure 3). PCA results showed
that only the tail length has the highest loading scores for both L. cumingi (loading score = 0.98024) and D. superciliosus (loading score = 0.9988) in PC1. Linear regression analysis showed that there is no significant correlation between island size and tail length for both species (p>0.05) (Figure 4).
Figure 2. Size distribution of the four morphometric characters of Lepidogrammus cumingi among island populations. Cat – Catanduanes, Luz – Luzon, Mar – Marinduque.
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Between Sexes
There were no significant differences on the four characters between sexes of L. cumingi using Welch’s t-test indicating the lack of sexual dimorphism based on the measured morphometric data (bill length: t29 = 0.01, p>0.05;
wing length: t32 = 0.05, p>0.05; tarsus length: t27 = 0.23, p>0.05;
tail length: t30 = 0.25, p>0.05). Similar results were observed in D. superciliosus indicating sexual monomorphism (bill length: t96 = 0.62, p>0.05; wing length: t96 = 0.62, p>0.05;
tarsus length: t77 = 0.98, p>0.05; tail length: t66 = 0.05, p>0.05).
Discussion
The data collected in this study provided a comprehensive comparative morphometric study in two Philippine malkohas endemic to the islands of Luzon, Catanduanes and Marinduque. The significant differences between subspecies of D. superciliosus can be attributed to several factors such as ecological partitioning (Petruf 2017), genetic differences (Braun 2000), and geographic variation (Tobias 2022). Results are concordant with the observations of Rand and Rabor (1967) where the Southern Luzon populations (ssp. superciliosus) are bigger in body size compared to the Northern Luzon population (ssp. cagayanensis). These morphometric differences can also be attributed to geographic variation between subspecies as hypothesized by Welton et al. (2010), Vallejo (2014), and Fortela and Gonzalez (2021). In addition, a comprehensive study using both genetic and phenotypic analyses showed that both ssp. cagayanensis and ssp. superciliosus exhibited low DNA sequence differences but with high phenotypic variation (score = 8 based on the Tobias criteria) suggesting significant morphological differences (Campbell et al. 2016).
Significant morphometric variations were observed in all four characters of L. cumingi between the Catanduanes and Marinduque island populations where the former group exhibited smaller mean body size compared to the latter group. It is hypothesized that interaction among island Figure 3. Size distribution of the four morphometric characters of
Dasylophus superciliosus among subpopulations. Cat – Catanduanes, Mar – Marinduque, NL – North Luzon, SL – South Luzon.
Figure 4. Linear regression analysis of island size (log transformed) and tail length of L. cumingi (tail length = 5.57 – 0.004*island size) and D.
superciliosus (tail length = 4.21 + 0.001*island size).
62 | © Assocation of Systematic Biologists in the Philippines Volume 16 Issue 1 - 2022 populations of terrestrial vertebrates in the Philippines play
significant role on morphological variations (Clegg and Owens 2002; Scott et al. 2003; Sandvig et al. 2019; Benitez- Lopez et al. 2021) as explained by the Pleistocene Aggregate Island Complex (PAIC) (Brown et al. 2013; Vallejo 2014).
Morphometric variations in L. cumingi can also be attributed to (1) phenotypic plasticity (Nussey et al. 2005; Grenier et al.
2016), (2) as a result of genetic drift (sampling bias) since only few samples were collected in these two islands based on the examined museum specimens (Trense and Tietze 2018) or (3) it can be due to anthropogenic activities (e.g. conversion of existing forest habitats to agricultural and residential areas).
Both malkoha species showed sexual monomorphism.
Sexual monomorphism in birds is hypothesized to be attributed to (1) biparental care of both male and female parents, (2) as a form of adaptation to avoid mating competition in monogamous species, (3) functional trait in males to signal its mates, or (4) can be due to weak sexual selection on the roles between males and females (Brennan 2010; Van Rooij and Griffith 2010).
Conclusion and Recommendations
This study highlights the importance of museum specimens in studying morphological variations in less studied tropical birds such as the malkohas despite their Least Concern conservation status (IUCN 2021). Future studies are recommended to determine the variations of the populations of L. cumingi using integrated phenotypic and genetic data to validate the differences between the Catanduanes and Marinduque populations, and to evaluate the distribution pattern and morphometric differences between ssp.
cagayanensis and ssp. superciliosus.
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