Change in Average Trophic Level of Marine Predators in the Bay of Biscay

D4 - Marine Food Webs

D4.2 - Proportion of selected species at the top of food webs

D4.3 - Abundance/distribution of key trophic groups/species

The assessment of changes to Mean Trophic Level in the Bay of Biscay showed no apparent change in overall food web structure over recent decades. However there were some signs of increase in the biomass of marine predators.

Area Assessed

Printable Summary

Background

Food webs are networks within which organisms are related by feeding relationships (i.e. predator-prey interactions). This is one of three food web indicators, which describes changes in the structure of the food web with respect to fish and invertebrates.

Trophic level, determined by diet studies, expresses the position of an organism in a food web. A low trophic level (TL) value (e.g. 1) is assigned to the primary producers at the base of the food web whereas a high TL value (e.g. 4 or more) is assigned to predators at the top.

Mean Trophic Level (MTL) is calculated using species biomass data from different sources (e.g. scientific surveys and fisheries landings), and their assigned TL values. As the diet of species may vary among regions, it is important to use regionally-specific diet studies to determine regionally relevant TL values. These values are used to represent the feeding pathways / relationships in a given region, i.e. what-eats-what.

This indicator, currently based on invertebrates and fish, is mainly sensitive to fishing pressure. Fisheries usually target species at a high TL and thus drive a decrease in the availability of predators within the ecosystem. This in turn forces fisheries into targeting species at ever lower trophic levels and thus a decline in the MTL of fisheries landings. This is referred to as ‘fishing down marine food webs’ (Figure 1). If the phenomenon persists, the changes in food web structure could leave marine ecosystems increasingly vulnerable to natural and human-induced pressures.

Figure 1: Representation of the “fishing down the marine food web” concept (adapted from Pauly et al., 1998)

Food webs represent the trophic interactions between predators and their prey. Each life stage of an organism is associated with a particular trophic level and, at its most simplistic, the energy is transferred from the lower trophic levels to the higher trophic levels following the interconnections between organisms within the food web. The tropic level (TL) value assigned to a particular organism is determined by the proportion of each category of species constituting the diet of a particular consumer (knowing that TL=1 for primary producers, and TL=2 for primary consumers, etc. (see Figure a)). TL can be estimated using dietary analysis (stomach content analysis), stable isotopes analysis, and modelling.

 

Figure a: Representation of the concept of Trophic Level in a food web. (adapted from 2007-2009 The University of Waikato)

Within the scientific community, it is considered to be important that food web status should be based on ecosystem indicators that do not just use fish data (i.e. high trophic level species such as hake, monkfish, sharks, rays) but also data concerning invertebrates and species from intermediate trophic levels. The Mean Trophic Level (MTL) indicator meets this requirement because it takes into account food web structure and uses a metric (the TL) that reflects energy transfer between predators and prey. MTL is calculated using biomass data from scientific surveys and fisheries landings and the associated TL of the species. In this assessment, the indicator has been calculated taking into consideration vertebrates and invertebrates where possible.  Eventually, however it is expected that this indicator will be adapted to consider all vertebrate and invertebrate.

The original concept that uses the MTL indicator, developed by Pauly et al. (1998), is known as ‘fishing down marine food webs’. A decline in the MTL of the global fisheries catch reveals a shift from intense fishing pressure on the highest trophic levels to increasing fishing pressure on lower trophic levels, due to the decline in biomass of high trophic level species. Thus, this indicator aims at highlighting the unsustainable fisheries practices of past decades. The indicator could inform political decisions to enforce regulations upon fisheries catches / quotas. The indicator was adopted by the Conference of the Parties to the Convention on Biological Diversity as one of eight indicators to monitor achievement of a significant reduction in the rate of biodiversity loss by 2010.

Since then, the use of MTL of landings has been further explored and additional hypotheses suggested to explain the patterns in MTL observed. The ‘fishing down food webs’ concept as defined above was actually detected in the North Atlantic. Other scenarios were described in other parts of the world (Essington et al., 2006; Morato et al., 2006; Swartz et al., 2010; Stergiou and Tsikliras, 2011; Shannon et al., 2014), for example, the concept of fishing through the food webs (sequential addition of low trophic level species in fisheries); fisheries expansion (into deeper and further offshore waters with the inclusion of new high trophic level species); and fishing up the food webs (addition of new previously unfished high trophic level species).

To compute the MTL indicator, landings have traditionally been the only source of biomass data, raising many concerns around their suitability for describing the ecosystem as a whole, due to the shortcomings and / or uncertainties associated with this type of data. First, the landings data are incomplete (i.e. they do not take into account discards, illegal, unreported, and unregulated fishing, or bycatch), and second, landings data are subject to multiple biases induced by fisheries drivers (Branch et al., 2010; Pauly et al., 2013). However, landings data do have the advantage of a high frequency of data availability that includes all gear types and thus many species. On the other hand, data from scientific surveys reflect actual changes in community structure because they are not influenced by market forces (i.e. selectively fishing for particular commercial species only). However, data from scientific surveys are usually limited to a specific season and one type of fishing gear. Thus, scientific surveys should be the main data source when using the MTL indicator to assess the food web, with landings providing complementary information.

The TL values of most species are available and can be easily found in online databases (e.g. www.fishbase.org). However, these values are worldwide averages based on data from different ecosystems. In many cases these global averages do not reflect the characteristics of a given region where trophic interactions between species can be specific to that region. Environmental or human-induced conditions can lead to variability in prey availability and predator selectivity, in turn causing variability in the TL values for a given species in space and time and even with size (Pinnegar et al., 2002; Chassot et al., 2008; Vinagre et al., 2012). Therefore, TL values need to be region-specific in order to be most accurate and best represent feeding interactions in the study region.

Mean trophic level (MTL) is calculated using two types of data: (1) biomass data per species for fish and invertebrates from surveys and landings and (2) data on the trophic level of each species.

Data Collection

Biomass Data

Past and present fish and invertebrate biomass data for the Bay of Biscay are compiled from research surveys and landings.

Surveys

Annual biomass per species, collected during the DEMERSALES surveys on ICES subdivisions VIIIc and IXa-north of the Bay of Biscay for the period 1992–2015 were used for the southern Bay of Biscay analyses. Data were directly extracted from the Instituto Español de Oceanografía (IEO) database and include both invertebrate and fish data because invertebrates constitute a large part of the survey catches.

Annual biomass per species collected during the EVHOE surveys on ICES subdivisions VIIIa and VIIIb of the Bay of Biscay for the period 1997-2015 were used for the northern Bay of Biscay analyses. Survey data were extracted from the 2017 OSPAR Groundfish survey monitoring and assessment data product (Moriarty and Greenstreet, in prep), which focuses on fish communities across the Northeast Atlantic region and does not include any invertebrate data.

Data were selected for the depth range of the continental shelf in the Bay of Biscay (<200 m depth).

The DEMERSALES and EVHOE surveys are bottom trawl surveys, which are part of the Data Collection Framework of the Common Fisheries Policy (EC regulation No. 665/2008).

Landings

Annual biomass per species, from the official landings dataset were used for the analyses in subdivisions VIIIa and VIIIb for the northern Bay of Biscay, and subdivisions VIIIc of the southern Bay of Biscay. These data can be downloaded from the ICES website (ICES Historical catch statistics 1950–2010 and Official catch statistics 2006–2014).

French landings data are the main data source for the northern Bay of Biscay. The data were however missing for 1999 and so could not be included in this analysis.

Trophic Level Data

Some preliminary work is needed to collate regional TL values per species. This improves the reliability of TL values for the Bay of Biscay because the diet of species (and hence the predator-prey relationships) may vary among regions. Three sources of TL information are prioritised to ensure the most appropriate TL value for each species (Figure b).


 

Figure b: Trophic Level value selection according to source type

However, because TL values are assigned at the species level, it did not seem appropriate to assign TL values to large groups that would include species from low to high trophic levels (e.g. Osteichthyes; the bony fishes). High taxonomic ranks (i.e. phylum, sub-phylum, class, superorder, order, suborder and infraorder) were thus removed from the MTL computation. Only the ranks of genus and family were considered. For these, their TL is derived by averaging the TL values of all relevant species present in the Bay of Biscay.

The regional TL values estimated from stomach content analyses were based on the IEO’s non-public database corresponding to DEMERSALES surveys in the Spanish part of the Bay of Biscay, for the period 1990–2013. The remaining TL values, estimated from stomach content analysis, stable isotope analysis or models, were collected from the published literature for regions and surrounding regions (Jennings et al., 2002; Pinnegar et al., 2002; Le Loc’h and Hily, 2005; Bodin et al., 2008; Le Loc’h et al., 2008; Navarro et al., 2011; Chouvelon et al., 2012; Lassalle et al. 2011; Lassalle et al., 2014).

Calculation of the MTL indicator

The MTL indicator for each year is calculated using the biomass and TL of species according to the following formula:

Formula a: The Mean Trophic Level indicator formula.

where MTLk refers to the MTL indicator for each year k, TLi refers to the trophic level value of species (group) I, and Yik refers to the biomass (Y) of species (group) i in year k, as included in landings data or in surveys data.

The MTL is then calculated each year in order to identify trends.

While assessing this indicator, the group of species considered can be changed by applying a TL cut-off (e.g. 3.25). The purpose of these cut-offs is to eliminate low trophic level species in order to focus on predators (i.e. high trophic level species) and detect changes in the upper food web structure.

Pauly and Watson (2005) stated that using the mean TL for the Marine Trophic Index should always be done with an explicitly stated cut off and proposed a first TL cut-off value of 3.25, it excluded all landed species under a TL of 3.25. In this assessment three TL cut-offs were identified: a TL cut-off value of 2.0 (expressed as MTL_2.0, which includes all consumers into the analysis; the MTI cut-off value of 3.25 described by Pauly and Watson (200t) (expressed as MTL_3.25). The third cut-off fixed at 4.0 has also been applied to the data (i.e. MTL_4.0) to focus on higher predators.

The MTL indicator with different cut-offs was first calculated using the whole community (all species included), and then by eliminating pelagic species from the computation to give information on bentho-pelagic species. Excluding pelagic species, helped reduce bias in the biomass data, linked to interannual variability in the pelagic species data. Indeed, the EVHOE and DEMERSALES surveys are bottom trawl surveys, meaning they are designed to capture and evaluate bentho-demersal species. The pelagic species of the Bay of Biscay were defined according to Quéro et al. (1989) and Fishbase (www.fishbase.org).

Uncertainty exists around each TL value estimated by diet studies, which is related to spatio-temporal variability and species ontogeny (Pinnegar et al., 2002; Chassot et al., 2008; Vinagre et al., 2012). This uncertainty was reported as a standard error for each TL value of a species. In order to include uncertainty in the MTL model, a bootstrap methodology was developed using the R software (R version 3.1.0). Random sampling was applied on TL values and their standard error, performing 500 MTL computations per year studied. The model was then fitted as a mean value of the 500 MTLs generated with an uncertainty related to its standard error. The uncertainty around the MTL model is thus linked to the uncertainty of the TL estimations.

For statistical analysis, preliminary tests of normality (Shapiro test), homoscedasticity (Harrison-McCabe test) and autocorrelation (Durbin–Watson test) of the data were applied for the use of parametric methods. When these tests were verified, a linear model was fitted to the temporal series (mean values for each year generated by the model) in order to test the significance of the trend. When normality or homoscedasticity were not verified, evolution of MTL over time was assessed by means of Mann-Kendall analyses (Scherrer, 1984). Differences were considered significant when p<0.05. R software and packages were used for statistics and graphics (R core team, 2015).

 

Results

The Mean Trophic Level (MTL) indicator was assessed over a period of 18 to 23 years for the northern and southern parts of the Bay of Biscay (Figure 2), using biomass survey data complemented by fisheries landings data and region-specific TL values for species concerned. Initially, the entire community was studied, followed by a focus on the bentho-demersal community (i.e. those species living on or close to the seabed) by excluding pelagic species (i.e. those living within the water column). Species above a certain TL value were selected in order to concentrate on the predator community.

In the Bay of Biscay (northern and southern parts), food webs indicate a general improvement from the unsustainable fishing pressure of previous decades, shown in this assessment by a significant increase in MTL. The biomass of predators has increased meaning that the structure of the food web is gaining stability and therefore resistance to perturbations.

To better reflect changes in the upper TLs of individual ecosystems, three MTL cut-off scenarios were used to assess trends in changes to MTL in the Bay of Biscay (Table 1): Above a TL of 2.0 (TL_2.0) includes all consumers; Above a TL of 3.25 (TL_3.25) includes higher trophic length fish; and Above a TL of 4 (TL_4.0) includes higher level predators.  

This increase in MTL was detected in the northern part of the Bay of Biscay when assigning the MTL_3.25 and MTL_4.0 cut-offs to both survey and landings data and thus selecting predators for the assessment (Table 1). The increase was also identified in the southern Bay of Biscay, but only for survey data when excluding pelagic species and low trophic level species (MTL_3.25). The positive trends observed for this indicator reflect an increase in predator biomass in the northern part of the Bay of Biscay and to a lesser extent in the southern part. It conveys an apparent reduction in fishing pressure on high trophic level bentho-demersal predators, presumably allowing communities to begin recovery from past perturbations.

There is moderate / low confidence in the methodology used and high / moderate confidence in the availability of data.

 

Figure 2: Bay of Biscay showing the regional subdivisions and the continental shelf (hatched area) of the northern and southern Bay of Biscay

Table 1: Trends in changes to MTL in the Bay of Biscay

Analyses performed using landings and survey data over different Mean Trophic Level (MTL) cut-off scenarios. Statistically demonstrated increases in MTL are shown as green with up arrows and significance; where no increase is calculated, this is shown as green with a horizontal arrow. p-value for the statistical tests significance (linear model), *: p<0.05, **: p<0.01 ***: p<0.001. sp. : species.

The collation of regional TL values for calculating MTL was possible for the main representative species of the landings and survey data, for both the northern and southern parts of the Bay of Biscay. Uncertainty around the MTL indicator is linked to uncertainty around the TL values. Arroyo et al. (2017) showed there was less uncertainty around the MTL indicator when using regional TL values as opposed to global average values (e.g. Fishbase). These results confirm the necessity of giving priority to the development of regional TL values in order to improve the confidence in the assessment of food webs.

Northern Bay of Biscay (subdivisions VIIIa and VIIIb)

Using the scientific survey data, the MTL_2.0 (considering all trophic levels) showed no significant trend in either scenario (i.e. with all species or excluding pelagic species) (Figure c). When applying a mid (MTL_3.25) or high (or MTL_4.0) cut-off, the MTL indicator displayed significant increasing trends (Figure c). The influence of the main species in terms of biomass on the indicator was investigated as part of the EcApRHA (Arroyo et al. 2017).

Figure c: Northern Bay of Biscay, EVHOE survey data analyses. Trends in the MTL indicator with different MTL cut-offs and trends in biomass, considering all species or excluding pelagic species

MTL: Mean Trophic Level, MTL_3.25 and MTL_4.0: MTL using the 3.25 and the 4.0 cut-offs respectively, p-value for the statistical tests significance (linear model), *: p<0.05, **: p<0.01 ***: p<0.001. Green line indicates the mean value and yellow shading shows the standard deviation related to the uncertainty of trophic level estimations.

The MTL calculated using landings data and considering all trophic levels (MTL_2.0 in Figure d) displayed no significant trend over the study period, whether all species were considered or pelagic species were excluded. However, significant increases in the MTL indicator were detected when MTL cut-offs were applied. A significant positive trend in MTL_3.25 was observed when pelagic species were excluded. It underlined the effect that the variability in pelagic species biomass has in masking the evolution of the bentho-demersal biomass. MTL_4.0 (top predators only) increased significantly in both cases (with or without pelagic species).

Figure d: Northern Bay of Biscay, landings data analyses

TrTrends in the MTL indicator with different cut-offs and trends in the total biomass caught, considering all species or excluding the pelagic ones. MTL: Mean Trophic Level, MTL_3.25 and MTL_4.0: MTL using the 3.25 and the 4.0 cut-offs respectively, p-value for the statistical tests significance (Mann-Kendal means), *: p<0.05, **: p<0.01, ***: p<0.001. Green line indicates the mean value and yellow shading shows the standard deviation related to the uncertainty of trophic level estimations.

Southern Bay of Biscay (subdivisions VIIIc and IXa-north)

The MTL_2.0 (including all trophic levels) based on the scientific survey data, showed no significant trend with all species included or with pelagic species excluded (Figure e). When applying a mid (MTL_3.25) or high (MTL_4.0) cut-off, analysis revealed a significant trend only for MTL_3.25 without pelagic species. The EcApRHA project (Arroyo et al., 2017) investigated the influence of the main species ontogeny on the MTL indicator to see if its variation could be due to differences in the age composition of the species caught during the survey (and thus in TL values). Results showed no apparent ontogenetic effect on overall MTL trends at any cut-off level, although further studies are needed to confirm these results with a larger number of species.

Figure e: Southern Bay of Biscay, DEMERSALES survey data analyses

Trends in the MTL indicator with different cut-offs, considering all species or excluding the pelagic ones. MTL: Mean Trophic Level, MTL_3.25 and MTL_4.0: MTL using the 3.25 and the 4.0 cut-offs respectively, p-value for the statistical tests significance (Mann-Kendal means), *: p<0.05, **: p<0.01, ***: p<0.001. Green line indicates the mean value and yellow shading shows the standard deviation related to the uncertainty of trophic level estimations.

No significant trends were detected in the MTL indicator on historical landings data whether considering all species, excluding pelagic species or applying different cut-offs (MTL_3.25 and MTL_4.0 in Figure f). However, the EcApRHA project highlighted that MTL trends for predator communities can vary depending on the length and the source of the landings time series chosen (Arroyo et al., 2017) and that short terms trends can be masked by long-term analysis. For example, an increasing trend of intermediate TL, driven by pelagic species and a decreasing trend in demersal top predators were observed in the last years of landings data.

Figure f: Southern Bay of Biscay, landings data analyses

Trends in the MTL indicator with different cut-offs, considering all species or excluding the pelagic ones. MTL: Mean Trophic Level, MTL_3.25 and MTL_4.0: MTL using the 3.25 and the 4.0 cut-offs respectively, p-value for the statistical tests significance (Mann-Kendal means), *: p<0.05, **: p<0.01, ***: p<0.001. Green line indicates the mean value and yellow shading shows the standard deviation related to the uncertainty of trophic level estimations.

Analyses of scientific survey data and landings data show no major variation in the MTL indicator in the Bay of Biscay. This indicates no apparent signal of the state of the marine food web. The results also highlight that the bentho-demersal predator community seems to have been slowly recovering in this area since the beginning of the 21st century, almost certainly due to management regulations set in place, especially in the northern part of the Bay of Biscay. Nevertheless, these findings need to be treated with care as they are highly dependent on the length and source of the time series considered, especially for the landings data (Arroyo et al., 2017).

Confidence assessment

The methodology has been commonly used but consensus in the scientific community has not yet been achieved, resulting in a confidence of low / moderate.

For data availability the rating is moderate / high. There is sufficient spatial coverage for landings data and ground fish survey data. There appears to be sufficient spatial scale for the trophic level information.

Conclusion

The Mean Trophic Level (MTL) in the southern and northern Bay of Biscay showed no apparent change in the overall food web structure resulting from fishing pressure (MTL 2.0 in Table 1). However there were some signs of improvements when focusing in on the predator community (MTL 3.25 and 4.0 in Table 1).

Using the MTL indicator results from survey data complemented by those from landings data, reinforces the signal of food web state. In the same way, using regional trophic level values provides a better view of community structure within the study region and strengthens the accuracy of this assessment. Examining the community as a whole (both with and without pelagic species) as well as focusing specifically on predators, makes it possible to detect changes in food web structure.
 

The Marine Trophic Level (MTL) in the southern and northern parts of the Bay of Biscay showed no apparent sign of changes in food web structure owing to fishing pressure. An increasing trend in the MTL indicator is considered to reflect decreasing impacts of fisheries on food webs; while a stable or decreasing trend should be further investigated in order to determine possible causes. Knowledge of the fisheries history in the region also helps to interpret trends: the implementation of fisheries regulations may have decreased fishing pressure on top predators. Other information about the communities inhabiting the area and the environmental variability may be necessary to confirm the findings of this assessment. Linking the MTL indicator to other biodiversity and food webs indicators (e.g. Typical Length) would also allow a more detailed examination of the impact of fisheries on the ecosystem.

Further work can be undertaken to improve the assessment of the state of the food web. This assessment is based on invertebrates and vertebrates species in most cases, mainly bentho-demersal species. Incorporating additional datasets on other biological compartments (e.g. benthos, mammals, or birds) and / or from other sources (e.g. pelagic survey data or models) into the MTL indicator will enable a more holistic assessment of the area. For instance, using the OSPAR Groundfish survey monitoring and assessment data product in the northern Bay of Biscay, was a first step in the assessment of this indicator. However, data on invertebrates (including cephalopods), which represent an important component of the biomass in the Bay of Biscay food web, which are important prey items with a fundamental role in the food web, and which can influence the indicator trends, should also be included.

It would beneficial for the further development of this indicator if the work started in the EcApRHAproject was continued. Specifically, the influence of some important demersal / pelagic species on the MTL indicator trends, and how they influence the overall assessment should be examined in more detail (Arroyo et al., 2017). Investigating the direct influence of particular anthropogenic pressures on MTL variations (e.g. fishing mortality of species or indicators linked to habitat loss due to fisheries) also needs to be further explored.

Applying the indicator to finer geographic scales and assessment units would help map regional variation in the MTL indicator, and so identify particularly impacted areas within those subject to high fishing pressure.

Another issue is the difficulty establishing strong reference conditions and assessment values. Indeed, the scientific survey time series used here started after the expansion of the fishing industry in this region and a period of high fishing pressure. The EcApRHA project has initiated work on setting reference values for the inclusion and testing of the MTL indicator in the Nested Environmental Assessment Tool (developed by the DEVOTES project). Arroyo et al. (2017) has underlined the need for expert knowledge to be shared on sub-regional ecosystems prior to the definition of sub-regional reference conditions or reference values. This work undertaken withinEcApRHA project proposed a way of defining reference values based on current knowledge of the ecosystems studied. However, these reference values need to be further refined. Application of the MTL indicator on a finer geographic scale, integrating the MTL with information on fishing pressure, is a promising approach that could help refine reference condition and assessment values in future work.

Knowledge Gaps

Understanding the feeding relationships between species occurring in a specific region is essential to conduct a robust assessment of the food web, whether using the MTL indicator or any other Trophic Level based indicator. It is not currently possible to apply the MTL indicator anywhere other than the Bay of Biscay, owing to a lack of detailed information on feeding interactions and region-specific Trophic Level (TL) values. Repeated dietary studies implemented at the (sub)-regional scale and the computation of TL values would help fill this gap in knowledge.

To improve the assessment of the state of the food web, further work on the MTL indicator could include: incorporating additional datasets on biological compartments that are not currently included (e.g. benthos, mammals, or birds); investigating the influence of various anthropogenic pressures; exploring finer geographic scales; and further defining assessment values.

In order to establish trophic relationships more accurately so that TL values can be determined, data are required on species feeding habits and their variations with ontogeny, where this is lacking. Comprehensive datasets on the feeding ecology of many of the key species in marine food webs are currently insufficient for the purposes of conducting this type of assessment, and this is especially the case for species at lower trophic levels.

The first step in filling these gaps in knowledge of food web structure and connectivity is to extend data collection on feeding ecology at a sub-regional scale (Carafa et al., 2007; Moloney et al., 2010; Rossberg et al., 2011). Large-scale surveys (such as the Data Collection Framework (DCF) bottom-trawl and pelagic surveys) could aim at systematically collecting; as many species as possible in the food web; and data for dietary analyses using stomach content and / or stable isotope analyses for the different size classes of a given species (in order to account for the ontogeny effect on species TL values). Analyses of stomach contents can provide accurate information on the species consumed as well as serving as a sampler of the smaller invertebrates and other benthic components not retained by the sampling gear and so not represented in the survey data. Stable isotope analyses indicate trophic level based on a longer feeding signature, and so provide a broader view of feeding strategy of a given species.

Both approaches provide complementary information about food web functioning. Repeat dietary analyses also provide information on spatial and temporal variability in the trophic relationships of the species present in a given ecosystem and thus, of their TL values. Such data would be useful not only for strengthening the MTL indicator, but also for all trophic-level and food-web based indicators as well as for models.

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