By Aaron Sneep (Summer Work Experience Program – SWEP – intern 2017)
Mapping Culverts at QUBS By Aaron Sneep (Summer Work Experience Program intern 2017) Queen’s University Biological Station (QUBS) strives to be one of the best field stations in North America. To provide more resources for researchers at the station, QUBS wishes to develop a detailed, fine-scale hydrological map not only its land holdings but also adjacent lands. This summer’s field and data management technicians, Dayna Zunder and myself, have been hard at work collecting data on the locations of culverts in the region to contribute to this hydrological map (Figure 1).
The culvert data will be used to complement and correct computer generated terrain models of the region produced from LIDAR (Light Detection and Ranging) data (see Figure 2). The reason we require the locations of culverts to supplement the LIDAR data is rooted in the process of LIDAR data collection. During LIDAR data collection, laser light is emitted from an aircraft flying overhead and each data point collected during the process represents a surface that reflected a laser back to the receiver. LIDAR data is often referred to as a point cloud due to the appearance of the data collected. Figure two shows an example of a LIDAR point cloud.
Using the point clouds, we can generate terrain models, often referred to as DEMs (Digital elevation model), or DTMs (Digital Terrain Model). With these models, we can simulate how water flows through the region (i.e. imagining how water flows from a high point in the landscape to lower elevations). However, there are concerns and caveats with this approach. The laser used during LIDAR collection cannot penetrate through solid objects such as a bridge or roadway overlying a culvert. In addition, due to limitations in spatial resolution it can be challenging to distinguish the locations of culvert openings using LIDAR data alone. Knowing the locations of culverts and bridges allows us to indicate their locations in the terrain models, and change our flow models that would otherwise appear as impediments to indicate that water is able to flow through these points in the landscape. Therefore, collecting spatial data for bridges and culverts in the region allows us to more accurately represent the flow of water through the watershed. Figure 3 shows a comparison of a DSM with and without culverts indicating where water flow can occur.
These models of water flow can be useful in biological research because of the important role connectivity can play in biological systems. For example, connectivity between different areas within the watershed can have implications for nutrient transport, species interactions, and dispersal and gene flow. As such, understanding hydrological connectivity within this watershed we hope will be widely applicable and encourage additional research at QUBS. There is still much work left to complete the hydrological model for this watershed, but future researchers at QUBS can look forward to using an accurate, fine-scale hydrological map to illuminate their research questions.
On October 1st and 2nd, 2015, I had the unqualified pleasure of joining the inimitable Richard Aaron, who teaches the “Fabulous Fall Fungi” workshops at the Queen’s University Biological Station (QUBS). Right, with a weapon in hand, Richard makes a point to the small class (limited to twelve people). Unlike previous field courses that I have covered for this blog that are intended for undergraduate university students, this one is open to anyone who is interested. It is a three-day workshop that was offered three times in 2015. Several participants have taken the workshop several times, as it provides the ideal blend of learning and invigorating outdoor activity. As extra enticement, no two workshops yield the same set of species. If luck prevails, a carefully selected specimen may be cooked for lunch! Before attempting this on your own (eating a specimen for lunch), take the workshop at least once.
I arrived on the afternoon of the second day of the workshop. Collecting and identifying had occurred the entire day before. Both identified and yet-to-be identified specimens were spread across the tables, with Richard sharing salient tidbits about the various fungi with the class.
The Real Reason for the Knife
Richard had just cut the mushroom shown below in half lengthwise. As you can see, the yellow flesh almost instantly turned blue when exposed to the air. This bolete mushroom (a bolete has pores on the underside of its cap rather than gills) is called Boletus subvelutipes, which grows on the ground under hardwoods, especially oak, and conifers, particularly hemlock.
Above is a Chanterelle (Cantharellus cibarius), the same kind served in fancy restaurants. Those wrinkles look like gills, but they aren’t!
Above is a Hexagonal-Pored Polypore (Favolus alveolaris), which grows on dead branches and is usually seen only after the branches fall to the ground.
Above, one of the most common and most recognized polypore mushrooms, Turkey Tail, found on forest floor logs. Unlike many other common names, this one is descriptive. There are other bracket fungi (polypores) which look like Turkey Tail. There’s even a fungus without pores called False Turkey Tail which that bears a striking resemblance.
Above, Richard explains a central characteristic for identifying gilled mushrooms: how the gills (lamellae) attach or do not attach to the stem. The latter arrangement shown by Richard above, is termed “free gills” because the gills are not attached to the stem. And if the attachment is more narrow, this is called “adnexed”, whereas “decurrent” gills attach at a downward angle along the stem, forming an angular whorl around the stem. The other two gill attachments Richard discussed were “notched” and “sinuate”, both of which are notched along each gill edge close to the stem.
Above, Polyporus squamosus, a Basidiomycete commonly known as Dryad’s Saddle, which grows on hardwood stumps, logs and trees. It is an annual bracket fungus, with the characteristic colours, flattened scales and black stem as seen in the photo of this mature specimen (immature specimens lack the black stem). Polypores, as their names suggests, have pores on the underside, which are the openings of tubes. The pores of some species can be seen with the naked eye, whereas other species require the use of a hand lens.
There are an estimated 5,000 macrofungi in Ontario (fungi that can be seen with the naked eye). Field guides don’t cover most of these. For example, Mushrooms of Ontario and Eastern Canada covers just over 600 species. Right, workshop participant Brett, who was a great help to me and others, as he has taken the workshop before, was identifying the following mushroom, with a partial veil, rosy-coloured cap and yellow flesh: a Suillus pictus (sometimes referred to as Suillus spraguei), which is found under White Pine trees.
We’ll get back to Brett later, as he provided a photo of a magical fungal phenomenon from the local woods.
Above is one of the “inky cap” mushrooms, which belongs to the order Agaricales (gilled mushrooms). It is a decomposer of wood, and can be found on wood chips, sawdust, and other woody debris. As this mushroom ages, the gills liquefy into a black inky mess, and the cap quickly changes from a bell shape to a split flat cap like the one shown above. This transformation aids in the distribution of spores, although making the species at this stage more difficult to identify. The one above was identified as Coprinus lagopus. Recent DNA studies suggest different evolutionary relationships, and it is now known as Coprinopsis lagopus, but Richard chose to use the name found in field guides in order to avoid confusion.
Above is a very special mushroom, Panellus stipticus, which is also featured below, doing its magical thing, bioluminescence. Yes, if you are a good mushroom detective, and find a colony of this mushroom during the day, go back at night to see the show. Thanks to Brett for taking this photo, and to Richard for sending it to me.
One peculiar characteristic sometimes used as aid in identifying fungi is odour. It so happens that a small percentage of fungi have distinct odours, reminiscent of coconut, anise, maple syrup, almond extract, coal tar, mouse, radish, cucumber, flour and more. Jennifer is seen below taking a close look at one of these, a Lobster Mushroom (Hypomyces lactifluorum), which she had collected. This unique species does indeed smell much like fresh lobster. It also has a different lifestyle, as it feeds on other mushrooms. Technically, this is not a mushroom, but a parasitic ascomycete fungus.
Fungi grow everywhere. They are a universal life form, making up a large proportion of the Earth’s living mass. Below is a gilled mushroom that grows on conifer cones, particularly white pine and Norway spruce, and also on magnolia cones: Baeospora myosura. The convex shaped cap is crowned with a papilla (literally, a nipple), a characteristic shared with many small, gilled mushrooms, particularly in the genus Inocybe.
After supper, we waited until sundown and then gathered in the lab. Once we were all seated in one corner of the lab, we gathered the sticks that hosted the Panellus stipticus. The lights were then turned off, and our eyes slowly adjusted to the dark. After a few minutes the Panellus stipticus was passed from person to person so we could see the light show (as shown in Brett’s photo above) close up. I must say this was a moving and mystical experience, one of the highlights of a glorious summer.
Afterwards, we went to the seminar room, where Richard played Taylor Lockwood’s tantalizing film, Spirits of the Forest, about his (Taylor’s) global search for as many species of bioluminescent mushrooms as he could find. It capped the perfect day.
You may find more about Taylor Lockwood, his film and his quest here.
The collecting continued the next day. Richard wrote to me to say that by the end of the workshop, 161 species had been identified. This is just shy of the record 165 species found in one of the 2014 workshops. Of the 161 species, 33 had not been found in any of the previous workshops.
I followed the participants out on Cow Island as they collected. Here, Karl is seen collecting two mushrooms for his basket. Ekky (short for Ekkehard) joined us to take a look. Their first guess, which proved to be correct, was that these were Boletus edulis, which is a great find (as this species is a choice edible).
As we left the trail, I took the above photo of a most impressive Northern Tooth Fungus, Climacodon septentrionalis. The Latin name translates as “Northern stair tooth”, alluding to the teeth on its underside, its staircase pattern of growth, and occurrence in the northern hemisphere. It forms massive (35 cm. high and 25 cm. wide is not unusual) clusters each year on wounds of standing hardwood trunks, especially maple.
We reached the Raleigh J. Robertson Biodiversity Centre in time for lunch, which included some especially tasty Oyster Mushrooms we had collected, along with several other species (Richard emailed to say that the class sampled five different species over the three days of the workshop). After lunch, I bid my adieus to Richard and his students. Thanks, Richard for an especially illuminating time. We will see you next Fall at QUBS!
Another fine summer day in August found me in the company of Grégory Bulté and his Ecology Field Course. Grégory is an instructor at Carleton University’s Biology Department, and according to the university’s website, he is:
“…broadly interested in the ecology, evolution and conservation of animals.”
What this does not tell you is that Grégory’s enthusiasm and knowledge about the life around Lake Opinicon and the wetlands bordering the lake, are boundless.
Officially the course is called “Field Ecology & Natural History” and this year was offered to 12 students during the last two weeks of August at QUBS.
Grégory, with his blue t-shirt in the foreground, here supervises the survey of some of the animals that live along the shores of Lake Opinicon, some rarely being seen at all. The purpose of this field study is to learn about the diversity of the lake and surrounding lands.
Turtles, fish, frogs and snakes are briefly captured, photographed, identified and then released. Lake Opinicon is home to some less common turtles, like the Northern Map Turtle (Graptemys geographica) and the Eastern Musk Turtle (Sternotherus odoratus). Note the excellent Latin species names, “geographica” and “odoratus”. They are both so descriptive of the animals. Map Turtles are named for the markings on their shells, which are reminiscent of the lines of a topographical map. Musk Turtles are also called Stinkpots, because they emit a stinky liquid from their musk glands when disturbed.
Below is a photo by your blogger of a very shy Musk Turtle taken at Lake Opinicon a few years ago. It is rare to see one out of the water. They do, on occasion, emerge onto a snag that angles out of the water, like this one, usually in an area that is well hidden. These are small turtles, usually less than 13 centimetres long. Map Turtles are among our larger turtles. Females in Lake Opinicon have measured up to 26.5 cms long and males up to half of that length. They are often seen basking on larger rocks in our rivers and lakes in Eastern Ontario.
Two of the many representatives of the Cyprinidae family (minnows and carp) in Lake Opinicon. Above is the Blackchin Shiner (Notropis heterodon) and below is the Golden Shiner (Notemigonus crysoleucas). The Blackchin Shiner is native to the Great Lakes‒St. Lawrence basin. It is a small fish, rarely exceeding 6 cms. The Golden Shiner may grow up to 30 cms., although most are in the size range pictured below. This popular bait fish is native to much of eastern and central North America and has been accidentally introduced well beyond its native range.
Frogs abound in and around the lake. The first two photos, above, feature a frog that rarely leaves the water, the American Bullfrog (Lithobates catesbeianus). Our largest frog in Ontario, the Bullfrog is very aggressive with other frogs—and anything else that moves! The third photo, above right, is a Green Frog (Lithobates clamitans). This is also a large, mostly aquatic frog, which is frequently mistaken for the Bullfrog. Note the clearly visible ridges running down the sides of this frog’s back. These ridges are distinguishing marks of the Green Frog. Below left is a photo of a Leopard Frog (Lithobates pipiens). Leopard Frogs travel far from the water during the summer months and return to overwinter in lakes and ponds. Below top centre is a Wood Frog (Lithobates sylvaticus), distinguished by facial side masks. Scrunched up on the Milkweed leaf, below right, is a Grey Tree Frog (Hyla versicolor), our loud summer frog. Its call is often mistaken for a bird. As the Latin name suggests, the Grey Tree Frog changes colour to match its surroundings for better camouflage. The Green Frog and Leopard Frog photos were taken by Art Goldsmith. The remaining four photos were taken by Grégory Bulté.
The other group of common, and usually hidden, amphibians is the salamander (above lower row). The three species above are best seen in early spring when spring melt waters and warm rains form ponds and pools where many salamanders breed in the evening hours. These salamanders spend most of their time dug into the soil or beneath rocks and fallen tree limbs in moist forests where they hunt for invertebrates. The three of Ontario’s 12 species shown here are, from left, Blue-spotted (Ambystoma laterale), Spotted (Ambystoma maculatum), and the lung-less Eastern Red-back (Plethodon cinereus). The latter is a member of the Plethodontidae family. The species in this family have no lungs, and therefore are restricted to moist, terrestrial habitats where they breed and lay their eggs. The other two Ontario members of this family are the Two-Lined and the Dusky Salamanders, neither of which have been recorded at QUBS.
Northern Water Snake 1
Northern Water Snake 2
For a slight change of focus, we look at a few reptiles. Above are two photos of a Northern Water Snake (Nerodia sipedon sipedon) that posed for students. This common reptile is found in and around ponds, lakes and rivers throughout the southeastern portion of Ontario. Below is a much rarer species, the Eastern or Grey Ratsnake (Pantherophis spiloides), an effective predator of rodents and other small animals. The large tracts of conservation lands protected by QUBS are vital to the Ratsnake’s survival as the population in the Rideau Lakes is threatened; whereas in southern Ontario, it is endangered.
Of course, the underpinnings of any functioning ecosystem are its wealth of native plants and fungi, both macroscopic and microscopic. Fungi make up a very large percentage of the Earth’s biomass. Then there are the invertebrates—the huge diversity of arthropods in Eastern Ontario, and the other invertebrate phyla—all forming the base of food and energy production for all of us vertebrates. The previous blog post featured the entomology field course and just a sample of the insects to be found in the area around QUBS. Here are a few more insects , other invertebrates and a small sample of the local plants.
Note that fungi will be the subject of my next post, Richard Aaron’s Fabulous Fall Fungi field course.
Widespread throughout North America and ecologically significant in our lakes, ponds and marshes, the Yellow Pond-lily (Nuphar lutea), pictured above left provides shelter, food and stabilization for many animals, including some of the aquatic invertebrates. To the right of the Pond-lily is a typical dragonfly (Order Odonata) nymph. The next photo is a freshwater crustacean (possibly the Waterlouse, a species of the genus Asellus, Order Isopoda). On the far right in this sequence of four photos, one of our Leech (Hirudinea) species is pictured. Healthy ponds and lakes are teeming with these and many other invertebrates, zooplankton and phytoplankton, which provide the basic food for all larger species.
We will explore in great detail the world of the fungi in our next post. I didn’t see this fungus (above) during the fungi course though. The Laetiporus sulphureus, which has a preference for Red Oak, has several common names, including Sulphur Shelf and Chicken-of-the-Woods.
Above, these are aquatic Leaf Beetles, Donacia sp., mating and another common aquatic invertebrate, a Damselfly nymph (Odonata).
We are not seeing as many of these on Milkweed as we have in the past. In a walk with two other naturalists recently, we thought it would be approrpiate to change the name of the Common Milkweed to Monarch Flower, to honour this plant which hosts the Monarch Butterfly caterpillar, like the one shown above.
Hay fields, as in the stunning photo above, are an excellent habitat to collect a wide diversity of insects and other Arthropods. Lastly, the Grégory Bulté Ecology Field Course class of 2015.
I spent quality time on two fine August days with THE Bugman of Ontario, Marvin Gunderman, an Entomology professor at McMaster University in Hamilton, Ontario. Each year, a maximum of 14 very fortunate students spend two weeks with Marvin and two very motivated co-instructors, one of whom is a very capable entomologist and photographer, while the other is a crop plant specialist.
The course is officially called “Field Entomology & Ecology“. Students receive a full Ontario Universities course credit for completing the course. For more information visit http://fieldentomology.com/.
After lunch on the first day, I found a Hickory Tussock Moth caterpillar (common at QUBS, but not in the upper Ottawa Valley, where I live).
Immediately, I showed the caterpillar to Dave, who identified it. Dave travels to QUBS from his job at the National Museum of Denmark, where he is the Collection Manager for Diptera (flies).
First thing in the morning, students gather around Marvin to take the long, long trek down the QUBS road to the first collecting site of the day, meadows and fields a-buzz with a diversity of insect life.
Tales in Horse Poop
We ecologists and naturalists are an easily distracted lot. We bring new meaning to the word “FOCUS”. Indeed, who could resist focusing on a very large Arachnid, which had decided to occupy equine waste. Certainly, Marvin could not resist. Nor could I. Marvin is seen below, fancy home-made diffuser and flash at the ready with super macro lens to take a photo to record the sighting. Initially identified as a “Nursery Web” spider, the evidence later pointed to one of many Wolf spiders (family Lycosidae), which are indeed close relatives of the Nursery Web spiders (family Pisauridae) and it does take a close inspection of the arrangement of the multiple eyes to sort out. Our largest Canadian spiders are members of these two families.
Fortunately, my own photo, below, does show the arrangement and decided the identification.
Inspired by this impressive Lycosidae, for comparative purposes I went onto the QUBS wharf to find the most commonly seen Pisauridae, the Dock or Wharf Spider, which has caused a few “starts” in many cottage vacationers in southern Canada. It took me seconds to find a half dozen, and another hour to get a decent photo of these shy creatures (below).
All students are required to bring cameras that are able to take macro photos (i.e., lenses which are able to get very close to a small object like an insect).
Above, Alex demonstrates the capture and preservation of an insect specimen. Students are required to create a collection of the most common insect orders, and to arrange and identify their specimens, as shown below. Pins are used to secure specimens onto Styrofoam.
Right, Skippers are common and diverse butterflies throughout North America. One of the most common Skippers that we see in late summer is the European Skipper (Thymelicus lineola), an exotic species from Europe that came to North America in the early part of the 20th century, when agriculture was planting a lot of Timothy grass (Phleum pretense), also from Europe. Until this summer, I often overlooked Skippers, assuming most were European. I found that many native Skippers still abound, such as the Crossline Skipper (Polites origenes). European Skippers are orange in colour. This Crossline Skipper is dull with a very faint pale band, clearly visible in this photo.
Above, one of the students was able to capture a newly emerged Cicada, the “warm-days-of-summer” buzzing True Bug, of the order Hemiptera. We have only one species in Eastern Ontario, the Dog Days Cicada, Neotibicen (Tibicen) canicularis.
And what else is in all of those jars the students used for collecting? Like the Diptera (the insect order that includes all of the flies, collectors will also find a lot of Coleopterans (the Beetles insect order). During late summer days in fields like the one in which we were collecting, there are many members of the Silphidae, Carrion Beetles, such as the one pictured below, feeding on insects. So far in North America, there are less than 50 species of Carrion Beetles described. Perhaps one of the budding entomologists on this course will describe many more in the future.
I was distracted by a very large spider (our SECOND spider distraction of the afternoon. See “Tales in Horse Poop” above for another scintillating story, which even Marvin could NOT resist). Female spiders are generally much larger than males. Therefore, I expect this is a female Shamrock Spider (Araneus trifolium), as it was just under an inch in length. Unlike the two spider families discussed under “horse poop”, which hide and surprise prey, this one is an orb weaver.
I took a break from the lab chemicals to visit the QUBS wharf, above. I was after the Wharf Spider, and I also was fortunate to see a common dragonfly of Eastern Ontario, the Black-shouldered Spinyleg (Dromogomphus spinosus), below.
Back on the trail, the intrepid class receives Marvin’s wisdom, above, before spreading out to capture insects in a very different habitat, the wetlands around Cow Island. Below, course instructor Jen, who annually takes leave in order to help Marvin deliver this course, briefly glances up before returning to her insect detective work.
Above left, enthusiasm abounds as students collect water insects, like the Water Scorpion (Genus Ranatra), a predatory insect, in the right-hand jar, above right.
Later that evening, Jen and Dave take a moment to pose for this awesome photo (above), after a job well done. Meanwhile, below, the incredibly handsome duo of Marvin Gunderman, and your blogger, Art Goldsmith, take a brief millisecond break from their very serious taxonomical deliberations. Note Marvin’s “insect” t-shirt and Art’s hand lens!
Constance Nozzolillo, BA Hon., MA Queen’s, PhD UOttawa Retired Professor of Biology, UOttawa
Life member of the Phytochemical Society of North America, emeritus and founding member of the Canadian Botanical Association and the Canadian Society of Plant Biologists, emeritus member of the Botanical Society of America and the American Society of Plant Biologists, member of Groupe Polyphenols
As the end of summer nears, the green leaves of our deciduous trees undergo a change in colour. Those of some become a brilliant red like the red maple while others change to a yellow or golden colour like the birch and all of them ultimately become a brown colour. Despite the economic importance to our tourist industry of the autumnal display of colour of the trees in our forests, relatively little scientific study has been made of this annual phenomenon. As a result, we are subjected in the newspapers and on websites to an imaginative description of the process too often only distantly based on established facts. Of a half dozen of the many websites turned up by a Google search of “autumn color”, not one explanation conforms entirely to the present incomplete state of knowledge. However, in the past two decades, ground-breaking work in the north-east USA and in northern Sweden has yielded a deeper understanding of the coordinated processes ongoing in the leaves as deciduous trees prepare for winter.
The reason for the autumnal change is variously attributed to lower light, cool temperatures, or various other environmental factors, although many descriptors have now grasped the fact that daylength is significant. In point of fact it is not the daylength itself that is important. The trees and shrubs recognize the increasing length of time between sunset and sunrise, i.e. the dark period, as the summer progresses and thus begin to make preparations for winter survival. They are able to do this because of an invisible blue-green pigment called phytochrome in their cells. This pigment serves as a timepiece, enabling the plant to ignore the suggestion of warm autumn days that summer may never end and to realize that ambient temperature is not a reliable marker of the seasons. Thus the process called leaf senescence is begun.
The colour change of the leaves is only one of many processes going on as the leaf senesces but it is the one most obvious to us. The green leaf of the maple and other trees contains several pigments in addition to phytochrome. Most visible are the green chlorophylls present in tiny intracellular structures called plastids. These pigments are the key to our survival on earth because of their ability to trap the energy of sunlight for food production by the leaf. Also present in the plastids but masked by the chlorophylls are several kinds of orange and yellow pigments called carotenoids, a name derived from the Latin name of the orange carrot root. Over the course of a few days or weeks, the green of chlorophyll disappears. The carotenoids also are destroyed but not so rapidly as the chlorophylls, thus the leaf becomes a yellow colour. They are yellow, not orange, because the xanthophylls, the yellow carotenoids, are three times more abundant than the carotenes , the orange carotenoids. At the same time, the leaves of some species begin to produce red-coloured pigments called anthocyanins. (These are the same pigments that are in the healthful blueberry and cranberry fruits we are encouraged to eat.) If nearly every cell of the leaf contains these pigments in high concentration, the leaf will be a brilliant red colour like those of the red maple, the carotenoids again masked from view. If the concentration is low, the leaf will appear orange like those of the sugar maple because we see the red of the anthocyanins mixed with the yellow of the carotenoids. Thus the orange colour seen in sugar maple leaves is not due to orange carotenoids as frequently stated, even in some botanical textbooks, but to the mixing of the primary red and yellow colours. Didn’t we all learn that as kids? Newly formed carotenoids do result in a red colouration in some species that retain their leaves in winter, red cedar being an example.
Since the above discusses the mixing of colours, at this time I will also point out that there are some tree leaves that produce anthocyanins all summer, a horticultural variety of Norway maple for example. It cannot be ignored that the leaves of these trees are very dark in colour, and certainly not a clear green. That is because nearly all the light passing through the leaf tissues is absorbed by the mixture of pigments thus yielding a very dark purplish or blackish colour.
How the annual disappearance of an amount estimated to be a billion tons of the green chlorophylls is brought about has been subjected to rigorous study only in the past three decades. Some popular reports state that chlorophyll is broken down and remade all summer long, that it is “used up” in the photosynthetic act. It is true that chlorophyll is easily broken as evidenced by the rapid bleaching of the leaves of an over-wintered houseplant abruptly put out into bright spring sunshine, but a leaf properly adjusted to bright light conditions does not bleach. One of the roles of the carotenoids is to protect the chlorophyll from such destruction. And of course, new chlorophyll must be made as new leaves are formed on the tree or to replace that damaged due to excessive light exposure, but the deliberate breakdown of chlorophyll in a senescing leaf seems to be a one-time event. It is now known to be a highly controlled, multi-step process associated with major changes in the structure of the plastids. An important result for the tree is the release of nitrogen, the most essential element for plant growth, from the proteins to which the chlorophylls had been attached. The removal of this nitrogen from the leaf for storage in the trunk or other parts of the tree before the leaf falls off is a significant activity. Results available to date demonstrate that trees vary considerably in their ability to do this. Some are able to remove as much as 80%, whereas others remove relatively little before the leaves fall. Surprisingly, the nitrogen bound into the chlorophyll molecule itself is not made available for transport and so remains in the fallen leaf.
And what is the purpose, if any, of synthesizing new complex chemical structures like the anthocyanins? Scientific study directed to answering this question has begun only in the past few decades and provides some evidence to indicate that the red pigmentation may protect the leaf from the damaging effects of light so that more of the valuable nitrogen and other nutrients can be transferred to the trunk. Another question frequently asked is “Won’t the process of anthocyanin synthesis require energy that the leaf will no longer have freely available because of the loss of chlorophyll?” Of course energy will be required both to make the anthocyanins and also to transport the nutrients but this energy can be provided by “burning” the residual sugars in the cells of the leaf in the tiny “furnaces” called mitochondria. These bodies provide the energy necessary for the activities of every living cell, plant or animal.
And how are the red pigments made? Contrary to statements frequently made in the past, these red pigments are not present in the leaf blade during the summer in the green leaf, although the leaf stalk may be red in some species, but are made anew in the autumn in those species equipped with the necessary genes. That fact is now recognized in most popular explanations. The answer usually provided to the “how” question, however, completely ignores the current state of knowledge of the process by stating that the sugars remaining in the leaf as a product of photosynthesis are converted into anthocyanins. This may sound reasonable especially since some sugars are incorporated into the final structure. However, innumerable studies over the past several decades have shown that building of the part of the anthocyanin molecule that is responsible for the red colour involves sugars only as a source of energy to drive the process. It occurs in the cytoplasm of the cell in a tightly coordinated multi-enzyme process, the final step of which is to add one or more sugars. Only then is the molecule so formed called an anthocyanin. It does not leave the cell in which it is formed but is deposited into the vacuole, a large sac filled with a slightly acidic watery solution that occupies most of the cell volume. The amounts of anthocyanins subsequently produced depend on many factors, including temperature, light exposure, and nutrient status. Scientific studies back up the observation that bright sunny days and chilly nights result in the best display of colour. A current “fashion” in popular explanations is to add that “chilly” cannot include sub-zero temperatures, but a touch of “jack frost” overnight does wonders to enhance the colouration of our hardy native species! It is true that freezing will kill the leaf cells but no one seems to have tested the frost hardiness of our maple leaves. If the weeds in our gardens can survive overnight temperatures of -1C or -2C with no ill effect, it seems logical that so can the leaves on a native tree. On the other hand, in warm weather, especially if the days are overcast, much of the chlorophyll remains and little of the red pigments is made. As any casual observer may note, more red colour is present in parts of the tree fully exposed to sunlight. It is important to keep in mind that a typical leaf is comprised of many individual cells each responding more or less independently to its environment. Although the overall process of preparing for winter is synchronized and ultimately leads to leaf fall, some cells may retain normal functioning much longer than others. Thus the colour of the leaves is not the same in all parts of the tree or even in all parts of the same leaf.
While all these colour changes are ongoing, the leaves are prepared for the phenomenon familiar to us as leaf fall. Preparation for separation from the tree is done so as not to leave an open wound at the point of attachment. An impermeable corky layer, called an abscission layer, is gradually built across the base of the leaf stalk. Such a layer is obviously incompatible with the already-mentioned desirability of removing as much as possible of the valuable nutrients in the leaf for storage in the trunk; how can nutrients be moved past an impermeable layer? The solution lies in the fact that the tissues through which the nutrients are moved, the vascular tissues which make up the veins of the leaf, are the last part of the leaf stalk to be cut off. The statement usually made in popular explanations is that the sugars (sucrose, the sugar we put in our coffee, is the form in which sugars are transported in the plant) are trapped in the leaf by this layer and are thus available for conversion to anthocyanins. But is it true that sugars are indeed trapped? How long into the autumn is water carried into the leaf? And how long does the part of the veins responsible for moving nutrients out of the leaf remain functional? All we know for certain is that finally the leaf is held onto the tree only by the veins which ultimately break off to allow it to float away. Its point of departure is marked by a characteristic leaf scar that can be used to identify the tree in winter, its smooth corky surface marred by the broken remnants of the vascular tissues.
And now we come to the matter of the final brown colour seen in the fallen leaves and also in leaves of some species that are still attached as in the white oak, for example. Again, explanation of the brown colour on websites is highly variable and mostly unrelated to the probable truth. There is no brown pigment already present in the tree leaves under discussion, or at least none that any phytochemist has isolated and reported on. The most likely cause of browning is the phenomenon familiar to anyone who has left a slice of apple or potato exposed to air. The exposed surface soon becomes brown because the tissues of apple and potato contain an abundance of colourless phenolic substances that are polymerized by enzymes to yield a brown shade. (There is now a genetically engineered variety of apple and another of potato that do not brown when cut, but will anti-GMO activists manage to prevent them from reaching the market? Personally, I hope not!)
Tree leaves also contain a complex mixture of phenolics, most of them formed at various steps of the same pathway that leads to anthocyanins as well as the enzymes noted above. Notable among them are two classes of vegetable tannins, condensed tannins, polymers of catechins whose synthesis branches off at a late stage of the pathway and hydrolysable tannins that are polymers of gallic acid combined with glucose. (The chemistry of these compounds is exceedingly complex but that has not prevented their use over countless centuries in the production of leather from animal skin!) Thus there are ample compounds available for the browning phenomenon to occur in senescing leaves.
Our trees must maintain the delicate balance of retaining normal functioning of the leaves for as long as possible consistent with making adequate preparations for winter! Beginning the process of leaf senescence too soon will rob the tree of the ability to make food during the warm days of autumn but, on the other hand, starting too late may result in an abrupt cessation of all metabolic activity due to a killing frost before the tree has time to recover nutrients from its leaves.
(unless otherwise credited, photos by Art Goldsmith, tree swallow photos by P-G Bentz )
Thanks to the following people for assisting with advice, content and research: Prof. Fran Bonier, Ph.D. candidate Catherine Dale, and Prof. Raleigh Robertson.
The Bird, The Research, The Sordid Truth: Do Tree Swallows Murder Nestlings and Cheat on Their Partners?
Yes, the daily tabloid newspapers are rife with sleazy debauchery, and so is this Blog, at least when it comes to Tree Swallows (Tachycineta bicolor) referred to by the abbreviation TRES. The story of the Tree Swallows at QUBS is integral to the development of the station by two remarkable leaders, Prof. Raleigh Robertson, who was Director of QUBS for 33 years, and Frank Phelan, who has managed the Station for 40 years, and who will be retiring at the end of 2015. Their story, which is also the saga of a small research station on the shores of Lake Opinicon morphing into a primary and pre-eminent 8500-acre regional research, education and conservation centre, deserves a separate post.
Back in 1974, Prof. Robertson had been continuing his studies of Red-winged Blackbirds (RWBL ) when, and this story is worthy of a movie script, the potential acquisition of 1000 acres (Hughson Farm) at the south end of Lake Opinicon prompted some thought about other studies. Coincidentally, Geoff Holroyd came to Queen’s from Long Point Bird Observatory (LPBO) with a number of nest boxes. As with so many human advances, the interplay of events prompted invention and the TRES studies commenced. Having already conducted RWBL habitat selection studies, Prof. Robertson decided to use the newly acquired nest boxes to study habitat selection of TRES on the Hughson property (in the illustration below by Dr. Raleigh Robertson, the Hughson tract is shown in green). The original pre-1974 QUBS is shown in light blue. The additional tracts, up to the year 2007, are shown in various other colours. The illustration shows several Tree Swallow photos, including a natural tree cavity nest and a nest box.
The following four paragraphs are paraphrased from personal communications with Prof. Bonier:
North American Breeding Bird Survey (BBS) data since the mid 1980s shows declining populations of aerial insectivorous birds, particularly in northeastern North America (Shutler et al).
Update: Prof. Bonier has informed me (November 9, 2015) that a new study (science is always progressing!) indicates this geographic pattern for aerial insectivores is not as strong as the Shutler team thought. The exception is Tree Swallows, which are, indeed, increasing or stable outside of northeastern North America.
Tree Swallows are aerial insectivores, and therefore, the network of TRES nest boxes afforded an opportunity to study the population at QUBS. Several hypotheses have been put forward regarding the drops in populations. I have spoken to people (at QUBS and elsewhere) who believe greater survival of parasites may be responsible. This is one of the disease parameters that Prof. Bonier mentioned in her communication with me. Prof. Bonier has determined that malaria parasites have not increased in Tree Swallows over time. Other parasites may have an effect on populations. Other climate-linked hypotheses include phenological changes, especially earlier life cycling of important insect prey.
Prof. Bonier inherited the QUBS TRES boxes from Prof. Robertson, and she ran studies on them since 2007. She compiled all of the demographic data on the population (from 1975 to present) and has used the data to test a couple of hypotheses about proximate causes of the population’s decline. The story seems to be this: the population has been declining fairly rapidly and steadily since ~1990, when it was at its peak (with every single box occupied by a breeding pair). The all time low of 23% box occupancy was last year (2014). That’s an even lower occupancy than 1975 when Prof. Robertson first put up about 70 boxes to start the population (and occupancy was 26%). This year, 2015, occupancy rebounded a bit to 35%. From this amazing data set, we can show that on average, per nest fledging success has not changed over time, nor have adult return rates (a proxy of adult survival). However, first-time breeders are coming into the population at a lower rate. This is true for immigrants into the population as well as resident nestlings returning. At its peak, 10% of all nestlings that hatched in boxes at QUBS in a given year returned later as breeders. Now there are rarely any coming back. So this would suggest that something is happening to dispersal and/or survival during the first year of life, between hatching and first breeding. Prof. Bonier and her colleagues are pursuing analyses on climate and disease to explore possible causes of this change, which might help us differentiate the two.
The population at QUBS started its decline in 1990’s. Significant climate change has been documented in our region from 1980 onward. That causes me to lean to that predominant factor as a major contributor to the drop in our local populations. The research also tells us that TRES are also expanding their range in the southeast, at the same time as return rates drop here. This raises even more questions. Climate change tends to be more pronounced from south to north. An expansion of the range to the south is interesting since it causes me to wonder why these birds have not occupied the southeast in the past, and what has changed to cause them to expand in the south now? More nesting opportunities? Less competition?
The conclusion of the Shutler (citation follows at the end of the TRES portion of this blog post) paper to which Prof. Bonier and Prof. Robertson contributed:
“The broad geographic patterns are consistent with a hypothesis of widespread changes in climate on wintering, migratory, or breeding areas that in turn may differentially affect populations of aerial insects, but other explanations are possible. It is also unclear whether these changes in occupancy rates reflect an increase or decrease in overall populations of Tree Swallows. Regardless, important conservation steps will be to unravel causes of changing populations of aerial insectivores in North America.”
Prof. Bonier also has links to the Virginia Tech people doing research in that part of the U.S. (probable increasing population southward). They have found that TRES displace Bluebirds at nest boxes. Prof. Bonier wrote:
“TRES in the northeast of North America are declining, whereas other locations are stable or increasing. We are studying TRES with collaborators Ignacio Moore (Virginia Tech) and Mark Stanback at Davidson College in North Carolina, where they have been displacing eastern bluebirds from his study site. TRES never used to breed there, and now are abundant and occupy almost all of his nest boxes. Ignacio put up nest boxes near the Virginia Tech campus last fall, and already has higher box occupancy than we have at QUBS. So in the southeast, it does seem that TRES are increasing and also expanding southward.”
For more about Prof. Bonier’s current research, see the news article posted on the Virginia Tech web site.
Thanks to Prof. Robertson’s long term research, we have learned a lot about the mating and nesting behaviour of Tree Swallows, and their selection of nesting sites.
Left, a male Tree Swallow stands guard while a first-year breeding female brings nesting material to one of the nest boxes at QUBS. Professor Robertson studied the unusual “late onset of adult plumage” in Tree Swallow females. Among the many interesting traits of these birds, the delayed adult female plumage characteristic is very unusual in the bird world. Delayed adult plumage is common among adult males of many bird species. Male TRES are fully iridescent blue by their second year. Females only attain such “blueness” later in their 2nd year. Why would this be?
It is this kind of observation and hypothesis development that characterizes good science.
So using a variety of methods, Prof. Robertson and colleagues went about testing their hypotheses regarding the late plumage onset of TRES females. And this is what they found.
When a one-year-old female TRES arrives at a nest box inhabited by a nesting pair, the resident male is less aggressive towards a one-year-old female than toward older intruders. The female is equally aggressive toward all females. Isn’t THAT special? It turns out these young, less brightly feathered females are, indeed, LOOKING for breeding opportunities, as they visit many nests to seek out a tryst with a resident male. And many males respond quite positively. Note that these visits last only a few seconds. Birds are quicker than people! Another interesting result: older females are much more successful at raising young early in the season. Later in the season, the younger females, which were experimenting at a lot of different nest boxes earlier are, later in the season, breeding much more than their older counterparts AND they are being just as successful.
This is a later vintage QUBS nest box, with the effective anti-rodent device pictured below the box. Its location beside the road into the QUBS buildings is not particularly suitable for TRES, which prefer the nest boxes in open hay fields, but are occasionally occupied by House Wrens and Black-capped Chickadees. Raccoon, snakes, and squirrels are among the most prevalent and successful predators of songbird nests. Next time you are thinking about how cute squirrels are, recall this fact! Larger snakes are the only predator capable of circumventing these collars.
A vigilant adult Tree Swallow is pictured above. After reading through this blog, I expect people will wonder more about what goes on in birds’ brains as they look at us. Perhaps some of these surprising revelations will prompt some to wonder all the more.
Sex and Infanticide: Tree Swallows, the Sordid Side
People look on small songbirds as benign, benevolent and harmless. Evidence abounds for these traits. Although, in my opinion, the following evidence doesn’t change an overall positive image, it does give one pause. Your blogger has observed the sweetest of birds, the Black-capped Chickadee joyfully feeding at a deer carcass in mid winter. During a winter snowshoe sojourn, a Red-breasted Nuthatch flew onto my shoulder demanding FOOD, and gave me a most malevolent look when the lack of bird seed was apparent. And, given an opportunity, male Tree Swallows will massacre a previous male’s offspring in order to start its own brood.
Prof. Robertson studied this behaviour by removing males from nest boxes. Sexually selected infanticide is quite rare in birds. It is more common in mammals. So seeing this behaviour in TRES is of great interest to ornithologists. During incubation, with eggs in the nest, Prof. Robertson removed 17 males. In three cases, the males were not replaced. However, a large proportion of the males, 11, killed the nestlings when they hatched. Three others adopted the newly hatched nestlings.
If the new male is introduced during egg-laying, (Robertson removed 11 in this instance), 4 were not replaced and all of the other 7 replacement males did adopt the eggs and nestlings. Finally, the same experiment was completed during the nestling stage (15 males removed), and five of the fifteen killed the nestlings. Of these 5, only 1 re-nested with the widowed female; two re-nested with a new female and two did not re-nest. So why would so many kill the newly hatched nestlings? Researchers studying with Prof. Robertson found that the behaviour is adaptive. That is, there is an advantage to those males who kill the previous male’s offspring, as they disproportionately pass on their genes. This raises more questions, which future Queen’s students may answer using the unequaled resources at QUBS.
Above and below: copulating Tree Swallows. You don’t have much time to see this happen, as the usual copulation event lasts just a few seconds!
Below, the happy couple look innocently toward the camera. The question is, is that the resident female for this nest box? It may not be … read on.
What about the secret mating among TRES, that is, one of a mated pair sneaking off to pair with another TRES, and, as already discussed, the young females with their juvenile plumage, visiting males in nest boxes? The facts are surprising. The euphemistic ornithological expression is “extra-pair” mating and paternity. Based on observations, it appeared that TRES are models of social monogamy. Hold on! That is another fun feature of good science. What appears to be happening based on observation may conflict with the facts. A good detective follows the evidence. And the evidence is:
80% of nests contain some extra-pair offspring!
50% of all nestlings are sired by extra-pair males!
So seeing ISN’T believing. There is a lot of “visiting” going on, and it happens quickly and surreptitiously…so much so that trained observers don’t see it.
Seeing this result from a MALE perspective, the benefits are obvious: the male has more offspring spread over more nests, making survival more likely (literally male Tree Swallows have their eggs in more than one basket!).
What does the female get? She still has her nestlings all in one basket, and she still gets the same contribution to care by one male. Once again, the facts are both interesting and unexpected. It is the FEMALES that control extra-pair copulation. They are the ones who stray.
After some very intensive study and some very difficult analysis, research has concluded that the female, as well as the overall population, does receive an important benefit. These pairings result in better genetic compatibility, not in overall better genes. Genetic compatibility (i.e. simply the genes from each partner vary in how well they work together. Some genes pair up for greater benefits. The more pairings, the greater likelihood of compatible pairings) is an adaptive advantage.
How Tree Swallows Select Nest Location
In the photo series below, Tree Swallows are photographed at various natural tree cavity nest locations. As you would expect, forestry, farming and other land uses have limited and reduced the numbers of tree swallow nests. Natural cavities produced by wood peckers, disease or physical damage must be, ideally, close to water or open fields, so Tree Swallows have a ready source of food, such as insects emerging from water and fields. Artificial boxes do help alleviate this limiting factor.
Tree Swallows, outside of nesting season, are very social. They form large flocks for migration and over-wintering. The author has seen flocks of thousands over bays in Florida. That changes when they nest. They like some space between nests.
On average, artificial nest boxes are larger, roomier and safer than natural cavities. However, whether a natural cavity or nest box is selected, TRES like their nests to be spaced an average of 28 meters apart. Researchers at QUBS determined this optimal distance through a spiral alignment of boxes in a field.. The second birds to arrive to nest usually choose the most distant nest box form the first pair. After a few weeks, nest selection becomes more random, but males do defend their nests aggressively from other TRES males. QUBS nest boxes are now set up in a grid pattern in optimum habitats. This territorial behaviour differentiates Tree Swallow from other swallow species which are more colonial.
Current research on TRES is focused on applied ecology, especially ecotoxicology. Professor Fran Bonier, who contributed greatly to this blog, is studying how Tree Swallows adapt to environmental stresses, for example through endocrinology field studies. See her current Queen’s web page for more information.
Spatiotemporal Patterns in Nest Box Occupancy by Tree Swallows Across North America, Avian Conservation and Ecology 7(1): 3., D. Shutler et al, 2012.
Field Ornithology-Agent for Science, Education and Conservation, presentation to the Society of Canadian Ornithologists Annual Meeting, Dr. Raleigh Robertson, September, 2007.
Personal Communication, Dr. Frances Bonier
Personal Communication, Dr. Raleigh Robertson
Personal Communication, Catherine Dale
I want to leave you with a few images of the Queen’s University Biological Station:
Your blogger, Art Goldsmith, with Professor Raleigh Robertson, left. The new Jack Hambleton Library (officially opened in June) is at the upper right. The building also now houses the Fowler Herbarium in state-of-the-art facilities. We believe this is the only field station with on-site access to such a large herbarium collection. Below, the large central QUBS building, with a cafeteria, labs, offices and a large seminar room, is named for Professor Robertson.
Photos, books, and artifacts belonging to Jack Hambleton are displayed in the new library named for Hambleton.
Next time, we will start our series of field course blogs. This includes the courses on Insects, Aquatic Ecology (a different course from the China-Canada Course), and Fabulous Fall Fungi. See you then.
We have gained many ecological and evolutionary insights from studying variation in DNA markers, from resolving the very base of the tree of life (genealogical affinities of bacteria, archaebacteria/extremophiles, eukaryotes), through overturning received truths about mating systems of birds (most are not in fact genetically monogamous), to quantifying impacts of human activities on connectivity of populations of species of conservation concern. Among the many revelations that come from such DNA studies are those from phenotypically cryptic taxa whose appearances often mask deep phyletic diversity. Indeed an increasing number of studies shows that myriad, traditionally-regarded ‘species’ are in fact complexes of separate, reproductively-isolated species. DNA studies have revealed such cryptic species in many groups, including mammals (Ceballosa & Ehrlich. 2009), birds (e.g. Lohman et al. 2010), amphibians (e.g. Elmer et al. 2007), and insects (e.g. Hebert et al. 2004). Many examples of cryptic diversity come from the tropics, but here are also some intriguing examples from higher latitudes like ours, with implications not only for understanding of evolutionary affinities of taxa in question, but also for their geographical distributions and the forces that have shaped them.
The trilling chorus frogs (a distinct lineage or clade within the treefrog genus Pseudacris) comprise one such group. This clade, distributed broadly across eastern North America, includes at least nine species: the mountain chorus frog (P. brachyphona), Brimley’s chorus frog (P. brimleyi), spotted chorus frog (P. clarkia), Cajun chorus frog (P. fouquettei), New Jersey chorus frog (P. kalmi), upland chorus frog (P. feriarum), southern chorus frog (P. nigrita), boreal chorus frog (P. maculata) and western chorus frog (P. triserieta) (Moriarty & Cannatella 2004).
Two of these species occur in Ontario, P. maculata and P. triserieta. The two are very similar in appearance – both are small (generally < 3.5 cms in snout-vent length), with smooth skin, and a dorsum varying in colour from brown to greenish-gray, and a dark stripe through the eye and longitudinal markings on the dorsum. The calls too are very similar being comprised of a trill that is often likened to running one’s fingers along a plastic comb. The boreal chorus frog was until recently considered to be distributed from northwestern Ontario to Alberta and north to the NWT, also being found in the USA in the Midwest south to Arizona and New Mexico. The western chorus frog was thought to range from southern Quebec and Ontario/northern New York state west to South Dakota, and south to the states of Kansas and Oklahoma (Harding 1997). In southern Ontario until recently there were considered to be two regional populations of P. triserieta: a “Carolinian population” found south and west of Toronto, and a Great Lakes–St. Lawrence population found east and north of Toronto, with the latter considered as ‘Threatened’ under the Canadian Species at Risk Act.
That’s the old view. Mitochondrial DNA evidence suggests that the Great Lakes–St. Lawrence population which was classified as P. triserieta is not in fact western chorus frog at all, but rather is a disjunct population of boreal chorus frog (Lemmon et al. 2007a,b, Rogic et al. 2015). Playbacks by Rogic et al. (2015) seem to affirm this, with eastern Ontario and western Quebec chorus frogs responding to previously recorded calls of P. maculata and not P. triserieta.
All of this has interesting implications for 1. Conservation (Is this western boreal chorus frog population genetically distinct and thus does it merit conservation priority?), 2. Biogeography (How did the species become disjunct and what paths of re-colonization did these distinct populations use?), and 3. Understanding the nature of species (these trilling chorus frogs are cryptic to us, but clearly they can tell each other apart – it is in the domain of mate recognition system and acoustics that the species differences are clear). As always there’s lots more work that can be done, not least of which is more finely mapping genetic diversity across the entire boreal chorus frog distribution.
Ceballosa, G. & P.R. Ehrlich. 2009. Discoveries of new mammal species and their implications for conservation and ecosystem services. Proc. Natl. Acad. Sci. USA 106: 3841–3846.
Elmer, K.R., J.A. Davila & S.C. Lougheed. 2007. Cryptic diversity, deep divergence, and Pleistocene expansion in an upper Amazonian frog, Eleutherodactylus ockendeni. BMC Evol. Biol. 2007, 7:247.
Harding, J. 1997. Amphibians and Reptiles of the Great Lakes Region. Univ. Michigan Press. Ann Arbor, MI.
Hebert, P.D.N., E.H. Penton, J.M. Burns, D.H. Janzen & W. Hallwachs. 2004. Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc. Natl. Acad. Sci. USA 101: 14812–14817.
Lemmon, E.M., A.R. Lemmon, J.T. Collins, J.A. Lee-Yaw & D.C. Cannatella. 2007a. Phylogeny-based delimitation of species boundaries and contact zones in the trilling chorus frogs (Pseudacris). Mol. Phylogenet. Evol. 44:1068–1082.
Lemmon, E.M., A.R. Lemmon & D. C. Cannatella. 2007b. Geological and climatic forces driving speciation in the continental distributed trilling chorus frogs (Pseudacris). Evolution 61: 2086–2103.
Lohman, D.J., K.K. Ingram, D.M. Prawiradilaga, K.Winker, F.H. Sheldon, R.G. Moyle, P.K.L. Ng, P.S. Ong, L.K. Wang, T.M. Braile, D. Astuti & R. Meier. 2010. Cryptic genetic diversity in “widespread” Southeast Asian bird species suggests that Philippine avian endemism is gravely underestimated. Biol. Conserv. 143: 1885-1890.
Moriarty, E.C. and D.C. Cannatella. 2004. Phylogenetic relationships of the North American chorus frogs (Pseudacris: Hylidae). Mol. Phylogenet. Evol. 30: 409–420
Rogic, A., N. Tessier, S. Noël, A. Gendron, A. Branchaud & F0J. Lapointe. 2015. A “trilling” case of mistaken identity: Call playbacks and mitochondrial DNA identify chorus frogs in Southern Québec (Canada) as Pseudacris maculata and not P. triseriata. Herp. Rev. 46: 1-7.