Introduction

Biodiversity or biological diversity refers to the variety and variability amongst all living organisms on earth. Therefore, the preservation of biodiversity is the basis for sustaining life. Biodiversity supplies a variety of genetic material that not only serves as food, but its sustainable use contributes to food and nutrition security (Frison et al. 2011), poverty reduction (Frison et al. 2005; Johns and Eyzaguirre 2007) and it is part of cultural heritage (Wahlqvist 2005). Worldwide, however, biological diversity from wild and agricultural ecosystems is declining. This trend negatively affects livelihoods, particularly of rural people who subsist from the foods supplied by the local biodiversity.

Today, about one billion people suffer from hunger and even more are deficient in micronutrients (FAO 2010c). In addition, one hundred million of disability adjusted life years are attributed to diet-related chronic diseases such as cardiovascular diseases and diabetes (Abegunde et al. 2007). This double burden of over- and under-nutrition-related diseases is rapidly increasing and particularly affects low and middle-income countries (Monteiro et al. 2004). For these countries, which highly depend on own food supply, food-based strategies rooted in the sustainable use of biological resources are needed to improve local diets. Unfortunately, the diet of most populations around the world nowadays are based on few crops (~30) which supply about 95% of the total energy (FAO 1997) and only few traditional societies still base their diets on about 200 species (Kuhnlein et al. 2009).

Several researchers consider that the promotion of biodiverse diets (diets with a high number of species) can be an effective and sustainable way to address the current dietary challenges by increasing the number of foods in the diet, and eradicating energy and micronutrient deficiencies (Burlingame et al. 2006; Flyman and Afolayan 2006; Johns and Eyzaguirre 2006; Englberger et al. 2010a; FAO 2010b). Diversified diets have been shown to contribute to food security (Hoddinott and Yohannes 2002), to be adequate in nutrients (Ruel 2003; Torheim et al. 2004; Steyn et al. 2006; Kennedy et al. 2007), and to be associated with improved nutritional status (Arimond and Ruel 2004; Savy et al. 2005).

Several traditional varieties of plants are known to have a higher micronutrient content compared with the intensively cultivated ones (Burlingame et al. 2009; Mouillé et al. 2010). The use of local plant and animal varieties in the human diet can thus be instrumental to enhance public health since the regular intake of bioactive compounds has been associated with positive health outcomes such as the reduction of serum cholesterol and carcinogen detoxification (Kris-Etherton et al. 2002). At the same time, it is imperative to conserve natural biodiversity as a way to meet present and future global food demand (Godfray et al. 2010), which can be achieved by integrating environmental and public health policies (Lang et al. 2001).

Against a background of biodiversity loss and dietary changes, the cross-cutting initiative on biodiversity and human nutrition has been launched to main stream the sustainable use of biological diversity to increase the diversity in the diets and to tackle both under- and over-nutrition (CBD 2006). The general aim of the initiative is to contribute to reach millennium development goal (MDG) 1 of reducing hunger and poverty, and at the same time to ensure environmental sustainability (MDG 7). This initiative acknowledges the urgent need to review current knowledge on the links between biodiversity and human nutrition. To monitor progress towards the targets set for biodiversity preservation, indicators for food composition (FAO 2008) and for consumption of food biodiversity (FAO 2010a) have been proposed by the Food and Agriculture Organization of the United Nations (FAO). The latter contains a list of dietary assessment methodologies which are recommended to record the diversity of plants, animals, and other organisms used for food.

To date, however, no systematic literature review on the contribution of biodiversity in human diets is available. Lack of such compiled evidence impairs biodiversity preservation strategies to set benchmarks that include dietary diversification as a key principle. In addition, it is unclear which methodologies are currently applied to measure and document biodiversity in diets. Because of the multidisciplinary of the topic the use of various biodiversity and nutrition terms have made the consensus difficult.

This article summarizes the current knowledge on the contribution of plant and animal biodiversity in human diets. During the review, we conceptualized biodiversity as both wild and agricultural products, with the latter also written as agro-biodiversity or agricultural biodiversity which is the variety and variability of animals, plants, and micro-organisms, at the genetic, species, and ecosystem levels, relevant to food and agriculture. In addition, we use the word “food biodiversity” when referring to the diversity of plants, animals, and other organisms used for food. We used the term “local foods” referring to those wild or agricultural food products, and “traditional foods” to foods with cultural significance.

We systematically reviewed all available information on the dietary contribution of biodiversity in terms of:

  1. (i)

    energy intake, as overall indicator of healthy diets (FAO 1995); and due to its potential importance to contribute to reduce energy malnutrition;

  2. (ii)

    micronutrient intake, as a proxy for the prevention of micronutrient deficiencies (FAO 1998);

  3. (iii)

    dietary diversity; as a reflection of overall dietary quality and nutrient adequacy (Ruel 2003).

Methodology

Peer-reviewed articles for this review were searched in May 2010 in ten scientific literature data bases, i.e., IngentaConnect, ISI web of Knowledge, Science Direct, Worldcat (multidisciplinary databases); Cochrane library, EMBASE, and PubMed (life science, biomedical databases); Bioline International (bioscience database for developing countries), AGRICOLA and AGRIS (agricultural database); and Google scholar which was used to retrieve documents through hand search. A second search was conducted in October 2010 to update our database with studies published after the main search. This second search was directed only in ISI web of knowledge, Science direct, and PubMed since these databases provided most of the selected papers in the first search. The second search, however, did not yield new papers. The search results were imported and managed using reference software (Endnote X2, The Thompson Corporation, NY, USA).

The initial search syntax was developed using the following key search terms “(food OR diet OR nutrition) AND biodiversity”, combined with wildcards and indexed terms specific to the database. The detailed search syntax for each database is included in Table 1. The search results were further refined for energy and micronutrient intake, and dietary diversification by means of the key words “energy”, “energy intake”, “micronutrient”, “dietary diversity”, and “food diversity”.

Table 1 Search strategy used to retrieve documents on biodiversity and the contribution to human diets
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Articles’ full titles were screened by the first author. Only studies potentially referring to food biodiversity and human nutrition were retained. Studies on animal nutrition, biofuels, food production simulations and/or modelling, microbiology, and genetically modified organisms were excluded, as well as short communications and reviews. Reviews were used as secondary sources for hand search. A second screening was conducted by reading the abstracts and selecting only studies with nutritional or dietary assessment of food biodiversity. When it was not clear from the abstract what type of methodology was used, the paper was referred to the full text review.

The full text evaluation of selected articles was carried out independently by the first and second author; when there was disagreement a third author was consulted. Eligibility criteria for the selection of the full papers of the review were (i) the study was an original study, (ii) food (plant or animal) biodiversity in the human diet was assessed, and (iii) results included dietary outcomes. Search was done for all years and restricted to languages familiar to the authors (i.e., English, French, Spanish, Dutch, and Portuguese).

The results were reported following the guidelines of STrengthening the Reporting of OBservational studies in Epidemiology (STROBE 2007), and Preferred Reporting Items for Systematic Reviews and Meta-Analyses (Moher et al. 2009). An adapted summary table from FAO was used to extract the information for every study (FAO 2010a). This summary table was used by us to discuss the results and to structure the findings of this review. We present the results for each of the categories regarding the contribution of biodiversity to diets (i.e., energy intake, micronutrients contributions, and dietary diversity) in Table 2.

Table 2 Evidence (n = 34) on the contribution of biodiversity to energy intake, micronutrient intake, and dietary diversification
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Results

General Findings

The search process, the number of studies initially retrieved, and the number of excluded studies are illustrated in Fig. 1. A total of 34 unique studies were selected for this review. We retrieved 7, 14, and 17 studies in relation to energy intake, micronutrient intake, and dietary diversification, respectively. Five studies reported findings for more than one category. The studies were mainly carried out in areas of high biodiversity of low- and middle-income countries, and focused on the dietary contribution of local foods (whether from wild or agricultural sources) particularly from plant origin (Table 3). Only five studies assessed the contribution of local foods in the diet of populations in high income countries as Canada (Kuhnlein et al. 2004, 2006) and Italy (Pieroni et al. 2005; Nebel et al. 2006; Orban et al. 2006), but these were limited to specific traditional diets. All studies were descriptive and mostly based on convenience sampling.

Figure 1
figure 1

Flow diagram of search strategy and selection process of articles on the contribution of biodiversity to human diets.

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Table 3 Food biodiversity investigated geographical regions
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Biodiversity and Energy Intake

The seven studies on energy intake reported a variety of outcome indicators including per capita energy intake of local foods (Begossi and Richerson 1993), proportion of total energy derived from local foods (Mennen and Mbanya 2000; Kuhnlein et al. 2004; Roche et al. 2008), and contributions of locally produced foods to energy requirements (Rajasekaran and Whiteford 1993; Orban et al. 2006; Rais et al. 2009). None of the studies quantified the energy intake from foods that were identified up to species level, which did not allow us to associate the absolute energy contribution of the species eaten.

Studies quantifying dietary intake as percentage of the total energy supplied by local foods included Mennen and Mbanya (2000), Kuhnlein et al. (2004), Roche et al. (2008); yet, these studies used only common names to refer to the foods. The reported energy contributions from local foods ranged between 10 and 90%, and these were associated with the consumption of about ten local food items in rural areas (Mennen and Mbanya 2000), forest (Roche et al. 2008), or arctic areas (Kuhnlein et al. 2004). Amongst these, several local or traditional foods including (but not limited to) banana, caribou, cassava, moose, seal, and whitefish were found to be important caloric contributors in the investigated areas.

One study (Begossi and Richerson 1993) reported energy intakes (per capita) of local animal food consumption (mainly fish) and named the species eaten, providing thereby some insight on the relevance of the local fish species to local fishermen. However, the results are based on intake estimations and are limited to animal consumption, during lunch time and dinner.

Various studies reported the percentage of energy requirements supplied by locally available foods. The results show that from 23% (Rajasekaran and Whiteford 1993) to 52% (Rais et al. 2009) of the recommended daily energy intake could be supplied by local foods. These studies, however, were based on estimated consumption of crab and agricultural products. In addition, one study reported that recommended protein and fat intakes can be reached by eating a serving of local fish (Orban et al. 2006).

Biodiversity and Micronutrient Intake

Studies on the contribution of local food intake to meet micronutrient recommendations reported nutrient adequacy of diversified diets (Hatloy et al. 1998; Roos et al. 2003), the proportion of micronutrient intake supplied from local foods (Ogle et al. 2001c; Kuhnlein et al. 2006; Singh and Garg 2006; Roche et al. 2008), and the percentage of recommended intake covered by the usual consumption of local foods (Ogle et al. 2001a; Englberger et al. 2006; Roos et al. 2007a, b; Englberger et al. 2008; Davey et al. 2009; Englberger et al. 2009, 2010b). Both studies evaluating micronutrient adequacy of local diets were based on actual intake, one used mean adequacy (Hatloy et al. 1998) and the other nutrient contribution ratios (Roos et al. 2003) to report the results. The latter reported the second highest proportion (31 and 40%) of the recommended intake of calcium and vitamin A, respectively, attributed to the consumption of small fish species. Hatloy et al. (1998) reported mean adequacy ratios for seven micronutrients as well as energy, fat, and protein, but did not describe the different food sources.

Three studies evaluated the proportion of micronutrient supplied from the consumption of traditional foods (Ogle et al. 2001c; Kuhnlein et al. 2006; Roche et al. 2008). Kuhnlein et al. (2006) and reported that 87, 23, and 37% of the total daily intake of cholecalciferol, vitamin A, and tocopherol, respectively, is supplied by the traditional food portion of arctic diets. Ogle et al. (2001c) reported the contribution of wild vegetables and staple foods to folate only, with values of 21 and 46%, respectively; whereas Roche et al. (2008) studied the contribution of all traditional foods to more than one micronutrient (i.e., iron, thiamine, riboflavin, and vitamin A).

Studies focusing on the micronutrient composition of some target foods were mainly based on chemical analysis, and used dietary estimations to report the contribution to daily recommendations. The study of Davey et al. (2009) and those of Englberger et al. (2006, 2008, 2009, 2010a, b) identified several vitamin A-rich Musa fruit varieties, Cyrtosperma, and Pandanus that could, under normal consumption patterns, potentially contribute to meet dietary recommendations for vitamin A. In addition, Ogle et al. (2001a) found that the daily intake of some naturally occurring vegetables can potentially contribute to meet up to 30 and 40% of the recommended allowances of vitamin A and calcium, respectively. Roos et al. (2007a, b) reported local fish consumption to contribute with 15 and 45% of the daily vitamin A and iron requirements, respectively. The study of Singh and Garg (2006) showed that the daily intake of a spice mix can contribute with 5–7% to the recommended daily intake of some micronutrients (i.e., chromium, iron, manganese, zinc, copper, phosphorous, and selenium).

Biodiversity and Dietary Diversity

Studies investigating the contribution of biodiversity to dietary diversification reported mainly the number of food items within the diet (Begossi and Richerson 1993; Nordeide et al. 1996; Osemeobo 2001; Steyn et al. 2001; Frei and Becker 2004; Kennedy et al. 2005; Pieroni et al. 2005; Nebel et al. 2006; Batal and Hunter 2007; Dovie et al. 2007; Passos et al. 2007; Rais et al. 2009). In addition, few studies used specific indicators of dietary diversification (Hatloy et al. 1998; Ogle et al. 2001b; Akrofi et al. 2008; Ekesa et al. 2008; Roche et al. 2008). The number of foods reported as part of habitual diets varied considerably. The highest reported values include 76 fish and other animal species (Begossi and Richerson 1993), 32 and 62 vegetables species (Ogle et al. 2001b; Steyn et al. 2001), 26 and 40 fruit species (Nordeide et al. 1996; Passos et al. 2007), and between 21 and 51 varieties of rice (Frei and Becker 2004; Kennedy et al. 2005). The studies also reported a wide interval of consumption frequencies for some foods, going from several times per day to a different number of times per year, and some indicated seasonal variations (data not shown).

Dietary diversity was expressed as diversity scores (DDS), food variety scores (FVS), and traditional food variety scores (TFVS). Ekesa et al. (2008), Hatloy et al. (1998), and Ogle et al. (2001b) reported the level of dietary diversity of local diets using both DDS and FVS. DDS was used to report dietary diversification by foods groups (i.e., 8 or 12 foods groups according to the context). When referring to the total number of food items consumed over a time period (usually 7 days), FVS was used. The highest reported value of FVS was 20.5, indicating that up to 21 food items were consumed in a week period in the investigated area. A more specific indicator used was the TFVS (Roche et al. 2008), which is the number of traditional/local foods present in a diet assessed by 24-h dietary recall. The indicator showed that diets of Peruvian communities in the Amazon area contain a mean of 9.5 local foods items per day, being wild or cultivated.

Additional Findings

The methodologies applied by the consulted studies estimated the contribution of biodiversity to diets and were very diverse. We identified three different methodologies that were categorized as: dietary assessment methods (tools to describe or record diets), nutritional assessment methods (tools to estimate the nutrient content of the investigated food items), and local food biodiversity assessment methods (tools to record, identify and list the local edible plant or animals included in the diet). Table 4 details the methods used to measure the contribution of biodiversity in the diet.

Table 4 Assessment tools (dietary, nutritional, and biodiversity) applied by studies exploring biodiversity and its contribution to human diets (n = 34)
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Often, a combination of dietary and nutritional assessments were used (n = 18). Only a few of these studies used a quantified dietary intake assessment (Rajasekaran and Whiteford 1993; Mennen and Mbanya 2000; Kuhnlein et al. 2004, 2006; Roche et al. 2008). Other studies (Begossi and Richerson 1993; Ogle et al. 2001a; Steyn et al. 2001; Lykke et al. 2002; Kennedy et al. 2005; Batal and Hunter 2007; Akrofi et al. 2008) used a combination of local food biodiversity and dietary assessments, exploring thereby the intake of local foods and naming the species involved.

The most frequently applied dietary assessment method was dietary recalls (n = 11), especially on energy intake studies (Begossi and Richerson 1993; Mennen and Mbanya 2000; Kuhnlein et al. 2004; Roche et al. 2008); followed by food frequency questionnaires (n = 8) which were particularly used to record dietary diversity (Nordeide et al. 1996; Ogle et al. 2001b; Ekesa et al. 2008). The dietary recalls were mostly 24-h recall (Rajasekaran and Whiteford 1993; Mennen and Mbanya 2000; Kuhnlein et al. 2004; Kennedy et al. 2005; Akrofi et al. 2008; Roche et al. 2008), recalls in relation to specific meals (Begossi and Richerson 1993), and recorded intakes on various days (Roos et al. 2003; Pieroni et al. 2005; Passos et al. 2007).

Local food biodiversity was mainly documented using a combination of interviews and by field observations (Rajasekaran and Whiteford 1993; Nordeide et al. 1996; Mennen and Mbanya 2000; Ogle et al. 2001a; Lykke et al. 2002; Kennedy et al. 2005; Englberger et al. 2006; Nebel et al. 2006; Orban et al. 2006; Dovie et al. 2007; Englberger et al. 2008, 2009, 2010b). These studies belong mostly to the category of dietary diversification.

Discussion

Sustainable use of wild and agricultural biodiversity is important to address the prevailing nutritional problems and global food supply. This review brings together the available evidence on the contribution of edible plant and animal biodiversity to human diets, information which was currently lacking (CBD 2006). We reviewed 34 studies reporting on biodiversity and energy intakes, micronutrient intakes, and dietary diversification. It was surprising to find this limited number of studies for a hot topic widely discussed in academia (Johns 2003; Wahlqvist 2003; Frison et al. 2006; Toledo and Burlingame 2006; Vinceti et al. 2008; Frison et al. 2011) and of global public concern.

All summarized information indicated biodiversity to be the mainstay of a variety of plant and animal food products and an important element in the local diets. However, this evidence was mainly restricted to highly biodiverse areas, such as rural and forest zones in which these studies were conducted. Since, the studies were on the diet of people who subsist from locally available foods, the dietary importance of biodiversity in these diets is hardly a surprise. It is not surprising that biodiversity investigations have been conceptualised and conducted in areas of high biodiversity, such as tropical forest. Answers to the global food security issues of the next generation, however, will require research and solutions to feed an increasingly urban population, in particular in low and middle-income countries. Urbanization not only leads to loss of arable land, it drives intensification of food provision and straining of existing agricultural and food provision systems (Godfray et al. 2010). Policy makers will need to carefully consider the role of agricultural biodiversity, local food supply, and small holder agriculture when designing the food system of tomorrow (UN 2010). Our review demonstrates how the current research on biodiversity and diets falls short to provide the necessary evidence to design agro-ecological models with respect to sustainable biodiversity preservation.

The evidence regarding local food biodiversity and its dietary energy contribution was reported mainly by the proportion of the total energy supplied by local foods. This and all other reported energy outcomes highlighted local and traditional foods as essential suppliers of enough calories to the people living on the investigated communities. Daily consumption of local foods is for people living in traditional societies and rural areas imperative for food security. In addition, reported outcomes on micronutrient intakes show that consumption of local and traditional foods contributes to meet daily micronutrient recommendations. This suggests that micronutrient deficiencies can be addressed through local food-based approaches, particularly by the consumption of micronutrient rich varieties (Tontisirin et al. 2002; Krawinkel 2009). Furthermore, the available evidence indicates that diets of people eating from highly biodiverse areas are also very diversified.

Animal foods were found to be important sources of biodiversity in the diet. Concerns have been raised, however, on how recommendations should be formulated with regard to the consumption of animal foods. Although, animal source food adds important sources of nutrients in diets of populations in low and middle-income countries (Allen 2003), the consumption has raised globally up to levels of overconsumption in various population groups (WHO 2003). Environmental concerns have been raised with regard to the contribution of the intensive production of animal source food production on greenhouse-gas emissions and fisheries on the depletion of oceans (McMichael et al. 2007; Bell et al. 2009; Godfray et al. 2010). Healthy promotion strategies should also incorporate recommendations for sustainable diets. The latter are defined as those diets with low environmental impacts, protective, and respectful of biodiversity and ecosystems; culturally acceptable, accessible, economically fair, and affordable; nutritionally adequate, safe, and healthy (Burlingame et al. 2011). A key strategy is to investigate which local consumption patterns are sustainable with regard to agriculture biodiversity and to incorporate these into the programming and interventions. Unfortunately, to date not one single study is available in this regard.

Our findings are constrained by the type and nature of the collected information. The reported outcomes varied widely and did not allow us to further generalize the main outcomes. In addition, a wide variety of assessment methodologies were used. This could be partially attributable to the use of both biodiversity and dietary assessments by all of the studies, which was a pre-condition of our selection criteria. Being a multidisciplinary topic, we believe that the use of combined methodologies is imperative to conduct this type of research. In addition, we acknowledge that the biggest obstacle for investigating biodiversity and its contributions to human nutrition is the absence of a standardized methodology that quantifies dietary intake of locally produced or wild foods, involves food identification and distinction of species and subspecies, and analyses food composition of the investigated genetic pools. Importantly, the initiative of FAO on nutrition indicators for biodiversity has given a first step by launching measurement tools and indicators to help to overcome these shortcomings (FAO 2008, 2010a).

Indexed terms and key words that would accurately retrieve the desired documents were not available. We therefore used a combination of dietary, health, and agricultural terms for the search and used a series of databases from various disciplines. However, a limited number of studies were retrieved, and these were mostly indexed under agricultural biodiversity terms. Given the limited use of quantified dietary assessment methods in the studies retrieved, this would suggest that research on biodiversity and human nutrition has been mainly conducted by botanists and agronomists and received less attention by nutritionist and health scientists. The complexity of linking agricultural and health research seems to be a setback to engage in a large comprehensiveness of this topic. Only future multidisciplinary research, incorporating appropriate biodiversity and nutritional assessment methodologies, would lead to a better understanding of the dietary contributions of local food biodiversity and diets.

Conclusions

Biodiversity could contribute to human diets with energy, micronutrient, and many a number of foods that count for dietary diversification, particularly in highly biodiverse areas, but strong evidence is lacking. Methodologically, better instruments to measure the dietary contribution of local biodiversity are needed. A standardized methodology would enable to better substantiate the link between biodiversity and the quality of the diet. Deeper knowledge on high biodiverse diets would contribute to design dietary guidelines which would be not only healthy but sustainable. Further research on the contribution of biodiversity in diets of industrialized countries and urban settings, however, is needed to gain knowledge on biodiversity contributions of other ecosystems.