Introduction

Habitat structure (HS) corresponds to the presence of physical structures in a system and is characterized by different dimensions, considering qualitative (type of structural elements, such as different kinds of rocks, vegetation and sediment fractions) and quantitative measures (number of distinct structural elements and relative or absolute abundance of them) (McCoy & Bell, 1991; Wiens, 2000; Tews et al., 2004; Tokeshi & Arakaki, 2012). A highly structured ecosystem provides a greater number of microhabitats and niches, increasing the potential persistence of populations, coexistence of competitors, as well as prey and predators, and can positively influence biodiversity (MacArthur & Levins, 1964; Wiens, 1976, 2000; Buhl-Mortensen et al., 2010). On the other hand, some studies such as Bourget et al. (1994), Feller & Mathis (1997), Kelaher (2003), and Sueiro et al. (2011) showed that biological aspects may not respond positively to the increase of HS. Reviews by McCoy & Bell (1991) and Tews et al. (2004) pointed out that one important explanation for these distinctive patterns might be the conceptual miscellany in the literature.

McCoy & Bell (1991) showed that characteristics of the HS have received different nominations (e.g., diversity, heterogeneity, complexity, topography), and most of them had a vague ecological application. Some terms are used with different definitions and applications, which is typically a consequence of the independent development of different specialties of knowledge in ecology (Pickett et al., 2007). Thus, there is a clear need to clarify the conceptual framework and facilitating communication between different specialties of knowledge.

McCoy & Bell (1991) proposed a description for HS based on three axes. The two main axes are heterogeneity and complexity, which are dependent on the third axis, the scale. Heterogeneity was defined as the relative abundance of different structural components of the environment and complexity as the absolute abundance of these components. Tokeshi & Arakaki (2012) diverged with McCoy & Bell (1991) and proposed that habitat complexity must be interpreted as encompassing different characteristics of structure, rather than referring solely to the abundance of structural components. Then, they recognized at least five traits that need to be taken into account when assessing habitat complexity (i.e., scale, diversity of elements, spatial arrangement, size, and abundance of elements). The disagreement between these two previously mentioned studies represents a problem observed in ecological literature, and the terms complexity and heterogeneity continue to be used in different ways (e.g., Bourget et al., 1994; Kelaher, 2003; Meager et al., 2011; Nunes et al., 2015).

Potential lack of clarity in the definition and implementation of concepts can mask ecological trends of the relationship between biological communities and HS (Wiens, 2000). HS has a crucial role for conservation, serving as a guideline for selection of protected areas, as well as the recovery of degraded areas (e.g., implementation of artificial reefs) (Bohnsack, 1991; Charton & Ruzafa, 1999). Therefore, misuse of concepts may lead to serious consequences in empirical context and conduct managers to wrong decisions.

From an extensive literature review, the present study performed a quantitative and qualitative analysis of the most used concepts in the context of HS in marine ecosystems and provides the current scenario of the use of these terms. The aim of this study was to investigate the disagreement in the use and empirical application of complexity and heterogeneity, and if different patterns of use of these terms would be observed in studies that investigated different marine habitats. Moreover, a conceptual clarification was also performed, taking in account the different dimensions of the concepts (Pickett & Cadenasso, 2002), in order to provide robust definitions aiming to allow comparisons of studies addressing different aspects of HS.

Materials and methods

Literature survey

A search was conducted in the ISI Web of Science platform database (considering a temporal scale of 13 years, 2003–2015) using the following keywords: habitat heterogeneity, spatial heterogeneity, habitat complexity, spatial complexity, structural heterogeneity, and structural complexity. Additionally, the search was refined according Web of Science categories: (i) Ecology, (ii) Marine Freshwater Biology, (iii) Environmental Sciences, (iv) Oceanography, (v) Biodiversity Conservation, (vi) Zoology, (vii) Fisheries, (viii) Evolutionary Biology, (ix) Behavioral Sciences, and (x) Water Resources. During the search, the following studies were not considered: (i) from freshwater and terrestrial environments, (ii) reviews, and (iii) that did not address habitat physical structure (e.g., articles that considered heterogeneity or complexity as environmental conditions as temperature, pH, and wave exposure or as stratification of water layers).

The search resulted in 181 empirical publications that used complexity and heterogeneity examining the influence of HS on marine communities (e.g., biodiversity, interaction rate between predator and prey, population oscillations) from different habitats. For each study analyzed, the following information was recorded: (i) type of marine habitat, (ii) year of publication, (iii) terms used to characterize the HS (i.e., complexity, heterogeneity or both), (iv) definition of terms (here literally registered), and (v) reference of the terms (studies cited, in the surveyed articles, as reference for the definition).

Data analysis

The use of the terms complexity and heterogeneity was analyzed and classified for all studies surveyed as: (i) complexity (only); (ii) heterogeneity (only); (iii) complexity and heterogeneity as synonymous; and (iv) complexity and heterogeneity, both used as non-synonymous. Marine physical HS studies encompass almost exclusively benthic habitats, and studies were categorized accordingly to which benthic habitat it was done: Coral reef, Rocky intertidal, Seagrass, Mussel bed/Oyster reef, Rocky subtidal, Kelps, Mangrove, Soft bottom, Macroalgae, Coastal water, Deep ocean, Salt marsh, Rhodolith bed, Laboratory experiments (Lab), and More than one habitat (MTOH) (Table 1).

Table 1 Comments about the habitat categories analyzed
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Hierarchical cluster analysis was performed (group average method) to analyze the similarity between the habitat categories based on the number of articles that use the terms in different ways (i.e., heterogeneity, complexity, heterogeneity, and complexity as synonymous, heterogeneity, and complexity as non-synonymous) and did not consider the definition of the terms. In this analysis, habitat categories that contain 90% of all sampled articles were considered (Coral reef, Rocky intertidal, Seagrass, Mussel bed/Oyster reef, Rocky subtidal, MTOH, Kelps, Soft bottom and Deep ocean), and the software PRIMER 6.0 (Clarke & Warwick, 2001) was used.

Conceptual clarification

Conceptual clarification of complexity and heterogeneity was performed with the surveyed articles that presented definitions (n = 31), following the methodology of Pickett & Cadenasso (2002). The clarification considered two conceptual dimensions: (1) the core concept, i.e., the most general definition of each concept; and (2) the model, i.e., how the concepts are operationalized in the context of the HS in marine ecosystems. The core concept is essential to understand the main meaning of the terms complexity and heterogeneity that must drive their uses in ecology to facilitate the communication between different fields of knowledge.

A survey of the terms complex, complexity, heterogeneous, and heterogeneity was conducted in two main dictionaries of English language (The Oxford and Cambridge English Dictionaries) in order to identify the most general definition of the concepts, i.e., core concepts. Additionally, to understand how the concepts are operationalized, the central ideas of the definitions were analyzed and grouped in order to build a scheme. In the present review, definitions were organized as synonymous or not, and in two kinds of classification. The first classification was: (i) multidimensional measurement, that corresponds to more than one space dimension (e.g., complexity or heterogeneity as topography, rugosity, tridimensional surface) or more than one characteristic of the HS (e.g., number, density and composition of structural elements); or (ii) unidimensional measurement, that corresponds to one characteristic of the HS (e.g., complexity as density or number of HS). The second classification was: (i) quantitative (e.g., density and/or number of distinct structural elements), (ii) qualitative (e.g., composition/type of structural elements), and iii) quali-quantitative measurements (e.g., number and composition of structural elements). Therefore, only multidimensional definitions of complexity or heterogeneity could be classified as quali-quantitative measurements. Definitions that do not fit clearly into these classifications and/or present vague ideas have been presented as unclear definitions.

Results

Uses and definitions of complexity and heterogeneity

There has been an increase in the number of publications discussing the role of HS on marine ecosystems over the last 13 years, especially using the term complexity (Fig. 1). In general, the use of complexity was the most frequent case (55.2% of all publications) compared with the other kinds of use and increased from 2003 to 2015. The second most common approach was the use of complexity and heterogeneity as synonymous (30.9%) (Fig. 1).

Fig. 1
figure 1

Number of publications documenting the use of the terms complexity and heterogeneity isolated, as synonymous and non-synonymous over time, in the context of HS in marine studies (n = 181)

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Overall, the five ecosystem categories that represented 70% of all publications (Coral reef, Rocky intertidal, Seagrass, Mussel bed/Oyster reef, Rocky subtidal, and MTOH) showed that the term complexity presented the greatest use and both terms as synonymous was the second greatest use observed, except Rocky subtidal category that the greatest use was both terms as synonymous (Fig. 2).

Fig. 2
figure 2

Percentages of publications that used the terms complexity and heterogeneity isolated, as synonymous and non-synonymous in context of HS for each marine habitat categorized (n = 181)

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Cluster analysis indicated two major groups of clustering of habitat categories considering different use of complexity and heterogeneity (Fig. 3). In the Soft bottom and Deep ocean categories (Group A), both terms were mainly used as synonymous. The second group (B), studies on all other habitats, mostly used complexity and with low occurrence of the other uses (heterogeneity, complexity, and heterogeneity as synonymous and non-synonymous). Moreover, the Group B was clustered in two subgroups: B1) Seagrass, Coral reef, and Rocky intertidal, that showed higher proportion in the use of terms as non-synonymous than B2) Rocky subtidal, Kelps, Coastal Water, MTOH, and Mussel bed/Oyster.

Fig. 3
figure 3

Cluster analysis of the number of publications considering the use of terms complexity and heterogeneity in habitat categories of the marine studies that contain 90% of all publications. A and B represent clustering groups, as well as B1 and B2 represent the subgroups clustered for group B

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Around 80% of all publications did not define the terms used to characterize the HS (Fig. 4). Mangrove and Rocky intertidal categories had the highest number of papers with definitions considering the total of publications belonging to each category (around 33% and 26%, respectively). In addition, of the 181 articles collected, 88% had no references for the definitions presented.

Fig. 4
figure 4

Number of publications surveyed that defined and not defined the terms complexity and heterogeneity in context of HS in marine studies (n = 181)

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The reference most cited by studies surveyed that defined the terms complexity and/or heterogeneity was McCoy & Bell (1991) (63% of publications with citation). Other references cited in the studies surveyed to define the terms used were Gee & Warwick (1994), Beck (2000), Loehle (2004), Dunn & Halpin (2009), Meager et al. (2011) and Tokeshi & Arakaki (2012). Beck (2000), Dunn & Halpin (2009), and Meager et al. (2011) did not present their own definitions (Table 2). Beck (2000) and Meager et al. (2011) are empirical studies that cited the definitions of complexity and heterogeneity developed by McCoy & Bell (1991). Besides, Dunn & Halpin (2009) is also empirical and did not define complexity (Table 2).

Table 2 Terms and definitions from references cited in the publications surveyed by this study
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Conceptual clarification of complexity and heterogeneity

The meanings of complex and complexity showed that the core of these concepts includes the connection between different parts (Online Resource 1), observed as “many different and connected parts,” “quality of being intricate” and “many parts related to each other.” In addition, meanings of heterogeneous and heterogeneity indicated that the core concept includes the existence of different types of things and the quotes “diverse in character or content” and “different parts or types” make this clear.

In the context of HS in marine ecosystems, complexity was frequently used alone, in a multidimensional approach and as a quantitative measure (Fig. 5; Online Resource 2). Moreover, the majority of definitions of heterogeneity were classified in unidimensional approach and as a quantitative measure (Fig. 5; Online Resource 2). No definition of complexity and/or heterogeneity was found in the surveyed studies that could be classified only as a qualitative measure in the multidimensional approach.

Fig. 5
figure 5

Scheme of the central ideas of complexity and heterogeneity definitions found in a subset (n = 31) of the 181 publications reviewed. Definitions of both terms used as non-synonymous in some publications was showed separated and the total of definitions in the scheme was 38. This scheme is organized in the multidimensional and unidimensional approaches of the concepts, and these were classified here as quantitative, qualitative, and quali-quantitative measures, as well as unclear definitions. Definitions for isolated use of complexity are represented by boxes filled with gray, isolated use of heterogeneity are showed in the boxes with no fill and for both terms as synonymous, definitions are represented by boxes with no fill and italic font

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Discussion

In the last decade, empirical studies dealing with the influence of HS on biological communities in marine environments were mostly done on benthic habitats. These studies showed the disagreement in the use and application of the terms complexity and heterogeneity. The occurrence of different uses of the terms on studies performed in distinct habitats (e.g., coral reefs, mangroves, rocky intertidal and subtidal shores, seagrasses, mussel beds) blurs the understanding of the effect of HS in marine ecology. However, a small overlap in central ideas of the concepts of complexity and heterogeneity was observed between the definitions found in the surveyed articles and in the core meanings of terms (dictionaries definitions). Considering the breadth of the core meanings, this slight overlap could be the starting point for clarification of heterogeneity and complexity concepts in the context of HS. Clarification is necessary to formulate clear general definitions that will help comparison between different studies in marine environments.

The marked increase in the number of publications that addressed HS in marine ecosystems reflects the importance of this topic for ecology, and the main habitat category responsible for this trend was coral reef. The number of publications documenting HS in coral reef is increasing since the 1960s (Graham & Nash, 2013). This habitat provides one of the most striking examples of the effect of HS on associated organisms, and presents pioneering studies in the quantification of HS in aquatic environment (Kovalenko et al., 2012). The tradition in research of coral reefs possibly influenced other research fields in the benthic marine environment, including the use of the term complexity in investigations of the effects of HS on different communities.

In empirical measurements of complexity and heterogeneity, scientists from distinct areas face different situations to evaluate the HS. For example, the kind of habitat in coral reefs and rocky intertidal (i.e., hard substrate) are clearly different compared to seagrass or kelp forests. The choice of measurements in empirical studies should consider the reality of study site (e.g., kinds of structural elements) and biological group faced in sampling or experimentation; however, there must be a general definition in order to allow comparison between different studies and ecosystems.

Heterogeneity to McCoy and Bell (1991), and to some studies surveyed here, corresponds to a quantitative measure, but its applicability usually refers to kinds of structural elements in some habitat (e.g., rocks, vegetation, crevices), i.e., composition. Then, the definition of heterogeneity used alone or as non-synonymous has a relation with the qualitative core meaning surveyed from the dictionaries (i.e., the existence of different types of things). Therefore, it is possible to define heterogeneity as a qualitative and unidimensional entity of HS that corresponds to types of structural components of the environment (e.g., rocks, crevices, shoots, sediment fractions).

Overall, complexity definition in the publications surveyed has been similar to its core concept (many different and connected parts), and these different parts in theoretical studies was discussed as different characteristics of structure (Loehle, 2004; Tokeshi & Arakaki, 2012). However, the idea of connection between parts expressed in the core meaning of the terms complexity and complex was not observed in the surveyed studies. Ecological relationships are not restricted to isolated traits of a multidimensional variable, as HS, and more likely those traits (e.g., distinct dimensions of HS) interact with each other (Corning, 2000). Then, structural habitat complexity could be defined as a multidimensional entity that corresponds to a set of qualitative (e.g., composition or spatial arrangement of structural elements) and quantitative structural traits of habitat (e.g., number, size, and density of the different structural elements) that may interact and affect ecosystems at different levels.

Here is proposed an integrative and multidimensional perspective of HS in marine systems, similar to what was indicated by Tokeshi and Arakaki (2012). The habitat complexity corresponds to the variation of HS in a given place (i.e., the most structured habitats correspond to the most complex habitats) and habitat heterogeneity refers to one dimension (or trait) of structural habitat complexity.

Conclusion

Review and conceptual clarification of use of the terms complexity and heterogeneity for HS studies in marine ecosystems demonstrated that they do not have a conventional use. Therefore, ecological empirical studies urgently need to make clear what concepts are behind the measurements performed and correctly cite them allowing closer communication between different areas of knowledge. This will contribute more robustly to generalizations, such as the positive influence of HS on the diversity of marine communities. The framework used here, which is addressing HS and the core meaning of the terms in marine empirical studies, indicated that the concept of complexity must be operationalized as a multidimensional measurement with parts that interact and consider heterogeneity as a part of the habitat complexity. Moreover, given the great importance of habitat complexity on functioning of ecosystems, further investigations addressing the influence of different traits of HS and the possible interaction of them on different levels of organization in marine ecosystems are required.