Naturwissenschaften DOI 10.1007/s00114-014-1194-y ORIGINAL PAPER Development and growth in synanthropic species: plasticity and constraints Simona Kralj-Fišer & Tatjana Čelik & TjašaLokovšek & Klavdija Šuen & Rebeka Šiling & Matjaž Kuntner Received: 2 April 2014 /Revised: 25 May 2014 /Accepted: 26 May 2014 # Springer-Verlag Berlin Heidelberg 2014 Abstract Urbanization poses serious extinction risks, yet had the smallest adults, but MF (♀=300, ♂=240 days) and some species thrive in urban environments. This may be due HF (♀=240, ♂=210 days) spiders reached comparable adult to a pronounced developmental plasticity in these taxa, since sizes through shorter development. While males and females phenotypically, plastic organisms may better adjust to unpre- had comparable instar numbers, females had longer develop- dictable urban food resources. We studied phenotypic plastic- ment, higher growth ratios, adult sizes and mass; and while ity in Nuctenea umbratica, a common European forest and males adjusted their moulting to food availability, female urban vegetation spider. We subjected spiderlings to low (LF), moulting depended on specific mass, not food treatment. We medium (MF) and high (HF) food treatments and documented discussed the patterns of Nuctenea sex-specific development their growth and developmental trajectories into adulthood. and compared our results with published data on two other Spiders from the three treatments had comparable numbers of Holarctic urban colonizers (Larinioides sclopetarius, Zygiella instars and growth ratios, but differed in developmental pe- x-notata) exhibiting high plasticity and fast generation turn- riods. Longest developing LF spiders (♀=390, ♂=320 days) over. We conclude that despite relatively unconstrained devel- opmental time in the laboratory enabling Nuctenea to achieve Communicated by: Sven Thatje maximal mass and size—main female fitness proxies—their S. Kralj-Fišer (*) : T. Čelik : T. Lokovšek : M. Kuntner relatively fixed growth ratio and long generation turn-over Institute of Biology, Scientific Research Centre, Slovenian Academy may explain their lower success in urban environments. of Sciences and Arts, Novi trg 2, P. O. Box 306, SI-1001 Ljubljana, Slovenia Keywords Arthropod development . Growth patterns . Life e-mail: [email protected] history . Nuctenea umbratica . Spider . Urban ecology S. Kralj-Fišer Faculty of Mathematics, Natural Sciences and Information š Technologies, University of Primorska, Glagolja ka 8, Introduction SI-6000 Koper, Slovenia K. Šuen Among human-induced environmental changes, urbanization Biotechnical faculty, University of Ljubljana, Jamnikarjeva 101, currently represents one of the major threats to Earth’sbiodi- SI-1000 Ljubljana, Slovenia versity. Urbanization causes loss or fragmentation of native R. Šiling habitats, modifications in community structures, pollution, Institute for Water of the Republic of Slovenia, Hajdrihova 28 c, and changes in sensory environments (McKinney 2002, SI-1000 Ljubljana, Slovenia 2008). In urban environments, food resources become spatial- ly concentrated and their temporal availability oscillates more M. Kuntner Department of Entomology, National Museum of Natural History, arbitrarily (Shochat et al. 2006; Sol et al. 2013). While human- Smithsonian Institution, NHB-105, PO Box 37012, Washington, induced changes imperil most taxa and place their populations DC 20013-7012, USA at risk of extinction, some organisms thrive in urban environ- ments, proliferating and expanding their ranges (McKinney M. Kuntner Centre for Behavioural Ecology & Evolution, College of Life 2002, 2008). This raises the question of what mechanisms Sciences, Hubei University, Wuhan 430062, Hubei, China enable them to tolerate urban environmental alterations. Naturwissenschaften Phenotypic plasticity, the ability of an organism to change a Detailed studies revealed considerable species differences phenotype in response to variation in the environment (West- in degrees of plasticity among developmental parameters, and Eberhard 2003), may be a salient quality of those species that various parameters are often interdependent (e.g. Davidowitz thrive in cities (Sol 2003; Yeh and Price 2004). The important and Nijhout 2004). Higgins and Rankin (1996) described components of phenotypic plasticity are adjustable life history eight possible combinations of canalized and plastic develop- traits, such as developmental and growth patterns, size and age mental and growth parameters in arthropods resulting in var- at maturation, reproductive investment, and longevity (Stearns ious outcomes regarding age and size at maturity. Four of 1992;Roff2002). Organisms that are able to adjust life these combinations (canalized inter-moult duration, canalized histories to rapid environmental changes are expected to fare instar number, canalized growth rate and fully plastic devel- better in urban environments than individuals with more can- opmental pattern) were documented in empirical field re- alized life history trajectories (e.g. Buczkowski 2010; search (Higgins and Rankin 1996). For instance, the Kleinteich and Schneider 2011). In the latter, developmental hawkmoth, Manduca sexta, exhibits canalized maximum traits show low ability for phenotypic changes in response to inter-moult duration, but plasticity in instar number, growth environmental conditions. However, both plasticity and cana- rate and pre-moult mass in response to diet (Nijhout and lization have fitness costs and benefits (Van Buskirk and Willams 1974;Nijhout1975; Safranek and Williams 1984). Steiner 2009;Dmitriew2011). The well-fed individuals might develop at higher growth rates Developmental and growth patterns determine age and size and might be able to reach critical mass for pupation and at maturity, which significantly affect fitness (Stearns 1992; metamorphosis through fewer instars (Kingsolver 2007). On Roff 2002). For instance, the growth rate and developmental the other hand, poor nutrition in M. sexta might lead to times affect vulnerability to predators’ exposure (Gotthard moulting after certain critical number of days even in the 2000) and determine a population’s generation time. In most absence of mass gain. In the milkweed bug, Oncopeltus arthropods, female adult mass—strongly correlated with fe- fasciatus, the number of instars is fixed, but the inter-moult cundity (Suter 1990;Higgins1992;Head1995)—affects the duration and growth rates are plastic (Nijhout 1979), and thus, net reproductive rate, R (mean number of female offspring a well-fed individuals develop earlier and at a higher mass. mother produces during her lifetime) whereas in males, size at Substantial difference in male and female body size is often maturity strongly relates to competitive abilities in male–male attributed to sex-specific selection, e.g. scramble competition contests and female choice (Christenson and Goist 1979; and male–male competition in males, and fecundity selection Vo ll ra th 1980;Andersson1994). Finally, the net reproductive in females (Andersson 1994;Head1995; Blanckenhorn 2005; rate and generation time strongly relate to intrinsic rate of Blanckenhorn et al. 2007). At proximate level, size dimorphic population, r (i.e. per capita rate of population increase). species exhibit sex-specific differences in growth and devel- In arthropods, the exoskeleton grows in discrete steps opment and also sex variation in plasticity in response to through moulting, whereas mass changes continuously environmental variation (reviewed in Stillwell et al. 2010). (Foelix 2010). According to Dyar’srule(Dyar1890), arthro- For example, in M. sexta, males and females differ in plasticity pods exhibit a determined (also “canalized”) growth rate in the parameters critical for adult body size, i.e. growth rate quantified as the ratio of two consecutive instar sizes and critical mass for metamorphosis, in response to diet and (Przibram and Megušar 1912;Cole1980) and are often con- temperature (Stillwell and Davidowitz 2010). sidered to have a constant number of instars (Esperk et al. Little is known about growth and developmental plasticity 2007). Growth plasticity, on the other hand, refers to variation in spiders, a species rich and ecologically important inverte- in growth rates in response to variation in environmental brate clade-important terrestrial predators of insects and conditions. A number of studies in arthropods have investi- known for some spectacular cases of female-biased sexual gated the effects of environmental conditions on variation in size dimorphism (e.g. Kuntner et al. 2012). In spiders, growth developmental trajectories and growth rate (e.g. Gimnig et al. and development are believed to largely depend on food 2002;Gillesetal.2010; Kleinteich and Schneider 2011), in availability (Miyashita 1968). Cursorial spiders actively particular, in response to different temperature regimes (e.g. Li search for food sources and seem to mostly exhibit plastic and Jackson 1996; Robinson and Partridge 2001; Flenner growth and development patterns (e.g. Miyashita 1968; et al. 2010). In insects, studies of growth and developmental Enders 1976; Li and Jackson 1997). On the other hand, orb- plasticity depending on diet regimes have yielded mixed web spiders are sit-and-wait predators whose ability to results. While in some taxa exhibiting fixed instar numbers behaviourally adjust to prey availability is limited to changing Dyar’s rule receives support (e.g. Acrida exaltata, Ahmad web site, web position, and web properties