Integrative and Comparative Biology Advance Access originally published online on October 20, 2006
Integrative and Comparative Biology 2006 46(6):1169-1190; doi:10.1093/icb/icl052
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Condition indices for conservation: new uses for evolving tools
* Department of Biology, University of Massachusetts Boston 100 Morrissey Blvd., Boston MA 02125-3393, USA
Department of Biology, Tufts University Medford, MA 02155, USA
Correspondence: 1E-mail: robert.stevenson{at}umb.edu
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Biologists have developed a wide range of morphological, biochemical and physiological metrics to assess the health and, in particular, the energetic status of individual animals. These metrics originated to quantify aspects of human health, but have also proven useful to address questions in life history, ecology and resource management of game and commercial animals. We review the application of condition indices (CI) for conservation studies and focus on measures that quantify fat reserves, known to be critical for energetically challenging activities such as migration, reproduction and survival during periods of scarcity. Standard methods score fat content, or rely on a ratio of body mass rationalized by some measure of size, usually a linear dimension such as wing length or total body length. Higher numerical values of these indices are interpreted to mean an animal has greater energy reserves. Such CIs can provide predictive information about habitat quality and reproductive output, which in turn can help managers with conservation assessments and policies. We review the issues about the methods and metrics of measurement and describe the linkage of CIs to measures of body shape. Debates in the literature about the best statistical methods to use in computing and comparing CIs remain unresolved. Next, we comment on the diversity of methods used to measure body composition and the diversity of physiological models that compute body composition and CIs. The underlying physiological regulatory systems that govern the allocation of energy and nutrients among compartments and processes within the body are poorly understood, especially for field situations, and await basic data from additional laboratory studies and advanced measurement systems including telemetry. For now, standard physiological CIs can provide supporting evidence and mechanistic linkages for population studies that have traditionally been the focus of conservation biology. Physiologists can provide guidance for the field application of conditions indices with validation studies and development of new instruments.
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Introduction |
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SynopsisIntroductionHistorical perspective on...Use of condition indices...Evolving approaches to the...Summary commentsChallengesReferences |
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A fundamental goal of conservation biology is to ensure the long-term survival of species (Meffe and Carroll 1997
; Hunter 2001; Primack 2006). Traditionally, conservation biologists have approached species health at the population level. They use tools such as population viability analysis to ascertain whether populations that make up a species are increasing, approximately stable or decreasing over time (Beissinger and McCullough 2002). If the populations are widely distributed and stable, conservation biologists conclude the species is not at risk, whereas if there are a few isolated populations or if the populations are declining, then the risk of extinction is concluded to be more immediate. Changes in populations can result from a great many causes. In the short term, across the range of a species, there are likely to be locations where populations are increasing, stable or decreasing. These changes can be driven by natural factors such as climatic events, population cycles or interspecific interactions. Over the long term, centrally located populations are generally more productive than populations at the edge of a species' range. The source and sink model (Pullium 1988) posits a net flow of individuals from higher quality, centrally located areas to the peripheral areas of the range. Species may also be impacted by human-related factors such as over harvesting, habitat loss or toxic substances (Soulé and Orians 2001). In such cases populations fail to reproduce, ranges shrink and populations go extinct. Scientists have now documented extinctions of populations and species on a global scale (Meffe and Carroll 1997; Hunter 2001; Primack 2006). Attempts to dissect population changes depend on understanding the mechanistic basis of reproduction and survival. A population flourishes or wanes based on the health of its individuals. Condition indices (CIs) are used to quantify individual health. In addition to ecological studies, conditions indices are widely used in the study of human health and, less often, in animal husbandry.
We begin this paper with a brief historical perspective of CIs emphasizing the body mass index and Fulton's index. We then review the wide range of other morphological metrics and outline other metrics that have been used to quantify body condition. Most often scientists are trying to measure the amount of energy reserves stored as fat. The next section discusses the broad uses of CIs in conservation and field biology. We present four case studies of the use of CIs for conservation purposes. Next, we review the methodological problems associated with CIs. These problems are based on a general absence of standards, statistical complications and the lack of an underlying framework to model changes in body condition. We contrast "cargo" or structural with dynamic models for studying changes over time. These models can compute CIs directly. Physiologists can advance the cause of conservation biology by validating these indices, building models that compute CIs and developing instrumentation for field use.
A word of caution is in order for the reader. This overview draws on literature from an unusually diverse range of disciplines, including human health, fisheries and wildlife management, animal husbandry, behavioral ecology, toxicology, and environmental physiology. Electronic versions of journals and tools such as Google Scholar have greatly enhanced our ability to find and obtain access to papers and the gray literature; inevitably there will be novel ideas and important papers that have been overlooked. Indeed the data presented by Brown (1996) and García-Berthou (2001) support our experience that the literature on CIs is very large. Despite its limitations, we hope this paper illustrates how physiological ideas, specifically the concept of body CIs, will further the development of physiological ecology and conservation biology.
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Historical perspective on condition indices |
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Body mass index (BMI)
More than 150 years ago, Quételet, a Belgian scientist and mathematician, proposed the body mass index (BMI) to quantify the physical condition of humans (Jelliffe and Jelliffe 1979
; Wikipedia 2006). This index is computed as body mass (kg) divided by the square of height (meters). The BMI for a normal body condition ranges between 18.5 and 25 (CDC 2006). Lower scores indicate a person is underweight (for example, Ferron and others 1997 for anorexia and bulimia) and higher scores suggest a person is overweight. Garrow and Webster (1985) concluded that BMI is a reliable measure of obesity. It is certainly much used; a search of NIH's PubMed database using the phrase "Body Mass Index" returned almost 50,000 references. However, subsequent studies (Gallagher and others 1996; Daniels and others 1997; Prentice and Jebb 2001) have pointed out limitations to the use of BMI. Specifically, they noted that when body fat is estimated with more sophisticated techniques (see Table 4), BMI can vary with age, sex or racial group. Notice also that the dimensions of BMI are mass divided by length squared making BMI dependent on size even for isometric changes in size. Alternatives for quantifying obesity exist [for example, the waist to hip ratio, the ponderal or Khosla–Lowe Index (M H–3) or the geometric model of Bagust and Walley (2000)]. Nonetheless, BMI remains popular for medical studies. In 2005 alone, over 6700 papers, about 1% of all the papers listed in NIH's PubMed database for the year, reference BMI. While not precise, the literature suggests that BMI is popular because it is an easy and inexpensive method to quantify the amount of body fat and because the data to calculate it are collected during routine examinations (Gallagher and others 2000). Furthermore, it was the standard adopted by the World Health Organization (de Onis and Habicht 1996) and remains so today (CDC 2006).
Fulton's condition factor
Fulton's condition factor (K) for fish is another example of a popular metric that has been used for a long period (Fulton 1904; Bolger and Connolly 1989). K is computed as body mass divided by the cube of body length. A multiplier may be included depending on the units of measurement (that is, a multiplier of 1000 is used when mass is measured in grams and length in mm, which gives K as kg m–3). Another multiplier may be included as a way to present the index as a whole number rather than a fraction. The calculation of K assumes isometric growth because length is raised to the 3rd power. Unlike BMI that is applied just to one species of mammal—humans—Fulton's condition factor has been applied to many species of fish. The assumption of isometric growth is a fair approximation for many species (Jones and others 1999; Bister and others 2000; Kimmer and others 2005), but not all. A variety of other metrics have been proposed that provide useful alternatives to the isometric assumption (see next section) but Fulton's condition factor continues to be widely used because of its simplicity and historical precedence.
Other morphological condition indices for fish
Le Cren (1951) and Ricker (1973, 1975) expanded on the notion of Fulton's condition factor by proposing the model Mass = a Lengthb, where both a and b are empirically determined by regression. Relative condition, Kn, is then computed as the observed mass of a specific individual divided by the mass predicted from equations for the population or species under study. The exponent b can be more or less than 3, meaning that fish become more or less rotund at larger sizes.
Wege and Anderson (1978) suggest a third index called relative mass, Wr (Brown and Murphy 1991; Murphy and others 1991). Wr is computed by dividing the measured mass by the computed mass (Ws) of a species-specific "standard fish." Bister and others (2000) described a procedure to establish the relationship of standard mass to body length. It requires using the regression-line-percentile (RLP) technique based on a large number of populations (>50 are recommended), removing individual outliers or population outliers and any other data suspected to have resulted from measurement errors, and establishing ranges of lengths for which the standard mass calculation is statistically valid. Gerow and others (2005) published a new statistical approach that overcomes biases of RLP. Hansen and Nate (2005), using a large dataset based on 640 surveys of walleye fish in Wisconsin, found a length-related bias for Ws for fish measured from January to April but not from other seasons.
More recently, Jones and others (1999) suggested a more general model in which body mass W = 
LaLbLc. symbolizes density, and L raised to the a, b and c powers represents three different linear dimensions. The exponents a, b and c are suggested to be independent of fish size. In practice, Jones and others (1999) used just two independent dimensions, girth and length. Their model reduced to W = BL2H where B is a coefficient determined by regression, L is length and H is height.
Bolger and Connolly (1989), Brown and Murphy (1991), Cone (1989), Patterson (1992), Jones and others (1999) and Blackwell and others (2000) provided useful comments about the three indices and their computation. Blackwell and others (2000) comment on two additional methods used in fisheries: direct comparison of regression lines appropriate for comparing populations and the use of residual analysis. Among governmental researchers the use of relative mass seems to be increasingly favored (Blackwell and others 2000). Having community-wide standards helps managers (Bonar and Hulbert 2002; Murphy and others 1991). Recently, Hansen and Nate (2005) suggested calculating body condition as the product of Ws and a seasonally calculated Kn.
Morphological condition indices for vertebrates
As Hayes and Shonkwiler (2001) noted in their very useful review of CIs, most published examples other than those from humans are of studies of fish, followed by those of birds. Our impression is that fish are more often studied in an applied context while birds are more commonly the focus of basic ecological research. Among vertebrates, however, amphibians are the most endangered group (Stuart and others 2004), so we thought it useful to provide examples of specific metrics that have been used across various vertebrate taxa (Table 1). Only instances in which we found examples of the same index being applied to more than 1 taxon are included. We found the overview papers listed in the first column in Table 1 to be very useful as introductions to methods and practices within each taxon.
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Perhaps the most surprising result from our survey of indices (Table 1) is that BMI, the most commonly applied metric for humans, is rarely, if ever, applied to animals. A second noteworthy observation is the diversity of the measures. They range from categorical scoring systems to advanced multivariate statistical techniques. In addition, we found that scientists rarely cited literature from other taxa but seemed to follow traditions within their taxonomic discipline or to invent a new metric that satisfied a current need.
Beyond morphological condition indices
Scientists have expanded the kinds of measurements they make to quantify condition beyond morphological approaches. In addition to external assessments based on photographs, physical examinations and measurements of mass and length, biologists examine internal organs and measure their dimensions, take fecal, blood, or tissue samples, or measure body composition directly (Table 2, Barton and others 2002; Hõrak and others 2002; Kalmbach and others 2004). Fecal, blood or tissue samples are obtained in the field but analysis is conducted in the laboratory. These samples are useful for conservation studies because they provide information about the endocrine and immune systems as well as about the state of energy reserves. The RNA/DNA ratio is a particularly interesting metric because it allows one to make inferences about rates of growth (changes in body mass over time) rather than just getting a snapshot of the components of body mass.
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Today more efforts are being made to compare CIs involving different levels of biological organization. For instance, scientists want to know whether blood chemistry and hormonal status are correlated with standard measures of body condition (see Galapagos marine iguana example below). While cellular and molecular CI are more expensive to obtain than are those based on physical measurements, they provide information about how subsystems of the body are functioning. Advances in science often depend on the weight of the evidence, so we think it is important to encourage complementing traditional CIs with cellular and molecular CIs when the appropriate samples can be collected.
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Use of condition indices in conservation |
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Condition indices have been used in a wide variety of contexts in conservation and environmental biology (Table 3). Some studies relate CIs to the primary drivers of environmental degradation such as habitat loss, pollution, overharvesting and climatic change. Other studies relate CIs to life history patterns (reproduction, juvenile survival and migration) and ecological interactions (parasite load, social dominance, diet and density) of threatened or endangered species. To illustrate in greater depth the diversity of uses and indices, we present four case studies focusing on Galapagos marine iguanas, desert tortoises, polar bears and caribou. These examples are all of vertebrates from environments in which there are large seasonal fluctuations in resources and in which scientists can detect changes in body condition at the population level.
Marine iguanas
Galapagos marine iguanas (Amblyrhynchus cristatus) offer an unusually complete example of an organism that has been studied under both natural and human-induced stressors, with both dimensionally based (Romero and Wikelski 2001) and hormonally based (Romero and Wikelski 2001; Romero and Wikelski 2002a; Romero and Wikelski 2002b) indicators of condition linked to fitness as measured by survival. The presence of marine iguanas on more than one island in the Galapagos, together with what can be very different conditions between islands and between years, have provided both treatments and controls in these studies.
The iguanas feed on marine algae, which can be in short supply during El Niño events; during these events, both dimensional and hormonal CIs are good predictors of fitness (Romero and Wikelski 2001). La Niña events are associated with abundant food, and serve as a control. During an El Niño event, there was high mortality associated both with a simple dimensional index (body mass/snout-vent length3) and with corticosterone levels (Romero and Wikelski 2001).
Human activity can cause increases in glucocorticoid concentrations in species of interest to conservation (for example, Wasser and others 1997). In the case of Galapagos marine iguanas, in which glucocorticoid levels have been linked directly to fitness (Romero and Wikelski 2001), such assays have a particularly strong relevance to conservation. For example, when an oil tanker broke up and exposed one island to low-level contamination while not affecting another island, iguanas on the affected island had a strong stress response as indicated by elevated plasma corticosterone levels. Based on stress responses measured in starving iguanas during an El Nino event, Romero and Wikelski (2002b) predicted mortality rates of 40% on the oil-impacted island; by the following season, actual mortality was 62%. This result underscores the value of glucocorticoid information, which can be obtained rather quickly after the onset of a human-induced impact and can serve as a long-term predictor of the consequences.
One potential value of such studies lies in their ability to provide information about which human activities do not reduce survival, thereby preventing misplaced or ineffective conservation practices. It is welcome news for wildlife managers that individuals in areas heavily exposed to tourism did not show chronic stress (Romero and Wikelski 2002a). This was tempered, however, by the finding that acute stress was lower than for iguanas in areas not visited by tourists (Romero and Wikelski 2002a), thus reducing the potential benefits of this response in the wild.
Desert tortoises
The desert tortoise (Gopherus agassizii), found in the western deserts of the United States (Nevada, California), is an endangered species (see Tracy and others 2005, Tracy and others this volume). This long-lived, slowly reproducing species is sensitive to disturbance by humans and to habitat destruction. For about 15 years now, state and federal agencies have supported research directed toward understanding its biology and to devising management plans. Like other desert reptiles, these tortoises have evolved mechanisms allowing them to endure long periods of time without water and food. They have the ability to store from 30 to 50% of their body mass as urine in their bladders. As herbivores they can also have large amounts of food in their digestive systems.
As a way to assess conditions in the field, Nagy and others (2002) devised a CI based on body mass divided by product of the length, width and height of the shell. Using grams and centimeters as units of measure, the index gives a ratio in units of g cm–3, familiar to most because water has a density of 1 g cm–3. The highest values of the index found in the field averaged 0.64. This fraction is to be expected because the dome-shape of a tortoise does not fill the rectangular prism described by the product of the three linear shell dimensions. Nagy and others (2002) demonstrated that body condition varies with season and among populations but is largely independent of age. They believed the CI to be a good first approximation of condition and hydration rates in the field.
Polar bears
Humphries and others (2004) reviewed the impact of climatic change on arctic mammals. They predicted the disappearance of current species and the emergence of new species as the direct result of, and as indirect effects through, the cascade of interactions in the trophic structure. Currently, species go through several seasonal bottlenecks in availability of energy and have complex seasonal patterns of movement and feeding related to energy demands.
Polar bears (Ursus maritimus) face significant challenges to their survival as a species. In addition to the accumulation of organophosphates in fat (Anderson and others 2001) that act as endrocrine disruptors (Braathen and others 2004), climatic change is affecting their feeding behavior (Derocher and others 2004). The bear's vulnerability is tied to its role as a top predator and its need to accumulate large energy stores during relatively brief hunting seasons. Amstrup and others (2006) reported the first observations of cannibalism in polar bears, which they suggest is the result of poor nutritional status. In late 2005, news reports noted that polar bears, for the first time, were found dead, floating in the ocean 20–60 km offshore (Carlton 2005). These bears are strong swimmers but it is speculated that a lack of sea ice for hunting or resting, perhaps combined with poor energy reserves, caused them to drown. Petitions from conservation groups to list U. maritimus as a threatened species are currently being considered by the United States government.
Almost 15 years ago, Stirling and Derocher (1993) predicted that global warming would increase the duration of ice-free periods and cause a decline in body condition, reproductive rates and survival of polar bear cubs. A series of subsequent studies have documented relationships among feeding biology, energetics, physiological condition and reproduction. The ratio between body fat and lean body mass (Atkinson and Ramsay 1995) and the log of body mass divided by the log of body length (Cattet and others 2002) can indicate physiological condition. During the course of an annual cycle, a polar bear's mass can vary from 200 to 400 kg (Atkinson and Ramsay 1995). Most gains in body mass come in the form of fat derived from hunting seals on the ice. During summer the ocean is ice-free and the bears must fast. During winter hibernation, they fast again. Female reproductive success is tied to the amount of fat stores (Atkinson and Ramsay 1995).
Caribou
Caribou (Rangifer tarandus) are not as threatened as polar bears. They still exist in several large herds across North America, Europe and Asia. However, the annual cycle of each herd is complex and success depends on the timing of resource availability. Recently, Heuer (2005) wrote a book documenting the dramatic life cycle of the Porcupine herd. He undertook this effort because of people's concerns about the calving grounds of the Porcupine herd that are threatened by proposals to develop the Arctic National Wildlife Refuge and offshore regions for oil extraction. Radiotelemetric studies have shown that a typical cow in this herd travels over 28,000 miles per year, traversing a range of 96,000–125,000 square miles. Systematic aerial surveys have documented long-term annual cycles in this population, which started at a low of 100,000 in 1972, peaked in 1989 at about 180,000 individuals, and then steadily declined to a low of 120,000 animals in 2001 (Douglas and others 2002).
A number of CIs have been used (Huot and Goudreault 1985; Gerhart and others 1996; Kofinas and others 2002) and scientists have established relationships between body condition and reproduction in caribou (Thomas 1982; Cameron and others 1993; Chan-McLeod and others 1999). A particularly interesting condition index, from a conservation perspective, is a categorical index of fat reserves. Because caribou are still hunted widely for subsistence, scientists (Lyver and Gunn 2004) have developed a method to enlist the community of Denesoline tribal hunters to help evaluate the health of local populations based on a score of fat reserves of freshly killed animals. The body condition index was based on a 1–4 scoring system indicating skinny, not so bad, fat and really fat. Scientists rated the depth of the fat of the brisket and back, the amount of stomach fat, the fat coverage of the kidney and the color of femur marrow. Lyver and Gunn (2004) compared the hunters' impression with this categorical index and found that both indicated that fatter females had a higher probability of being pregnant than leaner ones. This approach allows the aboriginal community and government biologists to jointly manage the caribou herd.
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Evolving approaches to the measurement and prediction of condition indices |
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Measurement techniques
Most morphological CIs are based on some combination of body mass and linear dimensions of the organism. Each of these measurements can present problems for interpretation unless investigators are familiar with the organisms under study and follow standard procedures. Consider the following three examples. Among feral mice, Krebs and Singleton (1993)
reported low repeatability in CIs because techniques for measuring length varied among observers. Fish "length" could be one of four different measurements: the distance from the nose (1) to the start of the tail (standard length), (2) to the notch in the tail (fork length), (3) to the end of the tail when the tail fin is in a relaxed position (natural total length) or (4) to the end of the tail when the tail is pulled in the lengthwise direction as far as it can go (maximum total length) (Anderson and Gutreuter 1983). For snakes and lizards, biologists often measure the snout-vent length from the nose to the cloaca or vent and the total length from the nose to the tip of the tail. These measurements are more variable than would be ideal because the animals resist being stretched out or because the ends of the tails become damaged or shed.
Which morphological index?
Morphological CIs (Table 1) fall into three categories. Some, such as mass/length or BMI, are ratios. Ratio indices give a relative number but the units are difficult to interpret. Most have dimensions that are not independent of mass or length so one assumes the ratios are likely to be correlated with size. Multipliers are often introduced to produce indices that vary between 1 and 100. Another set of CIs, Ws or residuals, represent differences from a predicted standard mass computed on the basis of a statistical formula. These indices have the dimensions of mass. To make them more meaningful, scientists sometimes standardize them by the predicted mass, yielding a number that gives a percentage difference (compare with coefficient of variation). A third set of indices is computed so as to produce a non-dimensional number. Mass is divided by density (assumed to be 1 g cm–3) to give the dimensions of volume and that result is divided by some combination of linear dimensions to yield a dimensionless number. We found few discussions of the relative merits of the biological meaning of these three types of CIs. The numbers themselves are difficult to interpret without direct experience with measuring the animals being studied. The underlying assumption in all these metrics is that body mass is a good measure of condition because size (= "structural mass") is constant or that mass is being scaled by some measure of size when the individuals vary in size. Normally the indices are based on data that are easy to measure rather than on something that has a strong justification from a physical or biological perspective. Problems arise with the scaling quantity, in part, because we have no convenient and inexpensive method of measuring body volume independent of mass.
Interestingly, the data on mass and length used for several CIs (Table 1) were also used by Kooijman (2000, p 23–29) to define shapes of organisms. His nondimensional shape factor is 
= (W/)1/3 L–1. This is mathematically equivalent to another CI (Table 1). Fulton's condition factor (K) is equal to 3 if first one divides K by body density (usually assumed to be 1 g cm–3). So, the question arises whether these CIs and Kooijman's shape factor are equivalent. The answer is "sort of." The role of CIs is to quantify the health of individuals in a population or to tell whether a population is healthy relative to other populations. Condition factors generally represent differences from some standardized "shape" that are important. Kooijman's , on the other hand, defines the shape of a species, with a goal of knowing how surface area-to-volume ratios change with body size. This comparison suggests one can view morphological CIs as individual deviates from a standardized healthy "species shape." It also draws attention to the lack of established procedure of definition of what is "healthy." In the literature on humans and the fish, large sample sizes have allowed scientists to detect differences between populations, but clearly differences from a population mean could result from underlying genetic differences as well as from physiological conditions.
Statistical considerations
First in the literature on humans (Khosla and Lowe 1967; Benn 1971; Lee 1981; Revicki and Israel 1986; Flegal 1990; Lazarus and others 1996; Mei 2002) and subsequently in that from fisheries (Bolger and Connolly 1989; Anderson and Neuman 1996) and ecology (Green 2001; Hayes and Shonkwiler 2001), scientists have raised concerns about statistical issues associated with CIs. Often they want to know if one index performs better than others relative to an independent measure of condition or if there is inherent bias. As noted previously, several CIs are ratios. Ratios can complicate analyses and are often size dependent (Lee and others 1981; Hayes and Shonkwiler 2001). Green (2001) and Hayes and Shonkwiler (2001) discussed some of the statistical errors in untransformed and log-transformed data in different types of regression models and in the use of residuals. Jakob and others (1996) suggested that residuals serve as a useful CI while García-Berthou (2001) described some of the complications introduced by using residuals. Recently, Schulte-Hostedde and others (2005) empirically tested some of the concerns raised by Hayes and Shonkwiler (2001) and Green (2001) and found their concerns unwarranted for the datasets being analyzed. As discussed above, some metrics are non-dimensional but because of allometric growth they are not independent of size. The relative condition factor aLb is inherently less biased than is mass/length, BMI or Fulton's index (Lee 1981), but Benn (1971) and Flegal (1990) state that a relative mass index is statistically unbiased over the entire size range. In the section "Other morphological CIs for fish" above, there are citations to literature that discusses statistical techniques for computing standard mass and relative mass index. Cone (1989) advocated use of straight regression techniques. We conclude that statistical approaches used for computing CIs, will continue to evolve and that this development will be supported by more rigorous experimental work such as that of Cook and others (2005).
Measurement of body composition
An important aspect of using a CI is to know that it represents something real within the body, such as a measure of the fat stores. Therefore, scientists compare morphological CIs with data on body composition. The traditional standard used for documenting body condition has been a four component molecular model of body composition (Wang and others 1992; Speakman 2001a), that is, to measure the relative amounts of water, fat, organic and inorganic matter (Reynolds and Kutz 2001). Typically, the gut contents, and often developing embryos, are dissected out and the carcass dried to a constant mass to determine water content. After grinding the carcass, fat is extracted chemically from aliquots. Finally, the remains are burned to determine the ash (= inorganic) content, with the organic content determined by subtraction. This traditional method requires that the animal be sacrificed. As a rule, conservation biologists do not want to kill their subjects, but sometimes animals can be analyzed in this way because they are already dead (for example, after from being hit by a car or killed accidentally in a trap).
Fortunately, there are many nondestructive alternatives for measuring body composition that have the inherent advantage of being able to measure the same individual repeatedly (Lukaski 1987; Davies and Cole 1995; Poskitt 1995; Piersma and Klaassen 1999; Ellis 2001; Speakman 2001b). They include relatively simple physical techniques (morphometrics, measuring skin-fold thickness with calipers, mass balance, air-displacement plethysmography and hydrostatic weighing), chemical dilution techniques (isotope dilution and gas dilution), electrical techniques (total body electrical conductivity and bioelectrical impedance) and scanning techniques (whole body counting, ultrasound scanning, dual-energy X-ray absorptiometry, computed tomography, in vivo neutron activation analysis, magnetic resonance imaging and infrared interactance) (Table 4).
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Unfortunately, the large number of alternatives reminds us that no one method is ideal. All the usual variables, the kind of data obtained, cost of the equipment, size of the organism relative to the instrument, accuracy, repeatability, training of operators, maintenance and operating costs, ethical rating, and opportunity for access to instruments, help experimentalists determine the best protocols (Garroway and Webster 1985
; Golet and Irons 1999; Ellis 2001). Body mass is made up of a number of different constituents depending on the level of biological organization (Fig. 1, Wang and others 1992). Most of the nondestructive techniques used to measure body composition, however, divide the body into just two components: fat and fat-free (Table 4). Scanning methods that image the entire body can parameterize three and four component models at the molecular level and they have the potential to provide spatial information at the tissue level. Development of these methods often depends on advancements in computer algorithms for interpreting the raw data.
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One of the most promising techniques applied to conservation was total-body electrical conductivity (TOBEC) because the instrument was portable and relatively inexpensive. A number of studies published in the 1990s used the technique, some with success but others less effectively. The technique appears to have fallen out of favor, however, because the commercial instrument is no longer available and the number of papers using the method declined greatly after 2000.
Modeling body composition change
A central feature of many physiological studies is the mechanistic approach to understanding biological processes. A number of different disciplines, including the agriculture sciences (Keele and others 1992; King 2001; de Lange and others 2003), fisheries (Iwama and Tautz 1981; Cacho 1990), physiological ecology (Cryan and Wolf 2003; Pennycuick and Battley 2003; Polishchuk and Vijverberg 2005) and behavioral ecology (Bednekoff and Houston 1994; Houston and others 1997; Brodin 2000; Thomas 2000; Stillman and others 2001; Bety and others 2003) model the physiological state of organisms. Body mass and body mass composition are usually central variables in these models, which often include specific compartments for fat, protein and water. Biophysical ecology (O'Connor and others 2006; Porter and others 2006), dynamic energy budgets (Kooijman 2000), metabolic theory of ecology (Brown and others 2004) and ecological stoichiometry (Sterner and Elser 2002; Vrede and others 2004) offer broad, mechanistic frameworks for developing models.
Using the simple "body as a machine" metaphor, biologists compare the functioning of animals with that of devices built by engineers. For instance, principles derived from the aerodynamics of airplanes and helicopters have provided insights about how birds, bats and insects fly. Models of processing for chemical factories, either continuously or by batches, have been applied to the digestive systems of animals. In contrast to the mechanical perspective, biologists have extensively documented a much more dynamic view of physiological processes in which organisms repair and modify themselves as they meet the challenges of new environments. It is now recognized, for example, that birds regulate muscle mass during migration and that snakes regrow their digestive systems after catching a prey item. While no one doubts the dynamic nature of biological systems, homeostatic mechanisms regulate body structures within narrow limits of mass, making the analogy to a human-built structure a good first approximation.
For purposes of studying body mass composition, the perspective outlined above suggests two contrasting models that represent the mechanical and dynamic perspectives. The mechanical perspective we deem the "cargo" or "structural" model, for which the underlying assumption is that the body is a fixed structure that can carry a load (Kooijman 2001). This load might be food from a meal, eggs being developed for reproduction, or fat stored for migration. This static view of the organism, while not explicitly stated, is often an underlying assumption of many CIs. In contrast, the "dynamical regulation" view assumes that body structures are constantly remade in ways that match the tasks being undertaken. Migrating birds are good examples. They reduce mass of flight muscles in accordance with their power needs as they burn fat along the migration route (Battley and others 1999; Lindstrom and others 2000; Dekinga and others 2001; Bauchinger 2005). Red knots can upregulate and downregulate the mass of their digestive systems in response to diet and to migration phase (Dekinga and others 2001; van Gils and others 2003). Snakes provide another clear example. Because most snakes so rarely eat, it is a better strategy to maintain the digestive tissues at minimal level most of the time and then rebuild the digestive system to process the meal after the prey has been swallowed (Secor and others 1994; Secor and Diamond 1995; Starck and Beese 2001; Starck and Beese 2002). Some evidence suggests that dramatic changes in organ size are accomplished by changing cell volume rather than cell number (Johnson 1973; Starck and Beese 2002), but few studies address this issue and very little is known about the control signals that regulate body mass (see Adams and others 2001).
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CIs will continue to be applied widely in ecological and conservation studies. Scientists find these simple metrics convenient for documenting differences among individuals and between populations. As yet, there is no clear consensus as to which morphological metrics are best but if sufficient data exist the relative mass, Wr seems to be preferred. We suggest that researchers consider carefully the statistical consequences of the indices they choose and the inferences that can be drawn from the data. If measurements are made at more than one level of biological organization (Table 2) such data are likely to add complementary and helpful information.
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1. Can physiologists develop guidelines as to the best CIs and statistical procedures to use? In other words, can physiologists agree on an equivalent of BMI that will work across species and provide a tool that would permit a much wider group of scientists and citizen scientists to gather data that could be shared?
Outside of fisheries research and studies of humans, there are few, if any, guidelines as to which metrics are best. Fisheries scientists have begun to establish standards and it may be that the broader community could build from their experiences. These recommendations would need to acknowledge the wide range of contexts in which CIs are used, address statistical issues and explore the relationship between CIs and shape metrics.
2. Can the scientific community compile data on body mass and body mass changes for animals in different environmental and physiological states and make it available in public databases analogous to current practices for DNA, RNA and many protein molecules?
Body mass and body mass changes are at the center of many ecophysiological interactions. Compiling information in a standard format would advance the ability to test ideas about body mass and body mass changes. Prentice and Jebb (2001) suggested this kind of compilation for humans.
3. Can physiologists invent better tools to measure body composition that are portable and require less experience to operate?
For all biologists, nondestructive methods that can be readily applied in the field will help advance the ability to quantify individual health and the relationship between individual success and species survival. Environmental and conservation physiologists can contribute to this goal by validating CIs using advanced instrumentation, comparing body CIs with a variety of other CIs that have been used.
4. Can physiologists produce a theory of body mass change based on first principles?
There are currently a variety of frameworks such as behavioral models, biophysical ecology, dynamic energy budgets, the metabolic theory of ecology and ecological stoichiometry that can provide insights into the regulation and change of body mass. These modeling paradigms provide insight and can predict CIs but as yet a clear understanding of the physiological processes and molecular circuits that regulate body mass are lacking.
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We wish to thank Celia Morris and Susan Speak for their advice about the organization and flow of the text. Cody Choate and Derek Berezdivin helped find and organize the literature. This work was supported in part by award 0344822 from the National Science Foundation.
Conflict of interest: None declared.
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From the symposium "Ecophysiology and Conservation: The Contributions of Energetics" presented at the annual meeting of the Society for Integrative and Comparative Biology, January 4–8, 2006, at Orlando, Florida.
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