A synthesis of feeding habits and reproduction rhythm in Italian seed-feeding ground beetles (Coleoptera: Carabidae)

Many species of carabid beetles are important preand post-dispersal seed feeders of herbaceous plants. Here we summarise data from dissections, fi eld observations, rearing and “cafeteria” experiments on 55 granivorous and 188 omnivorous species that occur in Italy. We tested the hypothesis that seed feeding carabids are restricted to taxa with pronounced morphological adaptations for manipulating and crushing seeds in both the larval and adult stages. The feeding guilds of carabids were rearranged into the following groups: (i) strict predators with long mandibles and predaceous larvae, often depending also on non-prey food; (ii) omnivorous species with stout mandibles and larvae of a seed-eating morphotype; (iii) granivorous species, feeding only on seeds with larvae sometimes of the scarabeoid c-form type. The seed feeding carabids in the Italian fauna belong to the tribe Zabrini (Amara and Zabrus genera) and to all the Harpalinae (sub)tribes, from Anisodactylini to Ditomina. The time of reproduction seems to be associated with habitat preference; wetland or dry open land, rather than true granivorous versus omnivorous habits, but in stenophagous seed feeders, a phenological coincidence with particular plants is sometimes recorded.

Many authors have studied the phytophagous habits of ground beetles.Forbes (1883) fi rst recognized the granivorous preferences of many species and described three general feeding guilds based on morphological differences in

FOOD PREFERENCE
Several aspects of seed consumption are poorly understood, including the preferences of particular species of carabid for specifi c species of seed.Many species of granivorous carabids climb plant stems and feed on the ripening seeds of grasses, umbelliferous, composite and cruciferous plants (Thiele, 1977;Hůrka, 1996;Martinkova et al., 2006).However, many less specialized carabids forage for seed mainly on the ground ("post-dispersal" seed predation, Honek et al., 2003;Mauchline et al., 2005).Some species of Amara prefer crucifer seeds and some Harpalus prefer seeds of composites (Lindroth, 1949;Thiele, 1977).Honek et al. (2007) studied the seed preferences of the adults of 30 species of carabids using the seeds of 28 common species of agricultural weeds in controlled laboratory experiments.The factors determining the preferences of carabids for particular species of seed are similar to that determining prey specifi city in other predator groups.Body size of both predator and seed (''prey'') are also important, probably because of the problems associated with handling seed of different sizes (Honek et al., 2003).It is also well known that primarily carnivorous insects utilize plant material as a food source in some phases of their development (Norris & Kogan, 2000).Many species (Zabrini and Harpalini) are mainly granivorous as adults (Thiele, 1977;Zetto Brandmayr, 1990) and carnivorous species often supplement their diet of insects with seeds (Lund & Turpin, 1977;Hurst & Doberski, 2003, Fawki & Toft, 2005).
This review aims to outline the extent of the knowledge on the seed eating ground beetles of Italy.Data for other European countries (except the Czech Republic) are scarce.All the experimental data on carabid species belonging to the Italian fauna were compared and updated using: (1) graduate theses produced during the past 25 years at the University of Calabria; (2) data on Italian species kept in the Zoocoenoses laboratory (DiBEST, University of Calabria) and used in rearing experiments or in "cafeteria" tests accumulated over about 35 years and (3) gut dissections performed on rare species found during fi eld trips.In this study we redefi ne the concept of phytophagous by using the terms carnivorous, omnivorous and granivorous.The term seed feeder refers to range of feeding adaptations from omnivory to true granivory.Moreover, we estimate the number of species of seed feeders and higher taxa present in Italy, and their relationship between plant seasonality and their reproduction rhythm.The taxonomic arrangement of all the data presented follows the updated version of the family Carabidae in the Fauna Europaea by Vigna Taglianti (http://www.fauna-eu.org).e.g.attacks on germinating seeds included under the well documented "non-prey food consumption" investigated by Lundgren (2009).All other cases studied belong to the phylogenetically easily identifi ed Zabrini and Harpalinae (tribe Harpalini of other authors).Within these two taxa, we have distinguished four different feeding strategies (for a complete list of references view Appendix 1).
(2) Plant specialist omnivorous, i.e. partially carnivorous, but highly specialized in feeding on the seeds of just one plant genus; such as Tetraplatypus ganglbaueri, which feeds only on Satureja seeds or T. rufi collis, which only feeds on Calluna seeds.Tetraplatypus ganglbaueri occurs only in calcareous grasslands on Dinaric Karst, from Trieste to southern Dalmatia, where Satureja bushes form dense mats, similar to those of Calluna or Erica in heathland.It feeds on seeds both on the ground and on plants, by opening the fl ower calyx laterally (Zetto Brandmayr & Brandmayr, 1978a).Tetraplatypus rufi collis possibly feeds in the same way on Calluna heaths.
(3) Imaginal omnivorous.Carabids that are omnivorous as adults but the larvae are strictly granivorous: Amara aulica and perhaps some other species/subgenera of Amara.

SEED FEEDING CARABIDS IN ITALY
Vigna Taglianti (2005) records 1313 species of carabids in the Italian fauna and among these 243 (18.50%) are seed feeders.This includes all the Zabrine and Harpaline taxa and the tentative inclusion of Amblystomina (seven species belonging to the genus Amblystomus), for which there is currently no data on food choice.Only 55 (4.2%) of these can be considered to be true granivores and the inclusion of Graniger and Oedesis is tentative due to the current lack of data on their food preferences (Fig. 3).Fig. 3.The genera to which the 24 3 seed feeding species of carabids recorded in Italy belong.Black columns are the strictly granivorous taxa, the feeding habits of the Amblystomines are still unknown.

PLANT SEASONALITY AND REPRODUCTION RHYTHM
Even though the importance of ground beetles as seed feeders is recognized (Luff, 1987;Kromp, 1999;Tooley & Brust, 2002;Mauchline et al., 2005), little is known about the omnivorous/granivorous taxa in other European countries, such as Spain, Greece and Southern Russia.In Central and Western Europe, ground beetles are the most important invertebrates that feed on the seeds of herbaceous plants (Honek et al., 2003;Martinkova et al., 2006).The granivorous species typical of arable land belong mainly to the tribes Harpalini (e.g., the genera Anisodactylus, Har-palus, Parophonus, Pseudoophonus and Stenolophus) and Zabrini (Amara, Zabrus) (Lindroth, 1949;Thiele, 1977;Hůrka, 1996).In northern temperate agricultural areas some studies report seasonal fl uctuations in the intensity of predation of weed seeds by carabid beetles (Tooley & Brust, 2002;Honek et al., 2003;Saska et al., 2010).This variation, however, cannot always be attributed to changes in the activity/density of these predators (Honek et al., 2003;Mauchline et al., 2005;Saska et al., 2010).This incongruence may be attributed to intrinsic seasonal variation in consumption (Honek et al., 2006), but temperature variation may also contribute to the seasonal variation in  & Brandmayr, 1978a), which seems to account for their phenological coincidence.In the taxa around Harpalus, the larvae of some lineages (Harpalus s. str., Harpalophonus, Semiophonus) occur in summer and others in winter (Pseudoophonus), depending mainly on climate or phylogenic constraints, as reported by Larsson (1939), Paarmann (1979) and Hůrka (1986) for Carabus, with no evident association with a particular nursing plant.
In granivorous taxa, a phenological coincidence with autumn ripening umbelliferous plants is widespread in the genus Ophonus (Zetto Brandmayr, 1983), but in some Ditomines (Ditomus, Dixus, Machozetus?) the evolution of brood care in paedotrophic nests enabled a shift to summer breeding (Sharova & Makarov, 1983;Brandmayr & Zetto Brandmayr, 1987).Thus, different granivorous taxa have different adaptive strategies associated with the same nursing plant.In contrast, the free-living winter larvae of Ophonus are "post-dispersal seed predators", whereas Ditomus and probably Carterus and Dixus care for their summer larvae by feeding them with Daucus carota or Plantago seeds.The associations between plant seasonality and reproduction rhythm of granivorous carabids are in need of further research.

DISCUSSION
The fi ndings of this study indicate that it would be appropriate to rearrange the three feeding guilds of Forbes (1883) and Zhavoronkova (1969) in the following way: (1) carnivorous, species with long mandibles and predaceous larvae, that are sometimes also dependent on nonprey food.There are a wide variety of morphotypes of larvae in this category of species (Zetto Brandmayr et al., 1998): soil pore walkers, surface runners, surface walkers, sand diggers, parasitoids, etc.Many taxa show a more or less pronounced prey specialization (Thiele, 1977), which is not discussed here; (2) omnivorous species with stout mandibles, capable of crushing hard seeds and with larvae that are of a seed-eating morphotype ("spermophagous"), with wide mandibles and terebra often with supernumerary teeth.All Zabrines and most Harpalines belong to this category, including the subtribes Anisodactylines and Selenophorines; (3) granivorous species, found only in some of the Harpalines (Ophonus, Ditomina), all the larvae of which have strongly enlarged heads, short mandibles and some genera have a characteristic c-shaped scarabeoid larva.This last characteristic may be associated with the parent providing the larva with seeds.
The new categorization means that sensu stricto only the Zabrini and Harpalinae are seed feeders and that the few cases of seed feeding in other taxa are due to non-prey food intake (Lundgren, 2009).
Considering all the carabids characterized as seed feeders, we identifi ed four levels of granivory: omnivorous (carnivorous + partly granivorous); omnivorous, but highly specialized in feeding on the seeds of just one plant genus; imaginal omnivorous and true granivorous species.
Within the omnivorous taxa, there are some interesting variations.Despite their predatory habits, both on seeds and animal food, some species may specialize on a restricted group (genus) of plants, which may infl uence their choice of habitat (Tetraplatypus ganglbaueri, T. rufi collis).In some species, such as Amara montivaga, an evident preference for species-specifi c seeds is recorded, (Honek et al., 2005) which is not congruent with their choice of habitat.Finally, some species may be omnivorous in the adult stage but more dependent on seeds during the larval stages (Saska, 2005).According to our data, the provision of fresh meat in cafeteria or no-choice experiments should be used as a preliminary test to distinguish omnivorous from granivorous taxa.
The number of species that can be classifi ed as seed feeders in the Italian fauna is 243 out of a total of 1313 (18.5%), 55 of which (4.2%) are true granivores.On the Iberian Peninsula, a total of 1255 carabid species are recorded (Serrano, 2003(Serrano, , 2013)), of which 276 (22%) are seed feeders and 57 (4.5%) are true granivores.In continental countries, e.g. in Central Europe (Koch, 1989), there are 179 (23.2%) seed feeders, and 21 (2.7%) true granivores out of a total of 770 species.In Russia and adjacent countries (Krizhanowskij et al., 1995), 630 taxa of seed feeders occur (20.5%), of which 79 (2.6%) are true granivores out of a total of 3075 species.In Fennoscandia (Lindroth, 1945(Lindroth, , 1985(Lindroth, -1986) ) there are 73 (18.1%) seed feeders and 7 (1.7%)true granivores out of a total of 403 species.Summing up, in Western Palearctic countries the percentage of seed feeders varies from 18 to 23%, and constitutes an important component of the faunas.The percentage of true granivores ranges from 1.7 to 4.4%, and they occur mainly in Mediterranean countries, such as Spain and Italy.
When the granivorous carabids breed is known only for a small fraction of the European fauna and very little is known about those in the Mediterranean area.For omnivorous carabids, when they breed depends mainly on climate and habitat factors (e.g.wet versus dry soil), and "phenological coincidence" is frequently recorded between breeding in granivorous species and seed production of a "main nursing plant".The reproductive rhythms of the Ditomines are exceptional, and currently summer reproduction in paedotrophic nests is only suggested for several genera living within and outside Europe.

Table 1 .
Number of species, habitat, diet, main nursing plant, reproduction rhythm and possible phenological coincidence of all the genera (subgenera) of Italian seed feeding ground beetles.OL -open land; SUMMER -reproduction in spring or summer, with summer larvae; WINTER -reproduction in autumn or late autumn with winter larvae; BIENNIAL -species that have a two year life cycle.* -Hesperophonus azureus in the laboratory will also eat small pieces of meat.