Schistosomiasis is a tropical disease affecting over 230 million people worldwide. Although effective drug treatment is available, reinfections are common and development of immunity is slow. Most antibodies raised during schistosome infection are directed against glycans, some of which are thought to be protective. Developing schistosomula are considered most vulnerable to immune attack and better understanding of local antibody responses raised against glycans expressed by this life stage might reveal possible glycan vaccine candidates for future vaccine research. We used antibody-secreting cell (ASC) probes to characterize local anti-glycan antibody responses against migrating S. japonicum schistosomula in different tissues of rats. Analysis by shotgun Schistosoma glycan microarray resulted in the identification of anti-glycan antibody response patterns which reflected the migratory pathway of schistosomula. Antibodies raised by skin-lymph node (LN) ASC probes mainly targeted N-glycans with terminal mannose-residues, Galbeta1-4GlcNAc (LacNAc) and Galbeta1-4(Fucalpha1-3)GlcNAc (LeX). Also responses towards antigenic and schistosome specific glycosphingolipid (GSL)-glycans containing highly fucosylated GalNAcbeta1-4(GlcNAcbeta1)n stretches that are believed to be present at the parasite s surface constitutively upon transformation were found. Antibody targets recognized by lung-LN ASC probes were mainly N-glycans presenting GalNAcbeta1-4GlcNAc (LDN) and GlcNAc-motifs. Surprisingly, antibodies against highly antigenic multi-fucosylated motifs of GSL-glycans were not observed in lung-LN ASC probes, indicating that these antigens are not expressed in lung stage schistosomula, or are not appropriately exposed to induce immune responses locally. The local anti-glycan responses observed in this study highlight the stage- and tissue-specific expression of antigenic parasite glycans and provide insights into glycan targets possibly involved in resistance to S. japonicum infection.