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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    The rin, nor and Cnr spontaneous mutations inhibit tomato fruit ripening in additive and epistatic manners
    Wang, Rufang ; Lammers, Michiel ; Tikunov, Yury ; Bovy, Arnaud G. ; Angenent, Gerco C. ; Maagd, Ruud A. de - \ 2020
    Plant Science 294 (2020). - ISSN 0168-9452
    Colorless non-ripening - Fruit ripening - non-ripening - ripening inhibitor - Spontaneous mutation - Tomato

    Tomato fruit ripening is regulated by transcription factors (TFs), their downstream effector genes, and the ethylene biosynthesis and signalling pathway. Spontaneous non-ripening mutants ripening inhibitor (rin), non-ripening (nor) and Colorless non-ripening (Cnr) correspond with mutations in or near the TF-encoding genes MADS-RIN, NAC-NOR and SPL-CNR, respectively. Here, we produced heterozygous single and double mutants of rin, nor and Cnr and evaluated their functions and genetic interactions in the same genetic background. We showed how these mutations interact at the level of phenotype, individual effector gene expression, and sensory and quality aspects, in a dose-dependent manner. Rin and nor have broadly similar quantitative effects on all aspects, demonstrating their additivity in fruit ripening regulation. We also found that the Cnr allele is epistatic to rin and nor and that its pleiotropic effects on fruit size and volatile production, in contrast to the well-known dominant effect on ripening, are incompletely dominant, or recessive.

    Early-life microbiota transplantation affects behavioural responses, serotonin and immune characteristics in chicken lines divergently selected on feather pecking
    Eijk, J.A.J. van der; Rodenburg, T.B. ; Vries, H.J.A. de; Kjaer, J.B. ; Smidt, H. ; Naguib, M. ; Kemp, B. ; Lammers, A. - \ 2020
    Scientific Reports 10 (2020). - ISSN 2045-2322 - 13 p.
    Gut microbiota influences host behaviour and physiology, such as anxiety, stress, serotonergic and immune systems. These behavioural and physiological characteristics are related to feather pecking (FP), a damaging behaviour in chickens that reduces animal welfare and productivity. Moreover, high FP (HFP) and low FP (LFP) lines differed in microbiota composition. However, it is unknown whether microbiota can influence the development of FP. For the first time, we identified the effects of microbiota transplantation on FP, and behavioural and physiological characteristics related to FP. HFP and LFP chicks received sterile saline (control), HFP or LFP microbiota transplantation during the first two weeks post-hatch. Microbiota transplantation influenced behavioural responses of the HFP line during treatment and of the LFP line after treatment. In both lines, homologous microbiota transplantation (i.e., receiving microbiota from their line) resulted in more active behavioural responses. Furthermore, microbiota transplantation influenced immune characteristics (natural antibodies) in both lines and peripheral serotonin in the LFP line. However, limited effects on microbiota composition, stress response (corticosterone) and FP were noted. Thus, early-life microbiota transplantation had immediate and long-term effects on behavioural responses and long-term effects on immune characteristics and peripheral serotonin; however, the effects were dependent on host genotype. Since early-life microbiota transplantation influenced behavioural and physiological characteristics that are related to FP, it could thus influence the development of FP later in life
    Gut microbiota affects behavioural responses of feather pecking selection lines
    Eijk, J.A.J. van der; Naguib, M. ; Kemp, B. ; Lammers, A. ; Rodenburg, T.B. - \ 2019
    In: Book of abstracts of the 70th Annual Meeting of the European Federation of Animal Science (EAAP). - Wageningen Academic Publishers (Book of Abstracts ) - ISBN 9789086863396 - p. 200 - 200.
    Early life environmental factors have a profound impact on an animal’s behavioural development. The gut microbiota could be such a factor as it inuences behavioural characteristics, such as stress and anxiety. Stress sensitivity and fearfulness are related to feather pecking (FP) in chickens, which involves pecking and pulling out feathers of conspecics. Furthermore, high (HFP) and low FP (LFP) lines differ in gut microbiota composition. Yet, it is unknown whether gut microbiota affects FP or behavioural characteristics related to FP. Therefore, HFP and LFP birds orally received a control, HFP or LFP microbiota treatment within 6 hrs post hatch and daily until 2 weeks of age. FP behaviour was observed via direct observations at pen-level between 0-5, 9-10 and 14-15 weeks of age. Birds were tested in novel object (3 days & 5 weeks of age), novel environment (1 week of age), open eld (13 weeks of age) and manual restraint (15 weeks of age) tests. Microbiota transplantation inuenced behavioural responses, but did not affect FP. HFP receiving HFP microbiota tended to approach a novel object sooner and more birds tended to approach than HFP receiving LFP microbiota at 3 days of age. HFP receiving HFP microbiota tended to vocalise sooner compared to HFP receiving control in a novel environment. LFP receiving LFP microbiota stepped and vocalised sooner compared to LFP receiving control in an open eld. Similarly, LFP receiving LFP microbiota tended to vocalise sooner during manual restraint than LFP receiving control or HFP microbiota. Thus, early life microbiota transplantation had short-term effects in HFP birds and long-term effects in LFP birds. Previously, HFP birds had more active responses compared to LFP birds. Thus, in this study HFP birds seemed to adopt behavioural characteristics of donor birds, but LFP birds did not. Interestingly, homologous microbiota transplantation resulted in more active responses, suggesting reduced fearfulness.
    The influence of genetic background on trained innate immunity in chicken macrophages
    Verwoolde, M.B. ; Biggelaar, Robin H.G.A. van den; Baal, J. van; Jansen, Christine A. ; Lammers, A. - \ 2019
    Short-term compensatory growth is observed after delayed nutrition in broiler chickens
    Hollemans, M.S. ; Lammers, A. ; Vries, S. de - \ 2019
    In: Proceedings of the 44th Animal Nutrition Research Forum. - - p. 22 - 23.
    Gut microbiota and feather pecking : Integrating microbiota, behaviour, stress, serotonin and the immune system
    Eijk, Jerine Alexandra Johanna van der - \ 2019
    Wageningen University. Promotor(en): M. Naguib; B. Kemp, co-promotor(en): T.B. Rodenburg; A. Lammers. - Wageningen : Wageningen University - ISBN 9789463951562 - 242

    Early-life factors can have a profound impact on an animal’s behavioural development. An important moment early in life is the rapid microbial colonization of the gut, leading to the establishment of the gut microbiota. From rodent studies it is clear that the gut microbiota influences host behaviour and physiology, such as anxiety, stress, and the serotonergic and immune systems. First indications show that microbiota affects similar behavioural and physiological characteristics in poultry. Through these effects microbiota could alter an animal’s ability to cope with environmental and social challenges, such as those encountered in animal production systems, and could thereby affect the development of damaging behaviours in production animals.

    Fearfulness, stress, and the serotonergic and immune systems have been related to severe feather pecking (FP), a damaging behaviour in chickens which involves pecking and pulling out feathers of conspecifics, negatively affecting animal welfare and productivity. Furthermore, high FP (HFP) and low FP (LFP) selection lines were shown to differ in gut microbial metabolites and microbiota composition determined from caecal droppings. These findings suggest a link between the gut microbiota and FP. Yet, it is unknown whether gut microbiota influences the development of FP. Therefore, the aim of this thesis was to identify effects of gut microbiota on the development of FP. First, I identified behavioural and physiological characteristics in FP genotypes (i.e. HFP and LFP lines) and FP phenotypes (i.e. feather pecker, victim, feather pecker-victim and neutral) that were related to FP and shown to be influenced by microbiota. Second, I identified whether microbiota influences FP, and behavioural and physiological characteristics related to FP.

    Feather pecking genotypes

    FP genotypes differed in behavioural responses, where HFP birds had more active behavioural responses compared to LFP birds (chapter 2, 3 and 6), especially at young age. The active behavioural responses suggest lower fearfulness, higher social and exploration motivation, or higher activity in HFP birds compared to LFP birds. For the stress response, HFP birds struggled later and less, but vocalized sooner and more compared to LFP birds during restraint (chapter 3 and 6). However, FP genotypes did not differ in corticosterone (CORT, the major stress hormone) level after restraint (chapter 3 and 6), suggesting differences in behavioural findings might not be related to stress. With regard to the serotonergic system, whole blood serotonin (5-Hydroxytryptamine or 5-HT) level was measured as indicator for central 5-HT and HFP birds had lower whole blood 5-HT levels compared to LFP birds (chapter 3 and 6). For the immune system, nitric oxide production by monocytes was measured as indicator for the innate immune system, specific antibody level was measured as part of the adaptive immune system, and natural (auto)antibody level was measured, as natural antibodies play an essential role in both innate and adaptive immunity. HFP birds had lower IgM and higher IgG natural (auto)antibody levels, higher nitric oxide production by monocytes, and a tendency for higher IgM and IgG specific antibody levels compared to LFP birds, but did not differ in relative abundances of immune cell subsets (chapter 3, 4 and 6). Moreover, FP genotypes had distinct luminal microbiota composition, where HFP birds had a higher relative abundance of genera of the order Clostridiales, but lower relative abundance of Lactobacillus compared to LFP birds (chapter 5). Yet, FP genotypes did not differ in mucosa-associated microbiota composition. In summary, these findings indicate that divergent selection on FP not only affects FP but also (in)directly affects behavioural responses, peripheral 5-HT level, different arms of the immune system and microbiota composition, but did not affect CORT level.

    Feather pecking phenotypes

    FP phenotypes differed in behavioural responses, where feather peckers tended to have more active behavioural responses compared to victims and neutrals at young age (chapter 2), which suggests lower fearfulness, higher exploration motivation or activity in feather peckers. Furthermore, victims had more active responses compared to neutrals at young age (chapter 2), which suggests lower fearfulness or higher activity in victims. For the stress response, feather peckers tended to have less active behavioural responses compared to neutrals, while victims had more active behavioural responses compared to other phenotypes during restraint (chapter 3). However, FP phenotypes did not differ in CORT level after restraint (chapter 3), suggesting differences in behavioural findings might not be related to stress. With regard to the serotonergic system, feather peckers had higher whole blood 5-HT levels compared to neutrals at adult age (chapter 3). However, FP phenotypes did not differ in natural antibody level (chapter 3) or gut microbiota composition (chapter 5). In summary, these findings indicate that performing and receiving FP is related to more active behavioural responses and that performing FP is further related to high peripheral 5-HT level.

    Feather pecking genotypes vs. phenotypes

    When comparing findings from FP genotypes to those from FP phenotypes, there is a similar relation between high FP and behavioural responses. HFP birds had more active responses compared to LFP birds (chapter 2, 3 and 6) and similarly feather peckers tended to have more active responses compared to victims and neutrals (chapter 2), especially at young age. Furthermore, victims had more active responses compared to other phenotypes at adult age (chapter 3). Thus, activity level might be used as potential indicator for FP at group level or even as indicator for individuals that perform or receive FP. Since feather peckers seem to have more active responses at young age (chapter 2), it would be interesting to identify whether activity level at young age could be used to predict which individuals will become feather peckers.

    There is an opposite relation between high FP and whole blood 5-HT level, where HFP birds had lower whole blood 5-HT levels compared to LFP birds (chapter 3 and 6), while feather peckers had higher whole blood 5-HT levels compared to neutrals (chapter 3). The actual performance of FP might increase peripheral 5-HT level in feather peckers, possibly due to feather eating. Feather peckers often ingest feathers, which may increase peripheral 5-HT level by providing structural components, as the gut releases 5-HT in reaction to these structural components. However, this relation between feather eating and increased peripheral 5-HT level needs further investigation.

    Similar to findings for FP genotypes, FP phenotypes did not differ in CORT level after restraint, indicating that the stress response might not be related to FP in FP genotypes and phenotypes. Furthermore, although differences between FP genotypes were found for the immune system and gut microbiota composition, no such differences were identified for FP phenotypes. This might indicate that differences in immune characteristics and gut microbiota composition are more related to genotype than to actual FP behaviour. Yet, cause and consequence cannot be disentangled from each other based on these findings. Therefore, microbiota transplantation was used to identify gut microbiota effects on the development of FP.

    Microbiota and the development of feather pecking

    Since FP genotypes differed in gut microbiota composition, but FP phenotypes did not, I focussed on FP genotypes for the second objective. The difference in microbiota composition was used to create a HFP and LFP microbiota pool. I identified effects of early-life microbiota transplantation on FP and on the same behavioural and physiological characteristics that were identified in chapter 2, 3 and 5. Newly hatched HFP and LFP chicks received a control treatment, HFP or LFP microbiota daily during the first two weeks post hatch.

    Although limited effects of early-life microbiota transplantation on microbiota composition were found, microbiota transplantation did affect behavioural responses, natural antibody level and whole blood 5-HT level. Thus, microbiota transplantation may have influenced brain, immune and serotonergic system functioning, which (in)directly resulted in differences in behavioural responses, natural antibody level and whole blood 5-HT level.

    With regard to behavioural responses, birds receiving microbiota from their own line (i.e. homologous transplantation) had more active behavioural responses compared to birds receiving microbiota from the other line or control treatment. These active behavioural responses suggest low fearfulness, high exploration and social motivation or activity in birds receiving homologous transplantation. For the stress response, LFP birds receiving homologous transplantation had more active stress responses compared to LFP birds that received HFP microbiota or control treatment. However, microbiota transplantation did not influence CORT level after restraint, suggesting these behavioural findings might not be related to stress.

    With regard to the serotonergic system, LFP birds receiving HFP microbiota tended to have lower whole blood 5-HT level compared to LFP birds receiving control treatment. Yet, microbiota transplantation effects on whole blood 5-HT level do not seem to be explained by the HFP pools’ microbiota composition. Especially since microbiota composition did not differ between treatments within the LFP line.

    For the immune system, birds receiving LFP microbiota had higher IgM natural antibody level compared to birds receiving control treatment, but microbiota transplantation did not affect IgG natural antibody level. Thus, being exposed to an adult microbiota composition might be sufficient to increase IgM natural antibody level. Further research is needed to identify whether microbiota transplantation could influence other immune characteristics in poultry, such as innate and adaptive immune characteristics.

    For the first time, effects of early-life microbiota transplantation on FP were investigated. However, early-life microbiota transplantation had limited effects on FP at young age (till 15 weeks of age) (chapter 6), which might be explained by FP usually increasing from the egg laying period onwards (around 20 weeks of age). Thus, further research is needed to identify effects of microbiota transplantation on FP at adult age.

    Effects of microbiota transplantation depend on genotype

    During treatment, microbiota transplantation influenced behavioural responses in the HFP line, while after treatment it influenced behavioural responses in the LFP line. A potential explanation for this could be that the HFP line has a more responsive immune system (chapter 3, 4 and 6), which responds more strongly to the environment or in this case to microbiota transplantation, with the synthesis and release of pro-inflammatory cytokines. These cytokines in turn act on the brain and alter neurotransmission, thereby potentially influencing behavioural responses. After treatment, microbiota transplantation influenced behavioural responses in the LFP line. These effects do not seem to be explained by the difference in whole blood 5-HT level. Still, it is interesting that LFP birds receiving HFP microbiota had lower whole blood 5-HT levels, as HFP birds had lower whole blood 5-HT levels compared to LFP birds (chapter 3 and 6). This might increase the risk for developing FP in LFP birds receiving HFP microbiota, as high FP is usually related to low whole blood 5-HT level. However, it remains unknown through which pathway microbiota transplantation influences behavioural responses in the LFP line.

    Homologous transplantation

    It is interesting to note that homologous transplantation resulted in birds having more active responses, suggesting reduced fearfulness. Therefore, homologous transplantation could be a potential approach to reduce fearfulness in chickens. High FP is usually related to high fearfulness, indicating that receiving homologous transplantation might reduce FP. Homologous transplantation might result in reduced fearfulness because of a match between transplanted microbiota composition and host genotype as opposed to a mismatch or control treatment. Homologous transplantation could be seen as a type of vertical transmission, where microbiota is transferred from mother hens to chicks. Vertical transmission might play an important role in initiating a host-specific gut microbiota, which might improve host immune system and brain development. Thus, homologous transplantation might have improved immune system and brain development, thereby altering behavioural responses. It would be interesting to identify whether homologous transplantation can be used to reduce fearfulness in poultry and FP in laying hens.

    Role for the immune system in feather pecking?

    There is increasing evidence for a role of the immune system in FP. For FP genotypes, HFP birds had higher specific antibody levels, IgG natural (auto)antibody levels and nitric oxide production by monocytes (chapter 3, 4 and 6), suggesting that high FP is related to a more responsive innate and adaptive immune system. Although it should be noted that FP phenotypes did not differ in natural antibody level (chapter 3). The immune system could be a potential route through which microbiota transplantation affects behavioural responses, especially in HFP birds as they seem to have a more responsive immune system (chapter 3, 4 and 6) and microbiota transplantation had immediate but no long-term effects on behavioural responses in HFP birds (chapter 6). Yet, the exact mechanisms through which the immune system affects the development of FP remain unknown, providing an interesting avenue for further research.

    Feather pecking selection lines as model system

    The HFP and LFP lines were used throughout this thesis as a model system to identify effects of gut microbiota on FP. As these lines are specifically selected on high and low FP, findings with regard to FP should be interpreted with caution when transferring them to other experimental or commercial lines. Overall, high FP was related to low fearfulness, low whole blood 5-HT level and a more responsive immune system in the FP selection lines (chapter 2-6). Previous studies in other experimental and commercial lines show that high FP is related to high fearfulness, low whole blood 5-HT level and a more responsive immune system. Findings with regard to CORT level after restraint are less consistent, with high FP being related to low CORT level after restraint or not. Thus, the FP selection lines seem to show similar relations between high FP, whole blood 5-HT level and immune responsiveness as commercial lines, but an opposite relation between high FP and fearfulness as other experimental and commercial lines. Furthermore, there is inconsistency with regard to the relation between high FP and the stress response. Therefore, findings from the FP selection lines should be used with caution when developing control or preventive methods that are to be applied in production systems. Still, this thesis provides new interesting insights into the relation between FP, behavioural and physiological characteristics related to FP and the gut microbiota.

    Conclusion

    Divergent selection on FP affects fearfulness, activity, peripheral serotonin, immune characteristics and gut microbiota composition, but not the physiological stress response (i.e. corticosterone). FP phenotypes differ in fearfulness, activity and peripheral serotonin, but not in the physiological stress response, immune characteristics or gut microbiota composition. Yet, relations between high FP and behavioural or physiological characteristics are not always similar for FP genotypes and phenotypes, indicating the importance of taking FP genotype and phenotype into account when studying FP.

    Gut microbiota could influence the development of FP, as early-life microbiota transplantation affects fearfulness, activity, peripheral serotonin and immune characteristics, with effects being either immediate or long-term. However, effects depend on age, donor’s and recipient’s genotype, indicating the importance of taking donor’s and recipient’s genotype into account when studying microbiota transplantation effects on behaviour. Overall, this thesis provides new interesting insights into the relationship between gut microbiota, host behaviour and physiology in poultry, which could further be of interest for other species.

    Chicken lines divergently selected on feather pecking differ in immune characteristics
    Eijk, Jerine A.J. van der; Verwoolde, Michel B. ; Vries Reilingh, Ger de; Jansen, Christine A. ; Rodenburg, Bas ; Lammers, Aart - \ 2019
    Physiology and Behavior 212 (2019). - ISSN 0031-9384
    Feather pecking - Immune system - Natural (auto)antibodies - Nitric oxide production - Specific antibodies

    It is crucial to identify whether relations between immune characteristics and damaging behaviors in production animals exist, as these behaviors reduce animal welfare and productivity. Feather pecking (FP) is a damaging behavior in chickens, which involves hens pecking and pulling at feathers of conspecifics. To further identify relationships between the immune system and FP we characterized high FP (HFP) and low FP (LFP) selection lines with regard to nitric oxide (NO) production by monocytes, specific antibody (SpAb) titers, natural (auto)antibody (N(A)Ab) titers and immune cell subsets. NO production by monocytes was measured as indicator for innate pro-inflammatory immune functioning, SpAb titers were measured as part of the adaptive immune system and N(A)Ab titers were measured as they play an essential role in both innate and adaptive immunity. Immune cell subsets were measured to identify whether differences in immune characteristics were reflected by differences in the relative abundance of immune cell subsets. Divergent selection on FP affected NO production by monocytes, SpAb and N(A)Ab titers, but did not affect immune cell subsets. The HFP line showed higher NO production by monocytes and higher IgG N(A)Ab titers compared to the LFP line. Furthermore the HFP line tended to have lower IgM NAAb titers, but higher IgM and IgG SpAb titers compared to the LFP line. Thus, divergent selection on FP affects the innate and adaptive immune system, where the HFP line seems to have a more responsive immune system compared to the LFP line. Although causation cannot be established in the present study, it is clear that relationships between the immune system and FP exist. Therefore, it is important to take these relationships into account when selecting on behavioral or immunological traits.

    Early life microbiota transplantation affects behaviour and peripheral serotonin in feather pecking selection lines
    Eijk, J.A.J. van der; Naguib, M. ; Kemp, B. ; Lammers, A. ; Rodenburg, T.B. - \ 2019
    In: Proceedings of the 53rd Congress of the International Society for Applied Ethology (ISAE). - Wageningen, The Netherlands : Wageningen Academic Publishers - ISBN 9789086863389 - p. 98 - 98.
    Early life environmental factors have a profound impact on an animal’s behavioural andphysiological development. In animal husbandry, early life factors that interfere with thebehavioural and physiological development could lead to the development of damagingbehaviours. The gut microbiota could be such a factor as it influences behaviour, such as stressand anxiety, and physiology, such as the serotonergic system. Stress sensitivity, fearfulness andserotonergic system functioning are related to feather pecking (FP), a damaging behaviourin chickens which involves pecking and pulling out feathers of conspecifics. Furthermore,high (HFP) and low FP (LFP) lines differ in gut microbiota composition. Yet, it is unknownwhether gut microbiota affects FP or behavioural and physiological characteristics related toFP. Therefore, HFP and LFP chicks orally received 100μL of a control, HFP or LFP microbiotatreatment within 6 hrs post hatch and daily until 2 weeks of age (n=96 per group) using apipette. FP behaviour was observed via direct observations at pen-level between 0-5, 9-10 and14-15 weeks of age. Birds were further tested in a novel object test at 3 days and 5 weeks of age,a novel environment test at 1 week of age, an open field test at 13 weeks of age and a manualrestraint test at 15 weeks of age after which whole blood was collected for serotonin analysis. Weanalysed treatment effects within lines using mixed models with treatment, batch, sex, observerand test time as fixed factors and pen within treatment as random factor or Kruskal-Wallistests. Early life microbiota transplantation influenced behavioural responses and peripheralserotonin, but did not affect FP. HFP receiving HFP microbiota tended to approach a novelobject sooner and more birds tended to approach than HFP receiving LFP microbiota at3 days of age (P<0.1). HFP receiving HFP microbiota tended to vocalise sooner comparedto HFP receiving control (P<0.1) in a novel environment. LFP receiving LFP microbiotastepped and vocalised sooner compared to LFP receiving control (P<0.05) in an open field.Similarly, LFP receiving LFP microbiota tended to vocalise sooner during manual restraintthan LFP receiving control or HFP microbiota (P<0.1). LFP receiving HFP microbiota tendedto have lower serotonin levels compared to LFP receiving control (P<0.1). Thus, early lifemicrobiota transplantation had short-term effects (during treatment) in HFP birds and longtermeffects (after treatment) in LFP birds. Previously, HFP birds had more active responsesand lower serotonin levels compared to LFP birds. Thus, in this study HFP birds seemed toadopt behavioural characteristics of donor birds, while LFP birds seemed to adopt physiologicalcharacteristics (i.e. serotonin level) of donor birds. Interestingly, homologous microbiotatransplantation resulted in more active responses, suggesting reduced fearfulness.
    Differences in gut microbiota composition of laying hen lines divergently selected on feather pecking
    Eijk, J.A.J. van der; Vries, H.J.A. de; Kjaer, Joergen B. ; Naguib, M. ; Kemp, B. ; Smidt, H. ; Rodenburg, T.B. ; Lammers, A. - \ 2019
    Poultry Science 98 (2019)12. - ISSN 0032-5791 - p. 7009 - 7021.
    Feather pecking (FP), a damaging behavior where laying hens peck and pull at feathers of conspecifics, is multifactorial and has been linked to numerous behavioral and physiological characteristics. The gut microbiota has been shown to influence host behavior and physiology in many species, and could therefore affect the development of damaging behaviors, such as FP. Yet, it is unknown whether FP genotypes (high FP [HFP] and low FP [LFP] lines) or FP phenotypes (i.e., individuals differing in FP, feather peckers and neutrals) differ in their gut microbiota composition. Therefore, we identified mucosa-associated microbiota composition of the ileum and cecum at 10 and 30 wk of age. At 30 wk of age, we further identified luminal microbiota composition from combined content of the ileum, ceca, and colon. FP phenotypes could not be distinguished from each other in mucosa-associated or luminal microbiota composition. However, HFP neutrals were characterized by a higher relative abundance of genera of Clostridiales, but lower relative abundance of Lactobacillus for the luminal microbiota composition compared to LFP phenotypes. Furthermore, HFP neutrals had a higher diversity and evenness for the luminal microbiota compared to LFP phenotypes. FP genotypes could not be distinguished from each other in mucosa-associated microbiota composition. Yet, FP genotypes could be distinguished from each other in luminal microbiota composition. HFP birds were characterized by a higher relative abundance of genera of Clostridiales, but lower relative abundance of Staphylococcus and Lactobacillus compared to LFP birds. Furthermore, HFP birds had a higher diversity and evenness for both cecal mucosa-associated and luminal microbiota compared to LFP birds at adult age. In conclusion, we here show that divergent selection on FP can (in)directly affect luminal microbiota composition. Whether differences in microbiota composition are causal to FP or a consequence of FP remains to be elucidated.
    Combining tree species and decay stages to increase invertebrate diversity in dead wood
    Andringa, Joke I. ; Zuo, Juan ; Berg, Matty P. ; Klein, Roy ; van't Veer, Jip ; Geus, Rick de; Beaumont, Marco de; Goudzwaard, Leo ; Hal, Jurgen van; Broekman, Rob ; Logtestijn, Richard S.P. van; Li, Yikang ; Fujii, Saori ; Lammers, Mark ; Hefting, Mariet M. ; Sass-Klaassen, Ute ; Cornelissen, Johannes H.C. - \ 2019
    Forest Ecology and Management 441 (2019). - ISSN 0378-1127 - p. 80 - 88.
    Biodiversity - Chilipoda - Coarse woody debris - Coleoptera - Diplopoda - Habitat heterogeneity - Invertebrates - Isopoda - Managed forest - Wood decomposition

    Dead wood availability and the variability in dead wood quality, i.e. tree species and decay stages, are often low in managed forests, which negatively affects biodiversity of invertebrate species. Leaving more (coarse) dead wood can increase invertebrate richness, but it remains unclear how many and which combinations of tree taxa and decay stages are required to optimize niche heterogeneity in managed forests. We investigated the diversity of the main arthropod groups associated with dead wood, i.e. millipedes, centipedes, isopods and beetles, through the first four years of decomposition of logs of twenty common temperate tree species placed in the “common garden” experiment LOGLIFE. We hypothesized that (1) invertebrate richness for combinations of a given number of tree species would be promoted by mixing both tree species and decay period and that (2) invertebrate richness increases up to a saturation point with more tree species at different decay stages added. We also hypothesized that (3) an increase in phylogenetic distance among the tree species in combinations would promote their overall invertebrate diversity. We found that the better combinations, in terms of invertebrate richness, after one and two years of decay, but not after four years, consisted of a mix of gymnosperms and angiosperms, indicating that variation in tree species is especially important during the initial decomposition period. The best combinations in terms of invertebrate richness consisted of at least one tree species from each decay period, indicating that also variation in the decay stage of the tree is important to promote invertebrate diversity. We observed that at least four wood types were required to approach the 95% saturation point for species richness. The third hypothesis, that dissimilarity in phylogenetic position could be a predictive tool for increasing invertebrate richness in combinations of tree species, was not supported by our results. Thus, in order to maintain diversity of dead wood invertebrates in forests we recommend not only to provide richness in tree species, but also to plant particular combinations of trees (preferably angiosperm-gymnosperm combinations) that differ in the invertebrate communities they typically host and to temporally spread the logging of trees. This way the logging residues cover different resources and habitats at each moment in time, which is likely to result in a large diversity of dead wood invertebrates.

    Early-life microbiota transplantation affects behavioural responses of chicken lines divergently selected on feather pecking
    Eijk, J.A.J. van der; Lammers, A. ; Kemp, B. ; Naguib, M. ; Rodenburg, T.B. - \ 2019
    In: Trade-offs in science – keeping the Balance. - Wageningen University & Research - p. 17 - 17.
    Trained innate immunity in chicken macrophages
    Verwoolde, M.B. ; Biggelaar, Robin H.G.A. van den; Baal, J. van; Jansen, Christine A. ; Lammers, A. - \ 2019
    In: Trade-offs in science – keeping the Balance. - Wageningen University & Research - p. 27 - 27.
    Re-evaluation of transcription factor function in tomato fruit development and ripening with CRISPR/Cas9-mutagenesis
    Wang, Rufang ; Rocha Tavano, Eveline Carla da; Lammers, Michiel ; Martinelli, Adriana Pinheiro ; Angenent, Gerco C. ; Maagd, Ruud A. de - \ 2019
    Scientific Reports 9 (2019)1. - ISSN 2045-2322

    Tomato (Solanum lycopersicum) is a model for climacteric fleshy fruit ripening studies. Tomato ripening is regulated by multiple transcription factors together with the plant hormone ethylene and their downstream effector genes. Transcription Factors APETALA2a (AP2a), NON-RIPENING (NOR) and FRUITFULL (FUL1/TDR4 and FUL2/MBP7) were reported as master regulators controlling tomato fruit ripening. Their proposed functions were derived from studies of the phenotype of spontaneous mutants or RNAi knock-down lines rather than, as it appears now, actual null mutants. To study TF function in tomato fruit ripening in more detail, we used CRISPR/Cas9-mediated mutagenesis to knock out the encoding genes, and phenotypes of these mutants are reported for the first time. While the earlier ripening, orange-ripe phenotype of ap2a mutants was confirmed, the nor null mutant exhibited a much milder phenotype than the spontaneous nor mutant. Additional analyses revealed that the severe phenotype in the spontaneous mutant is caused by a dominant-negative allele. Our approach also provides new insight into the independent and overlapping functions of FUL1 and FUL2. Single and combined null alleles of FUL1 and FUL2 illustrate that these two genes have partially redundant functions in fruit ripening, but also unveil an additional role for FUL2 in early fruit development.

    Stress response, peripheral serotonin and natural antibodies in feather pecking genotypes and phenotypes and their relation with coping style
    Eijk, Jerine A.J. van der; Lammers, Aart ; Kjaer, J.B. ; Rodenburg, T.B. - \ 2019
    Physiology and Behavior 199 (2019). - ISSN 0031-9384 - p. 1 - 10.
    Feather pecking - genotype - natural antibody - phenotype - serotonin - stress response

    Feather pecking (FP), a serious welfare and economic issue in the egg production industry, has been related to coping style. Proactive and reactive coping styles differ in, among others, the stress response, serotonergic activity and immune activity. Yet, it is unknown whether genetic lines divergently selected on FP (i.e. FP genotypes) or individuals differing in FP (i.e. FP phenotypes) can be categorized into coping styles. Therefore, we determined peripheral serotonin (5-HT) levels, natural antibody (NAb) titers, behavioral and corticosterone (CORT) responses to manual restraint (MR) in FP genotypes (high FP (HFP), low FP (LFP) and unselected control (CON) line) and FP phenotypes (feather pecker, feather pecker-victim, victim and neutral). We further examined the consistency of and relationships between behavioral and physiological measures. FP genotypes differed in behavioral responses to MR, 5-HT levels and NAb titers, but not in CORT levels after MR. HFP birds had less active responses at adolescent age, but more active responses at adult age compared to LFP and CON birds. The CON line had higher 5-HT levels at adolescent age, while the HFP line had lower 5-HT levels than the other lines at adult age. Overall, the HFP line had lower IgM NAb titers, while the LFP line had lower IgG NAb titers compared to the other lines. FP phenotypes differed in behavioral responses to MR and 5-HT levels, but not in CORT levels after MR or NAb titers. Within the HFP line, feather peckers tended to have less active responses compared to neutrals at adolescent age, while victims had more active responses compared to the other phenotypes at adult age. Feather peckers had higher 5-HT levels than neutrals at adult age. Behavioral and CORT responses to MR were not consistent over time, suggesting that responses to MR might not reflect coping style in this study. Furthermore, proactive behavioral responses were correlated with reactive physiological measures and vice versa. Thus, it was not possible to categorize FP genotypes or FP phenotypes into specific coping styles.

    Feather pecking phenotype affects behavioural responses of laying hens
    Eijk, J.A.J. van der; Lammers, A. ; Rodenburg, T.B. - \ 2018
    In: Proceedings of the 52nd Congress of the International Society for Applied Ethology. - Wageningen, The Netherlands : Wageningen Academic Publishers - ISBN 9789086863228 - p. 169 - 169.
    Feather pecking (FP) is a major welfare and economic issue in the egg production industry. It involves hens pecking and pulling at feathers of conspecics, thereby negatively aecting welfare. Behavioural characteristics, such as fearfulness, have been related to FP. Although many studies have identied dierences in fearfulness between lines that dier in FP, the relationship between actual FP behaviour (i.e. FP phenotypes) and fearfulness is not well understood. erefore, we compared responses of birds with diering FP phenotypes to several behavioural tests at young and adult ages. We used birds from a genetic line selected for high feather pecking. FP phenotypes of individual birds were identied via FP observations at 3-4, 12-13, 15-16 and 28-29 weeks of age. e total number of severe feather pecks (SFP) given and received over two subsequent weeks was used to categorize birds as feather peckers (P, SFP given >1), feather pecker-victims (P-V, SFP given and received >1), victims (V, SFP received >1) or neutrals (N, SFP given and received 0 or 1) at each age point. Birds were tested individually in a novel environment (NE) test at 4 weeks of age, an open eld (OF) test at 15 weeks of age and a tonic immobility (TI) test at 13 and 28 weeks of age. Experimenters were blinded to the phenotypes. Data were analysed using linear mixed models, with phenotype and batch as xed factors and pen as a random factor. Test time was added as a xed eect for the NE and OF test. Experimenter was added as a xed eect for the NE and TI test. Testing order was included as a xed eect for the TI test. Phenotype eects were tested for each behavioural test and age separately using the most recent FP phenotype categorization. FP phenotype aected the number of ight attempts (F3, 119=3.18, P<0.05) during the NE test, where victims showed more ight attempts compared to neutrals (V=2.3 vs n=1.6; P<0.05) and tended to show fewer ight attempts compared to feather peckers (V=2.3 vs P=2.7; P<0.1). FP phenotype further tended to aect step frequency (F3, 75=2.64, P<0.1) during the OF test, where feather peckers tended to walk more compared to neutrals (P=24.6 vs n=15.7; P<0.1). No FP phenotype eects were found for the TI test. Feather peckers tended to show more active responses (i.e. tended to show more ight attempts compared to victims and tended to walk more compared to neutrals), which could suggest lower fearfulness, compared to victims at 4 weeks of age and compared to neutrals at 15 weeks of age. ese ndings give rst indications that FP phenotypes seem to dier in fearfulness. It should be noted that we only found dierences in the NE and OF test, where behavioural responses could also be related to activity or coping style. Further research is needed to identify whether FP phenotypes dier in activity and whether they can be classied into dierent coping styles.
    In vitro model to study trained innate immunity in chicken primary monocytes
    Verwoolde, M.B. ; Biggelaar, Robin H.G.A. van den; Baal, J. van; Jansen, Christine A. ; Lammers, A. - \ 2018
    Early-life microbiota transplantation affects behavioural responses in feather pecking selection lines
    Weetering, Y. van de; Eijk, J.A.J. van der; Lammers, A. ; Rodenburg, T.B. - \ 2018
    Feather pecking (FP) is a major welfare and economic problem in the laying hen industry, as it can cause feather damage and could lead to injuries or even mortality of victims. FP is multifactorial and has been related to behaviours such as fearfulness. Gut microbiota might contribute to FP, as it influences behaviours in rodent models that have been linked to FP such as anxiety. Moreover, recent studies have found that high and low FP lines differ in their cecal microbial metabolites and composition. However, it is unknown whether a causal link between the gut microbiota and FP exists. Therefore, we orally administered adult microbiota to newly hatched chicks (daily, day 0-14 of age). We used genetic lines selected for high (HFP, n = 288) and low (LFP, n = 288) FP. The microbiota transplants were collected from pooled gut content of 30 week old HFP and LFP donor birds. Each line received either HFP microbiota, LFP microbiota or control treatment. FP behaviour was observed via direct observations on pen-level between 0-5, 8-10 and 13-15 weeks of age. Furthermore, birds were tested in two behavioural tests; the Novel Object (NO) test at 3 days and 5 weeks of age and the Open Field (OF) test at 13 weeks of age. Although we did not find an effect of line*treatment interactions or treatment on FP, we did observe that birds treated with LFP microbiota stepped sooner (P < 0.01) and more and vocalized sooner compared to the control treated birds during the OF test (P < 0.05). Additionally, they stepped sooner during the OF, yet took longer to approach the NO compared to HFP microbiota groups (P < 0.05). Therefore, we conclude that early-life microbiota treatment affects behavioural responses, which might be related to fearfulness, social motivation or coping style.
    Protein fermentation profiles in pigs
    Lammers-Jannink, Kim - \ 2018
    Growth rate of broiler chickens is influenced by early life feeding strategy
    Hollemans, M.S. ; Lammers, A. ; Vries, S. de - \ 2018
    In: The XVth European Poultry Conference (EPC). - Zagreb, Croatia : - ISBN 9789082915709 - p. 579 - 579.
    delayed nutrition - early nutrition - Intestinal permeability - compensatory growth
    After hatching in conventional systems, broiler chickens have a delay to nutrition thatcan last for 72h, depending on length of the hatch window, internal hatchery proceduresand transport duration. Previous research on early life feeding strategies has shownnegative effects on bodyweight (BW) gain after delayed nutrition (DN), compared withearly nutrition (EN). However, it is not known whether DN chickens can (partially)compensate for their lower BW between hatch and slaughter. In this study, we tested thehypothesis that DN chickens have an increased growth rate, as a result of compensatorygrowth. Data from 3 independent experiments were used. In these studies, broilerswere subjected to either EN or DN with different durations of DN (38 to 72 h) and daysto slaughter (14 to 35 d). In all experiments, DN groups had lower BW compared withEN which was sustained until slaughter. Relative differences in BW, however, decreasedfrom 114 to 176% post placement to 102 – 112 % at slaughter (35 d). Growth curves of DNand EN chickens were analysed to study whether compensatory growth could explain thedifferences in BW between EN and DN. Absolute average daily gain (aADG) was higher inEN chickens from start until slaughter. To analyse the growth curve independent of BW,relative ADG (rADG) between two ages was calculated as follows:Differences in rADG between DN and EN chickens were greater in the first 14 d (DN:63%, EN: 47%; P < 0.001), but smaller in the remaining grow-out period (14 – 28 d:DN: 18%, EN: 16%; 28 – 35 d: DN: 8%, EN: 7%; both P <0 .001). Based on these results,it seems that DN broilers compensate for their lag in BW during the first 14 d postplacement. As differences in absolute BW were still present at 35 d, the increase in rADGseems insufficient to catch up with EN broilers. EN chickens have higher aADG untilslaughter, however, rADG is lower, showing that growth rate is influenced by feedingstrategy. Previous literature describes interactions between compensatory growth andnutrient composition of diets on nitrogen and fat retention. This may give reason forfuture work to evaluate effects of early life feeding strategy on carcass traits.
    Body weight is affected by early life feeding strategy and hatch moment in broiler chickens
    Hollemans, M.S. ; Noorloos, Marit ; Vries, S. de; Lammers, A. - \ 2018
    In: The XVth European Poultry Conference (EPC). - Zagreb, Croatia : - ISBN 9789082915709 - p. 259 - 259.
    delayed nutrition - early nutrition - Intestinal permeability - compensatory growth
    After hatching in conventional systems, broiler chickens have a delay to nutrition that can last for 72h, depending on length of the hatch window, internal hatchery procedures and transport duration. Previous research on early life feeding strategies has shown negative effects on bodyweight (BW) gain after delayed nutrition (DN), compared with early nutrition (EN). However, it is not known whether DN chickens can (partially)compensate for their lower BW between hatch and slaughter. In this study, we tested the hypothesis that DN chickens have an increased growth rate, as a result of compensatory growth. Data from 3 independent experiments were used. In these studies, broilers were subjected to either EN or DN with different durations of DN (38 to 72 h) and days to slaughter (14 to 35 d). In all experiments, DN groups had lower BW compared withEN which was sustained until slaughter. Relative differences in BW, however, decreased from 114 to 176% post placement to 102 – 112 % at slaughter (35 d). Growth curves of DN and EN chickens were analysed to study whether compensatory growth could explain the differences in BW between EN and DN. Absolute average daily gain (aADG) was higher in EN chickens from start until slaughter. To analyse the growth curve independent of BW, relative ADG (rADG) between two ages was calculated as follows: Differences in rADG between DN and EN chickens were greater in the first 14 d (DN:63%, EN: 47%; P < 0.001), but smaller in the remaining grow-out period (14 – 28 d:DN: 18%, EN: 16%; 28 – 35 d: DN: 8%, EN: 7%; both P <0 .001). Based on these results,it seems that DN broilers compensate for their lag in BW during the first 14 d postplacement. As differences in absolute BW were still present at 35 d, the increase in rADG seems insufficient to catch up with EN broilers. EN chickens have higher aADG until slaughter, however, rADG is lower, showing that growth rate is influenced by feeding strategy. Previous literature describes interactions between compensatory growth and nutrient composition of diets on nitrogen and fat retention. This may give reason for future work to evaluate effects of early life feeding strategy on carcass traits.
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