6.1 Introduction

Picture a vertebrate in your head. What do you see? Do you see brightly colored feathers? Glistening fur? Smooth scales? Almost everything you see, covering the external surfaces of that animal, is a part of the integument. The integument is not just the skin but everything found within and derived from the skin. This includes all those structures you probably envisioned: feathers, scales, and hair. It even includes structures like talons, nails, claws, and antlers (Figure 6.1). The integument serves many functions in vertebrates, and while they share a common overall makeup, even tiny changes in structure have implications for the various functions of the integument.

The integument serves many functions, as we will discover in this chapter. However, the primary function of the integument is to isolate the organism from its external environment. Isolation occurs at multiple levels in our case. For example, shells and scales serve as armor, protecting an individual from the teeth and jaws of a potential predator. Thick layers of an epidermis full of keratin (like yours) help keep out infectious microbes and parasites. Keratin, acting with a class of molecules called glycolipids, helps prevent the loss of water from cells. Without the integument, predation, infection, and dehydration are just three of a host of problems that an organism would face. We will see that the basic structure of the integument is well suited to this task and is structured consistently across the groups of vertebrates. Our generalized structure in place, we see how changes in the structure of the integument allow for the many secondary functions to occur and are modified in individual groups. In addition, unlike many of the other systems discussed in this textbook, the integument is full of structures that provide for a plethora of different functions, many of which have been modified from their original function to best suit the current needs of that species/group. Hair, for example, is thought to have evolved originally in mammals for the purposes of thermoregulation. As we look across mammals, we can find examples of hair performing a multitude of tasks: Whiskers (vibrissae) are incredibly sensitive touch organs. The quills of porcupines are effective deterrents to predators. The stripes of a tiger allow it to disappear in tall grass. These are but a few examples of how modified structures of and within the integument contribute to the overall biology of vertebrates.

6.2 General Structure of the Integument

Across the vertebrates, we will find that the integument has the same basic components/layers, and it is the variation within the layers that allows for the diversity of functions we observe. The three major layers of the integument are the epidermis, dermis, and hypodermis. Note that the root of all these layers is “dermis,” which originates from the Greek “derma,” conveniently referring to skin and/or leather. We can think of the dermis as the base of the integument. Above that, closer to the surface/external environment (i.e., superficially), is the epidermis. Below that, deep to the dermis, is the hypodermis. Figure 6.2 illustrates these three layers as they are structured in the human. Broadly, these layers will look similar across the vertebrates. However, it is the thickness of these layers, and what they contain, that will provide insight into each group’s environment, ecology, and evolutionary history.

The epidermis is the topmost layer of the integument and is by definition the layer that separates the organism from its environment. As such, we will see that many of the adaptations that help an organism interact with its environment are contained within the epidermis. We will also see that the epidermis varies greatly in thickness and constituency across our groups. The epidermis is primarily epithelial tissue, of a type we refer to as stratified squamous epithelium. “Squamous” tells us that the cells are often flattened, and “stratified” tells us that there are many layers to this tissue. In many vertebrates, particularly our terrestrial vertebrates, the layers of the epidermis closest to the environment are dead and serve only as a physical barrier to the outside world. Figure 6.2 is a close-up of a piece of the human epidermis. The structures beginning with “stratum” are the individual layers of the epidermis. The stratum basale links the epidermis to the underlying dermis via a basement membrane, a characteristic of most epithelial tissues and where many cells are rapidly dividing. The stratum spinosum consists of cells that are rapidly undergoing mitosis, diving and pushing the layers above closer to the surface. At the level of stratum germinativum (granulosum, in humans), the differences between our terrestrial and aquatic vertebrates start to become obvious. In this layer, cells we ultimately call keratinocytes begin producing keratin within themselves. Keratin is an important constituent of the integument. In addition to being within the epidermis, keratin is the biggest component of hair, claws, and many of the derivatives of the integument. When a snake “sheds” its skin, it is actually multiple layers of keratin that are being replaced. Your fingernails and the scutes of a turtle shell are also keratin, albeit slightly different versions of keratin. It is the bird’s beak and simultaneously the feathers. Keratin is a key component of the integument. As cells move closer to the surface, more and more keratin is produced, becoming the major component of the cell. At the outermost region of the stratum germinativum, the cells have died, leaving only some organelles, the cell membrane, and the accumulated keratin. Above this point, there are no living cells in the epidermis, only layers of keratin linked together by glycolipids, the same molecules mentioned earlier. This is the stratum corneum, named for the remaining keratin. Within the epidermis, there are structures passing through from the dermis (see the hair follicle in Figure 6.2), but there are also structures unique to the epidermis.

In most vertebrates, the epithelial tissue is dominant within the epidermis, and there are few other cell or tissue types found. Connective tissue adheres the bottom layers of the epidermis to the dermis, and there is no skeletal muscle. Capillaries of the cardiovascular system do not extend into the epidermis, only reaching the upper layers of the dermis. There are a few types of cells and tissues that do extend into the epidermis, and their importance should not be understated. Some we will leave for other chapters, but it is worth noting their role within the integument. Sensory receptors abound in the integument, and many are rooted in the epidermis or run through the epidermis. Pressure and touch receptors, temperature receptors, the lateral line of fishes, and electroreceptors all are integrated into the epidermis. Most of the specialized receptors, like the lateral line and electroreceptors, may be found deep in the epidermis/dermis, with an opening in the epidermis that allows for interaction with the environment. The touch and pressure receptors are embedded within the epidermis, at the levels of the stratum basale and germinativum. Chapter 20 on the special senses will expand on these receptors in more detail. In addition to the sensory receptors, the epidermis is home to structures that give the integument its color. Structures like chromatophores, melanocytes, and other pigment-producing cells are found in the epidermis. Some of these elements are structural. As light passes through a structure, it can be reflected or refracted, which we (and other animals) interpret as a color. Blue is the most common structural color, while others such as reds, greens, and yellows are the products of the pigment-producing cells. As the integument is the first level of defense against outside pathogens and disease, it should not come as a surprise that cells of the immune system may be found in the epidermis as well. Specialized macrophages move through the epidermis and dermis.

The dermis can be found deep to the epidermis. In most vertebrates, the dermis is the larger of the two layers. The dermis can be composed of many different types of tissue, including representatives from the circulatory and nervous systems. In certain vertebrates, smooth muscle may also be present in the dermis to interact with hair, feathers, or glands. The major component of the dermis is connective tissue, which provides strength and flexibility to the integument. The most abundant component of that connective tissue is a molecule known as collagen. Collagen is a protein, the most common protein in the animal body. Collagen is a key component of the dermis, but it is also similarly important in bones, tendons, ligaments, joints, and many other places. The arrangement of collagen in the dermis is almost as important as the amount. Collagen is strong, but only strong in the direction of its fibers. To resist forces in multiple directions, the collagen must be found in multiple directions. We see this most obviously in the fishes. Collagen fibers are bundled together and wound around the body in a cross-helical fashion (Figure 6.3).

This gives the dermis strength and some flexibility to deal with all the bending that occurs in the body. How well suited is this arrangement? The passive stretching and relaxing of collagen in the dermis allows a dead fish to swim! There are other types of connective tissue found throughout the dermis; all help in anchoring the epidermis to the dermis and the dermis to the hypodermis, and all provide a combination of flexibility and strength that is unique to the integument.

The hypodermis sits below the dermis (Figure 6.2) and primarily anchors the dermis to the underlying tissue. In many organisms, this collection of connective tissue, blood vessels, and nerves is where we would meet the other systems of the body, such as the major nerves of the peripheral nervous system, the skeletal muscles, and the major arteries and veins. Absent are many of the elements of the sensory system that we would have seen in both the epidermis and dermis. We will not spend a considerable amount of time on the hypodermis in this chapter, except in the cases where it provides us a better understanding of an organism’s biology (the blubber in marine mammals, for example). In fact, this layer is crucial for human and veterinary medicine. Hypodermic needles are used to inject medication into this layer of the integument, where it can be taken up into the larger blood vessels for faster transportation around the body.

In our brief discussion of the general layers of the integument, we neglected to introduce some of the derivatives mentioned in the introduction, including antlers, claws, and so on. That is because these elements are not restricted to a single layer. Instead, these elements often arise from the interactions of the layers, typically the epidermis and dermis. Many of these will protrude from the integument (nails, claws, feathers), while some may reach through and empty their contents onto a layer (sweat glands, mucus glands). There are some notable structures arising from the integument that we should discuss now, as they have a drastic impact on the evolutionary history of vertebrates, while others will naturally come up as we work through the diversity of vertebrates and their integument.

Arguably, the most important element that arises from the integument is dermal bone. While not a feature you see frequently, dermal bone has played an outsized role in vertebrate evolution. Dermal bone is exactly what it sounds like, bone that arises from the dermal layer of the integument. Dermal bone arises in sheets via a process known as intramembranous ossification (discussed in more detail in Chapter 7—Bone and Cartilage). Because it develops in between these layers, dermal bone is often flat or has a slight curve to it. Dermal bone will make appearances in this chapter as well as the skull chapter (Chapter 8). The evolution of dermal bone was important for the fossil fishes and remains important for reptiles and mammals.

6.3 Development

While it is easy to assume that all of the integument is derived from ectoderm, the reality is more complex than that. Only the epidermis itself is derived from purely ectoderm, while the specialized cells and tissues found throughout the integument have different developmental origins. Like many other connective tissues, the dermis and hypodermis are primarily mesoderm, and it is their interactions with the ectodermal cells that help produce the underlying structures. All the glands embedded in the integument are derived from ectoderm. Blood vessels in the dermis are derived from mesoderm.

After gastrulation, that very early stage in development, something takes place that is relevant to the integument. The ectoderm, which will eventually become the epidermis, folds over a part of itself, forming the neural tube (neurulation). While the neural tube will eventually become the spinal cord and brain, there are other cells cast off at this stage that have widespread impact. These cells, which are derived from the interaction of the ectoderm and the neural plate (what folds to become the neural tube), are known as neural crest cells. Neural crest cells can be classified as mesenchymal cells, as they are extremely mobile and will migrate throughout the body. Neural crest cells will play a key role in many parts of the body: nerves for the integument and digestive tract, cartilage and bone development of the face, and regions of smooth muscle. Neural crest cells in the integument, in addition to some of the nervous system structure, become the smooth cells that move hair as well as melanocytes that provide coloration and UV protection.

6.4 Evolution of the Integument—a Phylogenetic Approach

As we explore the major groups of vertebrates, we will highlight structures unique to that group, what their function is, and how it relates to overall evolution and functional biology of that group. Remember that the ultimate purpose of the integument is to isolate the body from the external environment and protect the body from microscopic pathogens to large predators.

Hagfishes and Lampreys

While often neglected in discussions of vertebrate evolution, structure, and function, hagfishes and lampreys are considered to be highly modified representatives of the ancestral vertebrates. Hagfish skin is remarkably variable across species and is truly distinct from other vertebrates. Rather than muck about in the details of all the different varieties of hagfish integument, we will instead focus on two key elements of the skin that are important to the whole group. The first is that hagfish skin is only loosely connected to the underlying tissue. The dermis of the hagfish is separated from the hypodermis by a series of blood sinuses and only has a tight connection to the hypodermis at its basal membrane. In effect, the skin can move freely relative to the underlying body structures. The function of this adaptation is still unclear. Several researchers have attributed the hagfish’s unique ability to tie itself into knots to the loose skin, while others have suggested that it makes it very difficult for predators—for example, sharks—to securely bite and grasp the hagfish, as the skin slips loosely under their teeth. The other element of the hagfish integument worth exploring is their famous slime glands. Hagfish skin is full of glands with a special type of cell known as a thread cell. Thread cells produce a complex fiber, which reacts with water. The reaction is immediate, and hagfishes are able to produce an impressive volume of slime (Video 01). The purpose of this slime is obvious. Secreted in response to disturbance or harassment, the slime quickly fills the space around the hagfish, absorbing water rapidly. Any potential predator receives a mouthful of slime for its trouble.

Lamprey integument follows the generalized pattern of all vertebrate integuments. While not as remarkable as the hagfish, there are some elements to the lamprey that are worth noting. The first is that lampreys have a very large epidermis, larger than that of the dermis. This is worth noting because in other fishes, the opposite is the case. The second is that we start to see specialized glands embedded in the epidermis. These glands consist of singular cells, secretory granular cells, whose purpose is to produce mucus. Not quite the same thing as the thread cells in hagfishes, these granular cells cover the entirety of the epidermis in mucus. Mucus is extremely important to the integument in most fishes (in addition to many other systems in the body). Mucus helps reduce friction between a swimming fish and its watery environment. It can also trap and prevent infectious pathogens from crossing from the environment into the body. For the lamprey (and other fishes) the mucus helps the isolating function of the integument.

Ancestral Fishes

It is important to highlight a few groups of ancestral fishes to help our understanding of the evolution of the integument. This is because unlike other fossil vertebrates, where the skeleton is what was fossilized, in these groups it is the dermal bone that remains. The phylogenetic relationships of these groups to our extant species are a bit fishy, and so we will treat them as a separate entity to understand how the integument played a large role in the evolution of the vertebrates.

Placoderms are the most famous of these ancestral fishes. Their name comes from Greek, meaning “plate-skinned,” and they lived from the Silurian to the late Devonian (about 440 to 360 MYA). Placoderms not only had dermal bone but had no other type of bone throughout their body. Like in many of the other groups of ancestral fishes alive at this time, this dermal bone served as armor around the head region. This armor was also a key element to their jaws, and we currently consider the placoderms to be among the first jawed fishes. The dermal armor surrounded just about every available surface on the head of our placoderms, in species big and small. The largest known placoderms, the genus Dunkleosteus, have some well-preserved specimens that show the extent of the dermal bone (Figure 6.4). This dermal bone embedded in the integument serves as both armor and a feeding apparatus and appeared many millions of years prior to the evolution of bone as an internal skeletal feature. In fact, dermal armor appears in the evolutionary record before jaws do in many ancestral fishes, where the dermal bony armor is quite apparent but the jaws are clearly missing. These include such fascinating groups as the ostracoderms (a paraphyletic group of jawless fishes) and the Pteraspidomorphi (“wing-formed”), heavily armored jawless fishes that are currently considered to be the closest known relatives to the jawed fishes.

Chondrichthyes

The Chondrichthyes—sharks, rays, and chimeras—will serve as our first real introduction to vertebrate integument. An epidermis and dermis are present, with a strong anchoring to the hypodermis. The collagen fibers in the dermis are wound cross-helically across the body, which provides elastic energy back to a shark when it swims, through the stretching and relaxing of the collagen. The epidermis of sharks and rays is extremely thin—many times thinner than the dermis. There are few glands in the integument, but there are two key sensory structures that are embedded in the integument. On the rostrum of sharks, rays, and chimeras are a multitude of small pores. These small pores are part of the electroreceptive apparatus of chondrichthyans. Chondrichthyans can detect the electrical fields generated by muscle contractions of other animals in the water through small jelly-filled pores (see Chapter 20). These pores open through the epidermis. The receptors themselves are found below the dermis. Similarly, along the sides of sharks (and other fish), we find the openings to the lateral line, a special type of mechanical receptor that also has openings in the epidermis.

The most unique feature of the skin of chondrichthyan fishes is the denticle. Denticles are small, toothlike structures that completely cover the skin of cartilaginous fish (Figure 6.5). Also known as placoid scales, denticles strongly resemble teeth in structure and shape. In fact, they are currently considered to be homologous to all vertebrate teeth. Denticles have an inner pulp cavity, with blood vessels and nerves, and a thicker layer of dentine covered by a thin layer of enamel. The denticles form within the dermis but then “punch” through the epidermis, exposing them to the outside environment. Which developed first, teeth or denticles, is still being debated. One of the consequences of this similarity is clear. Divers who have brushed up against a shark, and even students in a dissection lab, may end up with a slight burn or abrasion as a result of the denticles. A lesser-known consequence of this structure has only been uncovered in the last 30 years. The shape of the denticles as well as their spacing and arrangement work to reduce the drag of a swimming shark. This means that it takes less energy to keep moving the shark forward. Despite performing similarly across sharks, denticles are species specific, greatly vary in shape, and have been used to identify fossil shark species.

Osteichthyes

One of the biggest changes when looking at the differences between Chondrichthyes and Osteichthyes is the development of bone for the internal skeleton (hence their names). However, there are obviously many other differences between the cartilaginous and bony fishes, and the integument is no exception. The most obvious difference between the two groups is that our bony fishes do not have denticles but instead are covered in scales. Both denticles and scales originate in the dermis, but it is there that the similarities end. All denticles, while varying greatly in shape, are composed of the same layers and materials. However, in our bony fishes, there are a large number of different scale types, the details of which are beyond the scope of our discussion here (for more information, see Elliott, 2011). Some fish have scales that retain elements found in denticles (e.g., gar), while many others do not. One element that the majority of bony fish scales have in common is that central regions of the scales are composed of bone. In Chapters 7–9, bone is going to be discussed heavily as it relates to the skeleton. However, as we discussed above, the presence of bone is not limited to the skeleton. Dermal bone, originating in the integument, is a key evolutionary feature of both extant and extinct Osteichthyes. The size of the scales and the amount of dermal bone present vary incredibly from species to species. The general consensus is that fast-swimming fishes (e.g., tuna) have a large number of small scales, while slower-moving fishes have larger, thicker scales but in smaller numbers (e.g., sturgeon). The theory is that smaller scales still provide some level of mechanical protection against predators but are more conducive to the faster lifestyle—that is, they generate less drag from their shape and size and therefore reduce the energy burden on these fish. Many of the freshwater catfish in the order Siluriformes have even lost scales!

In addition to the structural differences between denticles and scales, their position within the integument is also worth noting. As we mentioned, much of a denticle is exposed to the environment, with only its base being covered by the epidermis. The scales in bony fishes are completely embedded in the integument, completely covered by a thin epidermis. In most species, individual scales overlap each other (Figure 6.6), with a thin layer of epidermis found between the two scales.

This epidermis is full of living cells and tissues and is also the host to a large number of glandular cells. The most common glandular cells are mucus-producing cells known as goblet cells. Goblet cells are extremely common not only in the integument but throughout the body. They are also extremely common throughout vertebrates and are the most common cell found in humans. These are different from the glandular cells we observed in lampreys, though the function is the same (the homology of these structures is still unclear).

There are a few additional elements regarding the integument of bony fishes that must be considered before moving on to the tetrapods. The first is that while the hagfishes, lampreys, and cartilaginous fishes are limited to a narrow palette of coloration, the bony fishes have taken advantage of the entire color spectrum. Shades of purple, green, gold, orange, blue, red, and many more can be found throughout the world’s water bodies (Figure 6.7). The colors that we see in these fishes are the result of two different sources: pigments and structural colors. Structural colors are the result of different structural properties of material, particularly properties that impact how light passes through or is reflected. These could be fibers that scatter light, microscopic structures that reflect different wavelengths, and more. The most common colors that we refer to as structural are blues and anything we might describe as iridescent. Pigmental colors are colors that result from selective absorption of light by molecules. These pigments are often stored in cells called chromatophores, which can be distributed throughout the integument and give rise to all the color patterns we see. As varied as the fish in Figure 6.7 are, there are even more variations of chromatophores.

In our bony fishes, chromatophores mostly occur within the dermis, while the iridescent sheen many fish appear to have is the result of structural coloration within the scales and epidermis.

The last thing we need to discuss regarding the integument of the bony fishes is more functional than structural. With the hagfishes, lampreys, and cartilaginous fishes, ions and water freely move across the integument. This results in a water/ion balance of a fish’s tissue being the same as that in the external environment. However, in many freshwater fishes (and those that may move from fresh to salt water) either the epidermis and dermis act to block the movement of water/ions across the integument or there are ion channels that intentionally move ions. In this manner, the concentration of water and ions in a fish’s tissues may be different from that of the external environment. This will become more important when we discuss the tetrapods, which leave the watery environment behind for a life on land.

Tetrapods

The transition from an aquatic environment to a terrestrial one is going to have a drastic impact on many of the systems covered in this book, and the integument is no exception. Again, let us remind ourselves of the ultimate function of the integument, and that is to isolate the body from the external environment. To this point, we have discussed this function in terms of armor (against predators) with some mention of pathogens. As we noted in the last few sentences of the discussion on Osteichthyes, we should not neglect how the integument can regulate the movement of small molecules between the body and the environment. As we begin our discussion on the amphibians and reptiles, armor and protection are still going to be important, but one of the main drivers of the structure of the integument is going to be reducing water loss. Do these organisms have structures that help prevent the movement of water from the body to the environment? How does it impact their biology?

The other major transition that is going to occur is from organisms that are ectothermic (i.e., “outside heat”) to endothermic (i.e., “inside heat”). Ectothermic animals—including fishes (with few exceptions), amphibians, and reptiles—do not produce their own body heat and are more susceptible to changes in environmental temperatures. The birds and mammals are well-known endotherms, producing heat from metabolic processes that keep their body temperature above that of the external environment and within a relatively stable range of temperatures. The integument is the surface area of these animals and the site of heat loss. Many structures we will examine in these groups will mostly act to prevent the loss of body heat to the external environment, but in some cases, they may be called upon to dump excess heat. In humans, for example, our sweat glands are a large contributor to how we maintain our stable body temperature and provide a path for the loss of heat when we get too warm.

Amphibians

In many ways, the amphibians are still tied to the water. The majority of amphibians need to be near water for reproduction and are susceptible to the loss of water through their skin. They have largely lost the ancestral scales (with the exception of a few caecilians), and it is only in the skull where the vestiges of dermal bone can be found. Although the amphibians have not waterproofed their integument as well as the reptiles and mammals, that should not be taken to mean that they lack adaptations suitable to their environment.

What the amphibians can be said to be lacking in waterproofing their integument, they make up for in glands. The epidermis of amphibians varies greatly in thickness (it may be as large as the dermis in some species). Within the epidermis, there is a large variety of glands that can be found in extremely high densities. The majority of these are mucus glands. The mucus in amphibians helps trap and retain some water while also providing a physical barrier against the threat of pathogens. As amphibians have relatively permeable skin, it would seem that they are especially vulnerable to viruses and bacteria. However, many amphibians also have Leydig cells found within their epidermis. It is crucial to note that these are not the same Leydig cells in the reproductive systems of most vertebrates (see Chapter 17). They are similar in structure but vastly different in their function. In the epidermis of amphibians, Leydig cells are considered to assist in mucus production as well as produce secretions that deter the invasion of pathogens.

The other major type of gland found in the skin of amphibians is the poison gland. Poison glands are as variable as the amphibians themselves, not only in what they secrete, but also in where those materials come from and where they are found on the body. Some of these poison glands may be large, discrete structures embedded in the epidermis (e.g., parotoid glands of toads), spread across particular regions (e.g., the highly toxic dorsal skin of poison dart frogs), or distributed across the entirety of the body (e.g., the eastern newt of North America). The dangerous bufotoxin found in toads worldwide is produced by the parotoid glands (Figure 6.8), while the famous poison dart frogs acquire their poison by storing the noxious chemicals found in the ants and termites they consume. In fact, in captively maintained populations, the toxicity essentially vanishes, as they have been fed a diet of harmless crickets and springtails.

In addition to the multitude of glands in the integument, many amphibians also respire through their skin. As Chapter 14 on the respiratory system will show in more detail, respiration is fundamentally about moving oxygen and carbon dioxide across membranes, going from the environment to the blood and vice versa. Many amphibians will undertake gas exchange through their skin, and there are some species that will only exchange these gases through the skin, a process known as cutaneous respiration. The hellbender, North America’s largest salamander, lives in cold, fast-moving streams and is almost completely reliant on cutaneous respiration for its oxygen needs. The lungless salamanders (Plethodontidae), an extensive group of salamanders also found throughout North America (with a few members in Europe and the Koreas), are also completely reliant on cutaneous respiration, with no functional gills or lungs. The adaptations for cutaneous respiration are quite similar to those that we will see later in this book for gills and lungs, increasing the amount of gas exchange that can occur. The first adaptation is that we find a notable increase in the number of capillary beds positioned close to the surface of the skin. The second is that there is often an “excess” of skin, which can be found in folds along the length of the body. The function here is relatively straightforward. The excess skin and capillary beds increase the surface area available for the exchange of gases. With more potential surface area, more gas exchange can take place, enough that these species can get all their oxygen needs through their skin alone. It should be noted, however, that these animals either are relatively small (i.e., higher surface-area-to-volume relationship; e.g., the plethodontids) or live in aquatic environments with an increased amount of dissolved oxygen (e.g., cold and fast-moving streams, like the hellbender).

Nonavian Reptiles

When we get to the reptiles, we see a striking difference from what we just observed in the amphibians. The reptiles are fully divorced from the aquatic environment, and while many have moved back into the water, as a group they are no longer dependent on the aquatic environment. Waterproofing the body will be of paramount importance for these animals, and therefore many of the adaptations discussed are related to the prevention of water loss. And while several of these adaptations will become highly modified for other functions, many have their origins in the prevention of water loss. There are also some striking features of reptiles that originate in the integument but are subsumed into other systems. The best example of this is the turtle shell. The shell of turtles is one of the best-known structures in vertebrates, a combination of bony plates and scales. The bony underpinning of the shell begins as dermal bone, originating in the skin before fusing with the ribs and vertebrae. The scutes, or scaly parts of the shell overlying the bone, are primarily composed of keratinized scales that we will cover in more detail momentarily. While the bone may grow throughout the turtle’s life, the scutes must be shed like any other reptile scale.

The most obvious feature of the integument in reptiles is the return of scales. It is imperative to state that scales in reptiles are not the same as the scales in fishes. Reptile scales are derived from the epidermis as opposed to the dermally derived scales we saw in the fishes. In addition to the developmental differences, there are structural differences in the scales as well. Most scales are composed of two different types of keratin, alpha and beta. Beta-keratin is the most common type in reptiles and birds, making up many of the tougher scales, while alpha-keratin is more commonly found in mammals, making up your hair and fingernails. You can think of beta-keratin as being tougher and less pliable, while the alpha-keratin is much more flexible. The scales are part of the great thickening of the epidermis. The much thicker epidermis in reptiles is heavily cornified (filled with keratin), which plays a key role in the prevention of water loss, infection, and injury, acting as a physical barrier. As we recall, keratin is not a living tissue—instead, it is the product of keratinocytes. This means that occasionally it must be replaced as the keratin becomes damaged or simply no longer “fits” as the individual reptile grows larger. In reptiles, we call the process of replacing the keratin layers ecdysis or molting. For this process, let us focus on the lizards and snakes (Squamates). Snakes are famous for “shedding their skin” all at once, but what they are doing is shedding the external layers of older keratin. If you examine the shed skin of a snake, you will see not only the scales but the keratin bridges that form between them. If the head region of the skin has survived the process, you may even see the clear eye scale that is a distinguishing feature of snakes, sometimes known as the spectacle.

In a few groups of lizards and the crocodylians, a special type of scale and dermal bone combination known as the osteoderm can be found. Osteoderms are superficially similar to fish scales. They have thickened elements of dermal bone but in addition to that are covered superficially by more layers of keratin (Figure 6.9).

It was originally hypothesized that much like the osteoderm-like scales in fish, these function primarily as armor against potential predation. However, recent work suggests that osteoderms may also play a role in the biomechanics of feeding and movement in reptiles. In the crocodylians, some muscle tendons attach to osteoderms, enhancing their lateral undulations during swimming, while in skinks, the osteoderms in the head help distribute the high forces and stresses involved in biting. What is also fascinating about osteoderms is how they interact with each other. In many lizards, the osteoderms act similarly to fish scales, overlapping each other but otherwise functioning as independent units. For other lizards, like some geckos and the large Komodo dragon, individual osteoderms may fuse together into much larger bony plates. The remnants of the individual osteoderms can still be observed, but now they are structured as a single cohesive unit.

There are many unique structures within reptiles that we do not have the time to discuss here and are covered in more detail elsewhere (e.g., touch receptors near the jaws of alligators, infrared receptors in snakes). The last aspect of the nonavian reptiles we must discuss are the glands found in the skin. While their skin is not nearly as glandular as that of the amphibians, reptiles nevertheless have their own glands embedded throughout the integument. Both of the examples we will discuss here impact how reptiles are adapted to their environment and spread all over the Earth. The first are salt glands. Salt glands are found in reptiles that have reinvaded the marine environment (e.g., sea turtles and marine iguanas). The function of the salt glands can be elucidated by their name. Upon reinvading the marine environment, reptiles have to deal with not just the potential loss of water but also the additional salts that come from ingesting marine food and water. As we discussed earlier, the skin is much less penetrable in reptiles, and so they must expel these excess salts differently. The salt glands are not distributed across the body, as we might expect, but instead are concentrated in the head, near the eyes and nares. The second group of glands we can broadly classify as pheromone glands, glands that produce secretions involved in attracting and locating potential mates. Much like the pheromones themselves, these glands are specific to species in terms of their composition, structure, and location on the body. Ovary-bearing (see Chapter 1) red-sided garter snakes have lipid-producing pheromone glands scattered along their dorsal surface, while certain iguanas have only a few pores on the underside of their femoral region.

Aves

Before diving into all the structures in the bird integument, it is important to remind ourselves that birds are a lineage within the reptiles. Despite all the amazing structures that make birds unique, the origin of those structures is rooted in their evolutionary history. Birds do retain epidermal scales, particularly around the legs and feet, although there are some questions about the underlying genetics that obscure this homology. There is also a physiological innovation that is noted in birds that will impact the structure and function of the integument greatly. This innovation is endothermy, the use of metabolic heat production to maintain a stable internal body temperature. For almost all of the birds, this means the maintenance of an internal body temperature that is greater than the ambient temperature of the environment. Water loss was a major concern for our amphibians and reptiles, and now for our birds (and mammals later on), heat loss is going to be an additional concern. Much like we saw with our lungless amphibians, the surface area of the integument will impact the movement of heat. In this section, and again when we discuss the mammals, we will see how these groups mitigate the loss of heat using the integument and its derivatives. Additionally, birds are famous for their ability to fly. Flight affects many aspects of a bird’s body, and the integument is no different. While the thickness of the epidermis and dermis is not notable compared to other classes, it should be noted that these layers are only loosely attached to the underlying hypodermis and muscle. The looser connection provides flexibility for the skin to move freely during flight.

The most recognizable aspects of birds are the feathers. Feathers are truly amazing structures, accomplishing a wide variety of functions while being fundamentally structured like any other derivative of the integument. Feathers are responsible for powered flight, waterproofing, insulation against heat loss, and signaling to others (intraspecifically and interspecifically). Feathers are derived from the epidermis and are primarily composed of keratin. However, the type of keratin is different from that of reptile scales. Recent genetic work has found that alligators briefly make the same type of keratin found in bird feathers (an argument in favor of their shared ancestry), but then that gene is suppressed later in an alligator’s development. Beyond this, the origin of feathers is still being hotly contested, with fossils, development, and molecular evidence being weighed to this day. Even the function of the first feathers is debated (Box 6.1). Throughout their fossil history, feathers have varied greatly, as the dinosaurs and other contemporaries employed them through time. In modern birds, we can broadly classify feathers into two categories: vaned and downy feathers.

Vaned feathers have a central vane and shaft with barbs and filaments. The vane/shaft may be central to the feather, but asymmetrical feathers are quite common. These are the feathers that we most often associate with birds. These are the most external layer of feathers, the flight feathers, and may be brightly colored. These feathers can also be shed as they are damaged over time or as necessity dictates. The differences in these feathers can be pretty remarkable. The wood warblers, a group of migratory songbirds in the Western Hemisphere, are well known for such a change. In the spring, as the breeding season approaches, many sperm-producing individuals will become brightly colored with fantastical patterns and colors in an effort to attract mates. At the conclusion of the breeding season, prior to the onset of their southward migration, they will shed these brightly colored feathers. You would (and many do!) struggle to identify these birds in the fall, as they do not resemble their ostentatious past selves at all. The new feathers, much drabber in color, are fresher for the long migration back to their wintering grounds. The other type of feather is the downy feather. Downy feathers are seen in nestlings and are found close to the skin in adult birds. Downy feathers are much smaller with no vane and create a layer of insulation to prevent the loss of heat. Bird down is an incredibly effective insulator. How effective? We currently use bird down in comforters, pillows, and jackets! Within each category, both downy and vaned feathers can be differentiated into many other types. There are even different ways in which feathers interact with others. Some types of vaned feathers have small barbs on them that will hook together with adjacent feathers. An extreme example of this can be found in the penguins. In penguins, famous for inhabiting some of the coldest environments on Earth, the feathers are locked so tightly together they effectively act as a wetsuit. This creates an additional layer of insulation that helps the penguins retain that body heat.

Much like other reptiles, birds have several different types of glands that can be found throughout their integument. Many of the shorebirds and open-ocean birds have salt glands similar to the other reptiles discussed earlier. These salt glands open onto the dorsal surface of the bill, allowing the excess salt to be ejected. In addition to the salt glands, birds also possess uropygial glands, also known as oil glands, which are crucial to the function of feathers. Uropygial glands are located near the base of the tail, producing a secretion that birds spread all over the feathers. This is the behavior we know as preening. The reason they are also known as oil glands is that these secretions are primarily lipids and act to waterproof the feathers. This is extremely important for wading birds, particularly in cold climates, as wetting the feathers would drastically reduce the bird’s ability to retain body heat. Wet feathers may also stick or cling, making them ineffective if the bird needed to fly.

Mammals

As we conclude our tour of the vertebrate classes, we reach the mammals. In many ways, mammals are like many of the other vertebrate classes. There is a thick cornified epidermis with an even thicker underlying dermis. There are derivatives in the integument that are important. However, there are many facets of mammalian integument that are unique. With one very notable exception, mammals do not have scales of either epidermal or dermal origin. Mammals do not use osteoderms (or any dermal bone) for armoring, with the exception of the armadillos. Mammals have a myriad of glands embedded throughout their integument, several of which are completely new to the scene. Additionally, many mammals store copious amounts of fat in the hypodermis (humans included). This can serve two purposes. For mammals that slow down their activities in winter, this subcutaneous fat contains the energy reserves they need to survive until warmer weather returns and food is bountiful again. The second purpose involves insulation. Mammals are also endothermic animals, using heat produced from their metabolic processes to elevate their body temperature. Mammals living in colder environments have the same struggle as the birds: How do you prevent the loss of that heat? One good mechanism is to use a layer of body fat as insulation. This body fat is often poorly vascularized, preventing blood that has been warmed at the core of the body from losing that heat as it travels closer to the surface of the skin. Marine mammals, including whales, dolphins, seals, sea lions, and walruses, use a specialized type of subcutaneous fat that we know as blubber. To be clear, blubber is not the same structure as the body fat you or I have. Blubber is a specialized type of body fat that is incredibly efficient at controlling body heat. There are two key areas of difference between our body fat and blubber. The first is that blubber is extremely dense, and the second is that blubber is highly vascularized. While the increased number of capillaries may seem counterproductive to the retention of body heat, they actually allow for the animal to have effectively better control of heat retention or loss. If the body temperature begins to drop, blood flow can be directed away from those capillaries, and the incredibly dense blubber is a more than effective insulator. However, there may be times when the whale is moving through warmer waters or the walrus is sunning on the beach, and too much heat can be an issue. These capillaries can be opened and blood allowed to move to the surface, allowing heat to escape. Many mammals have similar mechanisms for the dispersion of excess body heat. Elephant ears are full of capillaries, and when an individual is getting too warm, they will flood those ears with blood. These elephants can be observed flapping their ears back and forth, cooling the blood before it returns to the core of the body.

The most recognizable feature of the mammalian integument is hair. Much like feathers to birds, hair is a trait that even at an early age we are taught is a distinguishing trait (synapomorphy) for the mammals. Fundamentally, hair is quite similar across the mammals and in many ways is similarly structured to other integumentary derivatives. Hair is composed primarily of keratin. Hair can be broken into two major regions, the shaft and the root. The root of a hair is where the keratin-producing cells (and other supportive cells) are still alive. The root is embedded in the dermis. The shaft of the hair contains only dead cells and keratin, found primarily in the epidermis and exposed to the outside environment. Hair itself has three regions internally as well, at the center a medulla, a cortex, and an external cuticle. Hair is also supported by several different cells, tissues, and glands. Collectively, we refer to the hair and its supporting structures as the follicle. Beyond this, hair is extremely variable. As we saw with vaned versus downy feathers in birds, there can be different layers of hair. In most mammals, we refer to the outer layer of hair as the guard hair and the underneath layer as down hair or underfur. The function of the down hair is similar to downy feathers in birds: It provides a layer of insulation.

Hair has been modified to perform a variety of different functions. The quills of porcupines, an apt deterrent of predators, are modified hairs. Wool from sheep is hair. The whiskers of dogs, cats, and many other mammals, formally known as vibrissae, are hairs that serve as incredibly sensitive touch receptors (Figure 6.11).

Most hair on the body has at least some sensory reception; with nerves wrapped around the base of the hair root, any deflection of the hair results in a signal being sent to the brain. The majestic mane of the lion serves as a signal, warning other lions of their prowess and physical threat. Zebras and tigers have stripes on their skin that are also reflected in their hair. For the tiger, this helps hide the predator in tall grass, disrupting their shape and outline as they approach potential prey. The color patterns in zebras were also thought to obscure their outline; however, recently it was determined that the zebra’s stripes actually disorient biting flies, making it difficult for them to land. Many mammals use hair for thermoregulation, much as the birds use feathers. The hair traps air close to the surface of the skin, providing an effective layer of insulation that prevents the loss of body heat. These mammals often have thick coats of fur that are composed of multiple layers and different types of hair. Additionally, there are smooth muscles embedded in the dermis known as arrector pili muscles. The arrector pili muscles pull on the base of the hair, causing it to straighten upward. When you get goose bumps, you are seeing these muscles in action! Even within the mammals that use hair to thermoregulate (which is most mammals), there are a few exceptional examples. The polar bear is a very interesting case. From our perspective, polar bears are completely white, broken only by black eyes and a small black nose. However, polar bear fur is not white at all but is instead almost perfectly clear. These clear hairs act much like fiber optic cables, trapping light and carrying it down the length of the hair. When that light reaches the skin, it is absorbed as heat. This system is so effective that it is not heat loss that polar bears must be concerned with but actually becoming too warm! Polar bears will roll around in the snow to dump the excess heat from their bodies. All mammals have hair at some point in their life history, though many are greatly reduced. The cetaceans (whales and dolphins) are almost entirely hairless. Hippopotamuses, rhinos, and pinnipeds have reduced amounts of hair as well.

In addition to hair, many mammals also possess a dramatic, obvious derivative of the integument. Broadly we refer to them as antlers or horns, and while they may serve a similar purpose, they are different structurally. For the most part, antlers and horns function during the mating season, as testes-bearing individuals will battle one another over access to mates and territory. However, such weaponry on the head also makes for an effective deterrent against predation. Water buffalo and rhinos will use their horns against any perceived threat, and while bighorn sheep battling with each other is quite impressive, wolves and mountain lions would not want to be on the receiving end of such a collision. Both antlers and horns begin as outcroppings of cartilage and bone on the skull. This is different from tusks, another popular mammalian weapon, which are actually enlarged teeth (teeth are covered in Chapter 8—The Skull). Antlers are only found within the family Cervidae, which we can think of as “true” deer, moose, reindeer, and others. Antlers begin in the dermis as cartilage, which quickly becomes ossified. During their growth phase, antlers are covered in velvet, a thin layer of highly vascularized integument that helps feed the developing antler. Once the antler is fully grown, the velvet begins to die off, and the underlying bone is exposed. Before weathering and damage take their toll, it is possible to see tracks from the blood vessels on the antler itself. Once the mating season has concluded, antlers are shed, the dermal bone at the base having been removed. The following season, the antlers will regrow. White-tailed deer, a North American cervid, will grow larger antlers in each following season, reaching a maximum size well after sexual maturity. Horns begin in a similar manner (the genetics are different, but that is beyond our scope). Dermal bone grows outward from a base rooted to the skull. There are a few key differences beyond this point. In the majority of species, horns are not shed during an individual’s lifetime; rather, they continuously grow until death. Horns also have some component of keratin as part of their structure. Rhino horns have small compartments filled with keratin throughout. The horns of bighorn sheep are covered by a relatively thick layer of keratin on top of the bone. As the bone continues to grow, so does the keratin.

Within the skin, mammals have an array of glands. We are going to focus on two of the major groups of glands: sweat and oil glands. Oil glands, also referred to as sebaceous glands, are most commonly associated with hair follicles. Rooted in the dermis, oil glands secrete their products directly onto the root of the hair. The secretion, known as sebum, helps lubricate the hair to pass through the epidermis while also assisting in the waterproofing of both the hair and the pore through which the hair emerges. Sweat glands can be subdivided into two further categories, eccrine and apocrine sweat glands. This distinction will become important later in this section, as we discuss mammary glands, a unique mammalian feature. Sweat glands are embedded within the dermis of mammals, with small ducts that lead to the surface of the epidermis, where a small pore allows their secretions to spread on the surface of the skin. The number of sweat glands and their locations vary quite a bit from species to species. Humans have sweat glands all over the body, in fairly high numbers. Domesticated dogs are well known for having many fewer sweat glands, and most of them are located on the pads of their paws. The function of sweat glands is obviously to produce sweat. Sweat, a mostly water-based secretion, has several functional roles. The primary function of sweat is to help get rid of excess body heat through evaporation. Sweat on the surface of the skin absorbs heat, and as it evaporates, it pulls that heat from the body. It also carries nitrogenous wastes that can be left on the skin surface and molecules that act to lower the pH. These lower-pH secretions are referred to in humans as the “acid mantle” and provide an extra level of protection against potentially harmful bacteria and viruses. Most sweat glands that function as we just discussed belong to the category of eccrine sweat glands. Apocrine sweat glands are slightly different. In addition to the water-based secretions, apocrine glands add relatively high numbers of lipids and proteins to the mix. This results in secretions that are thicker than those in the eccrine glands and can be highly specialized depending on location and ultimate function. Some musk glands are apocrine glands, creating the odors that mammals use to mark territories, advertise mating status, and more. The ceruminous glands of humans are apocrine glands, producing what we know as earwax to trap dirt and other materials that may enter the external ear canal.

Mammary glands, another hallmark of the mammals, are specialized apocrine glands. They produce what we commonly refer to as “milk” for the purposes of feeding offspring after birth. The milk, full of proteins and lipids and other nutrients, is crucial to the health and growth of young. The content of the milk is quite variable from species to species. Whale milk can be almost 50% fat, one of the highest concentrations in mammals. In the monotremes, our echidnas and platypus, each individual mammary gland opens to a pore on the skin, on the ventral surface of the mother. The mother essentially “sweats” milk, which the young then lap up. Other mammals have nipples or teats, individual openings through which multiple mammary glands empty their products. The marsupials concentrate these within the pouch. The placental or eutherian mammals have multiple openings (6–10) on the belly/ventral surface, with the exception of the primates, who often only have two openings in the chest region.

6.5 Humans—Anatomy and Applications

Humans, unsurprisingly, have all the traits of the integument that other mammals possess. We have a keratinized epidermis and a larger dermal layer. We have oil glands, sweat glands, mammary glands, and hair. There are sensory receptors wrapped around the hair that provide sensations when the hair is brushed or moved. Our epidermis and dermis have sensory receptors throughout, providing feedback on touch, pressure, temperature, and pain. In this section, we will focus on structures that are unique to humans, those that are of particular importance to human biology and health, or common diseases that are the result of damage/issues with the integument.

The epidermis in humans is similar to that of other mammals in terms of both its structure and its constituents. However, some of us develop an extra layer to our epidermis. Known as the stratum lucidum, this extra layer shows up in areas of higher physical stress. The bottoms of your feet, your heel and toes, may seem to have tougher skin than other parts of your body. If you use your hands for a lot of manual labor, you may develop “calluses.” This is the effect of the stratum lucidum. It helps prevent the underlying living tissues of both the epidermis and dermis from becoming damaged. In other areas, the epidermis may be thinner. If you were asked to identify an object without looking at it, you may pick the object up and run your fingertips over the object. Your fingertips have higher concentrations of touch receptors and a thinner epidermis, providing excellent feedback on the texture and composition of the object.

As we mentioned before, the sweat and oil glands open to the surface via pores in the epidermis. While the glands themselves are embedded deeper within the dermis, their openings in the epidermis serve as a potential point of entry for unwanted pathogens and other materials. Dirt and other materials may enter a pore and prevent the sweat/oil from being released, effectively clogging the pore. The sweat/oil begins to build up, and bacteria will enter as well. The buildup of sebum and dirt results in what we commonly refer to as a blackhead. They are not themselves dangerous, but if bacteria can enter, infection may occur. White blood cells rush to the scene, working to destroy the pathogens before they cause any damage. However, we might notice the response as the area around the infection becomes inflamed and there is buildup of dead cellular material and pus. This is known by many colloquial names—a pimple or zit, for example. Acne refers to the chronic infection of the skin in this regard. Repeated damage to these areas of the skin can result in painful scarring.

Healthy, normal epidermal tissue is constantly replacing itself. As the outer layers are damaged, new layers of keratin from dying cells are pushed upward to replace them. The rate at which these cells proliferate and produce keratin is tightly controlled. In many people suffering from the condition known as psoriasis, however, the cells of the stratum basale and germinativum grow and reproduce much faster than they should. A result of systemic inflammation, they push themselves to the surface, resulting in patches of skin that are dry and itchy and can be quite painful. Thought to be an immune disorder, there is no cure for psoriasis, but instead the symptoms are treated in an attempt to provide relief.

The lower levels of the epidermis are also where we find the cells that give color to the skin. The most common and medically relevant of these pigment-producing cells are the melanocytes. Melanocytes produce melanin, a dark pigment. Melanin absorbs solar radiation and is particularly important for absorbing UV radiation, which is known to damage the DNA within cells. In response to increased exposure to UV radiation, melanocytes will increase in number and in their production of melanin. However, there are two elements of this that are noteworthy for human health. The first is that too much UV exposure at once does not allow enough time for the melanocytes to adapt. The large volume of UV radiation is absorbed by other cells in the skin, resulting in damage to those cells, which you may notice as a sunburn. This is an immediate impact of excessive UV radiation exposure. Over longer periods of time, chronic exposure to excessive UV radiation damages the DNA of the melanocytes themselves, with one effect being that they begin to proliferate uncontrollably. This is a type of skin cancer that we know as melanoma. Melanoma is the most dangerous of skin cancers, as it will metastasize (spread) to other parts of the body, where it may ultimately cause death (Figure 6.12).

6.6 Summary

The integument is the barrier between an organism and its environment. Any interaction between an organism and its environment (including other organisms in that environment) involves the integument in some manner. It is important to take into account not only the evolutionary history of an organism when considering how its integument may be structured and function but also the environment it currently lives in and what it may encounter in that environment.

6.7 Further Reading

1. Lingham-Soliar, Theagarten. The Vertebrate Integument. Vol. 1, Origin and Evolution. Berlin: Springer Berlin Heidelberg, 2014.
2. Lingham-Soliar, Theagarten. 2015. The Vertebrate Integument. Vol. 2, Structure, Design and Function. Springer Berlin Heidelberg.

6.8 References

1. Benton, Michael J. “A colourful view of the origin of dinosaur feathers.” Nature 604 (2022): 630–631.
2. Kennedy, E. B. Lane Kennedy, Raj P. Patel, Crystina P. Perez, Benjamin L. Clubb, Theodore A. Uyeno, and Andrew J. Clark. “Comparative biomechanics of hagfish skins: Diversity in material, morphology, and movement.” Zoology 145 (2021): 125888.
3. Fudge, Douglas S., and Sarah Schorno. “The hagfish gland thread cell: A fiber-producing cell involved in predator defense.” Cells 5, no. 2 (2016): 25.
4. Elliott, D. G. “Functional morphology of the integumentary system in fishes.” In Encyclopedia of Fish Physiology: From Genome to Environment, Vol. 1, edited by Anthony P. Farrell, 476–488. San Diego: Academic Press, 2011.
5. Nasoori, Alireza. “Formation, structure, and function of extra-skeletal bones in mammals.” Biological Reviews 95, no. 4 (2020): 986–1019.
6. Akat, Esra, Melodi Yenmiş, Manuel A. Pombal, Pilar Molist, Manuel Megías, Sezgi Arman, Milan Veselỳ, Rodolfo Anderson, and Dinçer Ayaz. “Comparison of vertebrate skin structure at class level: A review.” The Anatomical Record 305, no. 12 (2022): 3543–3608.
7. Yenmiş, Melodi, and Dinçer Ayaz. “The story of the finest armor: Developmental aspects of reptile skin.” Journal of Developmental Biology 11, no. 1 (2023): 5.
8. Dhouailly, Danielle. “A new scenario for the evolutionary origin of hair, feather, and avian scales.” Journal of Anatomy 214, no. 4 (2009): 587–606.
9. Grant, Robyn A., and Victor G. A. Goss. “What can whiskers tell us about mammalian evolution, behaviour, and ecology?.” Mammal Review 52, no. 1 (2022): 148–163.
10. Leitch, Duncan B., and Kenneth C. Catania. “Structure, innervation and response properties of integumentary sensory organs in crocodilians.” Journal of Experimental Biology 215, no. 23 (2012): 4217–4230.