Staff Publications

Staff Publications

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    'Staff publications' is the digital repository of Wageningen University & Research

    'Staff publications' contains references to publications authored by Wageningen University staff from 1976 onward.

    Publications authored by the staff of the Research Institutes are available from 1995 onwards.

    Full text documents are added when available. The database is updated daily and currently holds about 240,000 items, of which 72,000 in open access.

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    Individual and cohort-specific gut microbiota patterns associated with tissue-specific insulin sensitivity in overweight and obese males
    Hermes, Gerben D.A. ; Reijnders, Dorien ; Kootte, Ruud S. ; Goossens, Gijs H. ; Smidt, Hauke ; Nieuwdorp, Max ; Blaak, Ellen E. ; Zoetendal, Erwin G. - \ 2020
    Scientific Reports 10 (2020)1. - ISSN 2045-2322

    A growing body of evidence suggests that the human gut microbiota plays a role in the development of obesity and related metabolic diseases. However, there is little consensus between studies, which could be due to biological as well as technical variation. In addition, little human data are available to investigate whether tissue-specific insulin sensitivity is related to specific microbial patterns. We examined this relation in two independent cohorts of overweight and obese pre-diabetic men, using phylogenetic microarray data and hepatic, peripheral and adipose tissue insulin sensitivity that were determined by a two-step hyperinsulinemic-euglycemic clamp with [6,6-2H2]-glucose tracer infusion. Despite a prominent subject-specific microbiota, we found significant associations of microbial taxa with tissue-specific insulin sensitivity using regression analysis. Using random forests we found moderate associations with other measures of glucose homeostasis in only one of the cohorts (fasting glucose concentrations AUC = 0.66 and HbA1c AUC = 0.65). However, all findings were cohort-specific due to pronounced variation in microbiota between cohorts, suggesting the existence of alternative states for dysbiosis in metabolic syndrome patients. Our findings suggest individual or group related dynamics, instead of universal microbiota signals, related to the host when the overweight or obese state has already developed and argue that care should be taken with extrapolating significant correlations from single cohorts, into generalized biological relevance.

    Herinneringen aan Wim Wolff
    Dankers, Norbert ; Reijnders, Peter ; Smit, Cor ; Veen, Jan - \ 2019
    Den Helder : Wageningen Marine Research (Wageningen Marine Research rapport 19.004) - 28
    Top-down pressure on a coastal ecosystem by harbor seals
    Aarts, Geert ; Brasseur, Sophie ; Poos, Jan Jaap ; Schop, Jessica ; Kirkwood, Roger ; Kooten, Tobias Van; Mul, Evert ; Reijnders, Peter ; Rijnsdorp, Adriaan D. ; Tulp, Ingrid - \ 2019
    Ecosphere 10 (2019)1. - ISSN 2150-8925 - p. e02538 - e02538.
    demersal fish - diet - harbor seal - impact - intertidaL - Phoca vitulina - predation pressure - sealing - Subtidal - top-down regulation - top predator
    Historic hunting has led to severe reductions of many marine mammal species across the globe. After hunting ceased, some populations have recovered to pre-exploitation levels and may have regained their prominent position as top predator in marine ecosystems. Also, the harbor seal population in the international Wadden Sea grew at an exponential rate following a ban on seal hunting in 1960s, and the current number ~38,000 is close to the historic population size. Here we estimate the impact of the harbor seal predation on the fish community in the Wadden Sea and nearby coastal waters. Fish remains in fecal samples and published estimates on the seal’s daily energy requirement were used to estimate prey selection and the magnitude of seal consumption. Estimates on prey abundance were derived from demersal fish surveys, and fish growth was estimated using a Dynamic Energy Budget model. GPS tracking provided information on where seals most likely caught their prey. Harbor seals hauling-out in the Dutch Wadden Sea fed predominantly on demersal fish, for example, flatfish species (flounder, sole, plaice, dab), but also on sandeel, cod, and whiting. Although harbor seals acquire the majority of prey further offshore in the adjacent North Sea, and only spend 14% of their diving time in the Wadden Sea, seal predation was still estimated to cause an average annual mortality of 43% of the remaining fish in the Wadden Sea and 60% in the nearby shallow coastal waters (<20 m). There were however large sources of uncertainty in the estimated impact of seals on fish, including the migration of fish between the North Sea and Wadden Sea, and catchability estimates of the fish survey sampling gear, particularly for sandeel and other pelagic fish species. Our estimate suggested a considerable top-down pressure by harbor seals on demersal fish. However, predation by seals may also alleviate density-dependent competition between the remaining fish, allowing for increased fish growth, and partly compensating for the reduction in fish numbers. This study shows that recovering coastal marine mammal populations could become an important component in the functioning of shallow coastal ecosystems.
    Effects of gut microbiota manipulation on ex vivo lipolysis in human abdominal subcutaneous adipocytes
    Jocken, Johan W.E. ; Reijnders, Dorien ; Canfora, Emanuel E. ; Boekschoten, Mark V. ; Plat, Joghum ; Goossens, Gijs H. ; Blaak, Ellen E. - \ 2018
    Adipocyte 7 (2018)2. - ISSN 2162-3945 - p. 106 - 112.
    Adipose Tissue - Fatty acid metabolism - Insulin resistance - Lipolysis - Microbiota - Obesity

    The intestinal microbiota may contribute to the development of obesity by affecting host lipid metabolism and insulin sensitivity. To investigate the effects of microbiota manipulation on ex vivo basal and β-adrenergically-stimulated lipolysis in human adipocytes, 36 obese men were randomized to amoxicillin (broad-spectrum antibiotic), vancomycin (narrow-spectrum antibiotic) or placebo treatment (7 d, 1500 mg/d). Before and after treatment, ex vivo adipose tissue lipolysis was assessed under basal conditions and during stimulation with the non-selective β-agonist isoprenaline using freshly isolated mature adipocytes. Gene (targeted microarray) and protein expression were analyzed to investigate underlying pathways. Antibiotics treatment did not significantly affect basal and maximal isoprenaline-mediated glycerol release from adipocytes. Adipose tissue β-adrenoceptor expression or post-receptor signalling was also not different between groups. In conclusion, 7 d oral antibiotics treatment has no effect on ex vivo lipolysis in mature adipocytes derived from adipose tissue of obese insulin resistant men.

    Improved functional annotations are key to realize the potential of algal biotechnology
    Reijnders, Maarten J.M.F. - \ 2018
    Wageningen University. Promotor(en): V.A.P. Martins dos Santos; G. Eggink, co-promotor(en): P.J. Schaap. - Wageningen : Wageningen University - ISBN 9789463435352 - 194

    Chapter 1 provides the background for the thesis. In it, I provide a short overview of what biotechnology is and how it has been utilized it for thousands of years. I then address how modern biotechnology has evolved over the past few decades. Its progress has been triggered by the discovery of nucleic acids and marked by a focus on genetic understanding of cell and organism function and on the subsequent manipulation to ultimately benefit society in one way or another. Furthermore, computational biology has been increasingly important to determine the success of biotechnological research, in for example an anti-malarial drug- producing yeast. However, for microalgae, which are very promising organisms for biotechnological applications, there are essentially no successful commercialized examples of modern biotechnology. The chapter further discusses the importance of computationally predicting protein functions and its role in bioinformatics and systems biology research, concluding that this is one of the challenges for microalgal biotechnology. This topic is discussed in all chapters of this thesis, as its overarching goal is to develop and deploy tools and methodologies that lead to increase our understanding of microalgae as cell factories.

    Chapter 2 is an review on the state of microalgal biotechnology in 2014, of which the major discussion points are still valid, and how bioinformatics and systems biology should be used to further microalgal research. It describes the challenges of microalgal genomics, bioinformatics, and systems biology research. The chapter addresses a few challenges for microalgae in particular: a lack of genomic data, a low amount of validated protein functions, and genome-scale metabolic models largely based off of Arabidopsis thaliana. Suggestions are made on how to overcome these challenges, by for example better utilizing bioinformatics methods and databases. Chapter 3 addresses a specific challenge: the need for accurate annotation of the functions of microalgal proteins. It exposes the lack of understanding we have of their protein functions, with a staggering 90% of their annotations also present in the distantly related plant Arabidopsis thaliana. Finally, this chapter outlines areas in which microalgal protein function prediction can be improved. In Chapter 4, I present CrowdGO, a prediction tool based on the “wisdom of the crowd” principle for protein function prediction that aims to overcome the major problem highlighted in Chapter 3. It operates by taking and merging the existing predictions made by other methods. These merged predictions are then put through a machine learning algorithm which is trained to recognize patterns in these predictions and correlate them to true or false positives. CrowdGO shows significantly higher accuracy, with a p-value < 2.22e-16, over existing prediction methods, as well as an improved precision and recall optimum.

    In Chapter 5 deploy CrowdGO to the genomics of the oleaginous yeast Cutaneotrichosporon curvatus, which thus serves as a real biological test case for the method. Comparisons between the CrowdGO annotated C. curvatus proteins to the existing ones of a related yeast showcases the potential of CrowdGO. GO enrichment analysis of C. curvatus between transcriptomes of normal growth conditions and nitrogen starved conditions shows cell maintenance functions enriched during the first, and stress functions enriched during the latter. This is in line with what one would expect for an oleaginous eukaryote and reassures us that the CrowdGO annotations are reliable. The CrowdGO annotations are further used in a manual annotation pipeline, which we used to manually curate over 700 metabolic C. curvatus proteins. These are used together with differential expression analysis to characterize triacylglycerol synthesis during nitrogen starvation conditions. Only one enzyme was missing after the first round of annotations, displaying a high recall for enzymes when using the manual annotation pipeline.

    In chapter 6 we study the comparative genomics between different Botryococcus braunii strains, an oleaginous eukaryote that either makes large amount of polysaccharides or hydrocarbons based on the strain. In this chapter, all methodologies discussed or developed in the previous chapters are used to try and identify the key genetic differences between the two strains that lead to polysaccharide or hydrocarbon synthesis. We use CrowdGO to annotate all the proteins, and perform manual annotation on a thousand metabolic proteins. These are used in conjunction with quantitative proteomics analysis of several conditions including light and dark, different nitrogen levels, and different cell phases. By combining the manual annotations and the proteomics analysis, we were able to characterize several key pathways including the non-mevalonate pathway, fucose synthesis pathway, and the TCA cycle. Analysis of these pathways reveals key differences in the expression of enzymes that are likely to correspond to polysaccharide or hydrocarbon synthesis. Apart from revealing some key features about Botryococcus braunii, this chapter serves as a template for future large-scale microalgal research.

    Chapter 7 is a general discussion on the thesis. In it, I discuss how the work in this thesis relates to the SPLASH project for microalgae. Furthermore, I discuss how microalgal annotations can still be improved through the use of various stages of bioinformatics, systems biology, and synthetic / metabolic engineering research. Finally, I discuss how microalgae have potential as protein farms, and how it might be possible to unlock this potential.

    Short-Term Microbiota Manipulation and Forearm Substrate Metabolism in Obese Men : A Randomized, Double-Blind, Placebo-Controlled Trial
    Reijnders, Dorien ; Goossens, Gijs H. ; Hermes, Gerben D.A. ; Smidt, Hauke ; Zoetendal, Erwin G. ; Blaak, Ellen E. - \ 2018
    Obesity Facts 11 (2018). - ISSN 1662-4025 - p. 318 - 326.

    Objective: To investigate the impact of gut microbiota manipulation on fasting and postprandial skeletal muscle metabolism in humans. Methods: 40 obese, insulin-resistant males were randomized to amoxicillin (broad-spectrum antibiotic), vancomycin (narrow-spectrum antibiotic), or placebo (7 days, 1,500 mg/day). Before and after treatment, forearm blood flow and metabolite fluxes across forearm muscle were measured under fasting and postprandial (high-fat mixed-meal) conditions. Results: Vancomycin decreased bacterial diversity, reduced the abundance of Gram-positive Firmicutes, and increased the abundance of Gram-negative Proteobacteria, whereas amoxicillin did not affect microbial composition. Neither vancomycin nor amoxicillin treatment affected fasting and postprandial plasma glucose, free fatty acid (FFA), triacylglycerol (TAG), glycerol, lactate, and insulin concentrations or forearm blood flow. Fasting and postprandial net forearm muscle glucose uptake and the release of lactate were not significantly altered by antibiotic treatment as compared to placebo. Finally, antibiotic treatment did not change fasting and postprandial glycerol, FFA, and TAG fluxes across forearm muscle. Conclusion: The present study demonstrates that short-term antibiotic treatment has no effects on fasting and postprandial forearm substrate metabolism and blood flow in obese men with impaired glucose metabolism. These data suggest that short-term strategies targeting the gut microbiota to improve metabolic health may not be effective in obese humans.

    Harbour seals are regaining top-down control in a coastal ecosystem
    Aarts, G.M. ; Brasseur, S.M.J.M. ; Poos, J.J. ; Schop, Jessica ; Kirkwood, R.J. ; Kooten, T. van; Mul, Evert ; Reijnders, P.J.H. ; Rijnsdorp, A.D. ; Tulp, I.Y.M. - \ 2018
    BioRxiv
    Historic hunting has led to severe reductions of many marine mammal species across the globe. After hunting ceased, some populations have recovered to pre-exploitation levels, and may again act as a top-down regulatory force on marine ecosystems. Also the harbour seal population in the international Wadden Sea grew at an exponential rate following a ban on seal hunting in 1960's, and the current number ~38,000 is close to the historic population size. Here we estimate the impact of the harbour seal predation on the fish community in the Wadden Sea and nearby coastal waters. Fish remains in faecal samples and published estimates on the seal's daily energy requirement were used to estimate prey selection and the magnitude of seal consumption. Estimates on prey abundance were derived from demersal fish surveys, and fish growth was estimated using a Dynamic Energy Budget model. GPS tracking provided information on where seals most likely caught their prey. Harbour seals from the Dutch Wadden Sea fed predominantly on demersal fish, e.g. flatfish species (flounder, sole, plaice, dab), but also sandeel, cod and whiting. Total fish biomass in the Wadden Sea was insufficient to sustain the estimated prey consumption of the entire seal population year-round. This probably explains why seals also acquire prey further offshore in the adjacent North Sea, only spending 13% of their diving time in the Wadden Sea. Still, seal predation was estimated to cause an average annual mortality of 43% and 60% on fish in the Wadden Sea and adjacent coastal zone, respectively. There were however large sources of uncertainty in the estimate, including the migration of fish between the North Sea and Wadden Sea, and catchability estimates of the fish survey sampling gear, particularly for sandeel and other pelagic fish species. Our estimate suggested a considerable top-down control by harbour seals on demersal fish. However predation by seals may also alleviate density-dependent competition between the remaining fish, increasing fish growth, and partly compensating for the reduction in fish numbers. This study shows that recovering coastal marine mammal populations could potentially become an important component in the functioning of shallow coastal systems.
    Echoes from the past : Regional variations in recovery within a harbour seal population
    Brasseur, Sophie M.J.M. ; Reijnders, Peter J.H. ; Cremer, Jenny ; Meesters, Erik ; Kirkwood, Roger ; Jensen, Lasse Fast ; Jeβ, Armin ; Galatius, Anders ; Teilmann, Jonas ; Aarts, Geert - \ 2018
    PLoS ONE 13 (2018)1. - ISSN 1932-6203
    Terrestrial and marine wildlife populations have been severely reduced by hunting, fishing and habitat destruction, especially in the last centuries. Although management regulations have led to the recovery of some populations, the underlying processes are not always well understood. This study uses a 40-year time series of counts of harbour seals (Phoca vitulina) in the Wadden Sea to study these processes, and demonstrates the influence of historical regional differences in management regimes on the recovery of this population. While the Wadden Sea is considered one ecologically coupled zone, with a distinct harbour seal population, the area is divided into four geo-political regions i.e. the Netherlands, Lower Saxony including Hamburg, Schleswig-Holstein and Denmark. Gradually, seal hunting was banned between 1962 and 1977 in the different regions. Counts of moulting harbour seals and pup counts, obtained during aerial surveys between 1974 and 2014, show a population growth from approximately 4500 to 39,000 individuals. Population growth models were developed to assess if population growth differed between regions, taking into account two Phocine Distemper Virus (PDV) epizootics, in 1988 and 2002 which seriously affected the population. After a slow start prior to the first epizootic, the overall population grew exponentially at rates close to assumed maximum rates of increase in a harbour seal population. Recently, growth slowed down, potentially indicative of approaching carrying capacity. Regional differences in growth rates were demonstrated, with the highest recovery in Netherlands after the first PDV epizootic (i.e. 17.9%), suggesting that growth was fuelled by migration from the other regions, where growth remained at or below the intrinsic growth rate (13%). The seals’ distribution changed, and although the proportion of seals counted in the German regions declined, they remained by far the most important pupping region, with approximately 70% of all pups being born there. It is hypothesised that differences in hunting regime, preceding the protection in the 1960’s and 1970’s, created unbalance in the distribution of breeding females throughout the Wadden Sea, which prevailed for decades. Breeding site fidelity promoted the growth in pup numbers at less affected breeding sites, while recolonisation of new breeding areas would be suppressed by the philopatry displayed by the animals born there. This study shows that for long-lived species, variable management regimes in this case hunting regulations, across a species’ range can drive population dynamics for several generations.
    Impact of harbour seals on declining fish stocks in and around the Wadden Sea
    Aarts, G.M. ; Brasseur, S.M.J.M. ; Poos, J.J. ; Schop, Jessica ; Mul, Evert ; Kooten, T. van; Kirkwood, R.J. ; Reijnders, P.J.H. ; Rijnsdorp, A.D. ; Tulp, I.Y.M. - \ 2017
    In: Abstracts book - 10th International Symposium Flatfish. - - p. 54 - 54.
    While some marine mammals haven't recovered from historic hunting, others have recovered rapidly to presumed pre-exploitation levels. Also harbour sea ls in the Wadden Sea grew at a rapid rate of 12% p.a. following the ban on seal hunting. As a consequence, - 40,000 seals are currently residing in the international Wadden Sea, and collectively, they might act as an important top-down regulatory force. The objective of this study was to estimate the potential impact of predation by harbour seals in The Netherlands on the f ish community in the Wadden Sea and nearby coastal waters. Hard fish remains in faecal samples and estimates on daily energy requirement were used to estimate prey selection and the magnitude of seal predation. GPS tracking data provided information on where they most likely caught their prey. Estimates of abundance and growth of demersal fish species, derived from fish surveys, provided estimates on total prey availability. Harbour seals in the Wadden Sea were found to feed predominantly on flatfish, flounder, sole, plaice and dab, sandeel, fivebearded rockling, whiting, cod, dragonet and bullrout. Given their high daily food requirement, the study suggests there is insufficient food available in the Wadden Sea to sustain the entire harbour seal population. Although harbour seals only spend 10-20% of their time foraging in the Wadden Sea, they may potentially reduce the demersal fish biomass by 50% in the period Sept-June. There are however large sources of uncerta inty, e.g. t he catchability of the fishing sampling gear, particularly for the larger fish specimens, and movement of f ish between the North Sea and Wadden Sea. These resu lts suggest it is important to take the harbour seal prey consumption into account when understanding the functioning of the Wadden Sea ecosystem, which acts as an important nursery area for both seals and several fish species.
    Pollution
    Reijnders, P.J.H. ; Borrell, P.J.H. ; Franeker, J.A. van; Aguilar, A. - \ 2017
    In: Encyclopedia of marine mammals / Wuersig, B., Thewissen, J.G.M., Kovacs, K.M., London : Academic Press - ISBN 9780128043271 - p. 746 - 759.
    Awareness of the threat of environmental contaminants to marine mammals is widespread. High concentration of certain compounds in the tissues of these animals has been associated with organ anomalies, impaired reproduction, and immune function and, as a consequence of the latter, with the occurrence of large die-offs among seal and cetacean species. This prompted alertness about the impact of pollution and stimulated research into the relationship between observed effects and pollutants. However, a clear causeand- effect relationship between residue levels of contaminants and observed effects has been might elicit a serious backlash, because in the absence of evidence, concerns expressed are easily interpreted as fear-mongering. This might lead to inertia in taking appropriate management measures, something which is undesirable for conservation and wise environmental management. The main reasons for the lack of proof of the impact of pollution on marine mammals are the difficulty or impossibility of experimenting in laboratory conditions with these animals, and
    the frequent occurrence of confounding factors that hamper the establishment of cause-and-effect relationships. Examples of these factors are the fact that pollution always occurs as a mixture of a large number of chemical compounds, the lack of data on biological variables influencing tissue levels, low quality of the samples usually analyzed, the limited information on pathology and
    occurrence of disease in the specimens studied, the absence of reliable population data, and the lack of information on the influence of other detrimental factors such as concurrent anthropogenic and natural changes acting as environmental, ecological, and physiological stressors.
    Seals in motion : how movements drive population development of harbour seals and grey seals in the North Sea
    Brasseur, Sophie Marie Jacqueline Michelle - \ 2017
    Wageningen University. Promotor(en): P.J.H. Reijnders, co-promotor(en): G.M. Aarts. - Wageningen : Wageningen University - ISBN 9789463436120 - 176
    seals - phoca vitulina - halichoerus grypus - pinnipedia - population biology - animal ecology - wadden sea - netherlands - zeehonden - phoca vitulina - halichoerus grypus - pinnipedia - populatiebiologie - dierecologie - waddenzee - nederland
    The harbour seal Phoca vitulina and the grey seal Halichoerus grypus have been inhabitants of the Wadden Sea since millennia. Prehistoric findings indicate the presence of both species around 5000 BC. This changed dramatically in the mid Middle-Ages as around 1500 AC, the grey seal disappeared from the Wadden Sea as a consequence of persecution. With growing hunting pressure, especially in the 20th century and concurrent habitat destruction and pollution, the harbour seals reached all time low numbers in the 1970’s. Banning the hunt in countries around the southern North Sea, limiting pollution and protection from disturbance allowed the harbour seals to slowly recover and the grey seals to return to the Wadden Sea. In this thesis the population trends and inherent dynamics of the recovery for both species is described. Also the movements of individual animals are studied to explain possible mechanisms.
    Identification of methylated GnTI-dependent N-glycans in Botryococcus brauni
    Schulze, Stefan ; Urzica, Eugen ; Reijnders, Maarten J.M.F. ; Geest, Henri van de; Warris, Sven ; Bakker, Linda V. ; Fufezan, Christian ; Martins dos Santos, Vitor A.P. ; Schaap, Peter J. ; Peters, Sander A. ; Hippler, Michael - \ 2017
    New Phytologist 215 (2017)4. - ISSN 0028-646X - p. 1361 - 1369.
    Botryococcus braunii - gene ontology annotation - mass spectrometry - N-glycosylation - post-translational modification
    In contrast to mammals and vascular plants, microalgae show a high diversity in the N-glycan structures of complex N-glycoproteins. Although homologues for β1,2-N-acetylglucosaminyltransferase I (GnTI), a key enzyme in the formation of complex N-glycans, have been identified in several algal species, GnTI-dependent N-glycans have not been detected so far. We have performed an N-glycoproteomic analysis of the hydrocarbon oils accumulating green microalgae Botryococcus braunii. Thereby, the analysis of intact N-glycopeptides allowed the determination of N-glycan compositions. Furthermore, insights into the role of N-glycosylation in B. braunii were gained from functional annotation of the identified N-glycoproteins. In total, 517 unique N-glycosylated peptides have been identified, including intact N-glycopeptides that harbored N-acetylhexosamine (HexNAc) at the nonreducing end. Surprisingly, these GnTI-dependent N-glycans were also found to be modified with (di)methylated hexose. The identification of GnTI-dependent N-glycans in combination with N-glycan methylation in B. braunii revealed an uncommon type of N-glycan processing in this microalgae.
    Doorontwikkeling van de precisielandbouw in Nederland : een 360 graden-verkenning van de stand van zaken rond informatie-intensieve landbouw en in het bijzonder de plantaardige, openluchtteelt
    Wal, T. van der; Vullings, L.A.E. ; Zaneveld-Reijnders, J. ; Bink, R.J. - \ 2017
    Wageningen : Wageningen Environmental Research (Wageningen Environmental Research rapport 2820) - 89
    precisielandbouw - landbouw - akkerbouw - drones - winsten - duurzaamheid (sustainability) - wetgeving - nederland - precision agriculture - agriculture - arable farming - drones - profits - sustainability - legislation - netherlands
    A survey of deleterious variants in highly managed commercial layer lines
    Derks, M.F.L. ; Megens, H.J.W.C. ; Bosse, M. ; Gross, Christian ; Reijnders, Marcel ; Ridder, D. de; Groenen, M. - \ 2017
    Survey of deleterious variants in highly managed commercial layer lines
    Derks, M.F.L. ; Megens, H.J.W.C. ; Bosse, M. ; Gross, Christian ; Reijnders, Marcel ; Ridder, D. de; Groenen, M. - \ 2017
    Baardrob Erignatus barbatus
    Brasseur, S.M.J.M. ; Reijnders, P.J.H. - \ 2016
    In: Atlas van de Nederlandse zoogdieren / Broekhuizen, S., van Loon, A.J., Leiden : Naturalis - ISBN 9789050115346 - p. 272 - 273.
    Grijze zeehond Halichoerus grypus
    Brasseur, S.M.J.M. ; Reijnders, P.J.H. - \ 2016
    In: Atlas van de Nederlandse zoogdieren / Broekhuizen, S., van Loon, A.J., Leiden : Naturalis - ISBN 9789050115346 - p. 276 - 278.
    Klapmuts Cystophora cristata
    Brasseur, S.M.J.M. ; Reijnders, P.J.H. - \ 2016
    In: Atlas van de Nederlandse zoogdieren / Broekhuizen, S., van Loon, A.J., Leiden : Naturalis - ISBN 9789050115346 - p. 274 - 275.
    Ringelrob Pusa hispida
    Brasseur, S.M.J.M. ; Reijnders, P.J.H. - \ 2016
    In: Atlas van de Nederlandse zoogdieren / Broekhuizen, S., van Loon, A.J., Leiden : Naturalis - ISBN 9789050115346 - p. 286 - 287.
    Walrus Odobenus rosmarus
    Brasseur, S.M.J.M. ; Reijnders, P.J.H. - \ 2016
    In: Atlas van de nederlandse zoogdieren / Broekhuizen, S., van Loon, A.J., Leiden : Naturalis - ISBN 9789050115346 - p. 207 - 271.
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