16 April 2008

What is a terrestrial animal?

If you think you know how to categorize animals as aquatic or terrestrial, think again. Are frogs aquatic or terrestrial? What about sea otters? And what about a human embryo floating in its amniotic fluid and breathing it into its lungs?

Strict definitions are not reliable, because there are always exceptions. Nevertheless, consider the following criteria, the best I can come up with so far, for aquatic and terrestrial animals.

A1. An aquatic animal spends its entire life cycle in a liquid medium that is mostly water.

A2. The volume of water making up the animal’s habitat is significantly larger than the body volume of the animal.


T1. A terrestrial animal spends its entire life cycle outside of water. If it enters the water to feed or for other activities, the total time spent in water is insignificant relative to the animal's life span.

T2. If there is an aqueous envelope around the animal, the envelope’s volume is significantly less than the body volume of the animal.

The problem is that if we go by these definitions, then there is no such thing as a terrestrial animal, because all animal embryos are surrounded by a watery medium and the volume of the medium is significantly larger than the body volume of the embryo at least during the early stages of its development. We need to modify the definition for terrestrial animals by adding a 3rd criterion.

T3. During the early stages of the animal's embryonic development, there may be an aqueous envelope around the embryo with a volume significantly larger than the body volume of the embryo if the egg or the parent’s body within which the embryo and the aqueous envelope are located are not themselves surrounded by a liquid medium.

Now the definitions are beginning to get cumbersome. It gets worse when we start considering those animals that fit into one set of criteria during one part of their lives and into the other one during the rest. For example, there are many snail species that live where the sea and the land meet. How do we decide if they are terrestrial snails or aquatic snails? Traditionally, those species that live outside the water and enter it only to reproduce have been classified as aquatic snails* (for example, Melampus bullaoides and Cerithidea scalariformis), while those that live and reproduce outside the water have been classified as land snails regardless of how close their habitats may be to the sea (for example, Truncatella species).

I have so far found only 3 relevant, but brief literature discussions of what it means to be terrestrial. The 1st one is by Labandeira & Beall (1990):

...we consider a "terrestrial organism" to be one that is obligately adapted to land; facultative behavioral adaptation of marine arthropods to a land-based existence is technically excluded...When both groups are discussed, we will refer to the first group as terrestrial and the last group as semiterrestrial. True terrestriality requires an obligate physiological commitment to life on land.
I don't find this a useful criterion, because it requires further explanation. What do they mean by "an obligate physiological commitment to life on land"?

The criterion used by Martens et al. (2004) to decide that the ostracods from forest leaf litter were terrestrial, however, agrees with mine. In response to another researcher, who did not consider similar ostracods to be terrestrial, this is what they said:
...did not consider his ostracods from terrestrial habitats themselves to be terrestrial, because these animals gather a film of moisture around and within their valves, so that they still breath through water. We reject this point of view, as nearly all forms of animal respiration, even that of humans, requires a degree of moisture, either externally or internally (within lungs). When animals live in terrestrial conditions, i.e. outside of free standing or flowing water, we consider them terrestrial.
Finally, here is Little's (1990) opinion:
If animals are effectively covered by a layer of water, then they are living as aquatic animals. If they are not so covered, which often means just that they are bigger, as earthworms are usually bigger than soil-dwelling nematodes, then they can be said to be truly terrestrial.
This criterion seem to introduce not a relative but an undefined absolute size criterion; in other words, very small animals can't be terrestrial. I don't find it convincing because of that reason.

A note of caution is necessary here. If we spend too much time thinking about such matters, we will be missing the point. Exercise is good for one's body and mind, an exercise in futility, on the other hand, is a waste of time. What matters is the characterization of the lifestyles of the animals of interest and the understanding of their evolutionary origins.

*If we applied the same reasoning to turtles, then there would be no such thing as a sea turtle, because they all lay their eggs on land.

Koen Martens, Patrick De Deckker & Giampaolo Rossetti. (2004). On a new terrestrial genus and species of Scottiinae (Crustacea, Ostracoda) from Australia, with a discussion on the phylogeny and the zoogeography of the subfamily,
Zoologischer Anzeiger, 243:21-36.

Labandeira, C. & Beall, B. S. (1990). Arthropod Terrestrialization. In
Arthropod Paleobiology, Short Courses in Paleontology No. 3: 214-232. Mikulic, D. & Culver, S. J. (Eds).

Little, C. (1990).
The Terrestrial Invasion. Cambridge University Press.



Marla Coppolino e-mailed this:

"I've recently come across some terrestrial-or-not thoughts, in making my species list of "Terrestrial gastropods of 6 southern Illinois counties". I had to decide whether to include Pomatiopsis lapidaria (Say, 1817) (a land prosobranch) and Fossaria obrussa (Say, 1825) (a freshwater pulmonate). Both tend to be amphibious. I finally decided that since I found shells of both on land, that I should include them. My list will be used by the IL Dept of Natural Resources folks, so needs to be comprehensive of any and all snails that can be found on land. In this case, terrestrial is in the eye of the terrestrial beholder.

Also very recently, I learned something new about Bryophytes (mosses, liverworts, hornworts). I always thought they were terrestrial, but some species are completely aquatic, and can't tolerate desiccation.

Evolutionarily speaking, it seems snails (and other animals) have some multiple transitions in their history, from water to land and vice versa. Yes?

It seems difficult to draw the line between terrestrial and aquatic in so many cases! There are in-betweens. Heard about the newly described frog that lacks lungs as an adult?"


Yes, gastropods have had multiple & independent transitions from the sea to land: Pulmonata, Helicinidae, Cochlostomatidae, Pomatiidae, Truncatellidae, Diplommatinidae, you name it. And then there are several semi-terrestrial groups: Littorinidae, Hydrobiidae, Potamididae, you name it.

Tim Pearce said...

Humans label things for the sake of convenience, but nature does not necessarily fit into one box or the other (look at the problem of defining species, for example).

My advice is to define how you are using the terms in a particular paper (which may differ from your definition in another of your papers!) or instance. The definition could even be a list. For example, you could say, "in this paper I treat Pomatiopsidae and Truncatellidae as terrestrial."

If you do try to make definitions, consider that different life stages might be predominantly in different habitats. Efts have a terrestrial lifestyle, but the larvae and newsts seem aquatic. Many insects have aquatic larvae, but terrestrial (or aerial) adults.

Two thoughts I briefly considered but then withdrew as not vqalid are(1) where does it reproduce (I love your sea turtle counter example), and (2) if you held it underwater would it survive (but whales would not survive).

I advocate terrestrial and aquatic as useful terms with fuzzy boundaries. Close to the boundaries, just define what you do at that particular use.

Frank Anderson said...

I agree with Tim. Obviously, some taxa are easy to define in one way or another (e.g., squid are aquatic, ostriches are terrestrial) and others are not (e.g., several taxa that you listed), as with species.

I had to laugh when I read this: "When animals live in terrestrial conditions, i.e. outside of free standing or flowing water, we consider them terrestrial." You noted the difficulties of such a definition. We just finished covering micrometazoans in my invertebrate zoology class. There are several freshwater micrometazoans -- tardigrades leap to mind -- that live in ostensibly terrestrial habitats at human scales (such as a clump of moss), but that are only metabolically active when these areas are "damp" (which, to a tardigrade, means "totally submerged"). Are they aquatic or terrestrial? Certainly they are aquatic.

Of course this -- "...in other words, very small animals can't be terrestrial." -- is also not necessarily true. Many mites are vanishingly small, but are unquestionably terrestrial.