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The term ‘ecology’ in 16 different languages overlaid on the oil on board ‘The Tower of Babel’ by Flemish Renaissance painter Pieter Bruegel the Elder (1563).

In his song ‘Balada de Babel’, the Spanish artist Luis Eduardo Aute sings several lyrics in unison with the same melody. The effect is a wonderful mess. This is what the scientific literature sounds like when authors generate synonymies (equivalent meaning) and polysemies (multiple meanings), or coin terms to show a point of view. In our recent paper published in Oecologia, we illustrate this problem with regard to ‘density dependence’: a key ecological concept. While the biblical reference is somewhat galling to our atheist dispositions, the analogy is certainly appropriate.

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A giant shoal of herring zigzagging in response to a predator; a swarm of social bees tending the multitudinous offspring of their queen; a dense pine forest depriving its own seedlings from light; an over-harvested population of lobsters where individuals can hardly find reproductive mates; pioneering strands of a seaweed colonising a foreign sea after a transoceanic trip attached to the hulk of boat; respiratory parasites spreading in a herd of caribou; or malaria protozoans making their way between mosquitoes and humans – these are all examples of population processes that operate under a density check. The number of individuals within those groups of organisms determines their chances for reproduction, survival or dispersal, which we (ecologists) measure as ‘demographic rates’ (e.g., number of births per mother, number of deaths between consecutive years, or number of immigrants per hectare).

In ecology, the causal relationship between the size of a population and a demographic rate is known as ‘density dependence’ (DD hereafter). This relationship captures the pace at which a demographic rate changes as population size varies in time and/or space. We use DD measurements to infer the operation of social and trophic interactions (cannibalism, competition, cooperation, disease, herbivory, mutualism, parasitism, parasitoidism, predation, reproductive behaviour and the like) between individuals within a population^1,2, because the intensity of these interactions varies with population size. Thus, as a population of caribou expands, respiratory parasites will have an easier job to disperse from one animal to another. As the booming parasites breed, increased infestations will kill the weakest caribou or reduce the fertility of females investing too much energy to counteract the infection (yes, immunity is energetically costly, which is why you get sick when you are run down). In turn, as the caribou population decreases, so does the population of parasites³. In cybernetics, such a toing-and-froing is known as ‘feedback’ (a system that controls itself, like a thermostat controls the temperature of a room) – a ‘density feedback’ (Figure 1) is the kind we are highlighting here.

Figure 1 – Three examples of density feedback

	(a) Spanish imperial eagle (Aquila adalberti) from Mediterranean scrubland (Doñana National Park) recovered from long-term poaching in the 1950s. As the population expanded by the mid-1970s, competition for decreasing high-quality nesting sites reduced fertility (compensatory density feedback). The population experienced stability at ~15-16 pairs in the 1970s and 1980s, but adult mortality increased in the 1990s. As a result, increased matings involving less-fertile juvenile mates decreased reproductive rates (depensatory feedback)27. Photo V. Penteriani.
	(b) Land transformation (agriculture, roads) confined Good’s banksia (Banksia goodii) to 16 known populations in Albany by the 1990s. Smaller patches had lower fertility (depensatory feedback) likely because of inbreeding failure and reduced visits by native pollinators (honey possums, honeyeaters)28. Photo B. Lamont.
	(c) Yellow-tailed damselfish (Dascyllus flavicaudus) use corals for shelter in Moorea (French Polynesia). Holbrook and Schmitt29 transplanted coral heads at two fish densities with and without protection (nets) from predatory fish. Mortality increased competition for coral shelter from low to high fish density (compensatory density feedback). Photo M. Holbrook-Schmitt.

Because the magnitude with which individuals are eaten by predators or compete for food, space or other resource (along with other factors such as climate, genetics or life history) determines how fast a population grows or declines, density-dependent relationships have wide applications in ecosystem management and conservation. Most of these are apparent at the highest and lowest ends of the spectrum of population abundances. At high numbers, if a fraction of a population dies off naturally due to limited food resources, killing the surplus of individuals should theoretically have a minor impact on a target population’s growth rate, and estimates of that surplus (= quotas) can guide strategies of predator protection, hunting⁴ and fishery limits⁵. At low numbers, measuring minimum populations sizes at which deaths outnumber births can be critical to establish a species’ conservation status, protected areas, harvest moratoria, predator releases for pest control or invasion thresholds^2,6. This link between density feedback and population persistence and extinction has made the concept prominent in important fields such as conservation biology⁷, biological control⁸ or fishery management⁵.

Terminological caveats

To ground their views in their publications, scientists use words and mathematical expressions; but count the number of words and equations in any publication, words always win! Unfortunately, when we use words in a style subject to no real rules (apart from grammatical, although science writing is increasingly fraught with terrible grammar), the odds for distorting the ecological vocabulary are fairly high. Indeed, the outcome of the last 100 years of demographic research is an impressive collection of more than 60 different terms to name DD relationships!

From the 1950s to recent times, experts have strived to tidy up this ever-growing jargon^9,10. The epic of the task was immortalised by George Varley¹⁰ who stated in 1958 that “biologists do not apply the term ‘chromosome’ to any coloured body”. The situation has provoked numerous confrontations in the specialised literature (much of which is indigestible for the average ecologist), and has consequently impacted communication among ecologists within and across taxa and disciplines. Herein we summarise the causes and consequences of terminological inconsistency of DD – which we fully elaborate in our article in Oecologia.

We detected 4 scenarios causing proliferation of jargon, as follows.

‘Capsicum’ and ‘bell pepper’ are the same thing (synonymy)

The effect of increasing population size on a demographic rate can either enhance or arrest population growth. Therefore, we essentially need two terms (not 60!) to define both types of relationship. Unfortunately, different authors have given different names to those two relationships, because they believed their terms were better than existing ones, or because they were unaware that the concept’s key terms had already been coined elsewhere. This situation partly reflects the problem that many scientists work secluded in their specialised areas of expertise.

The first DD terms for cases where population size arrests population growth were by the American entomologist Harry Smith¹¹, who referred to ‘density-dependent mortality factors’ where predators kill more individuals of an insect pest as the pest expands; and by the Japanese botanists Kichiro Shinozaki and Tatuo Kira¹², who coined ‘self-thinning’ where, as trees planted in an area of land grow in biomass, individuals end up competing for resources (light, nutrients) and some gradually die as a result. Thereafter, other authors created conceptually similar terms like: ‘centripetality’ (in the field of wildlife management), ‘compensation’ (botany, entomology, fisheries), ‘direct DD’ (protozoology), ‘disoperation’ (social biology), ‘intensity dependence’ (parasitology), ‘negative DD’ (genetics) or ‘negative feedback’ (systems theory).

The American social biologist Warder Allee¹³ branded the first DD terms for cases where population size boosts population growth. He referred to ‘inverse density-dependent factors’ where cultivated protozoans benefitted from cooperative interactions as the group grew in members; and by the Canadian fisheries biologist Ferris Neave¹⁴, who defined ‘depensatory mortality factors’ (Neave actually invented the term ‘depensatory’) where, for juvenile salmon migrating from their native river to the sea, the more compact the school of juveniles, the fewer the losses to predators. Likewise, other authors created synonyms like ‘cooperation’ (social biology), ‘positive DD’ (genetics), ‘underpopulation’ (entomology) or ‘positive feedback’ (systems theory).

‘Pear’ also means ‘banana’ (polysemy)

Researchers have re-invented the definition of existing DD terms, indicating that they did not read or take into consideration the foundational literature where the terms were originally coined and defined. This problem fits a general trend of neglect of older literature in which many hypotheses and theories of our modern science were laid out many decades ago¹⁵. With regard to DD, three terms have become intensively polysemous, namely ‘negative’, ’positive’ and ‘direct’.

A population can decline if an increase in population size causes an increase in mortality and emigration (positive relationship) and/or a decrease in fertility, survival and immigration (negative relationship). What is important here is that statistical relationships of different sign (positive or negative) contribute to the same effect on the population change (decline). The British geneticist Jack Haldane¹⁶ referred to ‘positive’ and ‘negative’ DD as any relationship between population size and a demographic rate that contributes to population boom or decline, respectively. The terminological confusion has emerged when ecologists have named the sign of the statistical relationships, but not the density effect on population change. For instance, if an increase in the number of limpets on a rock over summer causes increased mortality due to competition for space (positive correlation), many would call that ‘positive’ DD, but the effect is population decline, i.e., ‘negative’ DD according to Haldane’s terminology.

A different situation has occurred with the term ‘direct’ (in maths, ‘direct’ is, by definition, a positive relationship between any two variables) as opposed to ‘inverse’ (a negative relationship) DD. Allee coined those terms to differentiate negative and positive correlations between population size and mortality. Thereafter, the two terms have suffered two severe modifications. First, ecologists expanded their use to name effects rather than statistical relationships (i.e., ‘direct’ for DD [on any type of demographic rate] whereby higher densities leads to reduced population growth rate, and ‘inverse’ for cases where density increases lead to increasing population growth rates). Second, disregarding Allee’s foundational use, many authors now mean ‘immediate’ to refer to ‘direct’ DD for density feedback measured between two consecutive sampling times (e.g., eagles, cats, snakes and many other predators feed intensely on a population boom of a grassland  rodent, so ironically only a few rodents are left to reproduce next year), as opposed to ‘delayed’ DD over more than two sampling times (e.g., the booming rodent lives on an island with one fox species [which has longer generation time than the rodent] as its only predator, so it might take several years until the predator population increases enough to reduce rodent numbers).

Modifying the letters in ‘apple’ to spell ‘leppa’ or ‘ppale’ does not equate to the original meaning (inflation)

Most ecologists would agree with DD being defined as “…a dependence of per capita population growth rate on present and/or past population densities”¹⁷. However, behind such a simple definition lies an enormous body of controversial research that (in simple terms) has contrasted the demographic roles of biotic interactions (as inferred from DD) versus abiotic factors like climate. The topic would deserve an entire dissertation (which we summarise in our Oecologia paper to stress that ‘density dependence’ does not mean ‘population regulation’, and that much semantic and terminological inflation has originated from authors emphasising population change in time versus space). The point at issue is that, to explain their personal views, debating authors have created a battery of new terms with a strong philosophical flavour, such as ‘ineffective’, ‘explicit’, ‘phenomenological’, ‘weak’, ‘Nicholsonian’ or ‘classical’ DD. We believe that these controversies, and the resulting jargon, have impeded, rather than progressed, ecology. In particular, if we accept those terms created to distinguish DD that can be detected statistically and DD that truly underpins a demographic process, then we should be ready to do the same with any other statistical relationships with potential biological significance, e.g., is there statistical and causal pollination, or global warming, etc.? The distinction relates to statistical reporting and inferences rather than to terms and concepts.

‘Golden’ and ‘Red Delicious’ differentiate types of ‘apple’ (refinement)

As we progress in our understanding of how nature works, new concepts and new terms to name them are genuinely needed. For instance, the concept/term ‘Allee effect’ represents a particular case of ‘inverse’ DD¹³, only at low population numbers. In the last two decades, ecologists have refined our understanding of the measurement and meaning of Allee effects, hence producing new qualifiers like ‘dormant’, ‘multiple’, ‘non-additive’ or ‘strong’ – indeed, 17 terms are defined by Berec et al.¹⁸. ‘Allee effects’ stand for mechanisms only activated as populations decline to near extinction (e.g., by over-harvest or the starting point of a recently established invader). Those mechanisms are, for instance, that individuals cannot find conspecifics (too few to find over a large area) of the same sex (too many males for too few females, or vice versa), the dismantling of cooperative interactions (e.g., hunting or offspring rearing becoming inefficient as group size shrinks) or inbreeding depression (reduced fitness through genetic similarity). The magnitude of the former mechanisms is magnified by further population declines into a vortex of extinction. Obviously, this concept has enormous importance in biodiversity conservation and management^2,6.

Some consequences

It goes without saying that the messy triplet (synonymy, polysemy, terminological inflation) is a dominant feature of the ecological literature. This triplet becomes apparent when experts publish reviews of the history, evolution and involution of particular terms, e.g., ‘habitat’, ‘niche’ or ‘carrying capacity’, or one is at a conference where two speakers (apparently) disagree or talk about different topics because they are using a different lexicon.

Terminological inconsistency is indeed a serious problem at different levels:

• Terminology through intellectual dispute reflects, not concepts, but schools of thoughts; yet terminology driven by opinion rather than empirical/theoretical facts contributes little to scientific progress, as illustrated by the long-standing debate around population regulation¹⁹
• Poor terminological standards trouble students and early-career researchers trying to understand and apply concepts on which the very experts disagree²⁰ – the legacy of individual authors also relies on how understandable their published work is to the younger (but future) generation of scientists. I (Corey) remember as a lowly MSc student that I couldn’t quite get my head around the difference between ‘regulation’ and ‘limitation’, for exactly these reasons! I (Salva) spent hours of at the beginning of my PhD in search of a (non-existent) density-independent regulation in opposition to the common expression “density-dependent regulation”.
• A regular activity of any researcher is to browse databases for papers (SCI, ASFAS, Scopus), and we all be familiar with searches by key-word that yield hundreds to thousands of papers, many of which are not relevant to our target query
• More generally, English is taken as the rule (certainly the international one) for scientific communication, but many researchers do not comprehend, or have access to appropriate training in English – it is not surprising that publication rates across countries can be strongly driven by language²¹ (well, if you are English-speaking, try to write a paper in Italian or French, even if you are lucky to have funds for a translation). Certainly, the understanding and expression of scientific information by non-English speakers is seriously jeopardized by inconsistent terms – even the translation of specialised treatises or textbooks can be problematic because translation relies on context rather than terms – and… how do we translate a term created in English into Spanish or Arabic, or vice versa?
• The implementation of environmental policies across transnational jurisdictions can be challenged when country-based terminological frameworks conflict; for instance, Dauvin et al.²² satirised that we need ‘mental gymnastics’ to classify marine habitats according to the European Habitat’s Directive, in which terms and definitions reflect the rival English and French schools of thought, e.g., about what a habitat or ecotone means
• Finally, ecologists are increasingly interacting with society through policy makers, management and conservation planners and the media²³; therein, scientific discourse becomes a tool of communication with non-scientists, and clear terminology is instrumental to important matters like funding applications, and conveyance of scientific information for societal benefit

Controlled terminology is a reflection of scientific maturity

Ecologists use terminology the way they do because the editors of journals and books are mostly concerned that authors use terms that are understandable within the context of single publications (disciplines). Even if review journals (e.g., Trends in Ecology and Evolution) encourage glossaries of terms, authors are given freedom to make up their own definitions – change but one word and the entire meaning of a concept can change considerably.

Now, most of the DD terms we revise in our review paper can indeed be understood within individual publications, but is that enough? We don’t think so. Regulated terminology (excuse the pun) is taken as a logical necessity in fields such as astronomy, biochemistry, medicine and taxonomy, because unique names for a star, molecule, heart disease or species are critical for application, sharing and review of existing knowledge, and for avoiding redundant research. Terminology merits due recognition because it is the basis of the classification of knowledge, and so indicates the state of progress and maturation of any science. A person can be the smartest scientist around, but without a clear command of language to communicate his/her ideas, that intelligence is wasted.

Ecological journals could improve terminological standards through permanent sections on terminological review, as well as guidelines whereby authors were obliged to authorise foundational definition of terms in their papers. Yet, neither terminological reviews nor editorial guidelines are panacea to solve the Ecological Tower of Babel, because reviews are subject to readership rates (so they can go unnoticed to many), and because researchers are in no way bound to terminological rules proposed by their peers. Terminology represents one of those matters about which many voices complain but see no solution.

The establishment of regulatory rules for ecological terminology once attempted by the Ecological Society of America²⁴ is condemned to be an unpopular idea for many scientists. In a publication in preparation, we will argue that the creation of a ‘Code of Ecological Nomenclature’ – one that is endorsed by journals as a pre-requisite for manuscript acceptance – is the key for improving terminological standards and enforcing efficient communication in ecology.  For the time being, we outline in Boxes 1 and 2 a few suggestions to prevent terminological confusion when writing a scientific manuscript, in particular, on density feedback.

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Salvador Herrando-Pérez & CJA Bradshaw

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References

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