Introduction to Autecology

Part I. Physiological ecology: functional responses to environment

This Iguana is common in the canopies of Neotropical forests.
It controls its body temperature and activity state by behaviorally
varying its exposure to sunny and shady regions in the canopy.

Definition of Physiological Ecology: The study of physiological characteristics and responses of organisms with respect to a specific set of environmental factors acting as selective agents.

Terms that are frequently used with respect to maintenance of homeostasis in plants and animals:

• Acclimation: Reversible physiological changes that help maintain the functioning of the organism under changed environmental circumstances. Such changes may be obviously ontogenetic (i.e., developmental; such as the production of a new type of leaf in the new environment), or they may be less obvious to inspection (e.g., biochemical changes within a leaf after a change in the environment).
• Adaptation: A characteristic of the phenotype that improves an organism's ability for growth, maintenance and reproduction. The characteristic is acquired through the process of past organic evolution and has a genetic basis.
• Behavior: Phenotypic plasticity expressed within the lifetime of an individual.
• Foraging: Behavior that enhances resource acquisition.
• Ontogenetic change: Progress from one developmental stage to the next where the stages are fixed and do not have alternative phenotypes.
• Phenotypic plasticity: The response by an organism to an environmental stimulus.
• Potentiation: The effect of an initial stimulus in evoking a stronger response the next time the stimulus is received.
• Stress Response: perturbation from homeostasis by an environmental change that results in reduced ability for maintenance, growth, and reproduction. Does not include the organism's attempt to re-establish homeostasis.
• Ecotypes: ecologically and genetically distinct phenotypes of a species, usually living in distinct, contrasting environments to which they have adapted. These adaptations are the basis of the ecotypic differentiation of the organisms.

Physiological and behavioral ecology are central to the study of Life History and Allocation Theory:

Life history: The study of the schedule of births and deaths for a species.

Resource allocation theory: The study of how organisms acquire and allocate scarce resources (mainly carbon) to the competing functions of maintenance, growth and reproduction throughout the organism's lifetime.

Goals of Study:

• To identify and describe those physiological processes which have evolved as adaptations to specific selective factors affecting the ability to acquire and use resources.
• To understand the evolution of phenotypic plasticity and acclimation.

Sidebar: Scientific Methodology of Physiological Ecology

I. Descriptive

• Describe the Environment
  
• Describe Species Physiology

  II. Experimental Characterization of Environmentally-induced Phenotypic Changes: determination of physiological characters of organisms grown in selected environments. See the common-garden technique of Clausen, Keck, and Heisey, 1948. In this classic study, ecotypes of Achillea millefolium were studied over an elevational gradient in the Sierra Nevada mountains.
  
  

• Acclimation and plasticity - The evaluation of genotypically fixed characters (study of ecotypes - ecologically and genetically distinct phenotypes of a species). This is typically done using the Common Garden experiment; used to demonstrate which characters have a genetic basis AND do not change in response to an environmental change.
• Evaluation of adaptive significance of the response by transplanting phenotypes to alternative environments; reciprocal transplant experiment. Usually involves describing the Norm of Reaction for the ecotypes. This is a crucial step in order to differentiate acclimation from a simple stress response.
• Characterization of mechanisms: Describe the structural, biophysical, biochemical, and molecular-genetic basis of the response. What are the proximal stimuli and mechanism of induction of the phenotypic response?

III. Identification of Mechanisms of Natural Selection (population-level studies)

A. Breeding Experiments: Are the traits heritable?

B. Selection Experiments: Determine which combination of features results in higher fitness in a specific, experimental environments.



IV. Example - Sun and shade leaves - Why do shade leaves have a different size and shape than sun leaves? See the Photosynthetic Light-Response Curve below and in your text. Please learn the parts of this curve.

Introduction to Environmental Heterogeneity

I. Space and Time

There are two broad categories of environmental heterogeneity.

A. Spatial : e.g., The concept of microhabitat. (John Harper and studies of old field perennials.)

B. Temporal : e.g., intertidal variation. The tide changes twice per 24 hr period.

• high tide zone: includes protected organisms such as barnacles and other shell fish that can tolerate desiccation.
  
• middle tide zone: limpets chitons snails starfish worms. These are organisms which can tolerate moderate amounts of dessication largely by retreating to a shell.
• low tide zone: unprotected organisms sea anemones, nudibranchs, tunicates, sponges. Nearly always under sea water.

II. Graininess

Time: Fluctuations of long duration require a different response from those that are short.

Space: Spatial variation over great distances requires a different response from that to spatial variation over short distances.

What is long and brief, or near and far, depends on

• life span
• response time
• range - ie, mobility of the organism

e.g., passing storm has little effect on large mammals, but this is the entire life cycle of many insects, or example, mayflies.

A. Coarse-grained environment: patches are relatively so large that the individual can choose among them in time or space

B. Fine-grained: patches are so small that the individual cannot usefully distinguish among them in time or space - the environment appears essentially uniform.

Examples:

1. Daily cycles or shorter may be thought of as fine grained with respect to some organisms (daily cycles are so fast that most organisms cannot respond by an acclimation or adjustment) - vs. seasonal or longer cycles -> definitely coarse grained for most organisms - (e.g., hibernation and associated change in fat concentration).

2. Grassses and forbs in a prairie: all appear the same to a large browsing ungulate (or to people, unless you are a trained botanist). To a grasshopper the environment is coarse grained because the grasshopper must choose between plants in order to not be poisoned and derive maximum carbon from certain perferred species.

3. Graininess depends on the activity. For example, if we set out to pick flowers of a certain type, then the environment appears coarse grained to us, once we are able to identify that species. Moths travel at night to the region of light and dark of the horizon. In this instance the spatial aspect of the environment is coarse-grained.

4. Life cycle of an insect on a single, individual plant. The plant is thus a fine-grained environment relative to other plants. This concept can be extrapolated to parasites, etc..

III. Activity Space

That particular combination of time and space in which an organism is active in its environment.

Examples:

• Cactus Wren: Daily behavior reflects the temperature of the microhabitats used. The orientation of the nest changes during the breeding season in order to maximize cooling in this desert enviironment.
  
  
  
  
  
• Lizard: mallee dragon forages only between 0830-1130, midday must seek shade or die, 1430-1800 forages. Too cool in early morning and late evening.
• Desert Iguana (Dipsosaurus dorsalis) in the southwestern US desert. In summer temperatures can exceed 45^oC, and in winter temperatures are often below 0^o

  During mid-July the thermal environment changes so rapidly that activity is limited to 45 minutes in the morning, and 45 minutes in the afternoon. Figure below describes the diurnal and seasonal pattern of behavior:

  
  

Homeostasis and Acclimation

I. Homeostasis: maintenance of the internal conditions of an organism at some optimum level for its functioning.

Examples:

• shivering thermogenesis - caloric release due to cleavage of high energy phosphate bonds. Utilizes brown fat.
• tanning - melanin production
• sunning lizard
• muscles of butterfly warming up
• biochemical buffering of pH of blood

  H⁺ + HCO₃^- <-> H₂CO₃
  H₂CO₃ <-> CO₂ (aq) + H₂O
  CO₂ (aq) <-> CO₂ (g)

  Reaction balance is driven by blood pH and CO₂ tension.
  

II. Ultimate vs. Proximate Causes Revisited. What determines the best internal condition?

Ultimate causation is fitness, i.e., number of offspring that the organism produces.

Path of causation between temperature regulation and fitness is complex.

We treat this as a problem in the economics of the characters in question - cost vs. benefit analysis or, an optimization function.

Cost: e.g., measured in energy terms which may deplete fat reserves and make life difficult in face of a food shortage.

Benefits: e.g., activity under conditions which would otherwise be life threatening. This might be measured in terms of energy acquired by foraging.

III. The Concept of Optimality

Molecules responsible for biological function are extremely sensitive to changes in conditions of temperature, pH, and salt concentration.

A. Examples

1. Optimum temperature. Enzyme structures are altered under high and low temperature. Reaction kinetics are slower at low temperatures
2. Photoinhibition. Photosynthetic pigments break down under intense light. Other pigments that protect against photoinhibition are costly to make, and once present in the chloroplasts, they divert energy away from photosynthesis. Thus, they should only be produced only when their cost is more than balanced by their benefit to continued function of carbon gain in strong light.
3. Variation in salt concentration determines osmotic balance. For example, oyster larvae die if salt concentration changes more than 0.8%

Two possible causes: a. salt change directly determines internal salt concentration of larvae. b. cost of maintaining (respiration) osmotic balance is too high

4. Temperature affects fish swimming speed. The graph of temperature vs. swimming speed shows the typical form of optimality function and acclimation to different optima. That is to say, the curves are maximum at some temperature in the middle of the function.
5. Acclimation of assimilation (photosynthesis) to temperature. See figure below.





Note that the capacity for acclimation reflects the range of conditions encountered by the plant. In the figure above, the red line indicates hot growth conditions, while the blue line indicates moderate growth temperatures. Larrea grows where there are hot summers and cool winters. Thus it shows a shift in temperature optima when grown under contrasting temperatures. Atriplex does not experience hot conditions, and thus does best under cool temperatures. Tidestromia grows where it is perennially hot, and thus shows a very strong acclimation response to higher growth temperatures.

6. Adaptation and acclimation of photosynthesis to light intensity. See the graph below. The bottom graph in this figure is known as a "reaction norm". Note the differences between adaptation and acclimation.

Acclimation is a reversible change in structure or function. Note the concept of a "tradeoff" between efficiency in low light and high assimilation capacity in high light. Plants in high light show high photosynthetic capacity and have high maintenance costs (respiration). while the reverse is generally true for shade plants. Assimilation in both figures above is measured as NET CO₂ exchange on a leaf area basis. Thus, acclimation is a shift in the range of physiological tolerances of the individual due to a shift in phenotype, while adaptation is caused by natural selection and represents a change in genotype.

The Reaction Norm is defined as "the relationship between the appearance of a phenotype and variations in the environment produced by a particular genotype." In short, it is the phenotypic response of a genotype to variations in the environment.

Some examples of acclimation:

• growing thicker fur in winter
• producing smaller leaves in the dry season
• increasing the number of red blood cells at higher elevations
• producing enzymes with different temperature optima
• producing lipids that remain fluid at different temperatures

Acclimation potential is determined by the growth environment. At first glance, the figure above suggests that shade seedlings have higher assimilation than sun plants in all environments. This is correct when net assimilation is measured on a whole-plant mass basis (ie, the part above ground ). Plants initially grown in shade have smaller root systems and more foliage than seedlings grown in full sunlight. Because a shaded environment taxes a plant's water economy less, shade-grown seedlings can allocate more of their production to stem and needles; sun-grown seedlings develop more extensive root systems to obtain sufficient water. Thus, the greater proportion of needles in shade-grown plants enhances photosynthetic rate per unit plant mass, especially under low-light conditions.

Note: Uncle Bob and I have a point of disagreement with respect to the heading on page 188. Ricklefs states that developmental responses are irreversible changes. This is true in the sense that once a organ (leaf) is produced in a given environment, that organ cannot change its morphology. It can change its biochemistry to perform somewhat better in response to an environmental change. Moreover, the production of a new leaf phenotype in the changed environment is acclimation, and this is also a developmental response. Another word for developmental is ontogenetic.

 

7. Adjustment of root-to-shoot ratio when soil nutrients are scarce. This is accomplished by allocating photosynthate (carbon) differently under contrasting nutrient availability. The plant in (a) is growing in limiting soil nutrients and thus allocates more carbon to root growth (is this foraging?), while the plant in (b) allocates more to the above ground shoot under plentiful nutriients.

Point: When conditions in the surrounding environment differ from the optimum for cellular performance, organisms face a choice of impairment or investment in the metabolic and carbon costs to maintain proper cellular function.

B. Assessment of cost; two ways to measure

1. Energetic cost, as in heat to maintain body temperature, or the ATP necessary for locomotion. Both of these are maintenance costs.

How does this hummingbird find enough energy
to make its annual trip across the Gulf of Mexico.

2. In terms of constraints on organism function (opportunity cost) e.g., adaptations for water conservation in cactus - reduction of surface area to volume ratio limits its ability to compete in, say, a forest or grassland ecosystem; e.g., adaptation for optimal photosynthesis in shade may limit a plant's ability to grow in high light environments.

IV. Feedback Responses

A. Regulation of body temperature in endotherms (homeotherms).

1. Maintenance of 37^o C for endothermic organisms. Outside temperature can vary between -50 to +50 degrees C. Also known as homeotherms. Ricklefs gives them the designation of "regulators".

Mechanism in endotherms: sensitive thermostat in brain responds to temperature changes by secretion of hormones from hypothalamus. Hormones slow down or accelerate the generation of heat in body tissues.

Negative Feedback Loop:

Stimulus--> sensor---> effector---> response
Note that the response is always in opposition to the stimulus. This is in contrast to the feedforward response of stomata to the humidity of the air.

This is in contrast to ectothermic organisms, which are "conformers" such that activity is much more constrained by the environment. (note the older Zoological term, Poikilotherms).

Point: All organisms engage in homeostasis in some fashion.

2. Behavioral regulation is also used by many different organisms, endotherms and ectotherms (e.g.,birds fluff up feathers in cold). Note that behavior is part of the concept of a "functional response" to variation in the environment.

Figure above: During the winter, the Willow Ptarmigan produces a denser coat of feathers and actually down-regulates its basal metabolism, whch reduces the gradient between the internal body temperatue and the external temperature. This is the same as keeping your house at a cooler temperature in order to reduce your heating bill. Both responses reduce the amount of energy necessary to stay warm.

B. Regulation in ectotherms (Poikilotherms).

Often behavioral in conjunction with specialized morphology. See "cheap tricks" below.

Example: Lizard changing profile on rock. It will stay flat on rock to gain heat. but stands up on its toes to avoid receiving heat at midday.

V. Proximate Costs of Homeostasis.

To maintain a constant body temperature, an organism must replace heat that is lost by releasing heat energy metabolically. Thus the rate of metabolism required to maintain body temperature increases in direct proportion to the difference between body and ambient temperature.

A. Definitions

1. Basal metabolism: the lowest level of energy release under normal condition.

How does the basal metabolism of these Three-toed Sloths
compare to that of other mammals of similar size?

2. Lower Critical Temperature (T_lc): that amount of heat produced by basal metabolism. -> if the ambient temperature drops below this, then the organism must increase metabolism.

3. Lower Lethal Temperature (c): lowest temperature permissible by maximum rate of energy metabolism

4. Critical Ecological Temperature (b): Lowest temperature at which organism can maintain itself indefinitely. Set by rate at which food can be gathered.

Another way to express this is Ricklefs' figure 9.4. Note the inclusion of the population in this concept.

B. Cheap tricks: methods of conserving energy

1. Counter-current heat exchange:

• Bird legs - Penguins and Geese. (what does the plot of temperature of vessel vs distance from body core show?)
• Fish - Bluefin tuna.
  
• Kangaroo Rat nasal passages
  
• Vessel arterial net in the Circle of Willis (brain circulation) in high-performance organism (dog, cheetah etc.). Vascular net is literally for keeping a cool head.
• Fish Gill oxygenation mechanism (Ricklefs' Figure 3.22)

2. Torpor

Hummingbirds do not cease to regulate, but rather adjust the set point so that (a) the difference between ambient and internal temperature is less, and (b) metabolism is greatly slowed so that maintenance is less costly.



3. Dormancy - diapause and hibernation.

Examples:

• tropical and subtropical trees shed leaves during seasonal droughts
• mammals undergo hibernation
• some insects enter winter diapause, reducing their freezing point and metabolic rate
• other insects enter summer diapause, tolerating dessication
• plant seeds and spores of bacteria and fungi exhibit effective dormancy mechanisms

VI. Regulators and Conformers

Compare and contrast endotherms and ectotherms: few organism do each strategy perfectly. The extremities are cooler in homeotherms while many ectotherms do generate metabolic heat.

A. Examples:

1. Temperature

mammals: this is the most precise with regulation at 36 to 39 degrees C
opossum: marsupial -> 29 to 39 degrees C
python: high body temp when incubating eggs, but varies at other times
tuna: performance enhanced by countercurrent exchange net.
moth: preflight warm up of muscles necessary

2. Ionic: osmotic stress

Anadromous fishes - Please see this article on Salmon

Shrimp: Gammarus when moved from salt water to fresh water will begin to conform

Artemia (brine shrimp): critical conformer in salt water always below water.

B. Surface area-to-volume considerations. Note that homeothermy is rare, why?

1. As body size increases, volume increases as a power of 3, whereas surface area increases as a power of 2.

2. In general, for endotherms the lower the SA / V (e.g., big mammals), the more comprehensive and precise regulation can be because less heat is lost to the environment relative to the thermal intertia of the body fluids. The same is generally true for ectotherms, but behavioral regulation is the primary means of regulation, and this is generally less comprehensive and precise.

Surface area / Volume considerations apply
to plants too, such as this barrel cactus in Sonora.

C. Thermal inertia

1. Thermal inertia of the environmental medium can greatly alter the expense of regulation vs. conformation.

2. Body size vs. thermal interia. Large bodies tend to change temperature more slowly in response to an environmental change. We now have a controversial theory that some dinosaurs may have been endothermic in order to have persisted in the face of large changes in environmental temperature.

D. Oxygen consumption and metabolism in endotherms and ectotherms.

• Different classes of organisms are part of different regression between total metabolic rate and body mass. The larger and more endothermic organisms tend to have higher total metabolic costs.

• There is an inverse relationship between O₂ consumption per g body mass and total body mass during activity, such as locomotion shown in the figure below. (figures above and below from Schmidt-Nielsen, How Animals Work)

Question. Which matters more for survival: the per gram basal metabolic rate, or the total basal metabolism (i.e., cumulative energy consumption) of the organism? Please see this paper on Flying Foxes by our own Brian K. McNab. Note the figure and the units used for the vertical axis.

Question: Why are humans slightly above the regression line?

E. Other benefits of thermoregulation -> locomotion and maximizing performance

Water Balance in Hot Deserts

I. Relationship between water balance and heat:

Hot environments tend to be dry envronments (but not always so)


Sunken stomatal pits of Oleander

Evaporative cooling is necessary but costly for most organisms

II. Examples:

A. Kangaroo Rat: This organism does not consume liquid water because it lives in an environment where there is none. All water is from food (insects, seeds etc.) and metabolism.

Five mechanisms for life without liquid water: 1. fat metabolism results in production of water (? - albeit with a net energy loss), 2. nasal cooling and condensation of expired air, 3. acquires all water from food, 4. highly concentrated urine, 5. behavioral regulation through avoiding midday conditions and largely nocturnal activity.

B. Cactus Wren: This bird avoids direct water loss and does not pant like other birds to evaporatively cool. Ricklef's studied this bird's behavioral regulation of body temperature and water loss. (a) Nest orientation changes with season, and proper orientation is related to nest success. (b) Fecal sac left in the nest during the hottest time in order to evaporatively cool the nest.

C. Camel: This large animal has great thermal inertia. Remarkably, camels can allow their body temperature to rise in order to avoid water loss from evaporative cooling (as in previous examples, this lessens the temperature gradient between the organism and the environment).

Camel's hump -> Classic ecophysiological question of whether fat can be metabolized to water and thus used as a water reservoir is illustrated through ecophysiological study of the camel's hump. Is water production the primary function of the fat in the hump?

Everything in this critter is adapted for life on the desert. Feet are broadened to walk on sand. Eyelashes protect eyes from wind-blown sand. Nostrils close to keep sand out. Lips are thickened to withstand the coarsest of desert plants. Coloration matches the environment. Callouses are present on knees and other parts of the body that touch the hot sand when the animal sits down. Hump is a flesh mound not supported by bones. A reserve of fat (not water) is stored in the hump. Hump size varies with food supply and working conditions. Can tolerate a rise in temperature of 12 degrees Fahrenheit. Able to drink brackish or salt water. Camels exhibit unusual tolerance for dehydration. Most animals perish when 20% of their body weight is lost. Camels survive a 40% loss of body weight without serious consequences. Heavy fur and the fatty hump serve to insulate the body, preventing body temperature from rising to the sweating point (the major cause of water loss). When water again becomes available, camels are able to restore their body water quickly; they have been known to drink one third of their body weight in 10 minutes.

D. Nocturnal activity is a primary means of avoiding drought stress for most mammals and many birds and reptiles. Plants also employ this mechanism through CAM physiology.

E. Underground photosynthesis.



Archbold Biological Station sits on the Lake Wales Ridge and holds the last remaining patches of Florida Scrub. This habitat is home to many rare, endangered and unusual species of plants and animals. This part of the ridge is about 1.2 myo. Preservation of such habitat islands requires the maintenance of "buffer zones" around the fringe where agriculture and development are not permitted. Inset (a) shows flowers of Utricularia subulata L (flowers are cleistogamous). which fixes carbon dioxide via photosynthesis below the surface of the ground. Strong light is filtered through quartz sand and gas exchange occurs in the "roots". This species is also carnivorous via underground bladders that trap nematodes and very small insects. Inset (b) shows the chloroplasts in the epidermis of the rhizoids.

F. C₄ and CAM physiology in plants.

Adaptive Variations of Photosynthesis: C₃, C₄ & CAM

I. C₃

II. C₄

C₄ plants have spatial separation of the C₄ and C₃ pathways of carbon fixation.

In the mesophyll cell, PEPase (strictly a carboxylase) can fix CO₂ and does not interact with oxygen.

The bundle sheath cell is a location with high CO₂ concentration relative to O₂ concentration. Thus there is virtually no photorespiration ( which is the competitive inhibition by oxygen for the active site on RUBISCO - called "respiration" because CO₂ is produced).

PEPase is more active at higher temperatures than is RUBISCO. C4 plants tend to have high water-use efficiency and occur in warm environments. CAM plants, which employ a version of C4 metabolism, are better under true desert conditions. C4 plants are common in grasslands.

III. CAM

Crassulacean acid metabolism plants have a temporal separation of C₄ and C₃ pathways of carbon fixation.

At night, stomata are open and carbon dioxide is fixed using PEPase and stored in malate (malic acid)

During the day, when the stomata are closed and water loss is minimized, malate is decarboxylated and RUBISCO fixes the carbon via the Calvin Cycle.

Although oxygen may be present in the mesophyll during the day, photorespiration does not occur because of the high concentraton of CO₂.

Classic CAM plants. Saguaro Cacti (Carnegiea gigantea) in Sonora.

This is a Welwitschia growing in the Namib desert of South Africa. It has only two strap-like
leaves (highly dissected by wind in this photo) and gets all of its water from fog. It is a
Gymnosperm and exhibits C₃-CAM intermediate metabolism.

IV. Evolution of the C₄ pathway (Extra credit question)

Although clearly adaptive in hot, dry environments, note that both CAM and C₄ metabolism have extra ATP costs associated with the additional parts of carbon fixation associated with PEPase.

Question: Did C₄ metabolism evolve in response to drought and temperature stress, or is it primarily an adaptation to avoid photorespiration in an environment with a high concentration of oxygen? Note that the C₄ pathway has evolved independently in a number of different, taxonomically unrelated plant families.



The C₄ pathway works best at higher temperatures, but C₃ plants are vulnerable to photorespiration.

In the presence of present day atmospheric concentrations of oxygen (approx. 21%) and carbon dioxide (.03%), oxygen can outcompete carbon dioxide at the active site on RUBISCO. This results in a process known as photorespiration. So, what has been selected for in the evolutiion of C₄? Tolerance for high temperatures, or avoidance of photorespiration?

Question: What is a "Pre-adaptation"?